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The Caenorhabditis elegans nonmuscle myosin genes nmy-1 and nmy-2 function as redundant components of the let-502/Rho-binding kinase and mel-11/myosin phosphatase pathway during embryonic morphogenesis

Title:

The Caenorhabditis elegans nonmuscle myosin genes nmy-1 and nmy-2 function as redundant components of the let-502/Rho-binding kinase and mel-11/myosin phosphatase pathway during embryonic morphogenesis

Piekny, Alisa J and Johnson, Jacque-Lynne F. and Cham, Gwendolyn D. (2003) The Caenorhabditis elegans nonmuscle myosin genes nmy-1 and nmy-2 function as redundant components of the let-502/Rho-binding kinase and mel-11/myosin phosphatase pathway during embryonic morphogenesis. Development, 130 (23). pp. 5695-5704. ISSN 0950-1991

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Official URL: http://dx.doi.org/10.1242/dev.00807

Abstract

Rho-binding kinase and the myosin phosphatase targeting subunit regulate nonmuscle contractile events in higher eukaryotes. Genetic evidence indicates that the C. elegans homologs regulate embryonic morphogenesis by controlling the actin-mediated epidermal cell shape changes that transform the spherical embryo into a long, thin worm. LET-502/Rho-binding kinase triggers elongation while MEL-11/myosin phosphatase targeting subunit inhibits this contractile event. We describe mutations in the nonmuscle myosin heavy chain gene nmy-1 that were isolated as suppressors of the mel-11 hypercontraction phenotype. However, a nmy-1 null allele displays elongation defects less severe than mutations in let-502 or in the single nonmuscle myosin light chain gene mlc-4. This results because nmy-1 is partially redundant with another nonmuscle myosin heavy chain, nmy-2, which was previously known only for its role in anterior/posterior polarity and cytokinesis in the early embryo. At the onset of elongation, NMY-1 forms filamentous-like structures similar to actin, and LET-502 is interspersed with these structures, where it may trigger contraction. MEL-11, which inhibits elongation, is initially cytoplasmic. In response to LET-502 activity, MEL-11 becomes sequestered away from the contractile apparatus, to the plasma membrane, when elongation commences. Upon completion of morphogenesis, MEL-11 again appears in the cytoplasm where it may halt actin/myosin contraction.

Divisions:Concordia University > Faculty of Arts and Science > Biology
Item Type:Article
Refereed:Yes
Authors:Piekny, Alisa J and Johnson, Jacque-Lynne F. and Cham, Gwendolyn D.
Journal or Publication:Development
Date:01 December 2003
Keywords:C. elegans, Rho-binding kinase, Myosin phosphatase, Nonmuscle myosin, Morphogenesis
ID Code:7629
Deposited By:DANIELLE DENNIE
Deposited On:30 May 2011 12:45
Last Modified:30 May 2011 12:45
References:
Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T.,Matsuura, Y. and Kaibuchi, K. (1996). Phosphorylation and Activation of Myosin by Rho-associated Kinase (Rho-kinase). J. Biol. Chem. 271,20246 -20249

Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.

Chin-Sang, I. D. and Chisholm, A. D. (2000). Form of the worm: genetics of epidermal morphogenesis in C. elegans.Trends Genet. 16,544 -551.

Costa, M., Raich, W., Agbunag, C., Leung, B., Hardin, J. and Priess, J. R. (1998). A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J. Cell Biol. 141,297 -308.

Cuenca, A. A., Schetter, A., Aceto, D., Kemphues, K. and Seydoux, G. (2003). Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130,1255 -1265.

Edgley, M., Baillie, D. L., Riddle, D. L. and Rose, A. M. (1995). Genetic balancers. In Caenorhabditis elegans: Modern Biological Analysis of an Organism (ed. H. F. Epstein and D. C. Shakes), pp. 147-184. San Diego: Academic Press.

Edwards, K. A. and Kiehart, D. P. (1996). Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis. Development 122,1499 -1511.

Fire, A., Xu, S., Montgomery, M. K., Kosatas, S. A., Driver, S. E. andMello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans.Nature 391,806 -811.

Fraser, A. G., Kamath, R. S., Zipperlen, P., Martinez-Campos, M.,Sohrmann, M. and Ahringer, J. (2000). Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408,325 -330.

Guo, S. and Kemphues, K. J. (1996). A non-muscle myosin required for embryonic polarity in Caenorhabditis elegans. Nature 382,455 -458.

Hill, A. A., Hunter, C. P., Tsung, B. T., Tucker-Kellogg, G. and Brown, E.L. (2000). Genomic analysis of gene expression in C. elegans. Science 290,809 -812.

Hodgkin, J. (1997) Genetics. In C. elegans II (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer and J. R. Priess), pp. 881-1047. New York: Cold Spring Harbor Press.

Horvitz, H. R., Brenner, S., Hodgkin, J. and Herman, R. K. (1979). A uniform genetic nomenclature for the nematode Caenorhabditis elegans. Mol. Gen. Genet. 175,129 -133.

Horvitz, H. R. and Sulston, J. E. (1980). Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans. Genetics 96,435 -454.

Jordan, P. and Karess, R. (1997). Myosin light chain-activating phosphorylation sites are required for oogenesis in Drosophila. J. Cell Biol. 139,1805 -1819.

Kaibuchi, K., Kuroda, S. and Amano, M. (1999). Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 68,459 -486.

Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., Gotta, M.,Kanapin, A., le Bot, N., Moreno, S., Sohrmann, M. et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421,232 -237.

Mains, P. E., Sulston, I. A. and Wood, W. B. (1990). Dominant maternal-effect mutations causing embryonic lethality in Caenorhabditis elegans. Genetics 125,351 -369.

Mansfield, S. G., al-Shirawi, D. Y., Ketchum, A. S., Newbern, E. C. andKiehart, D. P. (1996). Molecular organization and alternative splicing in zipper, the gene that encodes the Drosophila non-muscle myosin II heavy chain. J. Mol. Biol. 255,98 -109.

McKeown, C., Praitis, V. and Austin, J. (1998). sma-1 encodes a βH-spectrin homolog required for Caenorhabditis elegans morphogenesis. Development 125,2087 -2098.

Mizuno, T., Tsutsui, K. and Nishida, Y. (2002). Drosophila myosin phosphatase and its role in dorsal closure. Development 129,1215 -1223.

Norman, K. R. and Moerman, D. G. (2002).α spectrin is essential for morphogenesis and body wall muscle formation in Caenorhabditis elegans. J. Cell Biol. 157,665 -667.

Pfitzer, G. (2001). Signal transduction in smooth muscle. Invited review: regulation of myosin phosphorylation in smooth muscle. J. Appl. Physiol. 91,497 -503.

Philips, C. L., Yamakawa, K. and Adelstein, R. S. (1995). Cloning of the cDNA encoding human nonmuscle myosin heavy chain-B and analysis of human tissues with isoform-specific antibodies. J. Muscle Res. Cell Motil. 16,379 -389.

Piekny, A. J., Wissmann, A. and Mains, P. E. (2000). Embryonic morphogenesis in Caenorhabditis elegans integrates the activity of LET-502 Rho-binding kinase, MEL-11 myosin phosphatase, DAF-2 insulin receptor and FEM-2 PP2c phosphatase. Genetics 156,1671 -1689.

Piekny, A. J. and Mains, P. E. (2002). Rho-binding kinase (LET-502) and myosin phosphatase (MEL-11) regulate cytokinesis in the early Caenorhabditis elegans embryo. J. Cell Sci. 115,2271 -2282.

Priess, J. R. and Hirsh, D. I. (1986). Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev. Biol. 117,156 -173.

Shelton, C. A., Carter, J. C., Ellis, G. C. and Bowerman, B. (1999). The nonmuscle myosin regulatory light chain gene mlc-4 is required for cytokinesis, anterior-posterior polarity, and body morphology during Caenorhabditis elegans embryogenesis. J. Cell Biol. 146,439 -451.

Shin, H. M., Je, H. D., Gallant, C., Tao, T. C., Hartshorne, D. J., Ito, M. and Morgan, K. G. (2002). Differential association and localization of myosin phosphatase subunits during agonist-induced signal transduction in smooth muscle. Circ. Res. 90,546 -553.

Simske, J. S. and Hardin, J. (2001). Getting into shape: epidermal morphogenesis in Caenorhabditis elegans embryos. BioEssays 23,12 -23.

Somlyo, A. P. and Somlyo, A. V. (2000). Signal transduction by G-proteins, Rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J. Physiol. 522,177 -185.

Tabara, H., Sarkissian, M., Kelly, W. G., Fleenor, J., Grishok, A.,Timmons, L., Fire, A. and Mello, C. C. (1999). The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99,123 -132.

Tan, C., Stronach, B. and Perrimon, N. (2003). Roles of myosin phosphatase during Drosophila development. Development 130,671 -681.

Trybus, K. M. (1996). Myosin regulation and assembly. In Biochemistry of Smooth Muscle Contraction (ed. M. Barany), pp. 37-45. San Diego: Academic Press.

Wheatley, S., Kulkarni, S. and Karess, R. (1995). Drosophila nonmuscle myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos. Development 121,1937 -1946.

Wicks, S. R., Yeh, R. T., Gish, W. R., Waterston, R. H. and Plasterk, R.H. (2001). Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28,160 -164.

Winter, C. G., Wang, B., Ballew, A., Royou, A., Karess, R., Axelrod, J. D. and Luo, L. (2001). Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105, 81-91.

Wissmann, A., Ingles, J., McGhee, J. D. and Mains, P. E. (1997). Caenorhabditis elegans LET-502 is related to Rho-binding kinases and human myotonic dystrophy kinase and interacts genetically with a homolog of the regulatory subunit of smooth muscle myosin phosphatase to affect cell shape. Genes Dev. 11,409 -422.

Wissmann, A., Ingles, J. and Mains, P. E. (1999). The Caenorhabditis elegans mel-11 myosin phosphatase regulatory subunit affects tissue contraction in the somatic gonad and the embryonic epidermis and genetically interacts with the Rac signaling pathway. Dev. Biol. 209,111 -127.

Young, P. E., Richman, A. M., Ketchum, A. S. and Kiehart, D. P. (1993). Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 7, 29-41.
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