The effect of Nrf2 pathway activation on human pancreatic islet cells

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Masuda, Yuichi ^a   Vaziri, Nosratola D ^a   Li, Shiri ^a   Le, Aimee ^a   Hajighasemi Ossareh, Mohammad ^a   Robles, Lourdes ^a   Foster, Clarence E ^a   Stamos, Michael J ^a   Al Abodullah, Ismail ^b   Ricordi, Camillo ^c   Ichii, Hirohito Ichii ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF MIAMI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE; BARDOXOLONE 9,11 DIHYDROTRIFLUOROETHYLAMIDE; GAMMA INTERFERON; HEME OXYGENASE 1; HYDROGEN PEROXIDE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; CHEMOKINE; CYTOKINE; DH404 COMPOUND; NFE2L2 PROTEIN, HUMAN; OLEANOLIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CADAVER; CELL NUCLEUS; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIABETES MELLITUS; DRUG EFFECT; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PANCREAS ISLET TRANSPLANTATION; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RAT; ACTIVE TRANSPORT; ANALOGS AND DERIVATIVES; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; METABOLISM; PANCREAS ISLET; SIGNAL TRANSDUCTION; UPREGULATION;

MUS MUSCULUS;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEUS; CELL SURVIVAL; CHEMOKINES; CYTOKINES; HUMANS; ISLETS OF LANGERHANS; NF-E2-RELATED FACTOR 2; OLEANOLIC ACID; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84938326417     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131012     Document Type: Article

References (45)

1. Larsen CE, Alper CA. The genetics of HLA-associated disease. Curr Opin Immunol 2004; 16: 660-667. PMID: 15342014
2. Rabinovitch A, Suarez-Pinzon WL. Cytokines and their roles in pancreatic islet beta-cell destruction and insulin-dependent diabetes mellitus. Biochem Pharmacol. 1998; 55: 1139-1149. PMID: 9719467
3. Eizirik DL, Mandrup-Poulsen T. A choice of death - the signal-transduction of immune-mediated beta-cell apoptosis. Diabetologia. 2001; 44: 2115-2133. PMID: 11793013
4. Rabinovitch A, Suarez-Pinzon WL, Strynadka K, Lakey JR, Rajotte RV. Human pancreatic islet beta-cell destruction by cytokines involves oxygen free radicals and aldehyde production. J Clin Endocrinol Metab. 1996; 81: 3197-202. PMID: 8784069
5. Lenzen S, Drinkgern J, Tiedge M. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic Biol Med. 1996; 20: 463-6. PMID: 8720919
6. Eizirik DL, Pipeleers DG, Ling Z, Welsh N, Hellerström C, Andersson A. Major species differences between humans and rodents in the susceptibility to pancreatic beta-cell injury. Proc Natl Acad Sci U S A. 1994; 91: 9253-6. PMID: 7937750
7. Kobayashi M, Yamamoto M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal. 2005; 7: 385-94. PMID: 15706085
8. Giudice A, Montella M. Activation of the Nrf2-ARE signaling pathway: a promising strategy in cancer prevention. Bioessays. 2006; 28: 169-81. PMID: 16435293
9. Surh YJ, Kundu JK, Na HK. Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals. Planta Med. 2008; 74:1526-39. doi: 10.1055/s-0028-1088302 PMID: 18937164
10. Copple IM, Goldring CE, Kitteringham NR, Park BK. The Nrf2-Keap1 defence pathway: role in protection against drug-induced toxicity. Toxicology. 2008; 246: 24-33. PMID: 18083283
11. Li W, Kong AN. Molecular mechanisms of Nrf2-mediated antioxidant response. Mol Carcinog. 2009; 48: 91-104. doi: 10.1002/mc.20465 PMID: 18618599
12. Giudice A, Arra C, Turco MC. Review of molecular mechanisms involved in the activation of the Nrf2-ARE signaling pathway by chemopreventive agents. Methods Mol Biol. 2010; 647:37-74. doi: 10.1007/978-1-60761-738-9-3 PMID: 20694660
13. Kundu JK, Surh YJ. Nrf2-Keap1 signaling as a potential target for chemoprevention of inflammation-associated carcinogenesis. Pharm Res. 2010; 27: 999-1013. doi: 10.1007/s11095-010-0096-8 PMID: 20354764
14. Yagishita Y, Fukutomi T, Sugawara A, Kawamura H, Takahashi T, Pi J, et al. Nrf2 protects pancreatic β-cells from oxidative and nitrosative stress in diabetic model mice. Diabetes. 2014; 63: 605-18. doi: 10.2337/db13-0909 PMID: 24186865
15. Li W, Wu W, Song H, Wang F, Li H, Chen L, et al. Targeting Nrf2 by dihydro-CDDO-trifluoroethyl amide enhances autophagic clearance and viability of β-cells in a setting of oxidative stress. FEBS Lett. 2014; 588: 2115-24. doi: 10.1016/j.febslet.2014.04.046 PMID: 24815692
16. Li S, Vaziri ND, Masuda Y, Hajighasemi-Ossareh M, Robles L, Le A, et al. Pharmacological activation of Nrf2 pathway improves pancreatic islet isolation and transplantation. Cell Transplant. 2015 Jan 9. [Epub ahead of print]
17. Aminzadeh MA, Reisman SA, Vaziri ND, Khazaeli M, Yuan J, Meyer CJ. The synthetic triterpenoid RTA dh404 (CDDO-dhTFEA) restores Nrf2 activity and attenuates oxidative stress, inflammation, and fibrosis in rats with chronic kidney disease. Xenobiotica. 2014; 44: 570-8. doi: 10.3109/00498254.2013.852705 PMID: 24195589
18. Bouzakri K, Plomgaard P, Berney T, Donath MY, Pedersen BK, Halban PA. Bimodal effect on pancreatic β-cells of secretory products from normal or insulin-resistant human skeletal muscle. Diabetes. 2011; 60: 1111-21. doi: 10.2337/db10-1178 PMID: 21378173
19. Ichii H, Inverardi L, Pileggi A, Molano RD, Cabrera O, Caicedo A, et al. A novel method for the assessment of cellular composition and beta-cell viability in human islet preparations. Am J Transplant. 2005; 5: 1635-45. PMID: 15943621
20. Nishikawa T, Araki E. Impact of mitochondrial ROS production in the pathogenesis of diabetes mellitus and its complications. Antioxid Redox Signal. 2007; 9: 343-53. PMID: 17184177
21. Tang C, Han P, Oprescu AI, Lee SC, Gyulkhandanyan AV, Chan GN, et al. Evidence for a role of superoxide generation in glucose-induced beta-cell dysfunction in vivo. Diabetes. 2007; 56: 2722-31. PMID: 17682092
22. Acharya JD, Ghaskadbi SS. Islets and their antioxidant defense. Islets. 2010; 2: 225-35. doi: 10.4161/isl.2.4.12219 PMID: 21099317
23. Robertson RP. Oxidative stress and impaired insulin secretion in type 2 diabetes. Curr Opin Pharmacol. 2006; 6: 615-9. PMID: 17045527
24. Grankvist K. Alloxan-induced luminol luminescence as a tool for investigating mechanisms of radical-mediated diabetogenicity. Biochem J. 1981; 200: 685-90. PMID: 7342976
25. Grankvist K, Marklund S, Täljedal IB. Superoxide dismutase is a prophylactic against alloxan diabetes. Nature. 1981; 294: 158-60. PMID: 7300898
26. Grankvist K, Marklund SL, Täljedal IB. CuZn-superoxide dismutase, Mn-superoxide dismutase, catalase and glutathione peroxidase in pancreatic islets and other tissues in the mouse. Biochem J. 1981; 199: 393-8. PMID: 7041886
27. Azevedo-Martins AK, Lortz S, Lenzen S, Curi R, Eizirik DL, Tiedge M. Improvement of the mitochondrial antioxidant defense status prevents cytokine-induced nuclear factor-kappaB activation in insulin-producing cells. Diabetes. 2003; 52: 93-101. PMID: 12502498
28. Hotta M, Tashiro F, Ikegami H, Niwa H, Ogihara T, Yodoi J, et al. Pancreatic beta cell-specific expression of thioredoxin, an antioxidative and antiapoptotic protein, prevents autoimmune and streptozotocin-induced diabetes. J Exp Med. 1998; 188: 1445-51. PMID: 9782121
29. Vajkoczy P, Menger MD, Simpson E, Messmer K. Angiogenesis and vascularization of murine pancreatic islet isografts. Transplantation. 1995; 60: 123-7. PMID: 7542814
30. Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol. 2007; 47: 89-116. PMID: 16968214
31. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999; 13: 76-86. PMID: 9887101
32. Magesh S, Chen Y, Hu L. Small molecule modulators of Keap1-Nrf2-ARE pathway as potential preventive and therapeutic agents. Med Res Rev. 2012; 32: 687-726. doi: 10.1002/med.21257 PMID: 22549716
33. Wakabayashi N, Slocum SL, Skoko JJ, Shin S, Kensler TW. When NRF2 talks, who's listening? Antioxid Redox Signal. 2010; 13: 1649-63. doi: 10.1089/ars.2010.3216 PMID: 20367496
34. Wasserman WW, Fahl WE. Comprehensive analysis of proteins which interact with the antioxidant responsive element: correlation of ARE-BP-1 with the chemoprotective induction response. Arch Biochem Biophys. 1997; 344: 387-96. PMID: 9264553
35. So HS, Kim HJ, Lee JH, Lee JH, Park SY, Park C, et al. Flunarizine induces Nrf2-mediated transcriptional activation of heme oxygenase-1 in protection of auditory cells from cisplatin. Cell Death Differ. 2006; 13:1763-75. PMID: 16485034
36. Velmurugan GV, Sundaresan NR, Gupta MP, White C. Defective Nrf2-dependent redox signalling contributes to microvascular dysfunction in type 2 diabetes. Cardiovasc Res. 2013; 100: 143-50. doi: 10.1093/cvr/cvt125 PMID: 23715558
37. Zhang J, Chen L, Zheng J, Zeng T, Li H, Xiao H, et al. The protective effect of resveratrol on islet insulin secretion and morphology in mice on a high-fat diet. Diabetes Res Clin Pract. 2012; 97: 474-82. doi: 10.1016/j.diabres.2012.02.029 PMID: 22497970
38. Balogun E, Hoque M, Gong P, Killeen E, Green CJ, Foresti R, et al. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem J. 2003; 371: 887-95. PMID: 12570874
39. Abdel Aziz MT, El-Asmar MF, El Nadi EG, Wassef MA, Ahmed HH, Rashed LA, et al. The effect of curcumin on insulin release in rat-isolated pancreatic islets. Angiology. 2010; 61: 557-66. doi: 10.1177/0003319709356424 PMID: 20395228
40. Kanitkar M, Bhonde RR. Curcumin treatment enhances islet recovery by induction of heat shock response proteins, Hsp70 and heme oxygenase-1, during cryopreservation. Life Sci. 2008; 82: 182-9. PMID: 18093618
41. Balamurugan AN, Akhov L, Selvaraj G, Pugazhenthi S. Induction of antioxidant enzymes by curcumin and its analogues in human islets: implications in transplantation. Pancreas. 2009; 38: 454-60. doi: 10.1097/MPA.0b013e318196c3e7 PMID: 19188863
42. Li W, Wu W, Song H, Wang F, Li H, Chen L, et al. Targeting Nrf2 by dihydro-CDDO-trifluoroethyl amide enhances autophagic clearance and viability of β-cells in a setting of oxidative stress. FEBS Lett. 2014; 588: 2115-24. doi: 10.1016/j.febslet.2014.04.046 PMID: 24815692
43. Pileggi A, Molano RD, Berney T, Ichii H, San Jose S, Zahr E, et al. Prolonged allogeneic islet graft survival by protoporphyrins. Cell Transplant. 2005; 14: 85-96. PMID: 15881418
44. Li Y, Li G, Dong W, Chen J, Lu D, Tan J. Transplantation of rat islets transduced with human heme oxygenase-1 gene using adenovirus vector. Pancreas. 2006; 33: 280-6. PMID: 17003650
45. Wang H, Ferran C, Attanasio C, Calise F, Otterbein LE. Induction of protective genes leads to islet survival and function. J Transplant. 2011: 141898. doi: 10.1155/2011/141898