Long-distance axonal regeneration induced by CNTF gene transfer is impaired by axonal misguidance in the injured adult optic nerve

Neurobiology of Disease

Volumn 51, Issue , 2013, Pages 202-213

  Pernet, Vincent ^a   Joly, Sandrine ^a   Dalkara, Deniz ^b   Jordi, Noémie ^a   Schwarz, Olivia ^a   Christ, Franziska ^a   Schaffer, David V ^b   Flannery, John G ^c   Schwab, Martin E ^a  

^a University of Zurich Brain Research Institute   (Switzerland)

^b University of California at Berkeley   (United States)

^c Berkeley   (United States)

Author keywords

Adeno associated virus; Axonal misguidance; Axonal regeneration; Ciliary neurotrophic factor; Gene therapy; M ller glia; Neuronal survival; Optic nerve lesion; Retinal ganglion cells

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXONAL INJURY; AXONAL MISGUIDANCE; CELL SURVIVAL; CONTROLLED STUDY; GENE TRANSFER; GLIA CELL; MALE; MOUSE; NERVE CELL GROWTH; NERVE FIBER REGENERATION; NERVE PLEXUS; NEURITE; NONHUMAN; OPTIC CHIASM; OPTIC NERVE CRUSH; OPTIC NERVE INJURY; PRIORITY JOURNAL; RETINA; RETINA GANGLION CELL;

ANIMALS; AXONS; BLOTTING, WESTERN; CELL SURVIVAL; CILIARY NEUROTROPHIC FACTOR; FLUORESCENT ANTIBODY TECHNIQUE; GENE TRANSFER TECHNIQUES; HUMANS; MALE; MICE; MICE, INBRED C57BL; NERVE REGENERATION; NEUROGLIA; OPTIC NERVE INJURIES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84872820097     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.11.011     Document Type: Article

References (41)

1. Agbulut O., Coirault C., Niederlander N., Huet A., Vicart P., Hagege A., Puceat M., Menasche P. GFP expression in muscle cells impairs actin-myosin interactions: implications for cell therapy. Nat. Methods 2006, 3:331.
2. Bainbridge J.W., Smith A.J., Barker S.S., Robbie S., Henderson R., Balaggan K., Viswanathan A., Holder G.E., Stockman A., Tyler N., Petersen-Jones S., Bhattacharya S.S., Thrasher A.J., Fitzke F.W., Carter B.J., Rubin G.S., Moore A.T., Ali R.R. Effect of gene therapy on visual function in Leber's congenital amaurosis. N. Engl. J. Med. 2008, 358:2231-2239.
3. Benowitz L.I., Yin Y. Combinatorial treatments for promoting axon regeneration in the CNS: strategies for overcoming inhibitory signals and activating neurons' intrinsic growth state. Dev. Neurobiol. 2007, 67:1148-1165.
4. Berkelaar M., Clarke D.B., Wang Y.C., Bray G.M., Aguayo A.J. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 1994, 14:4368-4374.
5. Bringmann A., Pannicke T., Grosche J., Francke M., Wiedemann P., Skatchkov S.N., Osborne N.N., Reichenbach A. Muller cells in the healthy and diseased retina. Prog. Retin. Eye Res. 2006, 25:397-424.
6. Cheng L., Sapieha P., Kittlerova P., Hauswirth W.W., Di Polo A. TrkB gene transfer protects retinal ganglion cells from axotomy-induced death in vivo. J. Neurosci. 2002, 22:3977-3986.
7. Cui Q., Yip H.K., Zhao R.C., So K.F., Harvey A.R. Intraocular elevation of cyclic AMP potentiates ciliary neurotrophic factor-induced regeneration of adult rat retinal ganglion cell axons. Mol. Cell. Neurosci. 2003, 22:49-61.
8. Dalkara D., Kolstad K.D., Caporale N., Visel M., Klimczak R.R., Schaffer D.V., Flannery J.G. Inner limiting membrane barriers to AAV-mediated retinal transduction from the vitreous. Mol. Ther. 2009, 17:2096-2102.
9. Dalkara D., Kolstad K.D., Guerin K.I., Hoffmann N.V., Visel M., Klimczak R.R., Schaffer D.V., Flannery J.G. AAV mediated GDNF secretion from retinal glia slows down retinal degeneration in a rat model of retinitis pigmentosa. Mol. Ther. 2011, 19:1602-1608.
10. Dittrich F., Thoenen H., Sendtner M. Ciliary neurotrophic factor: pharmacokinetics and acute-phase response in rat. Ann. Neurol. 1994, 35:151-163.
11. Duffy P., Wang X., Siegel C.S., Tu N., Henkemeyer M., Cafferty W.B., Strittmatter S.M. Myelin-derived ephrinB3 restricts axonal regeneration and recovery after adult CNS injury. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:5063-5068.
12. Goldberg J.L., Vargas M.E., Wang J.T., Mandemakers W., Oster S.F., Sretavan D.W., Barres B.A. An oligodendrocyte lineage-specific semaphorin, Sema5A, inhibits axon growth by retinal ganglion cells. J. Neurosci. 2004, 24:4989-4999.
13. Grieger J.C., Choi V.W., Samulski R.J. Production and characterization of adeno-associated viral vectors. Nat. Protoc. 2006, 1:1412-1428.
14. Harvey A.R., Hu Y., Leaver S.G., Mellough C.B., Park K., Verhaagen J., Plant G.W., Cui Q. Gene therapy and transplantation in CNS repair: the visual system. Prog. Retin. Eye Res. 2006, 25:449-489.
15. Hellstrom M., Muhling J., Ehlert E.M., Verhaagen J., Pollett M.A., Hu Y., Harvey A.R. Negative impact of rAAV2 mediated expression of SOCS3 on the regeneration of adult retinal ganglion cell axons. Mol. Cell. Neurosci. 2011, 46:507-515.
16. Jahrling N., Becker K., Dodt H.U. 3D-reconstruction of blood vessels by ultramicroscopy. Organogenesis 2009, 5:145-148.
17. Kirsch M., Trautmann N., Ernst M., Hofmann H.D. Involvement of gp130-associated cytokine signaling in Muller cell activation following optic nerve lesion. Glia 2010, 58:768-779.
18. Klimczak R.R., Koerber J.T., Dalkara D., Flannery J.G., Schaffer D.V. A novel adeno-associated viral variant for efficient and selective intravitreal transduction of rat Muller cells. PLoS One 2009, 4:e7467.
19. Krestel H.E., Mihaljevic A.L., Hoffman D.A., Schneider A. Neuronal co-expression of EGFP and beta-galactosidase in mice causes neuropathology and premature death. Neurobiol. Dis. 2004, 17:310-318.
20. Kurimoto T., Yin Y., Omura K., Gilbert H.Y., Kim D., Cen L.P., Moko L., Kugler S., Benowitz L.I. Long-distance axon regeneration in the mature optic nerve: contributions of oncomodulin, cAMP, and pten gene deletion. J. Neurosci. 2010, 30:15654-15663.
21. Leaver S.G., Cui Q., Bernard O., Harvey A.R. Cooperative effects of bcl-2 and AAV-mediated expression of CNTF on retinal ganglion cell survival and axonal regeneration in adult transgenic mice. Eur. J. Neurosci. 2006, 24:3323-3332.
22. Leaver S.G., Cui Q., Plant G.W., Arulpragasam A., Hisheh S., Verhaagen J., Harvey A.R. AAV-mediated expression of CNTF promotes long-term survival and regeneration of adult rat retinal ganglion cells. Gene Ther. 2006, 13:1328-1341.
23. Leon S., Yin Y., Nguyen J., Irwin N., Benowitz L.I. Lens injury stimulates axon regeneration in the mature rat optic nerve. J. Neurosci. 2000, 20:4615-4626.
24. Lingor P., Tonges L., Pieper N., Bermel C., Barski E., Planchamp V., Bahr M. ROCK inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells. Brain 2008, 131:250-263.
25. Ludwin S.K. Oligodendrocyte survival in Wallerian degeneration. Acta Neuropathol. (Berl) 1990, 80:184-191.
26. Maguire A.M., Simonelli F., Pierce E.A., Pugh E.N., Mingozzi F., Bennicelli J., Banfi S., Marshall K.A., Testa F., Surace E.M., Rossi S., Lyubarsky A., Arruda V.R., Konkle B., Stone E., Sun J., Jacobs J., Dell'Osso L., Hertle R., Ma J.X., Redmond T.M., Zhu X., Hauck B., Zelenaia O., Shindler K.S., Maguire M.G., Wright J.F., Volpe N.J., McDonnell J.W., Auricchio A., High K.A., Bennett J. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Engl. J. Med. 2008, 358:2240-2248.
27. Maguire A.M., High K.A., Auricchio A., Wright J.F., Pierce E.A., Testa F., Mingozzi F., Bennicelli J.L., Ying G.S., Rossi S., Fulton A., Marshall K.A., Banfi S., Chung D.C., Morgan J.I., Hauck B., Zelenaia O., Zhu X., Raffini L., Coppieters F., De Baere E., Shindler K.S., Volpe N.J., Surace E.M., Acerra C., Lyubarsky A., Redmond T.M., Stone E., Sun J., McDonnell J.W., Leroy B.P., Simonelli F., Bennett J. Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: a phase 1 dose-escalation trial. Lancet 2009, 374:1597-1605.
28. Mansour-Robaey S., Clarke D.B., Wang Y.-C., Bray G.M., 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. 1994, 91:1632-1636.
29. Muller A., Hauk T.G., Fischer D. Astrocyte-derived CNTF switches mature RGCs to a regenerative state following inflammatory stimulation. Brain 2007, 130:3308-3320.
30. Muller A., Hauk T.G., Leibinger M., Marienfeld R., Fischer D. Exogenous CNTF stimulates axon regeneration of retinal ganglion cells partially via endogenous CNTF. Mol. Cell. Neurosci. 2009, 41:233-246.
31. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., He Z. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
32. Pernet V., Hauswirth W.W., Di Polo A. Extracellular signal-regulated kinase 1/2 mediates survival, but not axon regeneration, of adult injured central nervous system neurons in vivo. J. Neurochem. 2005, 93:72-83.
33. Peterson W.M., Wang Q., Tzekova R., Wiegand S.J. Ciliary neurotrophic factor and stress stimuli activate the Jak-STAT pathway in retinal neurons and glia. J. Neurosci. 2000, 20:4081-4090.
34. Pfaffl M.W. Quantification strategies in real-time PCR. A-Z of Quantitative PCR 2004, 87-112. International University Line (IUL), La Jolla, CA, USA. S. Bustin (Ed.).
35. Saggio I., Gloaguen I., Poiana G., Laufer R. CNTF variants with increased biological potency and receptor selectivity define a functional site of receptor interaction. EMBO J. 1995, 14:3045-3054.
36. Sapieha P.S., Peltier M., Rendahl K.G., Manning W.C., Di Polo A. Fibroblast growth factor-2 gene delivery stimulates axon growth by adult retinal ganglion cells after acute optic nerve injury. Mol. Cell. Neurosci. 2003, 24:656-672.
37. Schwab M.E. Functions of Nogo proteins and their receptors in the nervous system. Nat. Rev. Neurosci. 2010, 11:799-811.
38. Smith P.D., Sun F., Park K.K., Cai B., Wang C., Kuwako K., Martinez-Carrasco I., Connolly L., He Z. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 2009, 64:617-623.
39. Wang Y., Smith S.B., Ogilvie J.M., McCool D.J., Sarthy V. Ciliary neurotrophic factor induces glial fibrillary acidic protein in retinal Muller cells through the JAK/STAT signal transduction pathway. Curr. Eye Res. 2002, 24:305-312.
40. Wohl S.G., Schmeer C.W., Kretz A., Witte O.W., Isenmann S. Optic nerve lesion increases cell proliferation and nestin expression in the adult mouse eye in vivo. Exp. Neurol. 2009, 219:175-186.
41. Xue W., Cojocaru R.I., Dudley V.J., Brooks M., Swaroop A., Sarthy V.P. Ciliary neurotrophic factor induces genes associated with inflammation and gliosis in the retina: a gene profiling study of flow-sorted, Muller cells. PLoS One 2011, 6:e20326.