Activation of peroxisome proliferator-activated receptor γ prolongs islet allograft survival

Cell Transplantation

Volumn 21, Issue 10, 2012, Pages 2111-2118

  Wang, Hongjun ^a,b   Wu, Hongju ^c   Rocuts, Fredy ^b   Gu, Zhuoying ^b   Bach, Fritz H ^b   Otterbein, Leo E ^b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Allograft survival; Carbon monoxide; Islet transplantation; Peroxisome proliferator activated receptor (PPAR )

Indexed keywords

15 DEOXY DELTA12,14 PROSTAGLANDIN J2; 2 CHLORO 5 NITROBENZANILIDE; CARBON MONOXIDE; CYTOKINE; GLUCOSE; INDUCIBLE NITRIC OXIDE SYNTHASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TROGLITAZONE; TUMOR NECROSIS FACTOR ALPHA;

ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; GRAFT RECIPIENT; GRAFT REJECTION; GRAFT SURVIVAL; MOUSE; NONHUMAN; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOZOCIN DIABETES; UPREGULATION;

ANIMALS; APOPTOSIS; CARBON MONOXIDE; GRAFT SURVIVAL; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NITRIC OXIDE SYNTHASE TYPE II; PPAR GAMMA; SURVIVAL ANALYSIS; TRANSPLANTATION, HOMOLOGOUS; TREATMENT OUTCOME; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

MUS;

EID: 84870473480     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368911X637399     Document Type: Article

References (51)

1. Anderson, C. C.; Matzinger, P. Danger: 1. The view from the bottom of the cliff. Semin. Immunol. 12(3):231-238; 2000.
2. Auboeuf, D.; Rieusset, J.; Fajas, L.; Vallier, P.; Frering, V.; Riou, J. P.; Staels, B.; Auwerx, J.; Laville, M.; Vidal, H. Tissue distribution and quantification of the expression of mRNAs of peroxisome proliferator-activated receptors and liver X receptor alpha in humans: No alteration in adipose tissue of obese and NIDDM patients. Diabetes 46(8):1319-1327; 1997.
3. Bilban, M.; Bach, F. H.; Otterbein, S. L.; Ifedigbo, E.; d'Avila, J. C.; Esterbauer, H.; Chin, B. Y.; Usheva, A.; Robson, S. C.; Wagner, O.; Otterbein, L. E. Carbon monoxide orchestrates a protective response through PPARgamma. Immunity 24 (5):601-610; 2006.
4. Caito, S.; Yang, S. R.; Kode, A.; Edirisinghe, I.; Rajendrasozhan, S.; Phipps, R. P.; Rahman, I. Rosiglitazone and 15-deoxy-Delta12,14-prostaglandin J2, PPARgamma agonists, differentially regulate cigarette smoke-mediated pro-inflammatory cytokine release in monocytes/macrophages. Antioxid. Redox. Signal. 10(2):253-260; 2008.
5. Camp, H. S.; Li, O.; Wise, S. C.; Hong, Y. H.; Frankowski, C. L.; Shen, X.; Vanbogelen, R.; Leff, T. Differential activation of peroxisome proliferator-activated receptor gamma by troglitazone and rosiglitazone. Diabetes 49(4):539-547; 2000.
6. Campbell, I. W.; Mariz, S. Beta-cell preservation with thiazolidinediones. Diabetes Res. Clin. Pract. 76(2):163-176; 2007.
7. Cechin, S. R.; Perez-Alvarez, I.; Fenjves, E.; Molano, R. D.; Pileggi, A.; Berggren, P. O.; Ricordi, C.; Pastori, R. L. Antiinflammatory properties of exenatide in human pancreatic islets. Cell Transplant. 21(4):633-648; 2012.
8. Chung, S. W.; Kang, B. Y.; Kim, S. H.; Pak, Y. K.; Cho, D.; Trinchieri, G.; Kim, T. S. Oxidized low density lipoprotein inhibits interleukin-12 production in lipopolysaccharide-activated mouse macrophages via direct interactions between peroxisome proliferator-activated receptor gamma and nuclear factor-kappa B. J. Biol. Chem. 275(42):32681-32687; 2000.
9. Davalli, A. M.; Scaglia, L.; Zangen, D. H.; Hollister, J.; Bonner-Weir, S.; Weir, G. C. Vulnerability of islets in the immediate posttransplantation period. Dynamic changes in structure and function. Diabetes 45(9):1161-1167; 1996.
10. Dixon, J.; DeLegge, M.; Morgan, K. A.; Adams, D. B. Impact of total pancreatectomy with islet cell transplant on chronic pancreatitis management at a disease-based center. Am. Surg. 74(8):735-738; 2008.
11. Dubois, M.; Pattou, F.; Kerr-Conte, J.; Gmyr, V.; Vandewalle, B.; Desreumaux, P.; Auwerx, J.; Schoonjans, K.; Lefebvre, J. Expression of peroxisome proliferator-activated receptor gamma (PPARgamma) in normal human pancreatic islet cells. Diabetologia 43(9):1165-1169; 2000.
12. Egerod, F. L.; Svendsen, J. E.; Hinley, J.; Southgate, J.; Bartels, A.; Brunner, N.; Oleksiewicz, M. B. PPARalpha and PPARgamma coactivation rapidly induces Egr-1 in the nuclei of the dorsal and ventral urinary bladder and kidney pelvis urothelium of rats. Toxicol. Pathol. 37(7):947-958; 2009.
13. Ek, J.; Urhammer, S. A.; Sorensen, T. I.; Andersen, T.; Auwerx, J.; Pedersen, O. Homozygosity of the Pro12Ala variant of the peroxisome proliferation-activated receptor gamma2 (PPARgamma2): Divergent modulating effects on body mass index in obese and lean Caucasian men. Diabetologia 42(7):892-895; 1999.
14. Escher, P.; Braissant, O.; Basu-Modak, S.; Michalik, L.; Wahli, W.; Desvergne, B. Rat PPARs: Quantitative analysis in adult rat tissues and regulation in fasting and refeeding. Endocrinology 142(10):4195-4202; 2001.
15. Fahmi, H.; Di Battista, J. A.; Pelletier, J. P.; Mineau, F.; Ranger, P.; Martel-Pelletier, J. Peroxisome proliferators activated receptor gamma activators inhibit interleukin-1beta-induced nitric oxide and matrix metalloproteinase 13 production in human chondrocytes. Arthritis Rheum. 44(3):595-607; 2001.
16. Fajas, L.; Fruchart, J. C.; Auwerx, J. PPARgamma3 mRNA: A distinct PPARgamma mRNA subtype transcribed from an independent promoter. FEBS Lett. 438(1/2):55-60; 1998.
17. Fan, W.; Yanase, T.; Morinaga, H.; Mu, Y. M.; Nomura, M.; Okabe, T.; Goto, K.; Harada, N.; Nawata, H. Activation of peroxisome proliferator-activated receptor gamma and retinoid X receptor inhibits aromatase transcription via nuclear factor-kappa B. Endocrinology 146(1):85-92; 2005.
18. Fogli, S.; Pellegrini, S.; Adinolfi, B.; Mariotti, V.; Melissari, E.; Betti, L.; Fabbrini, L.; Giannaccini, G.; Lucacchini, A.; Bardelli, C.; Stefanelli, F.; Brunelleschi, S.; Breschi, M. C. Rosiglitazone reverses salbutamol-induced beta(2)-adrenoceptor tolerance in airway smooth muscle. Br. J. Pharmacol. 162(2):378-391.
19. Forman, B. M.; Tontonoz, P.; Chen, J.; Brun, R. P.; Spiegelman, B. M.; Evans, R. M. 15-Deoxy-delta 12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPARgamma. Cell 83(5):803-812; 1995.
20. Foss, D. L.; Zilliox, M. J.; Meier, W.; Zuckermann, F.; Murtaugh, M. P. Adjuvant danger signals increase the immune response to porcine reproductive and respiratory syndrome virus. Viral. Immunol. 15(4):557-566; 2002.
21. Gardner, O. S.; Shiau, C. W.; Chen, C. S.; Graves, L. M. Peroxisome proliferator-activated receptor gamma-independent activation of p38 MAPK by thiazolidinediones involves calcium/calmodulin-dependent protein kinase II and protein kinase R: Correlation with endoplasmic reticulum stress. J. Biol. Chem. 280(11):10109-10118; 2005.
22. Goldberg, A.; Parolini, M.; Chin, B. Y.; Czismadia, E.; Otterbein, L. E.; Bach, F. H.; Wang, H. Toll-like receptor 4 suppression leads to islet allograft survival. FASEB J. 21(11):2840-2848; 2007.
23. Gunther, L.; Berberat, P. O.; Haga, M.; Brouard, S.; Smith, R. N.; Soares, M. P.; Bach, F. H.; Tobiasch, E. Carbon monoxide protects pancreatic beta-cells from apoptosis and improves islet function/survival after transplantation. Diabetes 51(4):994-999; 2002.
24. Halabi, C. M.; Beyer, A. M.; de Lange, W. J.; Keen, H. L.; Baumbach, G. L.; Faraci, F. M.; Sigmund, C. D. Interference with PPARgamma function in smooth muscle causes vascular dysfunction and hypertension. Cell Metab. 7(3):215-226; 2008.
25. Honda, T.; Kaikita, K.; Tsujita, K.; Hayasaki, T.; Matsukawa, M.; Fuchigami, S.; Sugiyama, S.; Sakashita, N.; Ogawa, H.; Takeya, M. Pioglitazone, a peroxisome proliferator-activated receptor gamma agonist, attenuates myocardial ischemia-reperfusion injury in mice with metabolic disorders. J. Mol. Cell. Cardiol. 44(5):915-926; 2008.
26. Hsieh, W. C.; Lan, B. S.; Chen, Y. L.; Chang, Y.; Chuang, H. C.; Su, I. J. Efficacy of peroxisome proliferator activated receptor agonist in the treatment of virus-associated haemophagocytic syndrome in a rabbit model. Antivir. Ther. 15(1):71-81.
27. Ihle, N. T.; Lemos, R.; Schwartz, D.; Oh, J.; Halter, R. J.; Wipf, P.; Kirkpatrick, L.; Powis, G. Peroxisome proliferatoractivated receptor gamma agonist pioglitazone prevents the hyperglycemia caused by phosphatidylinositol 3-kinase pathway inhibition by PX-866 without affecting antitumor activity. Mol. Cancer Ther. 8(1):94-100; 2009.
28. Klopper, J. P.; Sharma, V.; Berenz, A.; Hays, W. R.; Loi, M.; Pugazhenthi, U.; Said, S.; Haugen, B. R. Retinoid and thiazolidinedione therapies in melanoma: An analysis of differential response based on nuclear hormone receptor expression. Mol. Cancer 8:16; 2009.
29. Lehrke, M.; Lazar, M. A. The many faces of PPARgamma. Cell 123(6):993-999; 2005.
30. Loviscach, M.; Rehman, N.; Carter, L.; Mudaliar, S.; Mohadeen, P.; Ciaraldi, T. P.; Veerkamp, J. H.; Henry, R. R. Distribution of peroxisome proliferator-activated receptors (PPARs) in human skeletal muscle and adipose tissue: Relation to insulin action. Diabetologia 43(3):304-311; 2000.
31. Maggi, L. B., Jr.; Sadeghi, H.; Weigand, C.; Scarim, A. L.; Heitmeier, M. R.; Corbett, J. A. Anti-inflammatory actions of 15-deoxy-delta 12,14-prostaglandin J2 and troglitazone: Evidence for heat shock-dependent and -independent inhibition of cytokine-induced inducible nitric oxide synthase expression. Diabetes 49(3):346-355; 2000.
32. Matzinger, P. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12:991-1045; 1994.
33. Melzi, R.; Mercalli, A.; Sordi, V.; Cantarelli, E.; Nano, R.; Maffi, P.; Sitia, G.; Guidotti, L. G.; Secchi, A.; Bonifacio, E.; Piemonti, L. Role of CCL2/MCP-1 in islet transplantation. Cell Transplant. 19(8):1031-1046; 2010.
34. Miles, P. D.; Barak, Y.; He, W.; Evans, R. M.; Olefsky, J. M. Improved insulin-sensitivity in mice heterozygous for PPARgamma deficiency. J. Clin. Invest. 105(3):287-292; 2000.
35. Miller, D. M.; Rossini, A. A.; Greiner, D. L. Role of innate immunity in transplantation tolerance. Crit. Rev. Immunol. 28(5):403-439; 2008.
36. Nosjean, O.; Boutin, J. A. Natural ligands of PPARgamma: Are prostaglandin J(2) derivatives really playing the part? Cell. Signal. 14(7):573-583; 2002.
37. Ogawa, J.; Takahashi, S.; Fujiwara, T.; Fukushige, J.; Hosokawa, T.; Izumi, T.; Kurakata, S.; Horikoshi, H. Troglitazone can prevent development of type 1 diabetes induced by multiple low-dose streptozotocin in mice. Life Sci. 65(12):1287-1296; 1999.
38. Picard, F.; Auwerx, J. PPAR(gamma) and glucose homeostasis. Annu. Rev. Nutr. 22:167-197; 2002.
39. Pirmohamed, M.; Naisbitt, D. J.; Gordon, F.; Park, B. K. The danger hypothesis-potential role in idiosyncratic drug reactions. Toxicology 181-182:55-63; 2002.
40. Ramirez, S. H.; Heilman, D.; Morsey, B.; Potula, R.; Haorah, J.; Persidsky, Y. Activation of peroxisome proliferatoractivated receptor gamma (PPARgamma) suppresses Rho GTPases in human brain microvascular endothelial cells and inhibits adhesion and transendothelial migration of HIV-1 infected monocytes. J. Immunol. 180(3):1854-1865; 2008.
41. Reilly, C. M.; Oates, J. C.; Sudian, J.; Crosby, M. B.; Halushka, P. V.; Gilkeson, G. S. Prostaglandin J(2) inhibition of mesangial cell iNOS expression. Clin. Immunol. 98(3):337-345; 2001.
42. Ryan, E. A.; Paty, B. W.; Senior, P. A.; Bigam, D.; Alfadhli, E.; Kneteman, N. M.; Lakey, J. R.; Shapiro, A. M. Fiveyear follow-up after clinical islet transplantation. Diabetes 54(7):2060-2069; 2005.
43. Schmidt, S.; Moric, E.; Schmidt, M.; Sastre, M.; Feinstein, D. L.; Heneka, M. T. Anti-inflammatory and antiproliferative actions of PPARgamma agonists on T lymphocytes derived from MS patients. J. Leukoc. Biol. 75(3):478-485; 2004.
44. 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.
45. Spears, M.; Donnelly, I.; Jolly, L.; Brannigan, M.; Ito, K.; McSharry, C.; Lafferty, J.; Chaudhuri, R.; Braganza, G.; Bareille, P.; Sweeney, L.; Adcock, I. M.; Barnes, P. J.; Wood, S.; Thomson, N. C. Bronchodilatory effect of the PPARgamma agonist rosiglitazone in smokers with asthma. Clin. Pharmacol. Ther. 86(1):49-53; 2009.
46. Truong, W.; Shapiro, A. M. The TIM family of cosignaling receptors: Emerging targets for the regulation of autoimmune disease and transplantation tolerance. Cell Transplant. 16(10):977-986; 2008.
47. Uchimura, K.; Nakamuta, M.; Enjoji, M.; Irie, T.; Sugimoto, R.; Muta, T.; Iwamoto, H.; Nawata, H. Activation of retinoic X receptor and peroxisome proliferator-activated receptor gamma inhibits nitric oxide and tumor necrosis factor-alpha production in rat Kupffer cells. Hepatology 33(1):91-99; 2001.
48. Vandewalle, B.; Moerman, E.; Lefebvre, B.; Defrance, F.; Gmyr, V.; Lukowiak, B.; Kerr Conte, J.; Pattou, F. PPARgamma-dependent and -independent effects of rosiglitazone on lipotoxic human pancreatic islets. Biochem. Biophys. Res. Commun. 366(4):1096-1101; 2008.
49. Wang, H.; Lee, S. S.; Gao, W.; Czismadia, E.; McDaid, J.; Ollinger, R.; Soares, M. P.; Yamashita, K.; Bach, F. H. Donor treatment with carbon monoxide can yield islet allograft survival and tolerance. Diabetes 54(5):1400-1406; 2005.
50. Wolffenbuttel, B. H.; Graal, M. B. New treatments for patients with type 2 diabetes mellitus. Postgrad. Med. J. 72(853):657-662; 1996.
51. Zhang, H. L.; Xu, M.; Wei, C.; Qin, A. P.; Liu, C. F.; Hong, L. Z.; Zhao, X. Y.; Liu, J.; Qin, Z. H. Neuroprotective effects of pioglitazone in a rat model of permanent focal cerebral ischemia are associated with peroxisome proliferator-activated receptor gamma-mediated suppression of nuclear factor-kappa B signaling pathway. Neuroscience 176: 381-395; 2011.