RhoA/ROCK regulation of neuritogenesis via profilin IIa-mediated control of actin stability

Journal of Cell Biology

Volumn 162, Issue 7, 2003, Pages 1267-1279

  Da Silva, Jorge Santos ^a   Medina, Miguel ^a   Zuliani, Cecilia ^b   Di Nardo, Alessia ^c   Witke, Walter ^c   Dotti, Carlos G ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c Mouse Biology Programme   (Italy)

Author keywords

Actin dynamics; Actin binding proteins; Hippocampal neurons; Neuronal differentiation; Rho GTPases

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; PROFILIN; PROFILIN 2A; PROTEIN KINASE; PROTEIN ROCK; RHO FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; HIPPOCAMPUS; MITOSIS; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT;

ANIMALS; CELL SIZE; CELLS, CULTURED; CONTRACTILE PROTEINS; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROFILAMENT PROTEINS; MICROFILAMENTS; NERVE GROWTH FACTORS; NEURITES; NEURONS; PROFILINS; PROTEIN-SERINE-THREONINE KINASES; RATS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; STIMULATION, CHEMICAL;

ANIMALIA;

EID: 0141864656     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200304021     Document Type: Article

References (45)

1. Arber, S., F.A. Barbayannis, H. Hanser, C. Schneider, C.A. Stanyon, O. Bernard, and P. Caroni. 1998. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature. 393:805-809.
2. Bamburg, J.R. 1999. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 15:185-230.
3. Baum, P.D., and G. Garriga. 1997. Neuronal migrations and axon fasciculation are disrupted in ina-1 integrin mutants. Neuron. 19:51-62.
4. Billuart, P., C.G. Winter, A. Maresh, X. Zhao, and L. Luo. 2001. Regulating axon branch stability: the role of p190 RhoGAP in repressing a retraction signaling pathway. Cell. 107:195-207.
5. Bito, H., T. Furuyashiki, H. Ishihara, Y. Shibasaki, K. Ohashi, K. Mizuno, M. Maekawa, T. Ishizaki, and S. Narumiya. 2000. A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron. 26:431-441.
6. Bradke, F., and C.G. Dotti. 1999. The role of local actin instability in axon formation. Science. 283:1931-1934.
7. Da Silva, J.S., and C.G. Dotti. 2002. Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat. Rev. Neurosci. 3:694-704.
8. Di Nardo, A., R. Gareus, D. Kwiatkowski, and W. Witke. 2000. Alternative splicing of the mouse profilin II gene generates functionally different profilin isoforms. J. Cell Sci. 113:3795-3803.
9. Dotti, C.G., C.A. Sullivan, and G.A. Banker. 1988. The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8:1454-1468.
10. Evangelista, M., D. Pruyne, D.C. Amberg, C. Boone, and A. Bretscher. 2002. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 4:32-41.
11. Gleeson, J.G., and C.A. Walsh. 2000. Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci. 23:352-359.
12. Goslin, K., and G. Banker. 1991. Rat hippocampal neurons in low-density culture. In Culturin Nerve Cells. K. Goslin and G. Banker, editors. Massachusetts Institute of Technology Press, Cambridge, MA. 251-281.
13. Haarer, B.K., S.H. Lillie, A.E. Adams, V. Magdolen, W. Bandlow, and S.S. Brown. 1990. Purification of profilin from Saccharomyces cerevisiae and analysis of profilin-deficient cells. J. Cell Biol. 110:105-114.
14. Harten, M.E. 1999. Central nervous system neuronal migration. Annu. Rev. Neurosci. 22:511-539.
15. Haugwitz, M., A.A. Noegel, J. Karakesisoglou, and M. Schleicher. 1994. Dictyostelium amoebae that lack G-actin-sequestering profilins show defects in F-actin content, cytokinesis, and development. Cell. 79:303-314.
16. Hirose, M., T. Ishizaki, N. Watanabe, M. Uehata, O. Kranenburg, W.H. Moolenaar, F. Matsumura, M. Maekawa, H. Bito, and S. Narumiya. 1998. Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 141:1625-1636.
17. Hu, E., Z. Chen, T. Fredrickson, and Y. Zhu. 2001. Molecular cloning and characterization of profilin-3: a novel cytoskeleton-associated gene expressed in rat kidney and testes. Exp. Nephrol. 9:265-274.
18. Ishizaki, T., M. Uehata, I. Tamechika, J. Keel, K. Nonomura, M. Maekawa, and S. Narumiya. 2000. Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol. Pharmacol. 57:976-983.
19. Jalink, K., T. Eichholtz, F.R. Postma, E.J. van Corven, and W.H. Moolenaar. 1993. Lysophosphatidic acid induces neuronal shape changes via a novel, receptor-mediated signaling pathway: similarity to thrombin action. Cell Growth Differ. 4:247-255.
20. Jalink, K., E.J. van Corven, T. Hengeveld, N. Morii, S. Narumiya, and W.H. Moolenaar. 1994. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 126:801-810.
21. Kaibuchi, K., S. Kuroda, and M. Amano. 1999. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 68:459-486.
22. Kozma, R., S. Sarner, S. Ahmed, and L. Lim. 1997. Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell. Biol. 17:1201-1211.
23. Lambrechts, A., A. Braun, V. Jonckheere, A. Aszodi, L.M. Lanier, J. Robbens, I. Van Colen, J. Vandekerckhove, R. Fassler, and C. Ampe. 2000. Profilin II is alternatively spliced, resulting in profilin isoforms that are differentially expressed and have distinct biochemical properties. Mol. Cell. Biol. 20:8209-8219.
24. Leeuwen, F.N., H.E. Kain, R.A. Kammen, F. Michiels, O.W. Kranenburg, and J.G. Collard. 1997. The guanine nucleotide exchange factor Tiam1 affects neuronal morphology; opposing roles for the small GTPases Rac and Rho. J. Cell Biol. 139:797-807.
25. Leung, T., E. Manser, L. Tan, and L. Lim. 1995. A novel serine/threonine kinase binding the Ras-related RhoA GTPase which translocates the kinase to peripheral membranes. J. Biol. Chem. 270:29051-29054.
26. Liu, R.Y., R.S. Schmid, W.D. Snider, and P.F. Maness. 2002. NGF enhances sensory axon growth induced by laminin but not by the L1 cell adhesion molecule. Mol. Cell. Neurosci. 20:2-12.
27. Luo, L. 2000. Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 1:173-180.
28. Luo, L. 2002. Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu. Rev. Cell Dev. Biol. 18:601-635.
29. Maekawa, M., T. Ishizaki, S. Boku, N. Watanabe, A. Fujita, A. Iwamatsu, T. Obinata, K. Ohashi, K. Mizuno, and S. Narumiya. 1999. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science. 285:895-898.
30. Matsui, T., M. Amano, T. Yamamoto, K. Chihara, M. Nakafuku, M. Ito, T. Nakano, K. Okawa, A. Iwamatsu, and K. Kaibuchi. 1996. Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein. Rho. EMBO J. 15:2208-2216.
31. Nakagawa, O., K. Fujisawa, T. Ishizaki, Y. Saito, K. Nakao, and S. Narumiya. 1996. ROCK-I and ROCK-II, two isoforms of Rho-associated coiled-coil forming protein serine/threonine kinase in mice. FEBS Lett. 392:189-193.
32. Nakayama, A.Y., M.E. Harms, and L. Luo. 2000. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J. Nerrosci. 20:5329-5338.
33. Sagot, I., A.A. Rodal, J. Moseley, B.L. Goode, and D. Pellman. 2002. An actin nucleation mechanism mediated by Bni1 and profilin. Nat. Cell Biol. 4:626-631.
34. Schoenwaelder, S.M., S.C. Hughan, K. Boniface, S. Fernando, M. Holdsworth, P.E. Thompson, H.H. Salem, and S.P. Jackson. 2002. RhoA sustains integrin alpha IIbeta 3 adhesion contacts under high shear. J. Biol. Chem. 277:14738-14746.
35. Sekine, A., M. Fujiwara, and S. Narumiya. 1989. Asparagine residue in the rho gene product is the modification site for botulinum ADP-ribosyltransferase. J. Biol. Chem. 264:8602-8605.
36. Selden, L.A., H.J. Kinosian, J.E. Estes, and L.C. Gershman. 1999. Impact of profilin on actin-bound nucleotide exchange and actin polymerization dynamics. Biochemistry. 38:2769-2778.
37. Summerton, J., D. Stein, S.B. Huang, P. Matthews, D. Weller, and M. Partridge. 1997. Morpholino and phosphorothioate antisense oligomers compared in cell- free and in-cell systems. Antisense Nucleic Acid Drug Dev. 7:63-70.
38. Tapon, N., and A. Hall. 1997. Rho, Rac and Cdc42 GTPases regulate the organization of the actin cytoskeleton. Curr. Opin. Cell Biol. 9:86-92.
39. Verheyen, E.M., and L. Cooley. 1994. Profilin mutations disrupt multiple actin-dependent processes during Drosophila development. Development. 120:717-728.
40. Wills, Z., L. Marr, K. Zinn, C.S. Goodman, and D. Van Vactor. 1999. Profilin and the Abl tyrosine kinase are required for motor axon outgrowth in the Drosophila embryo. Neuron. 22:291-299.
41. Witke, W., A.V. Podtelejnikov, A. Di Nardo, J.D. Sutherland, C.B. Gurniak, C. Dotti, and M. Mann. 1998. In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly. EMBO J. 17:967-976.
42. Witke, W., J.D. Sutherland, A. Sharpe, M. Arai, and D.J. Kwiatkowski. 2001. Profilin I is essential for cell survival and cell division in early mouse development. Proc. Natl. Acad. Sci. USA. 98:3832-3836.
43. Wolven, A.K., L.D. Belmont, N.M. Mahoney, S.C. Almo, and D.G. Drubin. 2000. In vivo importance of actin nucleotide exchange catalyzed by profilin. J. Cell Biol. 15C:895-904.
44. Yamamoto, M., D.H. Hilgemann, S. Feng, H. Bito, H. Ishihara, Y. Shibasaki, and H.L. Yin. 2001. Phosphatidylinositol 4,5-bisphosphate induces actin stress-fiber formation and inhibits membrane ruffling in CV1 cells. J. Cell Biol. 152:867-876.
45. Yamashita, T., K.L. Tucker, and Y.A. Barde. 1999. Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron. 24:585-593.