Long-term gene therapy causes transgene-specific changes in the morphology of regenerating retinal ganglion cells

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Rodger, Jennifer ^a   Drummond, Eleanor S ^a   Hellström, Mats ^a   Robertson, Donald ^a   Harvey, Alan R ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; GREEN FLUORESCENT PROTEIN; NEUROMODULIN; PARVOVIRUS VECTOR; NERVE GROWTH FACTOR;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOTRANSPLANTATION; CELL POPULATION; CELL REGENERATION; CELL STRUCTURE; CELL SUBPOPULATION; CELL SURVIVAL; CELL TRANSFORMATION; CONTROLLED STUDY; DENDRITIC CELL; DRUG MECHANISM; FEMALE; GENE EXPRESSION; GENE THERAPY; GENETIC TRANSDUCTION; NERVE CELL LESION; NERVE FIBER REGENERATION; NERVE GRAFT; NONHUMAN; OPTIC NERVE; PERIPHERAL NERVE; RAT; RETINA GANGLION CELL; STRUCTURE ANALYSIS; TRANSGENE; VIRUS RECOMBINANT; ANIMAL; DRUG EFFECT; GENETICS; METABOLISM; METHODOLOGY; NERVE CELL; NERVE FIBER; NERVE REGENERATION; TREATMENT OUTCOME;

RATTUS;

ANIMALS; AXONS; GENE THERAPY; NERVE GROWTH FACTORS; NERVE REGENERATION; NEURONS; RATS; RETINAL GANGLION CELLS; TRANSDUCTION, GENETIC; TRANSGENES; TREATMENT OUTCOME;

EID: 84856699252     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031061     Document Type: Article

References (87)

1. Wu K, Klein RL, Meyers CA, King MA, Hughes JA, et al. (2003) Long-term neuronal effects and disposition of ectopic preproNGF gene transfer into the rat septum. Hum Gene Ther 14: 1463-1472.
2. Ruitenberg MJ, Blits B, Dijkhuizen PA, te Beek ET, Bakker A, et al. (2004) Adeno-associated viral vector-mediated gene transfer of brain-derived neurotrophic factor reverses atrophy of rubrospinal neurons following both acute and chronic spinal cord injury. Neurobiol Dis 15: 394-406.
3. Kells AP, Henry RA, Connor B, (2008) AAV-BDNF mediated attenuation of quinolinic acid-induced neuropathology and motor function impairment. Gene Ther 15: 966-977.
4. Ramaswamy S, McBride JL, Han I, Berry-Kravis EM, Zhou L, et al. (2009) Intrastriatal CERE-120 (AAV-Neurturin) protects striatal and cortical neurons and delays motor deficits in a transgenic mouse model of Huntington's disease. Neurobiol Dis 34: 40-50.
5. Yang X, Mertens B, Lehtonen E, Vercammen L, Bockstael O, et al. (2009) Reversible neurochemical changes mediated by delayed intrastriatal glial cell line-derived neurotrophic factor gene delivery in a partial Parkinson's disease rat model. J Gene Med 11: 899-912.
6. Schmeer C, Straten G, Kugler S, Gravel C, Bähr M, et al. (2002) Dose-dependent rescue of axotomized rat retinal ganglion cells by adenovirus-mediated expression of GDNF in vivo. Eur J Neurosci 15: 637-643.
7. Sapieha PS, Peltier M, Rendahl KG, Manning WC, Di Polo A, (2003) Fibroblast growth factor-2 gene delivery stimulates axon growth by adult retinal ganglion cells after acute optic nerve injury. Mol Cell Neurosci 24: 656-672.
8. Leaver SG, Cui Q, Plant GW, Arulpragasam A, Hisheh S, et al. (2006) AAV-mediated expression of CNTF promotes long-term survival and regeneration of adult rat retinal ganglion cells. Gene Ther 13: 1328-1341.
9. Hellström M, Harvey AR, (2011) Retinal ganglion cell gene therapy and visual system repair. Curr Gene Ther 11: 116-131.
10. Tuszynski MH, Thal L, Pay M, Salmon DP, U HS, et al. (2005) A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nat Med 11: 551-555.
11. Bjorklund A, Kordower JH, (2010) Gene therapy for Parkinson's Disease. Movement Disord 25: S161-S173.
12. Mandel RJ, (2010) CERE-110, an adeno-associated virus-based gene delivery vector expressing human nerve growth factor for the treatment of Alzheimer's disease. Curr Opin Mol Ther 12: 240-247.
13. Simonelli F, Maguire AM, Testa F, Pierce EA, Mingozzi F, et al. (2010) Gene therapy for Leber's congenital amaurosis is safe and effective through 1.5 years after vector administration. Mol Ther 18: 643-650.
14. Hellström M, Pollett MA, Harvey AR, (2011) Post-injury delivery of rAAV2-CNTF combined with short-term pharmacotherapy is neuroprotective and promotes extensive axonal regeneration after optic nerve trauma. J Neurotrauma 28: 2475-2483.
15. Guo X, Chandrasekaran V, Lein P, Kaplan P, Higgins D, (1999) Leukemia inhibitory factor and ciliary neurotrophic factor cause dendritic retraction in cultured rat sympathetic neurons. J Neurosci 19: 2113-2121.
16. Horch HW, (2004) Local effects of BDNF on dendritic growth. Rev Neurosci 15: 117-129.
17. Dijkuizen PA, Ghosh A, (2005) Regulation of dendritic growth by calcium and neurotrophin signalling. Prog Brain Res 147: 17-27.
18. Kuipers SD, Bramham CR, (2006) Brain-derived neurotrophic factor mechanisms and function in adult synaptic plasticity: new insights and implications for therapy. Curr Opin Drug Discov Devel 9: 580-586.
19. Parrish JZ, Emoto K, Kim MD, Jan YN, (2007) Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu Rev Neurosci 30: 399-423.
20. Klein RL, McNamara RK, King MA, Lenox RH, Muzyczka N, et al. (1999) Generation of aberrant sprouting in the adult rat brain by GAP-43 somatic gene transfer. Brain Res 832: 136-144.
21. Klein RL, Muir D, King MA, Peel AL, Zolotukhin S, et al. (1999) Long-term actions of vector-derived nerve growth factor or brain-derived neurotrophic factor on choline acetyltransferase and trk receptor levels in the adult rat basal forebrain. Neuroscience 90: 815-821.
22. Bray GM, Villegas-Perez MP, Vidal-Sanz M, Aguayo AJ, (1987) The use of peripheral nerve grafts to enhance survival, promote regrowth and permit terminal reconnection in the central nervous system of adult rats. J Exp Biol 132: 5-19.
23. Harvey AR, Hu Y, Leaver SG, Mellough CB, Park K, et al. (2006) Gene therapy and transplantation in CNS repair: the visual system. Prog Retin Eye Res 25: 449-489.
24. Hellström M, Mulling J, Ehrlert E, Verhaagen J, Pollett MA, et al. (2011) Negative impact of rAAV2 mediated expression of SOCS3 on the regeneration of adult retinal ganglion cell axons. Mol Cell Neurosci 46: 507-515.
25. de Winter W, Oxnard CE, (2001) Evolutionary radiations and convergences in the structural organization of mammalian brains. Nature 409: 710-714.
26. Milosević NT, Ristanović D, Jelinek HF, Rajković K, (2009) Quantitative analysis of dendritic morphology of the alpha and delta retinal ganglion cells in the rat: a cell classification study. J Theor Biol 259: 142-150.
27. Sholl DA, (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87: 387-406.
28. Fukuda Y, (1977) A three group classification of rat retinal ganglion cells: histological and physiological studies. Brain Research 119: 327-344.
29. Huxlin KR, Goodchild AK, (1997) Retinal ganglion cells in the albino rat: revised morphological classification. J Comp Neurol 385: 309-323.
30. Huberman AD, Manu M, Koch SM, Susman MW, Brosius Lutz A, et al. (2008) Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59: 425-438.
31. Lin B, Wang SW, Masland RH, (2004) Retinal ganglion cell type, size, and spacing can be specified independent of homotypic dendritic contacts. Neuron 43: 475-485.
32. Robinson GA, Madison RD, (2004) Axotomized mouse retinal ganglion cells containing melanopsin show enhanced survival, but not enhanced axon regrowth into a peripheral nerve graft. Vis Res 44: 2667-2674.
33. Dreher B, Sefton AJ, Ni SY, Nisbett G, (1985) The morphology, number, distribution and central projections of Class I retinal ganglion cells in albino and hooded rats. Brain Behav Evol 26: 10-48.
34. Perry VH, (1979) The ganglion cell layer of the retina of the rat: A Golgi study. Proc R Soc Lond B Biol Sci 204: 363-375.
35. Martin PR, (1986) The projection of different retinal ganglion cell classes to the dorsal lateral geniculate nucleus in the hooded rat. Exp Brain Res 62: 77-88.
36. Sun W, Li N, He S, (2002) Large-scale morphological survey of rat retinal ganglion cells. Vis Neurosci 19: 483-493.
37. Thanos S, Mey J, (1995) Type-specific stabilization and target-dependent survival of regenerating ganglion cells in the retina of adult rats. J Neurosci 15: 1057-1079.
38. Chiwitt C, Prokosch V, Seeger J, Thanos S, (2011) Long-term morphometric stabilization of regenerating retinal ganglion cells in the adult rat. Restor Neurol Neurosci 28: 127-139.
39. Weber AJ, Harman CD, (2008) BDNF preserves the dendritic morphology of alpha and beta ganglion cells in the cat retina after optic nerve injury. Invest Ophthalmol Vis Sci 49: 2456-2463.
40. Famiglietti EV, Kolb H, (1976) Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194: 193-195.
41. Bainbridge JW, Smith AJ, Barker SS, Robbie S, Henderson R, et al. (2008) Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med 358: 2231-2239.
42. Cideciyan AV, Hauswirth WW, Aleman TS, Kaushal S, Schwartz SB, et al. (2009) Human RPE65 gene therapy for Leber congenital amaurosis: persistence of early visual improvements and safety at 1 year. Hum Gene Ther 20: 999-1004.
43. Eberling JL, Jagust WJ, Christine CW, Starr P, Larson P, et al. (2008) Results from a phase I safety trial of hAADC gene therapy for Parkinson disease. Neurology 70: 1980-1983.
44. Marks WJ Jr, Ostrem JL, Verhagen L, Starr PA, Larson PS, et al. (2008) Safety and tolerability of intraputaminal delivery of CERE-120 (adeno-associated virus serotype 2-neurturin) to patients with idiopathic Parkinson's disease: an open-label, phase I trial. Lancet Neurol 7: 400-408.
45. Richardson RM, Kells AP, Rosenbluth KH, Salegio EA, Fiandaca MS, et al. (2011) Interventional MRI-guided putaminal delivery of AAV2-GDNF for a planned clinical trial in Parkinson's disease. Mol Ther 19: 1048-1057.
46. Germain F, Fernandez E, Villa P, (2003) Morphometrical analysis of dendritic arborisation in axotomized retinal ganglion cells. Eur J Neurosci 18: 1103-1109.
47. Baumgartner BJ, Shine HD, (1997) Targeted transduction of CNS neurons with adenoviral vectors carrying neurotrophic factor genes confers neuroprotection that exceeds the transduced population. J Neurosci 17: 6504-6511.
48. Lau KC, So K-F, Cho EYP, (1991) Morphological changes of retinal ganglion cells regenerating axons along peripheral nerve grafts: a Lucifer Yellow and silver staining study. Restor Neurol Neurosci 3: 235-246.
49. Quan MZ, Kosaka J, Watanabe M, Wakabayashi T, Fukuda Y, (1999) Survival of axotomized retinal ganglion cells in peripheral nerve-grafted ferrets. Invest Ophthalmol Vis Sci 40: 2360-2366.
50. Cui Q, Harvey AR, (2000) CNTF promotes the regrowth of retinal ganglion cell axons into murine peripheral nerve grafts. Neuroreport 11: 3999-4002.
51. Watanabe M, Sawai H, Fukuda Y, (1993) Number, distribution and morphology of retinal ganglion cells with axons regenerated into peripheral nerve graft in adult cats. J Neurosci 13: 2105-2117.
52. Miyoshi T, Watanabe M, Sawai H, Rasminsky M, Sugioka M, et al. (1999) Receptive-field properties of adult cat's retinal ganglion cells with regenerated axons. Exp Brain Res 124: 383-390.
53. Miller FD, Kaplan DR, (2003) Signaling mechanisms underlying dendrite formation. Curr Op Neurobiol 13: 391-398.
54. Kwon M, Fernandez JR, Zegared GF, Lo SB, Firestein BL, (2011) BDNF-promoted increases in proximal dendrites occur via CREB-dependent transcriptional regulation of cypin. J Neurosci 31: 9735-9745.
55. Tolwani RJ, Buckmaster PS, Varma S, Cosgaya JM, Wu Y, et al. (2002) BDNF overexpression increases dendrite complexity in hippocampal dentate gyrus. Neuroscience 114: 795-805.
56. Luikart BW, Zhang W, Wayman GA, Kwon C-H, Westbrook GL, et al. (2008) Neurotrophin-dependent dendritic filopodial motility: a convergence on PI3K signaling. J Neurosci 28: 7006-7012.
57. Zagrebelsky M, Holz A, Dechant G, Barde YA, Bonhoeffer T, et al. (2005) The p75 neurotrophin receptor negatively modulates dendrite complexity and spine density in hippocampal neurons. J Neurosci 25: 9989-9999.
58. Cohen-Cory S, Lom B, (2004) Neurotrophic regulation of retinal ganglion cell synaptic connectivity: from axons and dendrites to synapses. Int J Dev Biol 48: 947-956.
59. Horch HW, Katz LC, (2002) BDNF release from single cells elicits local dendritic growth in nearby neurons. Nat Neurosci 5: 1177-1184.
60. Sommerfeld MT, Schweigreiter R, Bard Y-A, Hoppe E, (2000) Down-regulation of the neurotrophin receptor TrkB following ligand binding. J Biol Chem 275: 8982-8990.
61. Yacoubian TA, Lo DC, (2000) Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth. Nat Neurosci 4: 342-349.
62. Chacon PJ, Arevalo MA, Tebar AR, (2010) NGF-activated protein tyrosine phosphatase 1B mediates the phosphorylation and degradation of I-κ-Bα coupled to NF-κ-B activation, thereby controlling dendrite morphology. Mol Cell Neurosci 43: 384-393.
63. Smith PD, Sun F, Park KK, Cai B, Wang C, et al. (2009) SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 64: 617-623.
64. Park KK, Hu Y, Muhling J, Pollett MA, Dallimore EJ, et al. (2009) Cytokine-induced SOCS expression is inhibited by cAMP analogue: impact on regeneration of injured retina. Mol Cell Neurosci 41: 313-324.
65. Biffo S, Verhaagen J, Schrama LH, Schotman P, Danho W, et al. (1990) B-50/GAP43 Expression correlates with process outgrowth in the embryonic mouse nervous system. Eur J Neurosci 2: 487-499.
66. Strittmatter SM, Igarashi M, Fishman MC, (1994) GAP-43 amino terminal peptides modulate growth cone morphology and neurite outgrowth. J Neurosci 14: 5503-5513.
67. Frey D, Laux T, Xu L, Schneider C, Caroni P, (2000) Shared and unique roles of CAP23 and GAP43 in actin regulation, neurite outgrowth and anatomical plasticity. J Cell Biol 149: 1443-1453.
68. Gauthier-Campbell C, Bredt DS, Murphy TH, El-Husseini Ael-D, (2004) Regulation of dendritic branching and filopodia formation in hippocampal neurons by specific acylated protein motifs. Mol Biol Cell 15: 2205-2217.
69. Reinhard E, Suidan HS, Pavlik A, Monard D, (1994) Glia-derived nexin/protease nexin-1 is expressed by a subset of neurons in the rat brain. J Neurosci Res 37: 256-270.
70. Niclou SP, Suidan HS, Pavlik A, Vejsada R, Monard D, (1998) Changes in the expression of protease-activated receptor 1 and protease nexin-1 mRNA during rat nervous system development and after nerve lesion. Eur J Neurosci 10: 1590-1607.
71. Meins M, Piosik P, Schaeren-Wiemers N, Franzoni S, Troncoso E, et al. (2001) Progressive neuronal and motor dysfunction in mice overexpressing the serine protease inhibitor protease nexin-1 in postmitotic neurons. J Neurosci 21: 8830-8841.
72. Zurn AD, Nick H, Monard D, (1988) A glia-derived nexin promotes neurite outgrowth in cultured chick sympathetic neurons. Dev Neurosci 10: 17-24.
73. Gurwitz D, Cunningham DD, (1990) Neurite outgrowth activity of protease nexin-1 on neuroblastoma cells requires thrombin inhibition. J Cell Physiol 142: 155-162.
74. Díaz-Nido J, Armas-Portela R, Avila J, (1991) Addition of protease inhibitors to culture medium of neuroblastoma cells induces both neurite outgrowth and phosphorylation of microtubule-associated protein MAP-1B. J Cell Sci 98: 409-414.
75. Suidan HS, Stone SR, Hemmings BA, Monard D, (1992) Thrombin causes neurite retraction in neuronal cells through activation of cell surface receptors. Neuron 8: 363-375.
76. Lagriffoul A, Charpentier, Carrette JC, Tougard C, Bockaert J, et al. (1996) Secretion of protease nexin-1 by C6 glioma cells is under the control of a heterotrimeric G protein, Go1. J Biol Chem 271: 31508-31516.
77. Choi BH, Kim RC, Vaughan PJ, Lau A, Van Nostrand WE, et al. (1995) Decreases in protease nexins in Alzheimer's disease brain. Neurobiol Aging 16: 557-562.
78. Thanos S, (1988) Alterations in the morphology of ganglion cell dendrites in the adult retina after optic nerve transection and grafting of peripheral nerve segments. Cell Tissue Res 254: 599-609.
79. Wässle H, (1988) Dendritic maturation of retinal ganglion cells. Trends Neurosci 11: 87-89.
80. Fukuda Y, Watanabe M, Sawai H, Miyoshi T, (1998) Functional recovery of vision in regenerated optic nerve fibers. Vision Res 38: 1545-1553.
81. Yata T, Nakamura M, Sagawa H, Tokita Y, Terasaki H, et al. (2007) Survival and axonal regeneration of OFF-centre retinal ganglion cells of adult cat are promoted with an anti-glaucoma drug, Nipradilol, but not BDNF and CNTF. Neuroscience 148: 53-64.
82. Deplano S, Gargini C, Bisti S, (1999) Electrical activity regulates dendritic reorganisation in ganglion cells after neonatal retinal lesion in the cat. J Comp Neurol 405: 262-270.
83. Deplano S, Gargini C, Maccarone R, Chalupa LM, Bisti S, (2004) Long-term treatment of the developing retina with the metabotropic glutamate agonist APB induces long-term changes in the stratification of retinal ganglion cell dendrites. Dev Neurosci 26: 396-405.
84. Du J-L, Poo M-M, (2004) Rapid BDNF-induced retrograde synaptic modification in a developing retinotectal system. Nature 429: 878-883.
85. Liang FQ, Dejneka NS, Cohen DR, Krasnoperova NV, Lem J, et al. (2001) AAV-mediated delivery of ciliary neurotrophic factor prolongs photoreceptor survival in the rhodopsin knockout mouse. Mol Ther 3: 241-248.
86. Mizuguchi H, Xu Z, Ishii-Watabe A, Uchida E, Hayakawa T, (2000) IRES-dependent second gene expression is significantly lower than cap-dependent first gene expression in a bicistronic vector. Mol Ther 1: 376-382.
87. Kong J-H, Fish DR, Rockhill RL, Masland R, (2005) Diversity of ganglion cells in the mouse retina: unsupervised morphological classification and its limits. J Comp Neurol 489: 293-310.