Cell motility driving mediolateral intercalation in explants of Xenopus laevis

Development (Cambridge) - Tập 116 Số 4 - Trang 901-914 - 1992
John Shih1, Ray Keller2
1Department of Molecular and Cell Biology, University of California, Berkeley 94720.
2Division of Cell and Developmental Biology, Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA

Tóm tắt

ABSTRACT In Xenopus, convergence and extension are produced by active intercalation of the deep mesodermal cells between one another along the mediolateral axis (medi- olateral cell intercalation), to form a narrower, longer array. The cell motility driving this intercalation is poorly understood. A companion paper shows that the endodermal epithelium organizes the outermost meso- dermal cells immediately beneath it to undergo conver- gence and extension, and other evidence suggests that these deep cells are the most active participants in medi- olateral intercalation (Shih, J. and Keller, R. (1992) Development 116, 887-899). In this paper, we shave off the deeper layers of mesodermal cells, which allows us to observe the protrusive activity of the mesodermal cells next to the organizing epithelium with high reso- lution video microscopy. These mesodermal cells divide in the early gastrula and show rapid, randomly directed protrusive activity. At the early midgastrula stage, they begin to express a characteristic sequence of behaviors, called mediolateral intercalation behavior (MIB): (1) large, stable, filiform and lamelliform protrusions form in the lateral and medial directions, thus making the cells bipolar; (2) these protrusions are applied directly to adjacent cell surfaces and exert traction on them, without contact inhibition; (3) as a result, the cells elongate and align parallel to the mediolateral axis and perpendicular to the axis of extension; (4) the elongate, aligned cells intercalate between one another along the mediolateral axis, thus producing a longer, narrower array. Explants of essentially a single layer of deep mesodermal cells, made at stage 10.5, converge and extend by mediolateral intercalation. Thus by stage 10.5 (early midgastrula), expression of MIB among deep mesodermal cells is physiologically and mechanically independent of the organizing influence of the endoder- mal epithelium, described previously (Shih, J. and Keller, R. (1992) Development 116 887-899), and is the fundamental cell motility underlying mediolateral inter- calation and convergence and extension of the body axis.

Từ khóa


Tài liệu tham khảo

Abercrombie, 1970, Contact inhibition in tissue culture, In vitro, 6, 128, 10.1007/BF02616114

Bragg, 1938, The organization of the early embryo of Bufo Cognatus as revealed especially by the mitotic index, Z. Zellforsch. Mikrosk. Anat, 28, 154, 10.1007/BF00369008

Cooke, 1973, Properties of the primary organization field in the embryo of Xenopus laevis IV. Pattern formation and regulation following early inhibition of mitosis, J. Embryol. Exp. Morph, 30, 49

Dettlaff, 1964, Cell division, duration of interkinetic states, and differentiation in early stages of embryonic development, Adv. Morph, 3, 323, 10.1016/B978-1-4831-9950-4.50011-4

Foe, 1989, Mitotic domains reveal early commitment of cells in Drosophila embryos, Development, 107, 1, 10.1242/dev.107.1.1

Gimlich, 1985, Improved fluorescent compounds for tracing cell lineage, Dev. Biol, 109, 509, 10.1016/0012-1606(85)90476-2

Graham, 1966, Changes in the cell cycle during early amphibian development, Dev. Biol, 14, 439, 10.1016/0012-1606(66)90024-8

Hara, 1977, The cleavage pattern of the axolotl egg studied by cinematography and cell counting, Wilhelm Roux Arch. Dev. Biol, 181, 73, 10.1007/BF00857269

Holtfreter, 1943, A study of the mechanics of gastrulation. Part I, J. Exp. Zool, 94, 261, 10.1002/jez.1400940302

Ikushima, 1971, Structure and developmental tendency of the dorsal marginal zone in the early amphibian gastrula, J. Embryol. Exp. Morph, 25, 263

Jacobson, 1976, Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically, and by computer simulation, J. Exp. Zool, 197, 191, 10.1002/jez.1401970205

Jacobson, 1981, Morphogenesis of the neural plate and tube, In Morphogenesis and Pattern Formation, 223

Jacobson, 1986, Neurulation and the cortical tractor model for epithelial folding, J. Embryol. Exp. Morph, 96, 19

Kageyama, 1987, Mitotic behavior and pseudopodial activity of cells in the embryo of Oryzias latipes during blastula and gastrula stages, J. Exp. Zool, 244, 243, 10.1002/jez.1402440208

Kay, 1991, Methods in Cell Biology, Vol. 36: Xenopus laevis: Practical Uses in Cell and Molecular Biology

Keller, 1975, Vital dye mapping of the gastrula and neurula of Xenopus laevis. I. Prospective areas and morphogenetic movements of the superficial layer, Dev. Biol, 42, 222, 10.1016/0012-1606(75)90331-0

Keller, 1976, Vital dye mapping of the gastrula and neurula of Xenopus laevis. II. Prospective areas and morphogenetic movements of the deep layer, Dev. Biol, 51, 118, 10.1016/0012-1606(76)90127-5

Keller, 1980, The cellular basis of epiboly: An SEM study of deep-cell rearrangement during gastrulation in Xenopus laevis, J. Embryol. Exp. Morph, 60, 201

Keller, 1984, The cellular basis of gastrulation in Xenopus laevis: active post-involution convergence and extension by mediolateral interdigitation, Am. Zool, 24, 589, 10.1093/icb/24.3.589

Keller, 1986, The cellular basis of amphibian gastrulation, In Developmental Biology: A Comprehensive Synthesis. Vol. 2. The Cellular Basis of Morphogenesis, 10.1007/978-1-4613-2141-5_7

Keller, 1987, Cell rearrangement in morphogenesis, Zool. Sci, 4, 763

Keller, 1991, Early embryonic development of Xenopus laevis, In Methods in Cell Biology, Vol. 36: Xenopus laevis: Practical Uses in Cell and Molecular Biology, 61

Keller, 1985, Convergent extension by cell intercalation during gastrulation of Xenopus laevis, In Molecular Determinants of Animal Form, 111

Keller, 1985, The function of convergent extension during gastrulation of Xenopus laevis, J. Embryol. Exp. Morph, 89, 185

Keller, 1987, Cell behavior during active cell rearrangement: evidence and speculations, J. Cell Sci. Supplement, 8, 369, 10.1242/jcs.1987.Supplement_8.21

Keller, 1988, Regional expression, pattern and timing of convergence and extension during gastrulation of Xenopus laevis, Development, 103, 193, 10.1242/dev.103.1.193

Keller, 1989, Mediolateral cell intercalation in the dorsal axial mesoderm of Xenopuslaevis, Dev. Biol, 131, 539, 10.1016/S0012-1606(89)80024-7

Keller, 1989, Cell intercalation during notochord development in Xenopus laevis, J. Exp. Zool, 251, 134, 10.1002/jez.1402510204

Keller, 1989, Morphological polarity of intercalating deep mesodermal cells in the organiser of Xenopus laevis gastrulae, Proceedings of the 47th annual meeting of the Electron Microscopy Society of America, 840

Keller, 1991, Cell motility, control and function of convergence and extension during gastrulation in Xenopus, In Gastrulation: Movements, Patterns, and Molecules, 101, 10.1007/978-1-4684-6027-8_6

Keller, 1991, Pattern and function of cell motility and cell interactions during convergence and extension in Xenopus. In Cell-Cell Interactions in Early Development, 49th Symp. Soc. Dev. Biol, 31

Keller, 1992, The cellular basis of the convergence and extension of the Xenopus neural plate, Dev. Dynamics, 193, 199, 10.1002/aja.1001930302

Keller, 1992, Planar induction of convergence and extension of the neural plate by the organizer of Xenopus, Dev. Dynamics, 193, 218, 10.1002/aja.1001930303

Keller, 1992, The patterning and functioning of protrusive activity during convergence and extension of the Xenopus organiser, Development, 1992, 81, 10.1242/dev.116.Supplement.81

Keller, 1992, The cellular basis of amphibian gastrulation, In Current Topics in Developmental Biology, 10.1016/S0070-2153(08)60532-3

Keller, 1992, Xenopus gastrulation in absence of the blastocoel roof

Kintner, 1984, Monoclonal antibodies identify blastemal cells derived from dedifferentiating muscle in newt limb regeneration, Nature, 308, 67, 10.1038/308067a0

Mishell, 1980, Appendex A, Selected Methods in Cellular Immunology

Miyamoto, 1985, Formation of the notochord in living ascidian embryos, J. Embryol. Exp. Morph, 86, 1

Nakatsuji, 1983, Cell locomotion in vitro by Xenopus laevis gastrula mesodermal cells, J. Cell Sci, 59, 43, 10.1242/jcs.59.1.43

Satoh, 1977, ’Metachronous’ cleavage and initiation of gastrulation in amphibian embryos, Dev., Growth Differ, 19, 111, 10.1111/j.1440-169X.1977.00111.x

Schechtman, 1942, The mechanics of amphibian gastrulation. I. Gastrulation-producing interactions between various regions of an anuran egg (Hyla regilia), Univ. Calif. Publ. Zool, 51, 1

Schoenwolf, 1989, Roles of neuroepithelial cell rearrangement and division in shaping the avian neural plate, Development, 106, 427, 10.1242/dev.106.3.427

Shih, 1992, The epithelium of the dorsal marginal zone of Xenopus has organizer properties, Development, 116, xx, 10.1242/dev.116.4.887

Shih, 1992, Patterns of cell motility in the organizer and dorsal mesoderm ofXenopus, Development, 116, xx, 10.1242/dev.116.4.915

Spemann, 1938, Embryonic Development and Induction, 10.1097/00000441-193811000-00047

Thorogood, 1987, Analysis of in vivo cell movement using transparent tissue systems, J. Cell Sci. Supplement, 8, 395, 10.1242/jcs.1987.Supplement_8.22

Trinkaus, 1991, In vivo analysis of convergent cell movements in the germ ring of Fundulus, In Gastrulation: Movements, Patterns, and Molecules, 121, 10.1007/978-1-4684-6027-8_7

Trinkaus, 1992, On the convergent cell movements of gastrulation in Fundulus, J. Exp. Zool, 261, 40, 10.1002/jez.1402610107

Vogt, 1929, Gestaltanalyse am Amphibienkein mit ortlicher Vitalfarbung. II.Teil. Gastrulation und Mesodermbildung bei Urodelen und Anuren, Wilhelm Roux Arch. EntwMech. Org, 120, 384, 10.1007/BF02109667

Warga, 1990, Cell movements during epiboly and gastrulation in zebrafish, Development, 108, 569, 10.1242/dev.108.4.569

Weliky, 1992, Notochord morphogenesis in Xenopus laevis: simulation of behavior underlying tissue convergence and extension, Development, 113, 1231, 10.1242/dev.113.4.1231

Wilson, 1990, The development of axial mesoderm in Xenopuslaevis

Wilson, 1989, Cell rearrangement and segmentation in Xenopus: direct observation of cultured explants, Development, 105, 155, 10.1242/dev.105.1.155

Wilson, 1991, Cell rearrangement during gastrulation of Xenopus: direct observation of cultured explants, Development, 112, 289, 10.1242/dev.112.1.289

Winklbauer, 1990, Mesodermal cell migration during Xenopus gastrulation, Dev Biol, 142, 155, 10.1016/0012-1606(90)90159-G

Winklbauer, 1991, Directional mesoderm cell migration in the Xenopus gastrula, Dev. Biol, 148, 573, 10.1016/0012-1606(91)90275-8

Thông tin
Thông tin xuất bản

Development (Cambridge)

Tập 116 Số 4

901-914

Thông tin tác giả