Intraganglionic AAV6 Results in Efficient and Long-Term Gene Transfer to Peripheral Sensory Nervous System in Adult Rats

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Yu, Hongwei ^a   Fischer, Gregory ^a   Ferhatovic, Lejla ^b   Fan, Fan ^c   Light, Alan R ^d   Weihrauch, Dorothee ^a   Sapunar, Damir ^b   Nakai, Hiroyuki ^e   Park, Frank ^a,g   Hogan, Quinn H ^a,f  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF SPLIT   (Croatia)

^c UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^f CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

^g UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; CALCITONIN GENE RELATED PEPTIDE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CELL MARKER; ENHANCED GREEN FLUORESCENT PROTEIN; NEUROFILAMENT 200 PROTEIN; NEUROFILAMENT PROTEIN; PARVOVIRUS VECTOR; PARVOVIRUS VECTOR 6; PARVOVIRUS VECTOR 8; PROTEIN IB4; PROTEIN TYROSINE KINASE A; PROTEIN VP1; PROTEIN VP2; PROTEIN VP3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; CELL SIZE; CELLULAR IMMUNITY; COMPARATIVE STUDY; CONTROLLED STUDY; GENE EXPRESSION; HYPERALGESIA; IMMUNOREACTIVITY; MALE; NERVE FIBER; NERVE PROJECTION; NERVOUS SYSTEM INFLAMMATION; NEUROTOXICITY; NEUROTROPISM; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PURIFICATION; RAT; SENSORY NERVE; SPINAL CORD DORSAL HORN; SPINAL GANGLION; VIRAL GENE DELIVERY SYSTEM; VIRUS PARTICLE;

ANIMALS; DEPENDOVIRUS; GANGLIA, SPINAL; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; MALE; RATS; SENSORY RECEPTOR CELLS;

ADENO-ASSOCIATED VIRUS; RATTUS;

EID: 84876189197     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061266     Document Type: Article

References (66)

1. Julius D, Basbaum AI, (2001) Molecular mechanisms of nociception. Nature 413: 203-210.
2. Fischer G, Kostic S, Nakai H, Park F, Sapunar D, et al. (2011) Direct injection into the dorsal root ganglion: technical, behavioral, and histological observations. J Neurosci Methods 199: 43-55.
3. Mason MR, Ehlert EM, Eggers R, Pool CW, Hermening S, et al. (2010) Comparison of AAV serotypes for gene delivery to dorsal root ganglion neurons. Mol Ther 18: 715-724.
4. Pfirrmann CW, Oberholzer PA, Zanetti M, Boos N, Trudell DJ, et al. (2001) Selective nerve root blocks for the treatment of sciatica: evaluation of injection site and effectiveness-a study with patients and cadavers. Radiology 221: 704-711.
5. Samad OA, Tan AM, Cheng X, Foster E, Dib-Hajj SD, et al. (2012) Virus-mediated shRNA Knockdown of Na(v)1.3 in Rat Dorsal Root Ganglion Attenuates Nerve Injury-induced Neuropathic Pain. Molecular therapy: the journal of the American Society of Gene Therapy.
6. Davidson BL, Breakefield XO, (2003) Viral vectors for gene delivery to the nervous system. Nature reviews Neuroscience 4: 353-364.
7. Beutler AS, Reinhardt M, (2009) AAV for pain: steps towards clinical translation. Gene Ther 16: 461-469.
8. Asokan A, Schaffer DV, Samulski RJ, (2012) The AAV vector toolkit: poised at the clinical crossroads. Molecular therapy: the journal of the American Society of Gene Therapy 20: 699-708.
9. Vasileva A, Jessberger R, (2005) Precise hit: adeno-associated virus in gene targeting. Nature reviews Microbiology 3: 837-847.
10. Jooss K, Yang Y, Fisher KJ, Wilson JM, (1998) Transduction of dendritic cells by DNA viral vectors directs the immune response to transgene products in muscle fibers. Journal of virology 72: 4212-4223.
11. Towne C, Pertin M, Beggah AT, Aebischer P, Decosterd I, (2009) Recombinant adeno-associated virus serotype 6 (rAAV2/6)-mediated gene transfer to nociceptive neurons through different routes of delivery. Mol Pain 5: 52.
12. Storek B, Reinhardt M, Wang C, Janssen WG, Harder NM, et al. (2008) Sensory neuron targeting by self-complementary AAV8 via lumbar puncture for chronic pain. Proceedings of the National Academy of Sciences of the United States of America 105: 1055-1060.
13. Vulchanova L, Schuster DJ, Belur LR, Riedl MS, Podetz-Pedersen KM, et al. (2010) Differential adeno-associated virus mediated gene transfer to sensory neurons following intrathecal delivery by direct lumbar puncture. Mol Pain 6: 31.
14. Xu Y, Gu Y, Wu P, Li GW, Huang LY, (2003) Efficiencies of transgene expression in nociceptive neurons through different routes of delivery of adeno-associated viral vectors. Human gene therapy 14: 897-906.
15. Xu Y, Gu Y, Xu GY, Wu P, Li GW, et al. (2003) Adeno-associated viral transfer of opioid receptor gene to primary sensory neurons: a strategy to increase opioid antinociception. Proceedings of the National Academy of Sciences of the United States of America 100: 6204-6209.
16. Kim J, Kim SJ, Lee H, Chang JW, (2009) Effective neuropathic pain relief through sciatic nerve administration of GAD65-expressing rAAV2. Biochemical and biophysical research communications 388: 73-78.
17. Hollis ER, 2nd, Jamshidi P, Lorenzana AO, Lee JK, Gray SJ, et al (2010) Transient demyelination increases the efficiency of retrograde AAV transduction. Molecular therapy: the journal of the American Society of Gene Therapy 18: 1496-1500.
18. Schaffer DV, Koerber JT, Lim KI, (2008) Molecular engineering of viral gene delivery vehicles. Annual review of biomedical engineering 10: 169-194.
19. Van Vliet KM, Blouin V, Brument N, Agbandje-McKenna M, Snyder RO, (2008) The role of the adeno-associated virus capsid in gene transfer. Methods in molecular biology 437: 51-91.
20. Bevan AK, Duque S, Foust KD, Morales PR, Braun L, et al. (2011) Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders. Molecular therapy: the journal of the American Society of Gene Therapy 19: 1971-1980.
21. Federici T, Taub JS, Baum GR, Gray SJ, Grieger JC, et al. (2012) Robust spinal motor neuron transduction following intrathecal delivery of AAV9 in pigs. Gene therapy 19: 852-859.
22. Hirai T, Enomoto M, Machida A, Yamamoto M, Kuwahara H, et al. (2012) Intrathecal shRNA-AAV9 inhibits target protein expression in the spinal cord and dorsal root ganglia of adult mice. Human gene therapy methods 23: 119-127.
23. Iwamoto N, Watanabe A, Yamamoto M, Miyake N, Kurai T, et al. (2009) Global diffuse distribution in the brain and efficient gene delivery to the dorsal root ganglia by intrathecal injection of adeno-associated viral vector serotype 1. The journal of gene medicine 11: 498-505.
24. Jacques SJ, Ahmed Z, Forbes A, Douglas MR, Vigenswara V, et al. (2012) AAV8(gfp) preferentially targets large diameter dorsal root ganglion neurones after both intra-dorsal root ganglion and intrathecal injection. Molecular and cellular neurosciences 49: 464-474.
25. Beutler AS, Banck MS, Walsh CE, Milligan ED, (2005) Intrathecal gene transfer by adeno-associated virus for pain. Current opinion in molecular therapeutics 7: 431-439.
26. Beutler AS, (2010) AAV provides an alternative for gene therapy of the peripheral sensory nervous system. Molecular therapy: the journal of the American Society of Gene Therapy 18: 670-673.
27. Ayuso E, Mingozzi F, Montane J, Leon X, Anguela XM, et al. (2010) High AAV vector purity results in serotype- and tissue-independent enhancement of transduction efficiency. Gene therapy 17: 503-510.
28. Klein RL, Dayton RD, Tatom JB, Henderson KM, Henning PP, (2008) AAV8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purification method. Molecular therapy: the journal of the American Society of Gene Therapy 16: 89-96.
29. Wright JF, (2008) Manufacturing and characterizing AAV-based vectors for use in clinical studies. Gene therapy 15: 840-848.
30. Samulski RJ, Chang LS, Shenk T, (1989) Helper-free stocks of recombinant adeno-associated viruses: normal integration does not require viral gene expression. Journal of virology 63: 3822-3828.
31. Grieger JC, Choi VW, Samulski RJ, (2006) Production and characterization of adeno-associated viral vectors. Nat Protoc 1: 1412-1428.
32. Wang Z, Ma HI, Li J, Sun L, Zhang J, et al. (2003) Rapid and highly efficient transduction by double-stranded adeno-associated virus vectors in vitro and in vivo. Gene Ther 10: 2105-2111.
33. Ayuso E, Mingozzi F, Montane J, Leon X, Anguela XM, et al. (2010) High AAV vector purity results in serotype- and tissue-independent enhancement of transduction efficiency. Gene Ther 17: 503-510.
34. Homs J, Ariza L, Pages G, Udina E, Navarro X, et al. (2011) Schwann cell targeting via intrasciatic injection of AAV8 as gene therapy strategy for peripheral nerve regeneration. Gene Ther 18: 622-630.
35. Sommer JM, Smith PH, Parthasarathy S, Isaacs J, Vijay S, et al. (2003) Quantification of adeno-associated virus particles and empty capsids by optical density measurement. Mol Ther 7: 122-128.
36. Yu H, Fischer G, Jia G, Reiser J, Park F, et al. (2011) Lentiviral gene transfer into the dorsal root ganglion of adult rats. Mol Pain 7: 63.
37. Hammond DL, Ackerman L, Holdsworth R, Elzey B, (2004) Effects of spinal nerve ligation on immunohistochemically identified neurons in the L4 and L5 dorsal root ganglia of the rat. The Journal of comparative neurology 475: 575-589.
38. Ruscheweyh R, Forsthuber L, Schoffnegger D, Sandkuhler J, (2007) Modification of classical neurochemical markers in identified primary afferent neurons with Abeta-, Adelta-, and C-fibers after chronic constriction injury in mice. The Journal of comparative neurology 502: 325-336.
39. Dixon WJ, (1980) Efficient analysis of experimental observations. Annual review of pharmacology and toxicology 20: 441-462.
40. Hogan Q, Sapunar D, Modric-Jednacak K, McCallum JB, (2004) Detection of neuropathic pain in a rat model of peripheral nerve injury. Anesthesiology 101: 476-487.
41. Wu HE, Gemes G, Zoga V, Kawano T, Hogan QH, (2010) Learned avoidance from noxious mechanical simulation but not threshold semmes weinstein filament stimulation after nerve injury in rats. The journal of pain: official journal of the American Pain Society 11: 280-286.
42. Lock M, Alvira M, Vandenberghe LH, Samanta A, Toelen J, et al. (2010) Rapid, simple, and versatile manufacturing of recombinant adeno-associated viral vectors at scale. Human gene therapy 21: 1259-1271.
43. Zeltner N, Kohlbrenner E, Clement N, Weber T, Linden RM, (2010) Near-perfect infectivity of wild-type AAV as benchmark for infectivity of recombinant AAV vectors. Gene therapy 17: 872-879.
44. Zolotukhin S, Byrne BJ, Mason E, Zolotukhin I, Potter M, et al. (1999) Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene therapy 6: 973-985.
45. Tsujino H, Kondo E, Fukuoka T, Dai Y, Tokunaga A, et al. (2000) Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: A novel neuronal marker of nerve injury. Molecular and cellular neurosciences 15: 170-182.
46. Glatzel M, Flechsig E, Navarro B, Klein MA, Paterna JC, et al. (2000) Adenoviral and adeno-associated viral transfer of genes to the peripheral nervous system. Proc Natl Acad Sci U S A 97: 442-447.
47. Snyder BR, Gray SJ, Quach ET, Huang JW, Leung CH, et al. (2011) Comparison of adeno-associated viral vector serotypes for spinal cord and motor neuron gene delivery. Human gene therapy 22: 1129-1135.
48. Fang X, Djouhri L, McMullan S, Berry C, Okuse K, et al. (2005) trkA is expressed in nociceptive neurons and influences electrophysiological properties via Nav1.8 expression in rapidly conducting nociceptors. The Journal of neuroscience: the official journal of the Society for Neuroscience 25: 4868-4878.
49. Belmonte C, Viana F, (2008) Molecular and cellular limits to somatosensory specificity. Molecular pain 4: 14.
50. Hunt SP, Mantyh PW, (2001) The molecular dynamics of pain control. Nature reviews Neuroscience 2: 83-91.
51. Todd A, Koerber H (2006) In:Neuroanatomical substrates of spinal nociception In Wall and Melzack's Textbook of Pain; SB. M, M. K, editors: Elsevier, Philadelphia; 73-90.
52. Ussher JE, Taylor JA, (2010) Optimized transduction of human monocyte-derived dendritic cells by recombinant adeno-associated virus serotype 6. Human gene therapy 21: 1675-1686.
53. Boutin S, Monteilhet V, Veron P, Leborgne C, Benveniste O, et al. (2010) Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) types 1, 2, 5, 6, 8, and 9 in the healthy population: implications for gene therapy using AAV vectors. Human gene therapy 21: 704-712.
54. Chen J, Wu Q, Yang P, Hsu HC, Mountz JD, (2006) Determination of specific CD4 and CD8 T cell epitopes after AAV2- and AAV8-hF.IX gene therapy. Molecular therapy: the journal of the American Society of Gene Therapy 13: 260-269.
55. Rapti K, Louis-Jeune V, Kohlbrenner E, Ishikawa K, Ladage D, et al. (2012) Neutralizing antibodies against AAV serotypes 1, 2, 6, and 9 in sera of commonly used animal models. Molecular therapy: the journal of the American Society of Gene Therapy 20: 73-83.
56. Lin SW, Hensley SE, Tatsis N, Lasaro MO, Ertl HC, (2007) Recombinant adeno-associated virus vectors induce functionally impaired transgene product-specific CD8+ T cells in mice. The Journal of clinical investigation 117: 3958-3970.
57. Rogers GL, Martino AT, Aslanidi GV, Jayandharan GR, Srivastava A, et al. (2011) Innate Immune Responses to AAV Vectors. Frontiers in microbiology 2: 194.
58. Homs J, Ariza L, Pages G, Udina E, Navarro X, et al. (2011) Schwann cell targeting via intrasciatic injection of AAV8 as gene therapy strategy for peripheral nerve regeneration. Gene therapy 18: 622-630.
59. Xu Q, Chou B, Fitzsimmons B, Miyanohara A, Shubayev V, et al. (2012) In vivo gene knockdown in rat dorsal root ganglia mediated by self-complementary adeno-associated virus serotype 5 following intrathecal delivery. PloS one 7: e32581.
60. Sun J, Li D, Hao Y, Zhang Y, Fan W, et al. (2009) Posttranscriptional regulatory elements enhance antigen expression and DNA vaccine efficacy. DNA and cell biology 28: 233-240.
61. Weeratna RD, Wu T, Efler SM, Zhang L, Davis HL, (2001) Designing gene therapy vectors: avoiding immune responses by using tissue-specific promoters. Gene therapy 8: 1872-1878.
62. Cordier L, Gao GP, Hack AA, McNally EM, Wilson JM, et al. (2001) Muscle-specific promoters may be necessary for adeno-associated virus-mediated gene transfer in the treatment of muscular dystrophies. Human gene therapy 12: 205-215.
63. Martino AT, Suzuki M, Markusic DM, Zolotukhin I, Ryals RC, et al. (2011) The genome of self-complementary adeno-associated viral vectors increases Toll-like receptor 9-dependent innate immune responses in the liver. Blood 117: 6459-6468.
64. Mingozzi F, Meulenberg JJ, Hui DJ, Basner-Tschakarjan E, Hasbrouck NC, et al. (2009) AAV-1-mediated gene transfer to skeletal muscle in humans results in dose-dependent activation of capsid-specific T cells. Blood 114: 2077-2086.
65. Urabe M, Xin KQ, Obara Y, Nakakura T, Mizukami H, et al. (2006) Removal of empty capsids from type 1 adeno-associated virus vector stocks by anion-exchange chromatography potentiates transgene expression. Molecular therapy: the journal of the American Society of Gene Therapy 13: 823-828.
66. Qu G, Bahr-Davidson J, Prado J, Tai A, Cataniag F, et al. (2007) Separation of adeno-associated virus type 2 empty particles from genome containing vectors by anion-exchange column chromatography. Journal of virological methods 140: 183-192.