Amylin exerts osteogenic actions with different efficacy depending on the diabetic status

Molecular and Cellular Endocrinology

Volumn 365, Issue 2, 2013, Pages 309-315

  Gutierrez Rojas I ^a,c   Lozano, D ^a,c,d   Nuche Berenguer, B ^a,c   Moreno, P ^a,c   Acitores, A ^a,c   Ramos alvarez I ^a,c   Rovira, A ^a,c   Novials, A ^b,c   Martin Crespo E ^a,c   Villanueva Penacarrillo M L ^a,c   Esbrit, P ^a,c  

^a UAM)   (Spain)

^b HOSPITAL CLÍNIC   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

Author keywords

Amylin; Bone; Diabetes; Insulin resistance

Indexed keywords

AMYLIN; FRUCTOSE; MESSENGER RNA; OSTEOCALCIN; OSTEOPROTEGERIN; PARATHYROID HORMONE; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MASS; CONTROLLED STUDY; GENE; GENE EXPRESSION REGULATION; HYPERINSULINEMIA; INSULIN RESISTANCE; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSSIFICATION; OSTEOCLASTOGENESIS; OSTEOPROTEGERIN GENE; PARATHYROID HORMONE BLOOD LEVEL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B GENE; STREPTOZOCIN DIABETES; STRUCTURE ANALYSIS; SURFACE PROPERTY; TRABECULAR BONE;

ANIMALS; BONE DENSITY CONSERVATION AGENTS; BONE DISEASES, METABOLIC; DIABETES COMPLICATIONS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; FEMUR; GENE EXPRESSION; ISLET AMYLOID POLYPEPTIDE; MALE; OSTEOCALCIN; OSTEOGENESIS; OSTEOPROTEGERIN; RANK LIGAND; RATS; RATS, WISTAR; TIBIA;

EID: 84871363877     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.11.013     Document Type: Article

References (56)

1. Alam A.S., Moonga B.S., Bevis P.J., Huang C.L., Zaidi M. Amylin inhibits bone resorption by a direct effect on the motility of rat osteoclasts. Exp. Physiol. 1993, 78:183-196.
2. Arnés L., González N., Tornero-Esteban P., Sancho V., Acitores A., Valverde I., Delgado E., Villanueva-Peñacarrillo M.L. Characteristics of the GLP-1 and exendins action upon glucose transport and metabolism in type 2 diabetic rat skeletal muscle. Int. J. Mol. Med. 2008, 22:127-132.
3. Asmar M., Bache M., Knop F.K., Madsbad S., Holst J.J. Do the actions of glucagon -like peptide-1 on gastric emptying, appetite, and food intake involve release of amylin in humans?. J. Clin. Endocrinol. Metab. 2010, 95:2367-2375.
4. Barth S.W., Riediger T., Lutz T.A., Rechkemmer G. Differential effects of amylin and salmon calcitonin on neuropeptide gene expression in the lateral hypothalamic area and the arcuate nucleus of the rat. Neurosci. Lett. 2003, 341:131-134.
5. Bello N.T., Kemm M.H., Ofeldt E.M., Moran T.H. Dose combinations of esendine-4 and salmon calcitonin produce additive and synergistic reductions in food intake in nonhuman primates. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:945-952.
6. Blakytny R., Spraul M., Jude E.B. The diabetic bone: a cellular and molecular perspective. Int. J. Low. Extrem. Wounds 2011, 10:16-32.
7. Boyle W.J., Simonet W.S., Lacey D.L. Osteoclast differentiation and activation. Nature 2003, 423:337-342.
8. Bronsky J., Prusa R. Amylin fasting plasma levels are decreased in patients with osteoporosis. Osteoporosis Int. 2004, 15:243-247.
9. Cancelas J., Prieto P.G., Garcia-Arevalo M., Sancho V., Villanueva-Peñacarrillo M.L., Malaisse W.J., et al. Induction and reversibility of insulin resistance in rats exposed to exogenous d-fructose. Horm. Metab. Res. 2008, 40:459-466.
10. Christopoulos G., Perry K.J., Morfis M., Tilakaratne N., Gao Y., Fraser N.J., Main M.J., Foord S.M., Sexton P.M. Multiple amylin receptors arise from receptor activity-modifying protein interaction with the calcitonin receptor gene product. Mol. Pharmacol. 1999, 56:235-242.
11. Clowes J.A., Khosla S., Eastell R. Perspective potential role of pancreatic and enteric hormones in regulating bone turnover. J. Bone Miner. Res. 2005, 9:1497-1506.
12. Compston J.E. Skeletal actions of intermittent parathyroid hormone: effects on bone remodelling and structure. Bone 2007, 6:1447-1452.
13. Cooper G.J.S. Amylin compared with calcitonin gene-related peptide: structure, biology, and relevance to metabolic disease. Endocr. Rev. 1994, 15:163-201.
14. Cornish J., Callon K.E., Cooper G.J.S., Reid I.R. Amylin stimulates osteoblast proliferation and increases mineralized bone volume in adult mice. Biochem. Biophys. Res. Commun. 1995, 207:133-139.
15. Cornish J., Callon K.E., King A.R., Cooper G.J.S., Reid I.R. Systemic administration of amylin increases bone mass, linear growth, and adiposity in adult male mice. Am. J. Physiol. Endocrinol. Metab. 1998, 275:E694-E699.
16. Cornish J., Callon K.E., Lin C.Q., Xiao C.L., Mulvey T.B., Coy D.H., Cooper G.J., Reid I.R. Dissociation of the effects of amylin on osteoblast proliferation and bone resorption. Am. J. Physiol. Endocrinol. Metab. 1998, 274:E827-E833.
17. Cornish J., Callon K.E., Gasser J.A., Bava U., Gardiner E.M., Coy D.H., Cooper G.J.S., Reid I.R. Systemic administration of a novel octapeptide, amylin-(1-8), increases bone volume in male mice. Am. J. Physiol. Endocrinol. Metab. 2000, 279:E730-E735.
18. Cornish J., Callon K.E., Bava U., Kamona S.A., Cooper G.J., Reid I.R. Effects of calcitonin, amylin, and calcitonin gene-related peptide on osteoclast development. Bone 2001, 29:162-168.
19. Cornish J., Grey A., Callon K.E., Naot D., Hill B.L., Lin C.Q., Balchin L.M., Reid I.R. Shared pathways of osteoblast mitogenesis induced by amylin, adrenomedullin, and IGF-1. Biochem. Biophys. Res. Commun. 2004, 318:240-246.
20. Creutzfeldt W. The entero-insular axis in type 2 diabetes. Incretins as therapeutic agents. Exp. Clin. Endocrinol. Diabetes 2001, 109:S288-S303.
21. Dacquin R., Davey R.A., Laplace C., Levasseur R., Morris H.A., Goldring S.R., Gebre-Medhin S., Galson D.L., Zajac J.D., Karsenty G. Amylin inhibits bone resorption while the calcitonin receptor controls bone formation in vivo. J. Cell. Biol. 2004, 164:509-514.
22. Dunican K.C., Adams N.M., Desilets A.R. The role of pramlintide for weight loss. Ann. Pharmacother. 2010, 44:538-545.
23. Ellegaard M., Thorkildsen C., Petersen J.S., Jorgensen N.R., Just R., Schwarz P., Ramirez M.T., Stahlhut M. Amylin (1-8) is devoid of anabolic activity in bone. Calcif. Tissue Int. 2010, 86:249-260.
24. Fujii H., Hamada Y., Fukagawa M. Bone formation in spontaneously diabetic Torii-newly established model of nonobese type 2 diabetes rats. Bone 2008, 42:372-379.
25. Herbert V., Lau K.S., Goltlieb C.W., Bleicher S.J. Coated charcoal inmunoassay of insulin. J. Clin. Invest. 1956, 25:1375-1384.
26. Horcajada-Molteni M.N., Chanteranne B., Lebecque P., Davicco M.J., Coxam V., Young A., Barlet J.P. Amylin and bone metabolism in streptozotocin-induced diabetic rats. J. Bone. Miner. Res. 2001, 16:958-965.
27. Iwase M., Kikuchi M., Nunoi K., Wakisaka M., Maki Y., Sadoshima S., Fujishima M. Blood pressure changes in spontaneously hypertensive and normotensive rats with neonatal streptozotocin induced type 2 diabetes. Clin. Exp. Hypertens. A. 1987, 9:2157-2168.
28. Kahn S.E., D́Alessio D.A., Schwartz M.W., Fujimoto W.Y., Ensinck J.W., Taborsky G.J., Porte D. Evidence of cosecretion of islet amyloid polypeptide and insulin by beta cells. Diabetes 1990, 39:634-638.
29. Kailasam M.T., Parmer R.J., Tyrell E.A., Henry R.R., O_Connor D.T. Circulating amylin in human essential hypertension: heritability and early increase in individuals at genetic risk. J. Hypertens. 2000, 18:1611-1620.
30. Khazai N.B., Beck G.R., Umpierrez G.E. Diabetes and fractures: an overshadowed association. Curr. Opin. Endocrinol. Diabetes Obes. 2009, 16:435-445.
31. Kowalczyk R., Harris P.W.R., Brimble M.A., Callon K.E., Watson M., Cornish J. Synthesis and evaluation of disulfide bond mimetics of amylin-(1-8) as agents to treat osteoporosis. Bioorgan. Med. Chem. 2012, 20:2661-2668.
32. Lebovitz H.E. Adjunct therapy for type 1 diabetes mellitus. Nat. Rev. Endocrinol. 2010, 6:324-326.
33. Lutz T.A. Pancreatic amylin as a centrally acting satiating hormone. Curr. Drug. Target 2005, 6:181-189.
34. Makimattila S., Fineman M.S., Yki-Jarvinen H. Deficiency of total and nonglycosylated amylin in plasma characterizes subjects with impaired glucose tolerance and type 2 diabetes. J. Clin. Endocrinol. Metab. 2000, 85:2822-2827.
35. Moreno P., Acitores A., Gutiérrez-Rojas I., Nuche-Berenguer B., El Assar M., Rodriguez-Mañas L., Gomis R., Valverde I., Visa M., Malaisse W.J., Novials A., González N., Villanueva-Peñacarrillo M.L. Amylin effect in extrapancreatic tissues participating in glucose homeostasis, in normal, insulin-resistant and type 2 diabetic state. Peptides 2011, 32:2077-2085.
36. Novials A., Sarri Y., Casamitjana R., Rivera F., Gomis R. Regulation of islet amyloid polypeptide in human pancreatic islets. Diabetes 1993, 42:1514-1519.
37. Nuche-Berenguer B., Moreno P., Esbrit P., Dapía S., Caeiro J.R., Cancelas J., Haro-Mora J.J., Villanueva-Peñacarrillo M.L. Effect of GLP-1 treatment on bone turnover in normal, type 2 diabetic, and insulin-resistant states. Calcif. Tissue. Int. 2009, 84:453-461.
38. Nuche-Berenguer B., Moreno P., Portal-Nuñez S., Dapía S., Esbrit P., Villanueva-Peñacarrillo M.L. Exendin-4 exerts osteogenic actions in insulin-resistant and type 2 diabetic states. Regul. Pept. 2010, 159:61-66.
39. Nuche-Berenguer B., Lozano D., Gutiérrez-Rojas I., Moreno P., Mariñoso María.L., Esbrit P., Villanueva-Peñacarrillo M.L. GLP-1 and exendine-4 can reverse hyperlipidic-related osteopenia. J. Endocrinol. 2011, 209:203-210.
40. Osaka T., Tsukamoto A., Koyama Y., Inoue S. Central and peripheral administration of amylin induces energy expenditure in anesthetized rats. Peptides 2008, 29:1028-1035.
41. Parfitt A.M., Drezner M.K., Glorieux F.H., Kanis J.A., Malluche H., Meunier P.J., Ott S.M., Recker R.R. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR histomorphometry nomenclature committee. J. Bone Miner. Res. 1987, 2:595-610.
42. Portha B., Picon L., Rosselin G. Chemical diabetes in the adult rat as the spontaneous evolution of neonatal diabetes. Diabetologia 1979, 17:371-377.
43. Power R.A., Iwaniec U.T., Magee K.A., Mitova-Caneva N.G., Wronski T.J. Basic fibroblast growth factor has rapid bone anabolic effects in ovariectomized rats. Osteoporos. Int. 2004, 15:716-723.
44. Riediger T., Zued D., Becskei C., Lutz T.A. The anoretic hormone amylin contributes to feeding-related changes of neuronal activity in key structures of the gutbrain axis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286:R114-122.
45. Roth J.D., Roland B.L., Cole R.L., Trevaskis J.L., Weyer C., Koda J.E., Anderson C.M., Parkes D.G., Baron A.D. Leptin responsiveness restored by amylin agonism in diet-induced obesity: evidence from nonclinical and clinical studies. Proc. Natl. Acad. Sci. USA 2008, 105:7257-7262.
46. Roth J.D., Erickson M.R., Chen S., Parkes D.G. GLP-1R and amylin agonism in metabolic disease: complementary mechanisms and future opportunities. Br. J. Pharmacol. 2012, 166:121-136.
47. Saito M., Fujii K., Marumo K. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos. Int. 2006, 17:1514-1523.
48. Sancho V., Trigo M.V., González N., Valverde I., Malaisse W.J., Villanueva-Peñacarrillo M.L. Effects of GLP-1 and exendins on kinase activity, 2-deoxy-D-glucose transport, lipolysis and lipogenesis in adipocytes from normal and streptozotocin induced type 2 diabetic rats. J. Mol. Endocrinol. 2005, 35:27-38.
49. Suzuki K., Kurose T., Takizawa M., Maruyama M., Ushikawa K., Kikuyama M., Sugimoto C., Seino Y., Nagamatsu S., Ishida H. Osteoclastic function is accelerated in male patients with type 2 diabetes mellitus: the preventive role of osteoclastogenesis inhibitory factor/osteoprotegerin (OCIF/OPG) on the decrease of bone mineral density. Diabetes Res. Clin. Pr. 2005, 68:117-125.
50. Thrailkill K.M., Lumpkin C.K., Bunn R.C., Kemp S.F., Fowlkes J.L. Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am. J. Physiol. Endocrinol. Metab. 2005, 289:E735-E745.
51. Tobias J.H., Chou J.W., Chambers T.J. Opposite effects of insulin-like growth factor-I on the formation of trabecular and cortical bone in adult female rats. Endocrinology 1992, 131:2387-2392.
52. Valverde I., Barreto M., Malaisse W.J. Stimulation by d-glucose of protein biosynthesis in tumoral insulin-producing cells (RINm5F line). Endocrinology 1988, 122:1443-1448.
53. Valverde I., Morales M., Clemente F., López-Delgado M.I., Delgado E., Perea A., Villanueva-Peñacarrillo M.L. Glucagon-like peptide-1: a potent glycogenic hormone. FEBS Lett. 1994, 349:313-316.
54. Villa I., Rubinacci A., Ravasi F., Ferrara A.F., Guidobono F. Effects of amylin on human osteoblast-like cells. Peptides 1997, 18:537-540.
55. Weng H.B., Gu Q., Liu M., Cheng N.N., Li D., Gao X. Increased secretion and expression of amylin in spontaneously diabetic Goto-Kakizaki rats treated with rhGLP-1 (7-36). Acta Pharmacol. Sin. 2008, 29:573-579.
56. Young A.A., Gedulin B.R., Rink T.J. Dose-responses for the slowing of gastric emptying in a rodent model by glucagon-like peptide (7-36) NH2, amylin, cholecystokinin, and other possible regulators of nutrient uptake. Metabolism 1996, 45:1-3.