Macrophage Migration Inhibitory Factor (MIF) Deficiency Exacerbates Aging-Induced Cardiac Remodeling and Dysfunction Despite Improved Inflammation: Role of Autophagy Regulation

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Xu, Xihui ^a   Pang, Jiaojiao ^a,b   Chen, Yuguo ^b   Bucala, Richard ^c   Zhang, Yingmei ^a,d   Ren, Jun ^a,d  

^a UNIVERSITY OF WYOMING COLLEGE OF HEALTH SCIENCES   (United States)

^b SHANDONG UNIVERSITY   (China)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ISOMERASE; MACROPHAGE MIGRATION INHIBITION FACTOR; MIF PROTEIN, MOUSE; RAPAMYCIN;

AGING; ANIMAL; AUTOPHAGY; C57BL MOUSE; CARDIAC MUSCLE; CELL AGING; CELL LINE; DRUG EFFECTS; GENETICS; HEART; HEART VENTRICLE REMODELING; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; MACROPHAGE; MALE; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; AGING; ANIMALS; AUTOPHAGY; CELL AGING; CELL LINE; HEART; INFLAMMATION; INTRAMOLECULAR OXIDOREDUCTASES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIUM; SIROLIMUS; VENTRICULAR REMODELING;

EID: 84960481468     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22488     Document Type: Article

References (56)

1. Ribeiro, A. L., Marcolino, M. S., Prineas, R. J. & Lima-Costa, M. F. Electrocardiographic abnormalities in elderly chagas disease patients: 10-year follow-up of the Bambui Cohort Study of Aging. J Am Heart Assoc 3, e000632, doi: 10.1161/JAHA.113.000632 (2014).
2. Veerasamy, M. et al. Association of Aging, Arterial Stiffness and Cardiovascular Disease: A Review. Cardiol Rev, doi: 10.1097/ CRD.0000000000000009 (2014).
3. Finkel, T. The metabolic regulation of aging. Nat Med 21, 1416-1423, doi: 10.1038/nm.3998 (2015).
4. Christoffersen, M. & Tybjaerg-Hansen, A. Visible aging signs as risk markers for ischemic heart disease: Epidemiology, pathogenesis and clinical implications. Ageing Res Rev 25, 24-41, doi: 10.1016/j.arr.2015.11.002 (2016).
5. Ceylan-Isik, A. F. et al. Cardiomyocyte-specific deletion of endothelin receptor A rescues aging-associated cardiac hypertrophy and contractile dysfunction: role of autophagy. Basic Res Cardiol 108, 335, doi: 10.1007/s00395-013-0335-3 (2013).
6. Hua, Y. et al. Chronic Akt activation accentuates aging-induced cardiac hypertrophy and myocardial contractile dysfunction: role of autophagy. Basic Res Cardiol 106, 1173-1191, doi: 10.1007/s00395-011-0222-8 (2011).
7. Lakatta, E. G. & Sollott, S. J. The "heartbreak" of older age. Mol Interv 2, 431-446, doi: 10.1124/mi.2.7.431 (2002).
8. Camici, G. G., Savarese, G., Akhmedov, A. & Luscher, T. F. Molecular mechanism of endothelial and vascular aging: implications for cardiovascular disease. Eur Heart J 36, 3392-3403, doi: 10.1093/eurheartj/ehv587 (2015).
9. Zhang, Y. et al. Mitochondrial aldehyde dehydrogenase 2 accentuates aging-induced cardiac remodeling and contractile dysfunction: role of AMPK, Sirt1, and mitochondrial function. Free Radic Biol Med 71, 208-220, doi: 10.1016/j.freeradbiomed.2014.03.018 (2014).
10. Levine, B., Packer, M. & Codogno, P. Development of autophagy inducers in clinical medicine. J Clin Invest 125, 14-24, doi: 10.1172/ JCI73938 (2015).
11. Choi, A. M., Ryter, S. W. & Levine, B. Autophagy in human health and disease. N Engl J Med 368, 651-662, doi: 10.1056/ NEJMra1205406 (2013).
12. Kim, K. H. & Lee, M. S. Autophagy-a key player in cellular and body metabolism. Nat Rev Endocrinol 10, 322-337, doi: 10.1038/ nrendo.2014.35 (2014).
13. Nakai, A. et al. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 13, 619-624, doi: 10.1038/nm1574 (2007).
14. Xu, X., Hua, Y., Nair, S., Zhang, Y. & Ren, J. Akt2 knockout preserves cardiac function in high-fat diet-induced obesity by rescuing cardiac autophagosome maturation. J Mol Cell Biol 5, 61-63, doi: 10.1093/jmcb/mjs055 (2013).
15. Xu, X. & Ren, J. Macrophage migration inhibitory factor (MIF) knockout preserves cardiac homeostasis through alleviating Aktmediated myocardial autophagy suppression in high-fat diet-induced obesity. Int J Obes (Lond) 39, 387-396, doi: 10.1038/ ijo.2014.174 (2015).
16. Guo, Y. et al. A novel protective mechanism for mitochondrial aldehyde dehydrogenase (ALDH2) in type i diabetes-induced cardiac dysfunction: role of AMPK-regulated autophagy. Biochim Biophys Acta 1852, 319-331, doi: 10.1016/j.bbadis.2014.05.017 (2015).
17. Kubli, D. A. & Gustafsson, A. B. Unbreak my heart: targeting mitochondrial autophagy in diabetic cardiomyopathy. Antioxid Redox Signal 22, 1527-1544, doi: 10.1089/ars.2015.6322 (2015).
18. Xu, X., Pacheco, B. D., Leng, L., Bucala, R. & Ren, J. Macrophage migration inhibitory factor plays a permissive role in the maintenance of cardiac contractile function under starvation through regulation of autophagy. Cardiovasc Res 99, 412-421, doi: 10.1093/cvr/cvt116 (2013).
19. Cao, D. J. et al. Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy. Proc Natl Acad Sci USA 108, 4123-4128, doi: 10.1073/pnas.1015081108 (2011).
20. Jahng, J. W. et al. Pressure Overload-Induced Cardiac Dysfunction in Aged Male Adiponectin Knockout Mice Is Associated With Autophagy Deficiency. Endocrinology 156, 2667-2677, doi: 10.1210/en.2015-1162 (2015).
21. Kubli, D. A., Quinsay, M. N. & Gustafsson, A. B. Parkin deficiency results in accumulation of abnormal mitochondria in aging myocytes. Commun Integr Biol 6, e24511, doi: 10.4161/cib.24511 (2013).
22. Xu, X., Hueckstaedt, L. K. & Ren, J. Deficiency of insulin-like growth factor 1 attenuates aging-induced changes in hepatic function: role of autophagy. J Hepatol 59, 308-317, doi: 10.1016/j.jhep.2013.03.037 (2013).
23. Zhang, C. & Cuervo, A. M. Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat Med 14, 959-965, doi: 10.1038/nm.1851 (2008).
24. Flynn, J. M. et al. Late-life rapamycin treatment reverses age-related heart dysfunction. Aging Cell 12, 851-862, doi: 10.1111/ acel.12109 (2013).
25. Harrison, D. E. et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460, 392-395, doi: 10.1038/nature08221 (2009).
26. Grieb, G., Kim, B. S., Simons, D., Bernhagen, J. & Pallua, N. MIF and CD74 - suitability as clinical biomarkers. Mini Rev Med Chem 14, 1125-1131 (2014).
27. Grieb, G., Merk, M., Bernhagen, J. & Bucala, R. Macrophage migration inhibitory factor (MIF): a promising biomarker. Drug News Perspect 23, 257-264, doi: 10.1358/dnp.2010.23.4.1453629 (2010).
28. Miller, E. J. et al. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature 451, 578-582, doi: 10.1038/nature06504 (2008).
29. Xu, X., Hua, Y., Nair, S., Bucala, R. & Ren, J. Macrophage migration inhibitory factor deletion exacerbates pressure overload-induced cardiac hypertrophy through mitigating autophagy. Hypertension 63, 490-499, doi: 10.1161/HYPERTENSIONAHA.113.02219 (2014).
30. Ma, H. et al. Impaired macrophage migration inhibitory factor-AMP-activated protein kinase activation and ischemic recovery in the senescent heart. Circulation 122, 282-292, doi: 10.1161/CIRCULATIONAHA.110.953208 (2010).
31. Maejima, Y., Adachi, S., Ito, H., Hirao, K. & Isobe, M. Induction of premature senescence in cardiomyocytes by doxorubicin as a novel mechanism of myocardial damage. Aging Cell 7, 125-136, doi: 10.1111/j.1474-9726.2007.00358.x (2008).
32. Spallarossa, P. et al. Doxorubicin induces senescence or apoptosis in rat neonatal cardiomyocytes by regulating the expression levels of the telomere binding factors 1 and 2. Am J Physiol Heart Circ Physiol 297, H2169-2181, doi: 10.1152/ajpheart.00068.2009 (2009).
33. Altieri, P. et al. Testosterone Antagonizes Doxorubicin-Induced Senescence of Cardiomyocytes. J Am Heart Assoc 5, doi: 10.1161/ JAHA.115.002383 (2016).
34. Zhang, Y. et al. Insulin-like growth factor 1 alleviates high-fat diet-induced myocardial contractile dysfunction: role of insulin signaling and mitochondrial function. Hypertension 59, 680-693, doi: 10.1161/HYPERTENSIONAHA.111.181867 (2012).
35. Xu, X., Roe, N. D., Weiser-Evans, M. C. & Ren, J. Inhibition of mammalian target of rapamycin with rapamycin reverses hypertrophic cardiomyopathy in mice with cardiomyocyte-specific knockout of PTEN. Hypertension 63, 729-739, doi: 10.1161/ HYPERTENSIONAHA.113.02526 (2014).
36. Kudo, N., Barr, A. J., Barr, R. L., Desai, S. & Lopaschuk, G. D. High rates of fatty acid oxidation during reperfusion of ischemic hearts are associated with a decrease in malonyl-CoA levels due to an increase in 5' -AMP-activated protein kinase inhibition of acetyl-CoA carboxylase. J Biol Chem 270, 17513-17520 (1995).
37. Yang, X. et al. Metallothionein prolongs survival and antagonizes senescence-associated cardiomyocyte diastolic dysfunction: role of oxidative stress. FASEB J 20, 1024-1026, doi: 10.1096/fj.05-5288fje (2006).
38. Yang, X., Sreejayan, N. & Ren, J. Views from within and beyond: narratives of cardiac contractile dysfunction under senescence. Endocrine 26, 127-137, doi: 10.1385/ENDO:26:2:127 (2005).
39. Gottlieb, R. A., Finley, K. D. & Mentzer, R. M., Jr. Cardioprotection requires taking out the trash. Basic Res Cardiol 104, 169-180, doi: 10.1007/s00395-009-0011-9 (2009).
40. Lakatta, E. G. Cardiovascular aging research: the next horizons. J Am Geriatr Soc 47, 613-625 (1999).
41. Boengler, K. et al. Cardioprotection by ischemic postconditioning is lost in aged and STAT3-deficient mice. Circ Res 102, 131-135, doi: 10.1161/CIRCRESAHA.107.164699 (2008).
42. Kappagoda, T. & Amsterdam, E. A. Exercise and heart failure in the elderly. Heart Fail Rev 17, 635-662, doi: 10.1007/s10741-011-9297-4 (2012).
43. Wei, J. Y. Age and the cardiovascular system. N Engl J Med 327, 1735-1739, doi: 10.1056/NEJM199212103272408 (1992).
44. Liang, Y. et al. Macrophage migration inhibitory factor promotes expression of GLUT4 glucose transporter through MEF2 and Zac1 in cardiomyocytes. Metabolism 64, 1682-1693, doi: 10.1016/j.metabol.2015.09.007 (2015).
45. Lopez, E. F. et al. Obesity superimposed on aging magnifies inflammation and delays the resolving response after myocardial infarction. Am J Physiol Heart Circ Physiol 308, H269-280, doi: 10.1152/ajpheart.00604.2014 (2015).
46. Matsui, Y. et al. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circulation research 100, 914-922, doi: 10.1161/01.RES.0000261924.76669.36 (2007).
47. Zhu, H. et al. Cardiac autophagy is a maladaptive response to hemodynamic stress. J Clin Invest 117, 1782-1793, doi: 10.1172/ JCI27523 (2007).
48. Gao, X. M. et al. Inhibition of mTOR reduces chronic pressure-overload cardiac hypertrophy and fibrosis. Journal of hypertension 24, 1663-1670, doi: 10.1097/01.hjh.0000239304.01496.83 (2006).
49. McMullen, J. R. et al. Inhibition of mTOR signaling with rapamycin regresses established cardiac hypertrophy induced by pressure overload. Circulation 109, 3050-3055, doi: 10.1161/01.CIR.0000130641.08705.45 (2004).
50. Shioi, T. et al. Rapamycin attenuates load-induced cardiac hypertrophy in mice. Circulation 107, 1664-1670, doi: 10.1161/01. CIR.0000057979.36322.88 (2003).
51. Cieslik, K. A. et al. AICAR-dependent AMPK activation improves scar formation in the aged heart in a murine model of reperfused myocardial infarction. J Mol Cell Cardiol 63, 26-36, doi: 10.1016/j.yjmcc.2013.07.005 (2013).
52. Turdi, S. et al. AMP-activated protein kinase deficiency exacerbates aging-induced myocardial contractile dysfunction. Aging Cell 9, 592-606, doi: 10.1111/j.1474-9726.2010.00586.x (2010).
53. Morselli, E. et al. Autophagy mediates pharmacological lifespan extension by spermidine and resveratrol. Aging (Albany NY) 1, 961-970 (2009).
54. Zajkowicz, A. & Rusin, M. The activation of the p53 pathway by the AMP mimetic AICAR is reduced by inhibitors of the ATM or mTOR kinases. Mech Ageing Dev 132, 543-551, doi: 10.1016/j.mad.2011.09.002 (2011).
55. Qi, D. et al. Cardiac macrophage migration inhibitory factor inhibits JNK pathway activation and injury during ischemia/ reperfusion. J Clin Invest 119, 3807-3816, doi: 10.1172/JCI39738 (2009).
56. Bollini, S., Smart, N. & Riley, P. R. Resident cardiac progenitor cells: at the heart of regeneration. J Mol Cell Cardiol 50, 296-303, doi: 10.1016/j.yjmcc.2010.07.006 (2011).