Efficient and Targeted Transduction of Nonhuman Primate Liver with Systemically Delivered Optimized AAV3B Vectors

Molecular Therapy

Volumn 23, Issue 12, 2015, Pages 1867-1876

  Li, Shaoyong ^a   Ling, Chen ^b,c   Zhong, Li ^a   Li, Mengxin ^a   Su, Qin ^a   He, Ran ^a   Tang, Qiushi ^a   Greiner, Dale L ^a   Shultz, Leonard D ^d   Brehm, Michael A ^a   Flotte, Terence R ^a   Mueller, Christian ^a   Srivastava, Arun ^b,c   Gao, Guangping ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

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

^d JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN G ANTIBODY; MESSENGER RNA; NEUTRALIZING ANTIBODY; PARVOVIRUS VECTOR; RECOMBINANT CHORIONIC GONADOTROPIN; CAPSID PROTEIN; GREEN FLUORESCENT PROTEIN;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS 8; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER CELL; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIVER CELL; MALE; MOUSE; MOUSE MODEL; NONHUMAN; RECOMBINANT ADENO ASSOCIATED VIRUS SEROTYPE 3B; RHESUS MONKEY; TISSUE DISTRIBUTION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS CAPSID; VIRUS RECOMBINANT; ANIMAL; CANCER TRANSPLANTATION; CYTOLOGY; DEPENDOPARVOVIRUS; DISEASE MODEL; GENE EXPRESSION REGULATION; GENE THERAPY; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; LIVER; LIVER NEOPLASMS; METABOLISM; TUMOR CELL LINE;

ANIMALS; CAPSID PROTEINS; CELL LINE, TUMOR; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC THERAPY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HEPATOCYTES; HUMANS; LIVER; LIVER NEOPLASMS; MACACA MULATTA; MICE; NEOPLASM TRANSPLANTATION; TRANSDUCTION, GENETIC;

EID: 84952638250     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2015.174     Document Type: Article

References (48)

1. Ahmed, SS, Li, J, Godwin, J, Gao, G and Zhong, L (2013). Gene transfer in the liver using recombinant adeno-associated virus. Curr Protoc Microbiol Chapter 14: Unit14D.6.
2. Manno, CS, Pierce, GF, Arruda, VR, Glader, B, Ragni, M, Rasko, JJ et al. (2006). Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat Med 12: 342-347.
3. Nathwani, AC, Tuddenham, EG, Rangarajan, S, Rosales, C, McIntosh, J, Linch, DC et al. (2011). Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med 365: 2357-2365.
4. Monteilhet, V, Saheb, S, Boutin, S, Leborgne, C, Veron, P, Montus, MF et al. (2011). A 10 patient case report on the impact of plasmapheresis upon neutralizing factors against adeno-associated virus (AAV) types 1, 2, 6, and 8. Mol Ther 19: 2084-2091.
5. Li, C, Narkbunnam, N, Samulski, RJ, Asokan, A, Hu, G, Jacobson, LJ et al.; Joint Outcome Study Investigators. (2012). Neutralizing antibodies against adenoassociated virus examined prospectively in pediatric patients with hemophilia. Gene Ther 19: 288-294.
6. Mingozzi, F, Maus, MV, Hui, DJ, Sabatino, DE, Murphy, SL, Rasko, JE et al. (2007). CD8(+) T-cell responses to adeno-associated virus capsid in humans. Nat Med 13: 419-422.
7. Glushakova, LG, Lisankie, MJ, Eruslanov, EB, Ojano-Dirain, C, Zolotukhin, I, Liu, C et al. (2009). AAV3-mediated transfer and expression of the pyruvate dehydrogenase E1 alpha subunit gene causes metabolic remodeling and apoptosis of human liver cancer cells. Mol Genet Metab 98: 289-299.
8. Ling, C, Lu, Y, Kalsi, JK, Jayandharan, GR, Li, B, Ma, W et al. (2010). Human hepatocyte growth factor receptor is a cellular coreceptor for adeno-associated virus serotype 3. Hum Gene Ther 21: 1741-1747.
9. Zhong, L, Li, B, Mah, CS, Govindasamy, L, Agbandje-McKenna, M, Cooper, M et al. (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 USA 105: 7827-7832.
10. Markusic, DM, Herzog, RW, Aslanidi, GV, Hoffman, BE, Li, B, Li, M et al. (2010). High-efficiency transduction and correction of murine hemophilia B using AAV2 vectors devoid of multiple surface-exposed tyrosines. Mol Ther 18: 2048-2056.
11. Aslanidi, GV, Rivers, AE, Ortiz, L, Govindasamy, L, Ling, C, Jayandharan, GR et al. (2012). High-efficiency transduction of human monocyte-derived dendritic cells by capsid-modified recombinant AAV2 vectors. Vaccine 30: 3908-3917.
12. Aslanidi, GV, Rivers, AE, Ortiz, L, Song, L, Ling, C, Govindasamy, L et al. (2013). Optimization of the capsid of recombinant adeno-associated virus 2 (AAV2) vectors: the final threshold PLoS One 8: e59142.
13. Cheng, B, Ling, C, Dai, Y, Lu, Y, Glushakova, LG, Gee, SW et al. (2012). Development of optimized AAV3 serotype vectors: mechanism of high-efficiency transduction of human liver cancer cells. Gene Ther 19: 375-384.
14. Ling, C, Wang, Y, Zhang, Y, Vercauteren, K, Verhoye, L, Lu, Y et al. (2014). Transduction of primary human hepatocytes in vitro and in humanized murine livers in vivo by recombinant AAV3 vectors. Mol Ther 22: S2.
15. Ling, C, Wang, Y, Zhang, Y, Ejjigani, A, Yin, Z, Lu, Y et al. (2014). Selective in vivo targeting of human liver tumors by optimized AAV3 vectors in a murine xenograft model. Hum Gene Ther 25: 1023-1034.
16. Lisowski, L, Dane, AP, Chu, K, Zhang, Y, Cunningham, SC, Wilson, EM et al. (2014). Selection and evaluation of clinically relevant AAV variants in a xenograft liver model. Nature 506: 382-386.
17. Blacklow, NR, Hoggan, MD, Sereno, MS, Brandt, CD, Kim, HW, Parrott, RH et al. (1971). A seroepidemiologic study of adenovirus-associated virus infection in infants and children. Am J Epidemiol 94: 359-366.
18. van der Marel, S, Comijn, EM, Verspaget, HW, van Deventer, S, van den Brink, GR, Petry, H et al. (2011). Neutralizing antibodies against adeno-associated viruses in inflammatory bowel disease patients: implications for gene therapy. Inflamm Bowel Dis 17: 2436-2442.
19. Ling, C, Wang, Y, Feng, YL, Zhang, YN, Li, J, Hu, XR et al. (2015). Prevalence of neutralizing antibodies against liver-tropic adeno-associated virus serotype vectors in 100 healthy Chinese and its potential relation to body constitutions. J Integr Med 13: 341-346.
20. Sprecher-Goldberger, S, Thiry, L, Lefébvre, N, Dekegel, D and de Halleux, F (1971). Complement-fixation antibodies to adenovirus-associated viruses, cytomegaloviruses and herpes simplex viruses in patients with tumors and in control individuals. Am J Epidemiol 94: 351-358.
21. Zincarelli, C, Soltys, S, Rengo, G and Rabinowitz, JE (2008). Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 16: 1073-1080.
22. Gao, G, Lu, Y, Calcedo, R, Grant, RL, Bell, P, Wang, L et al. (2006). Biology of AAV serotype vectors in liver-directed gene transfer to nonhuman primates. Mol Ther 13: 77-87.
23. Gao, GP, Lu, Y, Sun, X, Johnston, J, Calcedo, R, Grant, R et al. (2006). Highlevel transgene expression in nonhuman primate liver with novel adenoassociated virus serotypes containing self-complementary genomes. J Virol 80: 6192-6194.
24. Gao, G, Wang, Q, Calcedo, R, Mays, L, Bell, P, Wang, L et al. (2009). Adeno-associated virus-mediated gene transfer to nonhuman primate liver can elicit destructive transgene-specific T cell responses. Hum Gene Ther 20: 930-942.
25. Gao, G, Bish, LT, Sleeper, MM, Mu, X, Sun, L, Lou, Y et al. (2011). Transendocardial delivery of AAV6 results in highly efficient and global cardiac gene transfer in rhesus macaques. Hum Gene Ther 22: 979-984.
26. Dong, X, Tian, W, Wang, G, Dong, Z, Shen, W, Zheng, G et al. (2010). Establishment of an AAV reverse infection-based array. PLoS One 5: e13479.
27. Ellis, BL, Hirsch, ML, Barker, JC, Connelly, JP, Steininger, RJ, Porteus, MH (2013). A survey of ex vivo/in vitro transduction efficiency of mammalian primary cells and cell lines with nine natural adeno-associated virus (AAV1-9) and one engineered adenoassociated virus serotype. Virol J 10: 74.
28. Wang, L, Calcedo, R, Wang, H, Bell, P, Grant, R, Vandenberghe, LH et al. (2010). The pleiotropic effects of natural AAV infections on liver-directed gene transfer in macaques. Mol Ther 18: 126-134.
29. Wang, L, Calcedo, R, Bell, P, Lin, J, Grant, RL, Siegel, DL et al. (2011). Impact of preexisting immunity on gene transfer to nonhuman primate liver with adeno-associated virus 8 vectors. Hum Gene Ther 22: 1389-1401.
30. Gray, SJ, Matagne, V, Bachaboina, L, Yadav, S, Ojeda, SR and Samulski, RJ (2011). Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol Ther 19: 1058-1069.
31. Ponnazhagan, S, Mukherjee, P, Yoder, MC, Wang, XS, Zhou, SZ, Kaplan, J et al. (1997). Adeno-associated virus 2-mediated gene transfer in vivo: organ-tropism and expression of transduced sequences in mice. Gene 190: 203-210.
32. Snyder, RO, Miao, CH, Patijn, GA, Spratt, SK, Danos, O, Nagy, D et al. (1997). Persistent and therapeutic concentrations of human factor IX in mice after hepatic gene transfer of recombinant AAV vectors. Nat Genet 16: 270-276.
33. Mount, JD, Herzog, RW, Tillson, DM, Goodman, SA, Robinson, N, McCleland, ML et al. (2002). Sustained phenotypic correction of hemophilia B dogs with a factor IX null mutation by liver-directed gene therapy. Blood 99: 2670-2676.
34. Nathwani, AC, Reiss, UM, Tuddenham, EG, Rosales, C, Chowdary, P, McIntosh, J et al. (2014). Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N Engl J Med 371: 1994-2004.
35. Ling, C, Lu, Y, Cheng, B, McGoogan, KE, Gee, SW, Ma, W et al. (2011). Highefficiency transduction of liver cancer cells by recombinant adeno-associated virus serotype 3 vectors. J Vis Exp 49: Pii: 2538.
36. Vercauteren, K, Van Den Eede, N, Mesalam, AA, Belouzard, S, Catanese, MT, Bankwitz, D et al. (2014). Successful anti-scavenger receptor class B type I (SR-BI) monoclonal antibody therapy in humanized mice after challenge with HCV variants with in vitro resistance to SR-BI-targeting agents. Hepatology 60: 1508-1518.
37. Bissig-Choisat, B, Wang, L, Legras, X, Saha, PK, Chen, L, Bell, P et al. (2015). Development and rescue of human familial hypercholesterolaemia in a xenograft mouse model. Nat Commun 6: 7339.
38. Iyer, A, Kmiecik, TE, Park, M, Daar, I, Blair, D, Dunn, KJ et al. (1990). Structure, tissuespecific expression, and transforming activity of the mouse met protooncogene. Cell Growth Differ 1: 87-95.
39. Akache, B, Grimm, D, Pandey, K, Yant, SR, Xu, H and Kay, MA (2006). The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3, and 9. J Virol 80: 9831-9836.
40. Yan, G, Zhang, G, Fang, X, Zhang, Y, Li, C, Ling, F et al. (2011). Genome sequencing and comparison of two nonhuman primate animal models, the cynomolgus and Chinese rhesus macaques. Nat Biotechnol 29: 1019-1023.
41. Velazquez, VM, Bowen, DG and Walker, CM (2009). Silencing of T lymphocytes by antigen-driven programmed death in recombinant adeno-associated virus vectormediated gene therapy. Blood 113: 538-545.
42. Duan, D, Yue, Y, Yan, Z, Yang, J and Engelhardt, JF (2000). Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associated virus. J Clin Invest 105: 1573-1587.
43. Ayuso, E, Mingozzi, F, Montane, J, Leon, X, Anguela, XM, Haurigot, V et al. (2010). High AAV vector purity results in serotype-and tissue-independent enhancement of transduction efficiency. Gene Ther 17: 503-510.
44. Gao, G, and Sena-Esteves, M. Introducing genes into mammalian cells: viral vectors. In: Green, MR and J, Sambrook (eds). Molecular Cloning, vol. 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2012. pp. 1209-1334.
45. Calcedo, R, Vandenberghe, LH, Gao, G, Lin, J and Wilson, JM (2009). Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses. J Infect Dis 199: 381-390.
46. Hurlbut, GD, Ziegler, RJ, Nietupski, JB, Foley, JW, Woodworth, LA, Meyers, E et al. (2010). Preexisting immunity and low expression in primates highlight translational challenges for liver-directed AAV8-mediated gene therapy. Mol Ther 18: 1983-1994.
47. Carlson, JA, Rogers, BB, Sifers, RN, Finegold, MJ, Clift, SM, DeMayo, FJ et al. (1989). Accumulation of PiZ alpha 1-antitrypsin causes liver damage in transgenic mice. J Clin Invest 83: 1183-1190.
48. Wang, LN, Wang, Y, Lu, Y, Yin, ZF, Zhang, YH, Aslanidi, GV et al. (2014). Pristimerin enhances recombinant adeno-associated virus vector-mediated transgene expression in human cell lines in vitro and murine hepatocytes in vivo. J Integr Med 12: 20-34.