AAV8 gfp preferentially targets large diameter dorsal root ganglion neurones after both intra-dorsal root ganglion and intrathecal injection

Molecular and Cellular Neuroscience

Volumn 49, Issue 4, 2012, Pages 464-474

  Jacques, Steven J ^a   Ahmed, Zubair ^a   Forbes, Anna ^a   Douglas, Michael R ^a,b   Vigenswara, Vasanthy ^a   Berry, Martin ^a   Logan, Ann ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b RUSSELLS HALL HOSPITAL   (United Kingdom)

Author keywords

Adeno associated virus 8; Dorsal root ganglion neurones; Gene therapy; Green fluorescent protein; Spinal cord injury

Indexed keywords

GREEN FLUORESCENT PROTEIN; PARVOVIRUS VECTOR;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS 8; ANIMAL CELL; ARTICLE; ASTROCYTE; CONTROLLED STUDY; IMMUNOREACTIVITY; MALE; MICROGLIA; NERVE CELL NECROSIS; NERVE FIBER; NERVE PROJECTION; NEUROTROPISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL GANGLION; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; DEPENDOVIRUS; GANGLIA, SPINAL; GENE THERAPY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INJECTIONS, SPINAL; NEURONS; RATS; TRANSDUCTION, GENETIC;

ADENO-ASSOCIATED VIRUS - 8; RATTUS;

EID: 84859094442     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2012.03.002     Document Type: Article

References (51)

1. Ahmed Z., Dent R.G., Suggate E.L., Barrett L.B., Seabright R.J., Berry M., Logan A. Disinhibition of neurotrophin-induced dorsal root ganglion cell neurite outgrowth on CNS myelin by siRNA-mediated knockdown of NgR, p75NTR and Rho-A. Mol. Cell. Neurosci. 2005, 28:509-523.
2. Akache B., Grimm D., Pandey K., Yant S.R., Xu H., Kay M.A. The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3, and 9. J. Virol. 2006, 80:9831-9836.
3. Anand V., Chirmule N., Fersh M., Maguire A.M., Bennett J. Additional transduction events after subretinal readministration of recombinant adeno-associated virus. Hum. Gene Ther. 2000, 11:449-457.
4. Berry M., Carlile J., Hunter A. Peripheral nerve explants grafted into the vitreous body of the eye promote the regeneration of retinal ganglion cell axons severed in the optic nerve. J. Neurocytol. 1996, 25:147-170.
5. Berry M., Carlile J., Hunter A., Tsang W., Rosenstiel P., Sievers J. Optic nerve regeneration after intravitreal peripheral nerve implants: trajectories of axons regrowing through the optic chiasm into the optic tracts. J. Neurocytol. 1999, 28:721-741.
6. Berry M., Ahmed Z., Lorber B., Douglas M., Logan A. Regeneration of axons in the visual system. Restor. Neurol. Neurosci. 2008, 26:147-174.
7. Broekman M.L., Comer L.A., Hyman B.T., Sena-Esteves M. Adeno-associated virus vectors serotyped with AAV8 capsid are more efficient than AAV-1 or -2 serotypes for widespread gene delivery to the neonatal mouse brain. Neuroscience 2006, 138:501-510.
8. Byrod G., Rydevik B., Johansson B.R., Olmarker K. Transport of epidurally applied horseradish peroxidase to the endoneurial space of dorsal root ganglia: a light and electron microscopic study. J. Peripher. Nerv. Syst. 2000, 5:218-226.
9. Caillard O., Moreno H., Schwaller B., Llano I., Celio M.R., Marty A. Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:13372-13377.
10. Chamberlin N.L., Du B., de Lacalle S., Saper C.B. Recombinant adeno-associated virus vector: use for transgene expression and anterograde tract tracing in the CNS. Brain Res. 1998, 793:169-175.
11. De la Calle J.L., Paino C.L. A procedure for direct lumbar puncture in rats. Brain Res. Bull. 2002, 59:245-250.
12. Duan D., Yue Y., Yan Z., Yang J., Engelhardt J.F. Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associated virus. J. Clin. Invest. 2000, 105:1573-1587.
13. Dyck P.J., Peroutka S., Rask C., Burton E., Baker M.K., Lehman K.A., Gillen D.A., Hokanson J.L., O'Brien P.C. Intradermal recombinant human nerve growth factor induces pressure allodynia and lowered heat-pain threshold in humans. Neurology 1997, 48:501-505.
14. Fischer G., Kostic S., Nakai H., Park F., Sapunar D., Yu H., Hogan Q. Direct injection into the dorsal root ganglion: technical, behavioral, and histological observations. J. Neurosci. Methods 2011, 199:43-55.
15. Fleming J., Ginn S.L., Weinberger R.P., Trahair T.N., Smythe J.A., Alexander I.E. Adeno-associated virus and lentivirus vectors mediate efficient and sustained transduction of cultured mouse and human dorsal root ganglia sensory neurons. Hum. Gene Ther. 2001, 12:77-86.
16. Foust K.D., Poirier A., Pacak C.A., Mandel R.J., Flotte T.R. Neonatal intraperitoneal or intravenous injections of recombinant adeno-associated virus type 8 transduce dorsal root ganglia and lower motor neurons. Hum. Gene Ther. 2008, 19:61-70.
17. Gardiner N.J., Cafferty W.B., Slack S.E., Thompson S.W. Expression of gp130 and leukaemia inhibitory factor receptor subunits in adult rat sensory neurones: regulation by nerve injury. J. Neurochem. 2002, 83:100-109.
18. Gaudet A.D., Williams S.J., Hwi L.P., Ramer M.S. Regulation of TRPV2 by axotomy in sympathetic, but not sensory neurons. Brain Res. 2004, 1017:155-162.
19. Goncalves M.A. Adeno-associated virus: from defective virus to effective vector. Virol. J. 2005, 2:43.
20. Gonzalez A.M., Berry M., Greenlees L., Logan A., Baird A. Matrix-mediated gene transfer to brain cortex and dorsal root ganglion neurones by retrograde axonal transport after dorsal column lesion. J. Gene Med. 2006, 8:901-909.
21. Haller F.R., Haller C., Low F.N. The fine structure of cellular layers and connective tissue space at spinal nerve root attachments in the rat. Am. J. Anat. 1972, 133:109-123.
22. Himango W.A., Low F.N. The fine structure of a lateral recess of the subarachnoid space in the rat. Anat. Rec. 1971, 171:1-19.
23. Jamieson S.M., Liu J., Connor B., McKeage M.J. Oxaliplatin causes selective atrophy of a subpopulation of dorsal root ganglion neurons without inducing cell loss. Cancer Chemother. Pharmacol. 2005, 56:391-399.
24. Kaplitt M.G., Leone P., Samulski R.J., Xiao X., Pfaff D.W., O'Malley K.L., During M.J. Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat. Genet. 1994, 8:148-154.
25. Kaplitt M.G., Feigin A., Tang C., Fitzsimons H.L., Mattis P., Lawlor P.A., Bland R.J., Young D., Strybing K., Eidelberg D., During M.J. Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 2007, 369:2097-2105.
26. Klein R.L., Dayton R.D., Leidenheimer N.J., Jansen K., Golde T.E., Zweig R.M. Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins. Mol. Ther. 2006, 13:517-527.
27. Konishi M., Kawamoto K., Izumikawa M., Kuriyama H., Yamashita T. Gene transfer into guinea pig cochlea using adeno-associated virus vectors. J. Gene Med. 2008, 10:610-618.
28. LeWitt P.A., Rezai A.R., Leehey M.A., Ojemann S.G., Flaherty A.W., Eskandar E.N., Kostyk S.K., Thomas K., Sarkar A., Siddiqui M.S., Tatter S.B., Schwalb J.M., Poston K.L., Henderson J.M., Kurlan R.M., Richard I.H., Van Meter L., Sapan C.V., During M.J., Kaplitt M.G., Feigin A. AAV2-GAD gene therapy for advanced Parkinson's disease: a double-blind, sham-surgery controlled, randomised trial. Lancet Neurol. 2011, 10:309-319.
29. Lidster K., Jackson S., Coffey P., Baker M., Garthwaite J., Selwood D., Giovannoni G., Baker D. Neuroprotection in a novel optic neuritis model. Mult. Scler. 2011, 17. S277. P963.
30. Liu K., Lu Y., Lee J.K., Samara R., Willenberg R., Sears-Kraxberger I., Tedeschi A., Park K.K., Jin D., Cai B., Xu B., Connolly L., Steward O., Zheng B., He Z. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat. Neurosci. 2010, 13:1075-1081.
31. Lo W.D., Qu G., Sferra T.J., Clark R., Chen R., Johnson P.R. Adeno-associated virus-mediated gene transfer to the brain: duration and modulation of expression. Hum. Gene Ther. 1999, 10:201-213.
32. Marks W.J., Ostrem J.L., Verhagen L., Starr P.A., Larson P.S., Bakay R.A., Taylor R., Cahn-Weiner D.A., Stoessl A.J., Olanow C.W., Bartus R.T. 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. 2008, 7:400-408.
33. Mastakov M.Y., Baer K., Symes C.W., Leichtlein C.B., Kotin R.M., During M.J. Immunological aspects of recombinant adeno-associated virus delivery to the mammalian brain. J. Virol. 2002, 76:8446-8454.
34. McCown T.J., Xiao X., Li J., Breese G.R., Samulski R.J. Differential and persistent expression patterns of CNS gene transfer by an adeno-associated virus (AAV) vector. Brain Res. 1996, 713:99-107.
35. McLachlan E.M., Janig W., Devor M., Michaelis M. Peripheral nerve injury triggers noradrenergic sprouting within dorsal root ganglia. Nature 1993, 363:543-546.
36. Nauta H.J., Wehman J.C., Koliatsos V.E., Terrell M.A., Chung K. Intraventricular infusion of nerve growth factor as the cause of sympathetic fiber sprouting in sensory ganglia. J. Neurosurg. 1999, 91:447-453.
37. 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.
38. Peden C.S., Burger C., Muzyczka N., Mandel R.J. Circulating anti-wild-type adeno-associated virus type 2 (AAV2) antibodies inhibit recombinant AAV2 (rAAV2)-mediated, but not rAAV5-mediated, gene transfer in the brain. J. Virol. 2004, 78:6344-6359.
39. Peel A.L., Klein R.L. Adeno-associated virus vectors: activity and applications in the CNS. J. Neurosci. Methods 2000, 98:95-104.
40. Sanftner L.M., Sommer J.M., Suzuki B.M., Smith P.H., Vijay S., Vargas J.A., Forsayeth J.R., Cunningham J., Bankiewicz K.S., Kao H., Bernal J., Pierce G.F., Johnson K.W. AAV2-mediated gene delivery to monkey putamen: evaluation of an infusion device and delivery parameters. Exp. Neurol. 2005, 194:476-483.
41. Schmalbruch H. The number of neurons in dorsal root ganglia L4-L6 of the rat. Anat. Rec. 1987, 219:315-322.
42. Storek B., Harder N.M., Banck M.S., Wang C., McCarty D.M., Janssen W.G., Morrison J.H., Walsh C.E., Beutler A.S. Intrathecal long-term gene expression by self-complementary adeno-associated virus type 1 suitable for chronic pain studies in rats. Mol. Pain 2006, 2:4.
43. Storek B., Reinhardt M., Wang C., Janssen W.G., Harder N.M., Banck M.S., Morrison J.H., Beutler A.S. Sensory neuron targeting by self-complementary AAV8 via lumbar puncture for chronic pain. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:1055-1060.
44. Suggate E.L., Ahmed Z., Read M.L., Eaton-Charnock K., Douglas M.R., Gonzalez A.M., Berry M., Logan A. Optimisation of siRNA-mediated RhoA silencing in neuronal cultures. Mol. Cell. Neurosci. 2009, 40:451-462.
45. Sun F., Park K.K., Belin S., Wang D., Lu T., Chen G., Zhang K., Yeung C., Feng G., Yankner B.A., He Z. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 2011, 480:372-375.
46. van Velzen M., Laman J.D., Kleinjan A., Poot A., Osterhaus A.D., Verjans G.M. Neuron-interacting satellite glial cells in human trigeminal ganglia have an APC phenotype. J. Immunol. 2009, 183:2456-2461.
47. Vandenberghe L.H., Wilson J.M., Gao G. Tailoring the AAV vector capsid for gene therapy. Gene Ther. 2009, 16:311-319.
48. Willis, W.D., Coggeshall, R.E., 2004. Sensory mechanisms of the spinal cord, 3rd ed. ed. Kluwer Academic/Plenum, New York; London.
49. Xu Y., Gu Y., Xu G.Y., Wu P., Li G.W., Huang L.Y. Adeno-associated viral transfer of opioid receptor gene to primary sensory neurons: a strategy to increase opioid antinociception. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:6204-6209.
50. Zhang X., Bo X., Anderson P.N., Lieberman A.R., Zhang Y. Distribution and expression of tissue inhibitors of metalloproteinase in dorsal root entry zone and dorsal column after dorsal root injury. J. Neurosci. Res. 2006, 84:278-290.
51. Zheng H., Qiao C., Wang C.H., Li J., Yuan Z., Zhang C., Xiao X. Efficient retrograde transport of adeno-associated virus type 8 to spinal cord and dorsal root ganglion after vector delivery in muscle. Hum. Gene Ther. 2010, 21:87-97.