Mild exposure of RIN-5F β-cells to human islet amyloid polypeptide aggregates upregulates antioxidant enzymes via NADPH oxidase-RAGE: An hormetic stimulus

Redox Biology

Volumn 2, Issue 1, 2014, Pages 114-122

  Borchi, Elisabetta ^a   Bargelli, Valentina ^a   Guidotti, Valentina ^a   Berti, Andrea ^a,b   Stefani, Massimo ^a,b,c   Nediani, Chiara ^a   Rigacci, Stefania ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b Research Center on the Molecular Basis of Neurodegeneration   (Italy)

^c NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

Author keywords

Antioxidant enzyme; HIAPP; Hormesis; NADPH oxidase; RAGE; Type 2 diabetes

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; CATALASE; GLUTATHIONE PEROXIDASE; HUMAN ISLET AMYLOID POLYPEPTIDE; PEPTIDE HORMONE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; AMYLIN; IMMUNOGLOBULIN RECEPTOR;

ANIMAL CELL; ARTICLE; CELL PROTECTION; CELL STIMULATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HORMESIS; LIPID PEROXIDATION; MOLECULAR DYNAMICS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; UPREGULATION; BINDING AFFINITY; DENSITOMETRY; IMMUNOFLUORESCENCE; INSULINOMA CELL LINE; OLIGOMERIZATION; OXIDATION; PROTEIN AGGREGATION; PROTEIN BINDING; SEQUENCE HOMOLOGY; TRANSMISSION ELECTRON MICROSCOPY; UBIQUITINATION; ANIMAL; CYTOLOGY; DRUG EFFECTS; METABOLISM; TUMOR CELL LINE;

ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; ANIMALS; CATALASE; CELL LINE, TUMOR; GLUTATHIONE PEROXIDASE; INSULIN-SECRETING CELLS; ISLET AMYLOID POLYPEPTIDE; LIPID PEROXIDATION; NADPH OXIDASE; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES; RECEPTORS, IMMUNOLOGIC; SUPEROXIDE DISMUTASE; UP-REGULATION;

EID: 84891928361     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2013.12.005     Document Type: Article

References (59)

1. Phillips L., Horowitz M. Amylin. Curr. Opin. Endocrinol. Diabetes 2006, 13(2):191-198.
2. Butler A., Janson J., Bonner-Weir S., Ritzel R., Rizza R., Butler P. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003, 52(1):102-110.
3. Höppener J., Lips C. Role of islet amyloid in type 2 diabetes mellitus. Int. J. Biochem. Cell Biol. 2006, 38(5-6):726-736.
4. Stefani M. Generic cell dysfunction in neurodegenerative disorders: role of surfaces in early protein misfolding, aggregation, and aggregate cytotoxicity. Neuroscientist 2007, 13(5):519-531.
5. Weise K., Radovan D., Gohlke A., Opitz N., Winter R. Interaction of hIAPP with model raft membranes and pancreatic beta-cells: cytotoxicity of hIAPP oligomers. Chembiochem 2010, 11(9):1280-1290.
6. Stefani M. Protein folding and misfolding on surfaces. Int. J. Mol. Sci. 2008, 9(12):2515-2542.
7. Sakuraba H., Mizukami H., Yagihashi N., Wada R., Hanyu C., Yagihashi S. Reduced beta-cell mass and expression of oxidative stress-related DNA damage in the islet of Japanese type II diabetic patients. Diabetologia 2002, 45(1):85-96.
8. Tanaka Y., Tran P., Harmon J., Robertson R. A role for glutathione peroxidase in protecting pancreatic beta cells against oxidative stress in a model of glucose toxicity. Proc. Natl. Acad. Sci. U S A 2002, 99(19):12363-12368.
9. Welsh N., Margulis B., Borg L., Wiklund H., Saldeen J., Flodström M., Mello M., Andersson A., Pipeleers D., Hellerström C., et al. Differences in the expression of heat-shock proteins and antioxidant enzymes between human and rodent pancreatic islets: implications for the pathogenesis of insulin-dependent diabetes mellitus. Mol. Med. 1995, 1(7):806-820.
10. Hayden M., Sowers J. Isletopathy in type 2 diabetes mellitus: implications of islet RAS, islet fibrosis, islet amyloid, remodeling, and oxidative stress. Antioxid. Redox. Signal. 2007, 9(7):891-910.
11. Leung K., Leung P. Effects of hyperglycemia on angiotensin II receptor type 1 expression and insulin secretion in an INS-1E pancreatic beta-cell line. JOP 2008, 9(3):290-299.
12. Janciauskiene S., Ahrén B. Fibrillar islet amyloid polypeptide differentially affects oxidative mechanisms and lipoprotein uptake in correlation with cytotoxicity in two insulin-producing cell lines. Biochem. Biophys. Res. Commun. 2000, 267(2):619-625.
13. Konarkowska B., Aitken J., Kistler J., Zhang S., Cooper G. Thiol reducing compounds prevent human amylin-evoked cytotoxicity. FEBS J. 2005, 272(19):4949-4959.
14. Li X., Xu G., Chen T., Wong Y., Zhao H., Fan R., Gu X., Tong P., Chan J. Phycocyanin protects INS-1E pancreatic beta cells against human islet amyloid polypeptide-induced apoptosis through attenuating oxidative stress and modulating JNK and p38 mitogen-activated protein kinase pathways. Int. J. Biochem. Cell Biol. 2009, 41(7):1526-1535.
15. Jaikaran E., Nilsson M., Clark A. Pancreatic beta-cell granule peptides form heteromolecular complexes which inhibit islet amyloid polypeptide fibril formation. Biochem J. 2004, 377(Pt 3):709-716.
16. Juhl C., Pørksen N., Sturis J., Hansen A., Veldhuis J., Pincus S., Fineman M., Schmitz O. High-frequency oscillations in circulating amylin concentrations in healthy humans. Am. J. Physiol. Endocrinol. Metab. 2000, 278(3):E484-E490.
17. Brown D., Griendling K. Nox proteins in signal transduction. Free. Radic. Biol. Med. 2009, 47(9):1239-1253.
18. Lambeth J., Kawahara T., Diebold B. Regulation of Nox and Duox enzymatic activity and expression. Free Rad. Biol. Med. 2007, 43:319-331.
19. Opitz N., Drummond G.R., Selemidis S., Meurer S., Schmidt H. The 'A's and 'O's of NADPH oxidase regulation: a commentary on "subcellular localisation and function of alternatively spliced Noxo1 isoforms. Free Radic. Biol. Med. 2007, 42:175-179.
20. Uchizono Y., Takeya R., Iwase M., Sasaki N., Oku M., Imoto H., Iida M., Sumimoto H. Expression of isoforms of NADPH oxidase components in rat pancreatic islets. Life Sci. 2006, 80(2):133-139.
21. Rigacci S., Guidotti V., Bucciantini M., Parri M., Nediani C., Cerbai E., Stefani M., Berti A. Oleuropein aglycon prevents cytotoxic amyloid aggregation of human amylin. J. Nutr. Biochem. 2010, 21(8):726-735.
22. Ishihara Y., Ito F., Shimamoto N. Increased expression of c-Fos by extracellular signal-regulated kinase activation under sustained oxidative stress elicits BimEL upregulation and hepatocyte apoptosis. FEBS J. 2011, 278(11):1873-1881.
23. Rigacci S., Bucciantini M., Relini A., Pesce A., Gliozzi A., Berti A., Stefani M. The (1-63) region of the p53 transactivation domain aggregates in vitro into cytotoxic amyloid assemblies. Biophys. J. 2008, 94:3636-3646.
24. Nediani C., Borchi E., Giordano C., Baruzzo S., Ponziani V., Sebastiani M., Nassi P., Mugelli A., d'Amati G., Cerbai E. NADPH oxidase-dependent redox signaling in human heart failure: relationship between the left and right ventricle. J. Mol. Cell. Cardiol. 2007, 42(4):826-834.
25. LeBel C., Ischiropoulos H., Bondy S. Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 1992, 5(2):227-231.
26. Borchi E., Bargelli V., Stillitano F., Giordano C., Sebastiani M., Nassi P., d'Amati G., Cerbai E., Nediani C. Enhanced ROS production by NADPH oxidase is correlated to changes in antioxidant enzyme activity in human heart failure. Biochim. Biophys. Acta 2010, 1802:331-338.
27. Sebastiani M., Giordano C., Nediani C., Travaglini C., Borchi E., Zani M., Feccia M., Mancini M., Petrozza V., Cossarizza A., et al. Induction of mitochondrial biogenesis is a maladaptive mechanism in mitochondrial cardiomyopathies. J. Am. Coll. Cardiol. 2007, 50(14):1362-1369.
28. Chiti F., Dobson C. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 2006, 75:333-366.
29. Haataja L., Gurlo T., Huang C., Butler P. Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endocr. Rev. 2008, 29(3):303-316.
30. Brender J.R., Salamekh S., Ramamoorthy A. Membrane disruption and early events in the aggregation of the diabetes related peptide IAPP from a molecular perspective. Acc. Chem. Res. 2012, 45(3):454-462.
31. Engel M., Khemtémourian L., Kleijer C., Meeldijk H., Jacobs J., Verkleij A., de Kruijff B., Killian J., Höppener J Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane. Proc. Natl. Acad. Sci. U S A 2008, 105(16):6033-6038.
32. Borchi E., Parri M., Papucci L., Becatti M., Nassi N., Nassi P., Nediani C. Role of NADPH oxidase in H9c2 cardiac muscle cells exposed to simulated ischaemia-reperfusion. J. Cell. Mol. Med. 2009, 13:2724-2735.
33. Wind S., Beuerlein K., Eucker T., Müller H., Scheurer P., Armitage M., Ho H., Schmidt H., Wingler K. Comparative pharmacology of chemically distinct NADPH oxidase inhibitors. Br. J. Pharmacol. 2010, 161:885-898.
34. Yu J., Kim K., Kim D., Kim H. Diphenyleneiodonium suppresses apoptosis in cerulein-stimulated pancreatic acinar cells. Int.J.Biochem. Cell Biol. 2007, 39(11):2063-2075.
35. Du Yan S., Zhu H., Fu J., Yan S., Roher A., Tourtellotte W., Rajavashisth T., Chen X., Godman G., Stern D., et al. Amyloid-beta peptide-receptor for advanced glycation endproduct interaction elicits neuronal expression of macrophage-colony stimulating factor: a proinflammatory pathway in Alzheimer disease. Proc. Natl. Acad. Sci. U S A 1997, 94(10):5296-5301.
36. Onyango I., Tuttle J., Bennett J.J. Altered intracellular signaling and reduced viability of Alzheimer's disease neuronal cybrids is reproduced by beta-amyloid peptide acting through receptor for advanced glycation end products (RAGE). Mol. Cell. Neurosci. 2005, 29(2):333-343.
37. Yan S., Zhu H., Zhu A., Golabek A., Du H., Roher A., Yu J., Soto C., Schmidt A., Stern D., et al. Receptor-dependent cell stress and amyloid accumulation in systemic amyloidosis. Nat. Med. 2000, 6(6):643-651.
38. Wautier M., Chappey O., Corda S., Stern D., Schmidt A., Wautier J. Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am. J. Physiol. Endocrinol. Metab. 2001, 280(5):E685-E694.
39. Zraika S., Hull R., Udayasankar J., Aston-Mourney K., Subramanian S., Kisilevsky R., Szarek W., Kahn S. Oxidative stress is induced by islet amyloid formation and time-dependently mediates amyloid-induced beta cell apoptosis. Diabetologia 2009, 52(4):626-635.
40. Nakayama M., Inoguchi T., Sonta T., Maeda Y., Sasaki S., Sawada F., Tsubouchi H., Sonoda N., Kobayashi K., Sumimoto H., et al. Increased expression of NAD(P)H oxidase in islets of animal models of type 2 diabetes and its improvement by an AT1 receptor antagonist. Biochem. Biophys. Res. Commun. 2005, 332(4):927-933.
41. Oliveira H., Verlengia R., Carvalho C., Britto L., Curi R., Carpinelli A. Pancreatic beta-cells express phagocyte-like NAD(P)H oxidase. Diabetes 2003, 52(6):1457-1463.
42. Fan C., Katsuyama M., Yabe-Nishimura C. PKCdelta mediates up-regulation of NOX1, a catalytic subunit of NADPH oxidase, via transactivation of the EGF receptor: possible involvement of PKCdelta in vascular hypertrophy. Biochem J. 2005, 390(Pt3):761-767.
43. Lai A., McLaurin J. Mechanisms of amyloid-beta peptide uptake by neurons: the role of lipid rafts and lipid raft-associated proteins. Int. J. Alzheimers. Dis. 2011, 11.
44. Tanji N., Markowitz G., Fu C., Kislinger T., Taguchi A., Pischetsrieder M., Stern D., Schmidt A., D'Agati V. Expression of advanced glycation end products and their cellular receptor RAGE in diabetic nephropathy and nondiabetic renal disease. J. Am. Soc. Nephrol. 2000, 11(9):1656-1666.
45. Toth C., Rong L., Yang C., Martinez J., Song F., Ramji N., Brussee V., Liu W., Durand J., Nguyen M., et al. Receptor for advanced glycation end products (RAGEs) and experimental diabetic neuropathy. Diabetes 2008, 57(4):1002-1017.
46. Stern D., Yan S., Yan S., Schmidt A. Receptor for advanced glycation endproducts: a multiligand receptor magnifying cell stress in diverse pathologic settings. Adv. Drug. Deliv. Rev. 2002, 54(12):1615-1625.
47. Li X.L., Xu G., Chen T., Wong Y.S., Zhao H.L., Fan R.R., Gu X.M., Tong P.C., Chan J.C. Phycocyanin protects INS-1E pancreatic beta cells against human islet amyloid polypeptide-induced apoptosis through attenuating oxidative stress and modulating JNK and p38 mitogen-activated protein kinase pathways. Int. J. Biochem. Cell Biol. 2009, 41(7):1526-1535.
48. Kralik P., Xu B., Epstein P. Catalase transfection decreases hydrogen peroxide toxicity in a pancreatic beta cell line. Endocr. Res. 1998, 24(1):79-87.
49. Frey R., Ushio-Fukai M., Malik A.B. NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology. ARS 2009, 11:791-810.
50. Nediani C., Raimondi L., Borchi E., Cerbai E. NO/ROS generation and nitroso/redox imbalance in heart failure: from molecular mechanisms to therapeutic implications. Antioxid. Redox. Signal. 2011, 14(2):289-331.
51. Valko M., Leibfritz D., Moncola J., Cronin M., Mazura M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39:44-84.
52. Morley J., Farr S., Banks W., Johnson S., Yamada K., Xu L. A physiological role for amyloid-beta protein:enhancement of learning and memory. J. Alzheimers. Dis. 2010, 19(2):441-449.
53. Puzzo D., Privitera L., Palmeri A. Hormetic effect of amyloid-β peptide in synaptic plasticity and memory. Neurobiol. Aging 2012, 33(7). (14484 e14415-14424).
54. Fouillet A., Levet C., Virgone A., Robin M., Dourlen P., Rieusset J., Belaidi E., Ovize M., Touret M., Nataf S., et al. ER stress inhibits neuronal death by promoting autophagy. Autophagy 2012, 8(6):915-926.
55. Kolb H. Resistance to diabetes-promoting lifestyle factors - what is the mechanism?. Diabetes Res. Clin. Pract. 2012, 97:172-174.
56. Kolb H., Eizirik D. Resistance to type 2 diabetes mellitus: a matter of hormesis?. Nat. Rev. Endocrinol. 2011, 8:183-192.
57. Cohen G., Riahi Y., Sunda V., Deplano S., Chatgilialoglu C., Ferreri C., Kaiser N., Sasson S. Signaling properties of 4-hydroxyalkenals formed by lipid peroxidation in diabetes. Free Radic. Biol. Med. 2013, 65C:978-987.
58. Siow R., Ishii T., Mann G. Modulation of antioxidant gene expression by 4-hydroxynonenal: atheroprotective role of the Nrf2/ARE transcription pathway. Redox Rep. 2007, 12(1):11-15.
59. Zhao H., Sui Y., Guan J., He L., Gu X., Wong H., Baum L., Lai F., Tong P., Chan J. Amyloid oligomers in diabetic and nondiabetic human pancreas. Transl. Res. 2009, 153:24-32.