Adeno-associated virus vectors efficiently transduce mouse and rabbit sensory neurons coinfected with herpes simplex virus 1 following peripheral inoculation

Journal of Virology

Volumn 90, Issue 17, 2016, Pages 7894-7901

  Watson, Zachary L ^a,c   Ertel, Monica K ^b   Lewin, Alfred S ^a   Tuli, Sonal S ^a   Schultz, Gregory S ^a   Neumann, Donna M ^b   Bloom, David C ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

PARVOVIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; FOOT PAD; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; MIXED INFECTION; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SPINAL GANGLION; TRIGEMINUS GANGLION; VIRUS CAPSID; VIRUS LATENCY; VIRUS REACTIVATION; ANIMAL; DEPENDOPARVOVIRUS; EYE; FOOT; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOUSE; PARVOVIRUS INFECTION; RABBITS AND HARES; VIROLOGY;

ANIMALS; COINFECTION; DEPENDOVIRUS; EYE; FOOT; GANGLIA, SPINAL; GENETIC VECTORS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; MICE; PARVOVIRIDAE INFECTIONS; RABBITS; SENSORY RECEPTOR CELLS; TRANSDUCTION, GENETIC; TRIGEMINAL GANGLION;

EID: 84983546584     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01028-16     Document Type: Article

References (32)

1. Margolis TP, Dawson CR, LaVail JH. 1992. Herpes simplex viral infection of the mouse trigeminal ganglion. Immunohistochemical analysis of cell populations. Invest Ophthalmol Vis Sci 33:259-267.
2. Yang L, Voytek CC, Margolis TP. 2000. Immunohistochemical analysis of primary sensory neurons latently infected with herpes simplex virus type 1. J Virol 74:209-217. http://dx.doi.org/10.1128/JVI.74.1.209-217 .2000.
3. Russell DW, Miller AD, Alexander IE. 1994. Adeno-associated virus vectors preferentially transduce cells in S phase. Proc Natl Acad Sci U S A 91:8915-8919. http://dx.doi.org/10.1073/pnas.91.19.8915.
4. Lovric J, Mano M, Zentilin L, Eulalio A, Zacchigna S, Giacca M. 2012. Terminal differentiation of cardiac and skeletal myocytes induces permissivity to AAV transduction by relieving inhibition imposed by DNA damage response proteins. Mol Ther 20:2087-2097. http://dx.doi.org/10.1038=/mt.2012.144.
5. Ferrari FK, Samulski T, Shenk T, Samulski RJ. 1996. Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J Virol 70:3227-3234.
6. Fisher KJ, Gao GP, Weitzman MD, DeMatteo R, Burda JF, Wilson JM.1996. Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis. J Virol 70:520-532.
7. McCarty DM, Monahan PE, Samulski RJ. 2001. Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther 8:1248-1254. http://dx.doi.org/10.1038/sj.gt.3301514.
8. Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. 2008. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 16:1073-1080. http://dx.doi.org/10.1038/mt .2008.76.
9. Grieger JC, Samulski RJ. 2012. Adeno-associated virus vectorology, manufacturing, and clinical applications. Methods Enzymol 507:229-254. http://dx.doi.org/10.1016/B978-0-12-386509-0.00012-0.
10. Grimm D, Zolotukhin S. 2015. E pluribus unum: 50 years of research, millions of viruses, and one goal-tailored acceleration of AAV evolution. Mol Ther 23:1819-1831. http://dx.doi.org/10.1038/mt.2015.173.
11. Zhong L, Zhao W, Wu J, Li B, Zolotukhin S, Govindasamy L, Agbandje-McKenna M, Srivastava A. 2007. A dual role of EGFR protein tyrosine kinase signaling in ubiquitination of AAV2 capsids and viral second- strand DNA synthesis. Mol Ther 15:1323-1330. http://dx.doi.org/10 .1038/sj.mt.6300170.
12. Qi YF, Li QH, Shenoy V, Zingler M, Jun JY, Verma A, Katovich MJ, Raizada MK. 2013. Comparison of the transduction efficiency of tyrosine- mutant adeno-associated virus serotype vectors in kidney. Clin Exp Pharmacol Physiol 40:53-55. http://dx.doi.org/10.1111/1440-1681 .12037.
13. Song L, Li X, Jayandharan GR, Wang Y, Aslanidi GV, Ling C, Zhong L, Gao G, Yoder MC, Ling C, Tan M, Srivastava A. 2013. High-efficiency transduction of primary human hematopoietic stem cells and erythroid lineage-restricted expression by optimized AAV6 serotype vectors in vitro and in a murine xenograft model in vivo. PLoS One 8:e58757. http://dx .doi.org/10.1371/journal.pone.0058757.
14. Kay CN, Ryals RC, Aslanidi GV, Min SH, Ruan Q, Sun J, Dyka FM, Kasuga D, Ayala AE, Van Vliet K, Agbandje-McKenna M, Hauswirth WW, Boye SL, Boye SE. 2013. Targeting photoreceptors via intravitreal delivery using novel, capsid-mutated AAV vectors. PLoS One 8:e62097. http://dx.doi.org/10.1371/journal.pone.0062097.
15. Dalkara D, Byrne LC, Lee T, Hoffmann NV, Schaffer DV, Flannery JG. 2012. Enhanced gene delivery to the neonatal retina through systemic administration of tyrosine-mutated AAV9. Gene Ther 19:176-181. http://dx.doi.org/10.1038/gt.2011.163.
16. Li M, Jayandharan GR, Li B, Ling C, Ma W, Srivastava A, Zhong L. 2010. High-efficiency transduction of fibroblasts and mesenchymal stem cells by tyrosine-mutant AAV2 vectors for their potential use in cellular therapy. Hum Gene Ther 21:1527-1543. http://dx.doi.org/10.1089/hum .2010.005.
17. Markusic DM, Herzog RW, Aslanidi GV, Hoffman BE, Li B, Li M, Jayandharan GR, Ling C, Zolotukhin I, Ma W, Zolotukhin S, Srivastava A, Zhong L. 2010. High-efficiency transduction and correction of murine hemophilia B using AAV2 vectors devoid of multiple surface- exposed tyrosines. Mol Ther 18:2048 -2056. http://dx.doi.org/10 .1038/mt.2010.172.
18. Qiao C, Zhang W, Yuan Z, Shin JH, Li J, Jayandharan GR, Zhong L, Srivastava A, Xiao X, Duan D. 2010. Adeno-associated virus serotype 6 capsid tyrosine-to-phenylalanine mutations improve gene transfer to skeletal muscle.HumGene Ther 21:1343-1348. http://dx.doi.org/10.1089/hum.2010.003.
19. Petrs-Silva H, Dinculescu A, Li Q, Min SH, Chiodo V, Pang JJ, Zhong L, Zolotukhin S, Srivastava A, Lewin AS, Hauswirth WW. 2009. High-efficiency transduction of the mouse retina by tyrosinemutant AAV serotype vectors. Mol Ther 17:463- 471. http://dx.doi.org /10.1038/mt.2008.269.
20. Zhong L, Li B, Mah CS, Govindasamy L, Agbandje-McKenna M, Cooper M, Herzog RW, Zolotukhin I, Warrington KH, Jr, Weigel-Van Aken KA, Hobbs JA, Zolotukhin S, Muzyczka N, Srivastava A. 2008. Next generation of adeno-associated virus 2 vectors: point mutations in tyrosines lead to high-efficiency transduction at lower doses. Proc Natl Acad Sci U S A 105:7827-7832. http://dx.doi.org/10.1073/pnas.0802866105.
21. Yu H, Fischer G, Hogan QH. 2016. AAV-mediated gene transfer to dorsal root ganglion. Methods Mol Biol 1382:251-261. http://dx.doi.org /10.1007/978-1-4939-3271-9_18.
22. Fischer G, Kostic S, Nakai H, Park F, Sapunar D, Yu H, Hogan Q. 2011. Direct injection into the dorsal root ganglion: technical, behavioral, and histological observations. J Neurosci Methods 199:43-55. http://dx.doi .org/10.1016/j.jneumeth.2011.04.021.
23. Foust KD, Poirier A, Pacak CA, Mandel RJ, Flotte TR. 2008. Neonatal intraperitoneal or intravenous injections of recombinant adenoassociated virus type 8 transduce dorsal root ganglia and lower motor neurons. Hum Gene Ther 19:61-70. http://dx.doi.org/10.1089/hum.2007 .093.
24. Storek B, Reinhardt M, Wang C, Janssen WG, Harder NM, Banck MS, Morrison JH, Beutler AS. 2008. Sensory neuron targeting by selfcomplementary AAV8 via lumbar puncture for chronic pain. Proc Natl Acad Sci U S A 105:1055-1060. http://dx.doi.org/10.1073/pnas.0708003105.
25. Beutler AS, Banck MS, Walsh CE, Milligan ED. 2005. Intrathecal gene transfer by adeno-associated virus for pain. Curr Opin Mol Ther 7:431- 439.
26. Wang X, Wang C, Zeng J, Xu X, Hwang PY, Yee WC, Ng YK, Wang S. 2005. Gene transfer to dorsal root ganglia by intrathecal injection: effects on regeneration of peripheral nerves. Mol Ther 12:314-320. http://dx.doi .org/10.1016/j.ymthe.2005.03.032.
27. Vulchanova L, Schuster DJ, Belur LR, Riedl MS, Podetz-Pedersen KM, Kitto KF, Wilcox GL, McIvor RS, Fairbanks CA. 2010. Differential adeno-associated virus mediated gene transfer to sensory neurons following intrathecal delivery by direct lumbar puncture. Mol Pain 6:31. http://dx.doi.org/10.1186/1744-8069-6-31.
28. Margolis TP, Sedarati F, Dobson AT, Feldman LT, Stevens JG. 1992. Pathways of viral gene expression during acute neuronal infection with HSV-1. Virology 189:150-160. http://dx.doi.org/10.1016/0042-6822(92) 90690-Q.
29. Sawtell NM, Thompson RL. 1992. Herpes simplex virus type 1 latencyassociated transcription unit promotes anatomical site-dependent establishment and reactivation from latency. J Virol 66:2157-2169.
30. Aschauer DF, Kreuz S, Rumpel S. 2013. Analysis of transduction efficiency, tropism and axonal transport of AAV serotypes 1, 2, 5, 6, 8 and 9 in the mouse brain. PLoS One 8:e76310. http://dx.doi.org/10.1371/journal .pone.0076310.
31. Salegio EA, Samaranch L, Kells AP, Mittermeyer G, San Sebastian W, Zhou S, Beyer J, Forsayeth J, Bankiewicz KS. 2013. Axonal transport of adeno-associated viral vectors is serotype-dependent. Gene Ther 20:348-352. http://dx.doi.org/10.1038/gt.2012.27.
32. Castle MJ, Perlson E, Holzbaur EL, Wolfe JH. 8 October 2013. Longdistance axonal transport of AAV9 is driven by dynein and kinesin-2 and is trafficked in a highly motile Rab7-positive compartment. Mol Ther http://dx.doi.org/10.1038/mt.2013.237.