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JOURNAL ARTICLES
Neuronal cell migration in C. elegans: regulation of Hox gene expression and cell position
J. Harris, L. Honigberg, N. Robinson, C. Kenyon
Development 1996 122: 3117-3131;

Summary

In C. elegans, the Hox gene mab-5, which specifies the fates of cells in the posterior body region, has been shown to direct the migrations of certain cells within its domain of function. mab-5 expression switches on in the neuroblast QL as it migrates into the posterior body region. mab-5 activity is then required for the descendants of QL to migrate to posterior rather than anterior positions. What information activates Hox gene expression during this cell migration? How are these cells subsequently guided to their final positions? We address these questions by describing four genes, egl-20, mig-14, mig-1 and lin-17, that are required to activate expression of mab-5 during migration of the QL neuroblast. We find that two of these genes, egl-20 and mig-14, also act in a mab-5-independent way to determine the final stopping points of the migrating Q descendants. The Q descendants do not migrate toward any obvious physical targets in wild-type or mutant animals. Therefore, these genes appear to be part of a system that positions the migrating Q descendants along the anteroposterior axis.

Reference

    1. Ahn J.,
    2. Fire A.
    (1994) A screen for genetic loci required for body-wall muscle development during embryogenesis in Caenorhabditis elegans. Genetics 137, 483–498
    OpenUrlAbstract/FREE Full Text
    1. Brenner S.
    (1974) The genetics of C. elegans. Genetics 77, 71–94
    OpenUrlAbstract/FREE Full Text
    1. Chalfie M.,
    2. Sulston J.
    (1981) Developmental genetics of the mechanosensory neurons of C. elegans. Dev. Biol 82, 358–370
    OpenUrlCrossRefPubMedWeb of Science
    1. Chisholm A.
    (1991) Control of cell fate in the tail region of C. elegans by the gene egl-5. Development 111, 921–932
    OpenUrlAbstract/FREE Full Text
    1. Clark S. G.,
    2. Chisholm A. D.,
    3. Horvitz H. R.
    (1993) Control of cell fates in the central body region of C. elegans by the homeobox gene lin-39. Cell 74, 43–55
    OpenUrlCrossRefPubMedWeb of Science
    1. Costa M.,
    2. Weir M.,
    3. Coulson A.,
    4. Sulston J.,
    5. Kenyon C.
    (1988) Posterior pattern formation in C. elegans involves position-specific expression of a gene containing a homeobox. Cell 55, 747–756
    OpenUrlCrossRefPubMedWeb of Science
    1. Desai C.,
    2. Garriga G.,
    3. McIntire S. L.,
    4. Horvitz H. R.
    (1988) A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336, 638–646
    OpenUrlCrossRefPubMedWeb of Science
    1. Devore D. L.,
    2. Horvitz H. R.,
    3. Stern M. J.
    (1995) An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C. elegans hermaphrodites. Cell 83, 611–620
    OpenUrlCrossRefPubMedWeb of Science
    1. Ferguson E.,
    2. Horvitz H.
    (1985) Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode C. elegans. Genetics 110, 17–72
    OpenUrlAbstract/FREE Full Text
    1. Garriga G.,
    2. Desai C.,
    3. Horvitz H. R.
    (1993) Cell interactions control the direction of outgrowth, branching and fasciculation of the HSN axons of Caenorhabditis elegans. Development 117, 1071–1087
    OpenUrlAbstract
    1. Godin I.,
    2. Wylie C.,
    3. Heasman J.
    (1990) Genital ridges exert long-range effects on mouse primordial germ cell numbers and direction of migration in culture. Development 108, 357–363
    OpenUrlAbstract
    1. Hamelin M.,
    2. Scott I. M.,
    3. Way J. C.,
    4. Culotti J. G.
    (1992) The mec-7 beta-tubulin gene of Caenorhabditis elegans is expressed primarily in the touch receptor neurons. EMBO J 11, 2885–2893
    OpenUrlPubMedWeb of Science
    1. Hedgecock E. M.,
    2. Culotti J. G.,
    3. Hall D. H.
    (1990) The unc-5, unc-6 and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4, 61–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Hedgecock E. M.,
    2. Culotti J. G.,
    3. Hall D. H.,
    4. Stern B. D.
    (1987) Genetics of cell and axon migrations in Caenorhabditis elegans. Development 100, 365–382
    OpenUrlAbstract
    1. Howard K.
    (1990) The blastoderm prepattern. Semin. Cell Biol 1, 161–172
    OpenUrlPubMed
    1. Ingham P.
    (1991) Segment polarity genes and cell patterning within the Drosophila body segment. Current Opin. Genet. Dev 1, 261–267
    OpenUrlCrossRefPubMed
    1. Ishii N.,
    2. Wadsworth W. G.,
    3. Stern B. D.,
    4. Culotti J. G.,
    5. Hedgecock E.
    (1992) UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans. Neuron 9, 873–881
    OpenUrlCrossRefPubMedWeb of Science
    1. Jacobson L. A.,
    2. Jen J. L.,
    3. Hawdon J. M.,
    4. Owens G. P.,
    5. Bolanowski M. A.,
    6. Emmons S. W.,
    7. Shah M. V.,
    8. Pollock R. A.,
    9. Conklin D. S.
    (1988) Identification of a putative structural gene for cathepsin D in Caenorhabditis elegans. Genetics 119, 355–363
    OpenUrlAbstract/FREE Full Text
    1. Kennedy T. E.,
    2. Serafini T.,
    3. de la Torre J. R.,
    4. Tessier-Lavigne M.
    (1994) Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78, 425–435
    OpenUrlCrossRefPubMedWeb of Science
    1. Kenyon C.
    (1986) A gene involved in the development of the posterior body region of C. elegans. Cell 46, 477–487
    OpenUrlCrossRefPubMedWeb of Science
    1. Kenyon C.,
    2. Wang B.
    (1991) A cluster of Antennapedia-class homeobox genes in a nonsegmented animal. Science 253, 516–517
    OpenUrlFREE Full Text
    1. Ma C.,
    2. Moses K.
    (1995) wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye. Development 121, 2279–2289
    OpenUrlAbstract
    1. Montell D. J.
    (1994) Moving right along: regulation of cell migration during Drosophila development. Trends Genet 10, 59–62
    OpenUrlCrossRefPubMed
    1. Salser S.,
    2. Kenyon C.
    (1992) Activation of a C. elegansAntennapedia homolog within migrating cells controls their direction of migration. Nature 355, 255–258
    OpenUrlCrossRefPubMed
    1. Salser S.,
    2. Loer C.,
    3. Kenyon C.
    (1993) Multiple HOM-C gene interactions specify cell fates in the nematode central nervous system. Genes Dev 7, 1714–1724
    OpenUrlAbstract/FREE Full Text
    1. Salser S. J.,
    2. Kenyon C.
    (1996) A C. elegans Hox gene switches ON, OFF, ON, and OFF again to regulate proliferation, differentiation, and morphogenesis. Development 122, 1651–1661
    OpenUrlAbstract
    1. Serafini T.,
    2. Kennedy T. E.,
    3. Galko M. J.,
    4. Mirzayan C.,
    5. Jessel T. M.,
    6. Tessier-Lavigne M.
    (1994) The netrins define a family of axon outgrowth promoting proteins homologous to C. elegans UNC-6. Cell 78, 409–424
    OpenUrlCrossRefPubMedWeb of Science
    1. Shaller D.,
    2. Wittmann C.,
    3. Spicher A.,
    4. Muller F.,
    5. Tobler H.
    (1990) Cloning and analysis of three new homeobox genes from the nematode Caenorhabditis elegans. Nucl. Acids Res 18, 2033–2036
    OpenUrlAbstract/FREE Full Text
    1. Sternberg P. W.,
    2. Horvitz H. R.
    (1988) lin-17 mutations of Caenorhabditis elegans disrupt certain asymmetric cell divisions. Dev. Biol 130, 67–73
    OpenUrlCrossRefPubMedWeb of Science
    1. Stringham E. G.,
    2. Candido E. P.
    (1993) Targeted single-cell induction of gene products in Caenorhabditis elegans: a new tool for developmental studies. J. Exp. Zool 266, 227–233
    OpenUrlCrossRefPubMedWeb of Science
    1. Sulston J.,
    2. Horvitz H. R.
    (1977) Post-embryonic cell lineages of the nematode, C elegans. Dev. Biol 56, 110–156
    OpenUrlCrossRefPubMedWeb of Science
    1. Teragawa C.,
    2. Bode H.
    (1990) Spatial and temporal patterns of interstitial cell migration in Hydra vulgaris. Dev. Biol 138, 63–81
    OpenUrlCrossRefPubMed
    1. Tessier-Lavigne M.
    (1995) Eph receptor tyrosine kinases, axon repulsion, and the development of topographic maps. Cell 82, 345–348
    OpenUrlCrossRefPubMedWeb of Science
    1. Trent C.,
    2. Tsung N.,
    3. Horvitz H. R.
    (1983) Egg-laying defective mutants of the nematode C. elegans. Genetics 104, 619–647
    OpenUrlAbstract/FREE Full Text
    1. Wang B. B.,
    2. Muller-Immergluck M. M.,
    3. Austin J.,
    4. Robinson N. T.,
    5. Chisholm A.,
    6. Kenyon C.
    (1993) A homeotic gene cluster patterns the anteroposterior body axis of C. elegans. Cell 74, 29–42
    OpenUrlCrossRefPubMedWeb of Science
    1. Way J.,
    2. Run J.,
    3. Wang A.
    (1992) Regulation of anterior cell-specific mec-3 expression during asymmetric cell division in C. elegans. Dev. Dynam 194, 289–302
    OpenUrlPubMed
    1. Wehrli M.,
    2. Tomlinson A.
    (1995) Epithelial planar polarity in the developing Drosophila eye. Development 121, 2451–2459
    OpenUrlAbstract
    1. White J.,
    2. Southgate E.,
    3. Thomson J.,
    4. Brenner S.
    (1986) The structure of the nervous system of the nematode C. elegans. Philosophical Transactions of the Royal Society of London 314, 1–340
    OpenUrlCrossRef
    1. Wightman B.,
    2. Clark S. G.,
    3. Taskar A. M.,
    4. Forrester W. C.,
    5. Maricq A. V.,
    6. Bargmann C. I.,
    7. Garriga G.
    (1996) The C. elegans gene vab-8 guides posteriorly directed axon outgrowth and cell migration. Development 122, 671–682
    OpenUrlAbstract
    1. Williams B. D.,
    2. Schrank B.,
    3. Huynh C.,
    4. Shownkeen R.,
    5. Waterston R. H.
    (1992) A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites. Genetics 131, 609–624
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
Neuronal cell migration in C. elegans: regulation of Hox gene expression and cell position
J. Harris, L. Honigberg, N. Robinson, C. Kenyon
Development 1996 122: 3117-3131;
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