Islet amyloid polypeptide exerts a novel autocrine action in b-cell signaling and proliferation

FASEB Journal

Volumn 29, Issue 7, 2015, Pages 2970-2979

  Visa, Montse ^a,b   Alcarraz Viźan, Gema ^a,b   Montane, Joel ^a,b   Cadavez, Lisa ^a,b   Castaño, Carlos ^a,b   Villanueva Peñacarrillo, Maŕia Luisa ^b,c   Servitja, Joan Marc ^a,b   Novials, Anna ^a,b  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c 28400 Madrid   (Spain)

Author keywords

Akt; Amylin; Erk1 2; Pancreatic islets; Type 2 diabetes

Indexed keywords

AMYLIN; AMYLIN RECEPTOR; CALCITONIN[8-32][30 ASPARAGINE 32 TYROSINAMIDE]; GLUCOSE; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN KINASE B; RECEPTOR ACTIVITY MODIFYING PROTEIN 1; RECEPTOR ACTIVITY MODIFYING PROTEIN 2; RECEPTOR ACTIVITY MODIFYING PROTEIN 3; PEPTIDE FRAGMENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOCRINE EFFECT; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; INSULIN BLOOD LEVEL; INSULIN RELEASE; MALE; MIN6 CELL LINE; MITOGENESIS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL LINE; CYTOLOGY; DRUG EFFECTS; HUMAN; METABOLISM;

MURINAE;

ANIMALS; AUTOCRINE COMMUNICATION; CELL LINE; CELL PROLIFERATION; GLUCOSE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; ISLET AMYLOID POLYPEPTIDE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, ISLET AMYLOID POLYPEPTIDE;

EID: 84940383982     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-270553     Document Type: Article

References (51)

1. Kahn, S. E., D'Alessio, D. A., Schwartz, M. W., Fujimoto, W. Y., Ensinck, J. W., Taborsky Jr., G. J., and Porte, Jr. D. (1990) Evidence of cosecretion of islet amyloid polypeptide and insulin by beta-cells. Diabetes 39, 634-638.
2. Moore, C. X., and Cooper, G. J. (1991) Co-secretion of amylin and insulin from cultured islet beta-cells: modulation by nutrient secretagogues, islet hormones and hypoglycemic agents. Biochem. Biophys. Res. Commun. 179, 1-9.
3. Wookey, P. J., Lutz, T.A., andAndrikopoulos, S. (2006)Amylininthe periphery II: An updated mini-review. Scientific World Journal 6, 1642-1655.
4. Lorenzo, A., Razzaboni, B., Weir, G. C., and Yankner, B. A. (1994) Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature 368, 756-760.
5. Hull, R. L., Westermark, G. T., Westermark, P., and Kahn, S. E. (2004) Islet amyloid: A critical entity in the pathogenesis of type 2 diabetes. J. Clin. Endocrinol. Metab. 89, 3629-3643.
6. Jurgens, C. A., Toukatly, M. N., Fligner, C. L., Udayasankar, J., Subramanian, S. L., Zraika, S., Aston-Mourney, K., Carr, D. B., Westermark, P., Westermark, G. T., Kahn, S. E., and Hull, R. L. (2011) b-cell loss and b-cell apoptosis in human type 2 diabetes are related to islet amyloid deposition. Am. J. Pathol. 178, 2632-2640.
7. Casas, S., Gomis, R., Gribble, F. M., Altirriba, J., Knuutila, S., and Novials, A. (2007) Impairment of the ubiquitin-proteasome pathway is a downstream endoplasmic reticulum stress response induced by extracellular human islet amyloid polypeptide and contributes to pancreatic beta-cell apoptosis. Diabetes 56, 2284-2294.
8. Huang, C. J., Lin, C. Y., Haataja, L., Gurlo, T., Butler, A. E., Rizza, R. A., and Butler, P. C. (2007) High expression rates of human islet amyloid polypeptide induce endoplasmic reticulumstressmediated beta-cell apoptosis, a characteristic of humans with type 2 but not type 1 diabetes. Diabetes 56, 2016-2027.
9. Zraika, S., Hull, R. L., Udayasankar, J., Aston-Mourney, K., Subramanian, S. L., Kisilevsky, R., Szarek, W. A., and Kahn, S. E. (2009) Oxidative stress is induced by islet amyloid formation and time-dependently mediates amyloid-induced beta cell apoptosis. Diabetologia 52, 626-635.
10. Westwell-Roper, C. Y., Ehses, J. A., and Verchere, C. B. (2014) Resident macrophages mediate islet amyloid polypeptide-induced islet IL-1b production and b-cell dysfunction. Diabetes 63, 1698-1711.
11. Alcarraz-Vizan, G., Casini, P., Cadavez, L., Visa, M., Montane, J., Servitja, J. M., and Novials, A. (2015) Inhibition of BACE2 counteracts hIAPP-induced insulin secretory defects in pancreatic b-cells. FASEB J. 29, 95-104.
12. Poyner, D. R., Sexton, P. M., Marshall, I., Smith, D. M., Quirion, R., Born, W., Muff, R., Fischer, J. A., and Foord, S. M. (2002) International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol. Rev. 54, 233-246.
13. Hay, D. L., Christopoulos, G., Christopoulos, A., and Sexton, P. M. (2004) Amylin receptors: molecular composition and pharmacology. Biochem. Soc. Trans. 32, 865-867.
14. Lutz, T.A. (2012)Control of energy homeostasis by amylin. Cell. Mol. Life Sci. 69, 1947-1965.
15. Reidelberger, R. D., Arnelo, U., Granqvist, L., and Permert, J. (2001) Comparative effects of amylin and cholecystokinin on food intake and gastric emptying in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R605-R611.
16. Gedulin, B. R., Jodka, C.M., Herrmann, K., and Young, A. A. (2006) Role of endogenous amylin in glucagon secretion and gastric emptying in rats demonstrated with the selective antagonist, AC187. Regul. Pept. 137, 121-127.
17. Ciaraldi, T. P., Goldberg, M., Odom, R., and Stolpe, M. (1992) In vitro effects of amylin on carbohydrate metabolism in liver cells. Diabetes 41, 975-981.
18. Cooper, G. J., Leighton, B., Dimitriadis, G. D., Parry-Billings, M., Kowalchuk, J. M., Howland, K., Rothbard, J. B., Willis, A.C., and Reid, K. B. (1988) Amylin found in amyloid deposits in human type 2 diabetes mellitus may be a hormone that regulates glycogen metabolismin skeletal muscle. Proc.Natl. Acad. Sci.USA 85, 7763-7766.
19. Moreno, P., Acitores, A., Gutíerrez-Rojas, I., Nuche-Berenguer, B., El Assar, M., Rodriguez-Mañas, L., Gomis, R., Valverde, I., Visa, M., Malaisse, W. J., Novials, A., González, N., andVillanueva-Peñacarrillo, M. L. (2011) Amylin effect in extrapancreatic tissues participating in glucose homeostasis, in normal, insulin-resistant and type 2 diabetic state. Peptides 32, 2077-2085.
20. Akesson, B., Panagiotidis, G., Westermark, P., and Lundquist, I. (2003) Islet amyloidpolypeptide inhibits glucagonrelease andexerts a dual action on insulin release from isolated islets. Regul. Pept. 111, 55-60.
21. Ohsawa, H., Kanatsuka, A., Yamaguchi, T., Makino, H., and Yoshida, S. (1989) Islet amyloid polypeptide inhibits glucose-stimulated insulin secretion from isolated rat pancreatic islets. Biochem. Biophys. Res. Commun. 160, 961-967.
22. Salas, M., Silvestre, R. A., Garcia-Hermida, O., Fontela, T., Rodriguez-Gallardo, J., and Marco, J. (1995) Inhibitory effect of amylin (islet amyloid polypeptide) on insulin response to non-glucose stimuli. Study in perfused rat pancreas. Diabete Metab. 21, 269-273.
23. Gill, A. M., and Yen, T. T. (1991) Effects of ciglitazone on endogenous plasma islet amyloid polypeptide and insulin sensitivity in obese-diabetic viable yellow mice. Life Sci. 48, 703-710.
24. Huang, H. J., Young, A.A., Koda, J.E., Tulp, O.L., Johnson, M. J., and Cooper, G. J. (1992) Hyperamylinemia, hyperinsulinemia, and insulin resistance in genetically obese LA/N-cp rats. Hypertension 19 (1 Suppl), I101-I109.
25. Leckström, A., Lundquist, I., Ma, Z., andWestermark, P. (1999) Islet amyloid polypeptide and insulin relationship in a longitudinal study of the genetically obese (ob/ob) mouse. Pancreas 18, 266-273.
26. Gebre-Medhin, S., Mulder, H., Pekny, M., Westermark, G., Törnell, J., Westermark, P., Sundler, F., Ahŕen, B., and Betsholtz, C. (1998) Increased insulin secretion and glucose tolerance in mice lacking islet amyloid polypeptide (amylin). Biochem. Biophys. Res. Commun. 250, 271-277.
27. Wang, Z.L., Bennet, W.M., Ghatei, M.A., Byfield, P.G., Smith, D.M., and Bloom, S. R. (1993) Influence of islet amyloid polypeptide and the 8-37 fragment of islet amyloid polypeptide on insulin release from perifused rat islets. Diabetes 42, 330-335.
28. Bennet, W. M., Beis, C. S., Ghatei, M. A., Byfield, P. G., and Bloom, S. R. (1994) Amylin tonally regulates arginine-stimulated insulin secretion in rats. Diabetologia 37, 436-438.
29. Mather, K. J., Paradisi, G., Leaming, R., Hook, G., Steinberg, H. O., Fineberg, N., Hanley, R., and Baron, A. D. (2002)Role of amylin in insulin secretion and action in humans: Antagonist studies across the spectrum of insulin sensitivity. Diabetes Metab. Res. Rev. 18, 118-126.
30. Cornish, J., Grey, A., Callon, K. E., Naot, D., Hill, B. L., Lin, C. Q., Balchin, L. M., and Reid, I. R. (2004) Shared pathways of osteoblast mitogenesis inducedbyamylin, adrenomedullin, and IGF-1. Biochem. Biophys. Res. Commun. 318, 240-246.
31. Harris, P. J., Cooper, M. E., Hiranyachattada, S., Berka, J. L., Kelly, D. J., Nobes, M., andWookey, P. J. (1997)Amylinstimulates proximal tubular sodiumtransport and cell proliferation in the rat kidney. Am. J. Physiol. 272, F13-F21.
32. Datta, H., Rafter, P., Chen, Z., Wimalawansa, S., and Macintyre, I. (1990) Amylin-amide displays a proliferative effect on human umbilical vein endothelial cells. Biochem. Soc. Trans. 18, 1276.
33. Karlsson, E., and Sandler, S. (2001) Islet amyloid polypeptide promotes beta-cell proliferation in neonatal rat pancreatic islets. Diabetologia 44, 1015-1018.
34. Wookey, P. J., Xuereb, L., Tikellis, C., and Cooper, M. E. (2003) Amylin in the periphery. Scientific World Journal 3, 163-175.
35. Mulder, H., Gebre-Medhin, S., Betsholtz, C., Sundler, F., and Ahŕen, B. (2000) Islet amyloid polypeptide (amylin)-deficientmice develop a more severe form of alloxan-induced diabetes. Am. J. Physiol. Endocrinol. Metab. 278, E684-E691.
36. Bernal-Mizrachi, E., Wen, W., Stahlhut, S., Welling, C. M., and Permutt, M.A. (2001) Isletbetacell expressionof constitutively active Akt1/PKB alpha induces striking hypertrophy, hyperplasia, and hyperinsulinemia. J. Clin. Invest. 108, 1631-1638.
37. Fatrai, S., Elghazi, L., Balcazar, N., Cras-Méneur, C., Krits, I., Kiyokawa, H., and Bernal-Mizrachi, E. (2006) Akt induces beta-cell proliferation by regulating cyclin D1, cyclin D2, and p21 levels and cyclin-dependent kinase-4 activity. Diabetes 55, 318-325.
38. Costes, S., Broca, C., Bertrand, G., Lajoix, A.D., Bataille, D., Bockaert, J., and Dalle, S. (2006) ERK1/2 control phosphorylation andprotein level of cAMP-responsive element-binding protein: A key role in glucose-mediated pancreatic beta-cell survival. Diabetes 55, 2220-2230.
39. Wijesekara, N., Krishnamurthy, M., Bhattacharjee, A., Suhail, A., Sweeney, G., and Wheeler, M. B. (2010) Adiponectin-induced ERK and Akt phosphorylation protects against pancreatic beta cell apoptosis and increases insulin gene expression and secretion. J. Biol. Chem. 285, 33623-33631.
40. Moreno-Asso, A., Castaño, C., Grilli, A., Novials, A., and Servitja, J. M. (2013)Glucose regulationof a cell cyclegenemodule is selectively lost in mouse pancreatic islets during ageing. Diabetologia 56, 1761-1772.
41. Bonner-Weir, S., Deery, D., Leahy, J. L., and Weir, G. C. (1989) Compensatory growth of pancreatic beta-cells in adult rats after short-term glucose infusion. Diabetes 38, 49-53.
42. Porat, S., Weinberg-Corem, N., Tornovsky-Babaey, S., Schyr-Ben-Haroush, R., Hija, A., Stolovich-Rain, M., Dadon, D., Granot, Z., Ben-Hur, V., White, P., Girard, C. A., Karni, R., Kaestner, K.H., Ashcroft, F.M., Magnuson, M.A., Saada, A., Grimsby, J., Glaser, B., and Dor, Y. (2011) Control of pancreatic b cell regeneration by glucose metabolism. Cell Metab. 13, 440-449.
43. Assmann, A., Ueki, K., Winnay, J. N., Kadowaki, T., and Kulkarni, R. N. (2009) Glucose effects on beta-cell growth and survival require activation of insulin receptors and insulin receptor substrate 2. Mol. Cell. Biol. 29, 3219-3228.
44. Hay, D. L., Christopoulos, G., Christopoulos, A., Poyner, D. R., and Sexton, P. M. (2005) Pharmacological discrimination of calcitonin receptor: receptor activity-modifying protein complexes. Mol. Pharmacol. 67, 1655-1665.
45. Kulkarni, R. N., Bruning, J. C., Winnay, J. N., Postic, C., Magnuson, M.A., and Kahn, C. R. (1999)Tissue-specific knockout of the insulin receptor in pancreatic beta cells creates an insulin secretory defect similar to that in type 2 diabetes. Cell 96, 329-339.
46. Okada, T., Liew, C.W., Hu, J., Hinault, C., Michael, M. D., Krtzfeldt, J., Yin, C., Holzenberger, M., Stoffel, M., and Kulkarni, R. N. (2007) Insulin receptors in beta-cells are critical for islet compensatory growth response to insulin resistance. Proc. Natl. Acad. Sci. USA 104, 8977-8982.
47. Leibiger, I. B., Leibiger, B., and Berggren, P. O. (2008) Insulin signaling in the pancreatic beta-cell. Annu. Rev. Nutr. 28, 233-251.
48. Wang, M., Li, J., Lim, G. E., and Johnson, J. D. (2013) Is dynamic autocrine insulin signaling possible? Amathematicalmodel predicts picomolar concentrations of extracellularmonomeric insulin within human pancreatic islets. PLoS One 8, e64860.
49. Fucini, R. V., Okada, S., and Pessin, J. E. (1999) Insulin-induced desensitization of extracellular signal-regulated kinase activation results from an inhibition of Raf activity independent of Ras activation and dissociation of the Grb2-SOS complex. J. Biol. Chem. 274, 18651-18658.
50. Broderick, C. L., Brooke, G. S., DiMarchi, R.D., and Gold, G. (1991) Humanandrat amylinhave noeffectsoninsulin secretioninisolated rat pancreatic islets. Biochem. Biophys. Res. Commun. 177, 932-938.
51. Nagamatsu, S., Carroll, R. J., Grodsky, G.M., and Steiner, D. F. (1990) Lack of islet amyloid polypeptide regulationof insulinbiosynthesis or secretion in normal rat islets. Diabetes 39, 871-874.