Pre-immunization with an Intramuscular Injection of AAV9-Human Erythropoietin Vectors Reduces the Vector-Mediated Transduction following Re-Administration in Rat Brain

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Yang, Chun ^a   Yang, Wei Hua ^a   Chen, Sha Sha ^a   Ma, Bao Feng ^b   Li, Bin ^c   Lu, Tao ^a   Qu, Ting Yu ^d   Klein, Ronald L ^b   Zhao, Li Ru ^e   Duan, Wei Ming ^a  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c Louisiana State University Health Sciences Center at Shreveport   (United States)

^d UNIVERSITY OF ILLINOIS   (United States)

^e State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CAPSID PROTEIN; ERYTHROPOIETIN; OVALBUMIN;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN; CELLULAR IMMUNITY; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; FEMALE; GENE EXPRESSION; GENE TARGETING; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNIZATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROGLIA; NONHUMAN; RAT; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; VIRUS GENOME;

ANIMALS; CORPUS STRIATUM; DEPENDOVIRUS; ERYTHROPOIETIN; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; IMMUNIZATION; INJECTIONS, INTRAMUSCULAR; MAJOR HISTOCOMPATIBILITY COMPLEX; NEUTRALIZATION TESTS; RATS; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 84877248831     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063876     Document Type: Article

References (49)

1. Kaplitt MG, Feigin A, Tang C, Fitzsimons HL, Mattis P, et al. (2007) 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 369: 2097-2105.
2. Muramatsu S, Fujimoto K, Ikeguchi K, Shizuma N, Kawasaki K, et al. (2002) Behavioral recovery in a primate model of Parkinson's disease by triple transduction of striatal cells with adeno-associated viral vectors expressing dopamine-synthesizing enzymes. Hum Gene Ther 13: 345-354.
3. Bankiewicz KS, Forsayeth J, Eberling JL, Sanchez-Pernaute R, Pivirotto P, et al. (2006) Long-term clinical improvement in MPTP-lesioned primates after gene therapy with AAV-hAADC. Mol Ther 14: 564-570.
4. Mandel RJ, Manfredsson FP, Foust KD, Rising A, Reimsnider S, et al. (2006) Recombinant adeno-associated viral vectors as therapeutic agents to treat neurological disorders. Mol Ther 13: 463-483.
5. Lowenstein PR, Mandel RJ, Xiong WD, Kroeger K, Castro MG, (2007) Immune responses to adenovirus and adeno-associated vectors used for gene therapy of brain diseases: the role of immunological synapses in understanding the cell biology of neuroimmune interactions. Curr Gene Ther 7: 347-360.
6. Broekman ML, Comer LA, Hyman BT, Sena-Esteves M, (2006) 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 138: 501-510.
7. Cearley CN, Wolfe JH, (2006) Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol Ther 13: 528-537.
8. Foust KD, Nurre E, Montgomery CL, Hernandez A, Chan CM, et al. (2009) Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 27: 59-65.
9. 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. Mol Ther 16: 89-96.
10. Klein RL, Dayton RD, Tatom JB, Diaczynsky CG, Salvatore MF, (2008) Tau expression levels from various adeno-associated virus vector serotypes produce graded neurodegenerative disease states. Eur J Neurosci 27: 1615-1625.
11. Wang DB, Dayton RD, Henning PP, Cain CD, Zhao LR, et al. (2010) Expansive gene transfer in the rat CNS rapidly produces amyotrophic lateral sclerosis relevant sequelae when TDP-43 is overexpressed. Mol Ther 18: 2064-2074.
12. Xue YQ, Ma BF, Zhao LR, Tatom JB, Li B, et al. (2010) AAV9-mediated erythropoietin gene delivery into the brain protects nigral dopaminergic neurons in a rat model of Parkinson's disease. Gene Ther 17: 83-94.
13. 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. Hum Gene Ther 21: 704-712.
14. Calcedo R, Vandenberghe LH, Gao G, Lin J, Wilson JM, (2009) Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses. J Infect Dis 199: 381-390.
15. Veron P, Leborgne C, Monteilhet V, Boutin S, Martin S, et al. (2012) Humoral and cellular capsid-specific immune responses to adeno-associated virus type 1 in randomized healthy donors. J Immunol 188: 6418-6424.
16. Brockstedt DG, Podsakoff GM, Fong L, Kurtzman G, Mueller-Ruchholtz W, et al. (1999) Induction of immunity to antigens expressed by recombinant adeno-associated virus depends on the route of administration. Clin Immunol 92: 67-75.
17. Ciesielska A, Hadaczek P, Mittermeyer G, Zhou S, Wright JF, et al. (2012) Cerebral Infusion of AAV9 Vector-encoding Non-self Proteins Can Elicit Cell-mediated Immune Responses. Mol Ther.
18. Ge Y, Powell S, Van Roey M, McArthur JG, (2001) Factors influencing the development of an anti-factor IX (FIX) immune response following administration of adeno-associated virus-FIX. Blood 97: 3733-3737.
19. Mingozzi F, Hasbrouck NC, Basner-Tschakarjan E, Edmonson SA, Hui DJ, et al. (2007) Modulation of tolerance to the transgene product in a nonhuman primate model of AAV-mediated gene transfer to liver. Blood 110: 2334-2341.
20. Mingozzi F, Maus MV, Hui DJ, Sabatino DE, Murphy SL, et al. (2007) CD8(+) T-cell responses to adeno-associated virus capsid in humans. Nat Med 13: 419-422.
21. Peden CS, Burger C, Muzyczka N, Mandel RJ, (2004) 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 78: 6344-6359.
22. Peden CS, Manfredsson FP, Reimsnider SK, Poirier AE, Burger C, et al. (2009) Striatal readministration of rAAV vectors reveals an immune response against AAV2 capsids that can be circumvented. Mol Ther 17: 524-537.
23. Petry H, Brooks A, Orme A, Wang P, Liu P, et al. (2008) Effect of viral dose on neutralizing antibody response and transgene expression after AAV1 vector re-administration in mice. Gene Ther 15: 54-60.
24. 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. Mol Ther 20: 73-83.
25. Sanftner LM, Suzuki BM, Doroudchi MM, Feng L, McClelland A, et al. (2004) Striatal delivery of rAAV-hAADC to rats with preexisting immunity to AAV. Mol Ther 9: 403-409.
26. Xiao W, Chirmule N, Schnell MA, Tazelaar J, Hughes JV, et al. (2000) Route of administration determines induction of T-cell-independent humoral responses to adeno-associated virus vectors. Mol Ther 1: 323-329.
27. Zaiss AK, Muruve DA, (2008) Immunity to adeno-associated virus vectors in animals and humans: a continued challenge. Gene Ther 15: 808-816.
28. Halbert CL, Rutledge EA, Allen JM, Russell DW, Miller AD, (2000) Repeat transduction in the mouse lung by using adeno-associated virus vectors with different serotypes. J Virol 74: 1524-1532.
29. Manning WC, Zhou S, Bland MP, Escobedo JA, Dwarki V, (1998) Transient immunosuppression allows transgene expression following readministration of adeno-associated viral vectors. Hum Gene Ther 9: 477-485.
30. McIntosh JH, Cochrane M, Cobbold S, Waldmann H, Nathwani SA, et al. (2012) Successful attenuation of humoral immunity to viral capsid and transgenic protein following AAV-mediated gene transfer with a non-depleting CD4 antibody and cyclosporine. Gene Ther 19: 78-85.
31. Lo WD, Qu G, Sferra TJ, Clark R, Chen R, et al. (1999) Adeno-associated virus-mediated gene transfer to the brain: duration and modulation of expression. Hum Gene Ther 10: 201-213.
32. Mastakov MY, Baer K, Symes CW, Leichtlein CB, Kotin RM, et al. (2002) Immunological aspects of recombinant adeno-associated virus delivery to the mammalian brain. J Virol 76: 8446-8454.
33. Klein RL, Dayton RD, Leidenheimer NJ, Jansen K, Golde TE, et al. (2006) Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins. Mol Ther 13: 517-527.
34. Reimsnider S, Manfredsson FP, Muzyczka N, Mandel RJ, (2007) Time course of transgene expression after intrastriatal pseudotyped rAAV2/1, rAAV2/2, rAAV2/5, and rAAV2/8 transduction in the rat. Mol Ther 15: 1504-1511.
35. Signore AP, Weng Z, Hastings T, Van Laar AD, Liang Q, et al. (2006) Erythropoietin protects against 6-hydroxydopamine-induced dopaminergic cell death. J Neurochem 96: 428-443.
36. Siren AL, Fratelli M, Brines M, Goemans C, Casagrande S, et al. (2001) Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci U S A 98: 4044-4049.
37. Villa P, Bigini P, Mennini T, Agnello D, Laragione T, et al. (2003) Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis. J Exp Med 198: 971-975.
38. Liu R, Suzuki A, Guo Z, Mizuno Y, Urabe T, (2006) Intrinsic and extrinsic erythropoietin enhances neuroprotection against ischemia and reperfusion injury in vitro. J Neurochem 96: 1101-1110.
39. Digicaylioglu M, Lipton SA, (2001) Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 412: 641-647.
40. Xue YQ, Zhao LR, Guo WP, Duan WM, (2007) Intrastriatal administration of erythropoietin protects dopaminergic neurons and improves neurobehavioral outcome in a rat model of Parkinson's disease. Neuroscience 146: 1245-1258.
41. Duan WM, Widner H, Bjorklund A, Brundin P, (1993) Sequential intrastriatal grafting of allogeneic embryonic dopamine-rich neuronal tissue in adult rats: will the second graft be rejected? Neuroscience 57: 261-274.
42. Duan WM, Brundin P, Widner H, (1997) Addition of allogeneic spleen cells causes rejection of intrastriatal embryonic mesencephalic allografts in the rat. Neuroscience 77: 599-609.
43. Duan WM, Cameron RM, Brundin P, Widner H, (1997) Rat intrastriatal neural allografts challenged with skin allografts at different time points. Exp Neurol 148: 334-347.
44. Duan WM, Widner H, Brundin P, (1995) Temporal pattern of host responses against intrastriatal grafts of syngeneic, allogeneic or xenogeneic embryonic neuronal tissue in rats. Exp Brain Res 104: 227-242.
45. Duan WM, Widner H, Frodl EM, Brundin P, (1995) Immune reactions following systemic immunization prior or subsequent to intrastriatal transplantation of allogeneic mesencephalic tissue in adult rats. Neuroscience 64: 629-641.
46. Li C, Hirsch M, Asokan A, Zeithaml B, Ma H, et al. (2007) Adeno-associated virus type 2 (AAV2) capsid-specific cytotoxic T lymphocytes eliminate only vector-transduced cells coexpressing the AAV2 capsid in vivo. J Virol 81: 7540-7547.
47. Li H, Murphy SL, Giles-Davis W, Edmonson S, Xiang Z, et al. (2007) Pre-existing AAV capsid-specific CD8+ T cells are unable to eliminate AAV-transduced hepatocytes. Mol Ther 15: 792-800.
48. Klein RL, Dayton RD, Diaczynsky CG, Wang DB, (2010) Pronounced microgliosis and neurodegeneration in aged rats after tau gene transfer. Neurobiol Aging 31: 2091-2102.
49. West MJ, Slomianka L, Gundersen HJ, (1991) Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497.