Abstract
Embryogenesis involves biochemical patterning as well as mechanical morphogenetic movements, both regulated by the expression of the regulatory genes of development. The reciprocal interplay of morphogenetic movements with developmental gene expression is becoming an increasingly intense subject of investigation. The molecular processes through which differentiation patterning closely regulates the development of morphogenetic movements are today becoming well understood. Conversely, experimental evidence recently revealed the involvement of mechanical cues due to morphogenetic movements in activating mechano-transduction pathways that control both the differentiation and the active morphogenesis of fundamental events in embryonic tissue development. Here I will first focus on the central role the shape of biological structures of the molecular and mesoscopic cell scales plays in mechano-transduction. Then, after a short description of the genetic regulation of the Drosophila embryo mesoderm invagination at gastrulation—one of the best-understood morphogenetic movement of embryogenesis—I will detail the processes of differentiation and of active morphogenesis of Drosophila embryo gastrulation, which require mechano-transduction. Finally, I will explore the putative consequences in evolution of these mechano-transduction events. I speculate that the first ancient multicellular organisms might have emerged from primary morphological and differentiation patterns induced by primitive mechano-sensation effects allowed by mechano-transduction in response to their physical environment, such as touch by gravity or water flows, which might have acted as primitive motor–sensorial systems, thus conditioning the emergence of our primary animal ancestors.
Similar content being viewed by others
References
Alenghat FJ, Ingber DE (2002) Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Sci STKE 2002(119):pe6
Arendt D, Nubler-Jung K (1997) Dorsal or ventral: similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates. Mech Dev 61:7–21
Aristotle Generation of animals II, vol 22, p 523a15
Barrett K, Leptin M, Settleman J (1997) The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell 91:905–915
Bershadsky AD, Balaban NQ, Geiger B (2003) Adhesion-dependent cell mechanosensitivity. Annu Rev Cell Dev Biol 19:677–695
Bertet C, Sulak L, Lecuit T (2004) Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429:667–671
Brodland GW, Conte V, Cranston PG, Veldhuis J, Narasimhan S, Hutson MS, Jacinto A, Ulrich F, Baum B, Miodownik M (2010) Video force microscopy reveals the mechanics of ventral furrow invagination in Drosophila. Proc Natl Acad Sci USA 107:22111–22116
Brujic J, Hermans RI, Garcia-Manyes S, Walther KA, Fernandez JM (2007) Dwell-time distribution analysis of polyprotein unfolding using force-clamp spectroscopy. Biophys J 92:2896–2903
Conte V, Munoz JJ, Baum B, Miodownik M (2009) Robust mechanisms of ventral furrow invagination require the combination of cellular shape changes. Phys Biol 6:016010
Corey DP, Hudspeth AJ (1979) Ionic basis of the receptor potential in a vertebrate hair cell. Nature 281:675–677
Costa M, Sweeton D, Wieschaus E (1993) Gastrulation in Drosophila: cellular mechanisms of morphogenetic movements. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Woodbury, pp 425–464
Costa M, Wilson ET, Wieschaus E (1994) A putative cell signal encoded by the folded gastrulation gene coordinates cell shape changes during Drosophila gastrulation. Cell 76:1075–1089
Dautry-Varsat A, Ciechanover A, Lodish HF (1983) pH and the recycling of transferrin during receptor-mediated endocytosis. Proc Natl Acad Sci USA 80:2258–2262
De Robertis E, Sasai Y (1996) A common plan for dorsoventral patterning in bilateralia. Nature 380:37–40
Desprat N, Supatto W, Pouille PA, Beaurepaire E, Farge E (2008) Tissue deformation modulates twist expression to determine anterior midgut differentiation in Drosophila embryos. Dev Cell 15:470–477
Dike LE, Chen CS, Mrksich M, Tien J, Whitesides GM, Ingber DE (1999) Geometric control of switching between growth, apoptosis, and differentiation during angiogenesis using micropatterned substrates. In Vitro Cell Dev Biol Anim 35:441–448
Driquez B, Bouclet A, Farge E (2011) Mechanotransduction in mechanically coupled pulsating cells: transition to collective constriction and mesoderm invagination simulation. Phys Biol 8:066007
Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689
Farge E (1995) Increased vesicle endocytosis due to an increase in the plasma membrane phosphatidylserine concentration. Biophys J 69:2501–2506
Farge E (2003) Mechanical induction of twist in the Drosophila foregut/stomodeal primordium. Curr Biol 13:1365–1377
Farge E (2011) Mechanotransduction in development. Curr Top Dev Biol 95:243–265
Farge E, Devaux PF (1992) Shape changes of giant liposomes induced by an asymmetric transmembrane distribution of phospholipids. Biophys J 61:47–357
Farge E, Ojcius DM, Subtil A, Dautry-Varsat A (1999) Enhancement of endocytosis due to aminophospholipid transport across the plasma membrane of living cells. Am J Physiol 276:C725–C733
Fernandez-Gonzalez R, Simoes Sde M, Roper JC, Eaton S, Zallen JA (2009) Myosin II dynamics are regulated by tension in intercalating cells. Dev Cell 17:736–743
Fink J, Carpi N, Betz T, Betard A, Chebah M, Azioune A, Bornens M, Sykes C, Fetler L, Cuvelier D, Piel M (2011) External forces control mitotic spindle positioning. Nat Cell Biol 13:771–778
Gallop JL, Butler PJ, McMahon HT (2005) Endophilin and CtBP/BARS are not acyl transferases in endocytosis or Golgi fission. Nature 438:675–678
Gelbart MA, He B, Martin AC, Thiberge SY, Wieschaus EF, Kaschube M (2012) Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis. Proc Natl Acad Sci USA 109:19298–19303
Ghajar CM, Bissell MJ (2008) Extracellular matrix control of mammary gland morphogenesis and tumorigenesis: insights from imaging. Histochem Cell Biol 130:1105–1118
Gospodarowicz D, Greenburg G, Birdwell CR (1978) Determination of cellular shape by the extracellular matrix and its correlation with the control of cellular growth. Cancer Res 38:4155–4171
Gould KA (1977) Ontogeny and phylogeny. Harvard University Press, Cambridge
Grashoff C, Hoffman BD, Brenner MD, Zhou R, Parsons M, Yang MT, McLean MA, Sligar SG, Chen CS, Ha T, Schwartz MA (2010) Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466:263–266
Haeckel E (1874) Die Gastraea-Theorie, die phylogenetische Klassification des Tierreiches und Homologie der Keimblätter. Jena Z Naturwiss 8:1–55
Helfrich W (1973) Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch C 28:693–703
Hocevar Brezavscek A, Rauzi M, Leptin M, Ziherl P (2012) A model of epithelial invagination driven by collective mechanics of identical cells. Biophys J 103:1069–1077
Holley SA, Jackson PD, Sasai Y, Lu B, De Robertis EM, Hoffmann FM, Ferguson EL (1995) A conserved system for dorsal–ventral patterning in insects and vertebrates involving sog and chordin. Nature 376:249–253
Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M (2003) Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421:172–177
Huttner WB, Schmidt AA (2002) Membrane curvature: a case of endofeelin. Trends Cell Biol 12:155–158
Jaegerstem G (1956) The early phylogeny of the metazoa. The bilaterogastrea theory. Zoot Bidrag(Uppsala) 30:321–354
Jiang J, Kosman D, Ip YT, Levine M (1991) The dorsal morphogen gradient regulates the mesoderm determinant twist in early Drosophila embryos. Genes Dev 5:1881–1891
Jin AJ, Nossal R (2000) Rigidity of triskelion arms and clathrin nets. Biophys J 78:1183–1194
Kahn J, Shwartz Y, Blitz E, Krief S, Sharir A, Breitel DA, Rattenbach R, Relaix F, Maire P, Rountree RB, Kingsley DM, Zelzer E (2009) Muscle contraction is necessary to maintain joint progenitor cell fate. Dev Cell 16:734–743
Kolsch V, Seher T, Fernandez-Ballester GJ, Serrano L, Leptin M (2007) Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science 315:384–386
Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276:565–570
Logan CY, Miller JR, Ferkowicz MJ, McClay DR (1999) Nuclear beta-catenin is required to specify vegetal cell fates in the sea urchin embryo. Development 126:345–357
Mammoto A, Connor KM, Mammoto T, Yung CW, Huh D, Aderman CM, Mostoslavsky G, Smith LE, Ingber DE (2009) A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457:1103–1108
Martin AC, Kaschube M, Wieschaus EF (2009) Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457:495–499
Martindale MQ, Pang K, Finnerty JR (2004) Investigating the origins of triploblasty: “mesodermal” gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131:2463–2474
McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6:483–495
Mitrossilis D, Fouchard J, Guiroy A, Desprat N, Rodriguez N, Fabry B, Asnacios A (2009) Single-cell response to stiffness exhibits muscle-like behavior. Proc Natl Acad Sci USA 106:18243–18248
Muthusamy BP, Natarajan P, Zhou X, Graham TR (2009) Linking phospholipid flippases to vesicle-mediated protein transport. Biochim Biophys Acta 1791:612–619
Nusslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287:795–801
Pomorski T, Lombardi R, Riezman H, Devaux PF, van Meer G, Holthuis JC (2003) Drs2p-related P-type ATPases Dnf1p and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis. Mol Biol Cell 14:1240–1254
Pouille PA (2009) Biomécanique de la gastrulation chez Drosophila melanogaster. Institut Curie, UMR168, vol. PhD. Université Paris 7 Denis Diderot, Paris
Pouille PA, Ahmadi P, Brunet AC, Farge E (2009) Mechanical signals trigger myosin II redistribution and mesoderm invagination in Drosophila embryos. Sci Signal 2(66):ra16
Pouille PA, Farge E (2008) Hydrodynamic simulation of multicellular embryo invagination. Phys Biol 5:15005
Price TD, Qvarnstrom A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc Biol Sci 270:1433–1440
Rauch C, Brunet AC, Deleule J, Farge E (2002) C2C12 myoblast/osteoblast transdifferentiation steps enhanced by epigenetic inhibition of BMP2 endocytosis. Am J Physiol Cell Physiol 283:C235–C243
Rauch C, Farge E (2000) Endocytosis switch controlled by transmembrane osmotic pressure and phospholipid number asymmetry. Biophys J 78:3036–3047
Raucher D, Sheetz MP (1999) Membrane expansion increases endocytosis rate during mitosis. J Cell Biol 144:497–506
Rogers SL, Wiedemann U, Hacker U, Turck C, Vale RD (2004) Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr Biol 14:1827–1833
Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R, Tanaka S, Sheetz MP (2006) Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127:1015–1026
Scheiner S (2006) Contributions of NH⋯O and CH⋯O hydrogen bonds to the stability of beta-sheets in proteins. J Phys Chem B 110:18670–18679
Schneider S, Steinbeisser H, Warga RM, Hausen P (1996) Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech Dev 57:191–198
Seigneuret M, Devaux PF (1984) ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc Natl Acad Sci USA 81:3751–3755
Sherrard K, Robin F, Lemaire P, Munro E (2010) Sequential activation of apical and basolateral contractility drives ascidian endoderm invagination. Curr Biol 20:1499–1510
Sweeton D, Parks S, Costa M, Wieschaus E (1991) Gastrulation in Drosophila: the formation of the ventral furrow and posterior midgut invaginations. Development 112:775–789
Tseng Q, Duchemin-Pelletier E, Deshiere A, Balland M, Guillou H, Filhol O, Thery M (2012) Spatial organization of the extracellular matrix regulates cell–cell junction positioning. Proc Natl Acad Sci USA 109:1506–1511
Vieira AV, Lamaze C, Schmid SL (1996) Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274:2086–2089
Wikramanayake AH, Hong M, Lee PN, Pang K, Byrum CA, Bince JM, Xu R, Martindale MQ (2003) An ancient role for nuclear beta-catenin in the evolution of axial polarity and germ layer segregation. Nature 426:446–450
Wolpert L (1992) Gastrulation and the evolution of development. Dev Suppl: 7–13
Zallen JA, Wieschaus E (2004) Patterned gene expression directs bipolar polarity in Drosophila. Dev Cell 6:343–355
Zhang H, Landmann F, Zahreddine H, Rodriguez D, Koch M, Labouesse M (2011) A tension-induced mechanotransduction pathway promotes epithelial morphogenesis. Nature 471:99–103
Acknowledgments
We thank Joanne Whitehead for her reading of the manuscript. The author’s lab work here described was funded by the ANR (PiriBio ANR-09-Piri-0013-02, ANR 11-BSV5 014 01), the Labex CelTisPhyBio 11-LBX-0038, the ARC 5030 and 29324, the Fondation Pierre Gilles de Gennes, the INSERM, the CNRS, and the HFSP RGP001-14/2006 grants.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Farge, E. Mechano-sensing in Embryonic Biochemical and Morphologic Patterning: Evolutionary Perspectives in the Emergence of Primary Organisms. Biol Theory 8, 232–244 (2013). https://doi.org/10.1007/s13752-013-0119-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13752-013-0119-x