1932

Abstract

Since the proposal of the differential adhesion hypothesis, scientists have been fascinated by how cell adhesion mediates cellular self-organization to form spatial patterns during development. The search for molecular tool kits with homophilic binding specificity resulted in a diverse repertoire of adhesion molecules. Recent understanding of the dominant role of cortical tension over adhesion binding redirects the focus of differential adhesion studies to the signaling function of adhesion proteins to regulate actomyosin contractility. The broader framework of differential interfacial tension encompasses both adhesion and nonadhesion molecules, sharing the common function of modulating interfacial tension during cell sorting to generate diverse tissue patterns. Robust adhesion-based patterning requires close coordination between morphogen signaling, cell fate decisions, and changes in adhesion. Current advances in bridging theoretical and experimental approaches present exciting opportunities to understand molecular, cellular, and tissue dynamics during adhesion-based tissue patterning across multiple time and length scales.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-120420-100215
2022-10-06
2024-06-17
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/38/1/annurev-cellbio-120420-100215.html?itemId=/content/journals/10.1146/annurev-cellbio-120420-100215&mimeType=html&fmt=ahah

Literature Cited

  1. Amack JD, Manning ML. 2012. Knowing the boundaries: extending the differential adhesion hypothesis in embryonic cell sorting. Science 338:212–15
    [Google Scholar]
  2. Anastasiadis PZ, Moon SY, Thoreson MA, Mariner DJ, Crawford HC et al. 2000. Inhibition of RhoA by p120 catenin. Nat. Cell Biol. 2:637–44
    [Google Scholar]
  3. Barone V, Lang M, Krens SFG, Pradhan SJ, Shamipour S et al. 2017. An effective feedback loop between cell-cell contact duration and morphogen signaling determines cell fate. Dev. Cell 43:198–211.e12
    [Google Scholar]
  4. Barua D, Parent SE, Winklbauer R. 2017. Mechanics of fluid-filled interstitial gaps. II. Gap characteristics in Xenopus embryonic ectoderm. Biophys. J. 113:923–36
    [Google Scholar]
  5. Bekirov IH, Needleman LA, Zhang W, Benson DL. 2002. Identification and localization of multiple classic cadherins in developing rat limbic system. Neuroscience 115:213–27
    [Google Scholar]
  6. Bisogni AJ, Ghazanfar S, Williams EO, Marsh HM, Yang JY, Lin DM. 2018. Tuning of delta-protocadherin adhesion through combinatorial diversity. eLife 7:e41050
    [Google Scholar]
  7. Biswas S, Emond MR, Chenoweth KP, Jontes JD. 2021. δ-Protocadherins regulate neural progenitor cell division by antagonizing Ryk and Wnt/β-catenin signaling. iScience 24:102932
    [Google Scholar]
  8. Blevins CJ, Emond MR, Biswas S, Jontes JD. 2011. Differential expression, alternative splicing, and adhesive properties of the zebrafish δ1-protocadherins. Neuroscience 199:523–34
    [Google Scholar]
  9. Brasch J, Katsamba PS, Harrison OJ, Ahlsén G, Troyanovsky RB et al. 2018. Homophilic and heterophilic interactions of type II cadherins identify specificity groups underlying cell-adhesive behavior. Cell Rep 23:1840–52
    [Google Scholar]
  10. Brodland GW. 2002. The differential interfacial tension hypothesis (DITH): a comprehensive theory for the self-rearrangement of embryonic cells and tissues. J. Biomech. Eng. 124:188–97
    [Google Scholar]
  11. Calzolari S, Terriente J, Pujades C. 2014. Cell segregation in the vertebrate hindbrain relies on actomyosin cables located at the interhombomeric boundaries. EMBO J 33:686–701
    [Google Scholar]
  12. Canty L, Zarour E, Kashkooli L, François P, Fagotto F. 2017. Sorting at embryonic boundaries requires high heterotypic interfacial tension. Nat. Commun. 8:157
    [Google Scholar]
  13. Cayuso J, Xu Q, Wilkinson DG. 2015. Mechanisms of boundary formation by Eph receptor and ephrin signaling. Dev. Biol. 401:122–31
    [Google Scholar]
  14. Chal J, Guillot C, Pourquié O. 2017. PAPC couples the segmentation clock to somite morphogenesis by regulating N-cadherin-dependent adhesion. Development 144:664–76
    [Google Scholar]
  15. Chang L-H, Chen P, Lien M-T, Ho Y-H, Lin C-M et al. 2011. Differential adhesion and actomyosin cable collaborate to drive Echinoid-mediated cell sorting. Development 138:3803–12
    [Google Scholar]
  16. Chen J, Lu Y, Meng S, Han M-H, Lin C, Wang X 2009. α- and γ-Protocadherins negatively regulate PYK2. J. Biol. Chem. 284:2880–90
    [Google Scholar]
  17. Chen X, Gumbiner BM. 2006. Paraxial protocadherin mediates cell sorting and tissue morphogenesis by regulating C-cadherin adhesion activity. J. Cell Biol. 174:301–13
    [Google Scholar]
  18. Chihara D, Nance J. 2012. An E-cadherin-mediated hitchhiking mechanism for C. elegans germ cell internalization during gastrulation. Development 139:2547–56
    [Google Scholar]
  19. Cooper SR, Jontes JD, Sotomayor M. 2016. Structural determinants of adhesion by Protocadherin-19 and implications for its role in epilepsy. eLife 5:e18529
    [Google Scholar]
  20. Cortés F, Daggett D, Bryson-Richardson RJ, Neyt C, Maule J et al. 2003. Cadherin-mediated differential cell adhesion controls slow muscle cell migration in the developing zebrafish myotome. Dev. Cell 5:865–76
    [Google Scholar]
  21. Dessaud E, McMahon AP, Briscoe J. 2008. Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135:2489–503
    [Google Scholar]
  22. Dibbens LM, Tarpey PS, Hynes K, Bayly MA, Scheffer IE et al. 2008. X-linked protocadherin 19 mutations cause female-limited epilepsy and cognitive impairment. Nat. Genet. 40:776–81
    [Google Scholar]
  23. Duan X, Krishnaswamy A, De la Huerta I, Sanes JR. 2014. Type II cadherins guide assembly of a direction-selective retinal circuit. Cell 158:793–807
    [Google Scholar]
  24. Duguay D, Foty RA, Steinberg MS. 2003. Cadherin-mediated cell adhesion and tissue segregation: qualitative and quantitative determinants. Dev. Biol. 253:309–23
    [Google Scholar]
  25. Durdu S, Iskar M, Revenu C, Schieber N, Kunze A et al. 2014. Luminal signalling links cell communication to tissue architecture during organogenesis. Nature 515:120–24
    [Google Scholar]
  26. Emond MR, Biswas S, Blevins CJ, Jontes JD. 2011. A complex of Protocadherin-19 and N-cadherin mediates a novel mechanism of cell adhesion. J. Cell Biol. 195:1115–21
    [Google Scholar]
  27. Fagotto F. 2014. The cellular basis of tissue separation. Development 141:3303–18
    [Google Scholar]
  28. Fagotto F, Rohani N, Touret A-S, Li R 2013. A molecular base for cell sorting at embryonic boundaries: contact inhibition of cadherin adhesion by ephrin/Eph-dependent contractility. Dev. Cell 27:72–87
    [Google Scholar]
  29. Feng J, Hsu W-H, Patterson D, Tseng C-S, Hsing H-W et al. 2021. COUP-TFI specifies the medial entorhinal cortex identity and induces differential cell adhesion to determine the integrity of its boundary with neocortex. Sci. Adv. 7:eabf6808
    [Google Scholar]
  30. Fenz SF, Bihr T, Schmidt D, Merkel R, Seifert U et al. 2017. Membrane fluctuations mediate lateral interaction between cadherin bonds. Nat. Phys. 13:906–13
    [Google Scholar]
  31. Foty RA, Pfleger CM, Forgacs G, Steinberg MS. 1996. Surface tensions of embryonic tissues predict their mutual envelopment behavior. Development 122:1611–20
    [Google Scholar]
  32. Foty RA, Steinberg MS. 2005. The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278:255–63
    [Google Scholar]
  33. Franklin JL, Sargent TD. 1996. Ventral neural cadherin, a novel cadherin expressed in a subset of neural tissues in the zebrafish embryo. Dev. Dyn. 206:121–30
    [Google Scholar]
  34. Fraser SE, Murray BA, Chuong CM, Edelman GM. 1984. Alteration of the retinotectal map in Xenopus by antibodies to neural cell adhesion molecules. PNAS 81:4222–26
    [Google Scholar]
  35. Friedlander DR, Mège RM, Cunningham BA, Edelman GM. 1989. Cell sorting-out is modulated by both the specificity and amount of different cell adhesion molecules (CAMs) expressed on cell surfaces. PNAS 86:7043–47
    [Google Scholar]
  36. Gallin WJ, Chuong CM, Finkel LH, Edelman GM. 1986. Antibodies to liver cell adhesion molecule perturb inductive interactions and alter feather pattern and structure. PNAS 83:8235–39
    [Google Scholar]
  37. Garcia MA, Nelson WJ, Chavez N. 2018. Cell-cell junctions organize structural and signaling networks. Cold Spring Harb. Perspect. Biol. 10:a029181
    [Google Scholar]
  38. Giudicelli F, Taillebourg E, Charnay P, Gilardi-Hebenstreit P. 2001. Krox-20 patterns the hindbrain through both cell-autonomous and non cell-autonomous mechanisms. Genes Dev 15:567–80
    [Google Scholar]
  39. Glazier JA, Graner F. 1993. Simulation of the differential adhesion driven rearrangement of biological cells. Phys. Rev. E 47:2128–54
    [Google Scholar]
  40. Godt D, Tepass U. 1998. Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395:387–91
    [Google Scholar]
  41. Goodman KM, Rubinstein R, Thu CA, Mannepalli S, Bahna F et al. 2016. γ-Protocadherin structural diversity and functional implications. eLife 5:e20930
    [Google Scholar]
  42. Harley RJ, Murdy JP, Wang Z, Kelly MC, Ropp T-JF et al. 2018. Neuronal cell adhesion molecule (NrCAM) is expressed by sensory cells in the cochlea and is necessary for proper cochlear innervation and sensory domain patterning during development. Dev. Dyn. 247:934–50
    [Google Scholar]
  43. Harris AR, Daeden A, Charras GT. 2014. Formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers. J. Cell Sci. 127:2507–17
    [Google Scholar]
  44. Hatta K, Okada TS, Takeichi M. 1985. A monoclonal antibody disrupting calcium-dependent cell-cell adhesion of brain tissues: possible role of its target antigen in animal pattern formation. PNAS 82:2789–93
    [Google Scholar]
  45. Hayashi S, Inoue Y, Kiyonari H, Abe T, Misaki K et al. 2014. Protocadherin-17 mediates collective axon extension by recruiting actin regulator complexes to interaxonal contacts. Dev. Cell 30:673–87
    [Google Scholar]
  46. Hayashi T, Carthew RW. 2004. Surface mechanics mediate pattern formation in the developing retina. Nature 431:647–52
    [Google Scholar]
  47. Hertel N, Krishna-K Nuernberger M, Redies C 2008. A cadherin-based code for the divisions of the mouse basal ganglia. J. Comp. Neurol. 508:511–28
    [Google Scholar]
  48. Hirano S, Yan Q, Suzuki ST 1999. Expression of a novel protocadherin, OL-protocadherin, in a subset of functional systems of the developing mouse brain. J. Neurosci. 19:995–1005
    [Google Scholar]
  49. Holtfreter J. 1943. Properties and functions of the surface coat in amphibian embryos. J. Exp. Zool. 93:251–323
    [Google Scholar]
  50. Honda H, Yamanaka H, Eguchi G. 1986. Transformation of a polygonal cellular pattern during sexual maturation of the avian oviduct epithelium: computer simulation. J. Embryol. Exp. Morphol. 98:1–19
    [Google Scholar]
  51. Honda T, Shimizu K, Kawakatsu T, Yasumi M, Shingai T et al. 2003. Antagonistic and agonistic effects of an extracellular fragment of nectin on formation of E-cadherin-based cell-cell adhesion. Genes Cells 8:51–63
    [Google Scholar]
  52. Hughes ME, Bortnick R, Tsubouchi A, Bäumer P, Kondo M et al. 2007. Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 54:417–27
    [Google Scholar]
  53. Inagaki M, Irie K, Ishizaki H, Tanaka-Okamoto M, Morimoto K et al. 2005. Roles of cell-adhesion molecules nectin 1 and nectin 3 in ciliary body development. Development 132:1525–37
    [Google Scholar]
  54. Katsamba P, Carroll K, Ahlsen G, Bahna F, Vendome J et al. 2009. Linking molecular affinity and cellular specificity in cadherin-mediated adhesion. PNAS 106:11594–99
    [Google Scholar]
  55. Katsunuma S, Honda H, Shinoda T, Ishimoto Y, Miyata T et al. 2016. Synergistic action of nectins and cadherins generates the mosaic cellular pattern of the olfactory epithelium. J. Cell Biol. 212:561–75
    [Google Scholar]
  56. 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 125:4681–90
    [Google Scholar]
  57. Kindberg AA, Srivastava V, Muncie JM, Weaver VM, Gartner ZJ, Bush JO. 2021. EPH/EPHRIN regulates cellular organization by actomyosin contractility effects on cell contacts. J. Cell Biol. 220:e202005216
    [Google Scholar]
  58. Kraft B, Berger CD, Wallkamm V, Steinbeisser H, Wedlich D. 2012. Wnt-11 and Fz7 reduce cell adhesion in convergent extension by sequestration of PAPC and C-cadherin. J. Cell Biol. 198:695–709
    [Google Scholar]
  59. Krieg M, Arboleda-Estudillo Y, Puech P-H, Käfer J, Graner F et al. 2008. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 10:429–36
    [Google Scholar]
  60. Kubota F, Murakami T, Tajika Y, Yorifuji H. 2004. Expression of protocadherin 18 in the CNS and pharyngeal arches of zebrafish embryos. Int. J. Dev. Biol. 52:397–405
    [Google Scholar]
  61. Kullander K, Mather NK, Diella F, Dottori M, Boyd AW, Klein R. 2001. Kinase-dependent and kinase-independent functions of EphA4 receptors in major axon tract formation in vivo. Neuron 29:73–84
    [Google Scholar]
  62. Kuroda H, Inui M, Sugimoto K, Hayata T, Asashima M. 2002. Axial protocadherin is a mediator of prenotochord cell sorting in Xenopus. Dev. Biol. 244:267–77
    [Google Scholar]
  63. Laplante C, Nilson LA. 2006. Differential expression of the adhesion molecule Echinoid drives epithelial morphogenesis in Drosophila. Development 133:3255–64
    [Google Scholar]
  64. Lefebvre JL, Kostadinov D, Chen WV, Maniatis T, Sanes JR. 2012. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488:517–21
    [Google Scholar]
  65. Lin J, Wang C, Redies C. 2012. Expression of delta-protocadherins in the spinal cord of the chicken embryo. J. Comp. Neurol. 520:1509–31
    [Google Scholar]
  66. Lin J, Wang C, Yang C, Fu S, Redies C. 2016. Pax3 and Pax7 interact reciprocally and regulate the expression of cadherin-7 through inducing neuron differentiation in the developing chicken spinal cord. J. Comp. Neurol. 524:940–62
    [Google Scholar]
  67. Liu Q, Chen Y, Pan JJ, Murakami T. 2009. Expression of protocadherin-9 and protocadherin-17 in the nervous system of the embryonic zebrafish. Gene Expr. Patterns 9:490–96
    [Google Scholar]
  68. Maître J-L, Berthoumieux H, Krens SFG, Salbreux G, Jülicher F et al. 2012. Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 338:253–56
    [Google Scholar]
  69. Maître J-L, Heisenberg C-P. 2013. Three functions of cadherins in cell adhesion. Curr. Biol. 23:R626–33
    [Google Scholar]
  70. Maître J-L, Turlier H, Illukkumbura R, Eismann B, Niwayama R et al. 2016. Asymmetric division of contractile domains couples cell positioning and fate specification. Nature 536:344–48
    [Google Scholar]
  71. Manning ML, Foty RA, Steinberg MS, Schoetz E-M. 2010. Coaction of intercellular adhesion and cortical tension specifies tissue surface tension. PNAS 107:12517–22
    [Google Scholar]
  72. Mansouri A, Gruss P. 1998. Pax3 and Pax7 are expressed in commissural neurons and restrict ventral neuronal identity in the spinal cord. Mech. Dev. 78:171–78
    [Google Scholar]
  73. Matthews BJ, Kim ME, Flanagan JJ, Hattori D, Clemens JC et al. 2007. Dendrite self-avoidance is controlled by Dscam. Cell 129:593–604
    [Google Scholar]
  74. Mellitzer G, Xu Q, Wilkinson DG. 1999. Eph receptors and ephrins restrict cell intermingling and communication. Nature 400:77–81
    [Google Scholar]
  75. Mongera A, Rowghanian P, Gustafson HJ, Shelton E, Kealhofer DA et al. 2018. A fluid-to-solid jamming transition underlies vertebrate body axis elongation. Nature 561:401–5
    [Google Scholar]
  76. Moore S, Ribes V, Terriente J, Wilkinson D, Relaix F, Briscoe J. 2013. Distinct regulatory mechanisms act to establish and maintain Pax3 expression in the developing neural tube. PLOS Genet 9:e1003811
    [Google Scholar]
  77. Moscona A, Moscona H. 1952. The dissociation and aggregation of cells from organ rudiments of the early chick embryo. J. Anat. 86:287–301
    [Google Scholar]
  78. Müller K, Hirano S, Puelles L, Redies C. 2004. OL-protocadherin expression in the visual system of the chicken embryo. J. Comp. Neurol. 470:240–55
    [Google Scholar]
  79. Nagar B, Overduin M, Ikura M, Rini JM. 1996. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 380:360–64
    [Google Scholar]
  80. Nakajima Y, Morimoto M, Takahashi Y, Koseki H, Saga Y. 2006. Identification of Epha4 enhancer required for segmental expression and the regulation by Mesp2. Development 133:2517–25
    [Google Scholar]
  81. Nguyen TM, Arthur A, Gronthos S 2016. The role of Eph/ephrin molecules in stromal-hematopoietic interactions. Int. J. Hematol. 103:145–54
    [Google Scholar]
  82. Niessen CM, Gumbiner BM. 2002. Cadherin-mediated cell sorting not determined by binding or adhesion specificity. J. Cell Biol. 156:389–400
    [Google Scholar]
  83. Nonchev S, Vesque C, Maconochie M, Seitanidou T, Ariza-McNaughton L et al. 1996. Segmental expression of Hoxa-2 in the hindbrain is directly regulated by Krox-20. Development 122:543–54
    [Google Scholar]
  84. Nose A, Nagafuchi A, Takeichi M. 1988. Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54:993–1001
    [Google Scholar]
  85. Nose A, Takeichi M. 1986. A novel cadherin cell adhesion molecule: its expression patterns associated with implantation and organogenesis of mouse embryos. J. Cell Biol. 103:2649–58
    [Google Scholar]
  86. Novitch BG, Chen AI, Jessell TM. 2001. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31:773–89
    [Google Scholar]
  87. Ozaki-Kuroda K, Nakanishi H, Ohta H, Tanaka H, Kurihara H et al. 2002. Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr. Biol. 12:1145–50
    [Google Scholar]
  88. Palmer A, Zimmer M, Erdmann KS, Eulenburg V, Porthin A et al. 2002. EphrinB phosphorylation and reverse signaling: regulation by Src kinases and PTP-BL phosphatase. Mol. Cell 9:725–37
    [Google Scholar]
  89. Pancho A, Aerts T, Mitsogiannis MD, Seuntjens E. 2020. Protocadherins at the crossroad of signaling pathways. Front. Mol. Neurosci. 13:117
    [Google Scholar]
  90. Paré AC, Naik P, Shi J, Mirman Z, Palmquist KH, Zallen JA. 2019. An LRR receptor-teneurin system directs planar polarity at compartment boundaries. Dev. Cell 51:208–221.e6
    [Google Scholar]
  91. Paré AC, Vichas A, Fincher CT, Mirman Z, Farrell DL et al. 2014. A positional Toll receptor code directs convergent extension in Drosophila. Nature 515:523–27
    [Google Scholar]
  92. Park H-C, Mehta A, Richardson JS, Appel B. 2002. olig2 is required for zebrafish primary motor neuron and oligodendrocyte development. Dev. Biol. 248:356–68
    [Google Scholar]
  93. Pasquale EB. 1997. The Eph family of receptors. Curr. Opin. Cell Biol. 9:608–15
    [Google Scholar]
  94. Pasquale EB. 2004. Eph-ephrin promiscuity is now crystal clear. Nat. Neurosci. 7:417–18
    [Google Scholar]
  95. Patel SD, Chen CP, Bahna F, Honig B, Shapiro L. 2003. Cadherin-mediated cell-cell adhesion: sticking together as a family. Curr. Opin. Struct. Biol. 13:690–98
    [Google Scholar]
  96. Patel SD, Ciatto C, Chen CP, Bahna F, Rajebhosale M et al. 2006. Type II cadherin ectodomain structures: implications for classical cadherin specificity. Cell 124:1255–68
    [Google Scholar]
  97. Pawlizak S, Fritsch AW, Grosser S, Ahrens D, Thalheim T et al. 2015. Testing the differential adhesion hypothesis across the epithelial-mesenchymal transition. New J. Phys. 17:083049
    [Google Scholar]
  98. Pederick DT, Richards KL, Piltz SG, Kumar R, Mincheva-Tasheva S et al. 2018. Abnormal cell sorting underlies the unique X-linked inheritance of PCDH19 epilepsy. Neuron 97:59–66.e5
    [Google Scholar]
  99. Perez TD, Tamada M, Sheetz MP, Nelson WJ. 2008. Immediate-early signaling induced by E-cadherin engagement and adhesion. J. Biol. Chem. 283:5014–22
    [Google Scholar]
  100. Petridou NI, Corominas-Murtra B, Heisenberg C-P, Hannezo E. 2021. Rigidity percolation uncovers a structural basis for embryonic tissue phase transitions. Cell 184:1914–28.e19
    [Google Scholar]
  101. Price SR, De Marco Garcia NV, Ranscht B, Jessell TM 2002. Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109:205–16
    [Google Scholar]
  102. Priya R, Allanki S, Gentile A, Mansingh S, Uribe V et al. 2020. Tension heterogeneity directs form and fate to pattern the myocardial wall. Nature 588:130–34
    [Google Scholar]
  103. Raj A, van Oudenaarden A. 2008. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135:216–26
    [Google Scholar]
  104. Redies C, Takeichi M. 1996. Cadherins in the developing central nervous system: an adhesive code for segmental and functional subdivisions. Dev. Biol. 180:413–23
    [Google Scholar]
  105. Rohani N, Parmeggiani A, Winklbauer R, Fagotto F. 2014. Variable combinations of specific ephrin ligand/Eph receptor pairs control embryonic tissue separation. PLOS Biol 12:e1001955
    [Google Scholar]
  106. Rousso DL, Pearson CA, Gaber ZB, Miquelajauregui A, Li S et al. 2012. Foxp-mediated suppression of N-cadherin regulates neuroepithelial character and progenitor maintenance in the CNS. Neuron 74:314–30
    [Google Scholar]
  107. Rubinstein R, Goodman KM, Maniatis T, Shapiro L, Honig B. 2017. Structural origins of clustered protocadherin-mediated neuronal barcoding. Semin. Cell Dev. Biol. 69:140–50
    [Google Scholar]
  108. Rubinstein R, Thu CA, Goodman KM, Wolcott HN, Bahna F et al. 2015. Molecular logic of neuronal self-recognition through protocadherin domain interactions. Cell 163:629–42
    [Google Scholar]
  109. Sano K, Tanihara H, Heimark RL, Obata S, Davidson M et al. 1993. Protocadherins: a large family of cadherin-related molecules in central nervous system. EMBO J 12:2249–56
    [Google Scholar]
  110. Satoh-Horikawa K, Nakanishi H, Takahashi K, Miyahara M, Nishimura M et al. 2000. Nectin-3, a new member of immunoglobulin-like cell adhesion molecules that shows homophilic and heterophilic cell-cell adhesion activities. J. Biol. Chem. 275:10291–99
    [Google Scholar]
  111. Schier AF. 2001. Axis formation and patterning in zebrafish. Curr. Opin. Genet. Dev. 11:393–404
    [Google Scholar]
  112. Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J et al. 2000. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101:671–84
    [Google Scholar]
  113. Schötz E, Burdine RD, Jülicher F, Steinberg MS, Heisenberg C, Foty RA. 2008. Quantitative differences in tissue surface tension influence zebrafish germ layer positioning. HFSP J 2:42–56
    [Google Scholar]
  114. Schreiner D, Weiner JA. 2010. Combinatorial homophilic interaction between γ-protocadherin multimers greatly expands the molecular diversity of cell adhesion. PNAS 107:14893–98
    [Google Scholar]
  115. Sham MH, Vesque C, Nonchev S, Marshall H, Frain M et al. 1993. The zinc finger gene Krox20 regulates HoxB2 (Hox2.8) during hindbrain segmentation. Cell 72:183–96
    [Google Scholar]
  116. Shapiro L, Fannon AM, Kwong PD, Thompson A, Lehmann MS et al. 1995. Structural basis of cell-cell adhesion by cadherins. Nature 374:327–37
    [Google Scholar]
  117. Steinberg MS. 1963. Reconstruction of tissues by dissociated cells. Science 141:401–8
    [Google Scholar]
  118. Steinberg MS, Takeichi M. 1994. Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. PNAS 91:206–9
    [Google Scholar]
  119. Sugino H, Hamada S, Yasuda R, Tuji A, Matsuda Y et al. 2000. Genomic organization of the family of CNR cadherin genes in mice and humans. Genomics 63:75–87
    [Google Scholar]
  120. Sugino H, Yanase H, Hamada S, Kurokawa K, Asakawa S et al. 2004. Distinct genomic sequence of the CNR/Pcdhα genes in chicken. Biochem. Biophys. Res. Commun. 316:437–45
    [Google Scholar]
  121. Suo L, Lu H, Ying G, Capecchi MR, Wu Q. 2012. Protocadherin clusters and cell adhesion kinase regulate dendrite complexity through Rho GTPase. J. Mol. Cell Biol. 4:362–76
    [Google Scholar]
  122. Suzuki SC, Inoue T, Kimura Y, Tanaka T, Takeichi M. 1997. Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol. Cell. Neurosci. 9:433–47
    [Google Scholar]
  123. Tachibana K, Nakanishi H, Mandai K, Ozaki K, Ikeda W et al. 2000. Two cell adhesion molecules, nectin and cadherin, interact through their cytoplasmic domain-associated proteins. J. Cell Biol. 150:1161–76
    [Google Scholar]
  124. Tai K, Kubota M, Shiono K, Tokutsu H, Suzuki ST. 2010. Adhesion properties and retinofugal expression of chicken protocadherin-19. Brain Res 1344:13–24
    [Google Scholar]
  125. Takahashi K, Nakanishi H, Miyahara M, Mandai K, Satoh K et al. 1999. 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. 145:539–49
    [Google Scholar]
  126. Takai Y, Nakanishi H. 2003. Nectin and afadin: novel organizers of intercellular junctions. J. Cell Sci. 116:17–27
    [Google Scholar]
  127. Takeichi M. 1977. Functional correlation between cell adhesive properties and some cell surface proteins. J. Cell Biol. 75:464–74
    [Google Scholar]
  128. Tamura K, Shan W-S, Hendrickson WA, Colman DR, Shapiro L. 1998. Structure-function analysis of cell adhesion by neural (N-) cadherin. Neuron 20:1153–63
    [Google Scholar]
  129. Tasic B, Nabholz CE, Baldwin KK, Kim Y, Rueckert EH et al. 2002. Promoter choice determines splice site selection in protocadherin α and γ pre-mRNA splicing. Mol. Cell 10:21–33
    [Google Scholar]
  130. Theil T, Frain M, Gilardi-Hebenstreit P, Flenniken A, Charnay P, Wilkinson DG. 1998. Segmental expression of the EphA4 (Sek-1) receptor tyrosine kinase in the hindbrain is under direct transcriptional control of Krox-20. Development 125:443–52
    [Google Scholar]
  131. Thu CA, Chen WV, Rubinstein R, Chevee M, Wolcott HN et al. 2014. Single-cell identity generated by combinatorial homophilic interactions between α, β, and γ protocadherins. Cell 158:1045–59
    [Google Scholar]
  132. Toda S, Brunger JM, Lim W. 2019. Synthetic development: learning to program multicellular self-organization. Curr. Opin. Syst. Biol. 14:41–49
    [Google Scholar]
  133. Togashi H. 2016. Differential and cooperative cell adhesion regulates cellular pattern in sensory epithelia. Front. Cell Dev. Biol. 4:104
    [Google Scholar]
  134. Togashi H, Kominami K, Waseda M, Komura H, Miyoshi J et al. 2011. Nectins establish a checkerboard-like cellular pattern in the auditory epithelium. Science 333:1144–47
    [Google Scholar]
  135. Townes PL, Holtfreter J. 1955. Directed movements and selective adhesion of embryonic amphibian cells. J. Exp. Zool. 128:53–120
    [Google Scholar]
  136. Tsai TY-C, Sikora M, Xia P, Colak-Champollion T, Knaut H et al. 2020. An adhesion code ensures robust pattern formation during tissue morphogenesis. Science 370:113–16
    [Google Scholar]
  137. Vanhalst K, Kools P, Staes K, van Roy F, Redies C. 2005. δ-Protocadherins: a gene family expressed differentially in the mouse brain. Cell. Mol. Life Sci. 62:1247–59
    [Google Scholar]
  138. von der Hardt S, Bakkers J, Inbal A, Carvalho L, Solnica-Krezel L et al. 2007. The Bmp gradient of the zebrafish gastrula guides migrating lateral cells by regulating cell-cell adhesion. Curr. Biol. 17:475–87
    [Google Scholar]
  139. Watanabe T, Sato Y, Saito D, Tadokoro R, Takahashi Y. 2009. EphrinB2 coordinates the formation of a morphological boundary and cell epithelialization during somite segmentation. PNAS 106:7467–72
    [Google Scholar]
  140. Wilson HV. 1907. On some phenomena of coalescence and regeneration in sponges. J. Exp. Zool. 5:245–58
    [Google Scholar]
  141. Wilson HV, Penney JT. 1930. The regeneration of sponges (Microciona) from dissociated cells. J. Exp. Zool. 56:73–147
    [Google Scholar]
  142. Witzel S, Zimyanin V, Carreira-Barbosa F, Tada M, Heisenberg C-P. 2006. Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane. J. Cell Biol. 175:791–802
    [Google Scholar]
  143. Wolpert L. 1969. Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25:1–47
    [Google Scholar]
  144. Wu Q. 2005. Comparative genomics and diversifying selection of the clustered vertebrate protocadherin. Genetics 169:2179–88
    [Google Scholar]
  145. Wu Q, Maniatis T. 1999. A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97:779–90
    [Google Scholar]
  146. Xu Q, Alldus G, Holder N, Wilkinson DG. 1995. Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain. Development 121:4005–16
    [Google Scholar]
  147. Xu Q, Mellitzer G, Robinson V, Wilkinson DG 1999. In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature 399:267–71
    [Google Scholar]
  148. Yamada S, Nelson WJ. 2007. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J. Cell Biol. 178:517–27
    [Google Scholar]
  149. Yamagata K, Andreasson KI, Sugiura H, Maru E, Dominique M et al. 1999. Arcadlin is a neural activity-regulated cadherin involved in long term potentiation. J. Biol. Chem. 274:19473–79
    [Google Scholar]
  150. Yasuda S, Tanaka H, Sugiura H, Okamura K, Sakaguchi T et al. 2007. Activity-induced protocadherin arcadlin regulates dendritic spine number by triggering N-cadherin endocytosis via TAO2β and p38 MAP kinases. Neuron 56:456–71
    [Google Scholar]
  151. Yoshida K. 2003. Fibroblast cell shape and adhesion in vitro is altered by overexpression of the 7a and 7b isoforms of protocadherin 7, but not the 7c isoform. Cell. Mol. Biol. Lett. 8: 3 735–42
    [Google Scholar]
  152. Yoshida C, Takeichi M. 1982. Teratocarcinoma cell adhesion: identification of a cell-surface protein involved in calcium-dependent cell aggregation. Cell 28:217–24
    [Google Scholar]
  153. Youssef J, Nurse AK, Freund LB, Morgan JR. 2011. Quantification of the forces driving self-assembly of three-dimensional microtissues. PNAS 108:6993–98
    [Google Scholar]
  154. Zhang Y, Thomas GL, Swat M, Shirinifard A, Glazier JA. 2011. Computer simulations of cell sorting due to differential adhesion. PLOS ONE 6:e24999
    [Google Scholar]
  155. Zisch AH, Kalo MS, Chong LD, Pasquale EB. 1998. Complex formation between EphB2 and Src requires phosphorylation of tyrosine 611 in the EphB2 juxtamembrane region. Oncogene 16:2657–70
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-120420-100215
Loading
/content/journals/10.1146/annurev-cellbio-120420-100215
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error