Transmembrane proteins UNC-40/DCC, PTP-3/LAR, and MIG-21 control anterior-posterior neuroblast migration with left-right functional asymmetry in Caenorhabditis elegans

Genetics

Volumn 192, Issue 4, 2012, Pages 1373-1388

  Sundararajan, Lakshmi ^a   Lundquist, Erik A ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MIG 21 PROTEIN; PTP 3 PROTEIN; UNC 40 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL MIGRATION; CONTROLLED STUDY; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ACID ANHYDRIDE HYDROLASES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION MOLECULES; CELL MOVEMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MEMBRANE PROTEINS; NEURAL CREST; NEURONS;

CAENORHABDITIS ELEGANS;

EID: 84870665436     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.112.145706     Document Type: Article

References (52)

1. Ackley, B. D., R. J. Harrington, M. L. Hudson, L. Williams, C. J. Kenyon et al., 2005. The two isoforms of the Caenorhabditis elegans leukocyte-common antigen related receptor tyrosine phosphatase PTP-3 function independently in axon guidance and synapse formation. J. Neurosci. 25: 7517-7528
2. Aicher, B., M. M. Lerch, T. Muller, J. Schilling, and A. Ullrich, 1997. Cellular redistribution of protein tyrosine phosphatases LAR and PTPsigma by inducible proteolytic processing. J. Cell Biol. 138: 681-696
3. Alexander, M., K. K. Chan, A. B. Byrne, G. Selman, T. Lee et al., 2009. An UNC-40 pathway directs postsynaptic membrane extension in Caenorhabditis elegans. Development 136: 911-922
4. Bigelow, H., M. Doitsidou, S. Sarin, andO.Hobert, 2009. MAQGene: software to facilitate C. elegans mutant genome sequence analysis. Nat. Methods 6: 549
5. Branda, C. S., and M. J. Stern, 2000. Mechanisms controlling sex myoblast migration in Caenorhabditis elegans hermaphrodites. Dev. Biol. 226: 137-151
6. Calixto, A., D. Chelur, I. Topalidou, X. Chen, and M. Chalfie, 2010. Enhanced neuronal RNAi in C. elegans using SID-1. Nat. Methods 7: 554-559
7. Ch'ng, Q., L. Williams, Y. S. Lie, M. Sym, J. Whangbo et al., 2003. Identification of genes that regulate a left-right asymmetric neuronal migration in Caenorhabditis elegans. Genetics 164: 1355-1367
8. Chalfie, M., and J. Sulston, 1981. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev. Biol. 82: 358-370
9. Chalfie, M., J. N. Thomson, and J. E. Sulston, 1983. Induction of neuronal branching in Caenorhabditis elegans. Science 221: 61-63
10. Chapman, J. O., H. Li, and E. A. Lundquist, 2008. The MIG-15 NIK kinase acts cell-autonomously in neuroblast polarization and migration in C. elegans. Dev. Biol. 324: 245-257
11. Cordes, S., C. A. Frank, and G. Garriga, 2006. The C. elegans MELK ortholog PIG-1 regulates cell size asymmetry and daughter cell fate in asymmetric neuroblast divisions. Development 133: 2747-2756
12. Davis, M. W., M. Hammarlund, T. Harrach, P. Hullett, S. Olsen et al., 2005. Rapid single nucleotide polymorphism mapping in C. elegans. BMC Genomics 6: 118
13. Du, H., and M. Chalfie, 2001. Genes regulating touch cell development in Caenorhabditis elegans. Genetics 158: 197-207
14. Dyer, J. O., R. Demarco, and E. A. Lundquist, 2010. Distinct roles of Rac GTPases and the UNC-73/Trio and PIX-1 Rac GTP exchange factors in neuroblast protrusion and migration in C. elegans. Small GTPases 1: 44-61
15. Eisenmann, D. M., 2005. Wnt signaling (June 25, 2005), Worm-Book, ed. The C. elegans Research Community WormBook, doi/ 10.1895/wormbook.1.7.1, http://www.wormbook.org
16. Esposito, G., E. Di Schiavi, C. Bergamasco, and P. Bazzicalupo, 2007. Efficient and cell specific knock-down of gene function in targeted C. elegans neurons. Gene 395: 170-176
17. Gilleard, J. S., J. D. Barry, and I. L. Johnstone, 1997. cis regulatory requirements for hypodermal cell-specific expression of the Caenorhabditis elegans cuticle collagen gene dpy-7. Mol. Cell. Biol. 17: 2301-2311
18. Haapasalo, A., D. Y. Kim, B. W. Carey, M. K. Turunen, W. H. Pettingell et al., 2007. Presenilin/gamma-secretase-mediated cleavage regulates association of leukocyte-common antigenrelated (LAR) receptor tyrosine phosphatase with beta-catenin. J. Biol. Chem. 282: 9063-9072
19. Harrington, R. J., M. J. Gutch, M. O. Hengartner, N. K. Tonks, and A. D. Chisholm, 2002. The C. elegans LAR-like receptor tyrosine phosphatase PTP-3 and the VAB-1 Eph receptor tyrosine kinase have partly redundant functions in morphogenesis. Development 129: 2141-2153
20. Harris, J., L. Honigberg, N. Robinson, and C. Kenyon, 1996. Neuronal cellmigration in C. elegans: regulation of Hox gene expression and cell position. Development 122: 3117-3131
21. Harterink, M., D. H. Kim, T. C. Middelkoop, T. D. Doan, A. van Oudenaarden et al., 2011. Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein. Development 138: 2915-2924
22. Hedgecock, E. M., J. G. Culotti, and D. H. Hall, 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
23. Herman, M. A., 2003. Wnt signaling in C. elegans, pp. 187-212 in Wnt Signaling in Development, edited by M. Kühl. Landes Biosciences, Georgetown, TX
24. Hofmeyer, K., and J. E. Treisman, 2009. The receptor protein tyrosine phosphatase LAR promotes R7 photoreceptor axon targeting by a phosphatase-independent signaling mechanism. Proc. Natl. Acad. Sci. USA 106: 19399-19404
25. Honigberg, L., and C. Kenyon, 2000. Establishment of left/right asymmetry in neuroblast migration by UNC-40/DCC, UNC-73/Trio and DPY-19 proteins in C. elegans. Development 127: 4655-4668
26. Johnson, K. G., A. P. Tenney, A. Ghose, A. M. Duckworth, M. E. Higashi et al., 2006. The HSPGs Syndecan and Dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development. Neuron 49: 517-531
27. Keino-Masu, K., M. Masu, L. Hinck, E. D. Leonardo, S. S.-Y. Chan et al., 1996. Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87: 175-185
28. Kenyon, C., 1986. A gene involved in the development of the posterior body region of C. elegans. Cell 46: 477-487
29. Korswagen, H. C., M. A. Herman, and H. C. Clevers, 2000. Distinct beta-catenins mediate adhesion and signalling functions in C. elegans. Nature 406: 527-532
30. Langmead, B., C. Trapnell, M. Pop, and S. L. Salzberg, 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25
31. Levy-Strumpf, N., and J. G. Culotti, 2007. VAB-8, UNC-73 and MIG-2 regulate axon polarity and cell migration functions of UNC-40 in C. elegans. Nat. Neurosci. 10: 161-168
32. Mello, C., and A. Fire, 1995. DNA transformation. Methods Cell Biol. 48: 451-482
33. Middelkoop, T. C., L. Williams, P. T. Yang, J. Luchtenberg, M. C. Betist et al., 2012. The thrombospondin repeat containing protein MIG-21 controls a left-right asymmetric Wnt signaling response in migrating C. elegans neuroblasts. Dev. Biol. 361: 338-348
34. Pan, C. L., J. E. Howell, S. G. Clark, M. Hilliard, S. Cordes et al., 2006. Multiple Wnts and frizzled receptors regulate anteriorly directed cell and growth cone migrations in Caenorhabditis elegans. Dev. Cell 10: 367-377
35. Pawson, C., B. A. Eaton, and G. W. Davis, 2008. Formin-dependent synaptic growth: evidence that Dlar signals via Diaphanous to modulate synaptic actin and dynamic pioneer microtubules. J. Neurosci. 28: 11111-11123
36. Robinson, J. T., H. Thorvaldsdottir, W. Winckler, M. Guttman, E. S. Lander et al., 2011. Integrative genomics viewer. Nat. Biotechnol. 29: 24-26
37. Ruhe, J. E., S. Streit, S. Hart, and A. Ullrich, 2006. EGFR signaling leads to downregulation of PTP-LAR via TACE-mediated proteolytic processing. Cell. Signal. 18: 1515-1527
38. Salser, S. J., and C. Kenyon, 1992. Activation of a C. elegans Antennapedia homologue in migrating cells controls their direction of migration. Nature 355: 255-258
39. Srinivasan, S., A. P. Mahowald, and M. T. Fuller, 2012. The receptor tyrosine phosphatase Lar regulates adhesion between Drosophila male germline stem cells and the niche. Development 139: 1381-1390
40. Sulston, J., and J. Hodgkin, 1988. Methods, pp. 587-606 in The Nematode Caenorhabditis elegans, edited by W. B. Wood. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
41. Sulston, J. E., and H. R. Horvitz, 1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56: 110-156
42. Sym, M., N. Robinson, and C. Kenyon, 1999. MIG-13 positions migrating cells along the anteroposterior body axis of C. elegans. Cell 98: 25-36
43. Tabara, H., A. Grishok, and C. C. Mello, 1998. RNAi in C. elegans: soaking in the genome sequence. Science 282: 430-431
44. Terns, R. M., P. Kroll-Conner, J. Zhu, S. Chung, and J. H. Rothman, 1997. A deficiency screen for zygotic loci required for establishment and patterning of the epidermis in Caenorhabditis elegans. Genetics 146: 185-206
45. Thorvaldsdottir, H., J.T. Robinson, andJ. P. Mesirov,2012 Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. (in press)
46. Timmons, L., D. L. Court, and A. Fire, 2001. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103-112
47. Wang, F., S. N. Wolfson, A. Gharib, and A. Sagasti, 2012. LAR receptor tyrosine phosphatases and HSPGs guide peripheral sensory axons to the skin. Curr. Biol. 22: 373-382
48. Whangbo, J., and C. Kenyon, 1999. A Wnt signaling system that specifies two patterns of cell migration in C. elegans. Mol. Cell 4: 851-858
49. White, J. G., E. Southgate, J. N. Thomson, and S. Brenner, 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. 314: 1-340
50. Williams, L., 2003. A genetic analysis of the left-right asymmetric polarizations and migrations of the Q neuroblasts in C. elegans. Ph.D. Thesis, University of California, San Francisco
51. Winston, W. M., C. Molodowitch, and C. P. Hunter, 2002. Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295: 2456-2459
52. Zinovyeva, A. Y., Y. Yamamoto, H. Sawa, and W. C. Forrester, 2008. Complex network of Wnt signaling regulates neuronal migrations During Caenorhabditis elegans. Dev. Genet. 179: 1357-1371