Gene transfer of active Akt1 by an infectivity-enhanced adenovirus impacts β-cell survival and proliferation differentially in vitro and in vivo

Islets

Volumn 4, Issue 6, 2012, Pages 366-378

  Bone, Robert N ^a   Icyuz, Mert ^b   Zhang, Yanqing ^c   Zhang, Yuan ^b   Cui, Wanxing ^d   Wang, Hongjun ^e   Peng, Ji Bin ^b   Matthews, Qiana L ^b   Siegal, Gene P ^a   Wu, Hongju ^c  

^a University of Alabama at Birmingham   (United States)

^b and Clinical Center   (United States)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d University of Alabama at Birmingham   (United States)

^e MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

cell proliferation; Adenovirus; Akt1; Diabetes; Islets.

Indexed keywords

ADENOVIRUS VECTOR; PROTEIN KINASE B;

ADENOVIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL ISOLATION; CELL PROLIFERATION; CELL REGENERATION; CELL SURVIVAL; CONTROLLED STUDY; GENE TARGETING; GENE TRANSFER; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; STREPTOZOCIN DIABETES; VIRAL GENE DELIVERY SYSTEM; VIRUS INFECTIVITY;

Β-CELL PROLIFERATION; ADENOVIRUS; AKT1; DIABETES; ISLETS;

ADENOVIRIDAE; ANIMALS; CELL GROWTH PROCESSES; CELL SURVIVAL; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; IMMUNOHISTOCHEMISTRY; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84876253516     PISSN: 19382014     EISSN: 19382022     Source Type: Journal    
DOI: 10.4161/isl.22721     Document Type: Article

References (37)

1. Aikin R, Rosenberg L, Maysinger D. Phosphatidylinositol 3-kinase signaling to Akt mediates survival in isolated canine islets of Langerhans. Biochem Biophys Res Commun 2000; 277:455-61; PMID:11032744; http://dx.doi.org/ 10.1006/bbrc.2000.3664
2. Bos JL. A target for phosphoinositide 3-kinase: Akt/PKB. Trends Biochem Sci 1995; 20:441-2; PMID:8578585; http://dx.doi.org/10.1016/S0968-0004(00)89097- 0
3. Brazil DP, Yang ZZ, Hemmings BA. Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci 2004; 29:233-42; PMID:15130559; http://dx.doi.org/10.1016/j.tibs.2004.03.006
4. Hanada M, Feng J, Hemmings BA. Structure, regulation and function of PKB/AKT-A major therapeutic target. Biochim Biophys Acta 2004; 1697:3-16
5. Tuttle RL, Gill NS, Pugh W, Lee JP, Koeberlein B, Furth EE, et al. Regulation of pancreatic beta-cell growth and survival by the serine/threonine protein kinase Akt1/PKBalpha. Nat Med 2001; 7:1133-7; PMID:11590437; http://dx.doi.org/10.1038/nm1001-1133
6. Icyuz M, Bryant SM, Fortinberry HK, Molakandov K, Siegal GP, Contreras JL, et al. Adenovirus infection activates akt1 and induces cell proliferation in pancreatic islets1. Transplantation 2009; 87:821-4; PMID:19300183; http://dx.doi.org/10.1097/TP.0b013e318199c686
7. Bernal-Mizrachi E, Wen W, Stahlhut S, Welling CM, Permutt MA. Islet beta cell expression of constitutively active Akt1/PKB alpha induces striking hypertrophy, hyperplasia, and hyperinsulinemia. J Clin Invest 2001; 108:1631-8; PMID:11733558
8. Garofalo RS, Orena SJ, Rafidi K, Torchia AJ, Stock JL, Hildebrandt AL, et al. Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB beta. J Clin Invest 2003; 112:197-208; PMID:12843127
9. Contreras JL, Smyth CA, Bilbao G, Young CJ, Thompson JA, Eckhoff DE. Simvastatin induces activation of the serine-Threonine protein kinase AKT and increases survival of isolated human pancreatic islets. Transplantation 2002; 74:1063-9; PMID:12438947; http://dx.doi.org/10.1097/00007890-200210270-00001.
10. Maeda H, Rajesh KG, Maeda H, Suzuki R, Sasaguri S. Epidermal growth factor and insulin inhibit cell death in pancreatic beta cells by activation of PI3-kinase/AKT signaling pathway under oxidative stress. Transplant Proc 2004; 36:1163-5; PMID:15194403; http://dx.doi.org/10.1016/j.transproceed.2004.04.018
11. Srinivasan S, Bernal-Mizrachi E, Ohsugi M, Permutt MA. Glucose promotes pancreatic islet beta-cell survival through a PI 3-kinase/Akt-signaling pathway. Am J Physiol Endocrinol Metab 2002; 283:E784-93; PMID:12217896
12. Rao P, Roccisana J, Takane KK, Bottino R, Zhao A, Trucco M, et al. Gene transfer of constitutively active Akt markedly improves human islet transplant outcomes in diabetic severe combined immunodeficient mice. Diabetes 2005; 54:1664-75; PMID:15919787; http://dx.doi.org/10.2337/diabetes.54.6.1664.
13. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, Cohen P, et al. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 1996; 15:6541-51; PMID:8978681
14. Kohn AD, Takeuchi F, Roth RA. Akt, a pleckstrin homology domain containing kinase, is activated primarily by phosphorylation. J Biol Chem 1996; 271:21920-6; PMID:8702995; http://dx.doi.org/10.1074/jbc.271.36.2192015
15. Scheid MP, Woodgett Jr. Unravelling the activation mechanisms of protein kinase B/Akt. FEBS Lett 2003; 546:108-12; PMID:12829245; http://dx.doi.org/10. 1016/S0014-5793(03)00562-3
16. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005; 307:1098-101; PMID:15718470; http://dx.doi.org/10.1126/science.1106148
17. Contreras JL, Bilbao G, Smyth CA, Jiang XL, Eckhoff DE, Jenkins SM, et al. Cytoprotection of pancreatic islets before and soon after transplantation by gene transfer of the anti-Apoptotic Bcl-2 gene. Transplantation 2001; 71:1015-23; PMID:11374395; http://dx.doi.org/10.1097/00007890-200104270-00001
18. Garcia-Ocana A, Takane KK, Reddy VT, Lopez-Talavera JC, Vasavada RC, Stewart AF. Adenovirus-mediated hepatocyte growth factor expression in mouse islets improves pancreatic islet transplant performance and reduces beta cell death. J Biol Chem 2003; 278:343-51; PMID:12403787; http://dx.doi.org/10.1074/ jbc.M207848200
19. Kapturczak MH, Flotte T, Atkinson MA. Adeno-Associated virus (AAV) as a vehicle for therapeutic gene delivery: improvements in vector design and viral production enhance potential to prolong graft survival in pancreatic islet cell transplantation for the reversal of type 1 diabetes. Curr Mol Med 2001; 1:245-58; PMID:11899074; http://dx.doi.org/10.2174/1566524013363979
20. Mendoza V, Klein D, Ichii H, Ribeiro MM, Ricordi C, Hankeln T, et al. Protection of islets in culture by delivery of oxygen binding neuroglobin via protein transduction. Transplant Proc 2005; 37:237-40; PMID:15808606; http://dx.doi.org/10.1016/j.transproceed.2004.12.270
21. Ribeiro MM, Klein D, Pileggi A, Molano RD, Fraker C, Ricordi C, et al. Heme oxygenase-1 fused to a TAT peptide transduces and protects pancreatic beta-cells. Biochem Biophys Res Commun 2003; 305:876-81; PMID:12767912; http://dx.doi.org/10.1016/S0006-291X(03)00856-8
22. Contreras JL, Wu H, Smyth CA, Eckstein CP, Young CJ, Seki T, et al. Double genetic modification of adenovirus fiber with RGD polylysine motifs significantly enhances gene transfer to isolated human pancreatic islets. Transplantation 2003; 76:252-61; PMID:12865820; http://dx.doi.org/10.1097/01.TP. 0000066361.02042.CA
23. Dmitriev I, Krasnykh V, Miller CR, Wang M, Kashentseva E, Mikheeva G, et al. An adenovirus vector with genetically modified fibers demonstrates expanded tropism via utilization of a coxsackievirus and adenovirus receptor-independent cell entry mechanism. J Virol 1998; 72:9706-13; PMID:9811704
24. Han T, Tang Y, Ugai H, Perry LE, Siegal GP, Contreras JL, et al. Genetic incorporation of the protein transduction domain of Tat into Ad5 fiber enhances gene transfer efficacy. Virol J 2007; 4:103; PMID:17958897; http://dx.doi.org/ 10.1186/1743-422X-4-103.
25. Wickham TJ, Roelvink PW, Brough DE, Kovesdi I. Adenovirus targeted to heparan-containing receptors increases its gene delivery efficiency to multiple cell types. Nat Biotechnol 1996; 14:1570-3; PMID:9634823; http://dx.doi.org/10. 1038/nbt1196-1570
26. Wu H, Seki T, Dmitriev I, Uil T, Kashentseva E, Han T, et al. Double modification of adenovirus fiber with RGD and polylysine motifs improves coxsackievirus-Adenovirus receptor-independent gene transfer efficiency. Hum Gene Ther 2002; 13:1647-53; PMID:12228019; http://dx.doi.org/10.1089/ 10430340260201734
27. Taniguchi H, Yamato E, Tashiro F, Ikegami H, Ogihara T, Miyazaki J. beta-cell neogenesis induced by adenovirus-mediated gene delivery of transcription factor pdx-1 into mouse pancreas. Gene Ther 2003; 10:15-23; PMID:12525833; http://dx.doi.org/10.1038/sj.gt.3301846
28. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 2004; 429:41-6; PMID:15129273; http://dx.doi.org/10.1038/nature02520
29. Zhang Y, Zhang Y, Bone RN, Cui W, Peng JB, Siegal GP, et al. Regeneration of pancreatic non-β endocrine cells in adult mice following a single diabetes-inducing dose of streptozotocin. PLoS One 2012; 7:e36675; PMID:22586489; http://dx.doi.org/10.1371/journal.pone.0036675
30. Jones RG, Parsons M, Bonnard M, Chan VS, Yeh WC, Woodgett JR, et al. Protein kinase B regulates T lymphocyte survival, nuclear factor kappaB activation, and Bcl-X(L) levels in vivo. J Exp Med 2000; 191:1721-34; PMID:10811865; http://dx.doi.org/10.1084/jem.191.10.1721
31. Majumder PK, Yeh JJ, George DJ, Febbo PG, Kum J, Xue Q, et al. Prostate intraepithelial neoplasia induced by prostate restricted Akt activation: the MPAKT model. Proc Natl Acad Sci U S A 2003; 100:7841-6; PMID:12799464; http://dx.doi.org/10.1073/pnas.1232229100
32. Yang ZZ, Tschopp O, Baudry A, Dümmler B, Hynx D, Hemmings BA. Physiological functions of protein kinase B/Akt. Biochem Soc Trans 2004; 32:350-4; PMID:15046607; http://dx.doi.org/10.1042/BST0320350
33. Liu Q, White LR, Clark SA, Heffner DJ, Winston BW, Tibbles LA, et al. Akt/protein kinase B activation by adenovirus vectors contributes to NFkappaB-dependent CXCL10 expression. J Virol 2005; 79:14507-15; PMID:16282450; http://dx.doi.org/10.1128/JVI.79.23.14507-14515.2005
34. Miller-Jensen K, Janes KA, Wong YL, Griffith LG, Lauffenburger DA. Adenoviral vector saturates Akt pro-survival signaling and blocks insulin-mediated rescue of tumor necrosis-factor-induced apoptosis. J Cell Sci 2006; 119:3788-98; PMID:16940353; http://dx.doi.org/10.1242/jcs.03102
35. Muller D, Huang GC, Amiel S, Jones PM, Persaud SJ. Gene expression heterogeneity in human islet endocrine cells in vitro: the insulin signalling cascade. Diabetologia 2007; 50:1239-42; PMID:17440705; http://dx.doi.org/10. 1007/s00125-007-0671-7
36. Wu H, Dmitriev I, Kashentseva E, Seki T, Wang M, Curiel DT. Construction and characterization of adenovirus serotype 5 packaged by serotype 3 hexon. J Virol 2002; 76:12775-82; PMID:12438602; http://dx.doi.org/10.1128/JVI.76.24. 12775-12782.2002
37. Wu H, Curiel DT. Fiber-modified adenoviruses for targeted gene therapy. Methods Mol Biol 2008; 434:113-32; PMID:18470642