367
Views
19
CrossRef citations to date
0
Altmetric
Articles

Reg2 protects mouse insulinoma cells from streptozotocin-induced mitochondrial disruption and apoptosis

, &
Pages 370-378 | Received 30 Mar 2010, Accepted 23 Jun 2010, Published online: 05 Oct 2010

References

  • Anastasi E, Ponte E, Gradini R, Bulotta A, Sale P, Tiberti C, Okamoto H, Dotta F, Mario UD. 1999. Expression of Reg and cytokeratin 20 during ductal cell differentiation and proliferation in a mouse model of autoimmune diabetes. Eur J Endocrinol. 141:644–652.
  • Aughsteen AA. 2000. An ultrastructural study on the effect of streptozotocin on the islets of Langerhans in mice. J Electron Microsc. 49:681–690.
  • Bae MA, Song BJ. 2003. Critical role of c-Jun N-terminal protein kinase activation in troglitazone-induced apoptosis of human HepG2 hepatoma cells. Mol Pharmacol. 63:401–408.
  • Burkart V, Blaeser K, Kolb H. Potent beta-cell protection in vitro by an isoquinolinone-derived PARP inhibitor. Horm Metabol Res. 1999a; 31:641–644.
  • Burkart V, Wang ZQ, Radons J, Heller B, Herceg Z, Stingl L, Wagner EF, Kolb H. Mice lacking the poly(ADP-ribose) polymerase gene are resistant to pancreatic beta-cell destruction and diabetes development induced by streptozocin. Nat Med. 1999b; 5:314–319.
  • Cardinal JW, Allan DJ, Cameron DP. 1998. Differential metabolite accumulation may be the cause of strain differences in sensitivity to streptozotocin-induced beta cell death in inbred mice. Endocrinology. 139:2885–2891.
  • Costes S, Broca C, Bertrand G, Lajoix AD, Bataille D, Bockaert J, Dalle S. 2006. ERK1/2 control phosphorylation and protein level of cAMP-responsive element-binding protein: A key role in glucose-mediated pancreatic {beta}-cell survival. Diabetes. 55:2220–2230.
  • Cui W, De Jesus K, Zhao H, Takasawa S, Shi B, Srikant CB, Liu JL. 2009. Overexpression of Reg3alpha increases cell growth and the levels of cyclin D1 and CDK4 in insulinoma cells. Growth Factors (Chur, Switzerland). 27:195–202.
  • De Leon DD, Farzad C, Crutchlow MF, Brestelli J, Tobias J, Kaestner KH, Stoffers DA. 2006. Identification of transcriptional targets during pancreatic growth after partial pancreatectomy and exendin-4 treatment. Physiol Genom. 24:133–143.
  • Doi A, Shono T, Nishi M, Furuta H, Sasaki H, Nanjo K. 2006. IA-2beta, but not IA-2, is induced by ghrelin and inhibits glucose-stimulated insulin secretion. Proc Natl Acad Sci USA. 103:885–890.
  • Donath MY, Halban PA. 2004. Decreased beta-cell mass in diabetes: Significance, mechanisms and therapeutic implications. Diabetologia. 47:581–589.
  • Egan JM, Bulotta A, Hui H, Perfetti R. 2003. GLP-1 receptor agonists are growth and differentiation factors for pancreatic islet beta cells. Diabetes Metab Res Rev. 19:115–123.
  • Freeman H, Shimomura K, Horner E, Cox RD, Ashcroft FM. 2006. Nicotinamide nucleotide transhydrogenase: A key role in insulin secretion. Cell Metabol. 3:35–45.
  • Fukuda K, Tesch GH, Nikolic-Paterson DJ. 2008. c-Jun amino terminal kinase 1 deficient mice are protected from streptozotocin-induced islet injury. Biochem Biophys Res Commun. 366:710–716.
  • Gao Y, Parker GJ, Hart GW. 2000. Streptozotocin-induced beta-cell death is independent of its inhibition of O-GlcNAcase in pancreatic Min6 cells. Arch Biochem Biophys. 383:296–302.
  • Gonzalez C, Menissier De Murcia J, Janiak P, Bidouard JP, Beauvais C, Karray S, Garchon HJ, Levi-Strauss M. 2002. Unexpected sensitivity of nonobese diabetic mice with a disrupted poly(ADP-Ribose) polymerase-1 gene to streptozotocin-induced and spontaneous diabetes. Diabetes. 51:1470–1476.
  • Gurr W, Shaw M, Li Y, Sherwin R. 2007. RegII is a {beta}-cell protein and autoantigen in diabetes of NOD mice. Diabetes. 56:34–40.
  • Hussain MA, Miller CP, Habener JF. 2002. Brn-4 transcription factor expression targeted to the early developing mouse pancreas induces ectopic glucagon gene expression in insulin-producing beta cells. J Biol Chem. 277:16028–16032.
  • Ishihara H, Asano T, Tsukuda K, Katagiri H, Inukai K, Anai M, Kikuchi M, Yazaki Y, Miyazaki JI, Oka Y. 1993. Pancreatic beta cell line MIN6 exhibits characteristics of glucose metabolism and glucose-stimulated insulin secretion similar to those of normal islets. Diabetologia. 36:1139–1145.
  • Jamal AM, Lipsett M, Sladek R, Laganiere S, Hanley S, Rosenberg L. 2005. Morphogenetic plasticity of adult human pancreatic islets of Langerhans. Cell Death Differ. 12:702–712.
  • Kaneto H, Fujii J, Seo HG, Suzuki K, Matsuoka T, Nakamura M, Tatsumi H, Yamasaki Y, Kamada T, Taniguchi N. 1995. Apoptotic cell death triggered by nitric oxide in pancreatic beta-cells. Diabetes. 44:733–738.
  • Kaneto H, Sharma A, Suzuma K, Laybutt DR, Xu G, Bonner-Weir S, Weir GC. 2002. Induction of c-Myc expression suppresses insulin gene transcription by inhibiting NeuroD/BETA2-mediated transcriptional activation. J Biol Chem. 277:12998–13006.
  • Kayo T, Sawada Y, Suda M, Konda Y, Izumi T, Tanaka S, Shibata H, Takeuchi T. 1997. Proprotein-processing endoprotease furin controls growth of pancreatic beta-cells. Diabetes. 46:1296–1304.
  • Kobayashi S, Akiyama T, Nata K, Abe M, Tajima M, Shervani NJ, Unno M, Matsuno S, Sasaki H, Takasawa S, Okamoto H. 2000. Identification of a receptor for reg (regenerating gene) protein, a pancreatic beta-cell regeneration factor. J Biol Chem. 275:10723–10726.
  • Li B, Wang X, Liu J-L. Pancreatic acinar-specific overexpression of Reg2 gene offered no protection against either experimental diabetes or pancreatitis in mice. Am J Physiol Gastroint Liver Physiol. 2010 doi.10.1152/ajpgi.00500.2009.
  • Lilla V, Webb G, Rickenbach K, Maturana A, Steiner DF, Halban PA, Irminger J-C. 2003. Differential gene expression in well-regulated and dysregulated pancreatic {beta}-cell (MIN6) sublines. Endocrinology. 144:1368–1379.
  • Lingohr MK, Buettner R, Rhodes CJ. 2002. Pancreatic beta-cell growth and survival—a role in obesity-linked type 2 diabetes?. Trends Mol Med. 8:375–384.
  • Liu D, Martino G, Thangaraju M, Sharma M, Halwani F, Shen SH, Patel YC, Srikant CB. 2000. Caspase-8-mediated intracellular acidification precedes mitochondrial dysfunction in somatostatin-induced apoptosis. J Biol Chem. 275:9244–9250.
  • Liu JL, Cui W, Li B, Lu Y. 2008. Possible roles of reg family proteins in pancreatic islet cell growth. Endocr Metab Immune Disorders Drug Targets. 8:1–10.
  • Lu Y, Herrera PL, Guo Y, Sun D, Tang Z, LeRoith D, Liu JL. 2004. Pancreatic-specific inactivation of IGF-I gene causes enlarged pancreatic islets and significant resistance to diabetes. Diabetes. 53:3131–3141.
  • Lu Y, Ponton A, Okamoto H, Takasawa S, Herrera PL, Liu JL. 2006. Activation of the Reg family genes by pancreatic-specific IGF-I gene deficiency and after streptozotocin-induced diabetes in mouse pancreas. Am J Physiol. 291:E50–E58.
  • Masutani M, Suzuki H, Kamada N, Watanabe M, Ueda O, Nozaki T, Jishage K, Watanabe T, Sugimoto T, Nakagama H, Ochiya T, Sugimura T. 1999. Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes. Proc Natl Acad Sci USA. 96:2301–2304.
  • Mellado-Gil JM, Aguilar-Diosdado M. 2004. High glucose potentiates cytokine- and streptozotocin-induced apoptosis of rat islet cells: Effect on apoptosis-related genes. J Endocrinol. 183:155–162.
  • Miyazaki J, Araki K, Yamato E, Ikegami H, Asano T, Shibasaki Y, Oka Y, Yamamura K. 1990. Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: Special reference to expression of glucose transporter isoforms. Endocrinology. 127:126–132.
  • Mueller CM, Zhang H, Zenilman ME. 2008. Pancreatic reg I binds MKP-1 and regulates cyclin D in pancreatic-derived cells. J Surg Res. 150:137–143.
  • Oyadomari S, Takeda K, Takiguchi M, Gotoh T, Matsumoto M, Wada I, Akira S, Araki E, Mori M. 2001. Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci USA. 98:10845–10850.
  • Pieper AA, Brat DJ, Krug DK, Watkins CC, Gupta A, Blackshaw S, Verma A, Wang ZQ, Snyder SH. 1999. Poly(ADP-ribose) polymerase-deficient mice are protected from streptozotocin-induced diabetes. Proc Natl Acad Sci USA. 96:3059–3064.
  • Planas R, Alba A, Carrillo J, Puertas MC, Ampudia R, Pastor X, Okamoto H, Takasawa S, Gurr W, Pujol-Borrell R, Verdaguer J, Vives-Pi M. 2006. Reg (regenerating) gene overexpression in islets from non-obese diabetic mice with accelerated diabetes: Role of IFNbeta. Diabetologia. 49:2379–2387.
  • Rafaeloff R, Pittenger GL, Barlow SW, Qin XF, Yan B, Rosenberg L, Duguid WP, Vinik AI. 1997. Cloning and sequencing of the pancreatic islet neogenesis associated protein (INGAP) gene and its expression in islet neogenesis in hamsters. J Clin Invest. 99:2100–2109.
  • Rosenberg L, Lipsett M, Yoon JW, Prentki M, Wang R, Jun HS, Pittenger GL, Taylor-Fishwick D, Vinik AI. 2004. A pentadecapeptide fragment of islet neogenesis-associated protein increases beta-cell mass and reverses diabetes in C57BL/6J mice. Ann Surg. 240:875–884.
  • Saini KS, Thompson C, Winterford CM, Walker NI, Cameron DP. 1996. Streptozotocin at low doses induces apoptosis and at high doses causes necrosis in a murine pancreatic beta cell line, INS-1. Biochem Mol Biol Intl. 39:1229–1236.
  • Sasahara K, Yamaoka T, Moritani M, Yoshimoto K, Kuroda Y, Itakura M. 2000. Molecular cloning and tissue-specific expression of a new member of the regenerating protein family, islet neogenesis-associated protein-related protein. Biochim Biophys Acta. 1500:142–146.
  • Takasawa S, Okamoto H. 2002. Pancreatic beta-cell death, regeneration and insulin secretion: roles of poly(ADP-ribose) polymerase and cyclic ADP-ribose. Int J Exp Diabetes Res. 3:79–96.
  • Targonsky ED, Dai F, Koshkin V, Karaman GT, Gyulkhandanyan AV, Zhang Y, Chan CB, Wheeler MB. 2006. Alpha-Lipoic acid regulates AMP-activated protein kinase and inhibits insulin secretion from beta cells. Diabetologia. 49:1587–1598.
  • Taylor-Fishwick DA, Rittman S, Kendall H, Roy L, Shi W, Cao Y, Pittenger GL, Vinik AI. 2003. Cloning genomic INGAP: A Reg-related family member with distinct transcriptional regulation sites. Biochim Biophys Acta. 1638:83–89.
  • Terazono K, Yamamoto H, Takasawa S, Shiga K, Yonemura Y, Tochino Y, Okamoto H. 1988. A novel gene activated in regenerating islets. J Biol Chem. 263:2111–2114.
  • Tourian LJr, Zhao H, Srikant CB. 2004. p38{alpha}, but not p38{beta}, inhibits the phosphorylation and presence of c-FLIPS in DISC to potentiate Fas-mediated caspase-8 activation and type I apoptotic signaling. J Cell Sci. 117:6459–6471.
  • Turk J, Corbett JA, Ramanadham S, Bohrer A, McDaniel ML. 1993. Biochemical evidence for nitric oxide formation from streptozotocin in isolated pancreatic islets. Biochem Biophys Res Commun. 197:1458–1464.
  • Unno M, Yonekura H, Nakagawara K, Watanabe T, Miyashita H, Moriizumi S, Okamoto H, Itoh T, Teraoka H. 1993. Structure, chromosomal localization, and expression of mouse reg genes, reg I and reg II. A novel type of reg gene, reg II, exists in the mouse genome. J Biol Chem. 268:15974–15982.
  • Wada R, Yagihashi S. 2004. Nitric oxide generation and poly(ADP ribose) polymerase activation precede beta-cell death in rats with a single high-dose injection of streptozotocin. Virchows Arch. 444:375–382.
  • Wang J, Cao Y, Chen Y, Chen Y, Gardner P, Steiner DF. 2006. Pancreatic beta cells lack a low glucose and O2-inducible mitochondrial protein that augments cell survival. Proc Natl Acad Sci USA. 103:10636–10641.
  • Zhang B, Lu Y, Campbell-Thompson M, Spencer T, Wasserfall C, Atkinson M, Song S. 2007. Alpha1-antitrypsin protects beta-cells from apoptosis. Diabetes. 56:1316–1323.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.