Identification of adeno-associated viral vectors suitable for intestinal gene delivery and modulation of experimental colitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 302, Issue 3, 2012, Pages

  Polyak, Steven ^a,b   Mach, Annette ^b   Porvasnik, Stacy ^b   Dixon, Lisa ^b   Conlon, Thomas ^b,c   Erger, Kirsten E ^b,c   Acosta, Andres ^b   Wright, Amy J ^b   Campbell Thompson, Martha ^b   Zolotukhin, Irene ^b   Wasserfall, Clive ^b   Mah, Cathryn ^b,c  

^a UNIVERSITY OF IOWA   (United States)

^b Immunology and Laboratory Medicine   (United States)

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

Author keywords

Colon; GFP; IL 10; Small intestine

Indexed keywords

INTERLEUKIN 10; PARVOVIRUS VECTOR; PIROXICAM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CLINICAL EFFECTIVENESS; CLINICAL EVALUATION; COLITIS; CONTROLLED STUDY; GENE IDENTIFICATION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT RESPONSE; VIRAL GENE DELIVERY SYSTEM;

ADENOVIRIDAE; ANIMALS; COLON; ENTEROCOLITIS; GENE DOSAGE; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GENOME, VIRAL; GREEN FLUORESCENT PROTEINS; INFLAMMATION; INTERLEUKIN-10; INTESTINE, SMALL; INTESTINES; LIVER; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; STOMACH; TRANSGENES; VIRAL TROPISM;

EID: 84856206687     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00562.2010     Document Type: Article

References (52)

1. Berg DJ, Davidson N, Kuhn R, Muller W, Menon S, Holland G, Thompson-Snipes L, Leach MW, Rennick D. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4() TH1-like responses. J Clin Invest 98: 1010-1020, 1996.
2. Berg DJ, Zhang J, Weinstock JV, Ismail HF, Earle KA, Alila H, Pamukcu R, Moore S, Lynch RG. Rapid development of colitis in NSAID-treated IL-10-deficient mice. Gastroenterology 123: 1527-1542, 2002.
3. Bhavsar MD, Amiji MM. Oral IL-10 gene delivery in a microspherebased formulation for local transfection and therapeutic efficacy in inflammatory bowel disease. Gene Ther 15: 1200-1209, 2008.
4. Bish LT, Morine K, Sleeper MM, Sanmiguel J, Wu D, Gao G, Wilson JM, Sweeney HL. Adeno-associated virus (AAV) serotype 9 provides global cardiac gene transfer superior to AAV1, AAV6, AAV7, and AAV8 in the mouse and rat. Hum Gene Ther 19: 1359-1368, 2008.
5. Cearley CN, Wolfe JH. Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol Ther 13: 528-537, 2006.
6. Chidlow JH Jr, Glawe JD, Pattillo CB, Pardue S, Zhang S, Kevil CG. VEGF164 isoform specific regulation of T-cell-dependent experimental colitis in mice. Inflamm Bowel Dis 17: 1501-1512, 2011.
7. Chidlow JH Jr, Shukla D, Grisham MB, Kevil CG. Pathogenic angiogenesis in IBD and experimental colitis: new ideas and therapeutic avenues. Am J Physiol Gastrointest Liver Physiol 293: G5-G18, 2007.
8. Cryan SA, O'Driscoll CM. Mechanistic studies on nonviral gene delivery to the intestine using in vitro differentiated cell culture models and an in vivo rat intestinal loop. Pharm Res 20: 569-575, 2003.
9. Daya S, Berns KI. Gene therapy using adeno-associated virus vectors. Clin Microbiol Rev 21: 583-593, 2008.
10. Duan D, Yue Y, Yan Z, McCray PB Jr, Engelhardt JF. Polarity influences the efficiency of recombinant adenoassociated virus infection in differentiated airway epithelia. Hum Gene Ther 9: 2761-2776, 1998.
11. Farlow SJ, Jerusalmi A, Sano T. Enhanced transduction of colonic cell lines in vitro and the inflamed colon in mice by viral vectors, derived from adeno-associated virus serotype 2, using virus-microbead conjugates bearing lectin. BMC Biotechnol 7: 83, 2007.
12. Fasano A, Shea-Donohue T. Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat Clin Pract Gastroenterol Hepatol 2: 416-422, 2005.
13. Gao G, Lu Y, Calcedo R, Grant RL, Bell P, Wang L, Figueredo J, Lock M, Wilson JM. Biology of AAV serotype vectors in liver-directed gene transfer to nonhuman primates. Mol Ther 13: 77-87, 2006.
14. Gao G, Vandenberghe LH, Alvira MR, Lu Y, Calcedo R, Zhou X, Wilson JM. Clades of Adeno-associated viruses are widely disseminated in human tissues. J Virol 78: 6381-6388, 2004.
15. Gao GP, Alvira MR, Wang L, Calcedo R, Johnston J, Wilson JM. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci USA 99: 11854-11859, 2002.
16. Goudy K, Song S, Wasserfall C, Zhang YC, Kapturczak M, Muir A, Powers M, Scott-Jorgensen M, Campbell-Thompson M, Crawford JM, Ellis TM, Flotte TR, Atkinson MA. Adeno-associated virus vectormediated IL-10 gene delivery prevents type 1 diabetes in NOD mice. Proc Natl Acad Sci USA 98: 13913-13918, 2001.
17. Goudy KS, Burkhardt BR, Wasserfall C, Song S, Campbell-Thompson ML, Brusko T, Powers MA, Clare-Salzler MJ, Sobel ES, Ellis TM, Flotte TR, Atkinson MA. Systemic overexpression of IL-10 induces CD4 CD25 cell populations in vivo and ameliorates type 1 diabetes in nonobese diabetic mice in a dose-dependent fashion. J Immunol 171: 2270-2278, 2003.
18. Han Z, Zhong L, Maina N, Hu Z, Li X, Chouthai NS, Bischof D, Weigel-Van Aken KA, Slayton WB, Yoder MC, Srivastava A. Stable integration of recombinant adeno-associated virus vector genomes after transduction of murine hematopoietic stem cells. Hum Gene Ther 19: 267-278, 2008.
19. Hasbrouck NC, High KA. AAV-mediated gene transfer for the treatment of hemophilia B: problems and prospects. Gene Ther 15: 870-875, 2008.
20. Hu CH, Busuttil RW, Lipshutz GS. RH10 provides superior transgene expression in mice when compared with natural AAV serotypes for neonatal gene therapy. J Gene Med 12: 766-778, 2010.
21. Iborra M, Bernuzzi F, Invernizzi P, Danese S. MicroRNAs in autoimmunity and inflammatory bowel disease: crucial regulators in immune response. Autoimmun Rev. In Press. doi:10.1016/j.autrev.2010.07.002.
22. Kesisoglou F, Schmiedlin-Ren P, Fleisher D, Zimmermann EM. Adenoviral transduction of enterocytes and M-cells using in vitro models based on Caco-2 cells: the coxsackievirus and adenovirus receptor (CAR) mediates both apical and basolateral transduction. Mol Pharm 7: 619-629, 2010.
23. Klein RL, Dayton RD, Tatom JB, Henderson KM, Henning PP. AAV8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purification method. Mol Ther 16: 89-96, 2008.
24. Kucharzik T, Maaser C, Lugering A, Kagnoff M, Mayer L, Targan S, Domschke W. Recent understanding of IBD pathogenesis: implications for future therapies. Inflamm Bowel Dis 12: 1068-1083, 2006.
25. Lebherz C, Maguire A, Tang W, Bennett J, Wilson JM. Novel AAV serotypes for improved ocular gene transfer. J Gene Med 10: 375-382, 2008.
26. Lindsay JO, Ciesielski CJ, Scheinin T, Brennan FM, Hodgson HJ. Local delivery of adenoviral vectors encoding murine interleukin 10 induces colonic interleukin 10 production and is therapeutic for murine colitis. Gut 52: 363-369, 2003.
27. Liqun Wang R, McLaughlin T, Cossette T, Tang Q, Foust K, Camp-bell-Thompson M, Martino A, Cruz P, Loiler S, Mueller C, Flotte TR. Recombinant AAV serotype and capsid mutant comparison for pulmonary gene transfer of alpha-1-antitrypsin using invasive and noninvasive delivery. Mol Ther 17: 81-87, 2009.
28. Loiler SA, Conlon TJ, Song S, Tang Q, Warrington KH, Agarwal A, Kapturczak M, Li C, Ricordi C, Atkinson MA, Muzyczka N, Flotte TR. Targeting recombinant adeno-associated virus vectors to enhance gene transfer to pancreatic islets and liver. Gene Ther 10: 1551-1558, 2003.
29. 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 Ther 10: 2112-2118, 2003.
30. McCarty DM, Monahan PE, Samulski RJ. Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther 8: 1248-1254, 2001.
31. Mori S, Takeuchi T, Enomoto Y, Kondo K, Sato K, Ono F, Sata T, Kanda T. Tissue distribution of cynomolgus adeno-associated viruses AAV10, AAV11, and AAVcy.7 in naturally infected monkeys. Arch Virol 153: 375-380, 2008.
32. Mueller C, Braag SA, Martino AT, Tang Q, Campbell-Thompson M, Flotte TR. The pros and cons of immunomodulatory IL-10 gene therapy with recombinant AAV in a Cftr /-dependent allergy mouse model. Gene Ther 16: 172-183, 2009.
33. Murthy SN, Cooper HS, Shim H, Shah RS, Ibrahim SA, Sedergran DJ. Treatment of dextran sulfate sodium-induced murine colitis by intracolonic cyclosporin. Dig Dis Sci 38: 1722-1734, 1993.
34. Pacak CA, Conlon T, Mah CS, Byrne BJ. Relative persistence of AAV serotype 1 vector genomes in dystrophic muscle. Genet Vaccines Ther 6: 14, 2008.
35. Pavlick KP, Ostanin DV, Furr KL, Laroux FS, Brown CM, Gray L, Kevil CG, Grisham MB. Role of T-cell-associated lymphocyte functionassociated antigen-1 in the pathogenesis of experimental colitis. Int Immunol 18: 389-398, 2006.
36. Polyak S, Mah C, Porvasnik S, Herlihy JD, Campbell-Thompson M, Byrne BJ, Valentine JF. Gene delivery to intestinal epithelial cells in vitro and in vivo with recombinant adeno-associated virus types 1, 2 and 5. Dig Dis Sci 53: 1261-1270, 2008.
37. Porvasnik SL, Mah C, Polyak S. Targeting murine small bowel and colon through selective superior mesenteric artery injection. Microsurgery 30: 487-493, 2010.
38. Sandberg JW, Lau C, Jacomino M, Finegold M, Henning SJ. Improving access to intestinal stem cells as a step toward intestinal gene transfer. Hum Gene Ther 5: 323-329, 1994.
39. Sarkar R, Mucci M, Addya S, Tetreault R, Bellinger DA, Nichols TC, Kazazian HH Jr. Long-term efficacy of adeno-associated virus serotypes 8 and 9 in hemophilia a dogs and mice. Hum Gene Ther 17: 427-439, 2006.
40. Sasaki M, Mathis JM, Jennings MH, Jordan P, Wang Y, Ando T, Joh T, Alexander JS. Reversal of experimental colitis disease activity in mice following administration of an adenoviral IL-10 vector. J Inflamm (Lond) 2: 13, 2005.
41. Sferra TJ, McNeely D, Johnson PR. Gene transfer to the intestinal tract: a new approach using selective injection of the superior mesenteric artery. Hum Gene Ther 8: 681-687, 1997.
42. Shao G, Greathouse K, Huang Q, Wang CM, Sferra TJ. Gene transfer to the gastrointestinal tract after peroral administration of recombinant adeno-associated virus type 2 vectors. J Pediatr Gastroenterol Nutr 43: 168-179, 2006.
43. Sugimoto K, Ogawa A, Mizoguchi E, Shimomura Y, Andoh A, Bhan AK, Blumberg RS, Xavier RJ, Mizoguchi A. IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J Clin Invest 118: 534-544, 2008.
44. Vallance BA, Gunawan MI, Hewlett B, Bercik P, Van Kampen C, Galeazzi F, Sime PJ, Gauldie J, Collins SM. TGF- 1 gene transfer to the mouse colon leads to intestinal fibrosis. Am J Physiol Gastrointest Liver Physiol 289: G116-G128, 2005.
45. Vandenberghe LH, Wilson JM, Gao G. Tailoring the AAV vector capsid for gene therapy. Gene Ther 16: 311-319, 2009.
46. Vandenbroucke K, Hans W, Van Huysse J, Neirynck S, Demetter P, Remaut E, Rottiers P, Steidler L. Active delivery of trefoil factors by genetically modified Lactococcus lactis prevents and heals acute colitis in mice. Gastroenterology 127: 502-513, 2004.
47. Wilson DS, Dalmasso G, Wang L, Sitaraman SV, Merlin D, Murthy N. Orally delivered thioketal nanoparticles loaded with TNF-alpha-siRNA target inflammation and inhibit gene expression in the intestines. Nat Mater 9: 923-928, 2010.
48. Wirtz S, Becker C, Blumberg R, Galle PR, Neurath MF. Treatment of T cell-dependent experimental colitis in SCID mice by local administration of an adenovirus expressing IL-18 antisense mRNA. J Immunol 168: 411-420, 2002.
49. Yiu WH, Lee YM, Peng WT, Pan CJ, Mead PA, Mansfield BC, Chou JY. Complete normalization of hepatic G6PC deficiency in murine glycogen storage disease type Ia using gene therapy. Mol Ther 18: 1076-1084, 2010.
50. Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 16: 1073-1080, 2008.
51. Zolotukhin S, Potter M, Zolotukhin I, Sakai Y, Loiler S, Fraites TJ Jr, Chiodo VA, Phillipsberg T, Muzyczka N, Hauswirth WW, Flotte TR, Byrne BJ, Snyder RO. Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 28: 158-167, 2002.
52. Zuo L, Huang Z, Dong L, Xu L, Zhu Y, Zeng K, Zhang C, Chen J, Zhang J. Targeting delivery of anti-TNFalpha oligonucleotide into activated colonic macrophages protects against experimental colitis. Gut 59: 470-479, 2010.