Low-dose rapamycin unmasks the protective potential of targeting intragraft NF-κB for islet transplants

Cell Transplantation

Volumn 22, Issue 12, 2013, Pages 2355-2366

  Zammit, Nathan W ^a   Tan, Bernice M ^a   Walters, Stacey N ^a   Liuwantara, David ^a   Villanueva, Jeanette E ^a   Malle, Elisabeth K ^a   Grey, Shane T ^a  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Inhibitor of B protein (I B ); Islet transplantation; Inflammation; Nuclear factor light chain enhancer of activated B cells (NF B); Rapamycin

Indexed keywords

ADENOVIRUS VECTOR; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CYCLOPHILIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLUCOSE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; RAPAMYCIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; GRAFT REJECTION; GRAFT SURVIVAL; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LOW DRUG DOSE; LYMPHOCYTE DIFFERENTIATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROARRAY ANALYSIS; MONONUCLEAR CELL; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOZOCIN DIABETES; SURVIVAL TIME; TH17 CELL; TRANSCRIPTION REGULATION; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; CELLS, CULTURED; CHEMOKINES; DIABETES MELLITUS, EXPERIMENTAL; DRUG SYNERGISM; GRAFT SURVIVAL; I-KAPPA B KINASE; IMMUNOSUPPRESSIVE AGENTS; INTERCELLULAR ADHESION MOLECULE-1; INTERLEUKIN-6; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NF-KAPPA B; SIROLIMUS; SWINE; TRANSPLANTATION, HOMOLOGOUS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84890361935     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X658737     Document Type: Article

References (37)

1. Abdelli, S.; Ansite, J.; Roduit, R.; Borsello, T.; Matsumoto, I.; Sawada, T.; Allaman-Pillet, N.; Henry, H.; Beckmann, J. S.; Hering, B. J.; Bonny, C. Intracellular stress signaling pathways activated during human islet preparation and following acute cytokine exposure. Diabetes 53(11):2815-2823; 2004.
2. Anderson, C. C.; Carroll, J. M.; Gallucci, S.; Ridge, J. P.; Cheever, A. W.; Matzinger, P. Testing time-, ignorance-, and danger-based models of tolerance. J. Immunol. 166(6): 3663-3671; 2001.
3. Baeuerle, P. A.; Baltimore, D. I3B: A specific inhibitor of the NF-tB transcription factor. Science 242(4878):540-546; 1988.
4. Battaglia, M.; Stabilini, A.; Draghici, E.; Gregori, S.; Mocchetti, C.; Bonifacio, E.; Roncarolo, M. G. Rapamycin and interleukin-10 treatment induces T-regulatory type 1 cells that mediate antigen-specific transplantation tolerance. Diabetes 55(1):40-49; 2006.
5. Bettelli, E.; Carrier, Y.; Gao, W.; Korn, T.; Strom, T. B.; Oukka, M.; Weiner, H. L.; Kuchroo, V. K. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T-cells. Nature 441(7090):235-238; 2006.
6. Biarnes, M.; Montolio, M.; Nacher, V.; Raurell, M.; Soler, J.; Montanya, E. J-Cell death and mass in syngeneically transplanted islets exposed to short-and long-term hyperglycemia. Diabetes 51(1):66-72; 2002.
7. Bottino, R.; Balamurugan, A. N.; Tse, H.; Thirunavukkarasu, C.; Ge, X.; Profozich, J.; Milton, M.; Ziegenfuss, A.; Trucco, M.; Piganelli, J. D. Response of human islets to isolation stress and the effect of antioxidant treatment. Diabetes 53(10):2559-2568; 2004.
8. Cardozo, A. K.; Heimberg, H.; Heremans, Y.; Leeman, R.; Kutlu, B.; Kruhoffer, M.; Orntoft, T.; Eizirik, D. L. A comprehensive analysis of cytokine-induced and nuclear factor-kappaB-dependent genes in primary rat pancreatic f-cells. J. Biol. Chem. 276(52):48879-48886; 2001.
9. Chervonsky, A. V.; Wang, Y.; Wong, F. S.; Visintin, I.; Flavell, R. A.; Janeway, Jr., C. A.; Matis, L. A. The role of Fas in autoimmune diabetes. Cell 89(1):17-24; 1997.
10. Cowley, M. J.; Weinberg, A.; Zammit, N.; Walters, S. N.; Hawthorne, W. J.; Loudovaris, T.; Thomas, H.; Kay, T.; Gunton, J. E.; Alexander, S. I.; Kaplan, W.; Chapman, J.; O'Connell, P. J.; Grey, S. T. Human islets express a marked pro-inflammatory molecular signature prior to transplantation. Cell Transplant. 21(9):2063-2078; 2012.
11. Eldor, R.; Yeffet, A.; Baum, K.; Doviner, V.; Amar, D.; Ben-Neriah, Y.; Christofori, G.; Peled, A.; Carel, J. C.; Boitard, C.; Klein, T.; Serup, P.; Eizirik, D. L.; Melloul, D. Conditional and specific NF-CB blockade protects pancreatic a-cells from diabetogenic agents. Proc. Natl. Acad. Sci. USA 103(13):5072-5077; 2006.
12. Ferran, C.; Stroka, D. M.; Badrichani, A. Z.; Cooper, J. T.; Wrighton, C. J.; Soares, M.; Grey, S. T.; Bach, F. H. A20 inhibits NF-iB activation in endothelial cells without sensitizing to tumor necrosis factor-mediated apoptosis. Blood 91(7):2249-2258; 1998.
13. Frigerio, S.; Junt, T.; Lu, B.; Gerard, C.; Zumsteg, U.; Hollander, G. A.; Piali, L. H-Cells are responsible for CXCR3-mediated T-cell infiltration in insulitis. Nat. Med. 8(12):1414-1420; 2002.
14. Giannoukakis, N.; Rudert, W. A.; Trucco, M.; Robbins, P. D. Protection of human islets from the effects of interleukin-1P by adenoviral gene transfer of an IbB repressor. J. Biol. Chem. 275(47):36509-36513; 2000.
15. Grey, S. T. Regulating inflammation: The ying and yang of NF-oB activation. Immunol. Cell Biol. 86(4):299-300; 2008.
16. Grey, S. T.; Arvelo, M. B.; Hasenkamp, W.; Bach, F. H.; Ferran, C. A20 inhibits cytokine-induced apoptosis and nuclear factor nB-dependent gene activation in islets. J. Exp. Med. 190(8):1135-1146; 1999.
17. Grey, S. T.; Arvelo, M. B.; Hasenkamp, W. M.; Bach, F. H.; Ferran, C. Adenovirus-mediated gene transfer of the anti-apoptotic protein A20 in rodent islets inhibits IL-1ainduced NO release. Transplant. Proc. 31(1-2):789; 1999.
18. Grey, S. T.; Longo, C.; Shukri, T.; Patel, V. I.; Csizmadia, E.; Daniel, S.; Arvelo, M. B.; Tchipashvili, V.; Ferran, C. Genetic engineering of a suboptimal islet graft with A20 preserves p-cell mass and function. J. Immunol. 170(12): 6250-6256; 2003.
19. Hartman, M. G.; Lu, D.; Kim, M. L.; Kociba, G. J.; Shukri, T.; Buteau, J.; Wang, X.; Frankel, W. L.; Guttridge, D.; Prentki, M.; Grey, S. T.; Ron, D.; Hai, T. Role for activating transcription factor 3 in stress-induced i-cell apoptosis. Mol. Cell. Biol. 24(13):5721-5732; 2004.
20. Karin, M.; Lin, A. NF-2B at the crossroads of life and death. Nat. Immunol. 3(3):221-227; 2002.
21. Kono, H.; Rock, K. L. How dying cells alert the immune system to danger. Nat. Rev. Immunol. 8(4):279-289; 2008.
22. Kutlu, B.; Darville, M. I.; Cardozo, A. K.; Eizirik, D. L. Molecular regulation of monocyte chemoattractant protein-1 expression in pancreatic 1-cells. Diabetes 52(2):348-355; 2003.
23. Liuwantara, D.; Elliot, M.; Smith, M. W.; Yam, A. O.; Walters, S. N.; Marino, E.; McShea, A.; Grey, S. T. Nuclear factor-fB regulates B-cell death: A critical role for A20 in--cell protection. Diabetes 55(9):2491-2501; 2006.
24. Livak, K. J.; Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta DeltaC(T)] method. Methods 25(4):402-408; 2001.
25. Miyazaki, J.; Araki, K.; Yamato, E.; Ikegami, H.; Asano, T.; Shibasaki, Y.; Oka, Y.; Yamamura, K. Establishment of a pancreatic p-cell line that retains glucose-inducible insulin secretion: Special reference to expression of glucose transporter isoforms. Endocrinology 127(1):126-132; 1990.
26. Montana, E.; Bonner-Weir, S.; Weir, G. C. 2-Cell mass and growth after syngeneic islet cell transplantation in normal and streptozocin diabetic C57BL/6 mice. J. Clin. Invest. 91(3):780-787; 1993.
27. Porras, D. L.; Wang, Y.; Zhou, P.; Molinero, L. L.; Alegre, M. L. Role of T-cell-specific nuclear factor-kappaB in islet allograft rejection. Transplantation 93(10):976-982; 2012.
28. Rehman, K. K.; Bertera, S.; Bottino, R.; Balamurugan, A. N.; Mai, J. C.; Mi, Z.; Trucco, M.; Robbins, P. D. Protection of islets by in situ peptide-mediated transduction of the IoB kinase inhibitor Nemo-binding domain peptide. J. Biol. Chem. 278(11):9862-9868; 2003.
29. Ricordi, C.; Strom, T. B. Clinical islet transplantation: Advances and immunological challenges. Nat. Rev. Immunol. 4(4):259-268; 2004.
30. Rink, J. S.; Chen, X.; Zhang, X.; Kaufman, D. B. Conditional and specific inhibition of NF-CB in mouse pancreatic p-cells prevents cytokine-induced deleterious effects and improves islet survival posttransplant. Surgery 151(2):330-339; 2012.
31. Shapiro, A. M.; Lakey, J. R.; Ryan, E. A.; Korbutt, G. S.; Toth, E.; Warnock, G. L.; Kneteman, N. M.; Rajotte, R. V. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N. Engl. J. Med. 343(4):230-238; 2000.
32. Sorli, C. H.; Zhang, H. J.; Armstrong, M. B.; Rajotte, R. V.; Maclouf, J.; Robertson, R. P. Basal expression of cyclooxygenase-2 and nuclear factor-interleukin-6 are dominant and coordinately regulated by interleukin-1 in the pancreatic islet. Proc. Natl. Acad. Sci. USA 95(4): 1788-1793; 1998.
33. Takahashi, T.; Matsumoto, S.; Matsushita, M.; Kamachi, H.; Tsuruga, Y.; Kasai, H.; Watanabe, M.; Ozaki, M.; Furukawa, H.; Umezawa, K.; Todo, S. Donor pretreatment with DHMEQ improves islet transplantation. J. Surg. Res. 163(1):e23-34; 2010.
34. Thomson, A. W.; Turnquist, H. R.; Raimondi, G. Immunoregulatory functions of mTOR inhibition. Nat. Rev. Immunol. 9(5):324-337; 2009.
35. Ueki, S.; Yamashita, K.; Aoyagi, T.; Haga, S.; Suzuki, T.; Itoh, T.; Taniguchi, M.; Shimamura, T.; Furukawa, H.; Ozaki, M.; Umezawa, K.; Todo, S. Control of allograft rejection by applying a novel nuclear factor-rB inhibitor, dehydroxymethylepoxyquinomicin. Transplantation 82(12):1720-1727; 2006.
36. Walters, S.; Webster, K. E.; Sutherland, A.; Gardam, S.; Groom, J.; Liuwantara, D.; Marino, E.; Thaxton, J.; Weinberg, A.; Mackay, F.; Brink, R.; Sprent, J.; Grey, S. T. Increased CD4+Foxp3+ T-cells in BAFF-transgenic mice suppress T-cell effector responses. J. Immunol. 182(2):793-801; 2009.
37. Wood, K. J.; Goto, R. Mechanisms of rejection: Current perspectives. Transplantation 93(1):1-10; 2012.