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Morphogenesis

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Continuum Modeling in Mechanobiology

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Abstract

This chapter uses continuum theories for growth and contraction to simulate morphogenesis in embryos. First, the cellular activities underlying tissue-scale morphogenesis are discussed. Next, to illustrate basic concepts in epithelial morphogenesis, a linear theory for growing beams and plates is presented and used to solve illustrative examples involving some basic morphogenetic processes. The full nonlinear theory is then used to solve problems in embryonic development, including gastrulation, neurulation, and organogenesis. Examples of organogenesis include the development of the early heart and brain, the eyes, the gut, and the lung. A buckling analysis is used to simulate folding of the cerebral cortex. Finally, mechanical feedback and a theory for mesenchymal morphogenesis are discussed.

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Notes

  1. 1.

    Technically, stretching involves deformation caused by stress. For convenience, as used here, the term also includes dimensional changes that do not involve true deformation, such as growth that does not generate stress.

  2. 2.

    The linear theory also offers opportunities for creating homework and exam problems.

  3. 3.

    Procedures for including RHM growth theory in Comsol Multiphysics and Abaqus can be found in Hosseini et al. (2014) and Young et al. (2010), respectively.

  4. 4.

    It is a simple matter to enforce incompressibility of fiber volume during contraction, i.e., set \(\det \mathbf {G}=1\). For simplicity, however, this constraint is sometimes ignored in this chapter.

  5. 5.

    This expression represents an approximation to the exact relation κ = (dθ∕dx)∕(1 + θ 2)3∕2 for θ 2 << 1.

  6. 6.

    These boundary conditions are analogous to specifying either displacement or force for a traditional spring and either rotation angle or moment for a torsional spring.

  7. 7.

    For convenience, although the force and moment resultants are defined differently, their symbols are kept the same.

  8. 8.

    Some readers may want to verify this result for themselves.

  9. 9.

    To compare results with the “exact” solution, try Problem 8.5.

  10. 10.

    Hamburger and Hamilton (1951) divided the 21-day incubation period of the chick embryo into 46 stages (Table 8.1). In this chapter, HHx denotes Hamburger–Hamilton stage x.

  11. 11.

    The HT is relatively transparent at these stages.

  12. 12.

    In Fig. 8.39, tissue labels injected along the ventral midline of the HH10 HT move toward the right or left edge in ventral view.

  13. 13.

    As new information becomes available, developmental biologists sometimes change their terminology. Recently, the forebrain has been described as dividing into the diencephalon and secondary prosencephalon (Fig. 8.42, HH20). The secondary prosencephalon includes the optic vesicles, the hypothalamus, and the telencephalon.

  14. 14.

    The bar may eventually stop rotating at some rotation angle, which can be computed using a nonlinear analysis for large rotation (see Problem 8.7).

  15. 15.

    For p≠0 or M g≠0, the beam bends without buckling.

  16. 16.

    In general, for a differential equation of order n, boundary conditions should involve derivatives no higher than n − 1.

  17. 17.

    Other computational models for cortical folding are reviewed elsewhere (Wyczalkowski et al. 2012; Garcia et al. 2018).

  18. 18.

    The study of Shyer et al. (2013) represents an outstanding example of how clever experiments, computational models, and physical models can be integrated to solve a challenging problem in the mechanics of morphogenesis. It is highly recommended to all readers of this book.

  19. 19.

    Interestingly, Beloussov et al. (1975) used tissue dissection to characterize patterns of residual stress in embryos a decade before Y.C. Fung and others began using this technique to study residual stress in mature tissues (Vaishnav and Vossoughi 1983; Fung 1984).

  20. 20.

    Similarly, to obtain realistic growth in a developing artery, we earlier assumed that the target stresses increase with blood pressure [see Eq. (6.128)].

  21. 21.

    Tissue contraction is not always of the actomyosin variety. It also could occur, for example, by cell death (apoptosis), outward cell migration, or resorption of cell membranes.

  22. 22.

    For simplicity, contraction is not treated as an isovolumic process in this problem.

  23. 23.

    In this problem, the wall expands by radial intercalation, with deeper cells moving between those above. This process causes the wall to spread and become thinner.

References

  • Abu-Issa R, Kirby ML (2008) Patterning of the heart field in the chick. Dev Biol 319:223–233

    Article  Google Scholar 

  • Alberts B, Johnson A, Lewis J, Morgan D, Raff M, Roberts K, Walter P (2014) Molecular biology of the cell, 6th edn. W.W. Norton, New York

    Google Scholar 

  • Aleksandrova A, Czirok A, Kosa E, Galkin O, Cheuvront TJ, Rongish BJ (2015) The endoderm and myocardium join forces to drive early heart tube assembly. Dev Biol 404(1):40–54

    Article  Google Scholar 

  • Ambrosi D, Bussolino F, Preziosi L (2005) A review of vasculogenesis models. J Theor Med 6:1–19

    Article  MathSciNet  MATH  Google Scholar 

  • Balfour FM (1880) A treatise on comparative embryology. Macmillan and Company, London

    Book  Google Scholar 

  • Bardet SM, Ferran JL, Sanchez-Arrones L, Puelles L (2010) Ontogenetic expression of sonic hedgehog in the chicken subpallium. Front Neuroanat 4:28

    Google Scholar 

  • Bathe KJ (1996) Finite element procedures. Prentice-Hall, Englewood Cliffs

    MATH  Google Scholar 

  • Bayly PV, Okamoto RJ, Xu G, Shi Y, Taber LA (2013) A cortical folding model incorporating stress-dependent growth explains gyral wavelengths and stress patterns in the developing brain. Phys Biol 10:016005

    Article  Google Scholar 

  • Behrndt M, Salbreux G, Campinho P, Hauschild R, Oswald F, Roensch J, Grill SW, Heisenberg CP (2012) Forces driving epithelial spreading in zebrafish gastrulation. Science 338:257–260

    Article  Google Scholar 

  • Beloussov L, Logvenkov S, Stein A (2015) Mathematical model of an active biological continuous medium with account for the deformations and rearrangements of the cells. Fluid Dyn 50:1–11

    Article  MathSciNet  MATH  Google Scholar 

  • Beloussov LV (1998) The dynamic architecture of a developing organism: an interdisciplinary approach to the development of organisms. Kluwer, Dordrecht

    Book  Google Scholar 

  • Beloussov LV (2015) Morphomechanics of development. Springer, Berlin

    Book  Google Scholar 

  • Beloussov LV, Grabovsky VI (2006) Morphomechanics: goals, basic experiments and models. Int J Dev Biol 50:81–92

    Article  Google Scholar 

  • Beloussov LV, Dorfman JG, Cherdantzev VG (1975) Mechanical stresses and morphological patterns in amphibian embryos. J Embryol Exp Morph 34, 559–574

    Google Scholar 

  • Beloussov LV, Saveliev SV, Naumidi II, Novoselov VV (1994) Mechanical stresses in embryonic tissues: patterns, morphogenetic role, and involvement in regulatory feedback. Int Rev Cytol 150:1–34

    Article  Google Scholar 

  • Belytschko T, Liu WK, Moran B (2000) Nonlinear finite elements for continua and structures. Wiley, Chichester

    MATH  Google Scholar 

  • Bertet C, Sulak L, Lecuit T (2004) Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429:667–671

    Article  Google Scholar 

  • Biot MA (1957) Folding instability of a layered viscoelastic medium under compression. Proc R Soc Lond A Math Phys Sci 242:444–454

    MathSciNet  MATH  Google Scholar 

  • Brodland GW (2006) Do lamellipodia have the mechanical capacity to drive convergent extension? Int J Dev Biol 50:151–155

    Article  Google Scholar 

  • Brodland GW, Chen X, Lee P, Marsden M (2010) From genes to neural tube defects (NTDs): insights from multiscale computational modeling. HFSP J 4:142–152

    Article  Google Scholar 

  • Budday S, Raybaud C, Kuhl E (2014) A mechanical model predicts morphological abnormalities in the developing human brain. Sci Rep 4:5644

    Article  Google Scholar 

  • Budday S, Steinmann P, Kuhl E (2015) Secondary instabilities modulate cortical complexity in the mammalian brain. Philos Mag 95:3244–3256

    Article  Google Scholar 

  • Buskohl PR, Jenkins JT, Butcher JT (2012) Computational simulation of hemodynamic-driven growth and remodeling of embryonic atrioventricular valves. Biomech Model Mechanobiol 11:1205–1217

    Article  Google Scholar 

  • Chada S, Lamoureux P, Buxbaum RE, Heidemann SR (1997) Cytomechanics of neurite outgrowth from chick brain neurons. J Cell Sci 110(Pt 10):1179–1186

    Google Scholar 

  • Chen X, Brodland GW (2008) Multi-scale finite element modeling allows the mechanics of amphibian neurulation to be elucidated. Phys Biol 5:15003

    Article  Google Scholar 

  • Clausi DA, Brodland GW (1993) Mechanical evaluation of theories of neurulation using computer simulations. Development 118:1013–1023

    Google Scholar 

  • Colas JF, Schoenwolf GC (2001) Towards a cellular and molecular understanding of neurulation. Dev Dyn 221:117–145

    Article  Google Scholar 

  • Condic ML, Fristrom D, Fristrom JW (1991) Apical cell shape changes during drosophila imaginal leg disc elongation: a novel morphogenetic mechanism. Development 111:23–33

    Google Scholar 

  • Conte V, Munoz JJ, Miodownik M (2008) A 3d finite element model of ventral furrow invagination in the drosophila melanogaster embryo. J Mech Behav Biomed Mater 1:188–198

    Article  Google Scholar 

  • Coulombre AJ (1956). The role of intraocular pressure in the development of the chick eye. I. Control of eye size. J Exp Zool 133:211–225

    Google Scholar 

  • Czirok A, Little CD (2012) Pattern formation during vasculogenesis. Birth Defects Res C Embryo Today 96:153–162

    Article  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 121:2005–2018

    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. 209:221–238

    Article  Google Scholar 

  • Davies JA (2005) Mechanisms of morphogenesis: the creation of biological form. Elsevier, San Diego

    Google Scholar 

  • Davis GE, Bayless KJ, Mavila A (2002) Molecular basis of endothelial cell morphogenesis in three-dimensional extracellular matrices. Anat Rec 268:252–275

    Article  Google Scholar 

  • De Jong F, Geerts WJ, Lamers WH, Los JA, Moorman AF (1990) Isomyosin expression pattern during formation of the tubular chicken heart: a three-dimensional immunohistochemical analysis. Anat Rec 226:213–227

    Article  Google Scholar 

  • Desgrange A, Le Garrec JF, Meilhac SM (2018) Left-right asymmetry in heart development and disease: forming the right loop. Development 145, dev162776

    Google Scholar 

  • Desmond ME, Jacobson AG (1977) Embryonic brain enlargement requires cerebrospinal fluid pressure. Dev Biol 57:188–198

    Article  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 472:51–56

    Article  Google Scholar 

  • Eiraku M, Adachi T, Sasai Y (2012) Relaxation-expansion model for self-driven retinal morphogenesis: a hypothesis from the perspective of biosystems dynamics at the multi-cellular level. Bioessays 34:17–25

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Fernandez V, Llinares-Benadero C, Borrell V (2016) Cerebral cortex expansion and folding: what have we learned? Embo J 35:1021–1044

    Article  Google Scholar 

  • Filas BA, Bayly PV, Taber LA (2011) Mechanical stress as a regulator of cytoskeletal contractility and nuclear shape in embryonic epithelia. Ann Biomed Eng 39:443–454

    Article  Google Scholar 

  • Filas BA, Oltean A, Majidi S, Bayly PV, Beebe DC, Taber LA (2012) Regional differences in actomyosin contraction shape the primary vesicles in the embryonic chicken brain. Phys Biol 9:066007

    Article  Google Scholar 

  • Flugge W (1975) Viscoelasticity. Springer, New York

    Book  MATH  Google Scholar 

  • Fung YC (1984) Biomechanics: circulation, 1st edn. Springer, New York

    Google Scholar 

  • Garcia KE, Okamoto RJ, Bayly PV, Taber LA (2017) Contraction and stress-dependent growth shape the forebrain of the early chicken embryo. J Mech Behav Biomed Mater 65:383–397

    Article  Google Scholar 

  • Garcia KE, Kroenke C, Bayly P (2018) Mechanics of cortical folding: stress, growth and stability. Philos Trans R Soc B 373:20170321

    Article  Google Scholar 

  • Garcia KE, Stewart WG, Espinosa MG, Gleghorn JP, Taber LA (2019) Molecular and mechanical signals determine morphogenesis of the cerebral hemispheres in the chicken embryo. Development 146:dev174318

    Google Scholar 

  • Garcia-Castro MI, Vielmetter E, Bronner-Fraser M (2000) N-cadherin, a cell adhesion molecule involved in establishment of embryonic left-right asymmetry. Science 288:1047–1051

    Article  Google Scholar 

  • Garcia-Porrero JA, Collado JA, Ojeda JL (1979) Cell death during detachment of the lens rudiment from ectoderm in the chick embryo. Anat Rec 193:791–804

    Article  Google Scholar 

  • Gilbert SF (2010) Developmental biology, 9th edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Goriely A (2017) The mathematics and mechanics of biological growth. Springer, New York

    Book  MATH  Google Scholar 

  • Gupta S, Sen J (2015) Retinoic acid signaling regulates development of the dorsal forebrain midline and the choroid plexus in the chick. Development 142:1293–1298

    Article  Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92

    Article  Google Scholar 

  • Harris AK (1984) Tissue culture cells on deformable substrata: biomechanical implications. J Biomech Eng 106:19–24

    Article  Google Scholar 

  • Harris AK, Wild P, Stopak D (1980) Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208:177–179

    Article  Google Scholar 

  • Haas PA, Höhn SS, Honerkamp-Smith AR, Kirkegaard JB, and Goldstein RE (2018) The noisy basis of morphogenesis: Mechanisms and mechanics of cell sheet folding inferred from developmental variability. PLoS biology 16:e2005536

    Article  Google Scholar 

  • Heer NC, Miller PW, Chanet S, Stoop N, Dunkel J, Martin AC (2017) Actomyosin-based tissue folding requires a multicellular myosin gradient. Development 144:1876–1886

    Article  Google Scholar 

  • Hetenyi M (1971) Beams on elastic foundation: theory with applications in the fields of civil and mechanical engineering. University of Michigan, Ann Arbor

    Google Scholar 

  • Hibbeler RC (2010) Mechanics of materials, 8th edn. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Hilfer SR, Brady RC, Yang J-JW (1981) Intracellular and extracellular changes during early ocular development in the chick embryo. In: Hilfer SR, Sheffield JB (eds) Ocular size and shape regulation during development. Springer, New York, pp 47–78

    Chapter  Google Scholar 

  • Hoffman JI (1995) Incidence of congenital heart disease: II. Prenatal incidence. Pediatr Cardiol 16:155–165

    Article  Google Scholar 

  • Hogers B, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE (1997) Unilateral vitelline vein ligation alters intracardiac blood flow patterns and morphogenesis in the chick embryo. Circ Res 80:473–481

    Article  Google Scholar 

  • Hohn S, Hallmann A (2011) There is more than one way to turn a spherical cellular monolayer inside out: type b embryo inversion in volvox globator. BMC Biol 9:89

    Article  Google Scholar 

  • Hosseini HS, Taber LA (2018) How mechanical forces shape the developing eye. Prog Biophys Mol Biol 137:25–36

    Article  Google Scholar 

  • Hosseini HS, Beebe DC, Taber LA (2014) Mechanical effects of the surface ectoderm on optic vesicle morphogenesis in the chick embryo. J Biomech 47:3837–3846

    Article  Google Scholar 

  • Hosseini HS, Garcia KE, Taber LA (2017) A new hypothesis for foregut and heart tube formation based on differential growth and actomyosin contraction. Development 144:2381–2391

    Article  Google Scholar 

  • Huang J, Rajagopal R, Liu Y, Dattilo LK, Shaham O, Ashery-Padan R, Beebe DC (2011) The mechanism of lens placode formation: a case of matrix-mediated morphogenesis. Dev Biol 355:32–42

    Article  Google Scholar 

  • Hyer J, Kuhlman J, Afif E, Mikawa T (2003) Optic cup morphogenesis requires pre-lens ectoderm but not lens differentiation. Dev Biol 259:351–363

    Article  Google Scholar 

  • Itasaki N, Nakamura H, Sumida H, Yasuda M (1991) Actin bundles on the right side in the caudal part of the heart tube play a role in dextro-looping in the embryonic chick heart. Anat Embryol 183:29–39

    Article  Google Scholar 

  • Jelinek R, Pexieder T (1968) The pressure of encephalic fluid in chick embryos between the 2nd and 6th day of incubation. Physiol Bohemoslov 17:297–305

    Google Scholar 

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

    Article  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 Biol Sci 355:897–922

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kidokoro H, Okabe M, Tamura K (2008) Time-lapse analysis reveals local asymmetrical changes in c-looping heart tube. Dev Dyn 237:3545–3556

    Article  Google Scholar 

  • Kidokoro H, Yonei-Tamura S, Tamura K, Schoenwolf GC, Saijoh Y (2018) The heart tube forms and elongates through dynamic cell rearrangement coordinated with foregut extension. Development 145:dev152488

    Google Scholar 

  • Kim HY, Varner VD, Nelson CM (2013) Apical constriction initiates new bud formation during monopodial branching of the embryonic chicken lung. Development 140:3146–3155

    Article  Google Scholar 

  • Kim HY, Pang MF, Varner VD, Kojima L, Miller E, Radisky DC, Nelson CM (2015) Localized smooth muscle differentiation is essential for epithelial bifurcation during branching morphogenesis of the mammalian lung. Dev Cell 34:719–726

    Article  Google Scholar 

  • Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310

    Article  Google Scholar 

  • Kinoshita N, Sasai N, Misaki K, Yonemura S (2008) Apical accumulation of rho in the neural plate is important for neural plate cell shape change and neural tube formation. Mol Biol Cell 19:2289–2299

    Article  Google Scholar 

  • Kirby ML (2007) Cardiac development. Oxford University Press, Oxford

    Google Scholar 

  • Kominami T, Takata H (2004) Gastrulation in the sea urchin embryo: a model system for analyzing the morphogenesis of a monolayered epithelium. Dev Growth Differ 46:309–326

    Article  Google Scholar 

  • Kremnyov SV, Troshina TG, Beloussov LV (2012) Active reinforcement of externally imposed folding in amphibians embryonic tissues. Mech Develop 129:51–60

    Article  Google Scholar 

  • Kroenke CD, Taber EN, Leigland LA, Knutsen AK, Bayly PV (2009) Regional patterns of cerebral cortical differentiation determined by diffusion tensor MRI. Cerebral Cortex 19:2916–2929

    Article  Google Scholar 

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

    Google Scholar 

  • Latacha KS, Remond MC, Ramasubramanian A, Chen AY, Elson EL, Taber LA (2005) The role of actin polymerization in bending of the early heart tube. Dev Dyn 233:1272–1286

    Article  Google Scholar 

  • Lawson A, Anderson H, Schoenwolf GC (2001) Cellular mechanisms of neural fold formation and morphogenesis in the chick embryo. Anat Rec 262:153–168

    Article  Google Scholar 

  • Linask KK, Han MD, Linask KL, Schlange T, Brand T (2003) Effects of antisense misexpression of CFC on downstream flectin protein expression during heart looping. Dev. Dyn. 228:217–230

    Article  Google Scholar 

  • Linask KK, Han M, Cai DH, Brauer PR, Maisastry SM (2005) Cardiac morphogenesis: matrix metalloproteinase coordination of cellular mechanisms underlying heart tube formation and directionality of looping. Dev Dyn 233:739–753

    Article  Google Scholar 

  • Logvenkov S, Stein A (2015) Mathematical modeling of the stretching-induced elongation of the embryonic epithelium layer in the absence of an external load. Biophysics 60:977–982

    Article  Google Scholar 

  • Lowery LA, Sive H (2004) Strategies of vertebrate neurulation and a re-evaluation of teleost neural tube formation. Mech Dev 121:1189–1197

    Article  Google Scholar 

  • Mammoto T, Mammoto A, Ingber DE (2013) Mechanobiology and developmental control. Annu Rev Cell Dev Bi 29:27–61

    Article  Google Scholar 

  • Manasek FJ, Burnside MB, Waterman RE (1972) Myocardial cell shape changes as a mechanism of embryonic heart looping. Dev Biol 29:349–371

    Article  Google Scholar 

  • Manasek FJ, Isobe Y, Shimada Y, Hopkins W, Nora JJ, Takao A (1984) The embryonic myocardial cytoskeleton, interstitial pressure, and the control of morphogenesis. In Nora JJ, Takao A (eds), Congenital heart disease: causes and processes. Futura Publishing, Mount Kisco, pp 359–376

    Google Scholar 

  • Manner J (2000) Cardiac looping in the chick embryo: a morphological review with special reference to terminological and biomechanical aspects of the looping process. Anat Rec 259:248–262

    Article  Google Scholar 

  • Manner J (2009) The anatomy of cardiac looping: a step towards the understanding of the morphogenesis of several forms of congenital cardiac malformations. Clin Anat 22:21–35

    Article  Google Scholar 

  • Manoussaki D, Lubkin SR, Vernon RB, Murray JD (1996) A mechanical model for the formation of vascular networks in vitro. Acta Biotheor 44:271–282

    Article  Google Scholar 

  • Martin AC (2010) Pulsation and stabilization: contractile forces that underlie morphogenesis. Dev Biol 341:114–125

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Matt G, Umen J (2016) Volvox: a simple algal model for embryogenesis, morphogenesis and cellular differentiation. Dev Biol 419:99–113

    Article  Google Scholar 

  • Merle T, Farge E (2018) Trans-scale mechanotransductive cascade of biochemical and biomechanical patterning in embryonic development: the light side of the force. Curr Opin Cell Biol 55:111–118

    Article  Google Scholar 

  • Morrill J, Santos L (1985) A scanning electron microscopical overview of cellular and extracellular patterns during blastulation and gastrulation in the sea urchin, lytechinus variegatus. In: Sawyer RH, Showman RM (eds) The cellular and molecular biology of invertebrate development. University of South Carolina Press, Columbia, pp 3–33

    Google Scholar 

  • Moury JD, Schoenwolf GC (1995) Cooperative model of epithelial shaping and bending during avian neurulation: autonomous movements of the neural plate, autonomous movements of the epidermis, and interactions in the neural plate/epidermis transition zone. Dev. Dyn. 204:323–337

    Article  Google Scholar 

  • Munoz JJ, Barrett K, Miodownik M (2007) A deformation gradient decomposition method for the analysis of the mechanics of morphogenesis. J Biomech 40:1372–1380

    Article  Google Scholar 

  • Murray JD (2003) Mathematical biology: spatial models and biomedical applications. Springer, New York

    Book  MATH  Google Scholar 

  • Nakamura A, Manasek FJ (1978) Experimental studies of the shape and structure of isolated cardiac jelly. J Embryol Exp Morph 43:167–183

    Google Scholar 

  • Nelson CM (2016) On buckling morphogenesis. J Biomech Eng 138:021005

    Article  Google Scholar 

  • Odell GM, Oster G, Alberch P, Burnside B (1981) The mechanical basis of morphogenesis. I. Epithelial folding and invagination. Dev Biol 85:446–462

    Article  Google Scholar 

  • Ohkubo Y, Chiang C, Rubenstein JL (2002) Coordinate regulation and synergistic actions of bmp4, shh and fgf8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles. Neuroscience 111:1–17

    Article  Google Scholar 

  • Oltean A, Taber LA (2018) Apoptosis generates mechanical forces that close the lens vesicle in the chick embryo. Phys Biol 15:025001

    Article  Google Scholar 

  • Oltean A, Huang J, Beebe DC, Taber LA (2016) Tissue growth constrained by extracellular matrix drives invagination during optic cup morphogenesis. Biomech Model Mechanobiol 15:1405–1421

    Article  Google Scholar 

  • Oster GF, Murray JD, Harris AK (1983) Mechanical aspects of mesenchymal morphogenesis. J Embryol Exp Morph 78:83–125

    MATH  Google Scholar 

  • Patten BM (1922) The formation of the cardiac loop in the chick. Am J Anat 30:373–397

    Article  Google Scholar 

  • Patten BM (1971). Early embryology of the chick. 5th edn. McGraw-Hill, New York

    Google Scholar 

  • Patwari P, Lee RT (2008) Mechanical control of tissue morphogenesis. Circ Res 103:234–243

    Article  Google Scholar 

  • Plageman TF Jr, Chung MI, Lou M, Smith AN, Hildebrand JD, Wallingford JB, Lang RA (2010) Pax6-dependent shroom3 expression regulates apical constriction during lens placode invagination. Development 137:405–415

    Article  Google Scholar 

  • Plageman TF Jr, Chauhan BK, Yang C, Jaudon F, Shang X, Zheng Y, Lou M, Debant A, Hildebrand JD, Lang RA (2011) A trio-rhoa-shroom3 pathway is required for apical constriction and epithelial invagination. Development 138:5177–5188

    Article  Google Scholar 

  • Polyakov O, He B, Swan M, Shaevitz JW, Kaschube M, Wieschaus E (2014) Passive mechanical forces control cell-shape change during drosophila ventral furrow formation. Biophys J 107:998–1010

    Article  Google Scholar 

  • Pouille PA, Ahmadi P, Brunet AC, Farge E (2009) Mechanical signals trigger myosin II redistribution and mesoderm invagination in drosophila embryos. Sci Signal 2:ra16

    Google Scholar 

  • Ramasubramanian A, Taber LA (2008) Computational modeling of morphogenesis regulated by mechanical feedback. Biomech Model Mechanobiol 7:77–91

    Article  Google Scholar 

  • Ramasubramanian A, Nerurkar NL, Achtien KH, Filas BA, Voronov DA, Taber LA (2008) On modeling morphogenesis of the looping heart following mechanical perturbations. J Biomech Eng 130:061018

    Article  Google Scholar 

  • Ramasubramanian A, Chu-Lagraff QB, Buma T, Chico KT, Carnes ME, Burnett KR, Bradner SA, Gordon SS (2013) On the role of intrinsic and extrinsic forces in early cardiac s-looping. Dev Dyn 242:801–816

    Article  Google Scholar 

  • Ramasubramanian A, Capaldi X, Bradner S, and Gangi L (2019) On the biomechanics of cardiac s-looping: Insights from modeling and perturbation studies. J Biomech Eng:051011

    Google Scholar 

  • Rauzi M, Hocevar Brezavscek A, Ziherl P, Leptin M (2013) Physical models of mesoderm invagination in drosophila embryo. Biophys J 105:3–10

    Article  Google Scholar 

  • Rauzi M, Verant P, Lecuit T, Lenne PF (2008) Nature and anisotropy of cortical forces orienting drosophila tissue morphogenesis. Nat Cell Biol 10:1401–1410

    Article  Google Scholar 

  • Ray P, Chin AS, Worley KE, Fan J, Kaur G, Wu M, Wan LQ (2018) Intrinsic cellular chirality regulates left-right symmetry breaking during cardiac looping. Proc Natl Acad Sci USA 115:E11568–E11577

    Article  Google Scholar 

  • Razavi MJ, Zhang T, Li X, Liu T, Wang X (2015) Role of mechanical factors in cortical folding development. Phys Rev E Stat Nonlinear Soft Matter Phys 92:032701

    Article  Google Scholar 

  • Redd MJ, Cooper L, Wood W, Stramer B, Martin P (2004) Wound healing and inflammation: embryos reveal the way to perfect repair. Philos Trans R Soc Lond B Biol Sci 359:777–784

    Article  Google Scholar 

  • Reillo I, de Juan Romero C, Garcia-Cabezas MA, Borrell V (2011) A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb Cortex 21:1674–1694

    Article  Google Scholar 

  • Richman DP, Stewart RM, Hutchinson JW, Caviness VS Jr (1975) Mechanical model of brain convolutional development. Science 189:18–21

    Article  Google Scholar 

  • Risau W, Feinberg RN, Sherer GK, Auerbach R (1991) Vasculogenesis, angiogenesis, and endothelial cell differentiation during embryonic development. In: The development of the vascular system. Karger, Basel, pp 58–68

    Google Scholar 

  • Romanoff AL (1960) The avian embryo: structural and functional development. Macmillan, New York

    Google Scholar 

  • Savin T, Kurpios NA, Shyer AE, Florescu P, Liang H, Mahadevan L, Tabin CJ (2011) On the growth and form of the gut. Nature 476:57–62

    Article  Google Scholar 

  • 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 341:5–19

    Article  Google Scholar 

  • Schoenwolf GC, Alvarez IS (1989) Roles of neuroepithelial cell rearrangement and division in shaping of the avian neural plate. Development 106:427–439

    Google Scholar 

  • Schook P (1980) Morphogenetic movements during the early development of the chick eye. An ultrastructural and spatial reconstructive study. B. Invagination of the optic vesicle and fusion of its walls. Acta Morphol Neerl Scand 18:159–180

    Google Scholar 

  • Scianna M, Bell C, Preziosi L (2013) A review of mathematical models for the formation of vascular networks. J Theor Biol 333:174–209

    Article  MathSciNet  MATH  Google Scholar 

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

    Article  Google Scholar 

  • Shi Y, Yao J, Xu G, Taber LA (2014a) Bending of the looping heart: differential growth revisited. J Biomech Eng 136:081002

    Article  Google Scholar 

  • Shi Y, Yao J, Young JM, Fee JA, Perucchio R, Taber LA (2014b) Bending and twisting the embryonic heart: a computational model for c-looping based on realistic geometry. Front Physiol 5:297

    Article  Google Scholar 

  • Shi Y, Varner VD, Taber LA (2015) Why is cytoskeletal contraction required for cardiac fusion before but not after looping begins? Phys Biol 12:016012

    Article  Google Scholar 

  • Shore TW, Pickering J (1889) The proamnion and amnion in the chick. J Anat Physiol 24:1

    Google Scholar 

  • Shyer AE, Tallinen T, Nerurkar NL, Wei ZY, Gil ES, Kaplan DL, Tabin CJ, Mahadevan L (2013) Villification: how the gut gets its villi. Science 342:212–218

    Article  Google Scholar 

  • Soufan AT, van den Berg G, Ruijter JM, de Boer PA, van den Hoff MJ, Moorman AF (2006) Regionalized sequence of myocardial cell growth and proliferation characterizes early chamber formation. Circ Res 99:545–552

    Article  Google Scholar 

  • Spear PC, Erickson CA (2012) Interkinetic nuclear migration: a mysterious process in search of a function. Dev Growth Differ 54:306–316

    Article  Google Scholar 

  • Stalsberg H, DeHaan RL (1968) Endodermal movements during foregut formation in the chick embryo. Dev Biol 18:198–215

    Article  Google Scholar 

  • Striedter GF, Srinivasan S, Monuki ES (2015) Cortical folding: when, where, how, and why? Annu Rev Neurosci 38:291–307

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Taber LA (2006) Biophysical mechanisms of cardiac looping. Int J Dev Biol 50:323–332

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Taber LA (2009) Towards a unified theory for morphomechanics. Phil Trans Roy Soc A Math Phys Eng Sci 367:3555–3583

    Article  MathSciNet  MATH  Google Scholar 

  • Taber LA (2014a) Cellular forces in morphogenesis. In: Kaunas R, Zemel A (eds) Cell and matrix mechanics. Taylor & Francis, New York, pp 259–283

    Chapter  Google Scholar 

  • Taber LA (2014b) Morphomechanics: transforming tubes into organs. Curr Opin Genet Dev 27:7–13

    Article  Google Scholar 

  • Takamatsu T, Fujita S (1987) Growth of notochord and formation of cranial and mesencephalic flexures in chicken-embryo. Develop Growth Differ 29:497–502

    Article  Google Scholar 

  • Tallinen T, Chung JY, Rousseau F, Girard N, Lefevre J, Mahadevan L (2016) On the growth and form of cortical convolutions. Nat Phys 12:588–593

    Article  Google Scholar 

  • Thompson DW (1942) On growth and form. Cambridge University Press, Cambridge

    MATH  Google Scholar 

  • Turing AM (1952) The chemical basis of morphogenesis. Phil. Trans. Roy. Soc. London B237:37–72

    MathSciNet  MATH  Google Scholar 

  • Vaishnav RN, Vossoughi J (1983) Estimation of residual strains in aortic segments. In: Hall CW (ed.) Recent developments in biomedical engineering. Pergamon Press, New York, pp 330–333

    Google Scholar 

  • Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313–318

    Article  Google Scholar 

  • Varner VD, Taber LA (2012) Not just inductive: a crucial mechanical role for the endoderm during heart tube assembly. Development 139:1680–1690

    Article  Google Scholar 

  • Varner VD, Nelson CM (2017) Computational models of airway branching morphogenesis. Semin Cell Dev Biol 67:170–176

    Article  Google Scholar 

  • Varner VD, Voronov DA, Taber LA (2010) Mechanics of head fold formation: investigating tissue-level forces during early development. Development 137:3801–3811

    Article  Google Scholar 

  • Varner VD, Gleghorn JP, Miller E, Radisky DC, Nelson CM (2015) Mechanically patterning the embryonic airway epithelium. P Natl Acad Sci USA 112:9230–9235

    Article  Google Scholar 

  • Vernon RB, Angello JC, Iruela-Arispe ML, Lane TF, Sage EH (1992) Reorganization of basement membrane matrices by cellular traction promotes the formation of cellular networks in vitro. Lab Invest 66:536–547

    Google Scholar 

  • Viamontes GI, Fochtmann LJ, Kirk DL (1979) Morphogenesis in volvox: analysis of critical variables. Cell 17:537–550

    Article  Google Scholar 

  • Voronov DA, Alford PW, Xu G, Taber LA (2004) The role of mechanical forces in dextral rotation during cardiac looping in the chick embryo. Dev Biol 272:339–350

    Article  Google Scholar 

  • Welker W, Jones EG, Peters A (1990) Why does the cerebral cortex fissure and fold? A review of the determinants of gyri and sulci. In: Cerebral cortex. Plenum, New York, pp 3–136

    Chapter  Google Scholar 

  • Wolpert L (1969) Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25:1–47

    Article  Google Scholar 

  • Wyczalkowski MA, Chen Z, Filas BA, Varner VD, Taber LA (2012) Computational models for mechanics of morphogenesis. Birth Defects Res C Embryo Today 96:132–152

    Article  Google Scholar 

  • Xu G, Kemp PS, Hwu JA, Beagley AM, Bayly PV, Taber LA (2010a) Opening angles and material properties of the early embryonic chick brain. J Biomech Eng 132:011005

    Article  Google Scholar 

  • Xu G, Knutsen AK, Dikranian K, Kroenke CD, Bayly PV, Taber LA (2010b) Axons pull on the brain, but tension does not drive cortical folding. J Biomech Eng 132:071013

    Article  Google Scholar 

  • Young JM, Yao J, Ramasubramanian A, Taber LA, Perucchio R (2010) Automatic generation of user material subroutines for biomechanical growth analysis. J Biomech Eng 132:104505

    Article  Google Scholar 

  • Zamir EA, Taber LA (2004) Material properties and residual stress in the stage 12 chick heart during cardiac looping. J Biomech Eng 126:823–830

    Article  Google Scholar 

  • Zwaan J, Hendrix RW (1973) Changes in cell and organ shape during early development of the ocular lens. Am Zool 13:1039–1049

    Article  Google Scholar 

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    Larry A. Taber

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Taber, L.A. (2020). Morphogenesis. In: Continuum Modeling in Mechanobiology. Springer, Cham. https://doi.org/10.1007/978-3-030-43209-6_8

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