Enhanced transgene expression from recombinant single-stranded D-sequence-substituted adeno-associated virus vectors in human cell lines in vitro and in murine hepatocytes in vivo

Journal of Virology

Volumn 89, Issue 2, 2015, Pages 952-961

  Ling, Chen ^a   Wang, Yuan ^a,b,c   Lu, Yuan ^a   Wang, Lina ^a,b   Jayandharan, Giridhara R ^d,h   Aslanidi, George V ^a   Li, Baozheng ^a   Cheng, Binbin ^a,b   Ma, Wenqin ^a   Lentz, Thomas ^e   Ling, Changquan ^b,c   Xiao, Xiao ^e,f   Jude Samulski, R ^e   Muzyczka, Nicholas ^a   Srivastava, Arun ^a,g  

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

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^d CHRISTIAN MEDICAL COLLEGE   (India)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF NORTH CAROLINA   (United States)

^g UNIVERSITY OF FLORIDA   (United States)

^h INDIAN INSTITUTE OF TECHNOLOGY KANPUR   (India)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PARVOVIRUS VECTOR; SINGLE STRANDED DNA; TRANSCRIPTION FACTOR;

ADENOVIRIDAE; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA REPLICATION; DNA SYNTHESIS; GENE EXPRESSION; GENE SEQUENCE; GENE THERAPY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INVERTED TERMINAL REPEAT; LIVER CELL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY; VIRUS GENOME; VIRUS REPLICATION; ANIMAL; C57BL MOUSE; CELL LINE; DEPENDOPARVOVIRUS; GENE DELETION; GENE VECTOR; GENETICS; PHYSIOLOGY; PROCEDURES; TRANSGENE; VIROLOGY; VIRUS ASSEMBLY;

ADENO-ASSOCIATED VIRUS; MURINAE;

ANIMALS; CELL LINE; DEPENDOVIRUS; GENE EXPRESSION; GENETIC THERAPY; GENETIC VECTORS; HEPATOCYTES; HUMANS; MALE; MICE, INBRED C57BL; SEQUENCE DELETION; TRANSGENES; VIRUS ASSEMBLY;

EID: 84920848456     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02581-14     Document Type: Article

References (41)

1. Srivastava A, Lusby EW, Berns KI. 1983. Nucleotide sequence and organization of the adeno-associated virus 2 genome. J Virol 45:555-564.
2. Ling CQ, Wang LN, Wang Y, Zhang YH, Yin ZF, Wang M, Ling C. 2014. The roles of traditional Chinese medicine in gene therapy. J Integr Med 12:67-75. http://dx.doi.org/10.1016/S2095-4964(14)60019-4.
3. Mingozzi F, High KA. 2011. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet 12:341-355. http://dx.doi.org/10.1038/nrg2988.
4. 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.
5. 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.
6. Qing K, Wang XS, Kube DM, Ponnazhagan S, Bajpai A, Srivastava A. 1997. Role of tyrosine phosphorylation of a cellular protein in adenoassociated virus 2-mediated transgene expression. Proc Natl Acad Sci USA 94:10879-10884. http://dx.doi.org/10.1073/pnas.94.20.10879.
7. Zhong L, Chen L, Li Y, Qing K, Weigel-Kelley KA, Chan RJ, Yoder MC, Srivastava A. 2004. Self-complementary adeno-associated virus 2 (AAV)-T cell protein tyrosine phosphatase vectors as helper viruses to improve transduction efficiency of conventional single-stranded AAV vectors in vitro and in vivo. Mol Ther 10:950-957. http://dx.doi.org/10.1016/j.ymthe.2004.07.018.
8. 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.
9. Wang Z, Ma HI, Li J, Sun L, Zhang J, Xiao X. 2003. Rapid and highly efficient transduction by double-stranded adeno-associated virus vectors in vitro and in vivo. Gene Ther 10:2105-2111. http://dx.doi.org/10.1038/sj.gt.3302133.
10. McCarty DM, Fu H, Monahan PE, Toulson CE, Naik P, Samulski RJ. 2003. Adeno-associated virus terminal repeat (TR) mutant generates self-complementary vectors to overcome the rate-limiting step to transduction in vivo. Gene Ther 10:2112-2118. http://dx.doi.org/10.1038/sj.gt.3302134.
11. Nathwani AC, Tuddenham EG, Rangarajan S, Rosales C, McIntosh J, Linch DC, Chowdary P, Riddell A, Pie AJ, Harrington C, O'Beirne J, Smith K, Pasi J, Glader B, Rustagi P, Ng CY, Kay MA, Zhou J, Spence Y, Morton CL, Allay J, Coleman J, Sleep S, Cunningham JM, Srivastava D, Basner-Tschakarjan E, Mingozzi F, High KA, Gray JT, Reiss UM, Nienhuis AW, Davidoff AM. 2011. Adenovirus-associated virus vectormediated gene transfer in hemophilia B. N Engl J Med 365:2357-2365. http://dx.doi.org/10.1056/NEJMoa1108046.
12. Wu J, Zhao W, Zhong L, Han Z, Li B, Ma W, Weigel-Kelley KA, Warrington KH, Srivastava A. 2007. Self-complementary recombinant adeno-associated viral vectors: packaging capacity and the role of rep proteins in vector purity. Hum Gene Ther 18:171-182. http://dx.doi.org/10.1089/hum.2006.088.
13. Qing K, Hansen J, Weigel-Kelley KA, Tan M, Zhou S, Srivastava A. 2001. Adeno-associated virus type 2-mediated gene transfer: role of cellular FKBP52 protein in transgene expression. J Virol 75:8968-8976. http://dx.doi.org/10.1128/JVI.75.19.8968-8976.2001.
14. Qing K, Li W, Zhong L, Tan M, Hansen J, Weigel-Kelley KA, Chen L, Yoder MC, Srivastava A. 2003. Adeno-associated virus type 2-mediated gene transfer: role of cellular T-cell protein tyrosine phosphatase in transgene expression in established cell lines in vitro and transgenic mice in vivo. J Virol 77:2741-2746. http://dx.doi.org/10.1128/JVI.77.4.2741-2746.2003.
15. Jayandharan GR, Zhong L, Sack BK, Rivers AE, Li M, Li B, Herzog RW, Srivastava A. 2010. Optimized adeno-associated virus (AAV)-protein phosphatase-5 helper viruses for efficient liver transduction by singlestranded AAV vectors: therapeutic expression of factor IX at reduced vector doses. Hum Gene Ther 21:271-283. http://dx.doi.org/10.1089/hum.2009.100.
16. Zhao W, Wu J, Zhong L, Srivastava A. 2007. Adeno-associated virus 2-mediated gene transfer: role of a cellular serine/threonine protein phosphatase in augmenting transduction efficiency. Gene Ther 14:545-550. http://dx.doi.org/10.1038/sj.gt.3302886.
17. Jayandharan GR, Aslanidi G, Martino AT, Jahn SC, Perrin GQ, Herzog RW, Srivastava A. 2011. Activation of the NF-kappaB pathway by adenoassociated virus (AAV) vectors and its implications in immune response and gene therapy. Proc Natl Acad Sci USA 108:3743-3748. http://dx.doi.org/10.1073/pnas.1012753108.
18. Wang XS, Ponnazhagan S, Srivastava A. 1995. Rescue and replication signals of the adeno-associated virus 2 genome. J Mol Biol 250:573-580. http://dx.doi.org/10.1006/jmbi.1995.0398.
19. Wang XS, Ponnazhagan S, Srivastava A. 1996. Rescue and replication of adeno-associated virus type 2 as well as vector DNA sequences from recombinant plasmids containing deletions in the viral inverted terminal repeats: selective encapsidation of viral genomes in progeny virions. J Virol 70:1668-1677.
20. Wang XS, Qing K, Ponnazhagan S, Srivastava A. 1997. Adenoassociated virus type 2DNAreplication in vivo: mutation analyses of theD sequence in viral inverted terminal repeats. J Virol 71:3077-3082.
21. Ling C, Lu Y, Kalsi JK, Jayandharan GR, Li B, Ma W, Cheng B, Gee SW, McGoogan KE, Govindasamy L, Zhong L, Agbandje-McKenna M, Srivastava A. 2010. Human hepatocyte growth factor receptor is a cellular coreceptor for adeno-associated virus serotype 3. Hum Gene Ther 21: 1741-1747. http://dx.doi.org/10.1089/hum.2010.075.
22. Hirt B. 1967. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol 26:365-369. http://dx.doi.org/10.1016/0022-2836(67)90307-5.
23. Wang LN, Wang Y, Lu Y, Yin ZF, Zhang YH, Aslanidi GV, Srivastava A, Ling CQ, Ling C. 2014. Pristimerin enhances recombinant adenoassociated virus vector-mediated transgene expression in human cell lines in vitro and murine hepatocytes in vivo. J Integr Med 12:20-34. http://dx.doi.org/10.1016/S2095-4964(14)60003-0.
24. Liu Y, Joo KI, Wang P. 2013. Endocytic processing of adeno-associated virus type 8 vectors for transduction of target cells. Gene Ther 20:308-317. http://dx.doi.org/10.1038/gt.2012.41.
25. Ling C, Lu Y, Cheng B, McGoogan KE, Gee SW, Ma W, Li B, Aslanidi GV, Srivastava A. 2011. High-efficiency transduction of liver cancer cells by recombinant adeno-associated virus serotype 3 vectors. J Vis Exp http://dx.doi.org/10.3791/2538.
26. Dai Y, Bae K, Siemann DW. 2011. Impact of hypoxia on the metastatic potential of human prostate cancer cells. Int J Radiat Oncol Biol Phys 81:521-528. http://dx.doi.org/10.1016/j.ijrobp.2011.04.027.
27. Gu Y, Lin S, Li JL, Nakagawa H, Chen Z, Jin B, Tian L, Ucar DA, Shen H, Lu J, Hochwald SN, Kaye FJ, Wu L. 2012. Altered LKB1/CREBregulated transcription co-activator (CRTC) signaling axis promotes esophageal cancer cell migration and invasion. Oncogene 31:469-479. http://dx.doi.org/10.1038/onc.2011.247.
28. Dong B, Nakai H, Xiao W. 2010. Characterization of genome integrity for oversized recombinant AAV vector. Mol Ther 18:87-92. http://dx.doi.org/10.1038/mt.2009.258.
29. Wu Z, Yang H, Colosi P. 2010. Effect of genome size on AAV vector packaging. Mol Ther 18:80-86. http://dx.doi.org/10.1038/mt.2009.255.
30. Lai Y, Yue Y, Duan D. 2010. Evidence for the failure of adeno-associated virus serotype 5 to package a viral genome > or = 8.2 kb. Mol Ther 18:75-79. http://dx.doi.org/10.1038/mt.2009.256.
31. Samulski RJ, Srivastava A, Berns KI, Muzyczka N. 1983. Rescue of adeno-associated virus from recombinant plasmids: gene correction within the terminal repeats of AAV. Cell 33:135-143. http://dx.doi.org/10.1016/0092-8674(83)90342-2.
32. Zhou X, Zeng X, Fan Z, Li C, McCown T, Samulski RJ, Xiao X. 2008. Adeno-associated virus of a single-polarity DNA genome is capable of transduction in vivo. Mol Ther 16:494-499. http://dx.doi.org/10.1038/sj.mt.6300397.
33. Zhong L, Zhou X, Li Y, Qing K, Xiao X, Samulski RJ, Srivastava A. 2008. Single-polarity recombinant adeno-associated virus 2 vectormediated transgene expression in vitro and in vivo: mechanism of transduction. Mol Ther 16:290-295. http://dx.doi.org/10.1038/sj.mt.6300376.
34. Papadakis ED, Nicklin SA, Baker AH, White SJ. 2004. Promoters and control elements: designing expression cassettes for gene therapy. Curr Gene Ther 4:89-113. http://dx.doi.org/10.2174/1566523044578077.
35. Qing K, Khuntirat B, Mah C, Kube DM, Wang XS, Ponnazhagan S, Zhou S, Dwarki VJ, Yoder MC, Srivastava A. 1998. Adeno-associated virus type 2-mediated gene transfer: correlation of tyrosine phosphorylation of the cellular single-stranded D sequence-binding protein with transgene expression in human cells in vitro and murine tissues in vivo. J Virol 72:1593-1599.
36. Mah C, Qing K, Khuntirat B, Ponnazhagan S, Wang XS, Kube DM, Yoder MC, Srivastava A. 1998. Adeno-associated virus type 2-mediated gene transfer: role of epidermal growth factor receptor protein tyrosine kinase in transgene expression. J Virol 72:9835-9843.
37. Heinemeyer T, Wingender E, Reuter I, Hermjakob H, Kel AE, Kel OV, Ignatieva EV, Ananko EA, Podkolodnaya OA, Kolpakov FA, Podkolodny NL, Kolchanov NA. 1998. Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Res 26:362-367. http://dx.doi.org/10.1093/nar/26.1.362.
38. Marinescu VD, Kohane IS, Riva A. 2005. MAPPER: a search engine for the computational identification of putative transcription factor binding sites in multiple genomes. BMC Bioinformatics 6:79. http://dx.doi.org/10.1186/1471-2105-6-79.
39. 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.
40. Aslanidi GV, Rivers AE, Ortiz L, Govindasamy L, Ling C, Jayandharan GR, Zolotukhin S, Agbandje-McKenna M, Srivastava A. 2012. Highefficiency transduction of human monocyte-derived dendritic cells by capsid-modified recombinant AAV2 vectors. Vaccine 30:3908-3917. http://dx.doi.org/10.1016/j.vaccine.2012.03.079.
41. Aslanidi GV, Rivers AE, Ortiz L, Song L, Ling C, Govindasamy L, Van Vliet K, Tan M, Agbandje-McKenna M, Srivastava A. 2013. Optimization of the capsid of recombinant adeno-associated virus 2 (AAV2) vectors: the final threshold? PLoS One 8:e59142. http://dx.doi.org/10.1371/journal.pone.0059142.