Rationally designed capsid and transgene cassette of AAV6 vectors for dendritic cell-based cancer immunotherapy

Immunology and Cell Biology

Volumn 92, Issue 2, 2014, Pages 116-123

  Pandya, Jheel ^a   Ortiz, Luis ^a   Ling, Chen ^a   Rivers, Angela E ^a   Aslanidi, George ^a  

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

Author keywords

Adeno associated virus vectors; CD11c promoter; Dendritic cells; Gene expression serine threonine phosphorylation

Indexed keywords

ADENOCARCINOMA; DENDRITIC CELL; DEPENDOPARVOVIRUS; GENE VECTOR; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOTHERAPY; MALE; PROCEDURES; PROSTATIC NEOPLASMS; TRANSGENE; TUMOR CELL LINE; VIRUS CAPSID;

ADENOCARCINOMA; CAPSID; CELL LINE, TUMOR; DENDRITIC CELLS; DEPENDOVIRUS; GENETIC VECTORS; HUMANS; IMMUNOTHERAPY; MALE; PROSTATIC NEOPLASMS; TRANSGENES;

EID: 84893847671     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2013.74     Document Type: Article

References (49)

1. Hoos A, Britten CM, Huber C, O?Donnell-Tormey J. A methodological framework to enhance the clinical success of cancer immunotherapy. Nat Biotechnol 2011; 29: 867-870.
2. Palucka K, Ueno H, Banchereau J. Recent developments in cancer vaccines. J Immunol 2011; 186: 1325-1331.
3. Tacken PJ, de Vries IJM, Torensma R, Figdor CG. Dendritic-cell immunotherapy: from ex vivo loading to in vivo targeting. Nat Rev Immunol 2007; 7: 790-802. (Pubitemid 47480309)
4. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245-252. (Pubitemid 28155090)
5. Figdor CG, de Vries IJ, Lesterhuis WJ, Melief CJ. Dendritic cell immunotherapy: mapping the way. Nat Med 2004; 10: 475-480. (Pubitemid 38667904)
6. Schlom J, Gulley JL, Arlen PM. Role of vaccine therapy in cancer: biology and practice. Curr Oncol 2007; 14: 238-245.
7. Ueno H, Schmitt N, Klechevsky E, Pedroza-Gonzalez A, Matsui T, Zurawski G et al. Harnessing human dendritic cell subsets for medicine. Immunol Rev 2010; 234: 199-212.
8. Ueno H, Klechevsky E, Schmitt N, Ni L, Flamar A-L, Zurawski S et al. Targeting human dendritic cell subsets for improved vaccines. Semin Immunol 2011; 23: 21-27.
9. Humbert JM, Halary F. Viral and non-viral methods to genetically modify dendritic cells. Curr Gene Ther 2012; 12: 127-136.
10. Asokan A, Schaffer DV, Samulski RJ. The AAV vector toolkit: poised at the clinical crossroads. Mol Ther 2012; 20: 699-708.
11. Daya S, Berns KI. Gene therapy using adeno-associated virus vectors. Clin Microbiol Rev 2008; 21: 583-593.
12. High KA, Aubourg P. rAAV human trial experience. Methods Mol Biol 2011; 807: 429-457.
13. Srivastava A. Adeno-associated virus-mediated gene transfer. J Cell Biochem 2008; 105: 17-24.
14. Zhong L, Li B, Jayandharan G, Mah CS, Govindasamy L, Agbandje-McKenna M et al. Tyrosine-phosphorylation of AAV2 vectors and its consequences on viral intracellular trafficking and transgene expression. Virology 2008; 381: 194-202.
15. Aslanidi GV, Rivers AE, Ortiz L, Govindasamy L, Ling C, Jayandharan GR et al. Highefficiency transduction of human monocyte-derived dendritic cells by capsid-modified recombinant AAV2 vectors. Vaccine 2012; 30: 3908-3917.
16. Markusic DM, Herzog RW, Aslanidi GV, Hoffman BE, Li B, Li M et al. High-efficiency transduction and correction of murine hemophilia B using AAV2 vectors devoid of multiple surface-exposed tyrosines. Mol Ther 2010; 18: 2048-2056.
17. Petrs-Silva H, Dinculescu A, Li Q, Min S-H, Chiodo V, Pang J-J et al. High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol Ther 2009; 1: 463-471.
18. Zhong L, Li B, Mah CS, Govindasamy L, Agbandje-McKenna M, Cooper M et al. 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 2008; 105: 7827-7832. (Pubitemid 351872723)
19. Cheng B, Ling C, Dai Y, Lu Y, Glushakova LG, Gee SW et al. Development of optimized AAV3 serotype vectors: mechanism of high-efficiency transduction of human liver cancer cells. Gene Therapy 2012; 19: 375-384.
20. Papadakis ED, Nicklin SA, Baker AH, White SJ. Promoters and control elements: designing expression cassettes for gene therapy. Curr Gene Ther 2004; 4: 89-113. (Pubitemid 38854948)
21. McCarty DM, Fu H, Monahan PE, Toulson CE, Naik P, Samulski RJ. Adeno-associated virus terminal repeat (TR) mutant generates self-complementary vectors to overcome the rate-limiting step to transduction in vivo. Gene Therapy 2003; 10: 2112-2118. (Pubitemid 37536760)
22. Edelmann SL, Nelson PJ, Brocker T. Comparative promoter analysis in vivo: identification of a dendritic cell-specific promoter module. Blood 2011; 118: 40-49.
23. Ni J, Nolte B, Arnold A, Fournier P, Schirrmacher V. Targeting anti-tumor DNA vaccines to dendritic cells via a short CD11c promoter sequence. Vaccine 2009; 27: 5480-5487.
24. Aslanidi GV, Rivers AE, Ortiz L, Song L, Ling C, Govindasamy L et al. Optimization of the capsid of recombinant adeno-associated virus 2 (AAV2) vectors: the final threshold? PLoS One 2013; 8: e59142.
25. Ponnazhagan S, Mahendra G, Curiel DT, Shaw DR. Adeno-associated virus type 2- mediated transduction of human monocyte-derived dendritic cells: implications for ex vivo immunotherapy. J Virol 2001; 75: 9493-9501. (Pubitemid 32851951)
26. Shin O, Kim SJ, Lee WI, Kim JY, Lee H. Effective transduction by self-complementary adeno-associated viruses of human dendritic cells with no alteration of their natural characteristics. J Gene Med 2008; 10: 762-769. (Pubitemid 352003919)
27. Ussher JE, Taylor JA. Optimized transduction of human monocyte-derived dendritic cells by recombinant adeno-associated virus serotype 6. Hum Gene Ther 2010; 21: 1675-1686.
28. Veron P, Allo V, Riviere C, Bernard J, Douar A-M, Masurier C. Major subsets of human dendritic cells are efficiently transduced by self-complementary adeno-associated virus vectors 1 and 2. J Virol 2007; 81: 5385-5394. (Pubitemid 46744447)
29. Eisold S, Schmidt J, Ryschich E, Gock M, Klar E, von Knebel Doeberitz M et al. Induction of an antitumoral immune response by wild-type adeno-associated virus type 2 in an in vivo model of pancreatic carcinoma. Pancreas 2007; 35: 63-72. (Pubitemid 46956203)
30. Mahadevan M, Liu Y, You C, Luo R, You H, Mehta JL et al. Generation of robust cytotoxic T lymphocytes against prostate specific antigen by transduction of dendritic cells using protein and recombinant adeno-associated virus. Cancer Immunol Immunother 2007; 56: 1615-1624. (Pubitemid 47094391)
31. Yu Y, Pilgrim P, Zhou W, Gagliano N, Frezza EE, Jenkins M et al. rAAV/Her-2/neu loading of dendritic cells for a potent cellular-mediated MHC class I restricted immune response against ovarian cancer. Viral Immunol 2008; 21: 435-442.
32. Li C, Diprimio N, Bowles DE, Hirsch ML, Monahan PE, Asokan A et al. Single amino acid modification of adeno-associated virus capsid changes transduction and humoral immune profiles. J Virol 2012; 86: 7752-7759.
33. Muzyczka N, Warrington KH. Custom adeno-associated virus capsids: the next generation of recombinant vectors with novel tropism. Hum Gene Ther 2005; 16: 408-416. (Pubitemid 40647138)
34. Wu P, Xiao W, Conlon T, Hughes J, Agbandje-McKenna M, Ferkol T et al. Mutational analysis of the adeno-associated virus type 2 (AAV2) capsid gene and construction of AAV2 vectors with altered tropism. J Virol 2000; 74: 8635-8647. (Pubitemid 30666714)
35. Wu Z, Asokan A, Grieger JC, Govindasamy L, Agbandje-McKenna M, Samulski RJ. Single amino acid changes can influence titer, heparin binding, and tissue tropism in different adeno-associated virus serotypes. J Virol 2006; 80: 11393-11397. (Pubitemid 44706580)
36. Kay CN, Ryals RC, Aslanidi GV, Min SH, Ruan Q, Sun J et al. Targeting photoreceptors via intravitreal delivery using novel, capsid-mutated AAV vectors. PLoS One 2013; 8: e62097.
37. Aldrich WA, Ren C, White AF, Zhou SZ, Kumar S, Jenkins CB et al. Enhanced transduction of mouse bone marrow-derived dendritic cells by repetitive infection with self-complementary adeno-associated virus 6 combined with immunostimulatory ligands. Gene Therapy 2006; 13: 29-39. (Pubitemid 41823849)
38. Ng R, Govindasamy L, Gurda BL, McKenna R, Kozyreva OG, Samulski RJ et al. Structural characterization of the dual glycan binding adeno-associated virus serotype 6. J Virol 2010; 84: 12945-12957.
39. Xie Q, Lerch TF, Meyer NL, Chapman MS. Structure-function analysis of receptorbinding in adeno-associated virus serotype 6 (AAV-6). Virology 2011; 420: 10-19.
40. Song L, Kauss MA, Kopin E, Chandra M, Ul-Hasan T, Miller E et al. Optimizing the transduction efficiency of capsid-modified AAV6 serotype vectors in primary human hematopoietic stem cells in vitro and in a xenograft mouse model in vivo. Cytotherapy 2013; 15: 986-998.
41. Song L, Li X, Jayandharan GR, Wang Y, Aslanidi GV, Ling C et al. High-efficiency transduction of primary human hematopoietic stem cells and erythroid lineagerestricted expression by optimized AAV6 serotype vectors in vitro and in a murine xenograft model in vivo. PLoS One 2013; 8: e58757.
42. Castiello L, Sabatino M, Jin P, Clayberger C, Marincola FM, Krensky AM et al. Monocyte-derived DC maturation strategies and related pathways: a transcriptional view. Cancer Immunol Immunother 2011; 60: 457-466.
43. Wang Z, Ma HI, Li J, Sun L, Zhang J, Xiao X. Rapid and highly efficient transduction by double-stranded adeno-associated virus vectors in vitro and in vivo. Gene Therapy 2003; 10: 2105-2111. (Pubitemid 37536759)
44. Gray JT, Zolotukhin S. Design and construction of functional AAV vectors. Methods Mol Biol 2011; 807: 25-46.
45. Bharadwaj AS, Agrawal DK. Transcription factors in the control of dendritic cell life cycle. Immunol Res 2007; 37: 79-96. (Pubitemid 46742285)
46. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science 2010; 327: 656-661.
47. Zolotukhin S, Potter M, Zolotukhin I, Sakai Y, Loiler S, Fraites TJ et al. Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 2002; 28: 158-167. (Pubitemid 35341079)
48. Wang Y, Ling C, Song L, Wang L, Aslanidi GV, Tan M et al. Limitations of encapsidation of recombinant self-complementary adeno-associated viral genomes in different serotype capsids and their quantitation. Hum Gene Ther Methods 2012; 23: 225-233.
49. Mattis AE, Bernhardt G, Lipp M, Forster R. Analyzing cytotoxic T lymphocyte activity: a simple and reliable flow cytometry-based assay. J Immunol Methods 1997; 204: 135-142. (Pubitemid 27262007)