1932

Abstract

During organismal development, organs and systems are built following a genetic blueprint that produces structures capable of performing specific physiological functions. Interestingly, we have learned that the physiological activities of developing tissues also contribute to their own morphogenesis. Specifically, physiological activities such as fluid secretion and cell contractility generate hydrostatic pressure that can act as a morphogenetic force. Here, we first review the role of hydrostatic pressure in tube formation during animal development and discuss mathematical models of lumen formation. We then illustrate specific roles of the notochord as a hydrostatic scaffold in anterior-posterior axis development in chordates. Finally, we cover some examples of how fluid flows influence morphogenetic processes in other developmental contexts. Understanding how fluid forces act during development will be key for uncovering the self-organizing principles that control morphogenesis.

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2022-10-06
2024-04-19
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Literature Cited

  1. Abbas L, Whitfield TT. 2009. Nkcc1 (Slc12a2) is required for the regulation of endolymph volume in the otic vesicle and swim bladder volume in the zebrafish larva. Development 136:2837–48
    [Google Scholar]
  2. Adams DS, Keller R, Koehl MA. 1990. The mechanics of notochord elongation, straightening and stiffening in the embryo of Xenopus laevis. Development 110:115–30
    [Google Scholar]
  3. Alvers AL, Ryan S, Scherz PJ, Huisken J, Bagnat M. 2014. Single continuous lumen formation in the zebrafish gut is mediated by smoothened-dependent tissue remodeling. Development 141:1110–19
    [Google Scholar]
  4. Bagnat M, Cheung ID, Mostov KE, Stainier DY. 2007. Genetic control of single lumen formation in the zebrafish gut. Nat. Cell Biol. 9:954–60
    [Google Scholar]
  5. Bagnat M, Gray RS 2020. Development of a straight vertebrate body axis. Development 147:dev175794
    [Google Scholar]
  6. Bagwell J, Norman J, Ellis K, Peskin B, Hwang J et al. 2020. Notochord vacuoles absorb compressive bone growth during zebrafish spine formation. eLife 9:e51221
    [Google Scholar]
  7. Baldan A. 2002. Progress in Ostwald ripening theories and their applications to nickel-base superalloys Part I: Ostwald ripening theories. J. Mater. Sci. 37:2171–202
    [Google Scholar]
  8. Behringer RP, Chakraborty B. 2019. The physics of jamming for granular materials: a review. Rep. Prog. Phys. 82:012601
    [Google Scholar]
  9. Caille N, Thoumine O, Tardy Y, Meister JJ. 2002. Contribution of the nucleus to the mechanical properties of endothelial cells. J. Biomech. 35:177–87
    [Google Scholar]
  10. Caviglia S, Brankatschk M, Fischer EJ, Eaton S, Luschnig S. 2016. Staccato/Unc-13-4 controls secretory lysosome-mediated lumen fusion during epithelial tube anastomosis. Nat. Cell Biol. 18:727–39
    [Google Scholar]
  11. Chan CJ, Costanzo M, Ruiz-Herrero T, Monke G, Petrie RJ et al. 2019. Hydraulic control of mammalian embryo size and cell fate. Nature 571:112–16
    [Google Scholar]
  12. Chan CJ, Hiiragi T. 2020. Integration of luminal pressure and signalling in tissue self-organization. Development 147:dev181297
    [Google Scholar]
  13. Chartier NT, Mukherjee A, Pfanzelter J, Fürthauer S, Larson BT et al. 2021. A hydraulic instability drives the cell death decision in the nematode germline. Nat. Phys. 17:920–25
    [Google Scholar]
  14. Colegio OR, Van Itallie CM, McCrea HJ, Rahner C, Anderson JM. 2002. Claudins create charge-selective channels in the paracellular pathway between epithelial cells. Am. J. Physiol. Cell Physiol. 283:C142–47
    [Google Scholar]
  15. Dale RM, Topczewski J. 2011. Identification of an evolutionarily conserved regulatory element of the zebrafish col2a1a gene. Dev. Biol. 357:518–31
    [Google Scholar]
  16. Dasgupta A, Merkel M, Clark MJ, Jacob AE, Dawson JE et al. 2018. Cell volume changes contribute to epithelial morphogenesis in zebrafish Kupffer's vesicle. eLife 7:e30963
    [Google Scholar]
  17. Dasgupta S, Gupta K, Zhang Y, Viasnoff V, Prost J. 2018. Physics of lumen growth. PNAS 115:E4751–57
    [Google Scholar]
  18. Deneke VE, Puliafito A, Krueger D, Narla AV, De Simone A et al. 2019. Self-organized nuclear positioning synchronizes the cell cycle in Drosophila embryos. Cell 177:925–41.e17
    [Google Scholar]
  19. Deng W, Nies F, Feuer A, Bocina I, Oliver D, Jiang D. 2013. Anion translocation through an Slc26 transporter mediates lumen expansion during tubulogenesis. PNAS 110:14972–77
    [Google Scholar]
  20. Desmond ME, Jacobson AG. 1977. Embryonic brain enlargement requires cerebrospinal fluid pressure. Dev. Biol. 57:188–98
    [Google Scholar]
  21. Devine WP, Lubarsky B, Shaw K, Luschnig S, Messina L, Krasnow MA. 2005. Requirement for chitin biosynthesis in epithelial tube morphogenesis. PNAS 102:17014–19
    [Google Scholar]
  22. Dong B, Deng W, Jiang D. 2011. Distinct cytoskeleton populations and extensive crosstalk control Ciona notochord tubulogenesis. Development 138:1631–41
    [Google Scholar]
  23. Dong B, Kakihara K, Otani T, Wada H, Hayashi S. 2013. Rab9 and retromer regulate retrograde trafficking of luminal protein required for epithelial tube length control. Nat. Commun. 4:1358
    [Google Scholar]
  24. Dong B, Miao G, Hayashi S. 2014. A fat body-derived apical extracellular matrix enzyme is transported to the tracheal lumen and is required for tube morphogenesis in Drosophila. Development 141:4104–9
    [Google Scholar]
  25. Dray N, Lawton A, Nandi A, Julich D, Emonet T, Holley SA. 2013. Cell-fibronectin interactions propel vertebrate trunk elongation via tissue mechanics. Curr. Biol. 23:1335–41
    [Google Scholar]
  26. Duclut C, Prost J, Jülicher F. 2021. Hydraulic and electric control of cell spheroids. PNAS 118:e2021972118
    [Google Scholar]
  27. Duclut C, Sarkar N, Prost J, Jülicher F. 2019. Fluid pumping and active flexoelectricity can promote lumen nucleation in cell assemblies. PNAS 116:19264–73
    [Google Scholar]
  28. Dumortier JG, Le Verge-Serandour M, Tortorelli AF, Mielke A, de Plater L et al. 2019. Hydraulic fracturing and active coarsening position the lumen of the mouse blastocyst. Science 365:465–68
    [Google Scholar]
  29. 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]
  30. Ellis K, Bagwell J, Bagnat M. 2013a. Notochord vacuoles are lysosome-related organelles that function in axis and spine morphogenesis. J. Cell Biol. 200:667–79
    [Google Scholar]
  31. Ellis K, Hoffman BD, Bagnat M. 2013b. The vacuole within: how cellular organization dictates notochord function. Bioarchitecture 3:64–68
    [Google Scholar]
  32. Flecknoe S, Harding R, Maritz G, Hooper SB. 2000. Increased lung expansion alters the proportions of type I and type II alveolar epithelial cells in fetal sheep. Am. J. Physiol. Lung Cell. Mol. Physiol. 278:L1180–85
    [Google Scholar]
  33. Forgacs G, Foty RA, Shafrir Y, Steinberg MS. 1998. Viscoelastic properties of living embryonic tissues: a quantitative study. Biophys. J. 74:2227–34
    [Google Scholar]
  34. Forster D, Armbruster K, Luschnig S. 2010. Sec24-dependent secretion drives cell-autonomous expansion of tracheal tubes in Drosophila. Curr. Biol. 20:62–68
    [Google Scholar]
  35. Fox RM, Hanlon CD, Andrew DJ. 2010. The CrebA/Creb3-like transcription factors are major and direct regulators of secretory capacity. J. Cell Biol. 191:479–92
    [Google Scholar]
  36. Furuse M, Furuse K, Sasaki H, Tsukita S. 2001. Conversion of zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin-Darby canine kidney I cells. J. Cell Biol. 153:263–72
    [Google Scholar]
  37. Gad A, Callender DL, Killeen E, Hudak J, Dlugosz MA et al. 2009. Transient in utero disruption of cystic fibrosis transmembrane conductance regulator causes phenotypic changes in alveolar type II cells in adult rats. BMC Cell Biol. 10:24
    [Google Scholar]
  38. Grieder NC, Caussinus E, Parker DS, Cadigan K, Affolter M, Luschnig S. 2008. γCOP is required for apical protein secretion and epithelial morphogenesis in Drosophila melanogaster. PLOS ONE 3:e3241
    [Google Scholar]
  39. Gutzman JH, Sive H. 2010. Epithelial relaxation mediated by the myosin phosphatase regulator Mypt1 is required for brain ventricle lumen expansion and hindbrain morphogenesis. Development 137:795–804
    [Google Scholar]
  40. Harding R, Hooper SB. 1996. Regulation of lung expansion and lung growth before birth. J. Appl. Physiol. 81:209–24
    [Google Scholar]
  41. Herwig L, Blum Y, Krudewig A, Ellertsdottir E, Lenard A et al. 2011. Distinct cellular mechanisms of blood vessel fusion in the zebrafish embryo. Curr. Biol. 21:1942–48
    [Google Scholar]
  42. Hoijman E, Rubbini D, Colombelli J, Alsina B. 2015. Mitotic cell rounding and epithelial thinning regulate lumen growth and shape. Nat. Commun. 6:7355
    [Google Scholar]
  43. Husain N, Pellikka M, Hong H, Klimentova T, Choe K-M et al. 2006. The agrin/perlecan-related protein eyes shut is essential for epithelial lumen formation in the Drosophila retina. Dev. Cell 11:483–93
    [Google Scholar]
  44. Imran Alsous J, Romeo N, Jackson JA, Mason FM, Dunkel J, Martin AC. 2021. Dynamics of hydraulic and contractile wave-mediated fluid transport during Drosophila oogenesis. PNAS 118:e2019749118
    [Google Scholar]
  45. Irvine KD, Shraiman BI. 2017. Mechanical control of growth: ideas, facts and challenges. Development 144:4238–48
    [Google Scholar]
  46. Jaslove JM, Goodwin K, Sundarakrishnan A, Spurlin JW III, Mao S et al. 2022. Transmural pressure signals through retinoic acid to regulate lung branching. Development 149:dev199726
    [Google Scholar]
  47. Jaslove JM, Nelson CM. 2018. Smooth muscle: a stiff sculptor of epithelial shapes. Philos. Trans. R. Soc. B 373:20170318
    [Google Scholar]
  48. Jazwinska A, Ribeiro C, Affolter M. 2003. Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein. Nat. Cell Biol. 5:895–901
    [Google Scholar]
  49. Jenkins VK, Timmons AK, McCall K. 2013. Diversity of cell death pathways: insight from the fly ovary. Trends Cell Biol. 23:567–74
    [Google Scholar]
  50. Jiang D, Smith WC. 2007. Ascidian notochord morphogenesis. Dev. Dyn. 236:1748–57
    [Google Scholar]
  51. Karzbrun E, Khankhel AH, Megale HC, Glasauer SMK, Wyle Y et al. 2021. Human neural tube morphogenesis in vitro by geometric constraints. Nature 599:268–72
    [Google Scholar]
  52. Khan LA, Zhang H, Abraham N, Sun L, Fleming JT et al. 2013. Intracellular lumen extension requires ERM-1-dependent apical membrane expansion and AQP-8-mediated flux. Nat. Cell Biol. 15:143–56
    [Google Scholar]
  53. Kiefer SW, Morrow NS, Metzler CW. 1988. Alcohol aversion generalization in rats: specific disruption of taste and odor cues with gustatory neocortex or olfactory bulb ablations. Behav. Neurosci. 102:733–39
    [Google Scholar]
  54. Kolotuev I, Hyenne V, Schwab Y, Rodriguez D, Labouesse M. 2013. A pathway for unicellular tube extension depending on the lymphatic vessel determinant Prox1 and on osmoregulation. Nat. Cell Biol. 15:157–68
    [Google Scholar]
  55. Kovach IS. 1995. The importance of polysaccharide configurational entropy in determining the osmotic swelling pressure of concentrated proteoglycan solution and the bulk compressive modulus of articular cartilage. Biophys. Chem. 53:181–87
    [Google Scholar]
  56. Larsen EH, Sorensen JN. 2020. Stationary and nonstationary ion and water flux interactions in kidney proximal tubule: mathematical analysis of isosmotic transport by a minimalistic model. Rev. Physiol. Biochem. Pharmacol. 177:101–47
    [Google Scholar]
  57. Le Verge-Serandour M, Turlier H 2021. A hydro-osmotic coarsening theory of biological cavity formation. PLOS Comput. Biol. 17:e1009333
    [Google Scholar]
  58. Leung CF, Webb SE, Miller AL. 2000. On the mechanism of ooplasmic segregation in single-cell zebrafish embryos. Dev. Growth Differ. 42:29–40
    [Google Scholar]
  59. Lomakin AJ, Cattin CJ, Cuvelier D, Alraies Z, Molina M et al. 2020. The nucleus acts as a ruler tailoring cell responses to spatial constraints. Science 370:eaba2894
    [Google Scholar]
  60. Lowery LA, Sive H. 2005. Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie oko and snakehead/atp1a1a.1 gene products. Development 132:2057–67
    [Google Scholar]
  61. Lu W, Lakonishok M, Serpinskaya AS, Gelfand VI 2022. A novel mechanism of bulk cytoplasmic transport by cortical dynein in Drosophila ovary. eLife 11:e75538
    [Google Scholar]
  62. MacAulay N. 2021. Molecular mechanisms of brain water transport. Nat. Rev. Neurosci. 22:326–44
    [Google Scholar]
  63. Maki K, Nava MM, Villeneuve C, Chang M, Furukawa KS et al. 2021. Hydrostatic pressure prevents chondrocyte differentiation through heterochromatin remodeling. J. Cell Sci. 134:jcs247643
    [Google Scholar]
  64. McLaren SBP, Steventon BJ 2021. Anterior expansion and posterior addition to the notochord mechanically coordinate zebrafish embryo axis elongation. Development 148:dev199459
    [Google Scholar]
  65. Mellman K, Huisken J, Dinsmore C, Hoppe C, Stainier DY. 2012. Fibrillin-2b regulates endocardial morphogenesis in zebrafish. Dev. Biol. 372:111–19
    [Google Scholar]
  66. Mitchell NP, Cislo D, Shankar S, Lin Y, Shraiman BI, Streichan SJ. 2021. Visceral organ morphogenesis via calcium-patterned muscle contractions. bioRxiv 2021.11.07.467658. https://doi.org/10.1101/2021.11.07.467658
    [Crossref]
  67. Mitchison TJ, Charras GT, Mahadevan L. 2008. Implications of a poroelastic cytoplasm for the dynamics of animal cell shape. Semin. Cell Dev. Biol. 19:215–23
    [Google Scholar]
  68. Mittasch M, Gross P, Nestler M, Fritsch AW, Iserman C et al. 2018. Non-invasive perturbations of intracellular flow reveal physical principles of cell organization. Nat. Cell Biol. 20:344–51
    [Google Scholar]
  69. Mosaliganti KR, Swinburne IA, Chan CU, Obholzer ND, Green AA et al. 2019. Size control of the inner ear via hydraulic feedback. eLife 8:e39596
    [Google Scholar]
  70. Munjal A, Hannezo E, Tsai TY, Mitchison TJ, Megason SG. 2021. Extracellular hyaluronate pressure shaped by cellular tethers drives tissue morphogenesis. Cell 184:6313–25.e18
    [Google Scholar]
  71. Nardo L, Maritz G, Harding R, Hooper SB. 2000. Changes in lung structure and cellular division induced by tracheal obstruction in fetal sheep. Exp. Lung Res. 26:105–19
    [Google Scholar]
  72. Navis A, Bagnat M. 2015. Developing pressures: fluid forces driving morphogenesis. Curr. Opin. Genet. Dev. 32:24–30
    [Google Scholar]
  73. Navis A, Marjoram L, Bagnat M. 2013. Cftr controls lumen expansion and function of Kupffer's vesicle in zebrafish. Development 140:1703–12
    [Google Scholar]
  74. Nedvetsky PI, Emmerson E, Finley JK, Ettinger A, Cruz-Pacheco N et al. 2014. Parasympathetic innervation regulates tubulogenesis in the developing salivary gland. Dev. Cell 30:449–62
    [Google Scholar]
  75. Nelson CM, Gleghorn JP, Pang MF, Jaslove JM, Goodwin K et al. 2017. Microfluidic chest cavities reveal that transmural pressure controls the rate of lung development. Development 144:4328–35
    [Google Scholar]
  76. Nogawa H, Hasegawa Y. 2002. Sucrose stimulates branching morphogenesis of embryonic mouse lung in vitro: a problem of osmotic balance between lumen fluid and culture medium. Dev. Growth Differ. 44:383–90
    [Google Scholar]
  77. Norman J, Sorrell EL, Hu Y, Siripurapu V, Garcia J et al. 2018. Tissue self-organization underlies morphogenesis of the notochord. Philos. Trans. R. Soc. B 373:20170320
    [Google Scholar]
  78. Norotte C, Marga F, Neagu A, Kosztin I, Forgacs G. 2008. Experimental evaluation of apparent tissue surface tension based on the exact solution of the Laplace equation. Europhys. Lett 81:46003
    [Google Scholar]
  79. Palmer MA, Nelson CM. 2020. Fusion of airways during avian lung development constitutes a novel mechanism for the formation of continuous lumena in multicellular epithelia. Dev. Dyn. 249:1318–33
    [Google Scholar]
  80. Palmer MA, Nerger BA, Goodwin K, Sudhakar A, Lemke SB et al. 2021. Stress ball morphogenesis: how the lizard builds its lung. Sci. Adv. 7:eabk0161
    [Google Scholar]
  81. Paolini A, Fontana F, Pham VC, Rodel CJ, Abdelilah-Seyfried S. 2021. Mechanosensitive Notch-Dll4 and Klf2-Wnt9 signaling pathways intersect in guiding valvulogenesis in zebrafish. Cell Rep. 37:109782
    [Google Scholar]
  82. Peal DS, Burns CG, Macrae CA, Milan D. 2009. Chondroitin sulfate expression is required for cardiac atrioventricular canal formation. Dev. Dyn. 238:3103–10
    [Google Scholar]
  83. Peeters EA, Oomens CW, Bouten CV, Bader DL, Baaijens FP. 2005. Viscoelastic properties of single attached cells under compression. J. Biomech. Eng. 127:237–43
    [Google Scholar]
  84. Pepling ME, de Cuevas M, Spradling AC. 1999. Germline cysts: a conserved phase of germ cell development?. Trends Cell Biol. 9:257–62
    [Google Scholar]
  85. Rathbun LI, Colicino EG, Manikas J, O'Connell J, Krishnan N et al. 2020. Cytokinetic bridge triggers de novo lumen formation in vivo. Nat. Commun. 11:1269
    [Google Scholar]
  86. Rodriguez-Fraticelli AE, Auzan M, Alonso MA, Bornens M, Martin-Belmonte F. 2012. Cell confinement controls centrosome positioning and lumen initiation during epithelial morphogenesis. J. Cell Biol. 198:1011–23
    [Google Scholar]
  87. Rosa JB, Metzstein MM, Ghabrial AS. 2018. An Ichor-dependent apical extracellular matrix regulates seamless tube shape and integrity. PLOS Genet. 14:e1007146
    [Google Scholar]
  88. Rousso T, Schejter ED, Shilo BZ. 2016. Orchestrated content release from Drosophila glue-protein vesicles by a contractile actomyosin network. Nat. Cell Biol. 18:181–90
    [Google Scholar]
  89. Royou A, Sullivan W, Karess R. 2002. Cortical recruitment of nonmuscle myosin II in early syncytial Drosophila embryos: its role in nuclear axial expansion and its regulation by Cdc2 activity. J. Cell Biol. 158:127–37
    [Google Scholar]
  90. Ruiz-Herrero T, Alessandri K, Gurchenkov BV, Nassoy P, Mahadevan L. 2017. Organ size control via hydraulically gated oscillations. Development 144:4422–27
    [Google Scholar]
  91. Ryan AQ, Chan CJ, Graner F, Hiiragi T. 2019. Lumen expansion facilitates epiblast-primitive endoderm fate specification during mouse blastocyst formation. Dev. Cell 51:684–97.e4
    [Google Scholar]
  92. Shamipour S, Caballero-Mancebo S, Heisenberg CP. 2021. Cytoplasm's got moves. Dev. Cell 56:213–26
    [Google Scholar]
  93. Shamipour S, Kardos R, Xue SL, Hof B, Hannezo E, Heisenberg CP. 2019. Bulk actin dynamics drive phase segregation in zebrafish oocytes. Cell 177:1463–79.e18
    [Google Scholar]
  94. Sorrell EL, Lubkin SR. 2021. Bubble packing, eccentricity, and notochord development. Cells Dev 169:203753
    [Google Scholar]
  95. Stanton AE, Goodwin K, Sundarakrishnan A, Jaslove JM, Gleghorn JP et al. 2021. Negative transpulmonary pressure disrupts airway morphogenesis by suppressing Fgf10. Front. Cell Dev. Biol. 9:725785
    [Google Scholar]
  96. Starling EH. 1896. On the absorption of fluids from the connective tissue spaces. J. Physiol. 19:312–26
    [Google Scholar]
  97. Strilic B, Eglinger J, Krieg M, Zeeb M, Axnick J et al. 2010. Electrostatic cell-surface repulsion initiates lumen formation in developing blood vessels. Curr. Biol. 20:2003–9
    [Google Scholar]
  98. Sun X, Zhou Y, Zhang R, Wang Z, Xu M et al. 2020. Dstyk mutation leads to congenital scoliosis-like vertebral malformations in zebrafish via dysregulated mTORC1/TFEB pathway. Nat. Commun. 11:479
    [Google Scholar]
  99. Swinburne IA, Mosaliganti KR, Upadhyayula S, Liu T-L, Hildebrand DGC et al. 2018. Lamellar projections in the endolymphatic sac act as a relief valve to regulate inner ear pressure. eLife 7:e37131
    [Google Scholar]
  100. Syed ZA, Bouge AL, Byri S, Chavoshi TM, Tang E et al. 2012. A luminal glycoprotein drives dose-dependent diameter expansion of the Drosophila melanogaster hindgut tube. PLOS Genet. 8:e1002850
    [Google Scholar]
  101. Tanaka H, Tamura A, Suzuki K, Tsukita S. 2017. Site-specific distribution of claudin-based paracellular channels with roles in biological fluid flow and metabolism. Ann. N.Y. Acad. Sci. 1405:44–52
    [Google Scholar]
  102. Theurkauf WE, Hazelrigg TI. 1998. In vivo analyses of cytoplasmic transport and cytoskeletal organization during Drosophila oogenesis: characterization of a multi-step anterior localization pathway. Development 125:3655–66
    [Google Scholar]
  103. Thompson D. 1917. On Growth and Form Cambridge, UK: Cambridge Univ. Press. , 1st ed..
  104. Tonning A, Hemphala J, Tang E, Nannmark U, Samakovlis C, Uv A. 2005. A transient luminal chitinous matrix is required to model epithelial tube diameter in the Drosophila trachea. Dev. Cell 9:423–30
    [Google Scholar]
  105. Torres-Sánchez A, Kerr Winter M, Salbreux G 2021. Tissue hydraulics: physics of lumen formation and interaction. Cells Dev. July 30:203724. In press
    [Google Scholar]
  106. Tsarouhas V, Senti KA, Jayaram SA, Tiklova K, Hemphala J et al. 2007. Sequential pulses of apical epithelial secretion and endocytosis drive airway maturation in Drosophila. Dev. Cell 13:214–25
    [Google Scholar]
  107. Varner VD, Gleghorn JP, Miller E, Radisky DC, Nelson CM. 2015. Mechanically patterning the embryonic airway epithelium. PNAS 112:9230–35
    [Google Scholar]
  108. Vasquez CG, Vachharajani VT, Garzon-Coral C, Dunn AR. 2021. Physical basis for the determination of lumen shape in a simple epithelium. Nat. Commun. 12:5608
    [Google Scholar]
  109. Venturini V, Pezzano F, Català Castro F, Häkkinen HM, Jiménez-Delgado S et al. 2020. The nucleus measures shape changes for cellular proprioception to control dynamic cell behavior. Science 370:eaba2644
    [Google Scholar]
  110. Vignes H, Vagena-Pantoula C, Prakash M, Fukui H, Norden C et al. 2022. Extracellular mechanical forces drive endocardial cell volume decrease during zebrafish cardiac valve morphogenesis. Dev. Cell 57:598–609.e5
    [Google Scholar]
  111. von Dassow G, Schubiger G. 1994. How an actin network might cause fountain streaming and nuclear migration in the syncytial Drosophila embryo. J. Cell Biol. 127:1637–53
    [Google Scholar]
  112. Voorhees PW. 1985. The theory of Ostwald ripening. J. Stat. Phys. 38:231
    [Google Scholar]
  113. Yamamoto M, Morita R, Mizoguchi T, Matsuo H, Isoda M et al. 2010. Mib-Jag1-Notch signalling regulates patterning and structural roles of the notochord by controlling cell-fate decisions. Development 137:2527–37
    [Google Scholar]
  114. Yang Q, Xue S-L, Chan CJ, Rempfler M, Vischi D et al. 2021. Cell fate coordinates mechano-osmotic forces in intestinal crypt formation. Nat. Cell Biol. 23:733–44
    [Google Scholar]
  115. Yang YHC, Briant LJB, Raab CA, Mullapudi ST, Maischein HM et al. 2022. Innervation modulates the functional connectivity between pancreatic endocrine cells. eLife 11:e64526
    [Google Scholar]
  116. Yasuoka Y. 2020. Morphogenetic mechanisms forming the notochord rod: the turgor pressure-sheath strength model. Dev. Growth Differ. 62:379–90
    [Google Scholar]
  117. Zhang J, Piontek J, Wolburg H, Piehl C, Liss M et al. 2010. Establishment of a neuroepithelial barrier by Claudin5a is essential for zebrafish brain ventricular lumen expansion. PNAS 107:1425–30
    [Google Scholar]
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