Interactive effects of C3, cyclic AMP and ciliary neurotrophic factor on adult retinal ganglion cell survival and axonal regeneration

Molecular and Cellular Neuroscience

Volumn 34, Issue 1, 2007, Pages 88-98

  Hu, Ying ^a   Cui, Qi ^a   Harvey, Alan R ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

C3 transferase; Cyclic nucleotides; Cytokines; Neurotrauma; Optic nerve injury

Indexed keywords

BA 210; BETA III TUBULIN; BETA TUBULIN; CELL ANTIBODY; CELL PERMEANT ANALOGUE OF CYCLIC AMP; CILIARY NEUROTROPHIC FACTOR; CYCLIC AMP; CYCLIC AMP DERIVATIVE; EXOENZYME C3; FLUOROGOLD; PAN NEUROFILAMENT ANTIBODY; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOGRAFT; CELL LABELING; CELL SURVIVAL; CELL VIABILITY; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG MECHANISM; ENZYME INACTIVATION; FEMALE; IMMUNOHISTOCHEMISTRY; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NERVE GRAFT; NERVE TRANSPLANTATION; NERVOUS SYSTEM INJURY; NONHUMAN; OPTIC NERVE INJURY; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RETINA GANGLION CELL;

ADP RIBOSE TRANSFERASES; AGE FACTORS; ANIMALS; AXOTOMY; BOTULINUM TOXINS; CELL COUNT; CELL SURVIVAL; CILIARY NEUROTROPHIC FACTOR; CYCLIC AMP; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; FEMALE; GROWTH CONES; NERVE REGENERATION; RATS; RATS, INBRED F344; RETINAL GANGLION CELLS; THIONUCLEOTIDES; TUBULIN;

EID: 33845903340     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2006.10.005     Document Type: Article

References (88)

1. Ahmed Z., Suggate E.L., Brown E.R., Dent R.G., Armstrong S.J., Barrett L.B., Berry M., and Logan A. Schwann cell-derived factor-induced modulation of the NgR/p75NTR/EGFR axis disinhibits axon growth through CNS myelin in vivo and in vitro. Brain 129 (2006) 1517-1533
2. Bähr M., and Przyrembel C. Myelin from peripheral and central nervous system is a nonpermissive substrate for retinal ganglion cell axons. Exp. Neurol. 134 (1995) 87-93
3. Bandtlow C.E. Regeneration in the central nervous system. Exp. Gerontol. 38 (2003) 79-86
4. Berkelaar M., Clarke D.B., Wang Y.C., Bray G.M., and Aguayo A.J. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 14 (1994) 4368-4374
5. Bertrand J., Winton M.J., Rodriguez-Hernandez N., Campenot R.B., and McKerracher L. Application of rho antagonist to neuronal cell bodies promotes neurite growth in compartmented cultures and regeneration of retinal ganglion cell axons in the optic nerve of adult rats. J. Neurosci. 25 (2005) 1113-1121
6. Bertrand, J., Di Polo, A., McKerracher, L., 2006. Enhanced survival and regeneration of axotomized retinal neurons by repeated delivery of cell-permeable C3-like Rho antagonists. Neurobiol. Dis. doi:10.1016/j.nbd.2006.08.008.
7. Borisoff J.F., Chan C.C., Hiebert G.W., Oschipok L., Robertson G.S., Zamboni R., Steeves J.D., and Tetzlaff W. Suppression of Rho-kinase activity promotes axonal growth on inhibitory CNS substrates. Mol. Cell. Neurosci. 22 (2003) 405-416
8. Bregman B.S., Coumans J.V., Dai H.N., Kuhn P.L., Lynskey J., McAtee M., and Sandhu F. Transplants and neurotrophic factors increase regeneration and recovery of function after spinal cord injury. Prog. Brain Res. 137 (2002) 257-273
9. Bruce J.H., Norenberg M.D., Kraydieh S., Puckett W., Marcillo A., and Dietrich D. Schwannosis: role of gliosis and proteoglycan in human spinal cord injury. J. Neurotrauma 17 (2000) 781-788
10. Cai D., Deng K., Mellado W., Lee J., Ratan R.R., and Filbin M.T. Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 35 (2002) 711-719
11. Castro C., and Kuffler D.P. Membrane-bound CSPG mediates growth cone outgrowth and substrate specificity by Schwann cell contact with the DRG neuron cell body and not via growth cone contact. Exp. Neurol. 200 (2006) 19-25
12. Chen H., and Weber A.J. Brain-derived neurotrophic factor reduces TrkB protein and mRNA in the normal retina and following optic nerve crush in adult rats. Brain Res. 1011 (2004) 99-106
13. Cho E.Y., and So K.F. Rate of regrowth of damaged retinal ganglion cell axons regenerating in a peripheral nerve graft in adult hamsters. Brain Res. 419 (1987) 369-374
14. Cui Q., Lu Q., So K.F., and Yip H.K. CNTF, not other trophic factors, promotes axonal regeneration of axotomized retinal ganglion cells in adult hamsters. Invest. Ophthalmol. Visual Sci. 40 (1999) 760-766
15. Cui Q., Tang L.S., Hu B., So K.F., and Yip H.K. Expression of trkA, trkB, and trkC in injured and regenerating retinal ganglion cells of adult rats. Invest. Ophthalmol. Visual Sci. 43 (2002) 1954-1964
16. Cui Q., Yip H.K., Zhao R.C., So K.F., and Harvey A.R. Intraocular elevation of cyclic AMP potentiates ciliary neurotrophic factor-induced regeneration of adult rat retinal ganglion cell axons. Mol. Cell. Neurosci. 22 (2003) 49-61
17. Cui Q., Cho K.S., So K.F., and Yip H.K. Synergistic effect of Nogo-neutralizing antibody IN-1 and ciliary neurotrophic factor on axonal regeneration in adult rodent visual systems. J. Neurotrauma 21 (2004) 617-625
18. Danias J., Shen F., Goldblum D., Chen B., Ramos-Esteban J., Podos S.M., and Mittag T. Cytoarchitecture of the retinal ganglion cells in the rat. Invest. Ophthalmol. Visual Sci. 43 (2002) 587-594
19. Dergham P., Ellezam B., Essagian C., Avedissian H., Lubell W.D., and McKerracher L. Rho signaling pathway targeted to promote spinal cord repair. J. Neurosci. 22 (2002) 6570-6577
20. Desagher S., Severac D., Lipkin A., Bernis C., Ritchie W., Le Digarcher A., and Journot L. Genes regulated in neurons undergoing transcription-dependent apoptosis belong to signaling pathways rather than the apoptotic machinery. J. Biol. Chem. 280 (2005) 5693-5702
21. Dong J.M., Leung T., Manser E., and Lim L. cAMP-induced morphological changes are counteracted by the activated RhoA small GTPase and the Rho kinase ROKalpha. J. Biol. Chem. 273 (1998) 22554-22562
22. Dubreuil C.I., Winton M.J., and McKerracher L. Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system. J. Cell Biol. 162 (2003) 233-243
23. Dusart I., Ghoumari A., Wehrle R., Morel M.P., Bouslama-Oueghlani L., Camand E., and Sotelo C. Cell death and axon regeneration of Purkinje cells after axotomy: challenges of classical hypotheses of axon regeneration. Brain Res. Rev. 49 (2005) 300-316
24. Filbin M.T. Myelin-associated glycoprotein: a role in myelination and in the inhibition of axonal regeneration?. Curr. Opin. Neurobiol. 5 (1995) 588-595
25. Fischer D., Petkova V., Thanos S., and Benowitz L.I. Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation. J. Neurosci. 24 (2004) 8726-8740
26. Fouad K., Schnell L., Bunge M.B., Schwab M.E., Liebscher T., and Pearse D.D. Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J. Neurosci. 25 (2005) 1169-1178
27. Fournier A.E., Takizawa B.T., and Strittmatter S.M. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J. Neurosci. 23 (2003) 1416-1423
28. Frade J.M., and Barde Y.A. Genetic evidence for cell death mediated by nerve growth factor and the neurotrophin receptor p75 in the developing mouse retina and spinal cord. Development 126 (1999) 683-690
29. Gao Y., Nikulina E., Mellado W., and Filbin M.T. Neurotrophins elevate cAMP to reach a threshold required to overcome inhibition by MAG through extracellular signal-regulated kinase-dependent inhibition of phosphodiesterase. J. Neurosci. 23 (2003) 11770-11777
30. Gao Y., Deng K., Hou J., Bryson J.B., Barco A., Nikulina E., Spencer T., Mellado W., Kandel E.R., and Filbin M.T. Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 44 (2004) 609-621
31. Gillon R.S., Cui Q., Dunlop S.A., and Harvey A.R. Effects of immunosuppression on regrowth of adult rat retinal ganglion cell axons into peripheral nerve allografts. J. Neurosci. Res. 74 (2003) 524-532
32. Goldberg J.L., Espinosa J.S., Xu Y., Davidson N., Kovacs G.T., and Barres B.A. Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 33 (2002) 689-702
33. Grandpre T., and Strittmatter S.M. Nogo: a molecular determinant of axonal growth and regeneration. Neuroscientist 7 (2001) 377-386
34. Han S., Arvai A.S., Clancy S.B., and Tainer J.A. Crystal structure and novel recognition motif of rho ADP-ribosylating C3 exoenzyme from Clostridium botulinum: structural insights for recognition specificity and catalysis. J. Mol. Biol. 305 (2001) 95-107
35. Harvey A.R., Hu Y., Leaver S.G., Mellough C.B., Park K., Verhaagen J., Plant G.W., and Cui Q. Gene therapy and transplantation in CNS repair: the visual system. Prog. Retinal Eye Res. 25 (2006) 449-489
36. Hou B., You S.W., Wu M.M., Kuang F., Liu H.L., Jiao X.Y., and Ju G. Neuroprotective effect of inosine on axotomized retinal ganglion cells in adult rats. Invest. Ophthalmol. Visual Sci. 45 (2004) 662-667
37. Hu Y., Leaver S.G., Plant G.W., Hendriks W.T., Niclou S.P., Verhaagen J., Harvey A.R., and Cui Q. Lentiviral-mediated transfer of CNTF to Schwann cells within reconstructed peripheral nerve grafts enhances adult retinal ganglion cell survival and axonal regeneration. Mol. Ther. 11 (2005) 906-915
38. Isenmann S., Klöcker N., Gravel C., and Bähr M. Short communication: protection of axotomized retinal ganglion cells by adenovirally delivered BDNF in vivo. Eur. J. Neurosci. 10 (1998) 2751-2756
39. Isenmann S., Kretz A., and Cellerino A. Molecular determinants of retinal ganglion cell development, survival, and regeneration. Prog. Retinal Eye Res. 22 (2003) 483-543
40. Kanekura K., Hashimoto Y., Kita Y., Sasabe J., Aiso S., Nishimoto I., and Matsuoka M. A Rac1/phosphatidylinositol 3-kinase/Akt3 anti-apoptotic pathway, triggered by AlsinLF, the product of the ALS2 gene, antagonizes Cu/Zn-superoxide dismutase (SOD1) mutant-induced motoneuronal cell death. J. Biol. Chem. 280 (2005) 4532-4543
41. Kitaoka Y., Kumai T., Lam T.T., Kuribayashi K., Isenoumi K., Munemasa Y., Motoki M., Kobayashi S., and Ueno S. Involvement of RhoA and possible neuroprotective effect of fasudil, a Rho kinase inhibitor, in NMDA-induced neurotoxicity in the rat retina. Brain Res. 1018 (2004) 111-118
42. Klöcker N., Braunling F., Isenmann S., and Bähr M. In vivo neurotrophic effects of GDNF on axotomized retinal ganglion cells. NeuroReport 8 (1997) 3439-3442
43. Klöcker N., Cellerino A., and Bähr M. Free radical scavenging and inhibition of nitric oxide synthase potentiates the neurotrophic effects of brain-derived neurotrophic factor on axotomized retinal ganglion cells In vivo. J. Neurosci. 18 (1998) 1038-1046
44. Kobayashi K., Takahashi M., Matsushita N., Miyazaki J., Koike M., Yaginuma H., Osumi N., and Kaibuchi K. Survival of developing motor neurons mediated by Rho GTPase signaling pathway through Rho-kinase. J. Neurosci. 24 (2004) 3480-3488
45. Koprivica V., Cho K.S., Park J.B., Yiu G., Atwal J., Gore B., Kim J.A., Lin E., Tessier-Lavigne M., Chen D.F., and He Z. EGFR activation mediates inhibition of axon regeneration by myelin and chondroitin sulfate proteoglycans. Science 310 (2005) 106-110
46. Kuramoto H., Hozumi I., Inuzuka T., and Sato S. Occurrence of myelin-associated glycoprotein (MAG)-like immunoreactivity in some nervous, endocrine, and immune-related cells of the rat. An immunohistochemical study. Mol. Chem. Neuropathol. 31 (1997) 85-94
47. Lang P., Gesbert F., Delespine-Carmagnat M., Stancou R., Pouchelet M., and Bertoglio J. Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J. 15 (1996) 510-519
48. Leaver S.G., Cui Q., Plant G.W., Arulpragasam A., Hisheh S., Verhaagen J., and Harvey A.R. AAV-mediated expression of CNTF promotes long-term survival and regeneration of adult rat retinal ganglion cells. Gene Ther. 13 (2006) 1328-1341
49. Lehmann M., Fournier A., Selles-Navarro I., Dergham P., Sebok A., Leclerc N., Tigyi G., and McKerracher L. Inactivation of Rho signaling pathway promotes CNS axon regeneration. J. Neurosci. 19 (1999) 7537-7547
50. Li Y., Irwin N., Yin Y., Lanser M., and Benowitz L.I. Axon regeneration in goldfish and rat retinal ganglion cells: differential responsiveness to carbohydrates and cAMP. J. Neurosci. 23 (2003) 7830-7838
51. Lindqvist N., Peinado-Ramonn P., Vidal-Sanz M., and Hallbook F. GDNF, Ret, GFRalpha1 and 2 in the adult rat retino-tectal system after optic nerve transection. Exp. Neurol. 187 (2004) 487-499
52. Logan A., Ahmed Z., Baird A., Gonzalez A.M., and Berry M. Neurotrophic factor synergy is required for neuronal survival and disinhibited axon regeneration after CNS injury. Brain 129 (2006) 490-502
53. Loucks F.A., Le S.S., Zimmermann A.K., Ryan K.R., Barth H., Aktories K., and Linseman D.A. 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 (2006) 957-967
54. Lu P., Yang H., Jones L.L., Filbin M.T., and Tuszynski M.H. Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J. Neurosci. 24 (2004) 6402-6409
55. Mansour-Robaey S., Clarke D.B., Wang Y.C., Bray G.M., and Aguayo A.J. Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 1632-1636
56. Mey J., and Thanos S. Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Res. 602 (1993) 304-317
57. Meyer-Franke A., Wilkinson G.A., Kruttgen A., Hu M., Munro E., Hanson Jr. M.G., Reichardt L.F., and Barres B.A. Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron 21 (1998) 681-693
58. Monnier P.P., Sierra A., Schwab J.M., Henke-Fahle S., and Mueller B.K. The Rho/ROCK pathway mediates neurite growth-inhibitory activity associated with the chondroitin sulfate proteoglycans of the CNS glial scar. Mol. Cell. Neurosci. 22 (2003) 319-330
59. Morgenstern D.A., Asher R.A., Naidu M., Carlstedt T., Levine J.M., and Fawcett J.W. Expression and glycanation of the NG2 proteoglycan in developing, adult, and damaged peripheral nerve. Mol. Cell. Neurosci. 24 (2003) 787-802
60. Muir D., Engvall E., Varon S., and Manthorpe M. Schwannoma cell-derived inhibitor of the neurite-promoting activity of laminin. J. Cell Biol. 109 (1989) 2353-2362
61. Mukhopadhyay G., Doherty P., Walsh F.S., Crocker P.R., and Filbin M.T. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13 (1994) 757-767
62. Nakazawa T., Tamai M., and Mori N. Brain-derived neurotrophic factor prevents axotomized retinal ganglion cell death through MAPK and PI3K signaling pathways. Invest. Ophthalmol. Visual Sci. 43 (2002) 3319-3326
63. Ng T.F., So K.F., and Chung S.K. Influence of peripheral nerve grafts on the expression of GAP-43 in regenerating retinal ganglion cells in adult hamsters. J. Neurocytol. 24 (1995) 487-496
64. Nickells R.W. The molecular biology of retinal ganglion cell death: caveats and controversies. Brain Res. Bull. 62 (2004) 439-446
65. Orlando K.A., Stone N.L., and Pittman R.N. Rho kinase regulates fragmentation and phagocytosis of apoptotic cells. Exp. Cell Res. 312 (2006) 5-15
66. Oshitari T., and Adachi-Usami E. The effect of caspase inhibitors and neurotrophic factors on damaged retinal ganglion cells. NeuroReport 14 (2003) 289-292
67. Park J.B., Yiu G., Kaneko S., Wang J., Chang J., and He Z. A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 45 (2005) 345-351
68. Park K., Luo J.M., Hisheh S., Harvey A.R., and Cui Q. Cellular mechanisms associated with spontaneous and ciliary neurotrophic factor-cAMP-induced survival and axonal regeneration of adult retinal ganglion cells. J. Neurosci. 24 (2004) 10806-10815
69. Park K., Hisheh S., Turnley A.M., Cui Q., and Harvey A.R. Suppressor of cytokine signaling (SOCS) mRNA expression in axotomized retina subjected to peripheral nerve graft and ciliary neurotrophic factor (CNTF). Proc. Aust. Neurosci. Soc. 17 (2006) 155
70. Peinado-Ramon P., Salvador M., Villegas-Perez M.P., and Vidal-Sanz M. Effects of axotomy and intraocular administration of NT-4, NT-3, and brain-derived neurotrophic factor on the survival of adult rat retinal ganglion cells. A quantitative in vivo study. Invest. Ophthalmol. Visual Sci. 37 (1996) 489-500
71. Qiu J., Cai D., Dai H., McAtee M., Hoffman P.N., Bregman B.S., and Filbin M.T. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34 (2002) 895-903
72. Saito Y. Analysis of the cellular functions of the small GTP-binding protein rho p21 with Clostridium botulinum C3 exoenzyme. Nippon Yakurigaku Zasshi 109 (1997) 13-17
73. Sandvig A., Berry M., Barrett L.B., Butt A., and Logan A. Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration. Glia 46 (2004) 225-251
74. Schafer M., Fruttiger M., Montag D., Schachner M., and Martini R. Disruption of the gene for the myelin-associated glycoprotein improves axonal regrowth along myelin in C57BL/Wlds mice. Neuron 16 (1996) 1107-1113
75. Selles-Navarro I., Ellezam B., Fajardo R., Latour M., and McKerracher L. Retinal ganglion cell and nonneuronal cell responses to a microcrush lesion of adult rat optic nerve. Exp. Neurol. 167 (2001) 282-289
76. Shearer M.C., Niclou S.P., Brown D., Asher R.A., Holtmaat A.J., Levine J.M., Verhaagen J., and Fawcett J.W. The astrocyte/meningeal cell interface is a barrier to neurite outgrowth which can be overcome by manipulation of inhibitory molecules or axonal signalling pathways. Mol. Cell. Neurosci. 24 (2003) 913-925
77. Shen Y.J., DeBellard M.E., Salzer J.L., Roder J., and Filbin M.T. Myelin-associated glycoprotein in myelin and expressed by Schwann cells inhibits axonal regeneration and branching. Mol. Cell. Neurosci. 12 (1998) 79-91
78. Shen S., Wiemelt A.P., McMorris F.A., and Barres B.A. Retinal ganglion cells lose trophic responsiveness after axotomy. Neuron 23 (1999) 285-295
79. Snider W.D., Zhou F.Q., Zhong J., and Markus A. Signaling the pathway to regeneration. Neuron 35 (2002) 13-16
80. So K.F., and Aguayo A.J. Lengthy regrowth of cut axons from ganglion cells after peripheral nerve transplantation into the retina of adult rats. Brain Res. 328 (1985) 349-354
81. Spencer T., and Filbin M.T. A role for cAMP in regeneration of the adult mammalian CNS. J. Anat. 204 (2004) 49-55
82. Torigoe K., and Lundborg G. Selective inhibition of early axonal regeneration by myelin-associated glycoprotein. Exp. Neurol. 150 (1998) 254-262
83. Weise J., Isenmann S., Klöcker N., Kügler S., Hirsch S., Gravel C., and Bähr M. Adenovirus-mediated expression of ciliary neurotrophic factor (CNTF) rescues axotomized rat retinal ganglion cells but does not support axonal regeneration in vivo. Neurobiol. Dis. 7 (2000) 212-223
84. Winton M.J., Dubreuil C.I., Lasko D., Leclerc N., and McKerracher L. Characterization of new cell permeable C3-like proteins that inactivate Rho and stimulate neurite outgrowth on inhibitory substrates. J. Biol. Chem. 277 (2002) 32820-32829
85. Yan Q., Wang J., Matheson C.R., and Urich J.L. Glial cell line-derived neurotrophic factor (GDNF) promotes the survival of axotomized retinal ganglion cells in adult rats: comparison to and combination with brain-derived neurotrophic factor (BDNF). J. Neurobiol. 38 (1999) 382-390
86. Yin Y., Cui Q., Li Y., Irwin N., Fischer D., Harvey A.R., and Benowitz L.I. Macrophage-derived factors stimulate optic nerve regeneration. J. Neurosci. 23 (2003) 2284-2293
87. Yiu G., and He Z. Glial inhibition of CNS axon regeneration. Nat. Rev., Neurosci. 7 (2006) 617-627
88. Zuo J., Hernandez Y.J., and Muir D. Chondroitin sulfate proteoglycan with neurite-inhibiting activity is up-regulated following peripheral nerve injury. J. Neurobiol. 34 (1998) 41-54