Pro-oxidant/antioxidant balance controls pancreatic β-cell differentiation through the ERK1/2 pathway

Cell Death and Disease

Volumn 5, Issue 10, 2014, Pages

  Hoarau, E ^a,b   Chandra, V ^a,b   Rustin, P ^c   Scharfmann, R ^a,b   Duvillie, B ^a,b  

^a INSTITUT COCHIN   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HÔPITAL ROBERT DEBRÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ACETYLCYSTEINE; ANTIOXIDANT; CATALASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUROGENIN 3; OXIDIZING AGENT; PROOXIDANT; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; HYDROGEN PEROXIDE; NERVE PROTEIN; NEUROG3 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL STIMULATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; EXPERIMENT; EXPLANT; GENE TRANSFER; IN VIVO STUDY; NONHUMAN; OXIDATION REDUCTION STATE; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; STEM CELL; TISSUE CULTURE; ANIMAL; ANIMAL EMBRYO; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; EPITHELIUM; FEMALE; METABOLISM; PHOSPHORYLATION; WISTAR RAT;

ACETYLCYSTEINE; ANIMALS; ANTIOXIDANTS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARBONYL CYANIDE M-CHLOROPHENYL HYDRAZONE; CATALASE; CELL DIFFERENTIATION; EMBRYO, MAMMALIAN; EPITHELIUM; FEMALE; HYDROGEN PEROXIDE; INSULIN-SECRETING CELLS; MAP KINASE SIGNALING SYSTEM; NERVE TISSUE PROTEINS; OXIDANTS; PHOSPHORYLATION; RATS, WISTAR;

EID: 84928004394     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.441     Document Type: Article

References (44)

1. Sato A, Okada M, Shibuya K, Watanabe E, Seino S, Narita Y et al. Pivotal role for ROS activation of p38 MAPK in the control of differentiation and tumor-initiating capacity of gliomainitiating cells. Stem Cell Res 2014; 12: 119-131.
2. Waris G, Ahsan H. Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinog 2006; 5: 14.
3. D'Autreaux B, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 2007; 8: 813-824.
4. Arana L, Gangoiti P, Ouro A, Rivera IG, Ordonez M, Trueba M et al. Generation of reactive oxygen species (ROS) is a key factor for stimulation of macrophage proliferation by ceramide 1-phosphate. Exp Cell Res 2012; 318: 350-360.
5. Panieri E, Gogvadze V, Norberg E, Venkatesh R, Orrenius S, Zhivotovsky B. Reactive oxygen species generated in different compartments induce cell death, survival, or senescence. Free Radic Biol Med 2013; 57: 176-187.
6. Lee H, Lee YJ, Choi H, Ko EH, Kim JW. Reactive oxygen species facilitate adipocyte differentiation by accelerating mitotic clonal expansion. J Biol Chem 2009; 284: 10601-10609.
7. 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.
8. Tiedge M, Lortz S, Drinkgern J, Lenzen S. Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 1997; 46: 1733-1742.
9. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001; 414: 813-820.
10. Hunt JV, Smith CC, Wolff SP. Autoxidative glycosylation and possible involvement of peroxides and free radicals in LDL modification by glucose. Diabetes 1990; 39: 1420-1424.
11. Del Guerra S, Lupi R, Marselli L, Masini M, Bugliani M, Sbrana S et al. Functional and molecular defects of pancreatic islets in human type 2 diabetes. Diabetes 2005; 54: 727-735.
12. 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: 85-96.
13. Leloup C, Tourrel-Cuzin C, Magnan C, Karaca M, Castel J, Carneiro L et al. Mitochondrial reactive oxygen species are obligatory signals for glucose-induced insulin secretion. Diabetes 2009; 58: 673-681.
14. Chaudhari P, Ye Z, Jang YY. Roles of reactive oxygen species in the fate of stem cells. Antioxid Redox Signal 2014; 20: 1881-1890.
15. Arda HE, Benitez CM, Kim SK. Gene regulatory networks governing pancreas development. Dev Cell 2013; 25: 5-13.
16. Benitez CM, Goodyer WR, Kim SK. Deconstructing pancreas developmental biology. Cold Spring Harb Perspect Biol 2012; 4: pii: a012401.
17. Ahlgren U, Jonsson J, Edlund H. The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-deficient mice. Development 1996; 122: 1409-1416.
18. Stoffers DA, Zinkin NT, Stanojevic V, Clarke WL, Habener JF. Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat Genet 1997; 15: 106-110.
19. Bhushan A, Itoh N, Kato S, Thiery JP, Czernichow P, Bellusci S et al. Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 2001; 128: 5109-5117.
20. Gradwohl G, Dierich A, LeMeur M, Guillemot F. Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci USA 2000; 97: 1607-1611.
21. Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 2007; 110: 3056-3063.
22. Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, Pyle AD et al. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 2011; 8: 59-71.
23. Rhee SG, Kang SW, Jeong W, Chang TS, Yang KS, Woo HA. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol 2005; 17: 183-189.
24. Abramov JP, Wells PG. Embryonic catalase protects against endogenous and phenytoinenhanced DNA oxidation and embryopathies in acatalasemic and human catalaseexpressing mice. FASEB J 2011; 25: 2188-2200.
25. Rapoport R, Hanukoglu I, Sklan D. A fluorimetric assay for hydrogen peroxide, suitable for NAD(P)H-dependent superoxide generating redox systems. Anal Biochem 1994; 218: 309-313.
26. Dempsey PM, O'Leary J, Condon S. Polarographic assay of hydrogen peroxide accumulation in microbial cultures. Appl Microbiol 1975; 29: 170-174.
27. Ohlsson H, Karlsson K, Edlund T. IPF1, a homeodomain-containing transactivator of the insulin gene. Embo J 1993; 12: 4251-4259.
28. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009; 417: 1-13.
29. Zhang Y, Choksi S, Chen K, Pobezinskaya Y, Linnoila I, Liu ZG. ROS play a critical role in the differentiation of alternatively activated macrophages and the occurrence of tumor-associated macrophages. Cell Res 2013; 23: 898-914.
30. Briaud I, Lingohr MK, Dickson LM, Wrede CE, Rhodes CJ. Differential activation mechanisms of Erk-1/2 and p70(S6K) by glucose in pancreatic beta-cells. Diabetes 2003; 52: 974-983.
31. Fernandez E, Martin MA, Fajardo S, Escriva F, Alvarez C. Increased IRS-2 content and activation of IGF-I pathway contribute to enhance beta-cell mass in fetuses from undernourished pregnant rats. Am J Physiol Endocrinol Metabol 2007; 292: E187-E195.
32. Simmons RA. Role of metabolic programming in the pathogenesis of beta-cell failure in postnatal life. Rev Endocr Metab Disord 2007; 8: 95-104.
33. Laurent G, Solari F, Mateescu B, Karaca M, Castel J, Bourachot B et al. Oxidative stress contributes to aging by enhancing pancreatic angiogenesis and insulin signaling. Cell Metab 2008; 7: 113-124.
34. Attali M, Stetsyuk V, Basmaciogullari A, Aiello V, Zanta-Boussif MA, Duvillie B et al. Control of beta-cell differentiation by the pancreatic mesenchyme. Diabetes 2007; 56: 1248-1258.
35. Saleem S, Li J, Yee SP, Fellows GF, Goodyer CG, Wang R. beta1 integrin/FAK/ERK signalling pathway is essential for human fetal islet cell differentiation and survival. J Pathol 2009; 219: 182-192.
36. Costes S, Broca C, Bertrand G, Lajoix AD, Bataille D, Bockaert J et al. ERK1/2 control phosphorylation and protein level of cAMP-responsive element-binding protein: a key role in glucose-mediated pancreatic beta-cell survival. Diabetes 2006; 55: 2220-2230.
37. Yalcin S, Zhang X, Luciano JP, Mungamuri SK, Marinkovic D, Vercherat C et al. Foxo3 is essential for the regulation of ataxia telangiectasia mutated and oxidative stress-mediated homeostasis of hematopoietic stem cells. J Biol Chem 2008; 283: 25692-25705.
38. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004; 303: 2011-2015.
39. Kraft AD, Johnson DA, Johnson JA. Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult. J Neurosci 2004; 24: 1101-1112.
40. Kraft R, Grimm C, Grosse K, Hoffmann A, Sauerbruch S, Kettenmann H et al. Hydrogen peroxide and ADP-ribose induce TRPM2-mediated calcium influx and cation currents in microglia. Am J Physiol Cell Physiol 2004; 286: C129-C137.
41. Inomata K, Aoto T, Binh NT, Okamoto N, Tanimura S,Wakayama T et al. Genotoxic stress abrogates renewal of melanocyte stem cells by triggering their differentiation. Cell 2009; 137: 1088-1099.
42. Watson JD. Type 2 diabetes as a redox disease. Lancet 2014; 383: 841-843.
43. Heinis M, Soggia A, Bechetoille C, Simon MT, Peyssonnaux C, Rustin P et al. HIF1alpha and pancreatic beta-cell development. FASEB J 2012; 26: 2734-2742.
44. Guillemain G, Filhoulaud G, Da Silva-Xavier G, Rutter GA, Scharfmann R. Glucose is necessary for embryonic pancreatic endocrine cell differentiation. J Biol Chem 2007; 282: 15228-15237.