Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans

doi:10.1083/jcb.105.5.2123

This Article

	Full Text (PDF, 3833K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Hyman, A. A.
	Articles by White, J. G.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Hyman, A. A.
	Articles by White, J. G.


Social Bookmarking

	What's this?

ARTICLES

Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans

AA Hyman and JG White
Medical Research Council, Laboratory of Molecular Biology, Cambridge, England.

The establishment of cell division axes was examined in the early embryonic divisions of Caenorhabditis elegans. It has been shown previously that there are two different patterns of cleavage during early embryogenesis. In one set of cells, which undergo predominantly determinative divisions, the division axes are established successively in the same orientation, while division axes in the other set, which divide mainly proliferatively, have an orthogonal pattern of division. We have investigated the establishment of these axes by following the movement of the centrosomes. Centrosome separation follows a reproducible pattern in all cells, and this pattern by itself results in an orthogonal pattern of cleavage. In those cells that divide on the same axis, there is an additional directed rotation of pairs of centrosomes together with the nucleus through well-defined angles. Intact microtubules are required for rotation; rotation is prevented by inhibitors of polymerization and depolymerization of microtubules. We have examined the distribution of microtubules in fixed embryos during rotation. From these and other data we infer that microtubules running from the centrosome to the cortex have a central role in aligning the centrosome-nuclear complex.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Kieserman, E. K., Wallingford, J. B. (2009). In vivo imaging reveals a role for Cdc42 in spindle positioning and planar orientation of cell divisions during vertebrate neural tube closure. J. Cell Sci. 122: 2481-2490 [Abstract] [Full Text]
Zhang, H., Skop, A. R., White, J. G. (2008). Src and Wnt signaling regulate dynactin accumulation to the P2-EMS cell border in C. elegans embryos. J. Cell Sci. 121: 155-161 [Abstract] [Full Text]
Tsai, M.-C., Ahringer, J. (2007). Microtubules are involved in anterior-posterior axis formation in C. elegans embryos. JCB 179: 397-402 [Abstract] [Full Text]
Dinkelmann, M. V., Zhang, H., Skop, A. R., White, J. G. (2007). SPD-3 Is Required for Spindle Alignment in Caenorhabditis elegans Embryos and Localizes to Mitochondria. Genetics 177: 1609-1620 [Abstract] [Full Text]
Goulding, M. B., Canman, J. C., Senning, E. N., Marcus, A. H., Bowerman, B. (2007). Control of nuclear centration in the C. elegans zygote by receptor-independent G{alpha} signaling and myosin II. JCB 178: 1177-1191 [Abstract] [Full Text]
Lyczak, R., Zweier, L., Group, T., Murrow, M. A., Snyder, C., Kulovitz, L., Beatty, A., Smith, K., Bowerman, B. (2006). The puromycin-sensitive aminopeptidase PAM-1 is required for meiotic exit and anteroposterior polarity in the one-cell Caenorhabditis elegans embryo. Development 133: 4281-4292 [Abstract] [Full Text]
DeBella, L. R., Hayashi, A., Rose, L. S. (2006). LET-711, the Caenorhabditis elegans NOT1 Ortholog, Is Required for Spindle Positioning and Regulation of Microtubule Length in Embryos. Mol. Biol. Cell 17: 4911-4924 [Abstract] [Full Text]
Patalano, S., Pruliere, G., Prodon, F., Paix, A., Dru, P., Sardet, C., Chenevert, J. (2006). The aPKC-PAR-6-PAR-3 cell polarity complex localizes to the centrosome attracting body, a macroscopic cortical structure responsible for asymmetric divisions in the early ascidian embryo. J. Cell Sci. 119: 1592-1603 [Abstract] [Full Text]
Leslie, M. (2006). Centrosome choreography. JCB 172: 328-328 [Full Text]
Lu, C., Mains, P. E. (2005). Mutations of a Redundant {alpha}-Tubulin Gene Affect Caenorhabditis elegans Early Embryonic Cleavage via MEI-1/Katanin-Dependent and -Independent Pathways. Genetics 170: 115-126 [Abstract] [Full Text]
Encalada, S. E., Willis, J., Lyczak, R., Bowerman, B. (2005). A Spindle Checkpoint Functions during Mitosis in the Early Caenorhabditis elegans Embryo. Mol. Biol. Cell 16: 1056-1070 [Abstract] [Full Text]
Schmidt, D. J., Rose, D. J., Saxton, W. M., Strome, S. (2005). Functional Analysis of Cytoplasmic Dynein Heavy Chain in Caenorhabditis elegans with Fast-acting Temperature-sensitive Mutations. Mol. Biol. Cell 16: 1200-1212 [Abstract] [Full Text]
Labbe, J.-C., McCarthy, E. K., Goldstein, B. (2004). The forces that position a mitotic spindle asymmetrically are tethered until after the time of spindle assembly. JCB 167: 245-256 [Abstract] [Full Text]
Ogawa, S., Matsubayashi, Y., Nishida, E. (2004). An evolutionarily conserved gene required for proper microtubule architecture in Caenorhabditis elegans. GENES CELLS 9: 83-93 [Abstract] [Full Text]
Ellis, G. C., Phillips, J. B., O'Rourke, S., Lyczak, R., Bowerman, B. (2004). Maternally expressed and partially redundant {beta}-tubulins in Caenorhabditis elegans are autoregulated. J. Cell Sci. 117: 457-464 [Abstract] [Full Text]
Lu, C., Srayko, M., Mains, P. E. (2004). The Caenorhabditis elegans Microtubule-severing Complex MEI-1/MEI-2 Katanin Interacts Differently with Two Superficially Redundant {beta}-Tubulin Isotypes. Mol. Biol. Cell 15: 142-150 [Abstract] [Full Text]
Tsou, M.-F. B., Hayashi, A., Rose, L. S. (2003). LET-99 opposes G{alpha}/GPR signaling to generate asymmetry for spindle positioning in response to PAR and MES-1/SRC-1 signaling. Development 130: 5717-5730 [Abstract] [Full Text]
Bergmann, D. C., Lee, M., Robertson, B., Tsou, M.-F. B., Rose, L. S., Wood, W. B. (2003). Embryonic handedness choice in C. elegans involves the G{alpha} protein GPA-16. Development 130: 5731-5740 [Abstract] [Full Text]
Wright, A. J., Hunter, C. P. (2003). Mutations in a {beta}-Tubulin Disrupt Spindle Orientation and Microtubule Dynamics in the Early Caenorhabditis elegans Embryo. Mol. Biol. Cell 14: 4512-4525 [Abstract] [Full Text]
Yamashita, Y. M., Jones, D. L., Fuller, M. T. (2003). Orientation of Asymmetric Stem Cell Division by the APC Tumor Suppressor and Centrosome. Science 301: 1547-1550 [Abstract] [Full Text]
Cayouette, M., Raff, M. (2003). The orientation of cell division influences cell-fate choice in the developing mammalian retina. Development 130: 2329-2339 [Abstract] [Full Text]
Severson, A. F., Bowerman, B. (2003). Myosin and the PAR proteins polarize microfilament-dependent forces that shape and position mitotic spindles in Caenorhabditis elegans. JCB 161: 21-26 [Abstract] [Full Text]
Tsou, M.-F. B., Ku, W., Hayashi, A., Rose, L. S. (2003). PAR-dependent and geometry-dependent mechanisms of spindle positioning. JCB 160: 845-855 [Abstract] [Full Text]
Haydar, T. F., Ang, E. Jr., Rakic, P. (2003). Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc. Natl. Acad. Sci. USA 100: 2890-2895 [Abstract] [Full Text]
Ji, J.-Y., Haghnia, M., Trusty, C., Goldstein, L. S. B., Schubiger, G. (2002). A Genetic Screen for Suppressors and Enhancers of the Drosophila Cdk1-Cyclin B Identifies Maternal Factors That Regulate Microtubule and Microfilament Stability. Genetics 162: 1179-1195 [Abstract] [Full Text]
Gruneberg, U., Glotzer, M., Gartner, A., Nigg, E. A. (2002). The CeCDC-14 phosphatase is required for cytokinesis in the Caenorhabditis elegans embryo. JCB 158: 901-914 [Abstract] [Full Text]
Bulgheresi, S., Kleiner, E., Knoblich, J. A. (2002). Inscuteable-dependent apical localization of the microtubule-binding protein Cornetto suggests a role in asymmetric cell division. J. Cell Sci. 114: 3655-3662 [Abstract] [Full Text]
Tsou, M.-F. B., Hayashi, A., DeBella, L. R., McGrath, G., Rose, L. S. (2002). LET-99 determines spindle position and is asymmetrically enriched in response to PAR polarity cues in C. elegans embryos. Development 129: 4469-4481 [Abstract] [Full Text]
Kaltschmidt, J. A., Brand, A. H. (2002). Asymmetric cell division: microtubule dynamics and spindle asymmetry. J. Cell Sci. 115: 2257-2264 [Abstract] [Full Text]
Yamamoto, A., Tsutsumi, C., Kojima, H., Oiwa, K., Hiraoka, Y. (2001). Dynamic Behavior of Microtubules during Dynein-dependent Nuclear Migrations of Meiotic Prophase in Fission Yeast. Mol. Biol. Cell 12: 3933-3946 [Abstract] [Full Text]
Gomes, J.-E., Encalada, S. E., Swan, K. A., Shelton, C. A., Carter, J. C., Bowerman, B. (2001). The maternal gene spn-4 encodes a predicted RRM protein required for mitotic spindle orientation and cell fate patterning in early C. elegans embryos. Development 128: 4301-4314 [Abstract] [Full Text]
Caron, J. M., Vega, L. R., Fleming, J., Bishop, R., Solomon, F. (2001). Single Site alpha -Tubulin Mutation Affects Astral Microtubules and Nuclear Positioning during Anaphase in Saccharomyces cerevisiae: Possible Role for Palmitoylation of alpha -Tubulin. Mol. Biol. Cell 12: 2672-2687 [Abstract] [Full Text]
Cayouette, M., Whitmore, A. V., Jeffery, G., Raff, M. (2001). Asymmetric Segregation of Numb in Retinal Development and the Influence of the Pigmented Epithelium. J. Neurosci. 21: 5643-5651 [Abstract] [Full Text]
Ni, L., Snyder, M. (2001). A Genomic Study of the Bipolar Bud Site Selection Pattern in Saccharomyces cerevisiae. Mol. Biol. Cell 12: 2147-2170 [Abstract] [Full Text]
Schuyler, S., Pellman, D (2001). Search, capture and signal: games microtubules and centrosomes play. J. Cell Sci. 114: 247-255 [Abstract]
Miller, K. G., Rand, J. B. (2000). A Role for RIC-8 (Synembryn) and GOA-1 (Go{alpha}) in Regulating a Subset of Centrosome Movements During Early Embryogenesis in Caenorhabditis elegans. Genetics 156: 1649-1660 [Abstract] [Full Text]
Jantsch-Plunger, V., Gonczy, P., Romano, A., Schnabel, H., Hamill, D., Schnabel, R., Hyman, A. A., Glotzer, M. (2000). Cyk-4: A Rho Family Gtpase Activating Protein (Gap) Required for Central Spindle Formation and Cytokinesis. JCB 149: 1391-1404 [Abstract] [Full Text]
Pichler, S., Gonczy, P., Schnabel, H., Pozniakowski, A., Ashford, A., Schnabel, R., Hyman, A. A. (2000). OOC-3, a novel putative transmembrane protein required for establishment of cortical domains and spindle orientation in the P(1) blastomere of C. elegans embryos. Development 127: 2063-2073 [Abstract]
O'Connell, C. B., Wang, Y.-l. (2000). Mammalian Spindle Orientation and Position Respond to Changes in Cell Shape in a Dynein-dependent Fashion. Mol. Biol. Cell 11: 1765-1774 [Abstract] [Full Text]
Heil-Chapdelaine, R. A., Tran, N. K., Cooper, J. A. (2000). Dynein-dependent Movements of the Mitotic Spindle in Saccharomyces cerevisiae Do Not Require Filamentous Actin. Mol. Biol. Cell 11: 863-872 [Abstract] [Full Text]
Segal, M., Clarke, D. J., Maddox, P., Salmon, E.D., Bloom, K., Reed, S. I. (2000). Coordinated Spindle Assembly and Orientation Requires Clb5p-Dependent Kinase in Budding Yeast. JCB 148: 441-452 [Abstract] [Full Text]
Bobinnec, Y, Fukuda, M, Nishida, E (2000). Identification and characterization of Caenorhabditis elegans gamma-tubulin in dividing cells and differentiated tissues. J. Cell Sci. 113: 3747-3759 [Abstract]
Schaerer-Brodbeck, C, Riezman, H (2000). Saccharomyces cerevisiae Arc35p works through two genetically separable calmodulin functions to regulate the actin and tubulin cytoskeletons. J. Cell Sci. 113: 521-532 [Abstract]
Gonczy, P., Pichler, S., Kirkham, M., Hyman, A. A. (1999). Cytoplasmic Dynein Is Required for Distinct Aspects of Mtoc Positioning, Including Centrosome Separation, in the One Cell Stage Caenorhabditis elegans Embryo. JCB 147: 135-150 [Abstract] [Full Text]
Schlesinger, A., Shelton, C. A., Maloof, J. N., Meneghini, M., Bowerman, B. (1999). Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. Genes Dev. 13: 2028-2038 [Abstract] [Full Text]
Gonczy, P., Schnabel, H., Kaletta, T., Amores, A. D., Hyman, T., Schnabel, R. (1999). Dissection of Cell Division Processes in the One Cell Stage Caenorhabditis elegans Embryo by Mutational Analysis. JCB 144: 927-946 [Abstract] [Full Text]
Lee, L., Klee, S. K., Evangelista, M., Boone, C., Pellman, D. (1999). Control of Mitotic Spindle Position by the Saccharomyces cerevisiae Formin Bni1p. JCB 144: 947-961 [Abstract] [Full Text]
Miller, R. K., Matheos, D., Rose, M. D. (1999). The Cortical Localization of the Microtubule Orientation Protein, Kar9p, Is Dependent upon Actin and Proteins Required for Polarization. JCB 144: 963-975 [Abstract] [Full Text]
Gallagher, K, Smith, L. (1999). discordia mutations specifically misorient asymmetric cell divisions during development of the maize leaf epidermis. Development 126: 4623-4633 [Abstract]
Hawkins, N., Garriga, G. (1998). Asymmetric cell division: from A to Z. Genes Dev. 12: 3625-3638 [Full Text]
Sawin, K. E., Nurse, P. (1998). Regulation of Cell Polarity by Microtubules in Fission Yeast. JCB 142: 457-471 [Abstract] [Full Text]
O'Connell, K. F., Leys, C. M., White, J. G. (1998). A Genetic Screen for Temperature-Sensitive Cell-Division Mutants of Caenorhabditis elegans. Genetics 149: 1303-1321 [Abstract] [Full Text]
de Saint Phalle, B., Sullivan, W. (1998). Spindle Assembly and Mitosis without Centrosomes in Parthenogenetic Sciara Embryos. JCB 141: 1383-1391 [Abstract] [Full Text]
Giansanti, M. G., Bonaccorsi, S., Williams, B., Williams, E. V., Santolamazza, C., Goldberg, M. L., Gatti, M. (1998). Cooperative interactions between the central spindle and the contractile ring during Drosophila cytokinesis. Genes Dev. 12: 396-410 [Abstract] [Full Text]
Schumacher, J., Ashcroft, N, Donovan, P., Golden, A (1998). A highly conserved centrosomal kinase, AIR-1, is required for accurate cell cycle progression and segregation of developmental factors in Caenorhabditis elegans embryos. Development 125: 4391-4402 [Abstract]
Keating, H., White, J. (1998). Centrosome dynamics in early embryos of Caenorhabditis elegans. J. Cell Sci. 111: 3027-3033 [Abstract]
Hyman, A, Karsenti, E (1998). The role of nucleation in patterning microtubule networks. J. Cell Sci. 111: 2077-2083 [Abstract]
Reinsch, S, Gonczy, P (1998). Mechanisms of nuclear positioning. J. Cell Sci. 111: 2283-2295 [Abstract]
Neujahr, R, Albrecht, R, Kohler, J, Matzner, M, Schwartz, J., Westphal, M, Gerisch, G (1998). Microtubule-mediated centrosome motility and the positioning of cleavage furrows in multinucleate myosin II-null cells. J. Cell Sci. 111: 1227-1240 [Abstract]
Rose, L., Kemphues, K (1998). The let-99 gene is required for proper spindle orientation during cleavage of the C. elegans embryo. Development 125: 1337-1346 [Abstract]
Ding, D., Chikashige, Y, Haraguchi, T, Hiraoka, Y (1998). Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules, as revealed by continuous observation of chromosomes and microtubules in living cells. J. Cell Sci. 111: 701-712 [Abstract]
Voronov, D., Panchin, Y. (1998). Cell lineage in marine nematode Enoplus brevis. Development 125: 143-150 [Abstract]
Shaw, S. L., Yeh, E., Maddox, P., Salmon, E.D., Bloom, K. (1997). Astral Microtubule Dynamics in Yeast: A Microtubule-based Searching Mechanism for Spindle Orientation and Nuclear Migration into the Bud. JCB 139: 985-994 [Abstract] [Full Text]
Helmstetter, C. E. (1997). Gravity and the orientation of cell�division. Proc. Natl. Acad. Sci. USA 94: 10195-10198 [Abstract] [Full Text]
Stearns, T. (1997). Motoring to the Finish: Kinesin and Dynein Work Together to Orient the Yeast Mitotic Spindle. JCB 138: 957-960 [Full Text]
DeZwaan, T. M., Ellingson, E., Pellman, D., Roof, D. M. (1997). Kinesin-related KIP3 of Saccharomyces cerevisiae Is Required for a Distinct Step in Nuclear Migration. JCB 138: 1023-1040 [Abstract] [Full Text]
Cottingham, F. R., Hoyt, M. A. (1997). Mitotic Spindle Positioning in Saccharomyces cerevisiae Is Accomplished by Antagonistically Acting Microtubule Motor Proteins. JCB 138: 1041-1053 [Abstract] [Full Text]
Carminati, J. L., Stearns, T. (1997). Microtubules Orient the Mitotic Spindle in Yeast through Dynein-dependent Interactions with the Cell Cortex. JCB 138: 629-641 [Abstract] [Full Text]
Wheatley, S. P., Hinchcliffe, E. H., Glotzer, M., Hyman, A. A., Sluder, G., Wang, Y.-l. (1997). CDK1 Inactivation Regulates Anaphase Spindle Dynamics and Cytokinesis In Vivo. JCB 138: 385-393 [Abstract] [Full Text]
Morris, S. M., Anaya, P., Xiang, X., Morris, N. R., May, G. S., Yu-Lee, L.-y. (1997). A Prolactin-Inducible T Cell Gene Product Is Structurally Similar to the Aspergillus nidulans Nuclear Movement Protein NUDC. Mol. Endocrinol. 11: 229-236 [Abstract] [Full Text]
Yang, S., Ayscough, K. R., Drubin, D. G. (1997). A Role for the Actin Cytoskeleton of Saccharomyces cerevisiae in Bipolar Bud-Site Selection. JCB 136: 111-123 [Abstract] [Full Text]
Bowerman, B, Ingram, M., Hunter, C. (1997). The maternal par genes and the segregation of cell fate specification activities in early Caenorhabditis elegans embryos. Development 124: 3815-3826 [Abstract]
Wang, S., Griffin, F., Clark, W. (1997). Cell-cell association directed mitotic spindle orientation in the early development of the marine shrimp Sicyonia ingentis. Development 124: 773-780 [Abstract]
Adams, R. J. (1996). Metaphase Spindles Rotate in the Neuroepithelium of Rat Cerebral Cortex. J. Neurosci. 16: 7610-7618 [Abstract] [Full Text]
Roemer, T, Madden, K, Chang, J, Snyder, M (1996). Selection of axial growth sites in yeast requires Axl2p, a novel plasma membrane glycoprotein.. Genes Dev. 10: 777-793 [Abstract]
Watts, J., Etemad-Moghadam, B, Guo, S, Boyd, L, Draper, B., Mello, C., Priess, J., Kemphues, K. (1996). par-6, a gene involved in the establishment of asymmetry in early C. elegans embryos, mediates the asymmetric localization of PAR-3. Development 122: 3133-3140 [Abstract]
Fishkind, D., Silverman, J., Wang, Y. (1996). Function of spindle microtubules in directing cortical movement and actin filament organization in dividing cultured cells. J. Cell Sci. 109: 2041-2051 [Abstract]
Mickey, K., Mello, C., Montgomery, M., Fire, A, Priess, J. (1996). An inductive interaction in 4-cell stage C. elegans embryos involves APX-1 expression in the signalling cell. Development 122: 1791-1798 [Abstract]
Goldstein, B, Hird, S. (1996). Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122: 1467-1474 [Abstract]
Hird, S., Paulsen, J., Strome, S (1996). Segregation of germ granules in living Caenorhabditis elegans embryos: cell-type-specific mechanisms for cytoplasmic localisation. Development 122: 1303-1312 [Abstract]
Bissen, S., Smith, C. (1996). Unequal cleavage in leech embryos: zygotic transcription is required for correct spindle orientation in subset of early blastomeres. Development 122: 599-606 [Abstract]
Esteban, M., Giovinazzo, G, Goday, C (1995). Chromatin diminution is strictly correlated to somatic cell behavior in early development of the nematode Parascaris univalens. J. Cell Sci. 108: 2393-2404 [Abstract]
Cooley, L, Theurkauf, W. (1994). Cytoskeletal functions during Drosophila oogenesis. Science 266: 590-596 [Abstract]
Mango, S., Thorpe, C., Martin, P., Chamberlain, S., Bowerman, B (1994). Two maternal genes, apx-1 and pie-1, are required to distinguish the fates of equivalent blastomeres in the early Caenorhabditis elegans embryo. Development 120: 2305-2315 [Abstract]
Waddle, J., Cooper, J., Waterston, R. (1994). Transient localized accumulation of actin in Caenorhabditis elegans blastomeres with oriented asymmetric divisions. Development 120: 2317-2328 [Abstract]
Jimenez, M, Goday, C (1993). A centrosome-associated antibody from Drosophila melanogaster reveals a new microtubule-dependent structure in the equatorial zone of Parascaris univalens embryos. J. Cell Sci. 106: 719-730 [Abstract]
Kellogg, D.R., Sullivan, W., Theurkauf, W., Oegema, K., Raff, J.W., Alberts, B.M. (1991). Studies on the Centrosome and Cytoplasmic Organization in the Early Drosophila Embryo. Cold Spring Harb Symp Quant Biol 56: 649-662 [Abstract]
Kenyon, C (1988). The nematode Caenorhabditis elegans. Science 240: 1448-1453 [Abstract]