Modulation of the peroxiredoxin system by cytokines in insulin-producing RINm5F cells: Down-regulation of PRDX6 increases susceptibility of beta cells to oxidative stress

Molecular and Cellular Endocrinology

Volumn 374, Issue 1-2, 2013, Pages 56-64

  Paula, Flavia M M ^a   Ferreira, Sandra M ^a   Boschero, Antonio C ^a   Souza, Kleber L A ^a,b  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Diabetes; Gene expression regulation; Hydrogen peroxide; Proteolysis; PRX6; ROS

Indexed keywords

CALPAIN; CYTOKINE; GAMMA INTERFERON; HYDROGEN PEROXIDE; INTERLEUKIN 1BETA; INTERLEUKIN 4; MESSENGER RNA; PEROXIREDOXIN; PEROXIREDOXIN 1; PEROXIREDOXIN 3; PEROXIREDOXIN 6; PROTEASOME; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; GENE EXPRESSION REGULATION; INTRACELLULAR SIGNALING; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ANIMALS; CALPAIN; CELL LINE; GENE EXPRESSION REGULATION; INSULIN; INSULIN-SECRETING CELLS; INTERFERON-GAMMA; INTERLEUKIN-1BETA; INTERLEUKIN-4; MAP KINASE KINASE 4; OXIDATIVE STRESS; PEROXIREDOXIN VI; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; RATS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84878723903     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.04.009     Document Type: Article

References (29)

1. Budanova E.N., Bystrova M.F. Search for protein-protein interaction partners of peroxiredoxin 6 with the yeast two-hybrid system. Russ. J. Genet. 2008, 44:137-142.
2. Cardozo A.K., Berthou L., Kruhoffer M., Orntoft T., Nicolls M.R., Eizirik D.L. Gene microarray study corroborates proteomic findings in rodent islet cells. J. Proteome Res. 2003, 2:553-555.
3. Fatma N., Kubo E., Takamura Y., Ishihara K., Garcia C., Beebe D.C., Singh D.P. Loss of NF-kappaB control and repression of Prdx6 gene transcription by reactive oxygen species-driven SMAD3-mediated transforming growth factor beta signaling. J. Biol. Chem. 2009, 284:22758-22772.
4. Han Y., Weinman S., Boldogh I., Walker R.K., Brasier A.R. Tumor necrosis factor-alpha-inducible IkappaBalpha proteolysis mediated by cytosolic m-calpain. A mechanism parallel to the ubiquitin-proteasome pathway for nuclear factor-kappab activation. J. Biol. Chem. 1999, 274:787-794.
5. Han Y.H., Kim H.S., Kim J.M., Kim S.K., Yu D.Y., Moon E.Y. Inhibitory role of peroxiredoxin II (Prx II) on cellular senescence. FEBS Lett. 2005, 579:4897-4902.
6. Hastie C., Masters J.R., Moss S.E., Naaby-Hansen S. Interferon-gamma reduces cell surface expression of annexin 2 and suppresses the invasive capacity of prostate cancer cells. J. Biol. Chem. 2008, 283:12595-12603.
7. Jorns A., Gunther A., Hedrich H.J., Wedekind D., Tiedge M., Lenzen S. Immune cell infiltration, cytokine expression, and beta-cell apoptosis during the development of type 1 diabetes in the spontaneously diabetic LEW.1AR1/Ztm-iddm rat. Diabetes 2005, 54:2041-2052.
8. Kaminski A., Kaminski E.R., Morgan N.G. Pre-incubation with interleukin-4 mediates a direct protective effect against the loss of pancreatic beta-cell viability induced by proinflammatory cytokines. Clin. Exp. Immunol. 2007, 148:583-588.
9. Kaminski A., Welters H.J., Kaminski E.R., Morgan N.G. Human and rodent pancreatic beta-cells express IL-4 receptors and IL-4 protects against beta-cell apoptosis by activation of the PI3K and JAK/STAT pathways. Biosci. Rep. 2010, 30:169-175.
10. Kim S.Y., Kim T.J., Lee K.Y. A novel function of peroxiredoxin 1 (Prx-1) in apoptosis signal-regulating kinase 1 (ASK1)-mediated signaling pathway. FEBS Lett. 2008, 582:1913-1918.
11. Knoops B., Loumaye E., Van Der Eecken V. Evolution of the peroxiredoxins. Subcell. Biochem. 2007, 44:27-40.
12. Kwon G., Corbett J.A., Hauser S., Hill J.R., Turk J., McDaniel M.L. Evidence for involvement of the proteasome complex (26S) and NFkappaB in IL-1beta-induced nitric oxide and prostaglandin production by rat islets and RINm5F cells. Diabetes 1998, 47:583-591.
13. Lenzen S. Oxidative stress: the vulnerable beta-cell. Biochem. Soc. Trans. 2008, 36:343-347.
14. 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, 20:463-466.
15. Mehmeti I., Lortz S., Lenzen S. The H(2)O(2)-sensitive HyPer protein targeted to the endoplasmic reticulum as a mirror of the oxidizing thiol-disulfide milieu. Free Radic. Biol. Med. 2012, 53:1451-1458.
16. Moore F., Naamane N., Colli M.L., Bouckenooghe T., Ortis F., Gurzov E.N., Igoillo-Esteve M., Mathieu C., Bontempi G., Thykjaer T., et al. STAT1 is a master regulator of pancreatic {beta}-cell apoptosis and islet inflammation. J. Biol. Chem. 2011, 286:929-941.
17. Mukhopadhyay S.S., Leung K.S., Hicks M.J., Hastings P.J., Youssoufian H., Plon S.E. Defective mitochondrial peroxiredoxin-3 results in sensitivity to oxidative stress in Fanconi anemia. J. Cell Biol. 2006, 175:225-235.
18. Nozaki K., Das A., Ray S.K., Banik N.L. Calpain inhibition attenuates intracellular changes in muscle cells in response to extracellular inflammatory stimulation. Exp. Neurol. 2010, 225:430-435.
19. Ortis F., Naamane N., Flamez D., Ladriere L., Moore F., Cunha D.A., Colli M.L., Thykjaer T., Thorsen K., Orntoft T.F., et al. Cytokines interleukin-1beta and tumor necrosis factor-alpha regulate different transcriptional and alternative splicing networks in primary beta-cells. Diabetes 2010, 59:358-374.
20. Paula F.M., Barbosa H.C., Carneiro E.M., Persaud S.J., Gagliardino J.J., Boschero A.C., Souza K.L. Requirement of NF-kappaB signalling pathway for modulation of the cholinergic muscarinic M3 receptor expression by INGAP-PP in insulin-producing cells. Eur. J. Pharmacol. 2010, 642:37-46.
21. Peshenko I.V., Shichi H. Oxidation of active center cysteine of bovine 1-Cys peroxiredoxin to the cysteine sulfenic acid form by peroxide and peroxynitrite. Free Radic. Biol. Med. 2001, 31:292-303.
22. Pirot P., Cardozo A.K., Eizirik D.L. Mediators and mechanisms of pancreatic beta-cell death in type 1 diabetes. Arq. Bras Endocrinol. Metabol. 2008, 52:156-165.
23. Roumes H., Pires-Alves A., Gonthier-Maurin L., Dargelos E., Cottin P. Investigation of peroxiredoxin IV as a calpain-regulated pathway in cancer. Anticancer Res 2010, 30:5085-5089.
24. Seo M.S., Kim J.K., Lim Y., Kang S.W., Cho Y.J., Lee W.K., Kim H.J., Cho K.K., Lee K.H., Rhee S.G. Rapid degradation of PrxI and PrxII induced by silica in Rat2 cells. Biochem. Biophys. Res. Commun. 1999, 265:541-544.
25. Souza K.L., Elsner M., Mathias P.C., Lenzen S., Tiedge M. Cytokines activate genes of the endocytotic pathway in insulin-producing RINm5F cells. Diabetologia 2004, 47:1292-1302.
26. Souza K.L., Gurgul-Convey E., Elsner M., Lenzen S. Interaction between pro-inflammatory and anti-inflammatory cytokines in insulin-producing cells. J. Endocrinol. 2008, 197:139-150.
27. Todaro M., Di Gaudio F., Lavitrano M., Stassi G., Papaccio G. Islet beta-cell apoptosis triggered in vivo by interleukin-1beta is not related to the inducible nitric oxide synthase pathway: evidence for mitochondrial function impairment and lipoperoxidation. Endocrinology 2003, 144:4264-4271.
28. Wang X., Phelan S.A., Forsman-Semb K., Taylor E.F., Petros C., Brown A., Lerner C.P., Paigen B. Mice with targeted mutation of peroxiredoxin 6 develop normally but are susceptible to oxidative stress. J. Biol. Chem. 2003, 278:25179-25190.
29. Wood Z.A., Schroder E., Robin Harris J., Poole L.B. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 2003, 28:32-40.