Development, Vol 100, Issue 3 365-382, Copyright © 1987 by Company of Biologists

JOURNAL ARTICLES

Genetics of cell and axon migrations in Caenorhabditis elegans

EM Hedgecock, JG Culotti, DH Hall and BD Stern
Department of Cell Biology, Roche Institute of Molecular Biology, Nutley, New Jersey 07110.

The Caenorhabditis elegans epidermis comprises 78 cells which cover the external surface of the embryo as a single cell layer. These cells secrete the cuticle from their exterior faces and support the body wall muscles and most of the nervous system on their interior faces. The epidermal cells arise by autonomous embryonic cell lineages but show regulative interactions after their assembly into an epithelium. It is believed that the various epidermal cells express different kinds or amounts of surface molecules that govern their mutual assembly and also guide the attachments and migrations of the underlying body muscles and neurones. The first muscles and neurones may in turn express new surface molecules that refine later cell movements. Mutations in some 30 known genes disrupt the movements of cells or axons along the body wall.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				T. Kawano, H. Zheng, D. C. Merz, Y. Kohara, K. K. Tamai, K. Nishiwaki, and J. G. Culotti C. elegans mig-6 encodes papilin isoforms that affect distinct aspects of DTC migration, and interacts genetically with mig-17 and collagen IV Development, May 1, 2009; 136(9): 1433 - 1442. [Abstract] [Full Text] [PDF]

				M. Alexander, K. K. M. Chan, A. B. Byrne, G. Selman, T. Lee, J. Ono, E. Wong, R. Puckrin, S. J. Dixon, and P. J. Roy An UNC-40 pathway directs postsynaptic membrane extension in Caenorhabditis elegans Development, March 15, 2009; 136(6): 911 - 922. [Abstract] [Full Text] [PDF]

				Y. Kubota, K. Ohkura, K. K. Tamai, K. Nagata, and K. Nishiwaki MIG-17/ADAMTS controls cell migration by recruiting nidogen to the basement membrane in C. elegans PNAS, December 30, 2008; 105(52): 20804 - 20809. [Abstract] [Full Text] [PDF]

				A. Y. Zinovyeva, Y. Yamamoto, H. Sawa, and W. C. Forrester Complex Network of Wnt Signaling Regulates Neuronal Migrations During Caenorhabditis elegans Development Genetics, July 1, 2008; 179(3): 1357 - 1371. [Abstract] [Full Text] [PDF]

				S. Patrakitkomjorn, D. Kobayashi, T. Morikawa, M. M. Wilson, N. Tsubota, A. Irie, T. Ozawa, M. Aoki, N. Arimura, K. Kaibuchi, et al. Neurofibromatosis Type 1 (NF1) Tumor Suppressor, Neurofibromin, Regulates the Neuronal Differentiation of PC12 Cells via Its Associating Protein, CRMP-2 J. Biol. Chem., April 4, 2008; 283(14): 9399 - 9413. [Abstract] [Full Text] [PDF]

				S. L. Williams, S. Lutz, N. K. Charlie, C. Vettel, M. Ailion, C. Coco, J. J.G. Tesmer, E. M. Jorgensen, T. Wieland, and K. G. Miller Trio's Rho-specific GEF domain is the missing G{alpha}q effector in C. elegans Genes & Dev., November 1, 2007; 21(21): 2731 - 2746. [Abstract] [Full Text] [PDF]

				A. K. Mah, K. R. Armstrong, D. S. Chew, J. S. Chu, D. K. Tu, R. C. Johnsen, N. Chen, H. M. Chamberlin, and D. L. Baillie Transcriptional Regulation of AQP-8, a Caenorhabditis elegans Aquaporin Exclusively Expressed in the Excretory System, by the POU Homeobox Transcription Factor CEH-6 J. Biol. Chem., September 21, 2007; 282(38): 28074 - 28086. [Abstract] [Full Text] [PDF]

				S. Cordes, C. A. Frank, and G. Garriga The C. elegans MELK ortholog PIG-1 regulates cell size asymmetry and daughter cell fate in asymmetric neuroblast divisions Development, July 15, 2006; 133(14): 2747 - 2756. [Abstract] [Full Text] [PDF]

				R. W. Burgess, T. J. Jucius, and S. L. Ackerman Motor Axon Guidance of the Mammalian Trochlear and Phrenic Nerves: Dependence on the Netrin Receptor Unc5c and Modifier Loci J. Neurosci., May 24, 2006; 26(21): 5756 - 5766. [Abstract] [Full Text] [PDF]

				B. L. Chen, D. H. Hall, and D. B. Chklovskii Wiring optimization can relate neuronal structure and function PNAS, March 21, 2006; 103(12): 4723 - 4728. [Abstract] [Full Text] [PDF]

				Y. Kubota, M. Sano, S. Goda, N. Suzuki, and K. Nishiwaki The conserved oligomeric Golgi complex acts in organ morphogenesis via glycosylation of an ADAM protease in C. elegans Development, January 15, 2006; 133(2): 263 - 273. [Abstract] [Full Text] [PDF]

				B. Itoh, T. Hirose, N. Takata, K. Nishiwaki, M. Koga, Y. Ohshima, and M. Okada SRC-1, a non-receptor type of protein tyrosine kinase, controls the direction of cell and growth cone migration in C. elegans Development, December 1, 2005; 132(23): 5161 - 5172. [Abstract] [Full Text] [PDF]

				C. Rhiner, S. Gysi, E. Frohli, M. O. Hengartner, and A. Hajnal Syndecan regulates cell migration and axon guidance in C. elegans Development, October 15, 2005; 132(20): 4621 - 4633. [Abstract] [Full Text] [PDF]

				J. M. Muriel, C. Dong, H. Hutter, and B. E. Vogel Fibulin-1C and Fibulin-1D splice variants have distinct functions and assemble in a hemicentin-dependent manner Development, October 1, 2005; 132(19): 4223 - 4234. [Abstract] [Full Text] [PDF]

				G. Dalpe, L. Brown, and J. G. Culotti Vulva morphogenesis involves attraction of plexin 1-expressing primordial vulva cells to semaphorin 1a sequentially expressed at the vulva midline Development, March 15, 2005; 132(6): 1387 - 1400. [Abstract] [Full Text] [PDF]

				T. Kinnunen, Z. Huang, J. Townsend, M. M. Gatdula, J. R. Brown, J. D. Esko, and J. E. Turnbull Heparan 2-O-sulfotransferase, hst-2, is essential for normal cell migration in Caenorhabditis elegans PNAS, February 1, 2005; 102(5): 1507 - 1512. [Abstract] [Full Text] [PDF]

				S. P. Curran, E. P. Leverich, C. M. Koehler, and P. L. Larsen Defective Mitochondrial Protein Translocation Precludes Normal Caenorhabditis elegans Development J. Biol. Chem., December 24, 2004; 279(52): 54655 - 54662. [Abstract] [Full Text] [PDF]

				C. Y. Benard, H. Kebir, S. Takagi, and S. Hekimi mau-2 acts cell-autonomously to guide axonal migrations in Caenorhabditis elegans Development, December 1, 2004; 131(23): 5947 - 5958. [Abstract] [Full Text] [PDF]

				W. C. Forrester, C. Kim, and G. Garriga The Caenorhabditis elegans Ror RTK CAM-1 Inhibits EGL-20/Wnt Signaling in Cell Migration Genetics, December 1, 2004; 168(4): 1951 - 1962. [Abstract] [Full Text] [PDF]

				P. Syntichaki and N. Tavernarakis Genetic Models of Mechanotransduction: The Nematode Caenorhabditis elegans Physiol Rev, October 1, 2004; 84(4): 1097 - 1153. [Abstract] [Full Text] [PDF]

				N. Mehta, P. M. Loria, and O. Hobert A Genetic Screen for Neurite Outgrowth Mutants in Caenorhabditis elegans Reveals a New Function for the F-box Ubiquitin Ligase Component LIN-23 Genetics, March 1, 2004; 166(3): 1253 - 1267. [Abstract] [Full Text] [PDF]

				G.-d. Zhu and S. W. L'Hernault The Caenorhabditis elegans spe-39 Gene Is Required for Intracellular Membrane Reorganization During Spermatogenesis Genetics, September 1, 2003; 165(1): 145 - 157. [Abstract] [Full Text] [PDF]

				C.-c. Huang, D. H. Hall, E. M. Hedgecock, G. Kao, V. Karantza, B. E. Vogel, H. Hutter, A. D. Chisholm, P. D. Yurchenco, and W. G. Wadsworth Laminin {alpha} subunits and their role in C. elegans development Development, July 15, 2003; 130(14): 3343 - 3358. [Abstract] [Full Text] [PDF]

				K. Strange From Genes to Integrative Physiology: Ion Channel and Transporter Biology in Caenorhabditis elegans Physiol Rev, April 1, 2003; 83(2): 377 - 415. [Abstract] [Full Text] [PDF]

				E. Stringham, N. Pujol, J. Vandekerckhove, and T. Bogaert unc-53 controls longitudinal migration in C. elegans Development, March 9, 2003; 129(14): 3367 - 3379. [Abstract] [Full Text] [PDF]

				J. Nystrom, Z.-Z. Shen, M. Aili, A. J. Flemming, A. Leroi, and S. Tuck Increased or Decreased Levels of Caenorhabditis elegans lon-3, a Gene Encoding a Collagen, Cause Reciprocal Changes in Body Length Genetics, May 1, 2002; 161(1): 83 - 97. [Abstract] [Full Text] [PDF]

				J. Gao, L. Estrada, S. Cho, R. E. Ellis, and J. L. Gorski The Caenorhabditis elegans homolog of FGD1, the human Cdc42 GEF gene responsible for faciogenital dysplasia, is critical for excretory cell morphogenesis Hum. Mol. Genet., December 1, 2001; 10(26): 3049 - 3062. [Abstract] [Full Text] [PDF]

				A. G. Spencer, S. Orita, C. J. Malone, and M. Han A RHO GTPase-mediated pathway is required during P cell migration in Caenorhabditis elegans PNAS, October 25, 2001; (2001) 241504098. [Abstract] [Full Text] [PDF]

				K. Koh and J. H. Rothman ELT-5 and ELT-6 are required continuously to regulate epidermal seam cell differentiation and cell fusion in C. elegans Development, August 1, 2001; 128(15): 2867 - 2880. [Abstract] [Full Text] [PDF]

				D. C. Merz, H. Zheng, M. T. Killeen, A. Krizus, and J. G. Culotti Multiple Signaling Mechanisms of the UNC-6/netrin Receptors UNC-5 and UNC-40/DCC in Vivo Genetics, July 1, 2001; 158(3): 1071 - 1080. [Abstract] [Full Text] [PDF]

				H. Du and M. Chalfie Genes Regulating Touch Cell Development in Caenorhabditis elegans Genetics, May 1, 2001; 158(1): 197 - 207. [Abstract] [Full Text]

				G. Shioi, M. Shoji, M. Nakamura, T. Ishihara, I. Katsura, H. Fujisawa, and S. Takagi Mutations Affecting Nerve Attachment of Caenorhabditis elegans Genetics, April 1, 2001; 157(4): 1611 - 1622. [Abstract] [Full Text]

				J. Bateman and D. Van Vactor The Trio family of guanine-nucleotide-exchange factors: regulators of axon guidance J. Cell Sci., January 6, 2001; 114(11): 1973 - 1980. [Abstract] [Full Text] [PDF]

				S Alper and C Kenyon REF-1, a protein with two bHLH domains, alters the pattern of cell fusion in C. elegans by regulating Hox protein activity Development, January 5, 2001; 128(10): 1793 - 1804. [Abstract] [PDF]

				M Herman C. elegans POP-1/TCF functions in a canonical Wnt pathway that controls cell migration and in a noncanonical Wnt pathway that controls cell polarity Development, January 2, 2001; 128(4): 581 - 590. [Abstract] [PDF]

				L. Nilsson, T. Tiensuu, and S. Tuck Caenorhabditis elegans lin-25: A Study of Its Role in Multiple Cell Fate Specification Events Involving Ras and the Identification and Characterization of Evolutionarily Conserved Domains Genetics, November 1, 2000; 156(3): 1083 - 1096. [Abstract] [Full Text]

				K. Nishiwaki, N. Hisamoto, and K. Matsumoto A Metalloprotease Disintegrin That Controls Cell Migration in Caenorhabditis elegans Science, June 23, 2000; 288(5474): 2205 - 2208. [Abstract] [Full Text]

				L Honigberg and C Kenyon Establishment of left/right asymmetry in neuroblast migration by UNC-40/DCC, UNC-73/Trio and DPY-19 proteins in C. elegans Development, January 11, 2000; 127(21): 4655 - 4668. [Abstract] [PDF]

				N Pujol, P Torregrossa, J. Ewbank, and J. Brunet The homeodomain protein CePHOX2/CEH-17 controls antero-posterior axonal growth in C. elegans Development, January 8, 2000; 127(15): 3361 - 3371. [Abstract] [PDF]

				M Su, D. Merz, M. Killeen, Y Zhou, H Zheng, J. Kramer, E. Hedgecock, and J. Culotti Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating distal tip cells in Caenorhabditis elegans Development, January 2, 2000; 127(3): 585 - 594. [Abstract] [PDF]

				K. Nishiwaki Mutations Affecting Symmetrical Migration of Distal Tip Cells in Caenorhabditis elegans Genetics, July 1, 1999; 152(3): 985 - 997. [Abstract] [Full Text]

				M Koga, M Take-uchi, T Tameishi, and Y Ohshima Control of DAF-7 TGF-(alpha) expression and neuronal process development by a receptor tyrosine kinase KIN-8 in Caenorhabditis elegans Development, January 12, 1999; 126(23): 5387 - 5398. [Abstract] [PDF]

				D. Montell The genetics of cell migration in Drosophila melanogaster and Caenorhabditis elegans development Development, January 6, 1999; 126(14): 3035 - 3046. [Abstract] [PDF]

				C. Malone, W. Fixsen, H. Horvitz, and M Han UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development Development, January 6, 1999; 126(14): 3171 - 3181. [Abstract] [PDF]

				J. Wright, M. Snyder, K. Schwinof, S Combes, and P. Copenhaver A role for fasciclin II in the guidance of neuronal migration Development, January 6, 1999; 126(14): 3217 - 3228. [Abstract] [PDF]

				Y Liu and D. Montell Identification of mutations that cause cell migration defects in mosaic clones Development, January 5, 1999; 126(9): 1869 - 1878. [Abstract] [PDF]

				M. Herman, Q Ch'ng, S. Hettenbach, T. Ratliff, C Kenyon, and R. Herman EGL-27 is similar to a metastasis-associated factor and controls cell polarity and cell migration in C. elegans Development, January 2, 1999; 126(5): 1055 - 1064. [Abstract] [PDF]

				J. Maloof, J Whangbo, J. Harris, G. Jongeward, and C Kenyon A Wnt signaling pathway controls hox gene expression and neuroblast migration in C. elegans Development, January 1, 1999; 126(1): 37 - 49. [Abstract] [PDF]

				K. McArdle, T. StC. Allen, and E. A. Bucher Ca2+-dependent Muscle Dysfunction Caused by Mutation of the Caenorhabditis elegans Troponin T-1 Gene J. Cell Biol., November 30, 1998; 143(5): 1201 - 1213. [Abstract] [Full Text] [PDF]

				H. Yoshida, A. Watanabe, and Y. Ihara Collapsin Response Mediator Protein-2 Is Associated with Neurofibrillary Tangles in Alzheimer's Disease J. Biol. Chem., April 17, 1998; 273(16): 9761 - 9768. [Abstract] [Full Text] [PDF]

				A Antebi, J. Culotti, and E. Hedgecock daf-12 regulates developmental age and the dauer alternative in Caenorhabditis elegans Development, January 4, 1998; 125(7): 1191 - 1205. [Abstract] [PDF]

				J. Maloof and C Kenyon The Hox gene lin-39 is required during C. elegans vulval induction to select the outcome of Ras signaling Development, January 1, 1998; 125(2): 181 - 190. [Abstract] [PDF]

				K Ogura, M Shirakawa, T M Barnes, S Hekimi, and Y Ohshima The UNC-14 protein required for axonal elongation and guidance in Caenorhabditis elegans interacts with the serine/threonine kinase UNC-51. Genes & Dev., July 15, 1997; 11(14): 1801 - 1811. [Abstract] [PDF]

				S Takagi, C Benard, J Pak, D Livingstone, and S Hekimi Cellular and axonal migrations are misguided along both body axes in the maternal-effect mau-2 mutants of Caenorhabditis elegans Development, January 12, 1997; 124(24): 5115 - 5126. [Abstract] [PDF]

				W. Forrester and G Garriga Genes necessary for C. elegans cell and growth cone migrations Development, January 5, 1997; 124(9): 1831 - 1843. [Abstract] [PDF]

				K. D. Erttmann, D. W. Büttner, and M. Y. Gallin Molecular Cloning, Expression, and Localization of E1, an Onchocerca volvulus Antigen with Similarity to Brain Ankyrin J. Biol. Chem., January 19, 1996; 271(3): 1645 - 1650. [Abstract] [Full Text] [PDF]

				J Harris, L Honigberg, N Robinson, and C Kenyon Neuronal cell migration in C. elegans: regulation of Hox gene expression and cell position Development, January 10, 1996; 122(10): 3117 - 3131. [Abstract] [PDF]

				B Wightman, S. Clark, A. Taskar, W. Forrester, A. Maricq, C. Bargmann, and G Garriga The C. elegans gene vab-8 guides posteriorly directed axon outgrowth and cell migration Development, January 2, 1996; 122(2): 671 - 682. [Abstract] [PDF]

				K Fitzgerald and I Greenwald Interchangeability of Caenorhabditis elegans DSL proteins and intrinsic signalling activity of their extracellular domains in vivo Development, January 12, 1995; 121(12): 4275 - 4282. [Abstract] [PDF]

				P. Svendsen and J. McGhee The C. elegans neuronally expressed homeobox gene ceh-10 is closely related to genes expressed in the vertebrate eye Development, January 5, 1995; 121(5): 1253 - 1262. [Abstract] [PDF]

				K. L. Chow and S. W. Emmons HOM-C/Hox genes and four interacting loci determine the morphogenetic properties of single cells in the nematode male tail Development, September 1, 1994; 120(9): 2579 - 2592. [Abstract] [PDF]

				G Garriga, C Guenther, and H R Horvitz Migrations of the Caenorhabditis elegans HSNs are regulated by egl-43, a gene encoding two zinc finger proteins. Genes & Dev., November 1, 1993; 7(11): 2097 - 2109. [Abstract] [PDF]

				S J Salser, C M Loer, and C Kenyon Multiple HOM-C gene interactions specify cell fates in the nematode central nervous system. Genes & Dev., September 1, 1993; 7(9): 1714 - 1724. [Abstract] [PDF]

				G Garriga, C Desai, and H. Horvitz Cell interactions control the direction of outgrowth, branching and fasciculation of the HSN axons of Caenorhabditis elegans Development, January 3, 1993; 117(3): 1071 - 1087. [Abstract] [PDF]

				E. Aamodt, M. Chung, and J. McGhee Spatial control of gut-specific gene expression during Caenorhabditis elegans development Science, April 26, 1991; 252(5005): 579 - 582. [Abstract] [PDF]

				M Chalfie and M Au Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons Science, February 24, 1989; 243(4894): 1027 - 1033. [Abstract] [PDF]

				C Kenyon The nematode Caenorhabditis elegans Science, June 10, 1988; 240(4858): 1448 - 1453. [Abstract] [PDF]

				T. Matsuo, J. K. Stauffer, R. L. Walker, P. Meltzer, and C. J. Thiele Structure and Promoter Analysis of the Human unc-33-like Phosphoprotein Gene. E-BOX REQUIRED FOR MAXIMAL EXPRESSION IN NEUROBLASTOMA AND MYOBLASTS J. Biol. Chem., May 26, 2000; 275(22): 16560 - 16568. [Abstract] [Full Text] [PDF]

				A. G. Spencer, S. Orita, C. J. Malone, and M. Han A RHO GTPase-mediated pathway is required during P cell migration in Caenorhabditis elegans PNAS, November 6, 2001; 98(23): 13132 - 13137. [Abstract] [Full Text] [PDF]