Plasticity-related gene 5 (PRG5) induces filopodia and neurite growth and impedes lysophosphatidic acid- and nogo-A-mediated axonal retraction

Molecular Biology of the Cell

Volumn 21, Issue 4, 2010, Pages 521-537

  Broggini, Thomas ^a   Nitsch, Robert ^b   Savaskan, Nic E ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOPHOSPHATIDIC ACID; PROTEIN CDC42; PROTEIN NOGO A; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DEVELOPMENT; CELL MEMBRANE; CONTROLLED STUDY; FILOPODIUM; GENE; GENE EXPRESSION; MOLECULAR CLONING; MOUSE; NERVE CELL; NERVE CONDUCTION; NERVE FIBER GROWTH; NERVOUS SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASTICITY RELATED GENE 5; PRIORITY JOURNAL; RAT; SPINAL CORD;

AMINO ACID SEQUENCE; ANIMALS; AXONS; BRAIN; CDC42 GTP-BINDING PROTEIN; CELLS, CULTURED; LYSOPHOSPHOLIPIDS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MYELIN PROTEINS; NERVE TISSUE PROTEINS; NEURITES; NEURONS; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN CONFORMATION; PSEUDOPODIA; RATS; RATS, WISTAR; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SPINAL CORD;

EID: 76649144791     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-06-0506     Document Type: Article

References (67)

1. Abe, T., Kato, M., Miki, H., Takenawa, T., Endo, T. (2003). Small GTPase Tc10 and its homologue RhoT induce N-WASP-mediated long process formation and neurite outgrowth. J. Cell Sci. 116, 155-168.
2. Arakawa, Y., Bito, H., Furuyashiki, T., Tsuji, T., Takemoto-Kimura, S., Kimura, K., Nozaki, K., Hashimoto, N., and Narumiya, S. (2003). Control of axon elongation via an SDF-1alpha/Rho/mDia pathway in cultured cerebellar granule neurons. J. Cell Biol. 161, 381-391.
3. Atwal, J. K., Pinkston-Gosse, J., Syken, J., Stawicki, S., Wu, Y., Shatz, C., and Tessier-Lavigne, M. (2008). PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 322, 967-970.
4. Benfey, M., and Aguayo, A. J. (1982). Extensive elongation of axons from rat brain into peripheral nerve graft. Nature 296, 150-152.
5. Bräuer, A. U., Savaskan, N. E., Kühn, H., Prehn, S., Ninnemann, O., and Nitsch, R. (2003). A new phospholipid phosphatase, PRG-1, is involved in axon growth and regenerative sprouting. Nat. Neurosci. 6, 572-578.
6. Carramusa, L., Ballestrem, C., Zilberman, Y., and Bershadsky, A. D. (2007). Mammalian diaphanous-related formin Dia1 controls the organization of E-cadherin-mediated cell-cell junctions. J. Cell Sci. 120, 3870-3882.
7. Chen, M. S., Huber, A. B., van der Haar, M. E., Frank, M., Schnell, L., Spillmann, A. A., Christ, F., and Schwab, M. E. (2000). Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403, 434-439.
8. David, S., and Aguayo, A. J. (1981). Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214, 931-933.
9. Etienne-Manneville, S., and Hall, A. (2002). Rho GTPases in cell biology. Nature 420, 629-635.
10. Evangelista, M., Zigmond, S., and Boone, C. (2003). Formins: signaling effectors for assembly and polarization of actin filaments. J. Cell Sci. 116, 2603-2611.
11. Faix, J., Breitsprecher, D., Stradal, T. E., and Rottner, K. (2009). Filopodia: complex models for simple rods. Int. J. Biochem. Cell Biol. 41, 1656-1664.
12. Fournier, A. E., GrandPre, T., and Strittmatter, S. M. (2001). Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409, 341-346.
13. Fujiwara, T., Mammoto, A., Kim, Y., and Takai, Y. (2000). Rho small G-protein-dependent binding of mDia to an Src homology 3 domain-containing IRSp53/BAIAP2. Biochem. Biophys. Res. Commun. 271, 626-629.
14. Gallo, G., and Letourneau, P. C. (1998). Localized sources of neurotrophins initiate axon collateral sprouting. J. Neurosci. 18(14), 5403-5414.
15. GrandPré, T., Nakamura, F., Vartanian, T., and Strittmatter, S. M. (2000). Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature 403, 439-444.
16. GrandPré, T., Li, S., and Strittmatter, S. M. (2002). Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 417, 547-551.
17. Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
18. Harel, N. Y., and Strittmatter, S. M. (2006). Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury? Nat. Rev. Neurosci. 7(8), 603-616.
19. He, Z., and Koprivica, V. (2004). The Nogo signaling pathway for regeneration block. Annu. Rev. Neurosci. 27, 341-368.
20. Inoue, M., Rashid, M. H., Fujita, R., Contos, J. J., Chun, J., and Ueda, H. (2004). Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling. Nat. Med. 10(7), 712-718.
21. Jain, A., Brady-Kalnay, S. M., and Bellamkonda, R. V. (2004). Modulation of Rho GTPase activity alleviates chondroitin sulfate proteoglycan-dependent inhibition of neurite extension. J. Neurosci. Res. 77(2), 299-307.
22. 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(3), 801-810.
23. Kai, M., Wada, I., Imai, S., Sakane, F., and Kanoh, H. (1996). Identification and cDNA cloning of 35-kDa phosphatidic acid phosphatase (type 2) bound to plasma membranes. Polymerase chain reaction amplification of mouse H2O2-inducible hic53 clone yielded the cDNA encoding phosphatidic acid phosphatase. J. Biol. Chem. 271, 18931-18938.
24. Kai, M., Wada, I., Imai, S., Sakane, F., and Kanoh, H. (1997). Cloning and characterization of two human isozymes of Mg2+-independent phosphatidic acid phosphatase. J. Biol. Chem. 272, 24572-24578.
25. Kanoh, H., Kai, M., and Wada, I. (1997). Phosphatidic acid phosphatase from mammalian tissues: discovery of channel-like proteins with unexpected functions. Biochim. Biophys. Acta. 1348, 56-62.
26. Korobova, F., and Svitkina, T. (2008). Arp2/3 complex is important for filopodia formation, growth cone motility, and neuritogenesis in neuronal cells. Mol. Biol. Cell 19(4), 1561-1574.
27. Kozma, R., Sarner, S., Ahmed, S., and Lim, L. (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.
28. Kranenburg, O., Poland, M., van Horck, F. P., Drechsel, D., Hall, A., and Moolenaar, W. H. (1999). Activation of RhoA by lysophosphatidic acid and Galpha12/13 subunits in neuronal cells: induction of neurite retraction. Mol. Biol. Cell 10(6), 1851-1857.
29. Lein E. S., et al. (2007). Genome-wide atlas of gene expression in the adult mouse brain Nature 445, 168-176.
30. Lommel, S., Benesch, S., Rottner, K., Franz, T., Wehland, J., and Kühn, R. (2001). Actin pedestal formation by enteropathogenic Escherichia coli and intracellular motility of Shigella flexneri are abolished in N-WASP-defective cells. EMBO Rep. 2, 850-857.
31. Machesky, L. M., and Insall, R. H. (1998). Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr. Biol. 8(25), 1347-1356.
32. Mattila, P. K., and Lappalainen, P. (2008). Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9(6), 446-454.
33. Matusek, T., Gombos, R., Szécsényi, A., Sánchez-Soriano, N., Czibula, A., Pataki, C., Gedai, A., Prokop, A., Raskó, I., and Mihály, J. (2008). Formin proteins of the DAAM subfamily play a role during axon growth. J. Neurosci. 28(49), 13310-13319.
34. Mellor, H. (2009). The role of formins in filopodia formation. Biochim. Biophys. Acta Epub ahead of print.
35. Miao, R. Q., Gao, Y., Harrison, K. D., Prendergast, J., Acevedo, L. M., Yu, J., Hu, F., Strittmatter, S. M., and Sessa, W. C. (2006). Identification of a receptor necessary for Nogo-B stimulated chemotaxis and morphogenesis of endothelial cells. Proc. Natl. Acad. Sci. USA 103(29), 10997-11002.
36. Moolenaar, W. H. (1994). LPA: a novel lipid mediator with diverse biological actions. Trends Cell Biol. 4(6), 213-219.
37. Naito, Y., Yamada, T., Matsumiya, T., Ui-Tei, K., Saigo, K., and Morishita, S. (2005). dsCheck: highly sensitive off-target search software for double-stranded RNA-mediated RNA interference. Nucleic Acids Res. 33, W589-W591.
38. Nobes, C. D., and Hall, A. (1995a). Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem. Soc. Trans. 23, 456-459.
39. Nobes, C. D., and Hall, A. (1995b). Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
40. O'Donnell, M., Chance, R. K, and Bashaw, G. J. (2009). Axon growth and guidance: receptor regulation and signal transduction. Annu. Rev. Neurosci. 32, 383-412.
41. Passey, S., Pellegrin, S., and Mellor, H. (2004). What is in a filopodium? Starfish versus hedgehogs. Biochem. Soc. Trans. 32(Pt 6), 1115-1117.
42. Peng, J., Wallar, B. J., Flanders, A., Swiatek, P. J., and Alberts, A. S. (2003). Disruption of the Diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42. Curr. Biol. 13, 534-545.
43. Prehoda, K. E., Scott, J. A., Mullins, R. D., and Lim, W. A. (2000). Integration of multiple signals through cooperative regulation of the N-WASP-Arp2/3 complex. Science 290, 801-806.
44. Prinjha, R., Moore, S. E., Vinson, M., Blake, S., Morrow, R., Christie, G., Michalovich, D., Simmons, D. L., and Walsh, F. S. (2000). Inhibitor of neurite outgrowth in humans. Nature 403, 383-384.
45. Ridley, A. J. (2006). Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16(10), 522-529.
46. Rohatgi, R., Ma, L., Miki, H., Lopez, M., Kirchhausen, T., Takenawa, T., and Kirschner, M. W. (1999). The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97(2), 221-231.
47. Sarmiento, C., et al. (2008). WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. J. Cell Biol. 180, 1245-1260.
48. Savaskan, N. E., and Nitsch, R. (2001). Molecules involved in reactive sprouting in the hippocampus. Rev. Neurosci. 12(3), 195-215.
49. Savaskan, N. E., Brauer, A. U., and Nitsch, R. (2004). Molecular cloning and expression regulation of PRG-3, a new member of the plasticity-related gene family. Eur. J. Neurosci. 19(1), 212-220.
50. Savaskan, N. E., et al. (2007). Autotaxin (NPP-2) in the brain: cell type-specific expression and regulation during development and after neurotrauma. Cell Mol. Life Sci. 64(2), 230-243.
51. Svitkina, T. M., Bulanova, E. A., Chaga, O. Y., Vignjevic, D. M., Kojima, S., Vasiliev, J. M., and Borisy, G. G. (2003). Mechanism of filopodia initiation by reorganization of a dendritic network. J. Cell Biol. 160(3), 409-421.
52. Schnell, L., and Schwab, M. E. (1990). Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343, 269-272.
53. Sigal, Y. J., McDermott, M. I., and Morris, A. J. (2005). Integral membrane lipid phosphatases/phosphotransferases: common structure and diverse functions. Biochem. J. 387, 281-293.
54. Sigal, Y. J., Quintero, O. A., Cheney, R. E., and Morris, A. J. (2007). Cdc42 and ARP2/3-independent regulation of filopodia by an integral membrane lipid-phosphatase-related protein. J. Cell Sci. 120, 340-352.
55. Silver, J., and Miller J. H. (2004). Regeneration beyond the glial scar. Nat. Rev. Neurosci. 146-156.
56. Snapper, S. B., et al. (2001). N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat. Cell Biol. 3, 897-904.
57. Stein, E., Savaskan, N. E., Ninnemann, O., Nitsch, R., Zhou, R., and Skutella, T. (1999). A role for the Eph ligand ephrin-A3 in entorhino- hippocampal axon targeting. J. Neurosci. 19(20), 8885-93.
58. Steup, A., Ninnemann, O., Savaskan, N. E., Nitsch, R., Püschel, A. W., and Skutella, T. (1999). Semaphorin D acts as a repulsive factor for entorhinal and hippocampal neurons. Euro. J. Neurosci. 11, 729-734.
59. Steup, A., Lohrum, M., Hamscho, N., Savaskan, N. E., Ninnemann, O., Nitsch, R., Fujisawa, H., Püschel, A. W., and Skutella, T. (2000). Sema3C and netrin-1 differentially affect axon growth in the hippocampal formation. Mol. Cell Neurosci. 15(2), 141-155.
60. Sun, L., et al. (2005). Cloning and characterization of a novel human phosphatidic acid phosphatase type 2, PAP2d, with two different transcripts PAP2d-v1 and PAP2d-v2. Mol. Cell Biochem. 272(1-2), 91-96.
61. Tanabe, K., Tachibana, T., Yamashita, T., Che, Y. H., Yoneda, Y., Ochi, T., Tohyama, M., Yoshikawa, H., and Kiyama, H. (2000). The small GTP-binding protein TC10 promotes nerve elongation in neuronal cells, and its expression is induced during nerve regeneration in rats. J. Neurosci. 20(11), 4138-4144.
62. Tessier-Lavigne, M., and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
63. Tominaga, T., Sahai, E., Chardin, P., McCormick, F., Courtneidge, S. A., and Alberts, A. S. (2000). Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol. Cell 5, 13-25.
64. Trimbuch, T., et al. (2009). Synaptic PRG-1 modulates excitatory transmission via lipid phosphate-mediated signaling. Cell 138(6), 1222-1235.
65. Wang, X., Chun, S. J., Treloar, H., Vartanian, T., Greer, C. A., and Strittmatter, S. M. (2002). Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J. Neurosci. 22(13), 5505-5515.
66. Watanabe, N., Madaule, P., Reid, T., Ishizaki, T., Watanabe, G., Kakizuka, A., Saito, Y., Nakao, K., Jockusch, B. M., and Narumiya, S. (1997). p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J. 16, 3044-3056.
67. Whitford, K. L., Dijkhuizen, P., Polleux, F., and Ghosh, A. (2002). Molecular control of cortical dendrite development. Annu. Rev. Neurosci. 25, 127-149.