Different roles for RhoA during neurite initiation, elongation, and regeneration in PC12 cells

Journal of Neurochemistry

Volumn 73, Issue 3, 1999, Pages 949-960

  Sebök, Ágnes ^a,b   Nusser, Nóra ^a,b   Debreceni, Balázs ^a   Guo, Zhong ^a   Santos, Marinilce F ^a   Szeberenyi, József ^b   Tigyi, Gábor ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF PÉCS   (Hungary)

Author keywords

Chemorepulsion; Differentiation; Lsyophosphatidic acid; Nerve growth factor; Neurite; PC12; Rho

Indexed keywords

CYCLIC AMP; GUANOSINE TRIPHOSPHATASE; NERVE GROWTH FACTOR; PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL DIFFERENTIATION; CELL DIVISION; CELL MEMBRANE; CELLS, CULTURED; CLONE CELLS; ENZYME ACTIVATION; GTP-BINDING PROTEINS; GTPASE-ACTIVATING PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; MUTATION; NERVE GROWTH FACTORS; NERVE REGENERATION; NEURITES; PC12 CELLS; PLASMIDS; RATS;

EID: 0032876024     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0730949.x     Document Type: Article

References (59)

1. Adamson P., Paterson H. F., and Hall A. (1992) Intracellular localization of the P21rho proteins. J. Cell Biol. 119, 617-627.
2. WAF1/CIP1 is upregulated by the geranyltransferase I inhibitor GGTI-298 through a transforming growth factor β and Sp1-responsive element: involvement of the small GTPase RhoA. Mol. Cell. Biol. 18, 6962-6970.
3. Avraham H. (1990) rho gene amplification and malignant transformation. Biochem. Biophys. Res. Commun. 168, 114-124.
4. Beltman J., Erickson J. R., Martin G. A., Lyons J. F., and Cook S. J. (1999) C3 toxin activates the stress signaling pathways, JNK and p 38, but antagonizes the activation of AP-1 in rat-1 cells. J. Biol. Chem. 274, 3772-3780.
5. Bottenstein J. E. (1985) Growth and differentiation of neural cells in defined media, in Cell Culture in the Neurosciences (Bottenstein J. E. and Sato G., eds), pp. 1-35. Plenum Press, New York.
6. Bottenstein J. E., Skaper S. D., Varon S. S., and Sato G. H. (1980) Selective survival of neurons from ganglionic dissociates utilizing serum-free supplemented medium. Exp. Cell Res. 25, 183-190.
7. Denhardt D. T. (1996) Signal-transducing protein phosphorylation cascades mediated by Ras/Rho proteins in the mammalian cell: the potential for multiple signaling. Biochem. J. 318, 729-747.
8. Dillon S. T. and Feig L. A. (1995) Purification and assay of recombinant C3 transferase. Methods Enzymol. 256, 174-184.
9. Dong J. M., Leung T., Manser E., and Lim L. (1998) cAMP-induced morphological changes are counteracted by the activated rhoA small GTPase and rho kinase ROKalpha. J. Biol. Chem. 273, 22554-22562.
10. Dyer D. L., Tigyi G., and Miledi R. (1991a) The effect of serum albumin on PC12 cells. I. Neunte retraction and activation of the phosphoinositide second messenger system. Mol. Brain Res. 14, 293-301.
11. Dyer D. L., Tigyi G., and Miledi R. (1991b) The effect of serum albumin on PC12 cells. II. Intracellular calcium transients and their role in neunte retraction. Mol. Brain Res. 14, 302-309.
12. Fleming I. N., Elliott C. M., and Exton J. H. (1996) Differential translocation of Rho family GTPases by lysophosphatic acid, endothelin-1, and platelet-derived growth factor. J. Biol. Chem. 271, 33067-33073.
13. Greene L. A. and Kaplan D. R. (1995) Early events in neurotrophin signaling via Trk and p75 receptors. Curr. Opin. Neurobiol. 5, 579-587.
14. Greene L. A. and Tischler A. S. (1982) PC12 pheochromocytoma cultures in neurobiological research. Adv. Cell Neurobiol. 3, 373-414.
15. Hall A. (1998) Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
16. 2-terminal kinases. Mol. Cell. Biol. 16, 648-656.
17. 1 to S phase in growth-stimulated Rat FRTL-5 cells. J. Biol. Chem. 272, 13-16.
18. Jahner D. and Hunter T. (1991) The ras-related gene rhoB is an immediate-early gene inducible by v-Fps, epidermal growth factor, and platelet-derived growth factor in rat fibroblasts. Mol. Cell. Biol. 11, 3682-3690.
19. Jalink K., Eichholtz T., Postma F. R., van Corven E. J., and Moolenaar W. H. (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., van Corven E. J., Hengeveld T., Morii N., Narumiya S., and Moolenaar W. H. (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. Jin Z. and Strittmatter S. (1997) Rac1 mediates collapsin-1-induced growth cone collapse. J. Neurosci. 17, 6256-6263.
22. Kamata Y., Nishiki T., Matsumura K., Hiroi T., and Kozaki S. (1994) Morphological effects, rate of incorporation, and the enzymatic action of botulinum ADP-ribosyltransferase, known as C3 exoenzyme, on human neuroblastoma GOTO cells. Microbiol. Immunol. 38, 421-428.
23. Katoh H., Aoki J., Ichikawa A., and Negishi M. (1998) p160 RhoA-binding kinase ROKα induces neurite retraction. J. Biol. Chem. 273, 2489-2492.
24. Khosravi-Far R., Solski P. A., Clark G. J., Kinch M. S., and Der C. J. (1995) Activation of Rac1, RhoA, and mitogen-activated protein kinases is required for Ras transformation. Mol. Cell. Biol. 15, 6443-6453.
25. Kozma R., Sarner S., Ahmed S., and Lim L. (1997) Rho family GTPases and neuronal growth cone remodeling: relationship between increased complexity induced by Cdc42Hs, Rac1 and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell Biol. 17, 1201-1211.
26. Kranenburg O., Poland M., Gebbink M., Oomen L., and Moolenaar W. H. (1997) Dissociation of LPA-induced cytoskeletal contraction from stress fiber formation by differential localization of RhoA. J. Cell Sci. 110, 2417-2427.
27. Kuhn T. B., Brown M. D., Wilcox C. L., Raper J. A., and Bamburg J. R. (1999) Myelin and collapsin-1 induce motor neuron growth cone collapse through different pathways: inhibition of collapse by opposing mutants of Rac1. J. Neurosci. 19, 1965-1975.
28. Lang P., Gesbert F., Delespine-Carmagnat M., Stancou R., Pouchelet M., and Bertoglio J. (1996) Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J. 15, 510-519.
29. Laudanna C., Campbell J. J., and Butcher E. C. (1996) Role of Rho in chemoattractant-activated leukocyte adhesion through integrins. Science 271, 981-983.
30. Lebowitz P. F., Davide J. P., and Prendergast G. C. (1995) Evidence that farnesyltransferase inhibitors suppress Ras transformation by interfering with Rho activity. Mol. Cell. Biol. 15, 6613-6622.
31. Lehman M., Fournier A., Leclerc N., Tigyi G., and McKerracher L. (1997) Role of Rho in regulating inhibition of neunte growth by myelin-associated glycoprotein (MAG). Mol. Biol. Cell (Suppl. 8), 284.
32. Liliom K., Fischer D., Virag T., Sun G., Miller D. D., Tseng J.-L., Desiderio D. M., Seidel M. C., Erickson J. R., and Tigyi G. (1998) Identification of a novel growth factor-like lipid: 1-O-cis-alk-1′-enyl-2-lyso-sn-glycero-3-phosphate (alkenyl GP) that is present in commercial sphingolipid preparations. J. Biol. Chem. 273, 13461-13468.
33. Luo L., Liao Y. J., Jan L., and Jan Y. N. (1994) Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8, 1787-1802.
34. Luo L., Hensch T. K., Ackerman L., Barbel S., Jan L. Y., and Jan Y. N. (1996) Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines. Nature 379, 837-840.
35. Mackay D. J., Nobes C. D., and Hall A. (1995) The Rho's progress: a potential role during neuritogenesis for the Rho family of GTPases. Trends Neurosci. 18, 496-501.
36. Narumiya S. (1996) The small GTPase Rho: cellular functions and signal transduction. Biochem. J. 120, 215-228.
37. Nishiki T., Narumiya S., Morii N., Yamamoto M., Fujiwara M., Kamata Y., Sakaguchi G., and Kozaki S. (1990) ADP-ribosylation of the rho/rac proteins induces growth inhibition, neurite outgrowth and acetylcholine esterase in cultured PC-12 cells. Biochem. Biophys. Res. Commun. 167, 265-272.
38. Nobes C. D. and Hall A. (1995) Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
39. Olson M. F., Ashworth A., and Hall A. (1995) An essential role for Rho, Rac, and Cdc42 GTPases in cell cycle progression through G1. Science 269, 1270-1272.
40. Waf1/Cip1. Nature 394, 295-299.
41. Paterson H., Self A. J., Garrett M. D., Just I., Aktories K., and Hall A. (1990) Microinjection of recombinant p21rho induces rapid changes in cell morphology. J. Cell Biol. 111, 1001-1007.
42. Postma F. R., Jalink K., Hengeveld T., and Moolenaar W. H. (1996) Sphingosine-1-phosphate rapidly induces Rho-dependent neurite retraction: action through a specific cell surface receptor. EMBO J. 15, 2388-2392.
43. Qiu M. S. and Green S. H. (1992) PC12 cell neuronal differentiation is associated with prolonged p21ras activity and consequent prolonged ERK activity. Neuron 9, 705-707.
44. Qiu R. G., Chen J., Kirn D., McCormick F., and Symons M. (1995a) An essential role for Rac in Ras transformation. Nature 374, 457-459.
45. Qiu R. G., Chen J., McCormick F., and Symons M. (1995b) A role for Rho in Ras transformation. Proc. Natl Acad. Sci. USA 92, 11781-11785.
46. Robertson D., Paterson H. F., Adamson P., Hall A., and Monaghan P. (1995) Ultrastructural localization of ras-related proteins using epitope-tagged plasmids. J. Histochem. Cytochem. 43, 471-480.
47. Santos M., McCormack S., Guo Z., Okolicany J., Zheng Y., Johnson L., and Tigyi G. (1997) Rho proteins play a critical role in cell migration during the early phase of mucosal restitution. J. Clin. Invest. 100, 216-225.
48. Sebök A., Fischer D., Nusser N., Santos M. F., Zheng Y., and Tigyi G. (1996) Rho regulates neurite outgrowth in PC12 cells. Soc. Neurosci. Abstr. 22, 737.
49. Sekine A., Fujiwara M., and Narumiya S. (1989) Asparagine residue in the rho gene product is the modification site for botulinum ADP-ribosyltransferase. J. Biol. Chem. 264, 8602-8605.
50. Szeberenyi J. (1991) NGF-induced neurite regeneration is mediated by a ras-independent pathway in PC12 cells. Acta Biol. Hung. 42, 365-369.
51. Takahashi H. and Guroff G. (1993) Evidence for an indirect effect of nerve growth factor (NGF) on the ADP-ribosylation of a 22 kDa rho-like protein in PC12 cells. Biochem. Biophys. Res. Commun. 190, 1156-1162.
52. Takaishi K., Sasaki T., Kameyama T., Tsukita S., and Takai Y. (1995) Translocation of activated Rho from the cytoplasm to membrane ruffling area, cell-cell adhesion sites and cleavage furrows. Oncogene 11, 39-48.
53. Threadgill R., Bobb K., and Ghosh A. (1997) Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 19, 625-634.
54. Tigyi G. and Miledi R. (1992) Lysophosphatidates bound to serum albumin activate membrane currents in Xenopus oocytes and neurite retraction in PC12 pheochromocytoma cells. J. Biol. Chem. 267, 21360-21367.
55. 2+ signaling and Rho. J. Neurochem. 66, 537-548.
56. Tigyi G., Fischer D. J., Sebök A., Marshall F., Dyer D. L., and Miledi R. (1996b) Lysophosphatidic acid-induced neurite retraction in PC12 cells: neurite-protective effects of cyclic AMP signaling. J. Neurochem. 66, 549-558.
57. KIP1. J. Biol. Chem. 272, 32966-32971.
58. Wylie S. R., Wu P.-J., Patel H., and Chantler P. D. (1998) A conventional myosin motor drives neurite outgrowth. Proc. Natl. Acad. Sci. USA 95, 12967-12972.
59. Zipkin I., Kindt R., and Kenyon C. (1997) Role of a new Rho family member in cell migration and axon guidance in C. elegans. Cell 90, 883-894.