Cadherins in embryonic and neural morphogenesis

Nature Reviews Molecular Cell Biology - Tập 1 Số 2 - Trang 91-100 - 2000
Ulrich Tepaß1, Kevin Truong2, Dorothea Godt1, Mitsuhiko Ikura2, Mark Peifer3
1Department of Zoology, University of Toronto, Toronto, Canada
2Division of Molecular and Structural Biology, Ontario Cancer Institute and Department of Medical Biophysics, University of Toronto, Toronto, Canada
3Department of Biology, University of North Carolina, Chapel Hill, USA

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Steinberg, M. S. Reconstruction of tissue by dissociated cells. Science 141, 401?408. (1963).

Sperry, R. W. Chemoaffinity in the orderly growth of nerve fiber patterns and connections . Proc. Natl Acad. Sci. USA 50, 703? 710 (1963).

Gumbiner, B. M. Cell adhesion: The molecular basis of tissue architecture and morphogenesis . Cell 84, 345?579 (1996).

Hynes, R. O. Cell adhesion: Old and new questions. Trends Cell Biol. 9, M33?M37 (1999).

Townes, P. L. & Holtfreter, J. Directed movements and selective adhesion of embryonic amphibian cells. J. Exp. Zool. 128, 53?120 (1955).

Nose, A. & Nagafuchi, A., & Takeichi, M. Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54, 993? 1001 (1988).This paper shows for the first time cadherin-mediated cell sorting in cell-culture cells.

Steinberg, M. S. & Takeichi, M. Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc. Natl Acad. Sci. USA 91, 206?209 (1994).

Godt, D. & Tepass, U. Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395, 387?391 (1998). This paper documents for the first time an in vivo cell sorting process that is driven by differential expression of a cadherin.

Tessier-Lavigne, M. & Goodman, C. S. The molecular biology of axon guidance. Science 274, 1123 ?1133 (1996).

Takeichi, M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251, 1451?1455 ( 1991).

Wong, E. F. S., Brar, S. K., Sesaki, H., Yang, C. & Siu, C. H. Molecular cloning and characterization of DdCAD-1, a Ca2+-dependent cell?cell adhesion molecule, in Dictyostelium discoideum. J. Biol. Chem. 271, 16399 ?16408 (1996).

Gallin, W. J. Evolution of the 'classical' cadherin family of cell adhesion molecules in vertebrates. Mol. Biol. Evol. 15, 1099? 1107 (1998).

Yagi, T. & Takeichi, M. Cadherin superfamily genes: Functions, genomic organization, and neurologic diversity. Genes Dev. 14, 1169?1180 (2000).

Nollet, F., Kools, P. & van Roy, F. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J. Mol. Biol. 299, 551?72 (2000).

Wu, Q. & Maniatis, T. A. striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97, 779?790 ( 1999).

Sugino, H. et al. Genomic organization of the family of CNR cadherin genes in mice and humans. Genomics 63, 75? 87 (2000).

Hutter, H. et al. Conservation and novelty in the evolution of cell adhesion and extracellular matrix genes. Science 287, 989?994 (2000).

Overduin, M. et al. Solution structure of the epithelial cadherin domain responsible for selective cell adhesion. Science 267, 386?389 (1995).

Shapiro, L. et al. Structural basis of cell?cell adhesion by cadherins . Nature 374, 327?337 (1995).

Nagar, B., Overduin, M., Ikura, M. & Rini, J. M. Structural basis of calcium-induced E?cadherin rigidification and dimerization. Nature 380, 360?364 ( 1996).This is one of several papers (see also refs 18?26, 31 ) that describe the three-dimensional structure of the cadherin domain, and analyse the role of calcium ions in the formation of cadherin dimers.

Pertz, O. et al. A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E?cadherin homoassociation. EMBO J. 18, 1738?1747 ( 1999).

Tamura, K., Shan, W. S., Hendrickson, W. A., Colman, D. R. & Shapiro, L. Structure?function analysis of cell adhesion by neural (N-) cadherin. Neuron 20 , 1153?1163 (1998).

Ozawa, M., Engel, J. & Kemler, R. Single amino acid substitutions in one Ca2+ binding site of uvomorulin abolish the adhesive function. Cell 63,1033?1038 ( 1990).

Pokutta, S., Herrenknecht, K., Kemler, R. & Engel, J. Conformational changes of the recombinant extracellular domain of E?cadherin upon calcium binding. Eur. J. Biochem. 223, 1019?1026 (1994).

Baumgartner, W. et al. Cadherin interaction probed by atomic force microscopy. Proc. Natl Acad. Sci. USA 97, 4005? 4010 (2000).

Hyafil, F., Babinet, C. & Jacob, F. Cell?cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell 26 , 447?454 (1981)

Brieher, W. M., Yap, A. S., & Gumbiner, B. M. Lateral dimerization is required for the homophilic binding activity of C-cadherin. J. Cell Biol. 135, 487?496 (1996).

Alattia, J. R. et al. Lateral self-assembly of E-cadherin directed by cooperative calcium binding. FEBS Lett. 417, 405? 408 (1997).

Yap, A. S., Brieher, W. M., Pruschy, M. & Gumbiner, B. M. Lateral clustering of the adhesive ectodomain: a fundamental determinant of cadherin function. Curr. Biol. 7, 308? 315 (1997).

Shan, W. S. et al. Functional cis-heterodimers of N- and R-cadherins. J. Cell Biol. 148, 579?590 (2000).

Tomschy, A., Fauser, C., Landwehr, R. & Engel, J. Homophilic adhesion of E-cadherin occurs by a co-operative two-step interaction of N?terminal domains. EMBO J. 15, 3507? 3514 (1996).

Nose, A., Tsuji, K. & Takeichi, M. Localization of specificity determining sites in cadherin cell adhesion molecules. Cell 61,147? 155 (1990).

Blaschuk, O. W., Sullivan, R., David, S. & Pouliot, Y. Identification of a cadherin cell adhesion recognition sequence. Dev. Biol. 139, 227?229 (1990).

Sivasankar, S., Brieher, W., Lavrik, N., Gumbiner, B. & Leckband, D. Direct molecular force measurements of multiple adhesive interactions between cadherin ectodomains. Proc. Natl Acad. Sci. USA 96, 11820?11824 ( 1999).A recent paper that suggests a new model of cadherin trans -dimer formation.

Costa, M. et al. A putative catenin?cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J. Cell Biol. 141, 297?308 (1998).

Raich, W. B., Agbunag, C. & Hardin, J. Rapid epithelial-sheet sealing in the Caenorhabditis elegans embryo requires cadherin-dependent filopodial priming. Curr. Biol. 9, 1139?1146 (1999).This paper analyses the dynamics of cadherin-dependent contact formation between epithelial cells during C. elegans embryogenesis.

Uemura, T. et al. Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev. 10, 659? 671 (1996).

Tepass, U. et al. shotgun encodes Drosophila E?cadherin and is preferentially required during cell rearrangement in the neuroectoderm and other morphogenetically active epithelia. Genes Dev. 10, 672?685 (1996).

Ohsugi, M., Larue, L., Schwarz, H. & Kemler, R. Cell-junctional and cytoskeletal organization in mouse blastocysts lacking E-cadherin. Dev. Biol. 185, 261?271 (1997).

Mandai, K. et al. Afadin: A novel actin filament-binding protein with one PDZ domain localized at cadherin-based cell-to-cell adherens junction. J. Cell Biol. 139, 517?528 (1997).

Mandai, K. et al. Ponsin/SH3P12: An l-afadin- and vinculin-binding protein localized at cell-cell and cell-matrix adherens junctions. J. Cell Biol. 144, 1001?1017 ( 1999).

Takahashi, K. et al. Nectin/PRR: An immunoglobulin-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with Afadin, a PDZ domain-containing protein. J. Cell Biol. 145, 539?549 (1999).One of a series of papers (refs 40?44 ) that describe a new protein complex that localizes to adherens junctions, and that might interact with the cadherin?catenin complex functionally.

Tachibana, K. et al. Two cell adhesion molecules, nectin and cadherin, interact through their cytoplasmic domain-associated proteins. J. Cell Biol. 150, 1161?1175 ( 2000).

Ikeda, W. et al. Afadin: A key molecule essential for structural organization of cell?cell junctions of polarized epithelia during embryogenesis. J. Cell Biol. 146, 1117?1132 (1999).

Tepass, U. Genetic analysis of cadherin function in animal morphogenesis. Curr. Opin. Cell Biol. 11, 540?548 (1999).

Yeaman, C., Grindstaff, K. K. & Nelson, W. J. New perspectives on mechanisms involved in generating epithelial cell. Phys. Rev. 79, 73? 98 (1999).

Oda, H., Tsukita, S. & Takeichi, M. Dynamic behavior of the cadherin-based cell?cell adhesion system during Drosophila gastrulation. Dev. Biol. 203, 435?450 ( 1998).

Cano, A. et al. The transcription factor snail controls epithelial?mesenchymal transitions by repressing E-cadherin expression. Nature Cell Biol. 2, 76?83 (2000 ).

Batlle, E. et al. The transcription factor snail is a repressor of E?cadherin gene expression in epithelial tumour cells. Nature Cell Biol. 2, 84?89 (2000).

Adams, C. L. et al. Mechanisms of epithelial cell?cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin?green fluorescent protein. J. Cell Biol. 142, 1105?1119 (1998).

Vasioukhin, V., Bauer, C., Yin, M. & Fuchs, E. Directed actin polymerization is the driving force for epithelial cell?cell adhesion. Cell 100, 209?219 ( 2000).

Grindstaff, K. K. et al. Sec6/8 complex is recruited to cell?cell contacts and specifies transport vesicle delivery to the basal?lateral membrane in epithelial cells. Cell 93, 731? 740 (1998).This paper shows a close association between the sec6/8 complex, which is involved in lateral vesicle targeting, and cadherin-based adherens junctions.

Peifer, M. & Polakis, P. Wnt signaling in oncogenesis and embryogenesis ? a look outside the nucleus. Science 287, 1606?1609 (2000).

Adler, P. N., Charlton, J. & Liu, J. Mutations in the cadherin superfamily member gene dachsous cause a tissue polarity phenotype by altering Frizzled signaling . Development 125, 959? 968 (1998).

Usui, T. et al. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98 , 585?595 (1999).

Chae, J. et al. The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. Development 126 , 5421?5429 (1999). References 55 and 56 show a role for the Flamingo/Starry Night cadherin in planar epithelial polarity. Reference 55 also shows that the subcellular distribution of Flamingo/Starry Night depends on the direction of Wnt/Frizzled signalling.

Lu, B., Usui, T., Uemura, T., Jan, L. & Jan, Y. N. Flamingo controls the planar polarity of sensory bristles and asymmetric division of sensory organ precursors in Drosophila. Curr. Biol. 9, 1247?1250 (1999).

Gonzalez-Reyes, A. & St Johnston, D. The Drosophila AP axis is polarised by the cadherin-mediated positioning of the oocyte . Development 125, 3635? 3644 (1998).

Garcia-Castro, M. I., Vielmetter, E. & Bronner-Fraser, M. N-Cadherin, a cell adhesion molecule involved in establishment of embryonic left?right asymmetry. Science 288 , 1047?1051 (2000).

Shih, J. & Keller, R. Cell motility driving mediolateral intercalation in explants of Xenopus laevis. Development 116, 901?914 ( 1992).

Zhong, Y., Brieher, W. M. & Gumbiner, B. M. Analysis of C-cadherin regulation during tissue morphogenesis with an activating antibody. J. Cell Biol. 144, 351?359 (1999).

Lee, C. H. & Gumbiner, B. M. Disruption of gastrulation movements in Xenopus by a dominant?negative mutant for C-cadherin. Dev. Biol. 171, 363?373 (1995).

Kim, S. H., Yamamoto, A., Bouwmeester, T., Agius, E. & Robertis, E. M. The role of paraxial protocadherin in selective adhesion and cell movements of the mesoderm during Xenopus gastrulation. Development 125, 4681 ?4690 (1998).Experiments in this paper indicate an important role for a protocadherin in the convergent extension movements during frog gastrulation.

Yamamoto, A. et al. Zebrafish paraxial protocadherin is a downstream target of spadetail involved in morphogenesis of gastrula mesoderm. Development 125, 3389?3397 (1998).

Heisenberg, C. P. et al. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405, 76?81 (2000).

Wallingford, J. B. et al. Dishevelled controls cell polarity during Xenopus gastrulation . Nature 405, 81?85 (2000).

Tada, M. & Smith, J. C. Xwnt11 is a target of Xenopus brachyury: regulation of gastrulation movements via dishevelled, but not through the canonical wnt pathway. Development 127, 2227?2238 (2000).

Niewiadomska, P., Godt, D. & Tepass, U. DE?cadherin is required for intercellular motility during Drosophila oogenesis. J. Cell Biol. 144 , 533?547 (1999). This paper documents a cadherin-dependent cell migration process.

Palecek, S. P., Loftus, J. C., Ginsberg, M. H., Lauffenburger, D. A. & Horwitz, A. F. Integrin-ligand binding properties govern cell migration speed through cell?substratum adhesiveness. Nature 385, 537? 540 (1997).

Radice, G. L. et al. Developmental defects in mouse embryos lacking N-cadherin . Dev. Biol. 181, 64?78 (1997).

Redies, C. Cadherins in the central nervous system. Prog. Neurobiol. 61, 611?648 (2000).

Espeseth, A., Marnellos, G. & Kintner, C. The role of F?cadherin in localizing cells during neural tube formation in Xenopus embryos. Development 125, 301?312 (1998).

Senzaki, K., Ogawa, M. & Yagi, T. Proteins of the CNR family are multiple receptors for Reelin. Cell 99, 635?647 ( 1999).Protocadherins of the CNR family are identified as receptors of the extracellular matrix protein Reelin, an interaction that might contribute to the migration and differentiation of neurons within the brain cortex.

Gilmore, E. C. & Herrup, K. Cortical development: receiving reelin. Curr. Biol. 10, R162?R166 (2000).

Kohmura, N. et al. Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex. Neuron 20, 1137?1151 (1998). This paper identifies a closely related group of protocadherins that are differentially expressed in the brain and localize to synapses.

Riehl, R. et al. Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17, 837? 848 (1996).

Inoue, A. & Sanes, J. R. Lamina-specific connectivity in the brain: Regulation by N-cadherin, neurotrophins, and glycoconjugates. Science 276, 1428?1431 ( 1997).

Iwai, Y. et al. Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 19, 77?89 (1997).

Loureiro, M. et al. Anomalous origin of the left pulmonary artery (Sling): A case report and review of the literature. Rev. Port. Cardiol. 17, 811?815 (1998).

Gao, F. B., Brenman, J. E., Jan, L. Y. & Jan, Y. N. Genes regulating dendritic outgrowth, branching, and routing in Drosophila . Genes Dev. 13, 2549? 2561 (1999).

Yamagata, M., Herman, J. P. & Sanes, J. R. Lamina-specific expression of adhesion molecules in developing chick optic tectum. J. Neurosci. 15, 4556?4571 (1995).

Fannon, A. M. & Colman, D. R. A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron 17, 423? 434 (1996).

Uchida, N., Honjo, Y., Johnson, K. R., Wheelock, M. J. & Takeichi, M. The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J. Cell Biol. 135, 767?779 (1996).References 82 and 83 show that classic cadherins are components of synaptic adherens junctions.

Yamagata, K. et al. Arcadlin is a neural activity-regulated cadherin involved in long term potentiation. J. Biol. Chem. 274, 19473?19479 (1999).

Tanaka, H. et al. Molecular modification of N?cadherin in response to synaptic activity. Neuron 25, 93? 107 (2000).

Tang, L., Hung, C. P. & Schuman, E. M. A role for the cadherin family of cell adhesion molecules in hippocampal long-term potentiation. Neuron 20, 1165?1175 (1998).

Manabe, T. et al. Loss of Cadherin?11 adhesion receptor enhances plastic changes in hippocampal synapses and modifies behavioral responses. Mol. Cell. Neurosci. 15, 534?546 (2000).

Uemura, T. The cadherin superfamily at the synapse: More members, more missions. Cell 93, 1095?1098 ( 1998).

Shapiro, L. & Colman, D. R. The diversity of cadherins and implications for a synaptic adhesive code in the CNS. Neuron 23, 427?430 (1999).

Suzuki, S. C., Inoue, T., Kimura, Y., Tanaka, T. & Takeichi, M. Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol. Cell. Neurosci. 9, 433?447 ( 1997).

Obata, S. et al. A common protocadherin tail: Multiple protocadherins share the same sequence in their cytoplasmic domains and are expressed in different regions of brain. Cell. Adhes. Commun. 6, 323?333 (1998).

Hirano, S., Yan, Q. & Suzuki, S. T. Expression of a novel protocadherin, OL?protocadherin, in a subset of functional systems of the developing mouse brain. J. Neurosci. 19, 995?1005 (1999).

Missler, M. & Südhof, T. C. Neurexins: Three genes and 1001 products. Trends Genet. 14, 20? 26 (1998).

Schmücker, D. et al. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101, 671?684 (2000).

Oda, H. & Tsukita, S. Nonchordate classic cadherins have a structurally and functionally unique domain that is absent from chordate classic cadherins. Dev. Biol. 216, 406? 422 (1999).

Hazuka, C. D. et al. The sec6/8 complex is located at neurite outgrowth and axonal synapse-assembly domains. J. Neurosci. 19, 1324?1334 (1999).