Personnel > Research center

Izpisúa Belmonte, Juan Carlos

Izpisúa Belmonte, Juan Carlos

Our Director

izpisua@cmrb.eu


Juan Carlos Izpisúa Belmonte, professor in the Gene Expression Laboratory, studies how genes and molecules orchestrate the development of an embryo. The questions addressed by the laboratory include: How does one cell give rise to millions of cells, and how do they come to be organized into complete structures such as limbs, a heart or brain? How stems cells differentiate and give rise to over 200 cell types that constitute the human body? How certain animals are able to regenerate their tissues and organs, i.e., what are the genetic pathways responsible for epimorphic regeneration, a complex biological process by which animals can regenerate tissues and even entire organs throughout their lifetime after injury or amputation?

The Izpisúa Belmonte laboratory utilizes different in vivo (mouse, chick, frog, and axolotl) and in vitro (human and mouse stem cells) model systems, as well as in silico modeling approaches, with particular emphasis on the genetic pathways involved in heart and bone development and regeneration. Their research has helped to discover some of the molecules that instruct embryonic stem cells to give rise to specific cell types during embryo development, and how these cells interact with one another to form tissues and organs with proper morphology and function. This ensures that our body's organs develop and function correctly and, at the same time, are placed in their correct positions.



The research activities of Dr. Izpisúa Belmonte's laboratory are relevant to understanding the causes that underlie human birth defects, as well as to the future development of regenerative medicine

Selected Publications

  • Montserrat N, Jopling C, Izpisúa Belmonte JC. (2010) Understanding the molecular basis for cardiomyocyte cell cycle regulation: new insights in cardiac regeneration after injury? Expert Rev Cardiovasc Ther, Aug 8(8): 1043-5.
  • Masip M, Veiga A, Izpisúa JC, Simón C. (2010) Reprogramming with defined factors: from induced pluripotency to induced transdifferentiation. Mol Hum Reprod. Jul 8. [Epub ahead of print]
  • Isaacs MJ, Kawakami Y, Allendorph GP, Yoon B, Izpisúa Belmonte JC, and Choe S. (2010) Bone morphogenetic protein-2 and -6 heterodimer illustrates the nature of ligand-receptor assembly. Molecular Endocrinology, Jul 24(7): 1469-77.
  • Sleep E, Boué S, Jopling C, Raya M, Raya A, Izpisúa Belmonte, JC. (2010) Transcriptomics approach to investigate zebrafish heart regeneration. J Cardiovasc Med (Hagerstown) May, 11(5): 369-80.
  • Giorgetti A, Montserrat N, Rodriguez-Piza I, Azqueta C, Veiga A, Izpisúa Belmonte, JC. (2010) Generation of induced pluripotent stem cells from human cord blood cells with only two factors: Oct4 and Sox2. Nature Protocols 5(4): 811-20.
  • Raya, A, Rodriguez-Piza, I, Navarro, S, Richaud, Y, Guenechea, G, Sanchez-Danes, A, Consiglio, A, Bueren, J and Izpisúa Belmonte, JC. (2010) A protocol describing the genetic correction of somatic human cells and subsequent generation of iPS cells. Nature Protocols 5(4): 647-60.
  • Chris Jopling, Eduard Sleep, Marina Raya, Mercè Martí, Angel Raya & Izpisúa Belmonte JC. (2010) Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature Mar 25; 464 (7288): 606-9.
  • Michael J. Edel, Cristina Menchón, Sergio Menéndez, Antonella Consiglio, Angel Raya, and Izpisúa Belmonte JC. (2010) Rem2 GTPase maintains survival of human embryonic stem cells as well as enhancing reprogramming by regulating p53 and cyclin D1. Genes Dev 24: 561-573.
  • Christen, B, Robles, V, Raya, M, Paramonov, I and Izpisúa Belmonte JC. (2010) Regeneration and reprogramming compared. BMC Biol. Jan 20; 8:5.
  • Shigeki Sugiia, Yasuyuki Kida, Teruhisa Kawamura, Jotaro Suzuki, Rita Vassena, Yun-Qiang Yin, Margaret K. Lutz, W. Travis Berggren, Izpisúa Belmonte JC, and Ronald M. Evans. (2010) Human and mouse adipose-derived cells support feeder-independent induction of pluripotent stem cells. PNAS Feb 23; 107(8): 3558-63.
  • Aasen, T. and Izpisúa Belmonte JC. (2010) Isolation and cultivation of human keratinocytes from skin or plucked hair for the generation of induced pluripotent stem cells. Nature Protocols 5(2): 371-82.
  • Tramullas, M., Diaz, A., San-Emeterio, E.P., Morchon, N., Lantero, A., Merino, D., Buscher, D., Merino, R., Hurle, J.M., Izpisúa Belmonte JC and Hurle, M. (2010) BAMBI (bone morphogenetic protein and activin membrane-bound inhibitor) reveals the involvement of the transforming growth factor-beta family in pain modulation. Journal of Neuroscience Jan 27; 30(4): 1502-11.
  • Mizrak, S.C., Chikhovskaya, J.V., Sadri-Ardekani, H., van Daalen, S., Korver, C.M., Hovingh, S.E., Roepers-Gajadien, H.L., Raya, A., Fluiter, K., de Reijke, Th.M., de la Rosette, J.J.M.C.H., Izpisúa Belmonte JC, van der Veen, F., de Rooij, D.G. and van Pelt, A.M.M. (2010) Embryonic Stem Cell-like Cells Derived from Adult Human Testis. Human Reproduction, Jan 25(1): 158-67.
  • Rodriguez-Piza, I., Richaud-Patin, Y., Vassena, R., Gonzalez, F., Barrero, M.J., Veiga, A., Raya, A. and Izpisúa Belmonte JC. (2010) Reprogramming of human fibroblasts to induced pluripotent stem cells under xeno-free conditions. Stem Cells, Jan 28(1): 36-44.
  • Ibanes, M. and Izpisúa Belmonte JC. (2009) Left-right asymmetry determination. Wiley Interdisciplinary Reviews: Systems Biology and Medicine. Sept/Oct: 210-219.
  • Aran B, Rodriguez-Pizà I, Raya A, Consiglio A, Muñoz Y, Barri PN, Izpisúa Belmonte JC, Veiga A. (2010) Derivation of human embryonic stem cells at the Center of Regenerative Medicine in Barcelona. In Vitro Cellular & Developmental Biology - Animal, Apr 46(3-4): 356-66.
  • B.Aran, A.Veiga, Izpisúa Belmonte JC. (2009) Células madre pluripotentes Revista Arbor. In press.
  • Stewart, S., Tsun, Z.Y. and Izpisúa Belmonte JC. (2009) A histone demethylase is necessary for regeneration in zebrafish. PNAS  106(47):  19889-19894.
  • Giorgetti, A., Montserrat, N., Aasen, T., Rodriguez-Piza, I., Vassena, R., Gonzalez, F., Boue, S., Barrero, M.J., Aran Corbella, B., Raya, A., Torrebadella, M., Veiga, A. and Izpisúa Belmonte JC. (2009) Generation of induced pluripotent stem cells from cord blood using OCT4 and SOX2. Cell Stem Cell. 5:353-357.
  • Izpisúa Belmonte JC, Ellis, J., Hochedlinger, K. and Yamanaka, S. (2009) Induced pluripotent stem cells and reprogramming: seeing the science through the hype. Nature Reviews Genetics 10: 878-883.
  • Kawamura, T., Suzuki, J., Wang, Y.V., Menendez, S., Batlle, L., Wahl, G. and Izpisúa Belmonte JC. (2009) Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 460: 1140-1144.
  • Kan, N., Junghans, D. and Izpisúa Belmonte JC. (2009) Compensatory growth mechanisms regulated by BMP and FGF signaling pathways mediate liver regeneration in zebrafish after partial hepatectomy. FASEB 23: 3516-3525.
  • Raya, A., Rodriguez-Piza, I., Guenechea, G., Vassena, R., Navarro, S., Barrero, M.J., Consiglio, A., Rio, P., Sleep, E., Tiscornia, G., Garreta, E., Aasen, T., Veiga, A., Verma, I., Bueren, J. and Izpisúa Belmonte JC. (2009) Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature 460(7251): 53-9.
  • Kelber, J.A., Panopoulos, A.D., Shani, G., Booker, E.C., Izpisúa Belmonte JC, Vale, W.W. and Gray, P.C. (2009) Blockade of Cripto binding to cell surface GRP78 inhibits oncogenic Cripto signaling via MAPk/PI3K and Smad2/3 pathways. Oncogene 28: 2324-2336.
  • Gonzalez, F., Barragan Monasterio, M., Tiscornia, G., Montserrat Pulido, N., Vassena, R., Batlle Morera, L., Rodriguez Piza, I. and Izpsiua Belmonte JC. (2009) Generation of mouse induced pluripotent stem cells by transient expression of a single non-viral polycistronic vector. PNAS 106(22): 8918-8922.
  • Beck, C., Izpisúa Belmonte JC and Christen, B. (2009) Beyond Early Development: Xenopus as an emerging model for the study of regenerative mechanisms. Developmental Dynamics. 238(6): 1226-48.
  • Jopling, C. and Izpisúa Belmonte JC. (2009) Cilia-Where Two Wnts Collide. Zebrafish 6(1): 15-19.
  • Fink, M., Chu, A., Ruiz-Lozano, P., Callol, C., Izpisúa Belmonte JC, Giles, W., Bodmer, R. and Ocorr, K. (2009) A new method for detection and quantification of heartbeat parameters in Drosophila, zebrafish, and embryonic mouse hearts. Biotechniques 46: 101-113.
  • Rojas-Muñoz, A., Rajadhyksha, S., Gilmour, D., van Bebber, F., Rodríguez-Esteban, C., Nüsslein-Volhard, C., & Izpisúa Belmonte JC. (2009) ErbB2 and ErbB3 regulate amputation-induced proliferation and migation during vertebrate regeneration. Developmental Biology 327: 177-190.
  • Raya, A., Rodriguez-Piza, I., Aran, B., Consiglio, A., Barri, P., Veiga, A., and Izpisúa Belmonte JC. (2009) Generation of cardiomyocytes from new human embryonic stem cell lines derived from poor-quality blastocysts. 73rd Cold Spring Harbor Laboratory Symposium. 73:1-9.
  • Raya, A and Izpisúa Belmonte JC. (2009) Stem Cell Research in Spain: If Only They Were Windmills. Cell Stem Cell 4(6): 483-486.
  • Kawakami, Y., Uchiyama, Y., Rodriguez Esteban, C., Toshiaki, I., Kawakami, H., Marti, M., Kmita, M., Monaghan-Nicols, P., Nishinakamura, R. and Izpisúa Belmonte JC. (2008) Sall genes regulate region specific morphogenesis in the limb by modulating Hox activities. Development 136: 585-594.
  • Stubbs, J., Oishi, I., Izpisúa Belmonte JC and Kintner, C. (2008) The Forkhead protein, FoxJ1, specified node-like cilia in Xenopus and Zebrafish embryos. Nature Genetics. 40:1454-1460.
  • Ibanes, M. and Izpisúa Belmonte JC. (2008) Left-right asymmetry determination. Wiley Interdisciplinary Reviews: Systems Biology and Medicine. In Press.
  • Aasen, T., Raya, A., Barrero, M.J., Garreta, E., Consiglio, A., Gonzalez, F., Vassena, R., Bilic, J., Pekarik, V., Tiscornia, G., Edel, M., Boue, S. and Izpisúa Belmonte JC. (2008) Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nature Biotechnology. 26:1276-1284.
  • Raya, A. and Izpisúa Belmonte JC. (2008) Insights into the establishment of left-right asymmetries in vertebrates. BDRC: Embryo Today. 84(2):81-94.
  • Ibanes, M and Izpisúa Belmonte JC. (2008) Theoretical and experimental approaches to understand morphogen gradients. Nature Molecular Systems Biology. 4:176.
  • Pekarik, V. and Izpisúa Belmonte JC. (2008) NFIX-One Gene, Two Knockouts, Multiple Effects. Journal of Biology. 7:29.
  • Kurpios, N.A., Ibanes, M., Davis, N.M., Lui, W., Katz, T., Martin, J.F., Izpisúa Belmonte JC and Tabin, C.J. (2008) Directional gut looping is mediated by changes in the extracellular matrix and in cell:cell adhesion. PNAS. 105:8499-8506.
  • Moreno, T.A., Jappelli, R., Brenner, S., Izpisúa Belmonte JC, and Kintner, C. (2008) Retinoic Acid Regulation of the Mesp-Ripply Feedback Loop During Vertebrate Segmental Patterning. Developmental Biology. 315:317-330.
  • Suzuki, A., Sayaka, S., Buscher, D., Izpisúa Belmonte JC, and Taniguchi, H. (2008) Tbx3 controls hepatic stem cell fate in liver development by suppressing p19ARF expression. Development. 135:1589-1595
  • Garcia-Gonzalo, F.R. and Izpisúa Belmonte JC. (2008) Albumin-associated Lipids Regulate Human Embryonic Stem Cell Self-Renewal. PLoS ONE, Jan 2; 3(1): e1384.
  • Barrero, M.J. and Izpisua Belmonte J.C. (2008) Epigenetic Mechanisms Controlling Mesodermal Specification. StemBook, doi/10.3824/stembook.1.9.1 StemBook, ed (Harvard)
  • Allendorph, G.P., Isaacs, M.J., Kawakami, Y., Izpisúa Belmonte JC, Choe, S. (2007) BMP-3 and BMP-6 Structures Illuminate the Nature of Binding Specificity with Receptors. Biochemistry. 46:12238-12247.
  • Stewart, S., Rojas-Munoz, A., and Izpisúa Belmonte JC. (2007) Bioelectricity and epimorphic regeneration. Bioessays. 29(11):1133-1137.
  • Sahara, S., Kawakami, Y., Izpisúa Belmonte JC, O'Leary, D.D.M. (2007) Dual roles of Sp8 on cortical area patterning for anterior or posterior identities. Neuronal Development, 2:10.
  • Ribeiro, R., Kawakami, Y., Buscher, D., Raya, A., Rodriguez-Leon, J., Morita, M., Rodriguez Esteban, C., Izpisúa Belmonte JC. (2007) Tbx2 and Tbx3 regulate the dynamics of cell proliferation during heart regionalization and looping. PLoS One, Apr 25; 2(4): e398.
  • Rojas-Munoz, A., Bernad Miana, A., and Izpisúa Belmonte JC. (2007) El pez cebra:la navaja suiza de la biologia. Investigacion y Ciencia. 366:62-69.
  • Zuzarte-Luis, V., Montero, J.A., Kawakami, Y., Izpisúa Belmonte JC, and Hurle, J. (2007) Lysosomal cathepsins in embryonic programmed cell death. Developmental Biology. 301:205-217.
  • Matsui, T., Raya, A., Callol, C., Kawakami, Y., Oishi, I., Rodriguez-Esteban, C., and Izpisúa Belmonte JC. (2007) Miles apart-mediated regulation of cell-Fibronectin interaction is required for proper myocardial migration in zebrafish. Nature Clinical Practice Cardiovascular Medicine. 4:S77-S82.
  • Kawakami, Y., Rodriguez Esteban, C., Raya, M., Kawakami, H., Marti, M., Dubova, I., and Izpisúa Belmonte JC. (2006) Wnt/ß-catenin signaling regulates vertebrate limb regeneration. Genes and Development. 20:3232-3237.
  • Kawakami, Y., Rodriguez-Leon, J., Izpisúa Belmonte JC. (2006) The role of TGFßs and Sox9 during limb chondrogenesis. Current Opinion in Cell Biology. 18:723-729.
  • Oishi, I., Kawakami, Y., Raya, A., Callol-Massot, C., Izpisúa Belmonte JC. (2006) Regulation of primary cilia formation and left-right patterning in zebrafish by duboraya, a novel mediator of non-canonical Wnt signaling. Nature Genetics. 38:1316-1322.
  • Ibanes, M., Rasskin-Gutman, D., Kawakami, Y., and Izpisúa Belmonte JC. (2006) Cell lineage transport: a mechanism for molecular gradient formation. Nature Molecular Systems Biology. 2:57.
  • Suzuki, A.,Raya, A., Kawakami, Y., Morita, M., Matsui, T., Nakashima, K., Gage, F.H.,Rodriguez-Esteban, C., and Izpisúa Belmonte JC. (2006) Nanog binds to Smad1and blocks BMP-induced differentiation of embryonic stem cells. PNAS 103: 10294-10299.
  • Soler-Botija,C., Cervera, R.P., Oishi, I., Raya, R.M., Dubova, I., Rodriguez-Esteban, C., Izpisúa Belmonte JC. (2006) Understanding embryonic heart development as atool for cardiac cell based therapy. Annals of Pediatrics 64: 15-22.
  • Weninger,W.J., Geyer, S.H., Mohun, T.J., Rasskin-Gutman, D., Matsui, T., Ribeiro, I.,Costa, L., Izpisúa Belmonte JC, Muller, G. B. (2006) High resolutionepiscopic microscopy: a rapid technique for high detailed 3D analysis of geneactivity in the context of tissue architecture and morphology. Anatomy andEmbryology 211: 213-221.
  • Raya, A., Izpisúa Belmonte JC. (2006) Vertebrate left-right asymmetry: a convergence ofdivergences. Nature Reviews Genetics 7: 283-293.
  • Suzuki, A.,Raya, A., Kawakami, Y., Morita, M., Matsui, T., Nakashima, K., Gage, F.H.,Rodriguez-Esteban, C., Izpisúa Belmonte JC. (2006) Maintenance of embryonicstem cell pluripotency by Nanog-mediated reversal of mesoderm specification. Nature Clinical Practice Cardiovascular Medicine 3: S114-S122.
  • Merki, E., Zamora, M., Raya, A., Kawakami, Y., Zhang, X., Burch, J., Kubalak, S., Kaliman, P., Izpisúa Belmonte JC, Chien, K., Ruiz-Lozano, P. (2005) Epicardial RXRa is required for myocardial growth and coronary artery formation. PNAS 102: 18455-18460.
  • Leusch, H., Chanda,S.K., Raya, R.M., DeJesus, P.D., Orth, A.P. Walker, J.R., Izpisúa Belmonte JC, Schultz, P. (2006) A functional genomics approach to the mode of actionof apratoxin A. Nature Chemical Biology 2: 158-167.
  • Okada, Y.,Takeda, S., Tanaka Y., Izpisúa Belmonte JC, and Hirokawa, N. (2005) Mechanism of Ciliated Organ Flow: a Conserved Symmetry Breaking Event inLeft-Right Axis Determination. Cell 121: 633-644.
  • Kawakami,Y., Raya, A., Raya, R.M., Rodriguez-Esteban, C., Izpisúa Belmonte JC. (2005). Retinoic acid signaling links left-right asymmetric patterning andbilaterally symmetric somitogenesis in the zebrafish embryo. Nature May 12; 435(7039): 165-71.
  • Correa, R.,Matsui, T., Tergaonkar, V., Rodriguez-Esteban, C., Izpisúa Belmonte JC, Verma, I. (2005) Zebrafish IkB kinase 1 (Ikk1) negatively regulates NF-kBactivity. Current Biology 15: 1291-1295.
  • Da FontouraCosta, L., Travencolo, B.A.N., Azeredo, A., Beletti, M.E., Rasskin-Gutman, D.,Sternik, G., Izpisúa Belmonte JC, Ibanes, M., and Muller, G. (2005) A NovelFiel Approach to 3D Gne Expression Pattern Characterization. Applied PhysicsLetters 86: 143901-143903.
  • Francisco-Morcillo,J., Sanchez-Calderon, H., Kawakami, Y., Izpisúa Belmonte JC, Hidalgo-Sanchez, M., Martin-Partido, G. (2005) Expression of Fgf19 in thedeveloping eye. Developmental Brain Research 156: 104-109.
  • Kawakami,Y., Tsuda, M., Takahashi, S., Taniguchi, N., Rodriguez-Esteban, C., Zemmyo, M.,Furumatsu, T., Lotz, M., Izpisúa Belmonte JC and Asahara, H. (2005). Transcriptional co-activator PGC-1 regulates chondrogenesis via associationwith Sox 9. PNAS 102: 2414-2419.
  • Matsui, T.,Raya, A., Kawakami, Y., Callol, C., Capdevila, J., Rodriguez-Esteban, C., and Izpisúa Belmonte JC. (2005) Non-canonical Wnt signaling regulates midlineconvergence of organ primordia during zebrafish development. Genes andDevelopment 19: 164-175.
  • Buceta, J., Ibanes, M., Rasskin-Gutman,D., Okada, Y., Hirokawa, N., and Izpisúa Belmonte JC. (2005). Nodal CiliaDynamics and the Specification of the Left/Right Axis in Early EmbryoDevelopment. Biophysical Journal 89: 2199-2209.
  • Rasskin-Gutman, D. and Izpisúa Belmonte JC. (2004) Embryos at the core of life, Development 130: 5564-5566.
  • Raya, A., Consiglio, A., Kawakami, Y.,Rodriguez-Esteban, C., and Izpisúa Belmonte JC. (2004) The zebrafish asa model of heart regeneration. Cloning and Stem Cells 6(4): 345-351.
  • Kawakami, Y., Rodriguez Esteban, C.,Matsui, T., Rodriguez-Leon, J., Kato, S. and Izpisúa Belmonte JC. (2004) Sp8 and Sp9 regulate Fgf8 expression and limb outgrowth in vertebrateembryos. Development 31: 4763-4774.
  • Raya, A. and Izpisúa Belmonte JC. (2004) Unveiling the establishment of left-rightasymmetry in the chick embryo. Mech. Dev 121: 1043-1054.
  • Kang, J.S., Oohashi, T., Kawakami, Y.,Bekku, Y., Izpisúa Belmonte JC and Ninomiya, Y. (2004) Characterization ofdermacan, a novel zebrafish lectican gene, expressed in dermal bones. Mechanismsof Development 121(3): 301-312.
  • Huang Q, Raya A, DeJesus P, Chao SH,Quon KC, Caldwell JS, Chanda SK, Izpisúa Belmonte JC, Schultz PG. (2004) Identification of p53 regulators by genome-wide functional analysis. Proc.Natl. Acad. Sci. USA 101(10): 3456-3461.
  • Correa, R.,Tergaonkar, V., Ng, J., Izpisúa Belmonte JC, and Verma, I. (2004) Notochorddifferentiation by the T-box gene ntl in zebrafish is regulated by NFkb. MolecularCell Biology 24(12): 5257-5268.
  • Raya, A. and Izpisúa Belmonte JC. (2004) Sequential transfer of left-rightinformation during vertebrate embryo development. Curr. Op. Gen. and Dev 14: 575-581.
  • Rasskin-Gutman, D. and Izpisúa Belmonte JC. (2004) Theoretical morphology developmentalasymmetries. BioEssays  26(4): 405-412.
  • Saez, E., Rosenfeld, J., Livolsi, A.,Lombardo, E., Olson, P., Nelson,M., Banayo, E., Cardiff, R.D., Izpisúa Belmonte JC and Evans, R.M. (2004) PPARg signaling exacerbates mammary gland tumor development. Genesand Development 18(5): 528-540.
  • Timmerman, L.A., Grego-Bessa, J.,Bertrán, E., Pérez-Pomares, J.M., Diez, J., Aranda, S., Palomo, S., Raya, A., McCormick, F., Izpisúa Belmonte JC and de la Pompa, J.L. (2004) Notchpromotes epithelial-mesenchymal transitions during heart development andtransformation. Genes and Development 18(1): 99-115.
  • Raya, A., Kawakami, Y., Rodriguez-Esteban,C., Ibañes, M., Rasskin-Gutman, D., Rodriguez-León, J., Büscher, D., Feijó, J.A. and Izpisúa Belmonte JC. (2004) Notch activity acts as asensor for extracellular calcium during vertebrate left-rightdetermination. Nature 427: 121-128.
  • Raya, A., Koth, C.M., Büscher, D.,Kawakami, Y., Itoh, T., Raya, R.M., Sternik, G., Tsai, H.-J., Rodriguez-Esteban, C. and Izpisúa Belmonte JC. (2003) Activation of Notchsignaling pathway precedes heart regeneration in zebrafish. Proc. Natl.Acad. Sci. USA, Special Supplement on Stem Cells and the Future of Regenerative Medicine 100: 11889-11895.
  • Groppe, J., Greenwald, J., Wiater, E.,Rodriguez-Leon, J., Economides, A.N., Kwiatkowski, W., Baban, K., Affolter, M., Vale, W.W., Izpisúa Belmonte JC and Choe, S. (2003) Structural basis ofBMP signaling inhibition by Noggin, a novel twelve-membered cystine knotprotein. The Jnl. of Bone and Joint Surgery 85-A, Suppl. 3: 52-58.
  • Raya, A., Kawakami, Y.,Rodriguez-Esteban, C., Büscher, D., Koth, C.M., Itoh, T., Morita, M.,Raya, R.M., Dubova, I., Grego Bessa, J., de la Pompa, J.L. and Izpisúa Belmonte JC. (2003) Notch activity induces Nodal expression andmediates the establishment of left-right asymmetry in vertebrate embryos. GenesDev. 17: 1213-1218.
  • Kawakami, Y., Rodriguez-Leon, J., Koth,C.M., Büscher, D., Itoh, T., Raya, A., Ng, J.K., Rodriguez Esteban, C.,Takahashi, S., Henrique, D., Schwarz, M.F., Asahara, H. and Izpisúa Belmonte JC. (2003) MKP3 mediates the cellular response to FGF8signalling in the vertebrate limb. Nature Cell Biology 5: 513-519.
  • Groppe, J., Greenwald, J., Wiater, E.,Rodriguez-Leon, J., Economides, A.N., Kwiatkowski, W., Affolter, M., Vale, W.W., Izpisúa Belmonte JC and Choe, S. (2002) Structural basis of BMPsignalling inhibition by the cystine knot protein Noggin. Nature 420: 636-642.
  • Izpisúa Belmonte JC. (2002) The limb identitygene Tbx5 promotes limb initiation by interacting with Wnt-2band Fgf-10. Development 129: 5161-5170.
  • Ng, J., Kawakami, Y., Büscher, D., Raya,A., Itoh, T., Koth, C., Rodríguez Esteban, C., Rodriguez Leon, J., Garrity, D.M., Fishman, M.C. Hurle, J.M. and Izpisúa Belmonte JC. (Ed.). (2002) Limb Development, Special Issue. Intl.Jnl. of Dev. Biol., Volume 46, Issue No. 7.
  • Diaz Trelles, R., Rodriguez Leon, J., Kawakami, Y., Simoes, S. and Izpisúa Belmonte JC. (2002) Expression of thechick vascular endothelial growth factor D gene during limbdevelopment. Mechanisms of Development 116: 239-242.
  • Capdevila, J. and Izpisúa Belmonte JC. (2001) Patterning mechanisms controlling vertebrate limb development. Ann.Rev. Cell Dev. Biol. 17: 87-132.
  • Rodriguez-Esteban, C., Raya, A.,Capdevila, J. and Izpisúa Belmonte JC. (2001) ¿Cómo distingue el cuerpo la izquierda de la derecha? Investigacion y Ciencia 300: 62-69.
  • Mukhopadhyay, M., Shtrom, S.,Rodriguez-Esteban, C., Chen, L., Tsukui, T., Gomer, L., Dorward, D.W.,Glinka, A., Grinberg, A., Huang, S.-P., Niehrs, C., Izpisúa Belmonte JC and Westphal, H. (2001) Dickkopf1 is required for embryonic headinduction and limb morphogenesis in the mouse. Developmental Cell 1: 423-434.
  • Tavares, A.T., Izpisúa Belmonte JC and Rodriguez-Leon, J. (2001) Developmental expression of chick Twistand its regulation during limb patterning. Intl. Jnl. of Dev.Biol. 45: 707-713.
  • Rodriguez-Esteban, C., Capdevila, J., Kawakami, Y. and Izpisúa Belmonte JC. (2001) Wnt signaling and PKAcontrol Nodal expression and left-right determination in the chickembryo. Development 128: 3189-3195.
  • Sharma, K. and Izpisúa Belmonte JC. (2001) Development of the limb neuromuscular system. Curr. Opin. CellBiol. 13: 204-210.
  • Kawakami, Y., Capdevila, J., Büscher,D., Itoh, T., Rodriguez-Esteban, C., and Izpisúa Belmonte JC. (2001) Wnt signals control FGF-dependent limb initiation and AER induction in thechick embryo. Cell 104: 891-900.
  • Capdevila, J. and Izpisúa Belmonte JC. (2000) Perspectives on the evolutionary origin of tetrapod limbs. Jnl.of Exp. Zool 288: 287-303.
  • Ruiz-Lozano, P., Ryan, A.K. and Izpisúa Belmonte JC. (2000) Left-right axis determination. Trends inCardiovascular Med 10: 258-262.
  • Liang, J.O., Etheridge,A., Hantsoo, L., Rubinstein, A.L., Nowak, S.J., Izpisúa Belmonte JC, and Halpern, M.E. (2000) Asymmetric Nodal signaling in the zebrafish diencephalons positionsthe pineal organ. Development 127: 5101-5112.
  • Ryan, A.K. and Izpisúa Belmonte JC. (2000) Establishing a left-right axis in the embryo. IUBMB Life 50: 1-11.
  • Tavares, A.T., Tsukui, T., and Izpisúa Belmonte JC. (2000) Evidence that members of the Cut/Cux/CDP familymay be involved in AER positioning and polarizing activity during chicklimb development. Development 127: 5133-5144.
  • Yokoyama, H., Yonei-Tamura, S., Endo,T., Izpisúa Belmonte JC, Tamura, K. and Ide, H. (2000) Mesenchymewith Fgf-10 expression is responsible for regenerative capacity in Xenopuslimb buds. Developmental Biol 219: 18-29.
  • Capdevila, J., Vogan, K.J., Tabin, C.J.and Izpisúa Belmonte JC. (2000) Mechanisms of left-right determinationin vertebrates. Cell 101: 9-21.
  • Capdevila, J. and Izpisúa Belmonte JC. (2000) Knowing left from right: the molecular basis of lateralitydefects. Mol. Med. Today 6: 112-118.
  • Tamura, K., Yonei-Tamura, S. and Izpisúa Belmonte JC. (1999) Differential expression of Tbx4 and Tbx5in Zebrafish fin buds. Mech. Dev 87: 181-184.
  • Capdevila, J., Tsukui, T.,Rodriguez-Esteban, C., Zappavigna, V. and Izpisúa Belmonte JC. (1999) Control of vertebrate limb outgrowth by the proximal factor Meis2 anddistal antagonism of BMPs by Gremlin. Mol. Cell 4: 839-849.
  • Tamura, K., Yonei-Tamura, S. and Izpisúa Belmonte JC. (1999) Molecular basis of left-right asymmetry. Dev.Growth Differ 41: 645-656.
  • Tsukui, T., Capdevila, J., Tamura, K.,Ruiz-Lozano, P., Rodriguez-Esteban, C., Yonei-Tamura, S., Magallon, J.,Chandraratna, R.A.S., Chien, K., Blumberg, B., Evans, R.M. and Izpisúa Belmonte JC. (1999) Multiple left-right asymmetry defects in Shh-/-mutant mice unveil a convergence of the Shh and Retinoic Acid pathwaysin the control of Lefty-1. Proc. Natl. Acad. Sci. USA 96: 11376-11381.
  • Tavares, A., Capdevila, J. and Izpisúa Belmonte JC. (1999) Transcription factors during limb development. Scientific American (Sp. edit.) 4, 30-32.
  • Lin, C.R., Kioussi, C.,O'Connell, S., Briata, P., Szeto, D., Liu, F., Izpisúa Belmonte JC and Rosenfeld, M.G. (1999) Pitx2 regulates lung asymmetry, cardiac positioningand pituitary and tooth morphogenesis. Nature 401: 279-282.
  • Rodriguez-Esteban, C.,Capdevila, J., Economides, A.N., Pascual, J., Ortiz, A. and Izpisúa Belmonte JC. (1999) The novel Cer-like protein Caronte mediates the establishment ofembryonic left-right asymmetry. Nature 401: 243-251.
  • Yamada, G., Nakamura, S., Fukuzaki, K.,Izumi, H., Horai, N., Nagata, R., Minami, T., Tohno, Y., Suzuki, K.,Haraguchi, R., Miyado, K., Toyoda, T., Izpisúa Belmonte JC, Maruyama,I. and Kitajima, I. (1999) Dysregulation of trace element composition inovariectomized cynomolgus monkey bones. Cell. & Mol. Biol 44: 1205-1213.
  • Garcia-Domingo, D., Leonardo, E.,Grandien, A., Martinez, P., Albar, J.P., Izpisúa Belmonte JC and Martinez-A., C. (1999) DIO-1 is a gene involved in onset ofapoptosis in vitro, whose misexpression disrupts limb development. Proc.Natl. Acad. Sci. USA 96: 7992-7997.
  • Bach, I.,Rodriguez-Esteban, C., Carriere, C., Bhushan, A., Krones, A., Rose, D.W.,Glass, C.K., Andersen, B., Izpisúa Belmonte JC and Rosenfeld, M.G. (1999) RLIM inhibits functional activity of LIM homeodomain transcription factors viarecruitment of the histone deacetylase complex. Nature Genet 22: 394-399.
  • Huang, R., Zhi, Q., Izpisúa Belmonte JC, Christ, B. and Ketan, P. (1999) Origin and development of theavian tongue muscles. Anat. Embryol 200: 137-152.
  • Capdevila, J. and Izpisúa Belmonte JC. (1999) Extracellular modulation of the Hedgehog,Wnt and TGF-b signalling pathways during embryonicdevelopment. Curr. Opin. Genet. Dev 9: 427-433.
  • Merino, R., Macias, D.,Gañan, Y., Rodriguez-Leon, J., Economides, A.N., Rodriguez-Esteban, C., Izpisúa Belmonte JC and Hurle, J.M. (1999) Control of digit formation by activinsignalling. Development 126: 2161-2170.
  • Izpisúa Belmonte JC. (1999) How thebody tells left from right. Scientific American 280: 46-51.
  • Li, Q., Lu, Q., Hwang, J.Y., Büscher,D., Lee, K.-F., Izpisúa Belmonte JC and Verma, I.M. (1999) IKK1-deficient mice exhibit abnormal development of skin and skeleton. Genes Dev 13: 1322-1328.
  • Rodriguez-Esteban, C., Tsukui, T.,Yonei, S., Magallon, J., Tamura, K. and Izpisúa Belmonte JC. (1999) The T-Box genes Tbx4 and Tbx5 regulate limb outgrowth andidentity. Nature 398: 814-818.
  • Büscher, D. and Izpisúa Belmonte JC. (1999) Muscle development during vertebrate limb outgrowth. Cell & Tissue Res 296: 131-139.
  • Rincon-Limas, D.E., Lu, C.-H., Canal, I., Calleja, M., Rodriguez Esteban, C., Izpisúa Belmonte JC and Botas, J. (1999) Conservation of the expression and function of apterous orthologsin Drosophila and mammals. Proc. Natl. Acad. Sci. USA 96: 2165-2170.
  • Yonei-Tamura, S., Tamura, K., Tsukui, T. and Izpisúa Belmonte JC. (1999) Spatially and temporally-restrictedexpression of two T-box genes during zebrafish embryogenesis. Mech. Dev 80: 219-221.
  • Szeto, D.P., Rodriguez-Esteban, C., Ryan, A.K., O'Connell, S.M., Liu, F., Kioussi, C., Gleiberman, A.S., Izpisúa Belmonte JC and Rosenfeld, M.G. (1999) Role of the Bicoid-related homeodomain factor Pitx1 in specifying hindlimb morphogenesisand pituitary development. Genes Dev 13: 484-494.
  • Torok, M.A., Gardiner, D.M., Izpisúa Belmonte JC and Bryant, S.V. (1999) Sonic Hedgehog (shh) expressionin developing and regenerating Axolotl limbs. J. of Exp. Zool 284: 197-206.
  • Ng, J.K., Tamura, K., Büscher, D. and Izpisúa Belmonte JC. (1999) Outgrowth and patterning of the vertebratelimb. Molecular and cellular basis of pattern formation during vertebrate limb development. Current Topics in Dev. Biol 41: 37-66.
  • Takahashi, M., Tamura, K., Büscher, D.,Masuya, H., Yonei-Tamura, S., Matsumoto, K., Naitoh-Matsuo, M., Takeuchi,J., Ogura, K., Shiroishi, T., Ogura, T. and Izpisúa Belmonte JC. (1998) The role of Alx-4 in the establishment of anteroposteriorpolarity during vertebrate limb outgrowth. Development 125: 4417-4425.
  • Rodriguez-Esteban, C., Schwabe, J.W.R.,De La Peña, J., Rincon-Limas, D.E., Magallon, J., Botas, J. and Izpisúa Belmonte JC. (1998) Lhx2, a vertebrate homologue of apterous,regulates vertebrate limb outgrowth. Development 125: 3925-3934.
  • Ryan, A., Blumberg, B.,Rodriguez-Esteban, C., Yonei-Tamura, S., Tamura, K., Tsukui, T., De LaPeña, J., Sabbagh, W., Greenwald, J., Choe, S., Norris, D.P., Robertson,E.J., Evans, R.M., Rosenfeld, M.G. and Izpisúa Belmonte JC. (1998) Pitx2determines left-right asymmetry of internal organs in vertebrates. Nature 394: 545-551.
  • Schwabe, J.W.R., Rodriguez-Esteban, C.and Izpisúa Belmonte JC. (1998) Limbs are moving...where are they going? Trends in Genetics 14: 229-235.
  • Isaac, A., Rodriguez-Esteban, C., Ryan,A., Altabef, M., Tsukui, T., Patel, K., Tickle, C. and Izpisúa Belmonte JC. (1998) Tbx genes and limb identity in chick embryo development. Development 125: 1867-1875.
  • Kengaku, M., Capdevila, J., Rodriguez-Esteban, C., De La Peña, J., Johnson, R.L., Izpisúa Belmonte JC and Tabin, C.J. (1998) Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 280: 1274-1277.
  • Capdevila, J., Rodriguez-Esteban, C. and Izpisúa Belmonte JC. (1998) Molecular architecture of the vertebrate limb. Scientific American 12: 23-37 (Sp. edit.).
  • Kanegae, Y., Tavares, A.T., Izpisúa Belmonte JC and Verma, I.M. (1998) Role of Rel/NF-KB transcription factors during the outgrowth of the vertebrate limb. Nature 392: 611-614.
  • Heanue, T.A., Johnson, R.L., Izpisúa Belmonte JC, Stern, C.D., DeRobertis, E.M. and Tabin, C.J. (1997) Goosecoidmisexpression alters the morphology and Hox gene expression of the developing chick limb bud. Mech. Dev 69: 31-37.
  • Schwabe, J.W.R.,Rodriguez-Esteban, C., De La Peña, J., Tavares, A., Ng, J., Banayo, E.M., Foys,B., Eshelman, B., Magallon, J., Tam, R. and Izpisúa Belmonte JC. (1997) Outgrowth and patterning of the vertebrate limb. Cold Spring Harbor Symposia on Biology, Vol. LXII: 431-435.
  • Pfeffer, P., De Robertis, E. and Izpisúa Belmonte JC. (1997) Crescent, a novel chick gene encoding a Frizzled-like Cysteine-Rich Domain, is expressed in anterior regionsduring early embryogenesis. Int. J. Dev. Biol 41(3): 449-458.
  • Lemaire, L., Roser, T., Izpisúa Belmonte JC and Kessel, M. (1997) Segregating expression domains of two goosecoid genes during the transition from gastrulation to neurulationin chick embryos. Development 124: 1443-1452.
  • Rodriguez-Esteban, C., Schwabe, J.W.R.,De La Peña, J., Foys, B., Eshelman, B. and Izpisúa Belmonte JC. (1997) Radical fringe positions the apical ectodermal ridge at the dorsoventral boundary of the vertebrate limb. Nature 386: 360-366.
  • Rodriguez, C., Kos, R., Macias, D.,Abbott, U. K. and Izpisúa Belmonte JC. (1996) Shh, HoxD, Bmp-2, andFgf-4 gene expression during development of the polydactylous talpid2,diplopodia1, and diplopodia4 mutant chick limb buds. Dev. Genetics 19: 26-32.
  • Ros, M., Lopez Martinez, A., Simandl, B.K., Rodriguez, C., Izpisúa Belmonte JC, Dahn, R. and Fallon, J.(1996) The limb field mesoderm determines initial limb budanteroposterior asymmetry and budding independent of sonic hedgehogor apical ectodermal gene expressions. Development 122: 2319-2330.
  • Vogel, A., Rodriguez, C. and Izpisúa Belmonte JC. (1996) Involvement of FGF-8 in initiation, outgrowth,and patterning of the vertebrate limb. Development 122: 1737-1750.
  • Van der Hoeven, F., Sordino, P., Fraudeau, N., Izpisúa Belmonte JC and Duboule, D. (1996) Teleost HoxDand HoxA genes: comparison with tetrapods and functional evolution of the HOXD complex. Mech. Dev 54: 9-21.
  • Ogura, T., Alvarez, S., Vogel, A.,Rodriguez, C., Evans, R. and Izpisúa Belmonte JC. (1996) Evidence thatShh cooperates with a retinoic acid inducible co-factor to establish ZPA-like activity. Development 122: 537-542.
  • Vogel, A., Rodriguez, C., Warnken W. and Izpisúa Belmonte JC. (1995) Dorsal cell fate specified by chick Lmx1during vertebrate limb development. Nature 378: 716-720.
  • Hardy, A., Richardson, M. K., Philippa,H., Francis-West, P. H., Rodriguez, C., Izpisúa Belmonte JC, Duprez, D. and Wolpert, L. (1995) Gene expression, polarizing activity andskeletal patterning in reaggregated hind limb mesenchyme. Development 121: 4329-4337.
  • Sucov, H., Izpisúa Belmonte JC, Gañan, Y. and Evans R. (1995) Mouse embryos lacking RXRa are resistantto retinoic-acid-induced limb defects. Development 121: 3997-4003.
  • Cohn, M., Izpisúa Belmonte JC, Abud, H., Heath, J. K. and Tickle, C. (1995) FibroblastGrowth Factors induce additional limb development from the flank of chick embryos. Cell 80: 739-746.
  • Francis-West, P. H., Robertson, K., Ede, D. A., Rodriguez, C., Izpisúa Belmonte JC, Houston, B., Burt, D. W.,Gribbin, C., Brickell, P. M. and Tickle, C. (1995) Expression of genesencoding bone morphogenetic proteins and sonic hedgehog in Talpid (ta3)limb buds: their relationships in the signaling cascade involved in limb patterning. Dev. Dynamics 203: 187-197.
  • Fjose, A., Izpisúa Belmonte JC, Fromental, C. and Duboule, D. (1994) Expression of the zebrafish gene hlx-1in the prechordal plate and during CNS development. Development 120: 71-81.
  • Olivo, J., Izpisúa Belmonte JC, Tickle, C., Boulin, C. and Duboule, D. (1993) Reconstruction fromserial sections: a tool for developmental biology. Application to Hoxgenes expression in chicken wing buds. BioImaging 1: 115-158.
  • Dollé, P., Izpisúa Belmonte JC, Brown, J., Tickle, C. and Duboule, D. (1993) Hox genes and the morphogenesis of the vertebrate limb. Prog. Clin. Biol. Res 383A: 11-20.
  • Izpisúa Belmonte JC, De Robertis,E., Storey, K. and Stern, C. (1993) The homeobox gene goosecoid andthe origin of organizer cells in the early chick blastoderm. Cell 74: 645-659.
  • Morgan, B., Izpisúa Belmonte JC, Duboule, D. and Tabin C. (1992) Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature 358: 236-239.
  • Izpisúa Belmonte JC and Duboule, D. (1992) Homeobox genes and pattern formation in the vertebrate limb. Dev. Biol 152: 26-36.
  • Bastian, H., Gruss, P., Duboule, D. and Izpisúa Belmonte JC. (1992) The murine even-skipped-like gene Evx-2is closely linked to the Hox-4 complex, but is transcribed in the opposite direction. Mammalian Genome 3: 241-243.
  • Izpisúa Belmonte JC, Brown, J. M., Crawley, D., Duboule, D. and Tickle, C. (1992) HOX-4 gene expression in mouse/chicken heterospecific grafts of signaling regions to limb buds reveals similarities in patterning mechanisms. Development 115: 553-560.
  • Renucci, A., Zappavigna, V., Zakany, J., Izpisúa Belmonte JC, Bürki, K. and Duboule, D. (1992) Comparison ofmouse and human HOX-4 complexes defines conserved sequences involved in the regulation of Hox-4.4. EMBO J 11: 1459-1468.
  • Izpisúa Belmonte JC, Brown, J.M.,Duboule, D. and Tickle, C. (1992) Expression of HOX-4 genes in the chickwing links pattern formation to the epithelial-mesenchymal interactions that mediate growth. EMBO J 11: 1451-1457.
  • Izpisúa Belmonte JC, Ede, D., Tickle, C. and Duboule, D. (1992) The misexpression of posterior HOX-4 genes in talpid(ta3) mutant wings correlates with the absence of anteroposteriorpolarity. Development 114: 959-963.
  • Izpisúa Belmonte JC, Tickle, C.,Dollé, P. and Duboule, D. (1991) HOX-4 genes and the molecular basis ofvertebrate limb pattern formation. Seminars in Dev. Biol 2: 385-391.
  • Dollé, P., Izpisúa Belmonte JC, Boncinelli, E. and Duboule, D. (1991) The Hox-4.8 gene is localized at the 5' extremity of the HOX-4 complex and is expressed at the posteriorend of the body during development. Mech. Dev 36(1-2): 3-13.
  • Dollé, P., Izpisúa Belmonte JC, Brown, J., Tickle, C. and Duboule, D. (1991) HOX-4 genes and the morphogenesis of mammalian genitalia. Genes Dev 5: 1767-1776.
  • Zappavigna, V., Renucci, A., Izpisúa Belmonte JC, Urier, G., Peschle, C. and Duboule, D. (1991) HOX4 genes encode transcription factors with potential auto-andcross-regulatory capacities. EMBO J 10: 4177-4187.
  • Izpisúa Belmonte JC, Falkenstein, H., Dollé, P., Renucci, A. and Duboule, D. (1991) Murine genes related tothe Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J 10: 2279-2289.
  • Izpisúa Belmonte JC, Tickle, C.,Dollé, P., Wolpert, L. and Duboule, D. (1991) Expression of the homeoboxHox-4 genes and the specification of position in chick wing development. Nature 350: 585-589.
  • Izpisúa Belmonte JC, Dollé, P.,Renucci, A., Zappavigna, V., Falkenstein, H. and Duboule, D. (1990) Primary structure and embryonic expression pattern of the mouse Hox-4.3homeobox gene. Development 110: 733-745.
  • Dollé, P., Izpisúa Belmonte JC, Falkenstein, H., Renucci, A. and Duboule, D. (1989) Coordinate expression of the murine Hox-5 complex homeobox-containing genes duringlimb pattern formation. Nature 342: 767-772.
  • Bordoni A, Biagi PL, Parenti Castelli G,Hrelia S, Rossi CA, Lercker G, Izpisúa Belmonte JC, Barber T, Cabo J, a Lenaz G. (1989) Effect of a hyperlipidic diet on lipid composition, fluidity, and Na+-K+-ATPase activity of rat erythrocyte membranes. Membrane Biochem 8: 11-18.
  • Izpisúa Belmonte JC, Barber T, Cabo J, Hrelia S,Rossi CA, Parenti Castelli G, Lercker G, Biagi PL, Bordoni A, Lenaz G. (1989) Lipid composition, fluidity and enzymatic activities of rat liver plasmaand mitochondrial membranes in dietary obese rats. Int. J. Obesity 13: 531-542.


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