Skip to main content

Advertisement

SpringerLink
Log in

Epithelial machines of morphogenesis and their potential application in organ assembly and tissue engineering

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

Sheets of embryonic epithelial cells coordinate their efforts to create diverse tissue structures such as pits, grooves, tubes, and capsules that lead to organ formation. Such cells can use a number of cell behaviors including contractility, proliferation, and directed movement to create these structures. By contrast, tissue engineers and researchers in regenerative medicine seeking to produce organs for repair or replacement therapy can combine cells with synthetic polymeric scaffolds. Tissue engineers try to achieve these goals by shaping scaffold geometry in such a way that cells embedded within these scaffold self-assemble to form a tissue, for instance aligning to synthetic fibers, and assembling native extracellular matrix to form the desired tissue-like structure. Although self-assembly is a dominant process that guides tissue assembly both within the embryo and within artificial tissue constructs, we know little about these critical processes. Here, we compare and contrast strategies of tissue assembly used by embryos to those used by engineers during epithelial morphogenesis and highlight opportunities for future applications of developmental biology in the field of tissue engineering.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abu-Issa R, Kirby ML (2007) Heart field: from mesoderm to heart tube. Ann Rev Cell Dev Biol 23: 45–68. doi:10.1146/annurev.cellbio.23.090506.123331

    Google Scholar 

  • Alenghat FJ, Nauli SM, Kolb R, Zhou J, Ingber DE (2004) Global cytoskeletal control of mechanotransduction in kidney epithelial cells. Exp Cell Res 301(1): 23–30. doi:10.1016/j.yexcr.2004.08.003

    Google Scholar 

  • Atala A, Bauer SB, Soker S, Yoo JJ, Retik AB (2006) Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet 367(9518): 1241–1246. doi:10.1016/S0140-6736(06)68438-9

    Google Scholar 

  • Badylak SF, Taylor D, Uygun K (2011) Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Ann Rev Biomed Eng 13: 27–53. doi:10.1146/annurev-bioeng-071910-124743

    Google Scholar 

  • Badylak SF, Vorp DA, Spievack AR, Simmons-Byrd A, Hanke J, Freytes DO, Thapa A, Gilbert TW, Nieponice A (2005) Esophageal reconstruction with ECM and muscle tissue in a dog model. J Surg Res 128(1): 87–97. doi:10.1016/j.jss.2005.03.002

    Google Scholar 

  • Balaban NQ, Schwarz US, Riveline D, Goichberg P, Tzur G, Sabanay I, Mahalu D, Safran S, Bershadsky A, Addadi L, Geiger B (2001) Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol 3((5): 466–472

    Google Scholar 

  • Basu J, Ludlow JW (2010) Platform technologies for tubular organ regeneration. Trends Biotechnol 28(10): 526–533. doi:10.1016/j.tibtech.2010.07.007

    Google Scholar 

  • Bax DV, McKenzie DR, Bilek MM, Weiss AS (2011) Directed cell attachment by tropoelastin on masked plasma immersion ion implantation treated PTFE. Biomaterials 32(28): 6710–6718. doi:10.1016/j.biomaterials.2011.05.060

    Google Scholar 

  • Beloussov LV (2008) Mechanically based generative laws of morphogenesis. Phys Biol 5(1): 15009. doi:10.1088/1478-3975/5/1/015009

    Google Scholar 

  • Beloussov LV (2012) Morphogenesis as a macroscopic self-organizing process. Biosystems. doi:10.1016/j.biosystems.2012.05.003

  • Beloussov LV, Lakirev AV, Naumidi II (1988) The role of external tensions in differentiation of Xenopus laevis embryonic tissues. Cell Differ Dev 25(3): 165–176

    Google Scholar 

  • Berdichevsky F, Alford D, D’Souza B, Taylor-Papadimitriou J (1994) Branching morphogenesis of human mammary epithelial cells in collagen gels. J Cell Sci 107(Pt 12): 3557–3568

    Google Scholar 

  • Bernfield M, Banerjee SD (1982) The turnover of basal lamina glycosaminoglycan correlates with epithelial morphogenesis. Dev Biol 90((2): 291–305

    Google Scholar 

  • Bershadsky AD, Balaban NQ, Geiger B (2003) Adhesion-dependent cell mechanosensitivity. Ann Rev Cell Dev Biol 19: 677–695

    Google Scholar 

  • Bershadsky A, Kozlov M, Geiger B (2006) Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize. Curr Opin Cell Biol 18(5): 472–481

    Google Scholar 

  • Blanchard GB, Kabla AJ, Schultz NL, Butler LC, Sanson B, Gorfinkiel N, Mahadevan L, Adams RJ (2009) Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation. Nat Methods 6(6): 458–464. doi:10.1038/nmeth.1327

    Google Scholar 

  • Blanchard GB, Murugesu S, Adams RJ, Martinez-Arias A, Gorfinkiel N (2010) Cytoskeletal dynamics and supracellular organisation of cell shape fluctuations during dorsal closure. Development 137(16): 2743–2752. doi:10.1242/dev.045872

    Google Scholar 

  • Boland E, Wnek G, Simpson D, Pawlowski K, Bowlin G (2001) Tailoring tissue engineering scaffolds using electrostatic processing techniques: a study of poly(glycolic acid) electrospinning. J Macromol Sci Pure Appl Chem A38(12): 1231–1243

    Google Scholar 

  • Boland T, Xu T, Damon B, Cui X (2006) Application of inkjet printing to tissue engineering. Biotechnol J 1((9): 910–917. doi:10.1002/biot.200600081

    Google Scholar 

  • 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(51): 22111–22116. doi:10.1073/pnas.1006591107

    Google Scholar 

  • Burg KJ, Porter S, Kellam JF (2000) Biomaterial developments for bone tissue engineering. Biomaterials 21(23): 2347–2359

    Google Scholar 

  • Cai Y, Biais N, Giannone G, Tanase M, Jiang G, Hofman JM, Wiggins CH, Silberzan P, Buguin A, Ladoux B, Sheetz MP (2006) Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys J 91(10): 3907–3920

    Google Scholar 

  • Cao Y, Vacanti JP, Paige KT, Upton J, Vacanti CA (1997) Transplantation of chondrocytes utilizing a polymer-cell construct to produce tissue-engineered cartilage in the shape of a human ear. Plastic and reconstructive surgery 100(2):297–302 (discussion 303–294)

    Google Scholar 

  • Cao Y, Rodriguez A, Vacanti M, Ibarra C, Arevalo C, Vacanti CA (1998) Comparative study of the use of poly(glycolic acid), calcium alginate and pluronics in the engineering of autologous porcine cartilage. J Biomater Sci Poly Edn 9(5): 475–487

    Google Scholar 

  • Chan BP, Leong KW (2008) Scaffolding in tissue engineering: general approaches and tissue-specific considerations. Eur Spine J 17(Suppl 4):467–479. doi:10.1007/s00586-008-0745-3

    Google Scholar 

  • Chen CS (2008) Mechanotransduction—a field pulling together? J Cell Sci 121 (Pt 20):3285–3292. doi:10.1242/jcs.023507

  • Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1997) Geometric control of cell life and death. Science 276(5317): 1425–1428

    Google Scholar 

  • Chen G, Ushida T, Tateishi T (2002) Scaffold design for tissue engineering. Macromol Biosci 2: 67–77

    Google Scholar 

  • Chiu YC, Cheng MH, Engel H, Kao SW, Larson JC, Gupta S, Brey EM (2011) The role of pore size on vascularization and tissue remodeling in PEG hydrogels. Biomaterials 32(26): 6045–6051. doi:10.1016/j.biomaterials.2011.04.066

    Google Scholar 

  • Cortese JD, Schwab B    III, Frieden C, Elson EL (1989) Actin polymerization induces a shape change in actin-containing vesicles. Proc Natl Acad Sci USA 86(15): 5773–5777

    Google Scholar 

  • Cossu G, Kelly R, Di Donna S, Vivarelli E, Buckingham M (1995) Myoblast differentiation during mammalian somitogenesis is dependent upon a community effect. Proc Natl Acad Sci USA 92(6): 2254–2258

    Google Scholar 

  • Cuvelier D, Thery M, Chu YS, Dufour S, Thiery JP, Bornens M, Nassoy P, Mahadevan L (2007) The universal dynamics of cell spreading. Curr Biol 17((8): 694–699

    Google Scholar 

  • von Dassow M, Strother JA, Davidson LA (2010) Surprisingly simple mechanical behavior of a complex embryonic tissue. PLoS ONE 5(12): e15359. doi:10.1371/journal.pone.0015359

    Google Scholar 

  • Davidson L, Keller R (2007) Measuring mechanical properties of embryos and embryonic tissues. Methods Cell Biol 83: 425–439

    Google Scholar 

  • Davidson LA (2011) Epithelial machines that shape the embryo. Trends Cell Biol. doi:10.1016/j.tcb.2011.10.005

  • Davidson LA, Ezin AM, Keller R (2002) Embryonic wound healing by apical contraction and ingression in Xenopus laevis. Cell Motil Cytoskel 53(3): 163–176

    Google Scholar 

  • Davidson LA, Koehl MA, Keller R, Oster GF (1995) How do sea urchins invaginate? Using biomechanics to distinguish between mechanisms of primary invagination. Development 121(7): 2005–2018

    Google Scholar 

  • Davidson LA, Oster GF, Keller RE, Koehl MA (1999) Measurements of mechanical properties of the blastula wall reveal which hypothesized mechanisms of primary invagination are physically plausible in the sea urchin Strongylocentrotus purpuratus. Dev Biol 209(2): 221–238

    Google Scholar 

  • Deshpande VS, McMeeking RM, Evans AG (2006) A bio-chemo-mechanical model for cell contractility. Proc Natl Acad Sci USA 103(38): 14015–14020. doi:10.1073/pnas.0605837103

    Google Scholar 

  • 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(3): 470–477. doi:10.1016/j.devcel.2008.07.009

    Google Scholar 

  • Devin JE, Attawia MA, Laurencin CT (1996) Three-dimensional degradable porous polymer-ceramic matrices for use in bone repair. J Biomater Sci Polymer Edn 7(8): 661–669

    Google Scholar 

  • 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(8): 441–448. doi:10.1007/s11626-999-0050-4

    Google Scholar 

  • Discher DE, Janmey P, Wang YL (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310(5751): 1139–1143. doi:10.1126/science.1116995

    Google Scholar 

  • Dvir-Ginzberg M, Gamlieli-Bonshtein I, Agbaria R, Cohen S (2003) Liver tissue engineering within alginate scaffolds: effects of cell-seeding density on hepatocyte viability, morphology, and function. Tissue Eng 9(4): 757–766. doi:10.1089/107632703768247430

    Google Scholar 

  • Eiraku M, Takata N, Ishibashi H, Kawada M, Sakakura E, Okuda S, Sekiguchi K, Adachi T, Sasai Y (2011) Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472(7341): 51–56. doi:10.1038/nature09941

    Google Scholar 

  • Eisen R, Ratcliffe DR, Ojakian GK (2004) Modulation of epithelial tubule formation by Rho kinase. Am J Physiol Cell Physiol 286(4): C857–C866. doi:10.1152/ajpcell.00246.2003

    Google Scholar 

  • Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4): 677–689

    Google Scholar 

  • Ettensohn CA (1985) Mechanisms of epithelial invagination. Q Rev Biol 60(3): 289–307

    Google Scholar 

  • Ewald AJ, Brenot A, Duong M, Chan BS, Werb Z (2008) Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev Cell 14(4): 570–581. doi:10.1016/j.devcel.2008.03.003

    Google Scholar 

  • Farber MJ, Rizaldy R, Hildebrand JD (2011) Shroom2 regulates contractility to control endothelial morphogenesis. Mol Biol Cell 22(6): 795–805. doi:10.1091/mbc.E10-06-0505

    Google Scholar 

  • Farge E (2003) Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium. Curr Biol 13(16): 1365–1377

    Google Scholar 

  • 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(5): 736–743. doi:10.1016/j.devcel.2009.09.003

    Google Scholar 

  • Franzdottir SR, Axelsson IT, Arason AJ, Baldursson O, Gudjonsson T, Magnusson MK (2010) Airway branching morphogenesis in three dimensional culture. Resp Res 11: 162. doi:10.1186/1465-9921-11-162

    Google Scholar 

  • Fristrom D (1988) The cellular basis of epithelial morphogenesis. A review. Tissue Cell 20(5): 645–690

    Google Scholar 

  • Fu L, Hasebe T, Ishizuya-Oka A, Shi YB (2007) Roles of matrix metalloproteinases and ECM remodeling during thyroid hormone-dependent intestinal metamorphosis in Xenopus laevis. Organogenesis 3(1): 14–19

    Google Scholar 

  • Gassei K, Schlatt S, Ehmcke J (2006) De novo morphogenesis of seminiferous tubules from dissociated immature rat testicular cells in xenografts. J Androl 27(4): 611–618. doi:10.2164/jandrol.05207

    Google Scholar 

  • Gelb BD (2004) Genetic basis of congenital heart disease. Curr Opin Cardiol 19(2): 110–115

    Google Scholar 

  • Ghosh K, Ingber DE (2007) Micromechanical control of cell and tissue development: implications for tissue engineering. Adv Drug Deliv Rev 59(13): 1306–1318. doi:10.1016/j.addr.2007.08.014

    Google Scholar 

  • Gibson MC, Patel AB, Nagpal R, Perrimon N (2006) The emergence of geometric order in proliferating metazoan epithelia. Nature 442(7106): 1038–1041

    Google Scholar 

  • Gjorevski N, Nelson CM (2010) Endogenous patterns of mechanical stress are required for branching morphogenesis. Integr Biol 2(9): 424–434. doi:10.1039/c0ib00040j

    Google Scholar 

  • Gorfinkiel N, Blanchard GB (2011) Dynamics of actomyosin contractile activity during epithelial morphogenesis. Curr Opin Cell Biol 23: 531–539. doi:10.1016/j.ceb.2011.06.002

    Google Scholar 

  • Gorfinkiel N, Blanchard GB, Adams RJ, Martinez Arias A (2009) Mechanical control of global cell behaviour during dorsal closure in Drosophila. Development 136(11): 1889–1898. doi:10.1242/dev.030866

    Google Scholar 

  • Griffith LG, Naughton G (2002) Tissue engineering–current challenges and expanding opportunities. Science 295(5557): 1009–1014. doi:10.1126/science.1069210

    Google Scholar 

  • Grill SW (2011) Growing up is stressful: biophysical laws of morphogenesis. Curr Opin Genet Dev 21(5): 647–652. doi:10.1016/j.gde.2011.09.005

    Google Scholar 

  • Gurdon JB (1988) A community effect in animal development. Nature 336(6201): 772–774. doi:10.1038/336772a0

    Google Scholar 

  • Haigo SL, Hildebrand JD, Harland RM, Wallingford JB (2003) Shroom induces apical constriction and is required for hingepoint formation during neural tube closure. Curr Biol 13(24): 2125–2137

    Google Scholar 

  • Harris TJ, Peifer M (2005) The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila. J Cell Biol 170(5): 813–823

    Google Scholar 

  • Harunaga J, Hsu JC, Yamada KM (2011) Dynamics of salivary gland morphogenesis. J Dental Res 90(9): 1070–1077. doi:10.1177/0022034511405330

    Google Scholar 

  • Hasebe T, Ishizuya-Oka A (2007) Xenopus laevis as a model for the functional analysis of genes involved in embryogenesis and postembryonic organ regeneration. J Nihon Med Sch 74(4): 266–267

    Google Scholar 

  • Hayashi T, Carthew RW (2004) Surface mechanics mediate pattern formation in the developing retina. Nature 431(7009): 647–652

    Google Scholar 

  • Hecker L, Birla RK (2007) Engineering the heart piece by piece: state of the art in cardiac tissue engineering. Regener Med 2(2): 125–144. doi:10.2217/17460751.2.2.125

    Google Scholar 

  • Hilgenfeldt S, Erisken S, Carthew RW (2008) Physical modeling of cell geometric order in an epithelial tissue. Proc Natl Acad Sci USA 105(3): 907–911

    Google Scholar 

  • Holland ND, Panganiban G, Henyey EL, Holland LZ (1996) Sequence and developmental expression of AmphiDll, an amphioxus Distal-less gene transcribed in the ectoderm, epidermis and nervous system: insights into evolution of craniate forebrain and neural crest. Development 122(9): 2911–2920

    Google Scholar 

  • Hsu JC, Yamada KM (2010) Salivary gland branching morphogenesis–recent progress and future opportunities. Int J Oral Sci 2(3): 117–126. doi:10.4248/IJOS10042

    Google Scholar 

  • Hutmacher DW (2001) Scaffold design and fabrication technologies for engineering tissues–state of the art and future perspectives. J Biomater Sci Polym Edn 12(1): 107–124

    Google Scholar 

  • Hutmacher DW, Goh JC, Teoh SH (2001a) An introduction to biodegradable materials for tissue engineering applications. Ann Acad Med Singapore 30(2): 183–191

    Google Scholar 

  • Hutmacher DW, Schantz T, Zein I, Ng KW, Teoh SH, Tan KC (2001b) Mechanical properties and cell cultural response of polycaprolactone scaffolds designed and fabricated via fused deposition modeling. J Biomed Mater Res 55(2): 203–216

    Google Scholar 

  • Ingber DE (2005) Mechanical control of tissue growth: function follows form. Proc Natl Acad Sci USA 102(33): 11571–11572

    Google Scholar 

  • Ingber DE, Mow VC, Butler D, Niklason L, Huard J, Mao J, Yannas I, Kaplan D, Vunjak-Novakovic G (2006) Tissue engineering and developmental biology: going biomimetic. Tissue Eng 12(12): 3265–3283

    Google Scholar 

  • Jaalouk DE, Lammerding J (2009) Mechanotransduction gone awry. Nat Rev Mol Cell Biol 10(1): 63–73. doi:10.1038/nrm2597

    Google Scholar 

  • Jakab K, Damon B, Neagu A, Kachurin A, Forgacs G (2006) Three-dimensional tissue constructs built by bioprinting. Biorheology 43(3-4): 509–513

    Google Scholar 

  • Jakab K, Norotte C, Damon B, Marga F, Neagu A, Besch-Williford CL, Kachurin A, Church KH, Park H, Mironov V, Markwald R, Vunjak-Novakovic G, Forgacs G (2008) Tissue engineering by self-assembly of cells printed into topologically defined structures. Tissue Eng Part A 14(3): 413–421. doi:10.1089/tea.2007.0173

    Google Scholar 

  • Jayo MJ, Jain D, Wagner BJ, Bertram TA (2008) Early cellular and stromal responses in regeneration versus repair of a mammalian bladder using autologous cell and biodegradable scaffold technologies. J Urol 180(1): 392–397. doi:10.1016/j.juro.2008.02.039

    Google Scholar 

  • Joshi SD, von Dassow M, Davidson LA (2010) Experimental control of excitable embryonic tissues: three stimuli induce rapid epithelial contraction. Exp Cell Res 316(1): 103–114. doi:10.1016/j.yexcr.2009.08.005

    Google Scholar 

  • Joshi SD, Webb K (2008) Variation of cyclic strain parameters regulates development of elastic modulus in fibroblast/substrate constructs. J Orthop Res 26((8): 1105–1113. doi:10.1002/jor.20626

    Google Scholar 

  • Kafer J, Hayashi T, Maree AF, Carthew RW, Graner F (2007) Cell adhesion and cortex contractility determine cell patterning in the Drosophila retina. Proc Natl Acad Sci USA 104(47): 18549–18554

    Google Scholar 

  • Kamil SH, Vacanti MP, Aminuddin BS, Jackson MJ, Vacanti CA, Eavey RD (2004) Tissue engineering of a human sized and shaped auricle using a mold. Laryngoscope 114(5): 867–870. doi:10.1097/00005537-200405000-00015

    Google Scholar 

  • Kaneko T, Nomura F, Yasuda K (2011) On-chip constructive cell-network study (I): contribution of cardiac fibroblasts to cardiomyocyte beating synchronization and community effect. J Nanobiotechnol 9: 21. doi:10.1186/1477-3155-9-21

    Google Scholar 

  • Katsumi A, Naoe T, Matsushita T, Kaibuchi K, Schwartz MA (2005) Integrin activation and matrix binding mediate cellular responses to mechanical stretch. J Biol Chem 280(17): 16546–16549

    Google Scholar 

  • Kavlock KD, Whang K, Guelcher SA, Goldstein AS (2012) Degradable segmented polyurethane elastomers for bone tissue engineering: effect of polycaprolactone content. J Biomater Sci Polym Edn. doi:10.1163/156856212X624985

  • Keller R (2002) Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298(5600): 1950–1954

    Google Scholar 

  • Keller R (2006) Mechanisms of elongation in embryogenesis. Development 133(12): 2291–2302

    Google Scholar 

  • Keller R, Davidson L, Edlund A, Elul T, Ezin M, Shook D, Skoglund P (2000) Mechanisms of convergence and extension by cell intercalation. Philos Trans R Soc Lond B 355: 897–922

    Google Scholar 

  • Keller R, Davidson LA, Shook DR (2003) How we are shaped: the biomechanics of gastrulation. Differentiation 71(3): 171–205

    Google Scholar 

  • Kim HY, Davidson LA (2011) Punctuated actin contractions during convergent extension and their permissive regulation by the non-canonical Wnt-signaling pathway. J Cell Sci 124(Pt 4): 635–646. doi:10.1242/jcs.067579

    Google Scholar 

  • Lacalli TC (1994) Apical organs, epithelial domains, and the origin of the chordate central nervous system. Am Zool 34(4): 533–541

    Google Scholar 

  • Lane MC, Koehl MAR, Wilt F, Keller R (1993) A role for regulated secretion of apical extracellular matrix during epithelial invagination in the sea urchin. Development 117(3): 1049–1060

    Google Scholar 

  • Langer R, Vacanti JP (1993) Tissue engineering. Science 260(5110): 920–926

    Google Scholar 

  • Lecuit T, Lenne PF (2007) Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 8(8): 633–644. doi:10.1038/nrm2222

    Google Scholar 

  • Lecuit T, Lenne PF, Munro E (2011) Force generation, transmission, and integration during cell and tissue morphogenesis. Ann Rev Cell Dev Biol 27: 157–184. doi:10.1146/annurev-cellbio-100109-104027

    Google Scholar 

  • Lee JY, Harland RM (2007) Actomyosin contractility and microtubules drive apical constriction in Xenopus bottle cells. Dev Biol 311(1): 40–52

    Google Scholar 

  • Leptin M, Grunewald B (1990) Cell shape changes during gastrulation in Drosophila. Development 110(1): 73–84

    Google Scholar 

  • Liu Y, Ramanath HS, Wang DA (2008) Tendon tissue engineering using scaffold enhancing strategies. Trends Biotechnol 26(4): 201–209. doi:10.1016/j.tibtech.2008.01.003

    Google Scholar 

  • Lysaght MJ, Hazlehurst AL (2004) Tissue engineering: the end of the beginning. Tissue Eng 10(1-2): 309–320. doi:10.1089/107632704322791943

    Google Scholar 

  • Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133(4): 704–715. doi:10.1016/j.cell.2008.03.027

    Google Scholar 

  • Marsden M, DeSimone DW (2003) Integrin-ECM interactions regulate cadherin-dependent cell adhesion and are required for convergent extension in Xenopus. Curr Biol 13(14): 1182–1191

    Google Scholar 

  • Martin AC (2010) Pulsation and stabilization: contractile forces that underlie morphogenesis. Dev Biol 341(1): 114–125. doi:10.1016/j.ydbio.2009.10.031

    Google Scholar 

  • Martin AC, Kaschube M, Wieschaus EF (2008) Pulsed contractions of an actin-myosin network drive apical constriction. Nature. doi:10.1038/nature07522

  • Martin AC, Kaschube M, Wieschaus EF (2009) Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457(7228): 495–499. doi:10.1038/nature07522

    Google Scholar 

  • Martin AC, Gelbart M, Fernandez-Gonzalez R, Kaschube M, Wieschaus EF (2010) Integration of contractile forces during tissue invagination. J Cell Biol 188(5): 735–749. doi:10.1083/jcb.200910099

    Google Scholar 

  • Matkowski B, Martin A, Lepers R (2011) Comparison of maximal unilateral versus bilateral voluntary contraction force. Eur J Appl Physiol 111(8): 1571–1578. doi:10.1007/s00421-010-1775-1

    Google Scholar 

  • Mermelstein CS, Rebello MI, Amaral LM, Costa ML (2003) Changes in cell shape, cytoskeletal proteins and adhesion sites of cultured cells after extracellular Ca2+ chelation. Braz J Med Biol Res 36(8): 1111–1116

    Google Scholar 

  • Metcalfe AD, Ferguson MW (2007) Tissue engineering of replacement skin: the crossroads of biomaterials, wound healing, embryonic development, stem cells and regeneration. J R Soc Interf R Soc 4(14): 413–437. doi:10.1098/rsif.2006.0179

    Google Scholar 

  • Mori M, Miyazaki K (2000) Factors affecting morphogenesis of rabbit gallbladder epithelial cells cultured in collagen gels. Cell Tissue Res 300(2): 331–344

    Google Scholar 

  • Munro EM, Odell GM (2002) Polarized basolateral cell motility underlies invagination and convergent extension of the ascidian notochord. Development 129(1): 13–24

    Google Scholar 

  • Nakajima Y, Burke RD (1996) The initial phase of gastrulation in sea urchins is accompanied by the formation of bottle cells. Dev Biol 179(2): 436–446

    Google Scholar 

  • Nakaya Y, Sheng G (2008) Epithelial to mesenchymal transition during gastrulation: an embryological view. Dev Growth Differ 50(9): 755–766. doi:10.1111/j.1440-169X.2008.01070.x

    Google Scholar 

  • Nelson CM, Chen CS (2003) VE-cadherin simultaneously stimulates and inhibits cell proliferation by altering cytoskeletal structure and tension. J Cell Sci 116(Pt 17): 3571–3581

    Google Scholar 

  • Nelson CM, Jean RP, Tan JL, Liu WF, Sniadecki NJ, Spector AA, Chen CS (2005) Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci USA 102(33): 11594–11599

    Google Scholar 

  • Nemer M (2008) Genetic insights into normal and abnormal heart development. Cardiovasc Pathol 17(1): 48–54

    Google Scholar 

  • Niklason LE, Gao J, Abbott WM, Hirschi KK, Houser S, Marini R, Langer R (1999) Functional arteries grown in vitro. Science 284(5413): 489–493

    Google Scholar 

  • Nogawa H, Ito T (1995) Branching morphogenesis of embryonic mouse lung epithelium in mesenchyme-free culture. Development 121(4): 1015–1022

    Google Scholar 

  • Norotte C, Marga FS, Niklason LE, Forgacs G (2009) Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 30(30): 5910–5917. doi:10.1016/j.biomaterials.2009.06.034

    Google Scholar 

  • O’Farrell PH, Stumpff J, Su TT (2004) Embryonic cleavage cycles: how is a mouse like a fly?. Curr Biol 14(1): R35–R45

    Google Scholar 

  • Ohya Y, Matsunami H, Ouchi T (2004) Cell growth on the porous sponges prepared from poly(depsipeptide-co-lactide) having various functional groups. J Biomater Sci Polym Edn 15(1): 111–123

    Google Scholar 

  • Pardo L, Boland T (2003) A quantitative approach to studying structures and orientation at self-assembled monolayer/fluid interfaces. J Colloid Interf Sci 257(1): 116–120

    Google Scholar 

  • Pollard TD, Cooper JA (2009) Actin, a central player in cell shape and movement. Science 326(5957): 1208–1212. doi:10.1126/science.1175862

    Google Scholar 

  • Pouille PA, Ahmadi P, Brunet AC, Farge E (2009) Mechanical signals trigger myosin II redistribution and mesoderm invagination in Drosophila embryos. Sci Sig 2(66): ra16. doi:10.1126/scisignal.2000098

    Google Scholar 

  • Pulina MV, Hou SY, Mittal A, Julich D, Whittaker CA, Holley SA, Hynes RO, Astrof S (2011) Essential roles of fibronectin in the development of the left-right embryonic body plan. Dev Biol 354(2): 208–220. doi:10.1016/j.ydbio.2011.03.026

    Google Scholar 

  • Rau KR, Quinto-Su PA, Hellman AN, Venugopalan V (2006) Pulsed laser microbeam-induced cell lysis: time-resolved imaging and analysis of hydrodynamic effects. Biophys J 91(1): 317–329. doi:10.1529/biophysj.105.079921

    Google Scholar 

  • Reinhart-King CA, Dembo M, Hammer DA (2005) The dynamics and mechanics of endothelial cell spreading. Biophys J 89(1): 676–689

    Google Scholar 

  • Riveline D, Zamir E, Balaban NQ, Schwarz US, Ishizaki T, Narumiya S, Kam Z, Geiger B, Bershadsky AD (2001) Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol 153(6): 1175–1186

    Google Scholar 

  • Roh-Johnson M, Shemer G, Higgins CD, McClellan JH, Werts AD, Tulu US, Gao L, Betzig E, Kiehart DP, Goldstein B (2012) Triggering a cell shape change by exploiting preexisting actomyosin contractions. Science 335(6073): 1232–1235. doi:10.1126/science.1217869

    Google Scholar 

  • Rolo A, Skoglund P, Keller R (2009) Morphogenetic movements driving neural tube closure in Xenopus require myosin IIB. Dev Biol 327(2): 327–338. doi:10.1016/j.ydbio.2008.12.009

    Google Scholar 

  • Sachlos E, Czernuszka JT (2003) Making tissue engineering scaffolds work. Review: the application of solid freeform fabrication technology to the production of tissue engineering scaffolds. Eur cells Mater 5:29–39 (discussion 39–40)

    Google Scholar 

  • Saim AB, Cao Y, Weng Y, Chang CN, Vacanti MA, Vacanti CA, Eavey RD (2000) Engineering autogenous cartilage in the shape of a helix using an injectable hydrogel scaffold. Laryngoscope 110(10 Pt 1): 1694–1697. doi:10.1097/00005537-200010000-00023

    Google Scholar 

  • Sakai T, Larsen M, Yamada KM (2003) Fibronectin requirement in branching morphogenesis. Nature 423(6942): 876–881

    Google Scholar 

  • Sawyer JM, Harrell JR, Shemer G, Sullivan-Brown J, Roh-Johnson M, Goldstein B (2009) Apical constriction: a cell shape change that can drive morphogenesis. Dev Biol. doi:10.1016/j.ydbio.2009.09.009

  • Sawyer JM, Harrell JR, Shemer G, Sullivan-Brown J, Roh-Johnson M, Goldstein B (2010) Apical constriction: a cell shape change that can drive morphogenesis. Dev Biol 341(1): 5–19. doi:10.1016/j.ydbio.2009.09.009

    Google Scholar 

  • Sbrana F, Sassoli C, Meacci E, Nosi D, Squecco R, Paternostro F, Tiribilli B, Zecchi-Orlandini S, Francini F, Formigli L (2008) Role for stress fiber contraction in surface tension development and stretch-activated channel regulation in C2C12 myoblasts. Am J Physiol Cell Physiol 295(1): C160–C172. doi:10.1152/ajpcell.00014.2008

    Google Scholar 

  • Seliktar D, Black RA, Vito RP, Nerem RM (2000) Dynamic mechanical conditioning of collagen-gel blood vessel constructs induces remodeling in vitro. Ann Biomed Eng 28(4): 351–362

    Google Scholar 

  • Sherrard K, Robin F, Lemaire P, Munro E (2010) Sequential activation of apical and basolateral contractility drives ascidian endoderm invagination. Curr Biol 20(17): 1499–1510. doi:10.1016/j.cub.2010.06.075

    Google Scholar 

  • Shih J, Keller R (1992) Cell motility driving mediolateral intercalation in explants of Xenopus laevis. Development 116(4): 901–914

    Google Scholar 

  • Shih J, Keller R (1992) Patterns of cell motility in the organizer and dorsal mesoderm of Xenopus laevis. Development 116(4): 915–930

    Google Scholar 

  • Shimazu K, Toda S, Miyazono M, Sakemi T, Sugihara H (2001) Morphogenesis of MDCK cells in a collagen gel matrix culture under stromal adipocyte-epithelial cell interaction. Kidney Int 60(2): 568–578. doi:10.1046/j.1523-1755.2001.060002568.x

    Google Scholar 

  • Simons M, Mlodzik M (2008) Planar cell polarity signaling: from fly development to human disease. Ann Rev Genetics 42: 517–540. doi:10.1146/annurev.genet.42.110807.091432

    Google Scholar 

  • Simske JS, Hardin J (2001) Getting into shape: epidermal morphogenesis in Caenorhabditis elegans embryos. Bioessays 23(1): 12–23

    Google Scholar 

  • Smith JL, Schoenwolf GC, Quan J (1994) Quantitative analyses of neuroepithelial cell shapes during bending of the mouse neural plate. J Comp Neurol 342(1): 144–151

    Google Scholar 

  • Solon J, Kaya-Copur A, Colombelli J, Brunner D (2009) Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137(7): 1331–1342. doi:10.1016/j.cell.2009.03.050

    Google Scholar 

  • Sonnemann KJ, Bement WM (2011) Wound repair: toward understanding and integration of single-cell and multicellular wound responses. Annu Rev Cell Dev Biol 27: 237–263. doi:10.1146/annurev-cellbio-092910-154251

    Google Scholar 

  • Spooner BS, Wessells NK (1972) An analysis of salivary gland morphogenesis: role of cytoplasmic microfilaments and microtubules. Dev Biol 27(1): 38–54

    Google Scholar 

  • Stainier DY (2001) Zebrafish genetics and vertebrate heart formation. Nat Rev Genet 2(1): 39–48

    Google Scholar 

  • Taber LA (2008) Theoretical study of Beloussov’s hyper-restoration hypothesis for mechanical regulation of morphogenesis. Biomech Model Mechanobiol 7(6): 427–441

    Google Scholar 

  • ten Berge D, Koole W, Fuerer C, Fish M, Eroglu E, Nusse R (2008) Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell stem cell 3(5): 508–518. doi:10.1016/j.stem.2008.09.013

    Google Scholar 

  • Toyama Y, Peralta XG, Wells AR, Kiehart DP, Edwards GS (2008) Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 321(5896): 1683–1686. doi:10.1126/science.1157052

    Google Scholar 

  • Trepat X, Deng L, An SS, Navajas D, Tschumperlin DJ, Gerthoffer WT, Butler JP, Fredberg JJ (2007) Universal physical responses to stretch in the living cell. Nature 447(7144): 592–595. doi:10.1038/nature05824

    Google Scholar 

  • Varner VD, Taber LA (2012) On integrating experimental and theoretical models to determine physical mechanisms of morphogenesis. Biosystems. doi:10.1016/j.biosystems.2012.05.001

  • Voiculescu O, Bertocchini F, Wolpert L, Keller RE, Stern CD (2007) The amniote primitive streak is defined by epithelial cell intercalation before gastrulation. Nature 449(7165): 1049–1052

    Google Scholar 

  • Wang Y, Steinbeisser H (2009) Molecular basis of morphogenesis during vertebrate gastrulation. Cell Mol Life Sci 66(14): 2263–2273. doi:10.1007/s00018-009-0018-2

    Google Scholar 

  • Warkman AS, Krieg PA (2007) Xenopus as a model system for vertebrate heart development. Sem Cell Dev Biol 18(1): 46–53. doi:10.1016/j.semcdb.2006.11.010

    Google Scholar 

  • Wei C, Larsen M, Hoffman MP, Yamada KM (2007) Self-organization and branching morphogenesis of primary salivary epithelial cells. Tissue Eng 13(4): 721–735. doi:10.1089/ten.2006.0123

    Google Scholar 

  • Williams M, Burdsal C, Periasamy A, Lewandoski M, Sutherland A (2012) Mouse primitive streak forms in situ by initiation of epithelial to mesenchymal transition without migration of a cell population. Dev Dyn 241(2): 270–283. doi:10.1002/dvdy.23711

    Google Scholar 

  • Wozniak MA, Desai R, Solski PA, Der CJ, Keely PJ (2003) ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J Cell Biol 163(3): 583–595. doi:10.1083/jcb.200305010

    Google Scholar 

  • Wright LD, Young RT, Andric T, Freeman JW (2010) Fabrication and mechanical characterization of 3D electrospun scaffolds for tissue engineering. Biomed Mater 5(5): 055006. doi:10.1088/1748-6041/5/5/055006

    Google Scholar 

  • Xing ZC, Han SJ, Shin YS, Koo TH, Moon S, Jeong Y, Kang IK (2012) Enhanced osteoblast responses to poly(methyl methacrylate)/hydroxyapatite electrospun nanocomposites for bone tissue engineering. J Biomater Sci Polymer Edn. doi:10.1163/156856212X623526

  • Xu T, Jin J, Gregory C, Hickman JJ, Boland T (2005) Inkjet printing of viable mammalian cells. Biomaterials 26(1): 93–99. doi:10.1016/j.biomaterials.2004.04.011

    Google Scholar 

  • Zeng J, Aigner A, Czubayko F, Kissel T, Wendorff JH, Greiner A (2005) Poly(vinyl alcohol) nanofibers by electrospinning as a protein delivery system and the retardation of enzyme release by additional polymer coatings. Biomacromolecules 6(3): 1484–1488. doi:10.1021/bm0492576

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Bioengineering, University of Pittsburgh, 3501 Fifth Avenue, Pittsburgh, PA, 15213, USA

    Sagar D. Joshi & Lance A. Davidson

  2. Department of Developmental Biology, University of Pittsburgh, 3501 Fifth Avenue, Pittsburgh, PA, 15213, USA

    Lance A. Davidson

Authors
  1. Sagar D. Joshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lance A. Davidson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lance A. Davidson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Joshi, S.D., Davidson, L.A. Epithelial machines of morphogenesis and their potential application in organ assembly and tissue engineering. Biomech Model Mechanobiol 11, 1109–1121 (2012). https://doi.org/10.1007/s10237-012-0423-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-012-0423-6

Keywords

Search

Navigation