Edward De Robertis, M.D., Ph.D.

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Work Titles
UCLA Norman Sprague Professor, Biological Chemistry Member, Cell & Developmental Biology GPB Home Area Member, JCCC Cancer and Stem Cell Biology Program Area Investigator, Howard Hughes Medical Institute
Education:
Degrees:
M.D.
Ph.D.
Honors and Awards:
National Academy of Sciences, Member
Pontifical Academy of Sciences, Academician
American Academy of Arts and Sciences, Fellow
Latin American Academy of Sciences , Corresponding Member
2013 - Universite La Sorbonne, Doctor Honoris Causa
1997 - National Institutes of Health, MERIT Award
1997 - College de France, Paris, Public Lecture Series and Medal
European Molecular Biology Organization, Member
School of Medicine, Uruguay, Gold Medal to the top 1971 medical student
2009 - Ross Harrison Prize in Developmental Biology
Professional Societies:
2002 - International Society of Developmental Biologists (ISDB), President
1998 - Societe de Biologie, Paris, France, Foreign Corresponding Member

Contact Information:

Work Email Address:

ederobertis@mednet.ucla.edu


Website:

De Robertis Lab
HHMI Webpage
Profile

Work Phone Number:

(310) 206-1463

Work Address:

Office
5-612A MRL
Los Angeles, CA 90095

Campus 166222
CA

Laboratory
5-619 MRL
Los Angeles, CA 90095


Research Interest:

Cell-Cell Communication During Embryonic Induction

Research Summary

Edward De Robertis studies how long-range cell communication between the dorsal and ventral sides of the embryo occurs through the diffusion of growth factor antagonists. The discovery of Chordin, a BMP antagonist, provided a new paradigm in which facilitated diffusion of a morphogen takes place in the narrow extracellular space that separates the ectoderm from the endomesoderm. This gradient is further integrated with Wnt signaling through the sequestration of the enzyme GSK3 inside multivesicular endosomes.

Within the organism cells do not lead individual lives. They differentiate, proliferate, and die as part of groups of hundreds or thousands of cells called morphogenetic fields, which have the remarkable property of self-regulating pattern after perturbations such as bisection. The aim of our research is to discover the molecular mechanisms by which self-regulation works.

Spemann's Dorsal Organizer

A foundation for understanding self-regulation was provided by an experiment carried out by Spemann and Mangold more than 80 years ago involving grafting of the dorsal lip region of the amphibian embryo. They found that a small group of cells, called the organizer, is able to induce Siamese twins, including a complete central nervous system (CNS), in neighboring cells. Hans Spemann received the 1935 Nobel Prize in Physiology or Medicine for this discovery of embryonic induction. Isolating the molecules involved in these cell-cell inductions has been the Holy Grail of embryology. Using the frog Xenopus, we have isolated multiple genes that encode secreted proteins expressed specifically in Spemann's organizer. Studies on Chordin, Cerberus, Frzb-1, and Crescent have contributed to the current realization that growth factor antagonists secreted into the extracellular space mediate the formation of embryonic signaling gradients.

Dorsal-Ventral Communication

The entire embryo participates in the dorsal-ventral (D-V) morphogenetic field. Chordin is produced dorsally and another secreted protein, Sizzled, is expressed in the ventral side. We used molecular cloning and biochemical methods to unravel a network of Chordin-interacting proteins that form a self-regulating gradient of BMP activity. Key components are dorsal and ventral BMPs as well as Tolloid, a protease that we found specifically cleaves Chordin, releasing active BMPs in the ventral side. Sizzled and BMPs bind to Tolloid and inhibit its rate-limiting enzyme activity. Self-regulation results from the dorsal and ventral centers being under opposite transcriptional control: when BMP levels are lowered, production of dorsal ADMP and BMP2 is increased; at high BMP levels, feedback inhibitors such as Sizzled dampen the signal by inhibiting the degradation of Chordin.

The Chordin Gradient

In the ectoderm, BMP inhibition causes differentiation of CNS, and high levels of BMP signaling induce epidermis. In the mesoderm, at low levels of BMP signaling notochord is formed, and at progressively higher levels kidney, lateral plate mesoderm, and blood tissues are induced. Thus, histotypic differentiation in the vertebrate embryo depends on the graded activity of BMP. Remarkably, the three germ layers respond coordinately to changes in BMP signaling. A key question is whether a single signaling gradient or multiple ones are used to pattern the cell differentiation of the different germ layers. We developed a novel immunolocalization method to follow the distribution of endogenous Chordin during Xenopus gastrulation. Chordin protein secreted by the dorsal Spemann organizer was found to diffuse along a narrow region that separates the ectoderm from anterior endoderm and mesoderm. This fibronectin-rich extracellular matrix (ECM), called Brachet's cleft in Xenopus, is present in all vertebrate embryos. Chordin forms a smooth gradient that encircles the embryo, diffusing over a distance of 2 mm in this signaling highway between ectoderm and mesoderm. After embryo bisection or transplantation of an organizer, the gradient self-regulates. Chordin must reach very high concentrations in this narrow space. It appears that as ectoderm and mesoderm undergo morphogenetic movements during gastrulation, cells in both germ layers read their positional information from a common Chordin/BMP gradient in ECM.

Integrating BMP and Wnt Signaling

The Chordin/BMP biochemical pathway explains cell differentiation along the D-V axis. However, embryonic morphology is also regulated by other morphogens, such as Wnt and fibroblast growth factor (FGF). How are these signaling pathways integrated seamlessly in the embryo? Wnt signals by inhibiting a protein kinase called glycogen synthase kinase 3 (GSK3), but the mechanism by which this occurs is unclear. While investigating the BMP transcription factor Smad1 phosphorylation by GSK3, we discovered a novel cellular mechanism for cell signaling. Upon Wnt signaling, cytosolic GSK3 binds to the Wnt receptor complex, which consists of the Frizzled and LRP6 coreceptors, Axin, Dishevelled, and β-catenin. All of these proteins are substrates for GSK3, which is translocated together with them into small intraluminal vesicles located inside multivesicular bodies (MVBs). In this way, GSK3 becomes sequestered from its many cytosolic substrates. MVBs are an obligatory intermediate organelle for the trafficking of activated plasma membrane receptors destined for degradation in lysosomes. The sequestration of GSK3 requires the activity of ESCRT proteins required for the formation of MVB intraluminal vesicles, such as HRS/Vp27 and Vps4, which we found are also essential for canonical Wnt signaling.

The GSK3 sequestration mechanism has predictive value. Interfering with membrane trafficking downstream of MVB formation potentiates Wnt signaling by causing GSK3 to remain sequestered inside MVBs for longer periods. We found that depletion of Presenilin 1 and 2, two intramembrane proteases mutated in early-onset familial Alzheimer's disease and required for membrane trafficking, greatly increased Wnt/GSK3 signaling, suggesting novel pathogenic mechanisms in neurodegenerative disease.

Remarkably, the sequestration of GSK3 extended the half-life of many proteins in addition to the well-known Wnt target beta-catenin. Pulse-chase studies with radioactive amino acids showed that total cellular half-life is extended by Wnt3a treatment. Bioinformatic analyses revealed that 20 percent of human proteins contain three or more putative GSK3 sites in a row. This is a much higher frequency than expected at random. Our ongoing studies indicate that GSK3 sites can be predictors of proteins regulated by Wnt. For example, we find that in the presence of FGF, which promotes a mitogen-activated protein kinase that primes phosphorylation by GSK3, Smad4 activity is potently increased by Wnt. This suggests that the transforming growth factor beta/Nodal morphogen gradient, which is fundamental for mesoderm induction, may be intimately integrated with the FGF and Wnt gradients. Smad4 is a tumor suppressor that is depleted during progression of pancreatic, colorectal, and prostate cancers. The discovery that its activity is not constitutive but rather is regulated by FGF and Wnt may have applications in cancer treatment.

In conclusion, efforts to uncover the molecular basis of embryonic self-regulation have shown that the differentiation of embryonic tissue types is regulated by an extracellular gradient of proteins diffusing between ectoderm and endomesoderm. Studies of basic embryonic patterning mechanism led to the discovery of unexpected connections between endosomal trafficking, growth factor signaling, and protein degradation, which are being actively explored.

Cell-Cell Communication During Embryonic Induction

Within the organism cells do not lead individual lives. They differentiate, proliferate, and die as part of groups of hundreds or thousands of cells called morphogenetic fields, which have the remarkable property of self-regulating pattern after perturbations. Experimental embryology started in 1891 when Hans Driesch separated the first two cells of an embryo and obtained identical twins. The early embryo is considered the primary morphogenetic field. At later stages, secondary fields determine the formation of organs and body regions such as limbs, heart, and central nervous system (CNS), as first described by Ross Harrison in 1918. The aim of our research is to discover the molecular machinery through which self-regulation works.

Spemann's Dorsal Organizer

The embryo of the frog Xenopus provides an excellent system for unraveling how cells communicate with each other. Large numbers of embryos can be obtained and subjected to microsurgical manipulations before any histotypic differentiations occur. A rich heritage of experimental embryology exists, and classical transplantation techniques can now be combined with knockdowns of individual or multiple genes.

A foundation for understanding self-regulation was provided by an experiment carried out by Spemann and Mangold more than 80 years ago involving grafting of the dorsal lip region of the amphibian embryo. They found that a small group of cells, called the organizer, is able to induce Siamese twins, including a complete CNS, in neighboring cells. Hans Spemann received the 1935 Nobel Prize in Physiology or Medicine for this discovery of embryonic induction. Isolating the molecules involved in these cell-cell inductions has been the Holy Grail of embryology. We have isolated multiple genes that encode secreted proteins expressed specifically in Spemann's organizer. Studies on Chordin, Cerberus, Frzb-1, and Crescent have contributed to the current realization that growth factor antagonists secreted into the extracellular space mediate the formation of embryonic signaling gradients.

The Ventral Center

On the opposite side of the dorsal organizer, in what we call the ventral center, BMP4/7 (bone morphogenetic proteins, a type of growth factor) are expressed at midgastrula. On the dorsal side, other BMPs?called BMP2 and ADMP?are secreted, but only when BMP levels are low. Ventral center gene expression is driven by high BMP signaling, which phosphorylates and activates the transcription factor Smad1. The ventral center secretes a cocktail of proteins that participate in the extracellular biochemical pathway that mediates self-regulation . Ventral center cells secrete several proteins in addition to BMP4/7. (1) Tolloid is a zinc metalloproteinase that we found cleaves Chordin-BMP complexes flowing from the dorsal side, liberating active BMPs produced in more dorsal regions. (2) Sizzled (a secreted Frizzled-related protein similar to Crescent) functions as a competitive inhibitor of the Tolloid enzyme. (3) Twisted-gastrulation is a protein that binds to BMP (facilitating its solubility and signaling) and to Chordin (making it a better BMP antagonist). (4) Crossveinless-2 is a Chordin-like secreted BMP-binding protein that remains attached to ventral cell surfaces and binds and concentrates diffusing Chordin-BMP complexes on the ventral side, where BMPs can then be released by Tolloid.

Self-Regulation

The rate-limiting step in this novel biochemical pathway is the enzyme Tolloid, which provides, together with Crossveinless-2, a type of ventral ?sink? towards which BMP ligands flow. Self-regulation results from the dorsal and ventral centers being under opposite transcriptional control: if BMP levels are lowered, production of dorsal ADMP and BMP2 is increased; at high BMP levels, feedback inhibitors such as Sizzled and Crossveinless-2 dampen the signal.

When the four main BMPs are knocked down simultaneously, self-regulation collapses and the entire ectoderm becomes CNS. By transplanting wild-type tissue into these BMP-depleted embryos, I was able to show that both the dorsal and ventral centers serve as sources of BMPs that diffuse over long distances in the embryo, triggering changes in cell differentiation. This double gradient of BMP signals flowing from opposite poles of the embryo helps explain the resilience of the embryo.

Integrating the D-V and A-P Axes

The biochemical pathway described above explains cell differentiation along the dorsal-ventral (D-V) axis. However, when twins are produced the antero-posterior (A-P) and D-V axes are seamlessly integrated. How is this achieved? Christof Niehrs (German Cancer Research Center, Heidelberg) has discovered that the A-P axis is regulated by a gradient of Wnt signals, which are maximal in the posterior. Wnt signals by regulating the activity of a protein kinase called GSK3. We have recently found that the degradation of Smad1/Mad after activation by BMP requires its phosphorylation by GSK3, which triggers polyubiquitinylation and degradation in proteasomes located in the centrosomes. Because GSK3 is inhibited by Wnt signaling, Wnt causes the duration of the BMP signaling to increase.

In this view of self-regulation, the D-V (BMP) and A-P (Wnt) gradients are integrated at the level of the phosphorylations of Smad1. The BMP gradient determines the intensity and the Wnt gradient the duration of Smad1, a transcription factor that in turn regulates the activity of promoters and enhancers of hundreds of downstream genes coordinately. Cells are known to distinguish between duration and intensity of signals. Such a hardwired system of signaling integration might provide robustness to embryonic development, which must form perfect babies time after time.

New Research Avenues

The discovery of this novel branch of the Wnt pathway signaling through Smad1 has opened new and exciting research directions. We generated phosphospecific antibodies that recognize Smad1, or its Drosophila homolog Mad, targeted for degradation. These proteins accumulate in the pericentrosomal region. We found that many other proteins targeted for degradation are similarly localized.

Surprisingly, proteins destined for degradation are inherited asymmetrically when cells divide. The peripheral centrosomal material remains in one cell when the centrioles migrate to opposite poles, so that the other daughter remains pristine. Thus, many somatic cell mitoses, perhaps most, are asymmetrical rather than equal as previously thought. We are now studying the role of Wnt signaling in regulating these remarkable asymmetries of proteins destined for degradation.

The other new direction we are pursuing is to use the power of Drosophila molecular genetics to investigate the extent to which the Mad signaling pathway participates in cell differentiation decisions triggered by Wingless signaling. The results so far indicate that Mad is required, in cooperation with other factors, in a surprising number of developmental choices mediated by Wingless. The fact that vertebrate Smad and invertebrate Mad serve as integrators of BMP and Wnt signals may have profound biological implications for the evolution of animal body plans from a common ancestor, a central problem of the young science of Evo-Devo.

In conclusion, efforts to uncover the molecular basis of an embryological experiment carried out more than 80 years ago have shown that the differentiation of embryonic tissue types is regulated by secreted inhibitory proteins originating from dorsal and ventral organizing centers. These studies in Xenopus embryos have led to new insights on how a network of extracellular proteins controlled by the proteolysis of Chordin mediates pattern self-regulation and is integrated with the Wnt signaling pathway.

Detailed Biography:

Dr. De Robertis is also Norman Sprague Professor of Biological Chemistry at the University of California, Los Angeles, School of Medicine. He received an M.D. from the University of Uruguay and a Ph.D. in Chemistry from the University of Buenos Aires. His postdoctoral training was with Sir John Gurdon at the Medical Research Council Laboratory of Molecular Biology, Cambridge, U.K. Before moving to UCLA, he was professor at the University of Basel. Dr. De Robertis is a member of the Pontifical Academy of Sciences, the National Academy of Sciences, the European Molecular Biology Organization and the Latin American Academy of Sciences, and a Fellow of the American Academy of Arts and Sciences. He served as President of the International Society of Developmental Biologists until 2006.

Publications:

A selected list of publications:

Ding Yi, Colozza Gabriele, Zhang Kelvin, Moriyama Yuki, Ploper Diego, Sosa Eric A, Benitez Maria D J, De Robertis Edward M   Genome-wide analysis of dorsal and ventral transcriptomes of the Xenopus laevis gastrula Developmental biology, 2017; 426(2): 176-187.
Ding Yi, Ploper Diego, Sosa Eric A, Colozza Gabriele, Moriyama Yuki, Benitez Maria D J, Zhang Kelvin, Merkurjev Daria, De Robertis Edward M   Spemann organizer transcriptome induction by early beta-catenin, Wnt, Nodal, and Siamois signals in Xenopus laevis Proceedings of the National Academy of Sciences of the United States of America, 2017; 114(15): E3081-E3090.
De Robertis Edward M, Moriyama Yuki   The Chordin Morphogenetic Pathway Current topics in developmental biology, 2016; 116(15): 231-45.
Demagny Hadrien, De Robertis Edward M   Smad4/DPC4: A barrier against tumor progression driven by RTK/Ras/Erk and Wnt/GSK3 signaling Molecular & cellular oncology, 2016; 3(2): e989133.
Demagny Hadrien, De Robertis Edward M   Point mutations in the tumor suppressor Smad4/DPC4 enhance its phosphorylation by GSK3 and reversibly inactivate TGF-β signaling Molecular & cellular oncology, 2016; 3(1): e1025181.
De Robertis Edward M, Ploper Diego   Sperm Motility Requires Wnt/GSK3 Stabilization of Proteins Developmental cell, 2015; 35(4): 401-2.
Blum Martin, De Robertis Edward M, Wallingford John B, Niehrs Christof   Morpholinos: Antisense and Sensibility Developmental cell, 2015; 35(2): 145-9.
Ploper Diego, De Robertis Edward M   The MITF family of transcription factors: Role in endolysosomal biogenesis, Wnt signaling, and oncogenesis Pharmacological research, 2015; 99(2): 36-43.
Bier Ethan, De Robertis Edward M   EMBRYO DEVELOPMENT. BMP gradients: A paradigm for morphogen-mediated developmental patterning Science (New York, N.Y.), 2015; 348(6242): aaa5838.
Kim Hyunjoon, Vick Philipp, Hedtke Joshua, Ploper Diego, De Robertis Edward M   Wnt Signaling Translocates Lys48-Linked Polyubiquitinated Proteins to the Lysosomal Pathway Cell reports, 2015; 11(8): 1151-9.
Ploper Diego, Taelman Vincent F, Robert Lidia, Perez Brian S, Titz Björn, Chen Hsiao-Wang, Graeber Thomas G, von Euw Erika, Ribas Antoni, De Robertis Edward M   MITF drives endolysosomal biogenesis and potentiates Wnt signaling in melanoma cells Proceedings of the National Academy of Sciences of the United States of America, 2015; 112(5): E420-9.
Demagny Hadrien, Araki Tatsuya, De Robertis Edward M   The tumor suppressor Smad4/DPC4 is regulated by phosphorylations that integrate FGF, Wnt, and TGF-β signaling Cell reports, 2014; 9(2): 688-700.
De Robertis Edward M   Yoshiki Sasai 1962-2014 Cell, 2014; 158(6): 1233-5.
De Robertis Edward M   Lessons from a great developmental biologist Differentiation; research in biological diversity, 2014; 88(1): 3-8.
Colozza Gabriele, De Robertis Edward M   Maternal syntabulin is required for dorsal axis formation and is a germ plasm component in Xenopus Differentiation; research in biological diversity, 2014; 88(1): 17-26.
De Robertis Eddy M, Niehrs Christof   Herbert Steinbeisser: a life with the Xenopus embryo The International journal of developmental biology, 2014; 58(5): 299-302.
Plouhinec, Jean-Louis, Zakin, Lise, Moriyama, Yuki and De Robertis, Edward M.   Chordin forms a self-organizing morphogen gradient in the extracellular space between ectoderm and mesoderm in the Xenopus embryo Proc. Natl. Acad. Sci. USA, 2013; 110: 29372-20379.
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De Robertis, Edward M. and Colozza, Gabriele   Scaling to size by protease inhibition Curr. Biol, 2013; 23: R652-R654.
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Dobrowolski Radek, Vick Philipp, Ploper Diego, Gumper Iwona, Snitkin Harriet, Sabatini David D, De Robertis Edward M   Presenilin deficiency or lysosomal inhibition enhances Wnt signaling through relocalization of GSK3 to the late-endosomal compartment Cell reports, 2012; 2(5): 1316-28.
Dobrowolski, R. and De Robertis, E.M.   Endocytic control of growth factor signaling: multivesicular bodies as signaling organelles Nat. Rev. Mol. Cell Biol, 2012; 13: 53-60.
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Dobrowolski, R., Vick, P., Ploper, D., Gumper, I., Snitkin, H., Sabatini, D.D. and De Robertis, E.M.   Presenilin deficiency or lysosomal inhibition enhance Wnt signaling through relocalization of GSK3 to the late endosomal compartment Cell Reports, 2012; 2: 1316-1328.
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Dobrowolski Radek, De Robertis Edward M   Endocytic control of growth factor signalling: multivesicular bodies as signalling organelles Nature reviews. Molecular cell biology, 2012; 13(1): 53-60.
Plouhinec Jean-Louis, Zakin Lise, De Robertis Edward M   Systems control of BMP morphogen flow in vertebrate embryos Current opinion in genetics & development, 2011; 21(6): 696-703.
Vorwald-Denholtz Peggy P, De Robertis Edward M   Temporal pattern of the posterior expression of Wingless in Drosophila blastoderm Gene expression patterns : GEP, 2011; 11(7): 456-63.
Vorwald-Denholtz, P.P. and De Robertis, E.M.   Temporal pattern of the posterior expression of Wingless in Drosophila Gene Expr Patterns, 2011; 11: 456-463.
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Eivers, E., Demagny, H., Choi, R.H. and De Robertis, E.M.   Phosphorylation of Mad controls competition between Wingless and BMP signaling Science Signaling, 2011; 4: ra68.
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Plouhinec, J.L., Zakin, L. and De Robertis, E.M.   Systems control of BMP morphogen flow in vertebrate embryos Curr. Opin. Genet Dev, 2011; 21: 1-8.
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Ploper Diego, Lee Hojoon X, De Robertis Edward M   Dorsal-Ventral patterning: Crescent is a dorsally secreted Frizzled-related protein that competitively inhibits Tolloid proteases Developmental Biology, 2011; 352: 317-328.
Eivers Edward, Demagny Hadrien, Choi Renee H, De Robertis Edward M   Phosphorylation of Mad controls competition between wingless and BMP signaling Science signaling, 2011; 4(194): ra68.
Taelman Vincent F, Dobrowolski Radoslaw, Plouhinec Jean-Louis, Fuentealba Luis C, Vorwald Peggy P, Gumper Iwona, Sabatini David D, De Robertis Edward M   Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes Cell, 2010; 143(7): 1136-1148.
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Zakin Lise, Chang Ellen Y, Plouhinec Jean-Louis, De Robertis E M   Crossveinless-2 is required for the relocalization of Chordin protein within the vertebral field in mouse embryos Developmental biology, 2010; 347(1): 204-15.
Sander Veronika, Eivers Edward, Choi Renee H, De Robertis Edward M   Drosophila Smad2 opposes Mad signaling during wing vein development PloS one, 2010; 5(4): e10383.
De Robertis Edward M   Wnt signaling in axial patterning and regeneration: lessons from planaria Science signaling, 2010; 3(127): pe21.
Tran Uyen, Zakin Lise, Schweickert Axel, Agrawal Raman, Döger Remziye, Blum Martin, De Robertis E M, Wessely Oliver   The RNA-binding protein bicaudal C regulates polycystin 2 in the kidney by antagonizing miR-17 activity Development (Cambridge, England), 2010; 137(7): 1107-16.
Zakin Lise, De Robertis E M   Extracellular regulation of BMP signaling Current biology : CB, 2010; 20(3): R89-92.
Lee Hojoon X, Mendes Fabio A, Plouhinec Jean-Louis, De Robertis Edward M   Enzymatic regulation of pattern: BMP4 binds CUB domains of Tolloids and inhibits proteinase activity Genes & development, 2009; 23(21): 2551-62.
Lee, H.X., Mendes, F.A., Plouhinec, J.L. and De Robertis, E.M.   Enzymatic regulation of pattern: BMP4 binds CUB domains of Tolloids and inhibits proteinase activity Genes Dev, 2009; 23: 2551-2562.
Eivers, E., Demagny, H. and De Robertis, E.M.   Integration of BMP and Wnt signaling via vertebrate Smad1/5/8 and Drosophila Mad Cytokine Growth F. R, 2009; 20: 357-365.
Fuentealba, L.C., Eivers, E., Geissert, D., Taelman, V. and De Robertis, E.M.   Asymmetric mitosis: Unequal segregation of proteins destined for degradation PNAS, 2008; 105: 7732-7737.
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Ambrosio, A.L., Taelman, V.F., Lee, H.X., Metzinger, C.A., Coffinier, C. and De Robertis, E.M.   Crossveinless-2 is a BMP feedback inhibitor that binds Chordin/BMP to regulate Xenopus embryonic patterning Dev. Cell, 2008; 15: 248-260.
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Zakin, L., Metzinger, C.A., Chang, E.Y., Coffinier, C. and De Robertis, E.M.   Development of the vertebral morphogenetic field in the mouse: interactions between Crossveinless-2 and Twisted gastrulation Dev. Biol, 2008; 323: 6-18.
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De Robertis, E.M.   Evo-Devo: Variations on Ancestral themes Cell, 2008; 132: 185-195.
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De Robertis, E.M.   Evolutionary Biology Commentary: The molecular ancestry of segmentation mechanisms Proc. Natl. Acad. Sci. USA, 2008; 105: 16411-16412.
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Ishibashi, H., Matsumura, N., Hanafusa, H., Matsumoto, K., De Robertis, E.M. and Kuroda, H.   Expression of Siamois and Twin in the blastula Chordin/Noggin signaling center is required for brain formation in Xenopus laevis embryos, Mech. Dev, 2008; 125: 58-66.
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Eivers, E., Fuentealba, L.C. and De Robertis, E.M.   Integrating positional information at the level of Smad1/5/8 Curr. Opin. Genet. Dev. , 2008; 18: 304-310.
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Fuentealba Luis C, Eivers Edward, Ikeda Atsushi, Hurtado Cecilia, Kuroda Hiroki, Pera Edgar M, De Robertis Edward M   Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal Cell, 2007; 131(5): 980-93.
Yasuda, S., Tanaka, H., Sugiura, H., Okamura, K., Sakaguchi, T., Tran, U., Takemiya, T., Mizoguchi, A., Yagita, Y., Sakurai, T., De Robertis, E.M. and Yamagata, K.   Activity-induced protocadherin Arcadlin regulates dendritic spine number by triggering N-Cadherin endocytosis via TAO2β and p38 MAP kinases, Neuron, 2007; 56: 456-471.
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Fuentealba, L.C., Eivers, E., Ikeda, A., Hurtado, C., Kuroda, H., Pera, E.M. and De Robertis, E.M.   Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal Cell, 2007; 131: 980-993.
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Hurtado, C. and De Robertis, E. M.   Neural induction in the absence of organizer in salamanders is mediated by MAPK Dev. Biol, 2007; 307: 282-289.
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Plouhinec, J.-L. and De Robertis, E.M.   Systems biology of embryonic morphogens Mol. Biosyst, 2007; 3: 454-457.
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Sander, V., Reversade, B. and De Robertis E.M.   The opposing homeobox genes Goosecoid and Vent1/2 self-regulate Xenopus patterning EMBO J, 2007; 26: 2955-2965.
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Lee HX, Ambrosio AL, Reversade B, De Robertis EM   Embyonic dorsal-ventral signaling: secreted Frizzled-related proteins as inhibitors of Tolloid proteases Cell, 2006; 124: 147-159.
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De Robertis EM   Spemann's organizer and self-regulation in amphibian embryos Nature Reviews Molecular Cell Biology, 2006; 7: 296-302.
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De Robertis Edward M   Spemann's organizer and self-regulation in amphibian embryos Nature reviews. Molecular cell biology, 2006; 7(4): 296-302.
Wessely O, Kim JI, Tran U, Fuentealba L, De Robertis EM   xBtg-x regulates Wnt/beta-Catenin signaling during early Xenopus development Developmental biology. , 2005; 283(1): 17-28.
Reversade B, Kuroda H, Lee H, Mays A, De Robertis EM   Depletion of BMP2, 4, 7 and Spemann organizer signals induces massive brain formation in Xenopus embryo Development, 2005; 132: 3381-3392.
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Pera EM, Hou S, Strate I, Wessely O, De Robertis EM   Exploration of the extracellular space by a large-scale secretion screen in the early Xenopus embryo Int. J. Dev. Biol, 2005; 49: 781-796.
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Reversade B, De Robertis EM   Formation of a self-differentiating morphogenetic field via reciprocal regulation of Admp and Bmp2/4/7 at opposite poles of the Xenopus embryo Cell, 2005; 123: 1147-1160.
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Zakin L, Reversade B, Kuroda H, Lyons KM, De Robertis EM   Sirenomelia in Bmp7 and Twisted gastrulation composed mutant mice: requirement for Bmp signaling in the development of ventral posterior mesoderm Development, 2005; 132: 2489-2499.
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Kuroda H, Fuentealba L, Ikeda A, Reversade B, De Robertis EM   Default neural induction: neuralization of dissociated Xenopus cells is mediated by Ras/MAPK activation Genes & development. , 2005; 19(9): 1022-7.
Unterseher F, Hefele JA, Giehl K, De Robertis EM, Wedlich D, Schambony A   Paraxial protocadherin coordinates cell polarity during convergent extension via Rho A and JNK Embo J, 2004; 23(16): 3259-69.
De Robertis EM, Kuroda H   Dorsal-ventral patterning and neural induction in Xenopus embryos Annual Review of Cell and Developmental Biology. , 2004; 20: 285-308.
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Oelgeschlager M, Tran U, Grubisic K, De Robertis EM   Identification of a second Xenopus twisted gastrulation gene Int J Dev Biol, 2004; 48(1): 57-61.
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Wessely O, Kim JI, Geissert D, Tran U, De Robertis EM   Analysis of Spemann organizer formation in Xenopus embryos by cDNA macroarrays Developmental biology. , 2004; 269(2): 552-66.
Kuroda H, Wessely O, De Robertis EM   Neural induction in Xenopus: requirement for ectodermal and endomesodermal signals via Chordin, Noggin, beta-Catenin, and Cerberus PLoS biology. , 2004; 2(5): E92.
Zakin L, De Robertis EM   Inactivation of mouse Twisted gastrulation reveals its role in promoting Bmp4 activity during forebrain development Development (Cambridge, England) , 2004; 131(2): 413-24.
Pera EM, Ikeda A, Eivers E, De Robertis EM   Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction Genes & development. , 2003; 17(24): 3023-8.
Bachiller D, Klingensmith J, Shneyder N, Tran U, Anderson R, Rossant J, De Robertis EM   The role of chordin/Bmp signals in mammalian pharyngeal development and DiGeorge syndrome Development (Cambridge, England) , 2003; 130(15): 3567-78.
Oelgeschlager M, Kuroda H, Reversade B, De Robertis EM   Chordin is required for the Spemann organizer transplantation phenomenon in Xenopus embryos Dev Cell, 2003; 4(2): 219-30.
Larrain J, Brown C, De Robertis EM   Integrin-alpha3 mediates binding of Chordin to the cell surface and promotes its endocytosis EMBO Rep, 2003; 4(8): 813-8.
Oelgeschlager M, Reversade B, Larrain J, Little S, Mullins MC, De Robertis EM   The pro-BMP activity of Twisted gastrulation is independent of BMP binding Development, 2003; 130(17): 4047-56.
Pera EM, Martinez SL, Flanagan JJ, Brechner M, Wessely O, De Robertis EM   Darmin is a novel secreted protein expressed during endoderm development in Xenopus Gene expression patterns : GEP. , 2003; 3(2): 147-52.
Coffinier C, Ketpura N, Tran U, Geissert D, De Robertis EM   Mouse Crossveinless-2 is the vertebrate homolog of a Drosophila extracellular regulator of BMP signaling Mechanisms of development. , 2002; 119 Suppl 1: S179-84.
Pera EM, Kim JI, Martinez SL, Brechner M, Li SY, Wessely O, De Robertis EM   Isthmin is a novel secreted protein expressed as part of the Fgf-8 synexpression group in the Xenopus midbrain-hindbrain organizer Mechanisms of development. , 2002; 116(1-2): 169-72.
Garcia Abreu J, Coffinier C, Larrain J, Oelgeschlager M, De Robertis EM   Chordin-like CR domains and the regulation of evolutionarily conserved extracellular signaling systems Gene, 2002; 287(1-2): 39-47.
Abreu JG, Ketpura NI, Reversade B, De Robertis EM   Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta Nat Cell Biol, 2002; 4(8): 599-604.
Wessely O, De Robertis EM   Neural plate patterning by secreted signals Neuron. , 2002; 33(4): 489-91.
Pera EM, Wessely O, Li SY, De Robertis EM   Neural and head induction by insulin-like growth factor signals Developmental cell. , 2001; 1(5): 655-65.
Pera EM, Wessely O, Li SY, De Robertis EM   Neural and head induction by insulin-like growth factor signals Developmental cell. , 2001; 1(5): 655-65.
De Robertis EM, Bouwmeester T   New twists on embryonic patterning. EMBO workshop: embryonic organizer signaling: the next frontiers EMBO reports. , 2001; 2(8): 661-5.
De Robertis EM, Wessely O, Oelgeschlager M, Brizuela B, Pera E, Larrain J, Abreu J, Bachiller D   Molecular mechanisms of cell-cell signaling by the Spemann-Mangold organizer Int J Dev Biol, 2001; 45(1): 189-97.
Wessely O, Agius E, Oelgeschlager M, Pera EM, De Robertis EM   Neural induction in the absence of mesoderm: beta-catenin-dependent expression of secreted BMP antagonists at the blastula stage in Xenopus Dev Biol, 2001; 234(1): 161-73.
Coffinier C, Tran U, Larrain J, De Robertis EM   Neuralin-1 is a novel Chordin-related molecule expressed in the mouse neural plate Mech Dev, 2001; 100(1): 119-22.
Larrain J, Oelgeschlager M, Ketpura NI, Reversade B, Zakin L, De Robertis EM   Proteolytic cleavage of Chordin as a switch for the dual activities of Twisted gastrulation in BMP signaling Development, 2001; 128(22): 4439-47.
Wessely O, Tran U, Zakin L, De Robertis EM   Identification and expression of the mammalian homologue of Bicaudal-C Mechanisms of development. , 2001; 101(1-2): 267-70.
Brizuela BJ, Wessely O, De Robertis EM   Overexpression of the Xenopus tight-junction protein claudin causes randomization of the left-right body axis Developmental biology. , 2001; 230(2): 217-29.
Pera EM, De Robertis EM   A direct screen for secreted proteins in Xenopus embryos identifies distinct activities for the Wnt antagonists Crescent and Frzb-1 Mechanisms of development. , 2000; 96(2): 183-95.
Kim SH, Jen WC, De Robertis EM, Kintner C   The protocadherin PAPC establishes segmental boundaries during somitogenesis in xenopus embryos Current biology : CB. , 2000; 10(14): 821-30.
Larrain J, Bachiller D, Lu B, Agius E, Piccolo S, De Robertis EM   BMP-binding modules in chordin: a model for signalling regulation in the extracellular space Development, 2000; 127(4): 821-30.
Belo JA, Bachiller D, Agius E, Kemp C, Borges AC, Marques S, Piccolo S, De Robertis EM   Cerberus-like is a secreted BMP and nodal antagonist not essential for mouse development Genesis, 2000; 26(4): 265-70.
Agius E, Oelgeschlager M, Wessely O, Kemp C, De Robertis EM   Endodermal Nodal-related signals and mesoderm induction in Xenopus Development, 2000; 127(6): 1173-83.
Yamamoto A, Kemp C, Bachiller D, Geissert D, De Robertis EM   Mouse paraxial protocadherin is expressed in trunk mesoderm and is not essential for mouse development Genesis, 2000; 27(2): 49-57.
De Robertis EM, Larrain J, Oelgeschlager M, Wessely O   The establishment of Spemann's organizer and patterning of the vertebrate embryo Nat Rev Genet, 2000; 1(3): 171-81.
De Robertis EM, Larrain J, Oelgeschlager M, Wessely O   The establishment of Spemann?s Organizer and patterning of the vertebrate embryo, Nature Reviews Genetics, 2000; 1, 171-181.
Oelgeschlager M, Larrain J, Geissert D, De Robertis EM   The evolutionarily conserved BMP-binding protein Twisted gastrulation promotes BMP signalling Nature, 2000; 405(6788): 757-63.
Oelgeschlager M, Larrain J, Geissert D, De Robertis EM   The evolutionary conserved BMP-binding protein Twisted Gastrulation promotes BMP signalling, Nature, 2000; 405, 757-763.
Wessely O, De Robertis EM   The Xenopus homologue of Bicaudal-C is a localized maternal mRNA that can induce endoderm formation Development (Cambridge, England) , 2000; 127(10): 2053-62.
Bachiller D, Klingensmith J, Kemp C, Belo JA, Anderson RM, May SR, McMahon JA, McMahon AP, Harland RM, Rossant J, De Robertis EM   The organizer factors Chordin and Noggin are required for mouse forebrain development Nature. , 2000; 403(6770): 658-61.
Bachiller D, Klingensmith J, Kemp C, Belo JA, Anderson RM, May SR, McMahon JA, McMahon AP, Harland RM, Rossant J, De Robertis EM   The organizer factors Chordin and Noggin are required for mouse forebrain development Nature. , 2000; 403(6770): 658-61.
Duprez D, Leyns L, Bonnin MA, Lapointe F, Etchevers H, De Robertis EM, Le Douarin N   Expression of Frzb-1 during chick development Mechanisms of development. , 1999; 89(1-2): 179-83.
Zhu L, Belo JA, De Robertis EM, Stern CD   Goosecoid regulates the neural inducing strength of the mouse node Developmental biology. , 1999; 216(1): 276-81.
Konishi Y, Tominaga M, Watanabe Y, Imamura F, Goldfarb A, Maki R, Blum M, De Robertis EM, Tominaga A   GOOSECOID inhibits erythrocyte differentiation by competing with Rb for PU.1 binding in murine cells Oncogene. , 1999; 18(48): 6795-805.
De Robertis EM   A nose for the embryo: the work of Pieter Nieuwkoop The International journal of developmental biology. , 1999; 43(7): 603-4.
Agius PE, Piccolo S, De Robertis EM   [The head inducer Cerberus in a multivalent extracellular inhibitor] J Soc Biol, 1999; 193(4-5): 347-54.
Piccolo S, Agius E, Leyns L, Bhattacharyya S, Grunz H, Bouwmeester T, De Robertis EM   The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals Nature. , 1999; 397(6721): 707-10.
Piccolo S, Agius E, Leyns L, Bhattacharyya S, Grunz H, Bouwmeester T, De Robertis EM   The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals Nature. , 1999; 397(6721): 707-10.
Yamamoto A, Amacher SL, Kim SH, Geissert D, Kimmel CB, De Robertis EM   Zebrafish paraxial protocadherin is a downstream target of spadetail involved in morphogenesis of gastrula mesoderm Development (Cambridge, England) , 1998; 125(17): 3389-97.
Blumberg B, Kang H, Bolado Jr. J, Chen H, Craig AG, Moreno TA, Umesono K, Perlmann T, De Robertis EM, Evans RM   BXR, an embryonic orphan nuclear receptor activated by a novel class of endogenous benzoate metabolites Genes Dev, 1998; 12(9): 1269-77.
Belo JA, Leyns L, Yamada G, De Robertis EM   The prechordal midline of the chondrocranium is defective in Goosecoid-1 mouse mutants Mechanisms of development. , 1998; 72(1-2): 15-25.
Pillemer G, Epstein M, Blumberg B, Yisraeli JK, De Robertis EM, Steinbeisser H, Fainsod A   Nested expression and sequential downregulation of the Xenopus caudal genes along the anterior-posterior axis Mechanisms of development. , 1998; 71(1-2): 193-6.
Heanue TA, Johnson RL, Izpisua-Belmonte JC, Stern CD, De Robertis EM, Tabin CJ   Goosecoid misexpression alters the morphology and Hox gene expression of the developing chick limb bud Mechanisms of development. , 1997; 69(1-2): 31-7.
Belo JA, Bouwmeester T, Leyns L, Kertesz N, Gallo M, Follettie M, De Robertis EM   Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula Mechanisms of development. , 1997; 68(1-2): 45-57.
Piccolo S, Agius E, Lu B, Goodman S, Dale L, De Robertis EM   Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity Cell. , 1997; 91(3): 407-16.
Sasai Y, De Robertis EM   Ectodermal patterning in vertebrate embryos Dev Biol, 1997; 182(1): 5-20.
De Robertis EM   Evolutionary biology. The ancestry of segmentation Nature, 1997; 387(6628): 25-6.
De Robertis EM, Kim S, Leyns L, Piccolo S, Bachiller D, Agius E, Belo JA, Yamamoto A, Hainski-Brousseau A, Brizuela B, Wessely O, Lu B, Bouwmeester T   Patterning by genes expressed in Spemann's organizer Cold Spring Harb Symp Quant Biol, 1997; 62: 169-75.
Pfeffer PL, De Robertis EM, Izpisua-Belmonte JC   Crescent, a novel chick gene encoding a Frizzled-like cysteine-rich domain, is expressed in anterior regions during early embryogenesis The International journal of developmental biology. , 1997; 41(3): 449-58.
Leyns L, Bouwmeester T, Kim SH, Piccolo S, De Robertis EM   Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer Cell. , 1997; 88(6): 747-56.
Sasai Y, Lu B, Piccolo S, De Robertis EM   Endoderm induction by the organizer-secreted factors chordin and noggin in Xenopus animal caps The EMBO journal. , 1996; 15(17): 4547-55.
Catala M, Teillet MA, De Robertis EM, Le Douarin ML   A spinal cord fate map in the avian embryo: while regressing, Hensen's node lays down the notochord and floor plate thus joining the spinal cord lateral walls Development (Cambridge, England) , 1996; 122(9): 2599-610.
Piccolo S, Sasai Y, Lu B, De Robertis EM   Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4 Cell. , 1996; 86(4): 589-98.
Holley SA, Neul JL, Attisano L, Wrana JL, Sasai Y, O'Connor MB, De Robertis EM, Ferguson EL   The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor Cell. , 1996; 86(4): 607-17.
Bouwmeester T, Kim S, Sasai Y, Lu B, De Robertis EM   Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer Nature, 1996; 382(6592): 595-601.
De Robertis EM, Sasai Y   A common plan for dorsoventral patterning in Bilateria Nature. , 1996; 380(6569): 37-40.
Gont LK, Fainsod A, Kim SH, De Robertis EM   Overexpression of the homeobox gene Xnot-2 leads to notochord formation in Xenopus Developmental biology. , 1996; 174(1): 174-8.
Sasal Y, Lu B, Steinbelsser H, De Robertis EM   Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus Nature. , 1995; 378(6555): 419.
Steinbeisser H, Fainsod A, Niehrs C, Sasai Y, De Robertis EM   The role of gsc and BMP-4 in dorsal-ventral patterning of the marginal zone in Xenopus: a loss-of-function study using antisense RNA The EMBO journal. , 1995; 14(21): 5230-43.
Sasai Y, Lu B, Steinbeisser H, De Robertis EM   Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus Nature. , 1995; 377(6551): 757.
Yamada G, Mansouri A, Torres M, Stuart ET, Blum M, Schultz M, De Robertis EM, Gruss P   Targeted mutation of the murine goosecoid gene results in craniofacial defects and neonatal death Development (Cambridge, England) , 1995; 121(9): 2917-22.
Holley SA, Jackson PD, Sasai Y, Lu B, De Robertis EM, Hoffmann FM, Ferguson EL   A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin Nature. , 1995; 376(6537): 249-53.
Guenet JL, Simon-Chazottes D, de Robertis E, Blum M   The mouse goosecoid gene (Gsc) maps to the telomeric part of mouse chromosome 12 Mamm Genome, 1995; 6(11): 816-7.
De Robertis EM   Developmental biology. Dismantling the organizer Nature. , 1995; 374(6521): 407-8.
Sasai Y, Lu B, Steinbeisser H, Geissert D, Gont LK, De Robertis EM   Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes Cell. , 1994; 79(5): 779-90.
Schulte-Merker S, Hammerschmidt M, Beuchle D, Cho KW, De Robertis EM, Nusslein-Volhard C   Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos Development, 1994; 120(4): 843-52.
Niehrs C, Steinbeisser H, De Robertis EM   Mesodermal patterning by a gradient of the vertebrate homeobox gene goosecoid Science, 1994; 263(5148): 817-20.
Fainsod A, Steinbeisser H, De Robertis EM   On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo Embo J, 1994; 13(21): 5015-25.
De Robertis EM, Fainsod A, Gont LK, Steinbeisser H   The evolution of vertebrate gastrulation Dev Suppl, 1994; 117-24.
Blum M, De Robertis EM, Kojis T, Heinzmann C, Klisak I, Geissert D, Sparkes RS   Molecular cloning of the human homeobox gene goosecoid (GSC) and mapping of the gene to human chromosome 14q32.1 Genomics. , 1994; 21(2): 388-93.
Pfeffer PL, De Robertis EM   Regional specificity of RAR gamma isoforms in Xenopus development Mechanisms of development. , 1994; 45(2): 147-53.
Jones FS, Holst BD, Minowa O, De Robertis EM, Edelman GM   Binding and transcriptional activation of the promoter for the neural cell adhesion molecule by HoxC6 (Hox-3.3) Proceedings of the National Academy of Sciences of the United States of America. , 1993; 90(14): 6557-61.
Gaunt SJ, Blum M, De Robertis EM   Expression of the mouse goosecoid gene during mid-embryogenesis may mark mesenchymal cell lineages in the developing head, limbs and body wall Development, 1993; 117(2): 769-78.
Gont LK, Steinbeisser H, Blumberg B, de Robertis EM   Tail formation as a continuation of gastrulation: the multiple cell populations of the Xenopus tailbud derive from the late blastopore lip Development, 1993; 119(4): 991-1004.
Izpisua-Belmonte JC, De Robertis EM, Storey KG, Stern CD   The homeobox gene goosecoid and the origin of organizer cells in the early chick blastoderm Cell, 1993; 74(4): 645-59.
Steinbeisser H, De Robertis EM   Xenopus goosecoid: a gene expressed in the prechordal plate that has dorsalizing activity C R Acad Sci III, 1993; 316(9): 959-71.
Steinbeisser H, De Robertis EM, Ku M, Kessler DS, Melton DA   Xenopus axis formation: induction of goosecoid by injected Xwnt-8 and activin mRNAs Development (Cambridge, England) , 1993; 118(2): 499-507.
Niehrs C, Keller R, Cho KW, De Robertis EM   The homeobox gene goosecoid controls cell migration in Xenopus embryos Cell. , 1993; 72(4): 491-503.
Bittner D, De Robertis EM, Cho KW   Characterization of the Xenopus Hox 2.4 gene and identification of control elements in its intron Developmental dynamics : an official publication of the American Association of Anatomists. , 1993; 196(1): 11-24.
Jegalian BG, De Robertis EM   Homeotic transformations in the mouse induced by overexpression of a human Hox3.3 transgene Cell. , 1992; 71(6): 901-10.
Jegalian BG, Miller RW, Wright CV, Blum M, De Robertis EM   A Hox 3.3-lacZ transgene expressed in developing limbs Mechanisms of development. , 1992; 39(3): 171-80.
Blum M, Gaunt SJ, Cho KW, Steinbeisser H, Blumberg B, Bittner D, De Robertis EM   Gastrulation in the mouse: the role of the homeobox gene goosecoid Cell. , 1992; 69(7): 1097-106.
Niehrs C, De Robertis EM   Vertebrate axis formation Curr Opin Genet Dev, 1992; 2(4): 550-5.
Leroy P, De Robertis EM   Effects of lithium chloride and retinoic acid on the expression of genes from the Xenopus laevis Hox 2 complex Developmental dynamics : an official publication of the American Association of Anatomists. , 1992; 194(1): 21-32.
Jones FS, Prediger EA, Bittner DA, De Robertis EM, Edelman GM   Cell adhesion molecules as targets for Hox genes: neural cell adhesion molecule promoter activity is modulated by cotransfection with Hox-2.5 and -2.4 Proceedings of the National Academy of Sciences of the United States of America. , 1992; 89(6): 2086-90.
Blumberg B, Mangelsdorf DJ, Dyck JA, Bittner DA, Evans RM, De Robertis EM   Multiple retinoid-responsive receptors in a single cell: families of retinoid "X" receptors and retinoic acid receptors in the Xenopus egg Proceedings of the National Academy of Sciences of the United States of America. , 1992; 89(6): 2321-5.
Storey KG, Crossley JM, De Robertis EM, Norris WE, Stern CD   Neural induction and regionalisation in the chick embryo Development (Cambridge, England) , 1992; 114(3): 729-41.
Cho KW, Blumberg B, Steinbeisser H, De Robertis EM   Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid Cell. , 1991; 67(6): 1111-20.
Niehrs C, De Robertis EM   Ectopic expression of a homeobox gene changes cell fate in Xenopus embryos in a position-specific manner The EMBO journal. , 1991; 10(12): 3621-9.
Blumberg B, Wright CV, De Robertis EM, Cho KW   Organizer-specific homeobox genes in Xenopus laevis embryos Science. , 1991; 253(5016): 194-6.
De Robertis EM, Morita EA, Cho KW   Gradient fields and homeobox genes Development (Cambridge, England) , 1991; 112(3): 669-78.
Cho KW, Morita EA, Wright CV, De Robertis EM   Overexpression of a homeodomain protein confers axis-forming activity to uncommitted Xenopus embryonic cells Cell. , 1991; 65(1): 55-64.
Chuong CM, Oliver G, Ting SA, Jegalian BG, Chen HM, De Robertis EM   Gradients of homeoproteins in developing feather buds Development (Cambridge, England) , 1990; 110(4): 1021-30.
Jegalian BG, De Robertis EM   The Xenopus laevis Hox 2.1 homeodomain protein is expressed in a narrow band of the hindbrain The International journal of developmental biology. , 1990; 34(4): 453-6.
Cho KW, De Robertis EM   Differential activation of Xenopus homeo box genes by mesoderm-inducing growth factors and retinoic acid Genes & development. , 1990; 4(11): 1910-6.
Oliver G, De Robertis EM, Wolpert L, Tickle C   Expression of a homeobox gene in the chick wing bud following application of retinoic acid and grafts of polarizing region tissue The EMBO journal. , 1990; 9(10): 3093-9.
Livingston BD, De Robertis EM, Paulson JC   Expression of beta-galactoside alpha 2,6 sialyltransferase blocks synthesis of polysialic acid in Xenopus embryos Glycobiology. , 1990; 1(1): 39-44.
De Robertis EM, Oliver G, Wright CV   Homeobox genes and the vertebrate body plan Sci Am, 1990; 263(1): 46-52.
Molven A, Wright CV, Bremiller R, De Robertis EM, Kimmel CB   Expression of a homeobox gene product in normal and mutant zebrafish embryos: evolution of the tetrapod body plan Development (Cambridge, England) , 1990; 109(2): 279-88.
Wright CV, Morita EA, Wilkin DJ, De Robertis EM   The Xenopus XIHbox 6 homeo protein, a marker of posterior neural induction, is expressed in proliferating neurons Development (Cambridge, England) , 1990; 109(1): 225-34.
Wright CV, Cho KW, Hardwicke J, Collins RH, De Robertis EM   Interference with function of a homeobox gene in Xenopus embryos produces malformations of the anterior spinal cord Cell. , 1989; 59(1): 81-93.
Wright CV, Schnegelsberg P, De Robertis EM   XlHbox 8: a novel Xenopus homeo protein restricted to a narrow band of endoderm Development, 1989; 105(4): 787-94.
Oliver G, Sidell N, Fiske W, Heinzmann C, Mohandas T, Sparkes RS, De Robertis EM   Complementary homeo protein gradients in developing limb buds Genes & development. , 1989; 3(5): 641-50.
De Robertis EM, Oliver G, Wright CV   Determination of axial polarity in the vertebrate embryo: homeodomain proteins and homeogenetic induction Cell. , 1989; 57(2): 189-91.
Fritz AF, Cho KW, Wright CV, Jegalian BG, De Robertis EM   Duplicated homeobox genes in Xenopus Developmental biology. , 1989; 131(2): 584-8.
Wright CV, Cho KW, Oliver G, De Robertis EM   Vertebrate homeodomain proteins: families of region-specific transcription factors Trends in biochemical sciences. , 1989; 14(2): 52-6.
Oliver G, Wright CV, Hardwicke J, De Robertis EM   A gradient of homeodomain protein in developing forelimbs of Xenopus and mouse embryos Cell. , 1988; 55(6): 1017-24.
Fritz AF, Martin G, Wright CV, De Robertis EM   Site-specific inversions in repeated Xenopus laevis homeobox gene 2 sequences Nucleic acids research. , 1988; 16(18): 9058.
Cho KW, Goetz J, Wright CV, Fritz A, Hardwicke J, De Robertis EM   Differential utilization of the same reading frame in a Xenopus homeobox gene encodes two related proteins sharing the same DNA-binding specificity The EMBO journal. , 1988; 7(7): 2139-49.
Oliver G, Wright CV, Hardwicke J, De Robertis EM   Differential antero-posterior expression of two proteins encoded by a homeobox gene in Xenopus and mouse embryos Embo J, 1988; 7(10): 3199-209.
De Robertis EM, Burglin TR, Fritz A, Oliver G, Cho K, Wright CV   Sequence conservations in vertebrate homeo-box mRNAs Arch Biol Med Exp (Santiago), 1988; 21(3-4): 443-7.
Fritz A, De Robertis EM   Xenopus homeobox-containing cDNAs expressed in early development Nucleic acids research. , 1988; 16(4): 1453-69.
Sharpe CR, Fritz A, De Robertis EM, Gurdon JB   A homeobox-containing marker of posterior neural differentiation shows the importance of predetermination in neural induction Cell. , 1987; 50(5): 749-58.
Mattaj IW, Coppard NJ, Brown RS, Clark BF, De Robertis EM   42S p48--the most abundant protein in previtellogenic Xenopus oocytes--resembles elongation factor 1 alpha structurally and functionally Embo J, 1987; 6(8): 2409-13.
Wright CV, Cho KW, Fritz A, Burglin TR, De Robertis EM   A Xenopus laevis gene encodes both homeobox-containing and homeobox-less transcripts Embo J, 1987; 6(13): 4083-94.
Burglin TR, De Robertis EM   The nuclear migration signal of Xenopus laevis nucleoplasmin Embo J, 1987; 6(9): 2617-25.
Burglin TR, Wright CV, De Robertis EM   Translational control in homoeobox mRNAs? Nature, 1987; 330(6150): 701-2.
Newmeyer DD, Lucocq JM, Burglin TR, De Robertis EM   Assembly in vitro of nuclei active in nuclear protein transport: ATP is required for nucleoplasmin accumulation Embo J, 1986; 5(3): 501-10.
Mattaj IW, Lienhard S, Jiricny J, De Robertis EM   An enhancer-like sequence within the Xenopus U2 gene promoter facilitates the formation of stable transcription complexes Nature. , 1985; 316(6024): 163-7.
Mattaj IW, Zeller R, Carrasco AE, Jamrich M, Lienhard S, De Robertis EM   U snRNA gene families in Xenopus laevis Oxford surveys on eukaryotic genes. , 1985; 2: 121-40.
Mattaj IW, De Robertis EM   Nuclear segregation of U2 snRNA requires binding of specific snRNP proteins Cell. , 1985; 40(1): 111-8.
Fritz A, Parisot R, Newmeyer D, De Robertis EM   Small nuclear U-ribonucleoproteins in Xenopus laevis development. Uncoupled accumulation of the protein and RNA components Journal of molecular biology. , 1984; 178(2): 273-85.
Carrasco AE, McGinnis W, Gehring WJ, De Robertis EM   Cloning of an X. laevis gene expressed during early embryogenesis coding for a peptide region homologous to Drosophila homeotic genes Cell, 1984; 37(2): 409-14.
Shepherd JC, McGinnis W, Carrasco AE, De Robertis EM, Gehring WJ   Fly and frog homoeo domains show homologies with yeast mating type regulatory proteins Nature. , 1984; 310(5972): 70-1.
Zeller R, Carri MT, Mattaj IW, De Robertis EM   Xenopus laevis U1 snRNA genes: characterisation of transcriptionally active genes reveals major and minor repeated gene families The EMBO journal. , 1984; 3(5): 1075-81.
Zeller R, Nyffenegger T, De Robertis EM   Nucleocytoplasmic distribution of snRNPs and stockpiled snRNA-binding proteins during oogenesis and early development in Xenopus laevis Cell. , 1983; 32(2): 425-34.
Matter L, Schopfer K, Wilhelm JA, Nyffenegger T, Parisot RF, De Robertis EM   Molecular characterization of ribonucleoprotein antigens bound by antinuclear antibodies. A diagnostic evaluation Arthritis and rheumatism. , 1982; 25(11): 1278-83.
Nishikura K, Kurjan J, Hall BD, De Robertis EM   Genetic analysis of the processing of a spliced tRNA Embo J, 1982; 1(2): 263-8.
De Robertis EM, Lienhard S, Parisot RF   Intracellular transport of microinjected 5S and small nuclear RNAs Nature. , 1982; 295(5850): 572-7.
Nishikura K, De Robertis EM   RNA processing in microinjected Xenopus oocytes. Sequential addition of base modifications in the spliced transfer RNA Journal of molecular biology. , 1981; 145(2): 405-20.
De Robertis EM, Black P, Nishikura K   Intranuclear location of the tRNA splicing enzymes Cell. , 1981; 23(1): 89-93.
Melton DA, Cortese R, de Robertis EM, Trendelenburg MF, Gurdon JB   Gene injection into amphibian oocytes Results Probl Cell Differ, 1980; 11: 8-14.
Mills AD, Laskey RA, Black P, De Robertis EM   An acidic protein which assembles nucleosomes in vitro is the most abundant protein in Xenopus oocyte nuclei Journal of molecular biology. , 1980; 139(3): 561-8.
Melton DA, De Robertis EM, Cortese R   Order and intracellular location of the events involved in the maturation of a spliced tRNA Nature. , 1980; 284(5752): 143-8.
De Robertis EM, Gurdon JB   Gene transplantation and the analysis of development Sci Am, 1979; 241(6): 74-82.
Gurdon JB, Melton DA, De Robertis EM   Genetics in an oocyte Ciba Found Symp, 1979; (66): 63-80.
De Robertis EM   Probing the program of gene expression utilized in early development Arch Biol Med Exp (Santiago), 1979; 12(3): 325-9.
Gurdon JB, Laskey RA, De Robertis EM, Partington GA   Reprogramming of transplanted nuclei in amphibia International review of cytology. Supplement. , 1979; (9): 161-78.
De Robertis EM, Olson MV   Transcription and processing of cloned yeast tyrosine tRNA genes microinjected into frog oocytes Nature. , 1979; 278(5700): 137-43.
de Robertis EM, Black P   Hybrids of Xenopus laevis and Xenopus borealis express proteins from both parents Developmental biology. , 1979; 68(1): 334-9.
Gurdon JB, Wyllie AH, De Robertis EM   The transcription and translation of DNA injected into oocytes Philos Trans R Soc Lond B Biol Sci, 1978; 283(997): 367-72.
De Robertis EM, Partington GA, Gurdon JB   Selective gene expression by somatic nuclei injected into amphibian oocytes Philosophical transactions of the Royal Society of London. Series B, Biological sciences. , 1978; 283(997): 375-7.
De Robertis EM, Longthorne RF, Gurdon JB   Intracellular migration of nuclear proteins in Xenopus oocytes Nature. , 1978; 272(5650): 254-6.
De Robertis EM, Mertz JE   Coupled transcription-translation of DNA injected into Xenopus oocytes Cell. , 1977; 12(1): 175-82.
De Robertis EM, Partington GA, Longthorne RF, Gurdon JB   Somatic nuclei in amphibian oocytes: evidence for selective gene expression Journal of embryology and experimental morphology. , 1977; 40: 199-214.
De Robertis EM, Gurdon JB, Partington GA, Mertz JE, Laskey RA   Injected amphibian oocytes: a living test tube for the study of eukaryotic gene transcription? Biochemical Society symposium. , 1977; (42): 181-91.
De Robertis EM, Gurdon JB   Gene activation in somatic nuclei after injection into amphibian oocytes Proceedings of the National Academy of Sciences of the United States of America. , 1977; 74(6): 2470-4.
Wyllie AH, De Robertis EM   High tyrosinase activity in albino Xenopus laevis oocytes Journal of embryology and experimental morphology. , 1976; 36(3): 555-9.
Gurdon JB, Partington GA, De Robertis EM   Injected nuclei in frog oocytes:RNA synthesis and protein exchange Journal of embryology and experimental morphology. , 1976; 36(3): 541-53.
De Robertis EM, Jr. Judewicz ND, Torres HN   Regulation of uracil uptake in Escherichia coli by adenosine 3',5'-monophosphate Biochim Biophys Acta, 1976; 426(3): 451-63.
Gurdon JB, De Robertis EM, Partington G   Injected nuclei in frog oocytes provide a living cell system for the study of transcriptional control Nature, 1976; 260(5547): 116-20.
Judewicz ND, De Robertis EM, Jr. Torres HN   Control of uracil transport by cyclic AMP in E. coli FEBS Lett, 1974; 45(1): 155-8.
Judewicz ND, De Robertis EM, Torres HN   Inhibition of Escherichia coli growth by cyclic adenosine 3', 5'-monophosphate Biochemical and biophysical research communications. , 1973; 52(4): 1257-62.
De Robertis EM, Ezcurra PM, Judewicz ND, Pucci PR, Torres HN   Inhibition of E. coli RNA polymerase by polyadenylic acid FEBS Lett, 1972; 25(1): 175-178.
Narbaitz R, De Robertis EM   Steroid-producing cells in chick intersexual gonads General and comparative endocrinology. , 1970; 14(1): 164-9.

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