Obesity superimposed on aging magnifies inflammation and delays the resolving response after myocardial infarction

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 308, Issue 4, 2015, Pages H269-H280

  Lopez, Elizabeth F ^a   Kabarowski, Janusz H ^b   Ingle, Kevin A ^c   Kain, Vasundhara ^c   Barnes, Stephen ^d   Crossman, David K ^e   Lindsey, Merry L ^f   Halade, Ganesh V ^c  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

Inflammation; Lipid mediators; Lipidomics; Neutrophils; Polyunsaturated fatty acids; Proteomics

Indexed keywords

12 HYDROXYICOSATETRAENOIC ACID; ARACHIDONATE 5 LIPOXYGENASE; ARACHIDONIC ACID; CD40 LIGAND; CYCLOOXYGENASE 2; HEME OXYGENASE 1; MACROPHAGE INFLAMMATORY PROTEIN 1; MYELOPEROXIDASE; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; POLYUNSATURATED FATTY ACID; VASCULAR CELL ADHESION MOLECULE 1; CD40 ANTIGEN; LIPOXYGENASE; MACROPHAGE INFLAMMATORY PROTEIN;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOVASCULAR MORTALITY; CONTROLLED STUDY; CORONARY ARTERY LIGATION; FAT INTAKE; FAT MASS; FEEDING; FOOD COMPOSITION; HEART INFARCTION; HEART LEFT VENTRICLE FAILURE; INFLAMMATION; LIPID COMPOSITION; LIPID DIET; LIPIDOMICS; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEOMICS; WOUND HEALING IMPAIRMENT; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; COMPLICATION; HEART VENTRICLE FUNCTION; IMMUNOLOGY; METABOLISM; PATHOPHYSIOLOGY; WOUND HEALING;

12-HYDROXY-5,8,10,14-EICOSATETRAENOIC ACID; AGING; ANIMALS; ANTIGENS, CD40; ARACHIDONIC ACID; CYCLOOXYGENASE 2; DIET, HIGH-FAT; FATTY ACIDS, OMEGA-3; HEME OXYGENASE-1; INFLAMMATION; LIPOXYGENASE; MACROPHAGE INFLAMMATORY PROTEINS; MICE; MICE, INBRED C57BL; MYOCARDIAL INFARCTION; NEUTROPHIL INFILTRATION; OBESITY; VENTRICULAR FUNCTION; WOUND HEALING;

EID: 84922879861     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00604.2014     Document Type: Article

References (46)

1. Aurich AC, Niemann B, Pan R, Gruenler S, Issa H, Silber RE, Rohrbach S. Age-dependent effects of high fat-diet on murine left ventricles: role of palmitate. Basic Res Cardiol 108: 369, 2013.
2. Blasbalg TL, Hibbeln JR, Ramsden CE, Majchrzak SF, Rawlings RR. Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century. Am J Clin Nutr 93: 950-962, 2011.
3. Blomer N, Pachel C, Hofmann U, Nordbeck P, Bauer W, Mathes D, Frey A, Bayer B, Vogel B, Ertl G, Bauersachs J, Frantz S. 5-Lipoxy-genase facilitates healing after myocardial infarction. Basic Res Cardiol 108: 367, 2013.
4. Bloom DE, Cafiero ET, Jané-Llopis E, Abrahams-Gessel S, Bloom LR, Fathima S, Feigl AB, Gaziano T, Mowafi M, Pandya A, Prettner K, Rosenberg L, Seligman B, Stein AZ & Weinstein C. The Global Economic Burden of Noncommunicable Diseases. Geneva: World Economic Forum, 2011.
5. Boden G. Obesity, insulin resistance and free fatty acids. Curr Opin Endocrinol Diabetes Obes 18: 139-143, 2011.
6. Bonds DE, Harrington M, Worrall BB, Bertoni AG, Eaton CB, Hsia J, Robinson J, Clemons TE, Fine LJ, Chew EY. Effect of long-chain &-3 fatty acids and lutein + zeaxanthin supplements on cardiovascular outcomes: results of the Age-Related Eye Disease Study 2 (AREDS2) randomized clinical trial. JAMA Intern Med 174: 763–771, 2014.
7. Brainard RE, Watson LJ, Demartino AM, Brittian KR, Readnower RD, Boakye AA, Zhang D, Hoetker JD, Bhatnagar A, Baba SP, Jones SP. High fat feeding in mice is insufficient to induce cardiac dysfunction and does not exacerbate heart failure. PloS One 8: e83174, 2013.
8. Canete R, Gil-Campos M, Aguilera CM, Gil A. Development of insulin resistance and its relation to diet in the obese child. Eur J Nutr 46: 181–187, 2007.
9. Dayton S, Hashimoto S, Dixon W, Pearce ML. Composition of lipids in human serum and adipose tissue during prolonged feeding of a diet high in unsaturated fat. J Lipid Res 7: 103–111, 1966.
10. DeFilippis AP, Sperling LS. Understanding omega-3’s. Am Heart J 151: 564–570, 2006.
11. Dobaczewski M, Gonzalez-Quesada C, Frangogiannis NG. The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J Mol Cell Cardiol 48: 504–511, 2010.
12. Fernandez Peralbo MA, Priego-Capote F, Galache-Osuna JG, Luque de Castro MD. Targeted analysis of omega-6-derived eicosanoids in human serum by SPE-LC-MS/MS for evaluation of coronary artery disease. Electrophoresis 34: 2901–2909, 2013.
13. Galbo T, Perry RJ, Jurczak MJ, Camporez JP, Alves TC, Kahn M, Guigni BA, Serr J, Zhang D, Bhanot S, Samuel VT, Shulman GI. Saturated and unsaturated fat induce hepatic insulin resistance independently of TLR-4 signaling and ceramide synthesis in vivo. Proc Natl Acad Sci USA 110: 12780–12785, 2013.
14. Galvao TF, Brown BH, Hecker PA, O’Connell KA, O’Shea KM, Sabbah HN, Rastogi S, Daneault C, Des Rosiers C, Stanley WC. High intake of saturated fat, but not polyunsaturated fat, improves survival in heart failure despite persistent mitochondrial defects. Cardiovasc Res 93: 24–32, 2012.
15. Ghosh S, Molcan E, DeCoffe D, Dai C, Gibson DL. Diets rich in n-6 PUFA induce intestinal microbial dysbiosis in aged mice. The Br J Nutr 110: 515–523, 2013.
16. Green DP, Ruparel S, Roman L, Henry MA, Hargreaves KM. Role of endogenous TRPV1 agonists in a postburn pain model of partial-thickness injury. Pain 154: 2512–2520, 2013.
17. Halade GV, El Jamali A, Williams PJ, Fajardo RJ, Fernandes G. Obesity-mediated inflammatory microenvironment stimulates osteoclasto-genesis and bone loss in mice. Exp Gerontol 46: 43–52, 2011.
18. Halade GV, Ma Y, Ramirez TA, Zhang J, Dai Q, Hensler JG, Lopez EF, Ghasemi O, Jin YF, Lindsey ML. Reduced BDNF attenuates inflammation and angiogenesis to improve survival and cardiac function following myocardial infarction in mice. Am J Physiol Heart Circ Physiol 305: H1830–H1842, 2013.
19. Halade GV, Rahman MM, Bhattacharya A, Barnes JL, Chandrasekar B, Fernandes G. Docosahexaenoic acid-enriched fish oil attenuates kidney disease and prolongs median and maximal life span of autoimmune lupus-prone mice. J Immunol 184: 5280–5286, 2010.
20. Halade GV, Rahman MM, Williams PJ, Fernandes G. High fat diet-induced animal model of age-associated obesity and osteoporosis. J Nutr Biochem 21: 1162–1169, 2010.
21. Harris WS, Mozaffarian D, Rimm E, Kris-Etherton P, Rudel LL, Appel LJ, Engler MM, Engler MB, Sacks F. Omega-6 fatty acids and risk for cardiovascular disease: a science advisory from the American Heart Association Nutrition Subcommittee of the Council on Nutrition, Physical Activity, and Metabolism; Council on Cardiovascular Nursing; and Council on Epidemiology and Prevention. Circulation 119: 902–907, 2009.
22. Heaberlin JR, Ma Y, Zhang J, Ahuja SS, Lindsey ML, Halade GV. Obese and diabetic KKAy mice show increased mortality but improved cardiac function following myocardial infarction. Cardiovasc Pathol 22: 481–487, 2013.
23. Iggman D, Rosqvist F, Larsson A, Arnlov J, Beckman L, Rudling M, Riserus U. Role of dietary fats in modulating cardiometabolic risk during moderate weight gain: a randomized double-blind overfeeding trial (LI-POGAIN study). J Am Heart Assoc 3: e001095, 2014.
24. Kain V, Prabhu SD, Halade GV. Inflammation revisited: inflammation versus resolution of inflammation following myocardial infarction. Basic Res Cardiol 109: 444, 2014.
25. Lavie CJ, De Schutter A, Milani RV. Healthy obese versus unhealthy lean: the obesity paradox. Nat Rev Endocrinol; doi:10.1038/nrendo.2014.165.
26. Liao JK. Linking endothelial dysfunction with endothelial cell activation. J Clin Invest 123: 540–541, 2013.
27. Malhotra A. Saturated fat is not the major issue. BMJ 347: f6340, 2013.
28. Massiera F, Barbry P, Guesnet P, Joly A, Luquet S, Moreilhon-Brest C, Mohsen-Kanson T, Amri EZ, Ailhaud G. A Western-like fat diet is sufficient to induce a gradual enhancement in fat mass over generations. J Lipid Res 51: 2352-2361, 2010.
29. Meissner J, Irfan A, Twerenbold R, Mueller S, Reiter M, Haaf P, Reichlin T, Schaub N, Winkler K, Pfister O, Heinisch C, Mueller C. Use of neutrophil count in early diagnosis and risk stratification of AMI. Am J Med 124: 534-542, 2011.
30. Mozaffarian D, Lemaitre RN, King IB, Song X, Spiegelman D, Sacks FM, Rimm EB, Siscovick DS. Circulating long-chain co-3 fatty acids and incidence of congestive heart failure in older adults: the cardiovascular health study: a cohort study. Ann Intern Med 155: 160-170, 2011.
31. Nabel EG, Braunwald E. A tale of coronary artery disease and myocardial infarction. N Engl J Med 366: 54-63, 2012.
32. Odegaard JI, Chawla A. Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis. Science 339: 172-177, 2013.
33. Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 311: 806-814, 2014.
34. Patterson E, Wall R, Fitzgerald GF, Ross RP, Stanton C. Health implications of high dietary co-6 polyunsaturated Fatty acids. J Nutr Metab 2012: 539426, 2012.
35. Ramsden CE, Zamora D, Leelarthaepin B, Majchrzak-Hong SF, Faurot KR, Suchindran CM, Ringel A, Davis JM, Hibbeln JR. Use of dietary linoleic acid for secondary prevention of coronary heart disease and death: evaluation of recovered data from the Sydney Diet Heart Study and updated meta-analysis. BMJ 346: e8707, 2013.
36. Reina-Couto M, Carvalho J, Valente MJ, Vale L, Afonso J, Carvalho F, Bettencourt P, Sousa T, Albino-Teixeira A. Impaired resolution of inflammation in human chronic heart failure. Eur J Clin Invest 44: 527-538, 2014.
37. Ross EA, Douglas MR, Wong SH, Ross EJ, Curnow SJ, Nash GB, Rainger E, Scheel-Toellner D, Lord JM, Salmon M, Buckley CD. Interaction between integrin alpha9beta1 and vascular cell adhesion mol-ecule-1 (VCAM-1) inhibits neutrophil apoptosis. Blood 107: 1178-1183, 2006.
38. Sellers RS, Radi ZA, Khan NK. Pathophysiology of cyclooxygenases in cardiovascular homeostasis. Vet Pathol 47: 601-613, 2010.
39. Shih H, Lee B, Lee RJ, Boyle AJ. The aging heart and post-infarction left ventricular remodeling. J Am Coll Cardiol 57: 9-17, 2011.
40. Shioi T, Inuzuka Y. Aging as a substrate of heart failure. J Cardiol 60: 423-428, 2012.
41. Slee EL, McLennan PL, Owen AJ, Theiss ML. Low dietary fish-oil threshold for myocardial membrane n-3 PUFA enrichment independent of n-6 PUFA intake in rats. J Lipid Res 51: 1841-1848, 2010.
42. Stanley WC, Dabkowski ER, Ribeiro RF Jr, O’Connell KA. Dietary fat and heart failure: moving from lipotoxicity to lipoprotection. Circ Res 110: 764-776, 2012.
43. Thomsen M, Nordestgaard BG. Myocardial infarction and ischemic heart disease in overweight and obesity with and without metabolic syndrome. JAMA Intern Med 174: 15-22, 2014.
44. Wood KE, Lau A, Mantzioris E, Gibson RA, Ramsden CE, Muhlhausler BS. A low co-6 polyunsaturated fatty acid (n-6 PUFA) diet increases co-3 (n-3) long chain PUFA status in plasma phospholipids in humans. Prostaglandins Leukot Essent Fatty Acids 90: 133-138, 2014.
45. Xia Y, Frangogiannis NG. MCP-1/CCL2 as a therapeutic target in myocardial infarction and ischemic cardiomyopathy. Inflamm Allergy Drug Targets 6: 101-107, 2007.
46. Yet SF, Tian R, Layne MD, Wang ZY, Maemura K, Solovyeva M, Ith B, Melo LG, Zhang L, Ingwall JS, Dzau VJ, Lee ME, Perrella MA. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfu-sion injury in transgenic mice. Circ Res 89: 168-173, 2001.