Rac1 Selective Activation Improves Retina Ganglion Cell Survival and Regeneration

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Lorenzetto, Erika ^a   Ettorre, Michele ^a   Pontelli, Valeria ^a   Bolomini Vittori, Matteo ^a   Bolognin, Silvia ^a   Zorzan, Simone ^a   Laudanna, Carlo ^a   Buffelli, Mario ^a,b  

^a UNIVERSITY OF VERONA   (Italy)

^b National Institute of Neuroscience   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; P21 ACTIVATED KINASE 1; RAC1 PROTEIN; TRANSACTIVATOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ELONGATION; CELL SURVIVAL; CONTROLLED STUDY; DENDRITE; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; GLIA CELL; MOUSE; MUTATION; NERVE CELL; NERVE FIBER; NERVE FIBER REGENERATION; NONHUMAN; OPTIC NERVE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RETINA GANGLION CELL; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; CELL SURVIVAL; FLUORESCENT ANTIBODY TECHNIQUE; LUMINESCENT PROTEINS; MICE; MICE, INBRED CBA; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUTATION; NERVE CRUSH; NERVE REGENERATION; NEUROPEPTIDES; OPTIC NERVE; OPTIC NERVE INJURIES; P21-ACTIVATED KINASES; PHOSPHORYLATION; RAC1 GTP-BINDING PROTEIN; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; TIME FACTORS;

MAMMALIA;

EID: 84878442507     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064350     Document Type: Article

References (52)

1. Schwab JM, Brechtel K, Mueller CA, Failli V, Kaps HP, et al. (2006) Experimental strategies to promote spinal cord regeneration-an integrative perspective. Prog Neurobiol 78: 91-116.
2. Liu K, Tedeschi A, Park KK, He Z, (2011) Neuronal intrinsic mechanisms of axon regeneration. Annu Rev Neurosci 34: 131-152.
3. Di Giovanni S, (2009) Molecular targets for axon regeneration: focus on the intrinsic pathways. Expert Opin Ther Targets 13: 1387-1398.
4. de Lima S, Koriyama Y, Kurimoto T, Oliveira JT, Yin Y, et al. (2012) Full-length axon regeneration in the adult mouse optic nerve and partial recovery of simple visual behaviors. Proc Natl Acad Sci U S A 109: 9149-9154.
5. Gaub P, Joshi Y, Wuttke A, Naumann U, Schnichels S, et al. (2011) The histone acetyltransferase p300 promotes intrinsic axonal regeneration. Brain 134: 2134-2148.
6. Hall A, Lalli G, (2010) Rho and Ras GTPases in axon growth, guidance, and branching. Cold Spring Harb Perspect Biol 2: a001818.
7. Jain A, Brady-Kalnay SM, Bellamkonda RV, (2004) Modulation of Rho GTPase activity alleviates chondroitin sulfate proteoglycan-dependent inhibition of neurite extension. J Neurosci Res 77: 299-307.
8. Jain A, McKeon RJ, Brady-Kalnay SM, Bellamkonda RV, (2011) Sustained delivery of activated Rho GTPases and BDNF promotes axon growth in CSPG-rich regions following spinal cord injury. PLoS One 6: e16135.
9. Linseman DA, Laessig T, Meintzer MK, McClure M, Barth H, et al. (2001) An essential role for Rac/Cdc42 GTPases in cerebellar granule neuron survival. J Biol Chem 276: 39123-39131.
10. Le SS, Loucks FA, Udo H, Richardson-Burns S, Phelps RA, et al. (2005) Inhibition of Rac GTPase triggers a c-Jun- and Bim-dependent mitochondrial apoptotic cascade in cerebellar granule neurons. J Neurochem 94: 1025-1039.
11. Kusano K, Enomoto M, Hirai T, Wakabayashi Y, Itoh S, et al. (2011) Enhancement of sciatic nerve regeneration by adenovirus-mediated expression of dominant negative RhoA and Rac1. Neurosci Lett 492: 64-69.
12. Tybulewicz VL, Henderson RB, (2009) Rho family GTPases and their regulators in lymphocytes. Nat Rev Immunol 9: 630-644.
13. Lamarche N, Tapon N, Stowers L, Burbelo PD, Aspenstrom P, et al. (1996) Rac and Cdc42 induce actin polymerization and G1 cell cycle progression independently of p65PAK and the JNK/SAPK MAP kinase cascade. Cell 87: 519-529.
14. Nikolic M, Chou MM, Lu W, Mayer BJ, Tsai LH, (1998) The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 395: 194-198.
15. Bolomini-Vittori M, Montresor A, Giagulli C, Staunton D, Rossi B, et al. (2009) Regulation of conformer-specific activation of the integrin LFA-1 by a chemokine-triggered Rho signaling module. Nat Immunol 10: 185-194.
16. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, et al. (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28: 41-51.
17. Livet J, Weissman TA, Kang H, Draft RW, Lu J, et al. (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450: 56-62.
18. Bertrand J, Di Polo A, McKerracher L, (2007) Enhanced survival and regeneration of axotomized retinal neurons by repeated delivery of cell-permeable C3-like Rho antagonists. Neurobiol Dis 25: 65-72.
19. Berkelaar M, Clarke DB, Wang YC, Bray GM, Aguayo AJ, (1994) Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J Neurosci 14: 4368-4374.
20. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI, (2000) Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci 20: 4615-4626.
21. Kostyk SK, D'Amore PA, Herman IM, Wagner JA, (1994) Optic nerve injury alters basic fibroblast growth factor localization in the retina and optic tract. J Neurosci 14: 1441-1449.
22. Benowitz LI, Popovich PG, (2011) Inflammation and axon regeneration. Curr Opin Neurol 24: 577-583.
23. Cui Q, Yip HK, Zhao RC, So KF, Harvey AR, (2003) Intraocular elevation of cyclic AMP potentiates ciliary neurotrophic factor-induced regeneration of adult rat retinal ganglion cell axons. Mol Cell Neurosci 22: 49-61.
24. Leung CK, Weinreb RN, Li ZW, Liu S, Lindsey JD, et al. (2011) Long-term in vivo imaging and measurement of dendritic shrinkage of retinal ganglion cells. Invest Ophthalmol Vis Sci 52: 1539-1547.
25. Lin R, Cerione RA, Manor D, (1999) Specific contributions of the small GTPases Rho, Rac, and Cdc42 to Dbl transformation. J Biol Chem 274: 23633-23641.
26. Zhang QG, Wang R, Han D, Dong Y, Brann DW, (2009) Role of Rac1 GTPase in JNK signaling and delayed neuronal cell death following global cerebral ischemia. Brain Res 1265: 138-147.
27. Chen L, Melendez J, Campbell K, Kuan CY, Zheng Y, (2009) Rac1 deficiency in the forebrain results in neural progenitor reduction and microcephaly. Dev Biol 325: 162-170.
28. Loucks FA, Le SS, Zimmermann AK, Ryan KR, Barth H, et al. (2006) Rho family GTPase inhibition reveals opposing effects of mitogen-activated protein kinase kinase/extracellular signal-regulated kinase and Janus kinase/signal transducer and activator of transcription signaling cascades on neuronal survival. J Neurochem 97: 957-967.
29. Johnson K, D'Mello SR, (2005) p21-Activated kinase-1 is necessary for depolarization-mediated neuronal survival. J Neurosci Res 79: 809-815.
30. Marra C, Gomes Moret D, de Souza Correa A, Chagas da Silva F, Moraes P, et al. (2011) Protein kinases JAK and ERK mediate protective effect of interleukin-2 upon ganglion cells of the developing rat retina. J Neuroimmunol 233: 120-126.
31. Peng PH, Chiou LF, Chao HM, Lin S, Chen CF, et al. (2010) Effects of epigallocatechin-3-gallate on rat retinal ganglion cells after optic nerve axotomy. Exp Eye Res 90: 528-534.
32. Nakatani M, Shinohara Y, Takii M, Mori H, Asai N, et al. (2011) Periocular injection of in situ hydrogels containing Leu-Ile, an inducer for neurotrophic factors, promotes retinal ganglion cell survival after optic nerve injury. Exp Eye Res 93: 873-879.
33. Pernet V, Hauswirth WW, Di Polo A, (2005) Extracellular signal-regulated kinase 1/2 mediates survival, but not axon regeneration, of adult injured central nervous system neurons in vivo. J Neurochem 93: 72-83.
34. Hisanaga S, Endo R, (2010) Regulation and role of cyclin-dependent kinase activity in neuronal survival and death. J Neurochem 115: 1309-1321.
35. Cheung ZH, Gong K, Ip NY, (2008) Cyclin-dependent kinase 5 supports neuronal survival through phosphorylation of Bcl-2. J Neurosci 28: 4872-4877.
36. Zhong JL, Banerjee MD, Nikolic M, (2003) Pak1 and its T212 phosphorylated form accumulate in neurones and epithelial cells of the developing rodent. Dev Dyn 228: 121-127.
37. Mendoza-Naranjo A, Contreras-Vallejos E, Henriquez DR, Otth C, Bamburg JR, et al. (2012) Fibrillar amyloid-beta1-42 modifies actin organization affecting the cofilin phosphorylation state: a role for Rac1/cdc42 effector proteins and the slingshot phosphatase. J Alzheimers Dis 29: 63-77.
38. Muller A, Hauk TG, Leibinger M, Marienfeld R, Fischer D, (2009) Exogenous CNTF stimulates axon regeneration of retinal ganglion cells partially via endogenous CNTF. Mol Cell Neurosci 41: 233-246.
39. Lorber B, Berry M, Logan A, (2005) Lens injury stimulates adult mouse retinal ganglion cell axon regeneration via both macrophage- and lens-derived factors. Eur J Neurosci 21: 2029-2034.
40. Berry M, Ahmed Z, Lorber B, Douglas M, Logan A, (2008) Regeneration of axons in the visual system. Restor Neurol Neurosci 26: 147-174.
41. Sun F, Park KK, Belin S, Wang D, Lu T, et al. (2011) Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature.
42. Luo L, Liao YJ, Jan LY, Jan YN, (1994) Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 8: 1787-1802.
43. Linseman DA, Loucks FA, (2008) Diverse roles of Rho family GTPases in neuronal development, survival, and death. Front Biosci 13: 657-676.
44. Marler KJ, Kozma R, Ahmed S, Dong JM, Hall C, et al. (2005) Outgrowth of neurites from NIE-115 neuroblastoma cells is prevented on repulsive substrates through the action of PAK. Mol Cell Biol 25: 5226-5241.
45. Rashid T, Banerjee M, Nikolic M, (2001) Phosphorylation of Pak1 by the p35/Cdk5 kinase affects neuronal morphology. J Biol Chem 276: 49043-49052.
46. Banerjee M, Worth D, Prowse DM, Nikolic M, (2002) Pak1 phosphorylation on t212 affects microtubules in cells undergoing mitosis. Curr Biol 12: 1233-1239.
47. Nikolic M, (2002) The role of Rho GTPases and associated kinases in regulating neurite outgrowth. Int J Biochem Cell Biol 34: 731-745.
48. Kreis P, Barnier JV, (2009) PAK signalling in neuronal physiology. Cell Signal 21: 384-393.
49. Fujimura M, Usuki F, Kawamura M, Izumo S, (2011) Inhibition of the Rho/ROCK pathway prevents neuronal degeneration in vitro and in vivo following methylmercury exposure. Toxicol Appl Pharmacol 250: 1-9.
50. Fujimura M, Usuki F, Sawada M, Rostene W, Godefroy D, et al. (2009) Methylmercury exposure downregulates the expression of Racl and leads to neuritic degeneration and ultimately apoptosis in cerebrocortical neurons. Neurotoxicology 30: 16-22.
51. Yang D, Sun YY, Lin X, Baumann JM, Dunn RS, et al. (2013) Intranasal delivery of cell-penetrating anti-NF-kappaB peptides (Tat-NBD) alleviates infection-sensitized hypoxic-ischemic brain injury. Exp Neurol.
52. Dhuria SV, Hanson LR, Frey WH, 2nd (2010) Intranasal delivery to the central nervous system: mechanisms and experimental considerations. J Pharm Sci 99: 1654-1673.