Exendin-4 attenuates adverse cardiac remodelling in streptozocin-induced diabetes via specific actions on infiltrating macrophages

Basic Research in Cardiology

Volumn 111, Issue 1, 2016, Pages 1-13

  Tate, Mitchel ^a   Robinson, Emma ^a   Green, Brian D ^b   McDermott, Barbara J ^a   Grieve, David J ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b School of Biological Sciences   (United Kingdom)

Author keywords

Cardiac remodelling; Experimental diabetes; Extracellular matrix; Glucagon like peptide 1; Inflammation

Indexed keywords

EXENDIN 4; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; HEMOGLOBIN A1C; INSULIN; STREPTOZOCIN; TRIACYLGLYCEROL; ANTIDIABETIC AGENT; PEPTIDE; VENOM;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE RELEASE; DIASTOLIC DYSFUNCTION; DISEASE CONTROL; DRUG RESPONSE; EXPERIMENTAL DIABETES MELLITUS; EXTRACELLULAR MATRIX; FIBROSING ALVEOLITIS; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HEART FIBROBLAST; HEART PROTECTION; HEMOGLOBIN BLOOD LEVEL; INSULIN METABOLISM; MACROPHAGE; MALE; MOUSE; MYOCARDITIS; NONHUMAN; PARACRINE SIGNALING; SIGNAL TRANSDUCTION; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; C57BL MOUSE; DRUG EFFECTS; FIBROBLAST; FLOW CYTOMETRY; HEART; IMMUNOHISTOCHEMISTRY; PATHOLOGY; POLYMERASE CHAIN REACTION;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; EXTRACELLULAR MATRIX; FIBROBLASTS; FLOW CYTOMETRY; HEART; HYPOGLYCEMIC AGENTS; IMMUNOHISTOCHEMISTRY; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; PEPTIDES; POLYMERASE CHAIN REACTION; VENOMS;

EID: 84947967555     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-015-0518-1     Document Type: Article

References (49)

1. Adachi H, Kondo T, Koh GY, Nagy A, Oike Y, Araki E (2011) Angptl4 deficiency decreases serum triglyceride levels in low-density lipoprotein receptor knockout mice and streptozotocin-induced diabetic mice. Biochem Biophys Res Commun 409:177–180. doi:10.1016/j.bbrc.2011.04.110
2. Arakawa M, Mita T, Azuma K, Ebato C, Goto H, Nomiyama T, Fujitani Y, Hirose T, Kawamori R, Watada H (2010) Inhibition of monocyte adhesion to endothelial cells and attenuation of atherosclerotic lesion by a glucagon-like peptide-1 receptor agonist, exendin-4. Diabetes 59:1030–1037. doi:10.2337/db09-1694
3. Barouch LA, Berkowitz DE, Harrison RW, O’Donnell CP, Hare JM (2003) Disruption of leptin signaling contributes to cardiac hypertrophy independently of body weight in mice. Circulation 108:754–759. doi:10.1161/01.CIR.0000083716.82622.FD
4. Bertoni AG, Hundley WG, Massing MW, Bonds DE, Burke GL, Goff DC (2004) Heart failure prevalence, incidence, and mortality in the elderly with diabetes. Diabetes Care 27:699–703. doi:10.2337/diacare.27.3.699
5. Bishop JR, Foley E, Lawrence R, Esko JD (2010) Insulin-dependent diabetes mellitus in mice does not alter liver heparan sulfate. J Biol Chem 285:14658–14662. doi:10.1074/jbc.M110.112391
6. Bose AK, Mocanu MM, Carr RD, Yellon DM (2005) Glucagon like peptide-1 is protective against myocardial ischemia/reperfusion injury when given either as a preconditioning mimetic or at reperfusion in an isolated rat heart model. Cardiovasc Drugs Ther 19:9–11. doi:10.2337/diabetes.54.1.146
7. Breyer MD, Bottinger E, Brosius FC III, Coffman TM, Harris RC, Heilig CW, Sharma K, for the AMDCC (2005) Mouse models of diabetic nephropathy. J Am Soc Nephrol 16:27–45. doi:10.1681/ASN.2004080648
8. Bugger H, Abel ED (2014) Molecular mechanisms of diabetic cardiomyopathy. Diabetologia 57:660–671. doi:10.1007/s00125-014-3171-6
9. Chaudhuri A, Ghanim H, Vora M, Sia CL, Korzeniewski K, Dhindsa S, Makdissi A, Dandona P (2011) Exenatide exerts a potent antiinflammatory effect. J Clin Endocrinol Metab 97:198–207. doi:10.1210/jc.2011-1508
10. de Simone G, Devereux RB, Chinali M, Lee ET, Galloway JM, Barac A, Panza JA, Howard BV (2010) Diabetes and incident heart failure in hypertensive and normotensive participants of the Strong Heart Study. J Hypertens 28:353–360. doi:10.1097/HJH.0b013e3283331169
11. Demeterco C, Hao E, Lee SH, Itkin-Ansari P, Levine F (2009) Adult human β-cell neogenesis? Diabetes Obes Metab 11:46–53. doi:10.1111/j.1463-1326.2009.01105.x
12. DeNicola M, Du J, Wang Z, Yano N, Zhang L, Wang Y, Qin G, Zhuang S, Zhao TC (2014) Stimulation of glucagon-like peptide-1 receptor through exendin-4 preserves myocardial performance and prevents cardiac remodeling in infarcted myocardium. Am J Physiol Endocrinol Metab 307:E630–E643. doi:10.1152/ajpendo.00109.2014
13. Di Bonito P, Moio N, Cavuto L, Covino G, Murena E, Scilla C, Turco S, Capaldo B, Sibilio G (2005) Early detection of diabetic cardiomyopathy: usefulness of tissue Doppler imaging. Diabet Med 22:1720–1725. doi:10.1111/j.1464-5491.2005.01685.x
14. Grieve DJ, Cassidy RS, Green BD (2009) Emerging cardiovascular actions of the incretin hormone glucagon-like peptide-1: potential therapeutic benefits beyond glycaemic control? Br J Pharmacol 157:1340–1351. doi:10.1111/j.1476-5381.2009.00376.x
15. Hausenloy D, Whittington H, Wynne A, Begum S, Theodorou L, Riksen N, Mocanu M, Yellon D (2013) Dipeptidyl peptidase-4 inhibitors and GLP-1 reduce myocardial infarct size in a glucose-dependent manner. Cardiovasc Diabetol 12:154. doi:10.1186/1475-2840-12-154
16. Heusch G, Libby P, Gersh B, Yellon D, Bohm M, Lopaschuk G, Opie L (2014) Cardiovascular remodelling in coronary artery disease and heart failure. Lancet 383:1933–1943. doi:10.1016/S0140-6736(14)60107-0
17. Hogan A, Gaoatswe G, Lynch L, Corrigan M, Woods C, O’Connell J, O’Shea D (2014) Glucagon-like peptide 1 analogue therapy directly modulates innate immune-mediated inflammation in individuals with type 2 diabetes mellitus. Diabetologia 57:781–784. doi:10.1007/s00125-013-3145-0
18. How OJ, Aasum E, Severson DL, Chan WY, Essop MF, Larsen TS (2006) Increased myocardial oxygen consumption reduces cardiac efficiency in diabetic mice. Diabetes 55:466–473. doi:10.2337/diabetes.55.02.06.db05-1164
19. Kania G, Blyszczuk P, Eriksson U (2009) Mechanisms of cardiac fibrosis in inflammatory heart disease. Trends Cardiovasc Med 19:247–252. doi:10.1016/j.tcm.2010.02.005
20. Katare RG, Caporali A, Oikawa A, Meloni M, Emanueli C, Madeddu P (2010) Vitamin B1 analog benfotiamine prevents diabetes-induced diastolic dysfunction and heart failure through Akt/Pim-1-mediated survival pathway. Circ Heart Fail 3:294–305. doi:10.1161/CIRCHEARTFAILURE.109.903450
21. Kolterman OG, Buse JB, Fineman MS, Gaines E, Heintz S, Bicsak TA, Taylor K, Kim D, Aisporna M, Wang Y, Baron AD (2003) Synthetic exendin-4 (exenatide) significantly reduces postprandial and fasting plasma glucose in subjects with type 2 diabetes. J Clin Endocrinol Metab 88:3082–3089. doi:10.1210/jc.2002-021545
22. Lee YS, Park MS, Choung JS, Kim SS, Oh HH, Choi CS, Ha SY, Kang Y, Kim Y, Jun HS (2012) Glucagon-like peptide-1 inhibits adipose tissue macrophage infiltration and inflammation in an obese mouse model of diabetes. Diabetologia 55:2456–2468. doi:10.1007/s00125-012-2592-3
23. Liu Q, Anderson C, Broyde A, Polizzi C, Fernandez R, Baron A, Parkes D (2010) Glucagon-like peptide-1 and the exenatide analogue AC3174 improve cardiac function, cardiac remodeling, and survival in rats with chronic heart failure. Cardiovasc Diabetol 9:76. doi:10.1186/1475-2840-9-76
24. Lu HY, Huang CY, Shih CM, Chang WH, Tsai CS, Lin FY, Shih CC (2015) Dipeptidyl peptidase-4 inhibitor decreases abdominal aortic aneurysm formation through GLP-1-dependent monocytic activity in mice. PLoS One 10:e0121077. doi:10.1371/journal.pone.0121077
25. Ma F, Li Y, Jia L, Han Y, Cheng J, Li H, Qi Y, Du J (2012) Macrophage-stimulated cardiac fibroblast production of IL-6 is essential for TGF β/Smad activation and cardiac fibrosis induced by angiotensin II. PLoS One 7:e35144. doi:10.1371/journal.pone.0035144
26. Matsubara J, Sugiyama S, Sugamura K, Nakamura T, Fujiwara Y, Akiyama E, Kurokawa H, Nozaki T, Ohba K, Konishi M, Maeda H, Izumiya Y, Kaikita K, Sumida H, Jinnouchi H, Matsui K, Kim-Mitsuyama S, Takeya M, Ogawa H (2012) A dipeptidyl peptidase-4 inhibitor, des-fluoro-sitagliptin, improves endothelial function and reduces atherosclerotic lesion formation in apolipoprotein E-deficient mice. J Am Coll Cardiol 59:265–276. doi:10.1016/j.jacc.2011.07.053
27. Miyanaga F, Ogawa Y, Ebihara K, Hidaka S, Tanaka T, Hayashi S, Masuzaki H, Nakao K (2003) Leptin as an adjunct of insulin therapy in insulin-deficient diabetes. Diabetologia 46:1329–1337. doi:10.1007/s00125-003-1193-6
28. Moberly S, Mather K, Berwick Z, Owen M, Goodwill A, Casalini E, Hutchins G, Green M, Ng Y, Considine R, Perry K, Chisholm R, Tune J (2013) Impaired cardiometabolic responses to glucagon-like peptide 1 in obesity and type 2 diabetes mellitus. Basic Res Cardiol 108:1–15. doi:10.1007/s00395-013-0365-x
29. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958–969. doi:10.1038/nri2448
30. Movahed MR, Hashemzadeh M, Mazen Jamal M (2005) Diabetes mellitus is a strong, independent risk for atrial fibrillation and flutter in addition to other cardiovascular disease. Int J Cardiol 105:315–318. doi:10.1016/j.ijcard.2005.02.050
31. Nikolaidis LA, Elahi D, Hentosz T, Doverspike A, Huerbin R, Zourelias L, Stolarski C, Shen YT, Shannon RP (2004) Recombinant glucagon-like peptide-1 increases myocardial glucose uptake and improves left ventricular performance in conscious dogs with pacing-induced dilated cardiomyopathy. Circulation 110:955–961. doi:10.1161/01.CIR.0000139339.85840.DD
32. Noyan-Ashraf MH, Momen MA, Ban K, Sadi AM, Zhou YQ, Riazi AM, Baggio LL, Henkelman RM, Husain M, Drucker DJ (2009) GLP-1R agonist liraglutide activates cytoprotective pathways and improves outcomes after experimental myocardial infarction in mice. Diabetes 58:975–983. doi:10.2337/db08-1193
33. Poornima I, Brown S, Bhashyam S, Parikh P, Bolukoglu H, Shannon RP (2008) Chronic glucagon-like peptide-1 (GLP-1) infusion sustains LV systolic function and prolongs survival in the spontaneously hypertensive-heart failure prone rat. Circ Heart Fail 1:153–160. doi:10.1161/CIRCHEARTFAILURE.108.766402
34. Robinson E, Cassidy RS, Tate M, Zhao Y, Lockhart S, Calderwood D, Church R, McGahon MK, Brazil DP, McDermott BJ, Green BD, Grieve DJ (2015) Exendin-4 protects against post-myocardial infarction remodelling via specific actions on inflammation and the extracellular matrix. Basic Res Cardiol 110:20. doi:10.1007/s00395-015-0476-7
35. Schilling JD, Machkovech HM, Kim AH, Schwedwener R, Schaffer JE (2012) Macrophages modulate cardiac function in lipotoxic cardiomyopathy. Am J Physiol Heart Circ Physiol 303:H1366–H1373. doi:10.1152/ajpheart.00111.2012
36. Schilling JD, Mann DL (2012) Diabetic cardiomyopathy: bench to bedside. Heart Fail Clin 8:619–631. doi:10.1016/j.hfc.2012.06.007
37. Semeniuk LM, Kryski AJ, Severson DL (2002) Echocardiographic assessment of cardiac function in diabetic db/db and transgenic db/db-hGLUT4 mice. Am J Physiol Heart Circ Physiol 283:H976–H982. doi:10.1152/ajpheart.00088.2002
38. Shimizu M, Umeda K, Sugihara N, Yoshio H, Ino H, Takeda R, Okada Y, Nakanishi I (1993) Collagen remodelling in myocardia of patients with diabetes. J Clin Pathol 46:32–36. doi:10.1136/jcp.46.1.32
39. Shiraishi D, Fujiwara Y, Komohara Y, Mizuta H, Takeya M (2012) Glucagon-like peptide-1 (GLP-1) induces M2 polarization of human macrophages via STAT3 activation. Biochem Biophys Res Commun 425:304–308. doi:10.1016/j.bbrc.2012.07.086
40. Steven S, Hausding M, Kröller-Schön S, Mader M, Mikhed Y, Stamm P, Zinßius E, Pfeffer A, Welschof P, Agdauletova S, Sudowe S, Li H, Oelze M, Schulz E, Klein T, Münzel T, Daiber A (2015) Gliptin and GLP-1 analog treatment improves survival and vascular inflammation/dysfunction in animals with lipopolysaccharide-induced endotoxemia. Basic Res Cardiol 110:1–14. doi:10.1007/s00395-015-0465-x
41. Tate M, Chong A, Robinson E, Green BD, Grieve DJ (2015) Selective targeting of glucagon-like peptide-1 signalling as a novel therapeutic approach for cardiovascular disease in diabetes. Br J Pharmacol 172:721–736. doi:10.1111/bph.12943
42. Timmers L, Henriques JPS, de Kleijn DPV, DeVries JH, Kemperman H, Steendijk P, Verlaan CW, Kerver M, Piek JJ, Doevendans PA, Pasterkamp G, Hoefer IE (2009) Exenatide reduces infarct size and improves cardiac function in a porcine model of ischemia and reperfusion injury. J Am Coll Cardiol 53:501–510. doi:10.1016/j.jacc.2008.10.033
43. Urbina P, Singla DK (2014) BMP-7 attenuates adverse cardiac remodeling mediated through M2 macrophages in prediabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 307:H762–H772. doi:10.1152/ajpheart.00367.2014
44. Ussher JR, Baggio LL, Campbell JE, Mulvihill EE, Kim M, Kabir MG, Cao X, Baranek BM, Stoffers DA, Seeley RJ, Drucker DJ (2014) Inactivation of the cardiomyocyte glucagon-like peptide-1 receptor (GLP-1R) unmasks cardiomyocyte-independent GLP-1R-mediated cardioprotection. Mol Metab 3:507–517. doi:10.1016/j.molmet.2014.04.009
45. Wang Y, Ebermann L, Sterner-Kock A, Wika S, Schultheiss HP, Dorner A, Walther T (2009) Myocardial overexpression of adenine nucleotide translocase 1 ameliorates diabetic cardiomyopathy in mice. Exp Physiol 94:220–227. doi:10.1113/expphysiol.2008.044800
46. Westermann D, Rutschow S, Jager S, Linderer A, Anker S, Riad A, Unger T, Schultheiss HP, Pauschinger M, Tschope C (2007) Contributions of inflammation and cardiac matrix metalloproteinase activity to cardiac failure in diabetic cardiomyopathy. Diabetes 56:641–646. doi:10.2337/db06-1163
47. Wynn TA, Barron L (2010) Macrophages: master regulators of inflammation and fibrosis. Semin Liver Dis 30:245–257. doi:10.1055/s-0030-1255354
48. Xu G, Stoffers DA, Habener JF, Bonner-Weir S (1999) Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased beta-cell mass and improved glucose tolerance in diabetic rats. 48:2270–2276. doi:10.2337/diabetes.48.12.2270
49. Zhao Y, McLaughlin D, Robinson E, Harvey AP, Hookham MB, Shah AM, McDermott BJ, Grieve DJ (2010) Nox2 NADPH oxidase promotes pathologic cardiac remodeling associated with doxorubicin chemotherapy. Cancer Res 70:9287–9297. doi:10.1158/0008-5472.CAN-10-2664