The actin-binding protein UNC-115/abLIM controls formation of lamellipodia and filopodia and neuronal morphogenesis in Caenorhabditis elegans

Molecular and Cellular Biology

Volumn 25, Issue 12, 2005, Pages 5158-5170

  Yang, Yieyie ^a   Lundquist, Erik A ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; PROTEIN UNC 115; RAC PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CAENORHABDITIS ELEGANS; CELL MEMBRANE; CELL STRAIN 3T3; FIBROBLAST; FILOPODIUM; GROWTH CONE; LAMELLIPODIUM; MORPHOGENESIS; NERVE FIBER; NERVOUS SYSTEM; NEURITE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATOR GENE; SIGNAL TRANSDUCTION;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CYTOSKELETON; FIBROBLASTS; MICE; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; NEURONS; NIH 3T3 CELLS; PSEUDOPODIA; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

CAENORHABDITIS ELEGANS;

EID: 20344368574     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.12.5158-5170.2005     Document Type: Article

References (47)

1. Adams, M. D., S. E. Celniker, R. A. Holt, C. A. Evans, J. D. Gocayne, P. G. Amanatides, S. E. Scherer, P. W. Li, R. A. Hoskins, R. F. Galle, R. A. George, S. E. Lewis, S. Richards, M. Ashburner, S. N. Henderson, G. G. Sutton, J. R. Wortman, M. D. Yandell, Q. Zhang, L. X. Chen, R. C. Brandon, Y. H. Rogers, R. G. Blazej, M. Champe, B. D. Pfeiffer, K. H. Wan, C. Doyle, E. G. Baxter, G. Helt, C. R. Nelson, G. L. Gabor, J. F. Abril, A. Agbayani, H. J. An, C. Andrews-Pfannkoch, D. Baldwin, R. M. Ballew, A. Basu, J. Baxendale, L. Bayraktaroglu, E. M. Beasley, K. Y. Beeson, P. V. Benos, B. P. Berman, D. Bhandari, S. Bolshakov, D. Borkova, M. R. Botchan, J. Bouck, P. Brokstein, P. Brottier, K. C. Burtis, D. A. Busam, H. Butler, E. Cadieu, A. Center, I. Chandra, J. M. Cherry, S. Cawley, C. Dahlke, L. B. Davenport, P. Davies, B. de Pablos, A. Delcher, Z. Deng, A. D. Mays, I. Dew, S. M. Dietz, K. Dodson, L. E. Doup, M. Downes, S. Dugan-Rocha, B. C. Dunkov, P. Dunn, K. J. Durbin, C. C. Evangelista, C. Ferraz, S. Ferriera, W. Fleischmann, C. Fosler, A. E. Gabrielian, N. S. Garg, W. M. Gelbart, K. Glasser, A. Glodek, F. Gong, J. H. Gorrell, Z. Gu, P. Guan, M. Harris, N. L. Harris, D. Harvey, T. J. Heiman, J. R. Hernandez, J. Houck, D. Hostin, K. A. Houston, T. J. Howland, M. H. Wei, C. Ibegwam, et al. 2000. The genome sequence of Drosophila melanogaster. Science 287:2185-2195.
2. Aizawa, H., S. Wakatsuki, A. Ishii, K. Moriyama, Y. Sasaki, K. Ohashi, Y. Sekine-Aizawa, A. Sehara-Fujisawa, K. Mizuno, Y. Goshima, and I. Yahara. 2001. Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat. Neurosci. 4:367-373.
3. Altschul, S. F., and D. J. Lipman. 1990. Protein database searches for multiple alignments. Proc. Natl. Acad. Sci. USA 87:5509-5513.
4. Azim, A. C., J. H. Knoll, A. H. Beggs, and A. H. Chishti. 1995. Isoform cloning, actin binding, and chromosomal localization of human erythroid dematin, a member of the villin superfamily. J. Biol. Chem. 270:17407-17413.
5. Bogdan, S., and C. Klambt. 2003. Kette regulates actin dynamics and genetically interacts with Wave and Wasp. Development 130:4427-4437.
6. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
7. Chalfie, M., Y. Tu, G. Euskirchen, W. W. Ward, and D. C. Prasher. 1994. Green fluorescent protein as a marker for gene expression. Science 263:802-805.
8. Collet, J., C. A. Spike, E. A. Lundquist, J. E. Shaw, and R. K. Herman. 1998. Analysis of osm-6, a gene that affects sensory cilium structure and sensory neuron function in Caenorhabditis elegans. Genetics 148:187-200.
9. Dan, C., A. Kelly, O. Bernard, and A. Minden. 2001. Cytoskeletal changes regulated by the PAK4 serine/threonine kinase are mediated by LIM kinase 1 and cofilin. J. Biol. Chem. 276:32115-32121.
10. Dickson, B. J. 2002. Molecular mechanisms of axon guidance. Science 298:1959-1964.
11. Dickson, B. J. 2001. Rho GTPases in growth cone guidance. Curr. Opin. Neurobiol. 11:103-110.
12. Eden, S., R. Rohatgi, A. V. Podtelejnikov, M. Mann, and M. W. Kirschner. 2002. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790-793.
13. Erkman, L., P. A. Yates, T. McLaughlin, R. J. McEvilly, T. Whisenhunt, S. M. O'Connell, A. I. Krones, M. A. Kirby, D. H. Rapaport, J. R. Bermingham, D. D. O'Leary, and M. G. Rosenfeld. 2000. A POU domain transcription factor-dependent program regulates axon pathfinding in the vertebrate visual system. Neuron 28:779-792.
14. Friederich, E., K. Vancompernolle, C. Huet, M. Goethals, J. Finidori, J. Vandekerckhove, and D. Louvard. 1992. An actin-binding site containing a conserved motif of charged amino acid residues is essential for the morphogenetic effect of villin. Cell 70:81-92.
15. Gallo, G., and P. C. Letourneau. 2004. Regulation of growth cone actin filaments by guidance cues. J. Neurobiol. 58:92-102.
16. Gitai, Z., T. W. Yu, E. A. Lundquist, M. Tessier-Lavigne, and C. I. Bargmann. 2003. The netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through Enabled and, in parallel, Rac and UNC-115/AbLIM. Neuron 37:53-65.
17. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
18. Heo, W. D., and T. Meyer. 2003. Switch-of-function mutants based on morphology classification of Ras superfamily small GTPases. Cell 113:315-328.
19. Hing, H., J. Xiao, N. Harden, L. Lim, and S. L. Zipursky. 1999. Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila. Cell 97:853-863.
20. Hummel, T., K. Leifker, and C. Klambt. 2000. The Drosophila HEM-2/NAP1 homolog KETTE controls axonal pathfinding and cytoskeletal organization. Genes Dev. 14:863-873.
21. Husain-Chishti, A., W. Faquin, C. C. Wu, and D. Branton. 1989. Purification of erythrocyte dematin (protein 4.9) reveals an endogenous protein kinase that modulates actin-bundling activity. J. Biol. Chem. 264:8985-8991.
22. Innocenti, M, A. Zucconi, A. Disanza, E. Frittoli, L. B. Areces, A. Steffen, T. E. Stradal, P. P. Di Fiore, M. F. Carlier, and G. Scita. 2004. Abi1 is essential for the formation and activation of a WAVE2 signalling complex. Nat. Cell Biol. 6:319-327.
23. 2-terminal glycine of p60src prevents both myristoylation and morphological transformation. Proc. Natl. Acad. Sci. USA 82:4625-4628.
24. Kitamura, T., Y. Kitamura, K. Yonezawa, N. F. Totty, I. Gout, K. Hara, M. D. Waterfield, M. Sakaue, W. Ogawa, and M. Kasuga. 1996. Molecular cloning of p125Nap1, a protein that associates with an SH3 domain of Nck. Biochem. Biophys. Res. Commun. 219:509-514.
25. Knobel, K. M., E. M. Jorgensen, and M. J. Bastiani. 1999. Growth cones stall and collapse during axon outgrowth in Caenorhabditis elegans. Development 126:4489-4498.
26. Kobayashi, K., S. Kuroda, M. Fukata, T. Nakamura, T. Nagase, N. Nomura, Y. Matsuura, N. Yoshida-Kubomura, A. Iwamatsu, and K. Kaibuchi. 1998. p140Sra-1 (specifically Rac1-associated protein) is a novel specific target for Rac1 small GTPase. J. Biol. Chem. 273:291-295.
27. Kunda, P., G. Craig, V. Dominguez, and B. Baum. 2003. Abi, Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actin-based protrusions. Curr. Biol. 13:1867-1875.
28. Li, W., J. Fan, and D. T. Woodley. 2001. Nck/Dock: an adapter between cell surface receptors and the actin cytoskeleton. Oncogene 20:6403-6417.
29. Lundquist, E. A. 2003. Rac proteins and the control of axon development. Curr. Opin. Neurobiol. 13:384-390.
30. Lundquist, E. A., R. K. Herman, J. E. Shaw, and C. I. Bargmann. 1998. UNC-115, a conserved protein with predicted LIM and actin-binding domains, mediates axon guidance in C. elegans. Neuron 21:385-392.
31. Luo, L. 2000. Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 1:173-180.
32. Meberg, P. J. 2000. Signal-regulated ADF/cofilin activity and growth cone motility. Mol. Neurobiol. 21:97-107.
33. Mello, C., and A. Fire. 1995. DNA transformation. Methods Cell Biol. 48:451-482.
34. Miki, H., and T. Takenawa. 2002. WAVE2 serves a functional partner of IRSp53 by regulating its interaction with Rac. Biochem. Biophys. Res. Commun. 293:93-99.
35. Nozumi, M., H. Nakagawa, H. Miki, T. Takenawa, and S. Miyamoto. 2003. Differential localization of WAVE isoforms in filopodia and lamellipodia of the neuronal growth cone. J. Cell Sci. 116:239-246.
36. Rana, A. P., P. Ruff, G. J. Maalouf, D. W. Speicher, and A. H. Chishti. 1993. Cloning of human erythroid dematin reveals another member of the villin family. Proc. Natl. Acad. Sci. USA 90:6651-6655.
37. Reuther, G. W., J. E. Buss, L. A. Quilliam, G. J. Clark, and C. J. Der. 2000. Analysis of function and regulation of proteins that mediate signal transduction by use of lipid-modified plasma membrane-targeting sequences. Methods Enzymol. 327:331-350.
38. Ridley, A. J., H. F. Paterson, C. L. Johnston, D. Diekmann, and A. Hall. 1992. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70:401-410.
39. Roof, D. J., A. Hayes, M. Adamian, A. H. Chishti, and T. Li. 1997. Molecular characterization of abLIM, a novel actin-binding and double zinc finger protein. J. Cell Biol. 138:575-588.
40. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
41. Steffen, A., K. Rottner, J. Ehinger, M. Innocenti, G. Scita, J. Wehland, and T. E. Stradal. 2004. Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. EMBO J. 23:749-759.
42. Struckhoff, E. C., and E. A. Lundquist. 2003. The actin-binding protein UNC-115 is an effector of Rac signaling during axon pathfinding in C. elegans. Development 130:693-704.
43. Suetsugu, S., D. Yamazaki, S. Kurisu, and T. Takenawa. 2003. Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev. Cell. 5:595-609.
44. Sulston, J., and J. Hodgkin. 1988. Methods, p. 587-606. In W. B. Wood (ed.), The nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
45. Symons, M. 2000. Adhesion signaling: PAK meets Rac on solid ground. Curr. Biol. 10:R535-R537.
46. Welch, M. D., and R. D. Mullins. 2002. Cellular control of actin nucleation. Annu. Rev. Cell Dev. Biol. 18:247-288.
47. 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.