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How Cell-Cell Adhesion Contributes to Early Embryonic Development

  • Gui Ruan
  • Doris Wedlich
  • Almut Köhler
Chapter

Abstract

Cell-cell adhesion is a crucial process during embryonic development from earliest stages on. Keeping cells together during morphological changes in tissue composition is essential for the integrity of the developing organism and different cell-cell adhesion molecules including cadherins, immunoglobulins, and integrins contribute to this tissue cohesion. Cadherins dominate in early Xenopus development and for this reason the review will focus on this group. Cadherins are transmembrane glycoproteins mediating a calcium-dependent cell-cell adhesion. They consist of an intracellular and a transmembrane domain together with an extracellular domain with several repeats specific for the different cadherin types. The first described cadherins had five extracellular repeats with four calcium-binding sites each for three calcium ions as a common structure (Fig. 13.1, see type I). Typically, they possess an HAV tripeptide localized to function as binding site for homophilic trans dimerization. They were named classical cadherins or type I cadherins. In other cadherins, which were identified later, the HAV tripeptide is replaced mostly by a QAV tripeptide. Still there are striking similarities in gene structure justifying the term “cadherin” for these molecules as well. Therefore, the subfamily of type II or atypical cadherins (Fig. 13.1, type II) was created for them.

Keywords

Xenopus Laevis Early Embryonic Development Xenopus Embryo Blastula Stage Cranial Neural Crest 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Angres B, Müller AH, Kellermann J, Hausen P (1991) Differential expression of two cadherins in Xenopus laevis. Development 111: 829–844PubMedGoogle Scholar
  2. Angst BD, Marcozzi C, Magee AI (2001) The cadherin superfamily: diversity in form and function. J Cell Sci 114: 629–641PubMedGoogle Scholar
  3. Borchers A, David R, Wedlich D (2001) Xenopus Xcadherin-11 restrains cranial neural crest migration and influences neural crest specification. Development 128: 3049–3060Google Scholar
  4. Bradley RS, Espeseth A, Kintner C (1998) NF-protocadherin, a novel member of the cadherin superfamily, is required for Xenopus ectodermal ifferentiation. Curr Biol 8: 325–334PubMedCrossRefGoogle Scholar
  5. Brawerman G (1987) Determinants of messenger RNA stability. Cell 48: 5–6PubMedCrossRefGoogle Scholar
  6. Broders F, Thiery JP (1995) Contribution of cadherins to directional cell migration and histogenesis in Xenopus embryos. Cell Adhes Commun 3: 419–440PubMedCrossRefGoogle Scholar
  7. Broders F, Girault JM, Simonneau L, Suzuki S, Thiery JP (1993) Sequence and distribution of Xenopus laevis E-cadherin transcripts. Cell Adhes Commun 1: 265–277PubMedCrossRefGoogle Scholar
  8. Brown JD, Moon RT (1998) Wnt-signaling: why is everything so negative? Curr Opin Cell Biol 10: 182–187PubMedCrossRefGoogle Scholar
  9. Chappuis-Flament S, Wong E, Hicks LD, Kay CM, Gumbiner BM (2001) Multiple cadherin extracellular repeats mediate homophilic binding and adhesion. J Cell Biol 154: 231–243PubMedCrossRefGoogle Scholar
  10. Choi YS, Gumbiner B (1989) Expression of cell adhesion molecule E-cadherin in Xenopus embryos begins at gastrulation and predominates in the ectoderm. J Cell Biol 108: 2449–2458PubMedCrossRefGoogle Scholar
  11. Choi YS, Sehgal R, McCrea P, Gumbiner B (1990) A cadherin-like protein in eggs and cleaving embryos of Xenopus laevis is expressed in oocytes in response to progesterone. J Cell Biol 110: 1575–1582PubMedCrossRefGoogle Scholar
  12. Couly G, Le Douarin NM (1990) Head morphogenesis in embryonic avian chimeras: evidence for a segmental pattern in the ectoderm corresponding to the neuromeres. Development 108: 543–558PubMedGoogle Scholar
  13. David R, Wedlich D (2000) Xenopus Xcadherin-6 is expressed in the central and peripheral nervous system and in neurogenic placodes. Mech Dev 97: 187–190Google Scholar
  14. DeMarais AA, Moon RT (1992) The armadillo homologs beta-catenin and plakoglobin are differentially expressed during early development of Xenopus laevis. Dev Biol 153: 337–346PubMedCrossRefGoogle Scholar
  15. Detrick RJ, Dickey D, Kintner CR (1990) The effects of N-cadherin misexpression on morphogenesis in Xenopus embryos. Neuron 4: 493–506PubMedCrossRefGoogle Scholar
  16. Dufour S, Saint-Jeannet JP, Broders F, Wedlich D, Thiery JP (1994) Differential perturbations in the morphogenesis of anterior structures induced by overexpression of truncated XB- and Ncadherins in Xenopus embryos. J Cell Biol 127: 521–535PubMedCrossRefGoogle Scholar
  17. Dufour S, Beauvais-Jouneau A, Delouvee A, Thiery JP (1999) Differential function of N-cadherin and cadherin-7 in the control of embryonic cell motility. J Cell Biol 146: 501–516PubMedCrossRefGoogle Scholar
  18. Espeseth A, Johnson E, Kintner C (1995) Xenopus F-cadherin, a novel member of the cadherin family of cell adhesion molecules, is expressed at boundaries in the neural tube. Mol Cell Neurosci 6: 199–211Google Scholar
  19. Espeseth A, Marnellos G, Kintner C (1998) The role of F-cadherin in localizing cells during neural tube formation in Xenopus embryos. Development 125: 301–312PubMedGoogle Scholar
  20. Finnemann S, Mitrik I, Hess M, Otto G, Wedlich D (1997) Uncoupling of XB/U-cadherin-catenin complex formation from its function in cell-cell adhesion. J Biol Chem 272: 11856–11862PubMedCrossRefGoogle Scholar
  21. Fouquet B, Zimbelmann R, Franke WW (1992) Identification of plakoglobin in oocytes and early embryos of Xenopus laevis: maternal expression of a gene encoding a junctional plaque protein. Differentiation 51: 187–194PubMedCrossRefGoogle Scholar
  22. Fujimori T, Miyatani S, Takeichi M (1990) Ectopic expression of N-cadherin perturbs histogenesis in Xenopus embryos. Development 110: 97–104PubMedGoogle Scholar
  23. Geis K, Aberle H, Kühl M, Kemler R, Wedlich D (1998) Expression of the Armadillo family member p120`t11B in Xenopus embryos affects head differentiation but not axis formation. Dev Genes Evol 207: 471–481PubMedCrossRefGoogle Scholar
  24. Ginsberg D, DeSimone D, Geiger B (1991) Expression of a novel cadherin (EP-cadherin) in unfertilized eggs and early Xenopus embryos. Development 111: 315–325PubMedGoogle Scholar
  25. Green KJ, Gaudry CA (2000) Are desmosomes more than tethers for intermediate filaments? Nat Rev Mol Cell Biol 1: 208–216PubMedCrossRefGoogle Scholar
  26. Gumbiner BM (1998) Propagation and localization of Wnt-signaling. Curr Opin Genet Dev 8: 430–435PubMedCrossRefGoogle Scholar
  27. Hadeball B, Borchers A, Wedlich D (1998) Xenopus Xcadherin-11 (Xcad-11) expression requires the Wg/Wnt signal. Mech Dev 72: 101–113Google Scholar
  28. Haegel H, Larue L, Ohsugi M, Fedorov L, Herrenknecht K, Kemler R (1995) Lack of beta-catenin affects mouse development at gastrulation. Development 121: 3529–3537PubMedGoogle Scholar
  29. Heasman J, Ginsberg D, Geiger B, Goldstone K, Pratt T, Yoshida-Noro C, Wylie C (1994) A functional test for maternally inherited cadherin in Xenopus shows its importance in cell adhesion at the blastula stage. Development 120: 49–57PubMedGoogle Scholar
  30. Heasman J, Kofron M, Wylie C (2000) Beta-catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach. Dev Biol 222: 124–134PubMedCrossRefGoogle Scholar
  31. Hens MD, Nikolic I, Woolcock CM (2002) Regulation of Xenopus embryonic cell adhesion by the small GTPase, rac. Biochem Biophys Res Commun 298: 364–370PubMedCrossRefGoogle Scholar
  32. Herzberg F, Wildermuth V, Wedlich D (1991) Expression of XBcad, a novel cadherin, during oogenesis and early development of Xenopus. Mech Dev 35: 33–42PubMedCrossRefGoogle Scholar
  33. Ibrahim H, Winklbauer R (2001) Mechanisms of mesendoderm internalization in the Xenopus gastrula: lessons from the ventral side. Dev Biol 240: 108–122PubMedCrossRefGoogle Scholar
  34. Jarrett O, Stow JL, Yap AS, Key B (2002) Dynamin-dependent endocytosis is necessary for convergent-extension movements in Xenopus animal cap explants. Int J Dev Biol 46: 467–473PubMedGoogle Scholar
  35. Kaibuchi K, Kuroda S, Amano M (1999) Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu Rev Biochem 68: 459–486PubMedCrossRefGoogle Scholar
  36. Keller RE (1986) The cellular basis of amphibian gastrulation. In: Browder L (ed) Developmental biology: a comprehensive synthesis, vol 2. The cellular basis of morphogenesis. Plenum Press, New York, pp 241–327Google Scholar
  37. Keller R, Winklbauer R (1992) Cellular basis of amphibian gastrulation. Curr Top Dev Biol 27: 3989Google Scholar
  38. Kim SH, Yamamoto A, Bouwmeester T, Agius E, Robertis EM (1998) The role of paraxial protocadherin in selective adhesion and cell movements of the mesoderm during Xenopus gastrulation. Development 125: 4681–4690PubMedGoogle Scholar
  39. Kim SH, Jen WC, de Robertis EM, Kintner C (2000) The protocadherin PAPC establishes segmental boundaries during somitogenesis in Xenopus embryos. Curr Biol 10: 821–830PubMedCrossRefGoogle Scholar
  40. King MW, Ndiema M, Neff AW (1998) Anterior structural defects by misexpression of Xgbx-2 in early Xenopus embryos are associated with altered expression of cell adhesion molecules. Dev Dyn 212: 563–579PubMedCrossRefGoogle Scholar
  41. Kintner C (1992) Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain. Cell 69: 225–236PubMedCrossRefGoogle Scholar
  42. Kofron M, Spagnuolo A, Klymkowsky M, Wylie C, Heasman J (1997) The roles of maternal alphacatenin and plakoglobin in the early Xenopus embryo. Development 124: 1553–1560PubMedGoogle Scholar
  43. Kovacs EM, Ali RG, McCormack AJ, Yap AS (2002) E-cadherin homophilic ligation directly signals through Rac and PI3-kinase to regulate adhesive contacts. J Biol Chem 277: 6708–6718PubMedCrossRefGoogle Scholar
  44. Krufka A, Johnson RG, Wylie CC, Heasman J (1998) Evidence that dorsal-ventral differences in gap junctional communication in the early Xenopus embryo are generated by beta-catenin independent of cell adhesion effects. Dev Biol 200: 92–102PubMedCrossRefGoogle Scholar
  45. Kühl M, Wedlich D (1995) XB/U-cadherin mRNA contains cytoplasmic polyadenylation elements and is polyadenylated during oocyte maturation in Xenopus laevis. Biochim Biophys Acta 1262: 95–98PubMedCrossRefGoogle Scholar
  46. Kühl M, Wedlich D (1996) Xenopus cadherins: sorting out types and functions in embryogenesis. Dev Dyn 207: 121–134Google Scholar
  47. Kühl M, Wedlich D (1997) Wnt-signaling goes nuclear. BioEssays 19: 101–104PubMedCrossRefGoogle Scholar
  48. Kühl M, Finnemann S, Binder O, Wedlich D (1996) Dominant negative expression of a cytoplasmically deleted mutant of XB/U-cadherin disturbs mesoderm migration during gastrulation in Xenopus laevis. Mech Dev 54: 71–82PubMedCrossRefGoogle Scholar
  49. Kuroda H, Inui M, Sugimoto K, Hayata T, Asashima M (2002) Axial protocadherin is a mediator of prenotochord cell sorting in Xenopus. Dev Biol 244: 267–277PubMedCrossRefGoogle Scholar
  50. Lee CH, Gumbiner BM (1995) Disruption of gastrulation movements in Xenopus by a dominant-negative mutant for C-cadherin. Dev Biol 171: 363–373PubMedCrossRefGoogle Scholar
  51. Levi G, Ginsberg D, Girault JM, Sabanay I, Thiery JP, Geiger B (1991a) EP-cadherin in muscles and epithelia of Xenopus laevis embryos. Development 113: 1335–1344PubMedGoogle Scholar
  52. Levi G, Gumbiner B, Thiery JP (1991b) The distribution of E-cadherin during Xenopus laevis development. Development 111: 159–169PubMedGoogle Scholar
  53. Levine E, Lee CH, Kintner C, Gumbiner BM (1994) Selective disruption of E-cadherin function in early Xenopus embryos by a dominant negative mutant. Development 120: 901–909PubMedGoogle Scholar
  54. Lewis JE, Wahl JK 3rd, Sass KM, Jensen PJ, Johnson KR, Wheelock MJ (1997) Cross-talk between adherens junctions and desmosomes depends on plakoglobin. J Cell Biol 136: 919–934PubMedCrossRefGoogle Scholar
  55. Mary S, Charrasse S, Meriane M, Comunale F, Travo P, Blangy A, Gauthier-Rouviere C (2002) Biogenesis of N-cadherin-dependent cell-cell contacts in living fibroblasts is a microtubuledependent kinesin-driven mechanism. Mol Biol Cell 13: 285–301PubMedCrossRefGoogle Scholar
  56. Müller AH, Angres B, Hausen P (1992) U-cadherin in Xenopus oogenesis and oocyte maturation. Development 114: 533–543PubMedGoogle Scholar
  57. Müller HA, Kühl M, Finnemann S, Schneider S, van der Poel SZ, Hausen P, Wedlich D (1994) Xenopus cadherins: the maternal pool comprises distinguishable members of the family. Mech Dev 47: 213–223Google Scholar
  58. Narayanan CH, Narayanan Y (1980) Neural crest and placodal contributions in the development of the glossopharyngeal-vagal complex in the chick. Anat Rec 196: 71–82PubMedCrossRefGoogle Scholar
  59. Niessen CM, Gumbiner BM (2002) Cadherin-mediated cell sorting not determined by binding or adhesion specificity. J Cell Biol 156: 389–399PubMedCrossRefGoogle Scholar
  60. Nollet F, Kools P, van Roy F (2000) Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 299: 551–572PubMedCrossRefGoogle Scholar
  61. Northcutt RG, Brandle K, Fritzsch B (1995) Electroreceptors and mechanosensory lateral line organs arise from single placodes in axolotls. Dev Biol 168: 358–373PubMedCrossRefGoogle Scholar
  62. Palatnik CM, Wilkins C, Jacobson A (1984) Translational control during early Dictyostelium development: possible involvement of poly(A) sequences. Cell 36: 1017–1025PubMedCrossRefGoogle Scholar
  63. Paulson AF, Fang X, Ji H, Reynolds AB, McCrea PD (1999) Misexpression of the catenin p120(ctn)1A perturbs Xenopus gastrulation but does not elicit Wnt-directed axis specification. Dev Biol 207: 350–363PubMedCrossRefGoogle Scholar
  64. Paulson AF, Mooney E, Fang X, Ji H, McCrea PD (2000) Xarvcf, Xenopus member of the p120 catenin subfamily associating with cadherin juxtamembrane region. J Biol Chem 275: 30124–30131PubMedCrossRefGoogle Scholar
  65. Rizzoti K, Paquereau L, Shaw A, Knibiehler B, Audigier Y (1998) A constitutively activated mutant of galphaq down-regulates EP-cadherin expression and decreases adhesion between ectodermal cells at gastrulation. Mech Dev 76: 19–31PubMedCrossRefGoogle Scholar
  66. Schlosser G, Northcutt RG (2000) Development of neurogenic placodes in Xenopus laevis. J Comp Neurol 418: 121–146PubMedCrossRefGoogle Scholar
  67. Schlosser G, Roth G (1997) Evolution of nerve development in frogs. I. The development of the peripheral nervous system in Discoglossus pictus ( Discoglossidae ). Brain Behav Evol 50: 61–93Google Scholar
  68. Schmidt A, Langbein L, Rode M, Pratzel S, Zimbelmann R, Franke WW (1997) Plakophilins la and lb: widespread nuclear proteins recruited in specific epithelial cells as desmosomal plaque contents. Cell Tissue Res 290: 481–499PubMedCrossRefGoogle Scholar
  69. Schneider S, Herrenknecht K, Butz S, Kemler R, Hausen P (1993) Catenins in Xenopus embryogenesis and their relation to the cadherin-mediated cell-cell adhesion system. Development 118: 629–640PubMedGoogle Scholar
  70. Shapiro L, Fannon AM, Kwong PD, Thompson A, Lehmann MS, Grubel G, Legrand JF, Als-Nielsen J, Colman DR, Hendrickson WA (1995) Structural basis of cell-cell adhesion by cadherins. Nature 374: 327–337PubMedCrossRefGoogle Scholar
  71. Simonneau L, Broders F, Thiery JP (1992) N-cadherin transcripts in Xenopus laevis from early tailbud to tadpole. Dev Dyn 194: 247–260PubMedCrossRefGoogle Scholar
  72. Tashiro K, Tooi O, Nakamura H, Koga C, Ito Y, Hikasa H, Shiokawa K (1996) Cloning and expression studies of cDNA for a novel Xenopus cadherin ( XmN-cadherin), expressed maternally and later neural-specifically in embryogenesis. Mech Dev 54: 161–171Google Scholar
  73. Tooi O, Fujii G, Tashiro K, Shiokawa K (1994) Molecular cloning of cDNA for XTCAD-1, a novel Xenopus cadherin, and its expression in adult tissues and embryos of Xenopus laevis. Biochim Biophys Acta 1219: 121–128PubMedCrossRefGoogle Scholar
  74. Vallin J, Girault JM, Thiery JP, Broders F (1998) Xenopus Xcadherin-11 is expressed in different populations of migrating neural crest cells. Mech Dev 75: 171–174Google Scholar
  75. Wacker S, Brodbeck A, Lemaire P, Niehrs C, Winklbauer R (1998) Patterns and control of cell motility in the Xenopus gastrula. Development 125: 1931–1942PubMedGoogle Scholar
  76. Wacker S, Grimm K, Joos T, Winklbauer R (2000) Development and control of tissue separation at gastrulation in Xenopus. Dev Biol 224: 428–439PubMedCrossRefGoogle Scholar
  77. Winklbauer R (1989) Development of the lateral line system in Xenopus. Prog Neurobiol 32: 181–206PubMedCrossRefGoogle Scholar
  78. Winklbauer R, Schürfeld M (1999) Vegetal rotation, a new gastrulation movement involved in the internalization of the mesoderm and endoderm in Xenopus. Development 126: 3703–3713PubMedGoogle Scholar
  79. Winklbauer R, Medina A, Swain RK, Steinbeisser H (2001) Frizzled-7 signalling controls tissue separation during Xenopus gastrulation. Nature 413: 856–860PubMedCrossRefGoogle Scholar
  80. Wünnenberg-Stapleton K, Blitz IL, Hashimoto C, Cho KWY (1999) Involvement of the small GTPases XRhoA and XRndl in cell adhesion and head formation in early Xenopus development. Development 126: 5339–5351PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2004

Authors and Affiliations

  • Gui Ruan
  • Doris Wedlich
  • Almut Köhler
    • 1
  1. 1.Institut für Zoologie II (Molekulare Entwicklungs- und Zellphysiologie)Universität KarlsruheKarlsruheGermany

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