Betacellulin-induced beta cell proliferation and regeneration is mediated by activation of ErbB-1 and ErbB-2 receptors

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Oh, Yoon Sin ^a   Shin, Seungjin ^b   Lee, Youn Jung ^a   Kim, Eung Hwi ^a   Jun, Hee Sook ^a  

^a Gachon University College of Medicine   (South Korea)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; 5 (2 BENZOTHIAZOLYL)THIOMETHYL 4 HYDROXY 3 METHOXYBENZYLIDENECYANOACETAMIDE; BETACELLULIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; GLUCOSE; INSULIN RECEPTOR SUBSTRATE 2; MESSENGER RNA; SMALL INTERFERING RNA; INSULIN RECEPTOR SUBSTRATE; IRS2 PROTEIN, MOUSE; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELL REGENERATION; CELL SIZE; CONTROLLED STUDY; DIABETES MELLITUS; DNA SYNTHESIS; GLUCOSE BLOOD LEVEL; IMMUNOPRECIPITATION; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REMISSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; CELL LINE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY;

ADENOVIRIDAE; MUS;

ANIMALS; CELL LINE; CELL PROLIFERATION; DIABETES MELLITUS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN-SECRETING CELLS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2;

EID: 80052293598     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023894     Document Type: Article

References (44)

1. Harlan DM, Kenyon NS, Korsgren O, Roep BO, (2009) Current advances and travails in islet transplantation. Diabetes 58: 2175-2184.
2. Shing Y, Christofori G, Hanahan D, Ono Y, Sasada R, et al. (1993) Betacellulin: a mitogen from pancreatic beta cell tumors. Science 259: 1604-1607.
3. Dunbar AJ, Goddard C, (2000) Structure-function and biological role of betacellulin. Int J Biochem Cell Biol 32: 805-815.
4. Sasada R, Ono Y, Taniyama Y, Shing Y, Folkman J, et al. (1993) Cloning and expression of cDNA encoding human betacellulin, a new member of the EGF family. Biochem Biophys Res Commun 190: 1173-1179.
5. Seno M, Tada H, Kosaka M, Sasada R, Igarashi K, et al. (1996) Human betacellulin, a member of the EGF family dominantly expressed in pancreas and small intestine, is fully active in a monomeric form. Growth Factors 13: 181-191.
6. Mashima H, Ohnishi H, Wakabayashi K, Mine T, Miyagawa J, et al. (1996) Betacellulin and activin A coordinately convert amylase-secreting pancreatic AR42J cells into insulin-secreting cells. J Clin Invest 97: 1647-1654.
7. Sundaresan S, Roberts PE, King KL, Sliwkowski MX, Mather JP, (1998) Biological response to ErbB ligands in nontransformed cell lines correlates with a specific pattern of receptor expression. Endocrinology 139: 4756-4764.
8. Huotari MA, Palgi J, Otonkoski T, (1998) Growth factor-mediated proliferation and differentiation of insulin-producing INS-1 and RINm5F cells: identification of betacellulin as a novel beta-cell mitogen. Endocrinology 139: 1494-1499.
9. Shin S, Li N, Kobayashi N, Yoon JW, Jun HS, (2008) Remission of diabetes by beta-cell regeneration in diabetic mice treated with a recombinant adenovirus expressing betacellulin. Mol Ther 16: 854-861.
10. Dahlhoff M, Dames PM, Lechner A, Herbach N, van Burck L, et al. (2009) Betacellulin overexpression in transgenic mice improves glucose tolerance and enhances insulin secretion by isolated islets in vitro. Mol Cell Endocrinol 299: 188-193.
11. Grzech M, Dahlhoff M, Herbach N, Habermann FA, Renner-Muller I, et al. (2010) Specific transgene expression in mouse pancreatic beta-cells under the control of the porcine insulin promoter. Mol Cell Endocrinol 315: 219-224.
12. Wells A, (1999) EGF receptor. Int J Biochem Cell Biol 31: 637-643.
13. Yarden Y, Sliwkowski MX, (2001) Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2: 127-137.
14. Citri A, Yarden Y, (2006) EGF-ERBB signalling: towards the systems level. Nat Rev Mol Cell Biol 7: 505-516.
15. Miettinen PJ, Huotari M, Koivisto T, Ustinov J, Palgi J, et al. (2000) Impaired migration and delayed differentiation of pancreatic islet cells in mice lacking EGF-receptors. Development 127: 2617-2627.
16. Gassmann M, Casagranda F, Orioli D, Simon H, Lai C, et al. (1995) Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378: 390-394.
17. Erickson SL, O'Shea KS, Ghaboosi N, Loverro L, Frantz G, et al. (1997) ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice. Development 124: 4999-5011.
18. Shin HS, Lee HJ, Nishida M, Lee MS, Tamura R, et al. (2003) Betacellulin and amphiregulin induce upregulation of cyclin D1 and DNA synthesis activity through differential signaling pathways in vascular smooth muscle cells. Circ Res 93: 302-310.
19. Genetos DC, Rao RR, Vidal MA, (2010) Betacellulin inhibits osteogenic differentiation and stimulates proliferation through HIF-1alpha. Cell Tissue Res 340: 81-89.
20. Sarkar SA, Gunter J, Bouchard R, Reusch JE, Wiseman A, et al. (2007) Dominant negative mutant forms of the cAMP response element binding protein induce apoptosis and decrease the anti-apoptotic action of growth factors in human islets. Diabetologia 50: 1649-1659.
21. Jhala US, Canettieri G, Screaton RA, Kulkarni RN, Krajewski S, et al. (2003) cAMP promotes pancreatic beta-cell survival via CREB-mediated induction of IRS2. Genes Dev 17: 1575-1580.
22. Kitamura T, Nakae J, Kitamura Y, Kido Y, Biggs WH III, et al. (2002) The forkhead transcription factor Foxo1 links insulin signaling to Pdx1 regulation of pancreatic beta cell growth. J Clin Invest 110: 1839-1847.
23. Levitzki A, Gazit A, (1995) Tyrosine kinase inhibition: an approach to drug development. Science 267: 1782-1788.
24. Lee HK, Seo IA, Lee SH, Seo SY, Kim KS, et al. (2008) Tyrphostin ErbB2 Inhibitors AG825 and AG879 Have Non-specific Suppressive Effects on gp130/STAT3 Signaling. Korean J Physiol Pharmacol 12: 281-286.
25. Withers DJ, Gutierrez JS, Towery H, Burks DJ, Ren JM, et al. (1998) Disruption of IRS-2 causes type 2 diabetes in mice. Nature 391: 900-904.
26. Hennige AM, Burks DJ, Ozcan U, Kulkarni RN, Ye J, et al. (2003) Upregulation of insulin receptor substrate-2 in pancreatic beta cells prevents diabetes. J Clin Invest 112: 1521-1532.
27. Sorenson RL, Brelje TC, (1997) Adaptation of islets of Langerhans to pregnancy: beta-cell growth, enhanced insulin secretion and the role of lactogenic hormones. Horm Metab Res 29: 301-307.
28. Liu MJ, Shin S, Li N, Shigihara T, Lee YS, et al. (2007) Prolonged remission of diabetes by regeneration of beta cells in diabetic mice treated with recombinant adenoviral vector expressing glucagon-like peptide-1. Mol Ther 15: 86-93.
29. Brand SJ, Tagerud S, Lambert P, Magil SG, Tatarkiewicz K, et al. (2002) Pharmacological treatment of chronic diabetes by stimulating pancreatic beta-cell regeneration with systemic co-administration of EGF and gastrin. Pharmacol Toxicol 91: 414-420.
30. Tokui Y, Kozawa J, Yamagata K, Zhang J, Ohmoto H, et al. (2006) Neogenesis and proliferation of beta-cells induced by human betacellulin gene transduction via retrograde pancreatic duct injection of an adenovirus vector. Biochem Biophys Res Commun 350: 987-993.
31. Yamamoto K, Miyagawa J, Waguri M, Sasada R, Igarashi K, et al. (2000) Recombinant human betacellulin promotes the neogenesis of beta-cells and ameliorates glucose intolerance in mice with diabetes induced by selective alloxan perfusion. Diabetes 49: 2021-2027.
32. Li L, Seno M, Yamada H, Kojima I, (2001) Promotion of beta-cell regeneration by betacellulin in ninety percent-pancreatectomized rats. Endocrinology 142: 5379-5385.
33. Suarez-Pinzon WL, Lakey JR, Brand SJ, Rabinovitch A, (2005) Combination therapy with epidermal growth factor and gastrin induces neogenesis of human islet {beta}-cells from pancreatic duct cells and an increase in functional {beta}-cell mass. J Clin Endocrinol Metab 90: 3401-3409.
34. Lee HY, Yea K, Kim J, Lee BD, Chae YC, et al. (2008) Epidermal growth factor increases insulin secretion and lowers blood glucose in diabetic mice. J Cell Mol Med 12: 1593-1604.
35. Bonner-Weir S, (1994) Regulation of pancreatic beta-cell mass in vivo. Recent Prog Horm Res 49: 91-104.
36. Kuntz E, Broca C, Komurasaki T, Kaltenbacher MC, Gross R, et al. (2005) Effect of epiregulin on pancreatic beta cell growth and insulin secretion. Growth Factors 23: 285-293.
37. Nagaoka T, Fukuda T, Hashizume T, Nishiyama T, Tada H, et al. (2008) A betacellulin mutant promotes differentiation of pancreatic acinar AR42J cells into insulin-producing cells with low affinity of binding to ErbB1. J Mol Biol 380: 83-94.
38. Perry JE, Grossmann ME, Tindall DJ, (1998) Epidermal growth factor induces cyclin D1 in a human prostate cancer cell line. Prostate 35: 117-124.
39. Bonner-Weir S, Weir GC, (2005) New sources of pancreatic beta-cells. Nat Biotechnol 23: 857-861.
40. Zhan XR, Li XY, Liu XM, Zhou JH, Yang YL, et al. (2009) Generation of insulin-secreting cells from adult rat pancreatic ductal epithelial cells induced by hepatocyte growth factor and betacellulin-delta4. Biochem Biophys Res Commun 382: 375-380.
41. Kritzik MR, Krahl T, Good A, Gu D, Lai C, et al. (2000) Expression of ErbB receptors during pancreatic islet development and regrowth. J Endocrinol 165: 67-77.
42. Ishiyama M, Miyazono Y, Sasamoto K, Ohkura Y, Ueno K, (1997) A highly water-soluble disulfonated tetrazolium salt as a chromogenic indicator for NADH as well as cell viability. Talanta 44: 1299-1305.
43. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
44. Johns TG, Luwor RB, Murone C, Walker F, Weinstock J, et al. (2003) Antitumor efficacy of cytotoxic drugs and the monoclonal antibody 806 is enhanced by the EGF receptor inhibitor AG1478. Proc Natl Acad Sci U S A 100: 15871-15876.