1932

Abstract

Multicellular organisms generate tissues of diverse shapes and functions from cells and extracellular matrices. Their adhesion molecules mediate cell-cell and cell-matrix interactions, which not only play crucial roles in maintaining tissue integrity but also serve as key regulators of tissue morphogenesis. Cells constantly probe their environment to make decisions: They integrate chemical and mechanical information from the environment via diffusible ligand- or adhesion-based signaling to decide whether to release specific signaling molecules or enzymes, to divide or differentiate, to move away or stay, or even whether to live or die. These decisions in turn modify their environment, including the chemical nature and mechanical properties of the extracellular matrix. Tissue morphology is the physical manifestation of the remodeling of cells and matrices by their historical biochemical and biophysical landscapes. We review our understanding of matrix and adhesion molecules in tissue morphogenesis, with an emphasis on key physical interactions that drive morphogenesis.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-020223-031019
2023-10-16
2024-06-21
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/39/1/annurev-cellbio-020223-031019.html?itemId=/content/journals/10.1146/annurev-cellbio-020223-031019&mimeType=html&fmt=ahah

Literature Cited

  1. Afratis NA, Nikitovic D, Multhaupt HAB, Theocharis AD, Couchman JR, Karamanos NK. 2017. Syndecans—key regulators of cell signaling and biological functions. FEBS J. 284:127–41
    [Google Scholar]
  2. Amack JD, Manning ML. 2012. Knowing the boundaries: extending the differential adhesion hypothesis in embryonic cell sorting. Science 338:6104212–15
    [Google Scholar]
  3. Anastasiadis PZ, Moon SY, Thoreson MA, Mariner DJ, Crawford HC et al. 2000. Inhibition of RhoA by p120 catenin. Nat. Cell Biol. 2:9637–44
    [Google Scholar]
  4. Arikawa-Hirasawa E, Watanabe H, Takami H, Hassell JR, Yamada Y. 1999. Perlecan is essential for cartilage and cephalic development. Nat. Genet. 23:3354–58
    [Google Scholar]
  5. Asai R, Taguchi E, Kume Y, Saito M, Kondo S. 1999. Zebrafish Leopard gene as a component of the putative reaction-diffusion system. Mech. Dev. 89:187–92
    [Google Scholar]
  6. Bader BL, Smyth N, Nedbal S, Miosge N, Baranowsky A et al. 2005. Compound genetic ablation of nidogen 1 and 2 causes basement membrane defects and perinatal lethality in mice. Mol. Cell. Biol. 25:156846–56
    [Google Scholar]
  7. Bailles A, Gehrels EW, Lecuit T. 2022. Mechanochemical principles of spatial and temporal patterns in cells and tissues. Annu. Rev. Cell Dev. Biol. 38:321–47
    [Google Scholar]
  8. Bambardekar K, Clément R, Blanc O, Chardès C, Lenne P-F. 2015. Direct laser manipulation reveals the mechanics of cell contacts in vivo. PNAS 112:51416–21
    [Google Scholar]
  9. Bao M, Cornwall-Scoones J, Sanchez-Vasquez E, Chen D-Y, De Jonghe J et al. 2022. Stem cell-derived synthetic embryos self-assemble by exploiting cadherin codes and cortical tension. Nat. Cell Biol. 24:91341–49
    [Google Scholar]
  10. Barriga EH, Franze K, Charras G, Mayor R. 2018. Tissue stiffening coordinates morphogenesis by triggering collective cell migration in vivo. Nature 554:7693523–27
    [Google Scholar]
  11. Blauth E, Kubitschke H, Gottheil P, Grosser S, Käs JA. 2021. Jamming in embryogenesis and cancer progression. Front. Phys. 9:666709
    [Google Scholar]
  12. Boggon TJ, Murray J, Chappuis-Flament S, Wong E, Gumbiner BM, Shapiro L. 2002. C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 296:55711308–13
    [Google Scholar]
  13. Boucaut JC, Darribère T, Boulekbache H, Thiery JP. 1984. Prevention of gastrulation but not neurulation by antibodies to fibronectin in amphibian embryos. Nature 307:5949364–67
    [Google Scholar]
  14. Brandan E, Cabello-Verrugio C, Vial C. 2008. Novel regulatory mechanisms for the proteoglycans decorin and biglycan during muscle formation and muscular dystrophy. Matrix Biol. 27:8700–8
    [Google Scholar]
  15. Brodland GW. 2002. The differential interfacial tension hypothesis (DITH): a comprehensive theory for the self-rearrangement of embryonic cells and tissues. J. Biomech. Eng. 124:2188–97
    [Google Scholar]
  16. Buckley CD, Tan J, Anderson KL, Hanein D, Volkmann N et al. 2014. The minimal cadherin-catenin complex binds to actin filaments under force. Science 346:62091254211
    [Google Scholar]
  17. Campàs O, Mammoto T, Hasso S, Sperling RA, O'Connell D et al. 2014. Quantifying cell-generated mechanical forces within living embryonic tissues. Nat. Methods 11:2183–89
    [Google Scholar]
  18. Campbell ID, Humphries MJ. 2011. Integrin structure, activation, and interactions. Cold Spring Harb. Perspect. Biol. 3:3a004994
    [Google Scholar]
  19. Carta L, Pereira L, Arteaga-Solis E, Lee-Arteaga SY, Lenart B et al. 2006. Fibrillins 1 and 2 perform partially overlapping functions during aortic development. J. Biol. Chem. 281:128016–23
    [Google Scholar]
  20. Cerchiari AE, Garbe JC, Jee NY, Todhunter ME, Broaders KE et al. 2015. A strategy for tissue self-organization that is robust to cellular heterogeneity and plasticity. PNAS 112:72287–92
    [Google Scholar]
  21. Chaudhuri O, Cooper-White J, Janmey PA, Mooney DJ, Shenoy VB. 2020. Effects of extracellular matrix viscoelasticity on cellular behaviour. Nature 584:7822535–46
    [Google Scholar]
  22. Chen KH, Boettiger AN, Moffitt JR, Wang S, Zhuang X. 2015. Spatially resolved, highly multiplexed RNA profiling in single cells. Science 348:6233aaa6090
    [Google Scholar]
  23. Chen X-D, Fisher LW, Robey PG, Young MF. 2004. The small leucine-rich proteoglycan biglycan modulates BMP-4-induced osteoblast differentiation. FASEB J. 18:9948–58
    [Google Scholar]
  24. Chisholm AD, Hardin J. 2005. Epidermal morphogenesis. WormBook: The Online Review of C. elegans Biology n.p.: WormBook http://www.wormbook.org/chapters/www_epidermalmorphogenesis/epidermalmorphogenesis.html
    [Google Scholar]
  25. Cochet-Escartin O, Locke TT, Shi WH, Steele RE, Collins E-MS. 2017. Physical mechanisms driving cell sorting in Hydra. Biophys. J. 113:122827–41
    [Google Scholar]
  26. Costell M, Gustafsson E, Aszódi A, Mörgelin M, Bloch W et al. 1999. Perlecan maintains the integrity of cartilage and some basement membranes. J. Cell Biol. 147:51109–22
    [Google Scholar]
  27. Crest J, Diz-Muñoz A, Chen D-Y, Fletcher DA, Bilder D. 2017. Organ sculpting by patterned extracellular matrix stiffness. eLife 6:e24958
    [Google Scholar]
  28. Cruz Walma DA, Yamada KM 2020. The extracellular matrix in development. Development 147:10dev175596
    [Google Scholar]
  29. Cummings CF, Pedchenko V, Brown KL, Colon S, Rafi M et al. 2016. Extracellular chloride signals collagen IV network assembly during basement membrane formation. J. Cell Biol. 213:4479–94
    [Google Scholar]
  30. Cummins PM. 2012. Occludin: one protein, many forms. Mol. Cell. Biol. 32:2242–50
    [Google Scholar]
  31. Dai J, Estrada B, Jacobs S, Sánchez-Sánchez BJ, Tang J et al. 2018. Dissection of nidogen function in Drosophila reveals tissue-specific mechanisms of basement membrane assembly. PLOS Genet. 14:9e1007483
    [Google Scholar]
  32. Davis EC. 1993. Stability of elastin in the developing mouse aorta: a quantitative radioautographic study. Histochemistry 100:117–26
    [Google Scholar]
  33. Dicker KT, Gurski LA, Pradhan-Bhatt S, Witt RL, Farach-Carson MC, Jia X. 2014. Hyaluronan: a simple polysaccharide with diverse biological functions. Acta Biomater. 10:41558–70
    [Google Scholar]
  34. Doubrovinski K, Swan M, Polyakov O, Wieschaus EF. 2017. Measurement of cortical elasticity in Drosophila melanogaster embryos using ferrofluids. PNAS 114:51051–56
    [Google Scholar]
  35. Doyle AD, Nazari SS, Yamada KM. 2022. Cell-extracellular matrix dynamics. Phys. Biol. 19:2021002
    [Google Scholar]
  36. Economou AD, Ohazama A, Porntaveetus T, Sharpe PT, Kondo S et al. 2012. Periodic stripe formation by a Turing mechanism operating at growth zones in the mammalian palate. Nat. Genet. 44:3348–51
    [Google Scholar]
  37. Elosegui-Artola A, Oria R, Chen Y, Kosmalska A, Pérez-González C et al. 2016. Mechanical regulation of a molecular clutch defines force transmission and transduction in response to matrix rigidity. Nat. Cell Biol. 18:5540–48
    [Google Scholar]
  38. Elowitz MB, Levine AJ, Siggia ED, Swain PS. 2002. Stochastic gene expression in a single cell. Science 297:55841183–86
    [Google Scholar]
  39. Eng C-HL, Lawson M, Zhu Q, Dries R, Koulena N et al. 2019. Transcriptome-scale super-resolved imaging in tissues by RNA seqFISH+. Nature 568:7751235–39
    [Google Scholar]
  40. Farach-Carson MC, Carson DD. 2007. Perlecan—a multifunctional extracellular proteoglycan scaffold. Glycobiology 17:9897–905
    [Google Scholar]
  41. Fawzi NL. 2020. Elastin phase separation—structure or disorder?. Nat. Rev. Mol. Cell Biol. 21:10568–69
    [Google Scholar]
  42. Fidler AL, Darris CE, Chetyrkin SV, Pedchenko VK, Boudko SP et al. 2017. Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues. eLife 6:e24176
    [Google Scholar]
  43. Fiore VF, Krajnc M, Quiroz FG, Levorse J, Pasolli HA et al. 2020. Mechanics of a multilayer epithelium instruct tumour architecture and function. Nature 585:7825433–39
    [Google Scholar]
  44. Foty RA, Pfleger CM, Forgacs G, Steinberg MS. 1996. Surface tensions of embryonic tissues predict their mutual envelopment behavior. Development 122:51611–20
    [Google Scholar]
  45. Foty RA, Steinberg MS. 2005. The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278:1255–63
    [Google Scholar]
  46. Frantz C, Stewart KM, Weaver VM. 2010. The extracellular matrix at a glance. J. Cell Sci. 123:244195–200
    [Google Scholar]
  47. Fujita Y, Krause G, Scheffner M, Zechner D, Molina Leddy HE et al. 2002. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 4:3222–31
    [Google Scholar]
  48. Gao Y, Xiong X, Wong S, Charles EJ, Lim WA, Qi LS. 2016. Complex transcriptional modulation with orthogonal and inducible dCas9 regulators. Nat. Methods 13:121043–49
    [Google Scholar]
  49. Geiger B, Yamada KM. 2011. Molecular architecture and function of matrix adhesions. Cold Spring Harb. Perspect. Biol. 3:5a005033
    [Google Scholar]
  50. Gierer A, Meinhardt H. 1972. A theory of biological pattern formation. Kybernetik 12:130–39
    [Google Scholar]
  51. Gleghorn L, Ramesar R, Beighton P, Wallis G. 2005. A mutation in the variable repeat region of the aggrecan gene (AGC1) causes a form of spondyloepiphyseal dysplasia associated with severe, premature osteoarthritis. Am. J. Hum. Genet. 77:3484–90
    [Google Scholar]
  52. Haigo SL, Bilder D. 2011. Global tissue revolutions in a morphogenetic movement controlling elongation. Science 331:60201071–74
    [Google Scholar]
  53. Harris AK. 1976. Is cell sorting caused by differences in the work of intercellular adhesion? A critique of the Steinberg hypothesis. J. Theor. Biol. 61:2267–85
    [Google Scholar]
  54. Harrison OJ, Bahna F, Katsamba PS, Jin X, Brasch J et al. 2010. Two-step adhesive binding by classical cadherins. Nat. Struct. Mol. Biol. 17:3348–57
    [Google Scholar]
  55. Harrison OJ, Jin X, Hong S, Bahna F, Ahlsen G et al. 2011. The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins. Structure 19:2244–56
    [Google Scholar]
  56. Harunaga JS, Doyle AD, Yamada KM. 2014. Local and global dynamics of the basement membrane during branching morphogenesis require protease activity and actomyosin contractility. Dev. Biol. 394:2197–205
    [Google Scholar]
  57. Hiscock TW, Megason SG. 2015. Mathematically guided approaches to distinguish models of periodic patterning. Development 142:3409–19
    [Google Scholar]
  58. Honke K. 2013. Biosynthesis and biological function of sulfoglycolipids. Proc. Jpn. Acad. Ser. B 89:4129–38
    [Google Scholar]
  59. Hsu JC, Koo H, Harunaga JS, Matsumoto K, Doyle AD, Yamada KM. 2013. Region-specific epithelial cell dynamics during branching morphogenesis. Dev. Dyn. 242:91066–77
    [Google Scholar]
  60. Huet-Calderwood C, Rivera-Molina FE, Toomre DK, Calderwood DA. 2022. Fibroblasts secrete fibronectin under lamellipodia in a microtubule- and myosin II-dependent fashion. J. Cell Biol. 222:2e202204100
    [Google Scholar]
  61. Hulpiau P, van Roy F. 2009. Molecular evolution of the cadherin superfamily. Int. J. Biochem. Cell Biol. 41:2349–69
    [Google Scholar]
  62. Hynes RO. 2002. Integrins: bidirectional, allosteric signaling machines. Cell 110:6673–87
    [Google Scholar]
  63. Ilina O, Gritsenko PG, Syga S, Lippoldt J, La Porta CAM et al. 2020. Cell–cell adhesion and 3D matrix confinement determine jamming transitions in breast cancer invasion. Nat. Cell Biol. 22:91103–15
    [Google Scholar]
  64. Ishiyama N, Lee S-H, Liu S, Li G-Y, Smith MJ et al. 2010. Dynamic and static interactions between p120 catenin and E-cadherin regulate the stability of cell-cell adhesion. Cell 141:1117–28
    [Google Scholar]
  65. Janmey PA, Hinz B, McCulloch CA. 2021. Physics and physiology of cell spreading in two and three dimensions. Physiology 36:6382–91
    [Google Scholar]
  66. Jayadev R, Sherwood DR. 2017. Basement membranes. Curr. Biol. 27:6R207–11
    [Google Scholar]
  67. Jiang D, Smith WC. 2007. Ascidian notochord morphogenesis. Dev. Dyn. 236:71748–57
    [Google Scholar]
  68. Jo MH, Li J, Jaumouillé V, Hao Y, Coppola J et al. 2022. Single-molecule characterization of subtype-specific β1 integrin mechanics. Nat. Commun. 13:17471
    [Google Scholar]
  69. Kadler KE, Baldock C, Bella J, Boot-Handford RP. 2007. Collagens at a glance. J. Cell Sci. 120:121955–58
    [Google Scholar]
  70. Kang SH, Kramer JM. 2000. Nidogen is nonessential and not required for normal type IV collagen localization in Caenorhabditis elegans. Mol. Biol. Cell 11:113911–23
    [Google Scholar]
  71. Karkali K, Tiwari P, Singh A, Tlili S, Jorba I et al. 2022. Condensation of the Drosophila nerve cord is oscillatory and depends on coordinated mechanical interactions. Dev. Cell 57:7867–82.e5
    [Google Scholar]
  72. Katsamba P, Carroll K, Ahlsen G, Bahna F, Vendome J et al. 2009. Linking molecular affinity and cellular specificity in cadherin-mediated adhesion. PNAS 106:2811594–99
    [Google Scholar]
  73. Kaya-Okur HS, Wu SJ, Codomo CA, Pledger ES, Bryson TD et al. 2019. CUT&Tag for efficient epigenomic profiling of small samples and single cells. Nat. Commun. 10:11930
    [Google Scholar]
  74. Kechagia JZ, Ivaska J, Roca-Cusachs P. 2019. Integrins as biomechanical sensors of the microenvironment. Nat. Rev. Mol. Cell Biol. 20:8457–73
    [Google Scholar]
  75. Keegstra K. 2010. Plant cell walls. Plant Physiol. 154:2483–86
    [Google Scholar]
  76. Keeley DP, Hastie E, Jayadev R, Kelley LC, Chi Q et al. 2020. Comprehensive endogenous tagging of basement membrane components reveals dynamic movement within the matrix scaffolding. Dev. Cell 54:160–74.e7
    [Google Scholar]
  77. Kelwick R, Desanlis I, Wheeler GN, Edwards DR. 2015. The ADAMTS (A Disintegrin and Metalloproteinase with Thrombospondin motifs) family. Genome Biol. 16:1113
    [Google Scholar]
  78. Kerosuo L, Bronner-Fraser M. 2012. What is bad in cancer is good in the embryo: importance of EMT in neural crest development. Semin. Cell Dev. Biol. 23:3320–32
    [Google Scholar]
  79. Khoshnoodi J, Pedchenko V, Hudson BG. 2008. Mammalian collagen IV. Microsc. Res. Tech. 71:5357–70
    [Google Scholar]
  80. Kim HY, Pang M-F, Varner VD, Kojima L, Miller E et al. 2015. Localized smooth muscle differentiation is essential for epithelial bifurcation during branching morphogenesis of the mammalian lung. Dev. Cell 34:6719–26
    [Google Scholar]
  81. Kong F, García AJ, Mould AP, Humphries MJ, Zhu C. 2009. Demonstration of catch bonds between an integrin and its ligand. J. Cell Biol. 185:71275–84
    [Google Scholar]
  82. Kowalczyk AP, Green KJ. 2013. Structure, function and regulation of desmosomes. Prog. Mol. Biol. Transl. Sci. 116:95–118
    [Google Scholar]
  83. 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. 10:4429–36
    [Google Scholar]
  84. Ku H-Y, Harris LK, Bilder D. 2023. Specialized cells that sense tissue mechanics to regulate Drosophila morphogenesis. Dev. Cell 58:3211–23.e5
    [Google Scholar]
  85. Kyprianou C, Christodoulou N, Hamilton RS, Nahaboo W, Boomgaard DS et al. 2020. Basement membrane remodelling regulates mouse embryogenesis. Nature 582:7811253–58
    [Google Scholar]
  86. Leitinger B. 2014. Discoidin domain receptor functions in physiological and pathological conditions. International Review of Cell and Molecular Biology, Vol. 310 KW Jeon 39–87. Cambridge, MA: Academic
    [Google Scholar]
  87. Li DY, Brooke B, Davis EC, Mecham RP, Sorensen LK et al. 1998. Elastin is an essential determinant of arterial morphogenesis. Nature 393:6682276–80
    [Google Scholar]
  88. Liu S, Thomas SM, Woodside DG, Rose DM, Kiosses WB et al. 1999. Binding of paxillin to α4 integrins modifies integrin-dependent biological responses. Nature 402:6762676–81
    [Google Scholar]
  89. Lorand L, Graham RM. 2003. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4:2140–56
    [Google Scholar]
  90. Lovegrove HE, Bergstralh DT, St Johnston D. 2019. The role of integrins in Drosophila egg chamber morphogenesis. Development 146:23dev182774
    [Google Scholar]
  91. Lu J, Doyle AD, Shinsato Y, Wang S, Bodendorfer MA et al. 2020. Basement membrane regulates fibronectin organization using sliding focal adhesions driven by a contractile winch. Dev. Cell 52:5631–46.e4
    [Google Scholar]
  92. Lucero HA, Kagan HM. 2006. Lysyl oxidase: an oxidative enzyme and effector of cell function. Cell. Mol. Life Sci. 63:192304–16
    [Google Scholar]
  93. Luo B-H, Carman CV, Springer TA. 2007. Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25:619–47
    [Google Scholar]
  94. 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 338:6104253–56
    [Google Scholar]
  95. Malin-Mayor C, Hirsch P, Guignard L, McDole K, Wan Y et al. 2023. Automated reconstruction of whole-embryo cell lineages by learning from sparse annotations. Nat. Biotechnol. 41:144–49
    [Google Scholar]
  96. Martin AC. 2020. The physical mechanisms of Drosophila gastrulation: mesoderm and endoderm invagination. Genetics 214:3543–60
    [Google Scholar]
  97. Maruthamuthu V, Sabass B, Schwarz US, Gardel ML. 2011. Cell-ECM traction force modulates endogenous tension at cell-cell contacts. PNAS 108:124708–13
    [Google Scholar]
  98. McDole K, Guignard L, Amat F, Berger A, Malandain G et al. 2018. In toto imaging and reconstruction of post-implantation mouse development at the single-cell level. Cell 175:3859–76.e33
    [Google Scholar]
  99. Meng W, Mushika Y, Ichii T, Takeichi M. 2008. Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts. Cell 135:5948–59
    [Google Scholar]
  100. Miner JH, Li C, Mudd JL, Go G, Sutherland AE. 2004. Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation. Development 131:102247–56
    [Google Scholar]
  101. Mitchel JA, Das A, O'Sullivan MJ, Stancil IT, DeCamp SJ et al. 2020. In primary airway epithelial cells, the unjamming transition is distinct from the epithelial-to-mesenchymal transition. Nat. Commun. 11:15053
    [Google Scholar]
  102. 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 561:7723401–5
    [Google Scholar]
  103. Monster JL, Donker L, Vliem MJ, Win Z, Matthews HK et al. 2021. An asymmetric junctional mechanoresponse coordinates mitotic rounding with epithelial integrity. J. Cell Biol. 220:5e202001042
    [Google Scholar]
  104. Moore CJ, Winder SJ. 2010. Dystroglycan versatility in cell adhesion: a tale of multiple motifs. Cell Commun. Signal. 8:13
    [Google Scholar]
  105. Moscona A. 1957. The development in vitro of chimeric aggregates of dissociated embryonic chick and mouse cells. PNAS 43:1184–94
    [Google Scholar]
  106. Muiznieks LD, Weiss AS, Keeley FW. 2010. Structural disorder and dynamics of elastin. Biochem. Cell Biol. 88:2239–50
    [Google Scholar]
  107. Munjal A, Hannezo E, Tsai TY-C, Mitchison TJ, Megason SG. 2021. Extracellular hyaluronate pressure shaped by cellular tethers drives tissue morphogenesis. Cell 184:266313–25.e18
    [Google Scholar]
  108. Nagase H, Visse R, Murphy G. 2006. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 69:3562–73
    [Google Scholar]
  109. Nerger BA, Jaslove JM, Elashal HE, Mao S, Košmrlj A et al. 2021. Local accumulation of extracellular matrix regulates global morphogenetic patterning in the developing mammary gland. Curr. Biol. 31:91903–17.e6
    [Google Scholar]
  110. Nikolopoulou E, Galea GL, Rolo A, Greene NDE, Copp AJ. 2017. Neural tube closure: cellular, molecular and biomechanical mechanisms. Development 144:4552–66
    [Google Scholar]
  111. Oblander SA, Zhou Z, Gálvez BG, Starcher B, Shannon JM et al. 2005. Distinctive functions of membrane type 1 matrix-metalloprotease (MT1-MMP or MMP-14) in lung and submandibular gland development are independent of its role in pro-MMP-2 activation. Dev. Biol. 277:1255–69
    [Google Scholar]
  112. Özbek S, Balasubramanian PG, Chiquet-Ehrismann R, Tucker RP, Adams JC. 2010. The evolution of extracellular matrix. Mol. Biol. Cell 21:244300–5
    [Google Scholar]
  113. Palmquist KH, Tiemann SF, Ezzeddine FL, Yang S, Pfeifer CR et al. 2022. Reciprocal cell-ECM dynamics generate supracellular fluidity underlying spontaneous follicle patterning. Cell 185:111960–73.e11
    [Google Scholar]
  114. Pankov R, Cukierman E, Katz B-Z, Matsumoto K, Lin DC et al. 2000. Integrin dynamics and matrix assembly: tensin-dependent translocation of α5β1 integrins promotes early fibronectin fibrillogenesis. J. Cell Biol. 148:51075–90
    [Google Scholar]
  115. Pankov R, Yamada KM. 2002. Fibronectin at a glance. J. Cell Sci. 115:203861–63
    [Google Scholar]
  116. Pastor-Pareja JC, Xu T. 2011. Shaping cells and organs in Drosophila by opposing roles of fat body-secreted collagen IV and perlecan. Dev. Cell 21:2245–56
    [Google Scholar]
  117. 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. 17:8083049
    [Google Scholar]
  118. Petridou NI, Grigolon S, Salbreux G, Hannezo E, Heisenberg C-P. 2019. Fluidization-mediated tissue spreading by mitotic cell rounding and non-canonical Wnt signalling. Nat. Cell Biol. 21:2169–78
    [Google Scholar]
  119. Petridou NI, Heisenberg C-P. 2019. Tissue rheology in embryonic organization. EMBO J. 38:20e102497
    [Google Scholar]
  120. Pöschl E, Schlötzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U. 2004. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131:71619–28
    [Google Scholar]
  121. Pozzi A, Yurchenco PD, Iozzo RV. 2017. The nature and biology of basement membranes. Matrix Biol. 57–58:1–11
    [Google Scholar]
  122. Primakoff P, Myles DG. 2000. The ADAM gene family: surface proteins with adhesion and protease activity. Trends Genet. 16:283–87
    [Google Scholar]
  123. Rakshit S, Zhang Y, Manibog K, Shafraz O, Sivasankar S. 2012. Ideal, catch, and slip bonds in cadherin adhesion. PNAS 109:4618815–20
    [Google Scholar]
  124. Ramirez F, Sakai LY. 2010. Biogenesis and function of fibrillin assemblies. Cell Tissue Res. 339:171–82
    [Google Scholar]
  125. Ramos-Lewis W, Page-McCaw A. 2019. Basement membrane mechanics shape development: lessons from the fly. Matrix Biol. 75–76:72–81
    [Google Scholar]
  126. Randles MJ, Humphries MJ, Lennon R. 2017. Proteomic definitions of basement membrane composition in health and disease. Matrix Biol. 57–58:12–28
    [Google Scholar]
  127. Raspopovic J, Marcon L, Russo L, Sharpe J. 2014. Digit patterning is controlled by a Bmp-Sox9-Wnt Turing network modulated by morphogen gradients. Science 345:6196566–70
    [Google Scholar]
  128. Rauscher S, Pomès R. 2017. The liquid structure of elastin. eLife 6:e26526
    [Google Scholar]
  129. Romani P, Valcarcel-Jimenez L, Frezza C, Dupont S. 2021. Crosstalk between mechanotransduction and metabolism. Nat. Rev. Mol. Cell Biol. 22:122–38
    [Google Scholar]
  130. Sakai T, Larsen M, Yamada KM. 2003. Fibronectin requirement in branching morphogenesis. Nature 423:6942876–81
    [Google Scholar]
  131. Savin T, Kurpios NA, Shyer AE, Florescu P, Liang H et al. 2011. On the growth and form of the gut. Nature 476:735857–62
    [Google Scholar]
  132. Schaefer L, Schaefer RM. 2009. Proteoglycans: from structural compounds to signaling molecules. Cell Tissue Res. 339:1237–46
    [Google Scholar]
  133. 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. 2:142–56
    [Google Scholar]
  134. Scoones JC, Hiscock TW. 2020. A dot-stripe Turing model of joint patterning in the tetrapod limb. Development 147:8dev183699
    [Google Scholar]
  135. Scott JE. 2003. Elasticity in extracellular matrix ‘shape modules’ of tendon, cartilage, etc. A sliding proteoglycan-filament model. J. Physiol. 553:2335–43
    [Google Scholar]
  136. Sekiguchi R, Mehlferber MM, Matsumoto K, Wang S. 2023. Efficient gene knockout in salivary gland epithelial explant cultures. J. Dent. Res. 102:2197–206
    [Google Scholar]
  137. Shih HP, Panlasigui D, Cirulli V, Sander M. 2016. ECM signaling regulates collective cellular dynamics to control pancreas branching morphogenesis. Cell Rep. 14:2169–79
    [Google Scholar]
  138. Shoulders MD, Raines RT. 2009. Collagen structure and stability. Annu. Rev. Biochem. 78:929–58
    [Google Scholar]
  139. Shyer AE, Tallinen T, Nerurkar NL, Wei Z, Gil ES et al. 2013. Villification: how the gut gets its villi. Science 342:6155212–18
    [Google Scholar]
  140. Sivasankar S, Brieher W, Lavrik N, Gumbiner B, Leckband D. 1999. Direct molecular force measurements of multiple adhesive interactions between cadherin ectodomains. PNAS 96:2111820–24
    [Google Scholar]
  141. Skene PJ, Henikoff S. 2017. An efficient targeted nuclease strategy for high-resolution mapping of DNA binding sites. eLife 6:e21856
    [Google Scholar]
  142. Smyth N, Vatansever HS, Murray P, Meyer M, Frie C et al. 1999. Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J. Cell Biol. 144:1151–60
    [Google Scholar]
  143. Soares da Costa D, Reis RL, Pashkuleva I. 2017. Sulfation of glycosaminoglycans and its implications in human health and disorders. Annu. Rev. Biomed. Eng. 19:1–26
    [Google Scholar]
  144. Spurlin JW, Siedlik MJ, Nerger BA, Pang M-F, Jayaraman S et al. 2019. Mesenchymal proteases and tissue fluidity remodel the extracellular matrix during airway epithelial branching in the embryonic avian lung. Development 146:16dev175257
    [Google Scholar]
  145. Steinberg MS. 1963. Reconstruction of tissues by dissociated cells. Science 141:3579401–8
    [Google Scholar]
  146. Steinberg MS, Takeichi M. 1994. Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. PNAS 91:1206–9
    [Google Scholar]
  147. Sternlicht MD, Werb Z. 2001. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 17:463–516
    [Google Scholar]
  148. Stevens AJ, Harris AR, Gerdts J, Kim KH, Trentesaux C et al. 2023. Programming multicellular assembly with synthetic cell adhesion molecules. Nature 614:7946144–52
    [Google Scholar]
  149. Stringer C, Wang T, Michaelos M, Pachitariu M. 2021. Cellpose: a generalist algorithm for cellular segmentation. Nat. Methods 18:1100–6
    [Google Scholar]
  150. Takeichi M. 2014. Dynamic contacts: rearranging adherens junctions to drive epithelial remodelling. Nat. Rev. Mol. Cell Biol. 15:6397–410
    [Google Scholar]
  151. Tallinen T, Chung JY, Rousseau F, Girard N, Lefèvre J, Mahadevan L. 2016. On the growth and form of cortical convolutions. Nat. Phys. 12:6588–93
    [Google Scholar]
  152. Tambe DT, Fredberg JJ. 2015. And I hope you like jamming too. New J. Phys. 17:9091001
    [Google Scholar]
  153. Tanay A, Regev A. 2017. Scaling single-cell genomics from phenomenology to mechanism. Nature 541:7637331–38
    [Google Scholar]
  154. Thomson J, Singh M, Eckersley A, Cain SA, Sherratt MJ, Baldock C. 2019. Fibrillin microfibrils and elastic fibre proteins: functional interactions and extracellular regulation of growth factors. Semin. Cell Dev. Biol. 89:109–17
    [Google Scholar]
  155. Tsai TY-C, Garner RM, Megason SG. 2022. Adhesion-based self-organization in tissue patterning. Annu. Rev. Cell Dev. Biol. 38:349–74
    [Google Scholar]
  156. 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 370:6512113–16
    [Google Scholar]
  157. Tsukita S, Tanaka H, Tamura A. 2019. The claudins: from tight junctions to biological systems. Trends Biochem. Sci. 44:2141–52
    [Google Scholar]
  158. Turing AM. 1952. The chemical basis of morphogenesis. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 237:64137–72
    [Google Scholar]
  159. Vanacore R, Ham A-JL, Voehler M, Sanders CR, Conrads TP et al. 2009. A sulfilimine bond identified in collagen IV. Science 325:59451230–34
    [Google Scholar]
  160. Vorselen D, Wang Y, de Jesus MM, Shah PK, Footer MJ et al. 2020. Microparticle traction force microscopy reveals subcellular force exertion patterns in immune cell-target interactions. Nat. Commun. 11:120
    [Google Scholar]
  161. Wang JY, Doudna JA. 2023. CRISPR technology: a decade of genome editing is only the beginning. Science 379:6629eadd8643
    [Google Scholar]
  162. Wang S, Matsumoto K, Lish SR, Cartagena-Rivera AX, Yamada KM. 2021a. Budding epithelial morphogenesis driven by cell-matrix versus cell-cell adhesion. Cell 184:143702–16.e30
    [Google Scholar]
  163. Wang X, Ha T. 2013. Defining single molecular forces required to activate integrin and notch signaling. Science 340:6135991–94
    [Google Scholar]
  164. Wang Y, Zhang C, Yang W, Shao S, Xu X et al. 2021b. LIMD1 phase separation contributes to cellular mechanics and durotaxis by regulating focal adhesion dynamics in response to force. Dev. Cell 56:91313–25.e7
    [Google Scholar]
  165. Watanabe H, Kimata K, Line S, Strong D, Gao L et al. 1994. Mouse cartilage matrix deficiency (cmd) caused by a 7 bp deletion in the aggrecan gene. Nat. Genet. 7:2154–57
    [Google Scholar]
  166. Wendel DP, Taylor DG, Albertine KH, Keating MT, Li DY. 2000. Impaired distal airway development in mice lacking elastin. Am. J. Respir. Cell Mol. Biol. 23:3320–26
    [Google Scholar]
  167. Wittmann T, Dema A, van Haren J. 2020. Lights, cytoskeleton, action: optogenetic control of cell dynamics. Curr. Opin. Cell Biol. 66:1–10
    [Google Scholar]
  168. Wu T, Yoon H, Xiong Y, Dixon-Clarke SE, Nowak RP, Fischer ES. 2020. Targeted protein degradation as a powerful research tool in basic biology and drug target discovery. Nat. Struct. Mol. Biol. 27:7605–14
    [Google Scholar]
  169. Xu X-P, Pokutta S, Torres M, Swift MF, Hanein D et al. 2020. Structural basis of αE-catenin-F-actin catch bond behavior. eLife 9:e60878
    [Google Scholar]
  170. Yamada S, Nelson WJ. 2007. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J. Cell Biol. 178:3517–27
    [Google Scholar]
  171. Yamada S, Sugahara K, Özbek S. 2011. Evolution of glycosaminoglycans. Commun. Integr. Biol. 4:2150–58
    [Google Scholar]
  172. Yavitt FM, Kirkpatrick BE, Blatchley MR, Speckl KF, Mohagheghian E et al. 2023. In situ modulation of intestinal organoid epithelial curvature through photoinduced viscoelasticity directs crypt morphogenesis. Sci. Adv. 9:3eadd5668
    [Google Scholar]
  173. Youssef J, Nurse AK, Freund LB, Morgan JR. 2011. Quantification of the forces driving self-assembly of three-dimensional microtissues. PNAS 108:176993–98
    [Google Scholar]
  174. Yurchenco PD. 2011. Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb. Perspect. Biol. 3:2a004911
    [Google Scholar]
  175. Yurchenco PD, Ruben GC. 1987. Basement membrane structure in situ: evidence for lateral associations in the type IV collagen network. J. Cell Biol. 105:62559–68
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-020223-031019
Loading
/content/journals/10.1146/annurev-cellbio-020223-031019
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