Summary
Morphornetry and computerized three-dimensional reconstruction were used to study the relationship between apical constriction of neuroepithelial cells and the pattern of bending of the neuroepithelium in the developing neural tube of the 12-somite mouse embryo. The neuroepithelium of the mouse exhibits prominent regional variations in size and shape along the embryo axis. The complex shape of most of the cephalic neural tube (e.g., forebrain and midbrain) is due to the coexistence of concave and convex bending sites whereas more caudal regions (e.g., hindbrain and spinal cord) generally lack sites of convex bending and have a relatively simple shape. The apical morphology of neuroepithelial cells was found to be correlated more closely with the local status of bending of the neuroepithelium than with the specific region of the neural tube in which they are located. In areas of enhanced apical constriction, microfilament bundles were particularly prominent. Morphornetry revealed that patterns of bending of the neuroepithelium were correlated almost exactly with those of apical constriction throughout the forming neural tube. These findings support the idea that apical constriction of neuroepithelial cells, resulting from tension generated by microfilament bundles, plays a major role in bending of the neuroepithelium during neural tube formation in the mouse.
Similar content being viewed by others
References
Burnside B (1973) Microtubules and microfilaments in amphibian neurulation. Am Zool 13:989–1006
Campbell LR, Dayton DH, Sohal GS (1986) Neural tube defects: A review of human and animal studies on the etiology of neural tube defects. Teratology 34:171–187
Clarke A, Spudich JA (1977) Nonmuscle contractile proteins: The role of actin and myosin in cell motility and shape determinations. Annu Rev Biochem 46:797–822
Geelen JAG, Langman J (1977) Closure of the neural tube in the cephalic region of the mouse embryo. Anat Rec 189:625–640
Geelen JAG, Langman J (1979) Ultrastructure observations on closure of the neural tube in the mouse. Anat Embryol 156:73–88
Gordon R (1985) A review of the theories of vertebrate neurulation and their relationship to the neural tube birth defects. J Embryol Exp Morphol 87:229–255
Groschel-Stewart U (1980) Immunocytochemistry of cytoplasmic contractile proteins. Int Rev Cytol 65:193–254
Jacobson AG, Gordon R (1976) Changes in the shape of the developing nervous system analyzed experimentally, and by computer simulation. J Exp Zool 197:191–246
Jacobson AG, Tam PPL (1982) Cephalic neurulation in the mouse embryo analyzed by SEM and morphometry. Anat Rec 203:375–396
Karfunkel P (1974) The mechanisms of neural tube formation. Int Rev Cytol 38:245–271
Lee H, Kalmus GW (1976) Effects of cytochalasin B on the morphogenesis of explanted early chick embryos. Growth 40:153–162
Lee H, Nagele RG (1979) Neural tube closure defects caused by papaverine in explanted early chick embryos. Teratology 20:321–332
Lee H, Nagele RG (1985a) Neural tube defects caused by local anesthetics in early chick embryos. Teratology 31:119–127
Lee H, Nagele RG (1985b) Studies on the mechanisms of neurulation in the chick. Correlationship of microfilaments, contractile proteins, and the shape of neuroepithelial cells. J Exp Zool 235:205–215
Lee H, Nagele RG (1985c) Possible involvement of calmodulin in apical constriction of neuroepithelial cells and elevation of neural folds in the chick. Experientia 41:1186–1188
Lee H, Nagele RG (1986) Toxic and teratologie effects of verapamil on early chick embryos. Teratology 33:203–211
Lee H, Nagele RG, Karasanyi N (1978) Inhibition of neural tube closure by ionophore A23187 in chick embryos. Experientia 34:518–519
Moore DCP, Stanisstreet M, Evans GE (1987) Morphometric analysis of changes in cell shape in the neuroepithelium of mammalian embryos. J Anat 155:87–99
Moran D (1976) Scanning electron microscopic and flame spectrometry study on the role of Ca2+ in amphibian neurulation using papaverine inhibition and ionophore induction of morphogenetic movements. J Exp Zool 198:409–416
Moran D, Rice RW (1976) Action of papaverine and ionophore A23187 on neurulation. Nature 261:497–499
Morriss-Kay GM (1981) Growth and development of pattern in the cranial neural epithelium of rat embryos during neurulation. J Embryol Exp Morphol 65:225–241
Morriss GM, New DAT (1979) Effect of oxygen concentration on morphogenesis of cranial neural folds and neural crest in cultured rat embryos. J Embryol Exp Morphol 54:17–35
Morriss-Kay GM, Tuckett F (1985) The role of microfilaments in cranial neurulation in rat embryos: effects of short-term exposure to cytochalasin D. J Embryol Exp Morphol 88:333–348
Nagele RG, Lee H (1980) Studies on the mechanisms of neurulation in the chick: microfilament-mediated changes in cell shape during uplifting of neural folds. J Exp Zool 213:391–398
Nagele RG, Lee H (1987) Studies on the mechanisms of neurulation in the chick: Morphometric analysis of the relationship between regional variation in cell shape and sites of motive force generation. J Exp Zool 241:197–205
Nagele RG, Pietrolungo JF, Lee H, Roisen FJ (1981) Diazepaminduced neural tube closure defects in explanted early chick embryos. Teratology 23:343–349
Nagele RG, Hunter E, Bush K, Lee H (1987) Studies on the mechanisms of neurulation in the chick: morphometric analysis of force distribution within the neuroepithelium during neural tube formation. J Exp Zool 244:425–436
Nagele RG, Bush KT, Hunter ET, Kosciuk MC, Lee H (1989a) Biomechanical basis of diazepam-induced neural tube defects in early chick embryos. A morphometric study. Teratology 40:29–36
Nagele RG, Bush KT, Kosciuk MC, Lee H (1989b) Intrinsic and extrinsic factors collaborate to generate driving forces for neural tube formation in the chick: a study using morphometry and computerized three-dimensional reconstruction. Dev Brain Res (in press)
O'Shea KS, Kaufman MH (1980) Neural tube closure defects following in vitro exposure of mouse embryos to xylocaine. J Exp Zool 214:235–238
Sadler TW, Greenberg D, Coughlin P, Lessard JL (1982) Actin distribution patterns in the mouse neural tube during neurulation. Science 215:172–174
Schoenwolf GC (1982) On the morphogenesis of the early rudiments of the developing central nervous system. Scanning Elec Microsc 1:289–308
Schroeder TE (1973) Cell constriction: contractile role of microfilaments in division and development. Am Zool 13:949–960
Schliwa M (1982) Action of cytochalasin D on cytoskeletal networks. J Cell Biol 92:79–91
Waterman RE (1976) Topographical changes along the neural fold associated with neurulation in the hampster and mouse. Am J Anat 146:151–172
Wilson DB, Finta LA (1980) Fine structure of the lumbrosacral neural folds in the mouse embryo. J Embryol Exp Morphol 55:279–290
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bush, K.T., Lynch, F.J., DeNittis, A.S. et al. Neural tube formation in the mouse: a morphometric and computerized three-dimensional reconstruction study of the relationship between apical constriction of neuroepithelial cells and the shape of the neuroepithelium. Anat Embryol 181, 49–58 (1990). https://doi.org/10.1007/BF00189727
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00189727