Skip to main content
Top
Published in: BMC Physiology 1/2017

Open Access 01-12-2017 | Research article

Myocardial susceptibility to ischaemia/reperfusion in obesity: a re-evaluation of the effects of age

Authors: I. Webster, R. Salie, E. Marais, W.-J. Fan, G. Maarman, B. Huisamen, A. Lochner

Published in: BMC Physiology | Issue 1/2017

Login to get access

Abstract

Background

Reports on the effect of age and obesity on myocardial ischaemia/reperfusion (I/R) injury and ischaemic preconditioning are contradictory. The aim of this study was to re-evaluate the effects of age and diet-induced obesity (DIO) on myocardial I/R injury and preconditioning potential.

Methods

Four groups of Wistar male rats were used: age-matched controls (AMC) receiving standard rat chow for (i) 16 weeks and (ii) 16 months respectively; DIO rats receiving a sucrose-supplemented diet for (iii) 16 weeks and (iv) 16 months respectively. The ages of groups (i) and (iii) were 22 weeks (“young”) and groups (ii) and (iv) 17 months (“middle-aged”) at time of experimentation. Isolated perfused working hearts were subjected to 35 min regional ischaemia/1 h reperfusion. Endpoints were infarct size (tetrazolium staining) and functional recovery. Hearts were preconditioned by 3 × 5 min ischaemia/5 min reperfusion. Results were processed using GraphPad Prism statistical software.

Results

Age did not affect baseline heart function before induction of ischaemia and I/R damage as indicated by infarct size and similar values were obtained in hearts from both age groups. Age also had no effect on functional recovery of hearts during reperfusion after regional ischaemia in AMC rats, but cardiac output during reperfusion was better in hearts from middle-aged than young DIO rats.
The diet reduced infarct size in hearts from young rats (% of area at risk: AMC: 32.4 ± 3.6; DIO: 20.7 ± 2.9, p < 0.05), with no differences in hearts from middle-aged rats (AMC: 24.6 ± 4.6; DIO: 28.3 ± 13.5, p = NS). Compared to their respective AMC, diet-induced obesity had no significant effect on functional recovery of hearts from both age groups after exposure to regional ischaemia.
When exposed to the more severe stress of global ischaemia, the functional recovery potential of middle-aged DIO rats appeared to be impeded compared to hearts of young DIO rats, while age had no effect on the functional recovery of AMC hearts.
Preconditioning reduced infarct size in hearts from young control rats and both middle-aged groups, but not from young DIO rats. Age had a significant effect on functional recovery in preconditioning: it was improved in hearts from young control and DIO rats, but depressed in both middle-aged groups.

Conclusions

The data showed that middle-age and obesity had no effect on baseline myocardial function and did not increase susceptibility to I/R damage upon exposure to regional ischaemia. On the contrary, obesity reduced I/R damage in young rats. Preconditioned aging hearts showed a decreased infarct size, but a reduction in functional recovery.
Literature
1.
go back to reference Juhaszova M, Rabuel C, Zorov DB, Lakatta EG, Sollot SJ. Protection in the aged heart: preventing the heart-break of old age. Cardiovasc Res. 2005;66:233–44.CrossRefPubMed Juhaszova M, Rabuel C, Zorov DB, Lakatta EG, Sollot SJ. Protection in the aged heart: preventing the heart-break of old age. Cardiovasc Res. 2005;66:233–44.CrossRefPubMed
2.
go back to reference Boengler K, Schulz R, Heusch G. Loss of cardioprotection with ageing. Cardiovasc Res. 2009;83:247–61.CrossRefPubMed Boengler K, Schulz R, Heusch G. Loss of cardioprotection with ageing. Cardiovasc Res. 2009;83:247–61.CrossRefPubMed
3.
go back to reference Abete P, Cacciatore F, Testa G, Dellas-Morte D, Galizia G, de Santis D, Calabrese C, Cioppa A, Ferrara N, Rengo F. Ischemic preconditioning in the ageing heart: from bench to bedside. Ageing Res Rev. 2010;9:153–62.CrossRefPubMed Abete P, Cacciatore F, Testa G, Dellas-Morte D, Galizia G, de Santis D, Calabrese C, Cioppa A, Ferrara N, Rengo F. Ischemic preconditioning in the ageing heart: from bench to bedside. Ageing Res Rev. 2010;9:153–62.CrossRefPubMed
4.
go back to reference Apaijai N, Chattipakorn SC, Chattipakorn N. Roles of obese-insulin resistance and anti-diabetic drugs on the heart with ischemia-reperfusion injury. Cardiovasc Drugs Ther. 2014;28:549–62.CrossRefPubMed Apaijai N, Chattipakorn SC, Chattipakorn N. Roles of obese-insulin resistance and anti-diabetic drugs on the heart with ischemia-reperfusion injury. Cardiovasc Drugs Ther. 2014;28:549–62.CrossRefPubMed
5.
go back to reference Lakatta EG. Cardiovascular regulatory mechanisms in advanced age. Physiol Rev. 1993;73:413–67.PubMed Lakatta EG. Cardiovascular regulatory mechanisms in advanced age. Physiol Rev. 1993;73:413–67.PubMed
7.
go back to reference Lakatta EG, Levy D. Arterial and cardiac ageing: major shareholders in cardiovascular disease enterprises: Part II. The aging heart in health: links to heart disease. Circulation. 2003;107:346–54.CrossRefPubMed Lakatta EG, Levy D. Arterial and cardiac ageing: major shareholders in cardiovascular disease enterprises: Part II. The aging heart in health: links to heart disease. Circulation. 2003;107:346–54.CrossRefPubMed
8.
go back to reference Xiao RP, Tomhave ED, Wand DJ, Ji X, Boluyt MO, Cheng H, et al. Age-associated reductions in cardiac beta-1 and beta2-adrenergic responses without changes in inhibitory G-proteins or receptor kinases. J Clin Invest. 1998;101:1273–82.CrossRefPubMedPubMedCentral Xiao RP, Tomhave ED, Wand DJ, Ji X, Boluyt MO, Cheng H, et al. Age-associated reductions in cardiac beta-1 and beta2-adrenergic responses without changes in inhibitory G-proteins or receptor kinases. J Clin Invest. 1998;101:1273–82.CrossRefPubMedPubMedCentral
9.
go back to reference Kilts JD, Akazawa T, Richardson MD, Kwatra MM. Age increases cardiac G alpha(i2) expression, resulting in enhanced coupling to G protein-coupled receptors. J Biol Chem. 2002;277:31257–62.CrossRefPubMed Kilts JD, Akazawa T, Richardson MD, Kwatra MM. Age increases cardiac G alpha(i2) expression, resulting in enhanced coupling to G protein-coupled receptors. J Biol Chem. 2002;277:31257–62.CrossRefPubMed
10.
go back to reference Di Lisa F, Canton M, Menabo R, Kaludercic N, Bernardi P. Mitochondria and cardioprotection. Heart Fail Rev. 2007;12:249–60.CrossRefPubMed Di Lisa F, Canton M, Menabo R, Kaludercic N, Bernardi P. Mitochondria and cardioprotection. Heart Fail Rev. 2007;12:249–60.CrossRefPubMed
11.
go back to reference Willems L, Zatta A, Holgren K, Ashton KJ, Headrick JP. Age-related changes in ischemic tolerance in male and female mouse hearts. J Mol Cell Cardiol. 1996;38:245–56.CrossRef Willems L, Zatta A, Holgren K, Ashton KJ, Headrick JP. Age-related changes in ischemic tolerance in male and female mouse hearts. J Mol Cell Cardiol. 1996;38:245–56.CrossRef
12.
go back to reference Zhang H, Tao L, Jiao X, Gao E, Lopez BL, Christopher TA, et al. Nitrative thioredoxin inactivation as a cause of enhanced myocardial ischemia/reperfusion injury in the aging heart. Free Radic Biol Med. 2007;43:39–47.CrossRefPubMedPubMedCentral Zhang H, Tao L, Jiao X, Gao E, Lopez BL, Christopher TA, et al. Nitrative thioredoxin inactivation as a cause of enhanced myocardial ischemia/reperfusion injury in the aging heart. Free Radic Biol Med. 2007;43:39–47.CrossRefPubMedPubMedCentral
13.
go back to reference Lesnefsky EJ, Gallo DS, Ye J, Whittingham TS, Lust WD. Aging increases ischemia-reperfusion injury in the isolated buffer-perfused heart. J Lab Clin Med. 1994;124:843–51.PubMed Lesnefsky EJ, Gallo DS, Ye J, Whittingham TS, Lust WD. Aging increases ischemia-reperfusion injury in the isolated buffer-perfused heart. J Lab Clin Med. 1994;124:843–51.PubMed
14.
go back to reference Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, Misu H, et al. Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism. 2008;57:1071–7.CrossRefPubMed Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, Misu H, et al. Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism. 2008;57:1071–7.CrossRefPubMed
15.
go back to reference Hausenloy DJ, Yellon DM. Reperfusion injury salvage kinase signalling: taking a RISK for protection. Heart Fail Rev. 2007;12:217–34.CrossRefPubMed Hausenloy DJ, Yellon DM. Reperfusion injury salvage kinase signalling: taking a RISK for protection. Heart Fail Rev. 2007;12:217–34.CrossRefPubMed
16.
go back to reference Carillon J, Romain C, Bardy G, Fouret G, Feillet-Coudray C, Gaillet S, et al. Cafeteria diet induces obesity and insulin resistance associated with oxidative stress but not with inflammation: improvement by dietary supplementation with a melon superoxide dismutase. Free Radic Biol Med. 2013;65C:254–61.CrossRef Carillon J, Romain C, Bardy G, Fouret G, Feillet-Coudray C, Gaillet S, et al. Cafeteria diet induces obesity and insulin resistance associated with oxidative stress but not with inflammation: improvement by dietary supplementation with a melon superoxide dismutase. Free Radic Biol Med. 2013;65C:254–61.CrossRef
17.
go back to reference Clark C, Smith W, Lochner A, du Toit EF. Effects of gender and obesity on myocardial tolerance to ischemia. Physiol Res. 2011;60:291–301.PubMed Clark C, Smith W, Lochner A, du Toit EF. Effects of gender and obesity on myocardial tolerance to ischemia. Physiol Res. 2011;60:291–301.PubMed
18.
go back to reference Wensley I, Salaveria K, Bulmer AC, Donner DG, du Toit EF. Myocardial structure, function and ischaemic tolerance in a rodent model of obesity with insulin resistance. Exp Physiol. 2013;98:1552–64.CrossRefPubMed Wensley I, Salaveria K, Bulmer AC, Donner DG, du Toit EF. Myocardial structure, function and ischaemic tolerance in a rodent model of obesity with insulin resistance. Exp Physiol. 2013;98:1552–64.CrossRefPubMed
19.
go back to reference Du Toit EF, Smith W, Muller C, Strijdom H, Stouthammer B, Woodiwiss A, Norton GR, Lochner A. Myocardial susceptibility to ischemic-reperfusion injury in a prediabetic model of dietary-induced obesity. Am J Physiol Heart Circ Physiol. 2008;294:H2336–43.CrossRefPubMed Du Toit EF, Smith W, Muller C, Strijdom H, Stouthammer B, Woodiwiss A, Norton GR, Lochner A. Myocardial susceptibility to ischemic-reperfusion injury in a prediabetic model of dietary-induced obesity. Am J Physiol Heart Circ Physiol. 2008;294:H2336–43.CrossRefPubMed
20.
go back to reference Nduhirabandi F, du Toit EF, Blackhurst D, Marais D, Lochner A. Chronic melatonin consumption prevents obesity-related metabolic abnormalities and protects the heart against ischaemia and reperfusion injury in a pre-diabetic model of diet-induced obesity. J Pineal Res. 2012;50:171–92. Nduhirabandi F, du Toit EF, Blackhurst D, Marais D, Lochner A. Chronic melatonin consumption prevents obesity-related metabolic abnormalities and protects the heart against ischaemia and reperfusion injury in a pre-diabetic model of diet-induced obesity. J Pineal Res. 2012;50:171–92.
21.
go back to reference Maarman G, Marais E, Lochner A, du Toit EF. Effect of chronic CPT-inhibition on myocardial ischaemia-reperfusion injury in a model of diet-induced obesity. Cardiovasc Drugs Ther. 2012;26:305–16.CrossRef Maarman G, Marais E, Lochner A, du Toit EF. Effect of chronic CPT-inhibition on myocardial ischaemia-reperfusion injury in a model of diet-induced obesity. Cardiovasc Drugs Ther. 2012;26:305–16.CrossRef
22.
go back to reference Donner D, Headrick JP, Peart JN, du Toit EF. Obesity improves myocardial ischemic tolerance and RISK signalling in insulin-insensitive rats. Dis Model Mech. 2013;6:457–66.CrossRefPubMed Donner D, Headrick JP, Peart JN, du Toit EF. Obesity improves myocardial ischemic tolerance and RISK signalling in insulin-insensitive rats. Dis Model Mech. 2013;6:457–66.CrossRefPubMed
23.
go back to reference Salie R, Huisamen B, Lochner A. High carbohydrate and high fat diets protect the heart against ischaemia/reperfusion injury. Cardiovasc Diabetol. 2014;13:109–21.CrossRefPubMedPubMedCentral Salie R, Huisamen B, Lochner A. High carbohydrate and high fat diets protect the heart against ischaemia/reperfusion injury. Cardiovasc Diabetol. 2014;13:109–21.CrossRefPubMedPubMedCentral
24.
go back to reference Lekli I, Szabo G, Juhasz B, Das S, Das M, Varga E, et al. Protective mechanisms of resveratrol against ischemia-reperfusion damage in hearts obtained from Zucker obese rats: the role of GLUT-4 and endothelin. Am J Physiol Heart Circ Physiol. 2008;294:H859–66.CrossRefPubMed Lekli I, Szabo G, Juhasz B, Das S, Das M, Varga E, et al. Protective mechanisms of resveratrol against ischemia-reperfusion damage in hearts obtained from Zucker obese rats: the role of GLUT-4 and endothelin. Am J Physiol Heart Circ Physiol. 2008;294:H859–66.CrossRefPubMed
25.
go back to reference Chase PJ, Davis PG, Bensimhon DR. The obesity paradox in chronic heart failure: what does it mean? Curr Heart Fail Rep. 2014;11:111–7.CrossRefPubMed Chase PJ, Davis PG, Bensimhon DR. The obesity paradox in chronic heart failure: what does it mean? Curr Heart Fail Rep. 2014;11:111–7.CrossRefPubMed
26.
go back to reference Clark AL, Fonarow GC, Horwich TB. Obesity and the obesity paradox in heart failure. Prog Cardiovasc Dis. 2014;56:409–10.CrossRefPubMed Clark AL, Fonarow GC, Horwich TB. Obesity and the obesity paradox in heart failure. Prog Cardiovasc Dis. 2014;56:409–10.CrossRefPubMed
27.
go back to reference Abete P, Ferrara N, Cioppa A, Ferrara P, Bianco P, Calabrese C, et al. Preconditioning does not prevent postischemic dysfunction in aging heart. J Am Coll Cardiol. 1996;27:1777–86.CrossRefPubMed Abete P, Ferrara N, Cioppa A, Ferrara P, Bianco P, Calabrese C, et al. Preconditioning does not prevent postischemic dysfunction in aging heart. J Am Coll Cardiol. 1996;27:1777–86.CrossRefPubMed
28.
go back to reference Tani M, Suganuma Y, Hasegawa H, Shinmura K, Ebihara Y, Hayashi Y, et al. Decrease in ischemic tolerance with aging in isolated perfused Fischer 344 rat hearts: relation to increases in intracellular Na + after ischemia. J Mol Cell Cardiol. 1997;29:3081–9.CrossRefPubMed Tani M, Suganuma Y, Hasegawa H, Shinmura K, Ebihara Y, Hayashi Y, et al. Decrease in ischemic tolerance with aging in isolated perfused Fischer 344 rat hearts: relation to increases in intracellular Na + after ischemia. J Mol Cell Cardiol. 1997;29:3081–9.CrossRefPubMed
29.
go back to reference Lu R, Hu CP, Deng HW, Li YJ. Calcitonin gene-related peptide-mediated ischemic preconditioning in the rat heart: influence of age. Regul Pept. 2001;99:183–9.CrossRefPubMed Lu R, Hu CP, Deng HW, Li YJ. Calcitonin gene-related peptide-mediated ischemic preconditioning in the rat heart: influence of age. Regul Pept. 2001;99:183–9.CrossRefPubMed
30.
go back to reference Abete P, Testa G, Ferrara N, De Santis D, Capaccio P, Viati L, et al. Cardioprotective effect of ischemic preconditioning is preserved in food-restricted senescent rats. Am J Physiol Heart Circ Physiol. 2002;282:H1978–87.CrossRefPubMed Abete P, Testa G, Ferrara N, De Santis D, Capaccio P, Viati L, et al. Cardioprotective effect of ischemic preconditioning is preserved in food-restricted senescent rats. Am J Physiol Heart Circ Physiol. 2002;282:H1978–87.CrossRefPubMed
31.
go back to reference Schulman D, Latchman DS, Yellon DM. Effect of ageing on the ability of preconditioning to protect hearts from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol. 2001;281:H1630–6.PubMed Schulman D, Latchman DS, Yellon DM. Effect of ageing on the ability of preconditioning to protect hearts from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol. 2001;281:H1630–6.PubMed
32.
go back to reference Burns PG, Krunkenkamp IB, Calderone CA, Kirvaitis RJ, Gaudette GR, Levitsky S. Is the preconditioning response conserved in senescent myocardium? Ann Thorac Surg. 1996;61:925–9.CrossRefPubMed Burns PG, Krunkenkamp IB, Calderone CA, Kirvaitis RJ, Gaudette GR, Levitsky S. Is the preconditioning response conserved in senescent myocardium? Ann Thorac Surg. 1996;61:925–9.CrossRefPubMed
34.
go back to reference Pickavance LC, Tadayyon M, Widdowson PS, Buckingham RE, Wilding JPH. Therapeutic index for rosiglitazone in dietary obese rats: separation of efficacy and haemodilution. Br J Pharmacol. 1999;128:1570–6.CrossRefPubMedPubMedCentral Pickavance LC, Tadayyon M, Widdowson PS, Buckingham RE, Wilding JPH. Therapeutic index for rosiglitazone in dietary obese rats: separation of efficacy and haemodilution. Br J Pharmacol. 1999;128:1570–6.CrossRefPubMedPubMedCentral
35.
go back to reference Lochner A, Genade S, Tromp E, Podzuweit T, Moolman JA. Ischaemic preconditioning and the beta-adrenergic pathway. Circulation. 1999;100:958–66.CrossRefPubMed Lochner A, Genade S, Tromp E, Podzuweit T, Moolman JA. Ischaemic preconditioning and the beta-adrenergic pathway. Circulation. 1999;100:958–66.CrossRefPubMed
36.
go back to reference Lochner A, Genade S, Moolman JA. Ischaemic preconditioning: infarct size is a more reliable endpoint than functional recovery. Basic Res Cardiol. 2003;98:337–46.CrossRefPubMed Lochner A, Genade S, Moolman JA. Ischaemic preconditioning: infarct size is a more reliable endpoint than functional recovery. Basic Res Cardiol. 2003;98:337–46.CrossRefPubMed
37.
go back to reference Sutherland FJ, Hearse DJ. The isolated blood and perfusion fluid perfused heart. Pharmacol Res. 2000;44:597–603. Sutherland FJ, Hearse DJ. The isolated blood and perfusion fluid perfused heart. Pharmacol Res. 2000;44:597–603.
38.
go back to reference Huisamen B, Dietrich D, Bezuidenhout N, Lopes J, Flepisi B, Blackhurst D, Lochner A. Early cardiovascular changes occurring in diet-induced obese insulin-resistant rats. Mol Cell Biochem. 2012;368:37–45.CrossRefPubMed Huisamen B, Dietrich D, Bezuidenhout N, Lopes J, Flepisi B, Blackhurst D, Lochner A. Early cardiovascular changes occurring in diet-induced obese insulin-resistant rats. Mol Cell Biochem. 2012;368:37–45.CrossRefPubMed
39.
40.
go back to reference Fenton RA, Dickson EW, Meyer TE, Dobson Jr JG. Aging reduced the cardioprotective effect of preconditioning in the rat heart. J Mol Cell Cardiol. 2000;32:1371–5.CrossRefPubMed Fenton RA, Dickson EW, Meyer TE, Dobson Jr JG. Aging reduced the cardioprotective effect of preconditioning in the rat heart. J Mol Cell Cardiol. 2000;32:1371–5.CrossRefPubMed
41.
42.
go back to reference Huisamen B, Havner TL, Lumkwana D, Lochner A. The impact of chronic glycogen synthase kinase-3 inhibition on remodelling of normal and prediabetic rat hearts. Cardiovasc Drugs Ther. 2016;30:237–46.CrossRefPubMed Huisamen B, Havner TL, Lumkwana D, Lochner A. The impact of chronic glycogen synthase kinase-3 inhibition on remodelling of normal and prediabetic rat hearts. Cardiovasc Drugs Ther. 2016;30:237–46.CrossRefPubMed
43.
go back to reference Jordan JE, Simandle SA, Tulbert CD, Busija DW, Miller AW. Fructose-fed rats are protected against ischemia/reperfusion injury. J Pharmacol Exp Ther. 2003;307:1007–11.CrossRefPubMed Jordan JE, Simandle SA, Tulbert CD, Busija DW, Miller AW. Fructose-fed rats are protected against ischemia/reperfusion injury. J Pharmacol Exp Ther. 2003;307:1007–11.CrossRefPubMed
44.
go back to reference Honda T, Kaikita K, Tsujita K, Hayasaki T, Matsukawa M, Fuchigami S, et al. Pioglitazone, a peroxisome proliferator-activated receptor-gamma agonist, attenuates myocardial ischemia-reperfusion injury in mice with metabolic disorders. J Mol Cell Cardiol. 2008;44:915–26.CrossRefPubMed Honda T, Kaikita K, Tsujita K, Hayasaki T, Matsukawa M, Fuchigami S, et al. Pioglitazone, a peroxisome proliferator-activated receptor-gamma agonist, attenuates myocardial ischemia-reperfusion injury in mice with metabolic disorders. J Mol Cell Cardiol. 2008;44:915–26.CrossRefPubMed
45.
go back to reference Bouhidel O, Pons S, Souktani R, Zini R, Berdeaux A, Ghaleh B. Myocardial ischemic postconditioning against ischemia-reperfusion is impaired in ob/ob mice. Am J Physiol Heart Circ Physiol. 2008;295:H1580–6.CrossRefPubMedPubMedCentral Bouhidel O, Pons S, Souktani R, Zini R, Berdeaux A, Ghaleh B. Myocardial ischemic postconditioning against ischemia-reperfusion is impaired in ob/ob mice. Am J Physiol Heart Circ Physiol. 2008;295:H1580–6.CrossRefPubMedPubMedCentral
46.
go back to reference Pons S, Martin V, Portal L, Zini R, Morin D, Berdeaux A, et al. Regular treadmill exercise restores cardioprotective signalling pathways in obese mice independently from improvement in associated comorbidities. J Mol Cell Cardiol. 2013;54:82–9.CrossRefPubMed Pons S, Martin V, Portal L, Zini R, Morin D, Berdeaux A, et al. Regular treadmill exercise restores cardioprotective signalling pathways in obese mice independently from improvement in associated comorbidities. J Mol Cell Cardiol. 2013;54:82–9.CrossRefPubMed
47.
go back to reference Huhn R, Heinen A, Hollmann MW, Schlack W, Preckel B, Weber NC. Cyclosporine administered during reperfusion fails to restore cardioprotection in prediabetic Zucker obese rats in vivo. Nutr Metab Cardiovasc Dis. 2010;20:706–12.CrossRefPubMed Huhn R, Heinen A, Hollmann MW, Schlack W, Preckel B, Weber NC. Cyclosporine administered during reperfusion fails to restore cardioprotection in prediabetic Zucker obese rats in vivo. Nutr Metab Cardiovasc Dis. 2010;20:706–12.CrossRefPubMed
48.
go back to reference Lacerda L, Opie LH, Lecour S. Influence of tumour necrosis factor alpha on the outcome of ischaemic postconditioning in the presence of obesity and diabetes. Exp Diabetes Res. 2012;2012:502654.CrossRefPubMedPubMedCentral Lacerda L, Opie LH, Lecour S. Influence of tumour necrosis factor alpha on the outcome of ischaemic postconditioning in the presence of obesity and diabetes. Exp Diabetes Res. 2012;2012:502654.CrossRefPubMedPubMedCentral
49.
go back to reference Song T, Lv LY, Xu J, Tian ZY, Cui WY, Wang QS, et al. Diet-induced obesity suppresses sevoflurane preconditioning against myocardial ischemia-reperfusion injury: role of AMP-activated protein kinase pathway. Exp Biol Med (Maywood). 2011;236:1427–36.CrossRef Song T, Lv LY, Xu J, Tian ZY, Cui WY, Wang QS, et al. Diet-induced obesity suppresses sevoflurane preconditioning against myocardial ischemia-reperfusion injury: role of AMP-activated protein kinase pathway. Exp Biol Med (Maywood). 2011;236:1427–36.CrossRef
50.
go back to reference Hausenloy DJ, Yellon DM. New directions for protecting the heart against ischaemia-reperfusion injury: targeting the Reperfusion Injury Salvage Kinase (RISK) pathway. Cardiovasc Res. 2004;61:448–60.CrossRefPubMed Hausenloy DJ, Yellon DM. New directions for protecting the heart against ischaemia-reperfusion injury: targeting the Reperfusion Injury Salvage Kinase (RISK) pathway. Cardiovasc Res. 2004;61:448–60.CrossRefPubMed
51.
go back to reference Lecour S. Activation of the Survivor Activating Factor Enhancement (SAFE) pathway against reperfusion injury: Does it go beyond the RISK pathway? J Mol Cell Cardiol. 2009;47:32–40.CrossRefPubMed Lecour S. Activation of the Survivor Activating Factor Enhancement (SAFE) pathway against reperfusion injury: Does it go beyond the RISK pathway? J Mol Cell Cardiol. 2009;47:32–40.CrossRefPubMed
52.
go back to reference Huisamen B, Genis A, Marais E, Lochner A. Pretreatment with a DPP-4 inhibitor is infarct sparing in hearts from obese, pre-diabetic rats. Cardiovasc Drugs Ther. 2011;25:13–20.CrossRefPubMed Huisamen B, Genis A, Marais E, Lochner A. Pretreatment with a DPP-4 inhibitor is infarct sparing in hearts from obese, pre-diabetic rats. Cardiovasc Drugs Ther. 2011;25:13–20.CrossRefPubMed
53.
go back to reference O’Brien JD, Ferguson JH, Howlett SE. Effects of ischemia and reperfusion on isolated ventricular myocytes from young adult and aged Fischer 344 rat hearts. Am J Physiol Heart Circ Physiol. 2008;294:H2174–83.CrossRefPubMed O’Brien JD, Ferguson JH, Howlett SE. Effects of ischemia and reperfusion on isolated ventricular myocytes from young adult and aged Fischer 344 rat hearts. Am J Physiol Heart Circ Physiol. 2008;294:H2174–83.CrossRefPubMed
54.
go back to reference Griecsova L, Farkasova V. Gablovsky, Khandelwal VKM et al. Effect of maturation on the resistance of rat hearts against ischemia. Study of potential molecular mechanisms. Physiol Res. 2015;64 Suppl 5:S685–96.PubMed Griecsova L, Farkasova V. Gablovsky, Khandelwal VKM et al. Effect of maturation on the resistance of rat hearts against ischemia. Study of potential molecular mechanisms. Physiol Res. 2015;64 Suppl 5:S685–96.PubMed
55.
go back to reference Przyklenk K, Li G, Whittaker P. No loss in the in vivo efficacy of ischemic preconditioning in middle-aged and old rabbits. J Am Coll Cardiol. 2001;38:1741–7.CrossRefPubMed Przyklenk K, Li G, Whittaker P. No loss in the in vivo efficacy of ischemic preconditioning in middle-aged and old rabbits. J Am Coll Cardiol. 2001;38:1741–7.CrossRefPubMed
56.
go back to reference Wider J, Przyklenk K. Ischemic conditioning: the challenge of protecting the diabetic heart. Cardiovasc Diagn Ther. 2014;4:383–96.PubMedPubMedCentral Wider J, Przyklenk K. Ischemic conditioning: the challenge of protecting the diabetic heart. Cardiovasc Diagn Ther. 2014;4:383–96.PubMedPubMedCentral
57.
go back to reference Balakumar P, Singh H, Singh M, Anand-Srivastava MB. The impairment of preconditioning-mediated cardioprotection in pathological conditions. Pharmacol Res. 2009;60:18–23.CrossRefPubMed Balakumar P, Singh H, Singh M, Anand-Srivastava MB. The impairment of preconditioning-mediated cardioprotection in pathological conditions. Pharmacol Res. 2009;60:18–23.CrossRefPubMed
59.
go back to reference Harmancy R, Vasquez HG, Guthrie PH, Taegtmeyer H. Decreased long-chain fatty acid oxidation impairs postischemic recovery of the insulin-resistant rat heart. FASEB J. 2013;27:3966–78.CrossRef Harmancy R, Vasquez HG, Guthrie PH, Taegtmeyer H. Decreased long-chain fatty acid oxidation impairs postischemic recovery of the insulin-resistant rat heart. FASEB J. 2013;27:3966–78.CrossRef
60.
go back to reference Bolli R, Marban E. Molecular and cellular mechanisms of myocardial stunning. Physiol Rev. 1999;79:609–3458.PubMed Bolli R, Marban E. Molecular and cellular mechanisms of myocardial stunning. Physiol Rev. 1999;79:609–3458.PubMed
61.
go back to reference Abete P, Cioppa A, Calabrese C, et al. Ischemic threshold and myocardial stunning in the aging heart. Exp Gerontol. 1999;34:875–8459.CrossRefPubMed Abete P, Cioppa A, Calabrese C, et al. Ischemic threshold and myocardial stunning in the aging heart. Exp Gerontol. 1999;34:875–8459.CrossRefPubMed
62.
go back to reference Iemitsu M, Maeda S, Jesmin S, Otsuki T, Miyauchi T. Exercise training improves aging-induced downregulation of VEGF angiogenic signalling cascade in hearts. Am J Physiol Heart Circ Physiol. 2006;291:H1290–8.CrossRefPubMed Iemitsu M, Maeda S, Jesmin S, Otsuki T, Miyauchi T. Exercise training improves aging-induced downregulation of VEGF angiogenic signalling cascade in hearts. Am J Physiol Heart Circ Physiol. 2006;291:H1290–8.CrossRefPubMed
Metadata
Title
Myocardial susceptibility to ischaemia/reperfusion in obesity: a re-evaluation of the effects of age
Authors
I. Webster
R. Salie
E. Marais
W.-J. Fan
G. Maarman
B. Huisamen
A. Lochner
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Physiology / Issue 1/2017
Electronic ISSN: 1472-6793
DOI
https://doi.org/10.1186/s12899-017-0030-y

Other articles of this Issue 1/2017

BMC Physiology 1/2017 Go to the issue