Hyperamylinemia contributes to cardiac dysfunction in obesity and diabetes: A study in humans and rats

Circulation Research

Volumn 110, Issue 4, 2012, Pages 598-608

  Despa, Sanda ^a   Margulies, Kenneth B ^b   Chen, Le ^a   Knowlton, Anne A ^a   Havel, Peter J ^c   Taegtmeyer, Heinrich ^d   Bers, Donald M ^a   Despa, Florin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

calcium; diabetic cardiomyopathy; HIP rat; hyperamylinemia; hyperinsulinemia; UCD T2DM rat

Indexed keywords

AMYLIN; CALCIUM ION; HISTONE DEACETYLASE; OLIGOMER; TRANSCRIPTION FACTOR NFAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; FIBER; HEART FAILURE; HEART FUNCTION; HEART MUSCLE; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HUMAN; HUMAN TISSUE; HYPERAMYLINEMIA; IMPAIRED GLUCOSE TOLERANCE; MORPHOLOGY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SARCOLEMMA;

ADULT; AGED; ANIMALS; BLOTTING, WESTERN; CALCIUM SIGNALING; CARDIOMEGALY; DIABETES MELLITUS, TYPE 2; DIABETIC CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; FEMALE; HEART FAILURE; HISTONE DEACETYLASES; HUMANS; IMMUNOHISTOCHEMISTRY; ISLET AMYLOID POLYPEPTIDE; MALE; MIDDLE AGED; MYOCARDIUM; NFATC TRANSCRIPTION FACTORS; OBESITY; PREDIABETIC STATE; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT; VENTRICULAR PRESSURE; VENTRICULAR REMODELING; YOUNG ADULT;

EID: 84862792335     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.258285     Document Type: Article

References (52)

1. Biddinger SB, Kahn CR. From mice to men: insights into the insulin resistance syndromes. Annu Rev Physiol. 2006;68:123-158.
2. Lopaschuk GD, Ussher JR, Folmes CD, Jaswal JS, Stanley WC. Myocardial fatty acid metabolism in health and disease. Physiol Rev. 2010;90:207-258.
3. Reaven GM. Relationships among insulin resistance, type 2 diabetes, essential hypertension, and cardiovascular disease: similarities and differences. J Clin Hypertens. 2011;13:238-243.
4. Battiprolu PK, Gillette TG, Wang ZV, Lavandero S, Hill JA. Diabetic cardiomyopathy: mechanisms and therapeutic targets. Drug Discov Today Dis Mech. 2010;7:e135-e143.
5. Guha A, Harmancey R, Taegtmeyer H. Nonischemic heart failure in diabetes mellitus. Curr Opin Cardiol. 2008;23:241-248.
6. Boudina S, Abel ED. Diabetic cardiomyopathy, causes and effects. Rev Endocr Metab Disord. 2010;11:31-39.
7. Lebeche D, Davidoff AJ, Hajjar RJ. Interplay between impaired calcium regulation and insulin signaling abnormalities in diabetic cardiomyopathy. Nat Clin Pract Cardiovasc Med. 2008;5:715-724.
8. Young LH. Diet-induced obesity obstructs insulin signaling in the heart. Am J Physiol Heart Circ Physiol. 2010;298:H306-H307.
9. Swan JW, Anker SD, Walton C, Godsland IF, Clark AL, Leyva F, Stevenson JC, Coats AJ. Insulin resistance in chronic heart failure: relation to severity and etiology of heart failure. J Am Coll Cardiol. 1997;30:527-532.
10. Ashrith G, Algahim MF, Taegtmeyer H. Insulin resistance: marker or mediator? Am J Med. 2009;122:e13-e15.
11. Utriainen T, Takala T, Luotolahti M, Ronnemaa T, Laine H, Ruotsalainen U, Haaparanta M, Nuutila P, Yki-Jarvien H. Insulin resistance characterizes glucose uptake in skeletal muscle but not in the heart in NIDDM. Diabetologia. 1998;41:555-559.
12. Jagasia D, Whiting JM, Concato J, Pfau S, McNulty PH. Effect of non-insulin-dependent diabetes mellitus on myocardial insulin responsiveness in patients with ischemic heart disease. Circulation. 2001;103:1734-1739.
13. Johnson KH, O'Brien TD, Jordan K, Westermark P. Impaired glucose tolerance is associated with increased islet amyloid polypeptide (IAPP) immunoreactivity in pancreatic beta cells. Am J Pathol. 1989;135:245-250.
14. Johnson KH, O'Brien TD, Betsholtz C, Westermark P. Islet amyloid, islet amyloid polypeptide and diabetes mellitus. N Engl J Med. 1989;321:513-518.
15. Enoki S. Mitsukawa T, Takemura J, Nakazato M, Aburaya J, Toshimori H, Matsukara S. Plasma islet amyloid polypeptide levels in obesity, impaired glucose tolerance and non-insulin-dependent diabetes mellitus. Diabetes Res Clin Pract. 1992;15:97-102.
16. Gong W, Liu ZH, Zeng CH, Peng A, Chen HP, Zhou H, Li LS. Amylin deposition in the kidney of patients with diabetic nephropathy. Kidney Int. 2007;72:213-218.
17. Despa S, Chen L, Cummings B, Havel PJ, Margulies KB, Knowlton AA, Bers DM, Despa F. Cardiac consequences of increased amylin secretion in diabetics. Circulation. 2009;120:S457.
18. Despa S, Bers DM, Despa F. Accumulation of islet amyloid polypetide (IAPP) oligomers in the heart in type 2 diabetes alters Ca cycling in myocytes. Circulation. 2010;122:A18345.
19. Colby DW, Prusiner SB. Prions. Cold Spring Harb Perspect Biol. 2011;3:1-22.
20. Haass C, Selkoe DJ. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol. 2007;8:101-112.
21. Janson J, Ashley RH, Harrison D, McIntyre S, Butler PC. The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles. Diabetes. 1999;48:491-498.
22. Engel MF, Khemtémourian L, Kleijer CC, Meeldijk HJ, Jacobs J, Verkleij AJ, de Kruijff B, Killian JA, Höppener JW. Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane. Proc Natl Acad Sci U S A. 2008;105:6033-6038.
23. Anguiano M, Nowak RJ, Lansbury PT Jr. Protofibrillar islet amyloid polypeptide permeabilizes synthetic vesicles by a pore-like mechanism that may be relevant to type II diabetes. Biochemistry. 2002;41:11338-11343.
24. Mattson MP, Goodman Y. Different amyloidogenic peptides share a similar mechanism of neurotoxicity involving reactive oxygen species and calcium. Brain Res. 1995;676:219-224.
25. Kawahara M, Kuroda Y, Arispe N, Rojas E. Alzheimer's beta-amyloid, human islet amylin, and prion protein fragment evoke intracellular free calcium elevations by a common mechanism in a hypothalamic GnRH neuronal cell line. J Biol Chem. 2000;275:14077-14083.
26. Casas S, Novials A, Reimann F, Gomis R, Gribble FM. Calcium elevation in mouse pancreatic beta cells evoked by extracellular human islet amyloid polypeptide involves activation of the mechanosensitive ion channel TRPV4. Diabetologia. 2008;51:2252-2262.
27. Pattison JS, Sanbe A, Maloyan A, Osinska H, Klevitsky R, Robbins J. Cardiomyocyte expression of a polyglutamine preamyloid oligomer causes heart failure. Circulation. 2008;117:2743-2751.
28. Gianni D, Li A, Tesco G, McKay KM, Moore J, Raygor K, Rota M, Gwathmey JK, Dec. GW, Aretz T, Leri A, Semigran MJ, Anversa P, Macgillivray TE, Tanzi RE, Del Monte F. Protein aggregates and novel presenilin gene variants in idiopathic dilated cardiomyopathy. Circulation. 2010;121:1216-1226.
29. Westermark P, Engström U, Johnson KH, Westermark GT, Betsholtz C. Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation. Proc Natl Acad Sci U S A. 1990;87:5036-5040.
30. Matveyenko AV, Butler PC. Islet amyloid polypeptide (IAPP) transgenic rodents as models for type 2 diabetes. ILAR J. 2006;47:225-233.
31. Matveyenko AV, Butler PC. β-cell deficit due to increased apoptosis in the human islet amyloid polypeptide transgenic (HIP) rat recapitulates the metabolic defects present in type 2 diabetes. Diabetes. 2006;55:2106-2114.
32. Cummings BP, Digitale EK, Stanhope KL, Graham JL, Baskin DG, Reed BJ, Sweet IR, Griffen SC, Havel PJ. Development and characterization of a novel rat model of type 2 diabetes mellitus: the UC Davis type 2 diabetes mellitus UCD-T2DM rat. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1782-R1793.
33. http://www.nlm.nih.gov/medlineplus/ency/article/000313.htm.
34. Despa S, Bers DM. Functional analysis of Na/K-ATPase isoform distribution in rat ventricular myocytes. Am J Physiol Cell Physiol. 2007;293:C321-C327.
35. Lin L, Kim SC, Wang Y, Gupta S, Davis B, Simon SI, Torre-Amione G, Knowlton AA. HSP60 in heart failure: abnormal distribution and role in cardiac myocyte apoptosis. Am J Physiol Heart Circ Physiol. 2007;293:H2238-H2247.
36. Walton JH, Berry RS, Despa F, Amyloid oligomer formation probed by water proton magnetic resonance spectroscopy. Biophys J. 2010;100:2302-2308.
37. Huang CJ, Gurlo T, Haataja L, Costes S, Daval M, Ryazantsev S, Wu X, Butler AE, Butler PC. Calcium-activated calpain-2 is a mediator of beta cell dysfunction and apoptosis in type 2 diabetes. J Biol Chem. 2010;285:339-348.
38. 2+-cycling proteins may underlie sarcoplasmic reticulum dysfunction in the diabetic heart. Diabetes. 2001;50:2133-2138.
39. Pereira L, Matthes J, Schuster I, Valdivia HH, Herzig S, Richard S, Gómez AM. Mechanisms of [Ca2+]i transient decrease in cardiomyopathy of db/db type 2 diabetic mice. Diabetes. 2006;55:608-615.
40. Bers DM. Calcium cycling and signaling in cardiac myocytes. Annu Rev Physiol. 2008;70:23-49.
41. Hill JA, Olson EN, Cardiac plasticity. N Engl J Med. 2008;358:1370-80.
42. Luchner A, Stevens TL, Borgeson DD, Redfield M, Wei CM, Porter JG, Burnett JC Jr. Differential atrial and ventricular expression of myocardial BNP during evolution of heart failure. Am J Physiol Heart Circ Physiol. 1998;274:H1684-H1689.
43. Ellmers LJ, Knowles JW, Kim HS, Smithies O, Maeda N, Cameron VA. Ventricular expression of natriuretic peptides in Npr1 (-/-) mice with cardiac hypertrophy and fibrosis. Am J Physiol Heart Circ Physiol. 2002;283:H707-H714.
44. Bell D, Schluter K-D, Zhou X-J, McDermott BJ, Piper HM. Hypertrophic effects of calcitonin gene related peptide (CGRP) and amylin on adult mammalian ventricular cardiomyocytes. J Mol Cell Cardiol. 1995;27:2433-2443.
45. Ionescu-Tirgoviste C, Despa F. Biophysical alteration of the secretory track in β-cells due to molecular overcrowding: the relevance for diabetes. Integr Biol (Camb). 2011;3:173-179.
46. Despa F. Endoplasmic reticulum overcrowding as a mechanism of beta-cell dysfunction in diabetes. Biophys J. 2010;98:1641-1648.
47. Falk RH, Dubrey SW. Amyloid heart disease. Prog Cardiovasc Dis. 2010;52:347-361.
48. Palladini G, Lavatelli F, Russo P, Perlini S, Perfetti V, Bosoni T, Obici L, Bradwell AR, D'Eril GM, Fogari R, Moratti R, Merlini G. Circulating amyloidogenic free light chains and serum N-terminal natriuretic peptide type B decrease simultaneously in association with improvement of survival in AL. Blood. 2006;107:3854-3858.
49. Liao R, Jain M, Teller P, Connors LH, Ngoy S, Skinner M, Falk RH, Apstein CS. Infusion of light chains from patients with cardiac amyloidosis causes diastolic dysfunction in isolated mouse hearts. Circulation. 2001;104:1594-1597.
50. Green KN, La Ferla FM. Linking calcium to abeta and Alzheimer's disease. Neuron. 2008;59:190-194.
51. Razeghi P, Young ME, Cockrill TC, Frazier OH, Taegtmeyer H. Downregulation of myocardial myocyte enhancer factor 2C and myocyte enhancer factor 2C-regulated gene expression in diabetic patients with nonischemic heart failure. Circulation. 2002;106:407-411.
52. Seward JB, Casaclang-Verzosa G. Infiltrative cardiovascular diseases: cardiomyopathies that look alike, J Am Coll Cardiol. 2010;55:1769-1779.