Modulation of Macrophage Polarization and HMGB1-TLR2/TLR4 Cascade Plays a Crucial Role for Cardiac Remodeling in Senescence-Accelerated Prone Mice

PLoS ONE

Volumn 11, Issue 4, 2016, Pages

  Karuppagounder, Vengadeshprabhu ^a   Giridharan, Vijayasree V ^b   Arumugam, Somasundaram ^a   Sreedhar, Remya ^a   Palaniyandi, Suresh S ^c   Krishnamurthy, Prasanna ^d   Quevedo, Joao ^b   Watanabe, Kenichi ^a   Konishi, Tetsuya ^e,f   Thandavarayan, Rajarajan A ^d  

^a NIIGATA UNIVERSITY OF PHARMACY AND APPLIED LIFE SCIENCES   (Japan)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c HENRY FORD HEALTH SYSTEM   (United States)

^d HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^e Basic Studies on Second Generation Functional Foods   (Japan)

^f CHANGCHUN UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; CD68 ANTIGEN; CYCLOOXYGENASE 2; GAMMA INTERFERON; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; HMGB1 PROTEIN, MOUSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PTGS2 PROTEIN, MOUSE; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POLARITY; CONTROLLED STUDY; HEART DISEASE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; HEART; HEART VENTRICLE REMODELING; INFLAMMATION; METABOLISM; PHYSIOLOGY; UPREGULATION;

AGING; ANIMALS; CYCLOOXYGENASE 2; HEART; HMGB1 PROTEIN; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-1BETA; INTERLEUKIN-6; MACROPHAGES; MALE; MICE; NF-KAPPA B; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; VENTRICULAR REMODELING;

EID: 84963756182     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0152922     Document Type: Article

References (40)

1. Johnson FB, Sinclair DA, Guarente L. Molecular biology of aging. Cell. 1999; 96(2):291-302. PMID: 9988222.
2. Odden MC, Coxson PG, Moran A, Lightwood JM, Goldman L, Bibbins-Domingo K. The impact of the aging population on coronary heart disease in the United States. The American journal of medicine. 2011; 124(9):827-33 e5. doi: 10.1016/j.amjmed.2011.04.010 PMID: 21722862; PubMed Central PMCID: PMC3159777.
3. Moslehi J, DePinho RA, Sahin E. Telomeres and mitochondria in the aging heart. Circ Res. 2012; 110 (9):1226-37. doi: 10.1161/CIRCRESAHA.111.246868 PMID: 22539756; PubMed Central PMCID: PMC3718635.
4. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, et al. Heart disease and stroke statistics-2011 update: A report from the American Heart Association. Circulation. 2011; 123(4):e18-e209. doi: 10.1161/CIR.0b013e3182009701 PMID: 21160056; PubMed Central PMCID: PMC4418670.
5. Hosokawa M, Abe T, Higuchi K, Shimakawa K, Omori Y, Matsushita T, et al. Management and design of the maintenance of SAM mouse strains: An animal model for accelerated senescence and age-associated disorders. Exp Gerontol. 1997; 32(1-2):111-6. PMID: 9088908.
6. Stoger JL, Gijbels MJ, Van Der Velden S, Manca M, Van Der Loos CM, Biessen EA, et al. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis. 2012; 225(2):461-8. doi: 10.1016/j.atherosclerosis.2012.09.013 PMID: 23078881.
7. Takahashi M. High-mobility group box 1 protein (HMGB1) in ischaemic heart disease: Beneficial or deleterious? Cardiovasc Res. 2008; 80(1):5-6. doi: 10.1093/cvr/cvn212 PMID: 18684705.
8. Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-tomacrophage differentiation and polarization: New molecules and patterns of gene expression. J Immunol. 2006; 177(10):7303-11. PMID: 17082649.
9. Karuppagounder V, Arumugam S, Thandavarayan RA, Pitchaimani V, Sreedhar R, Afrin R, et al. Naringenin ameliorates daunorubicin induced nephrotoxicity by mitigating AT1R, ERK1/2-NFkappaB p65 mediated inflammation. Int Immunopharmacol. 2015; 28(1):154-9. doi: 10.1016/j.intimp.2015.05.050 PMID: 26072060.
10. Gounder VK, Arumugam S, Arozal W, Thandavarayan RA, Pitchaimani V, Harima M, et al. Olmesartan protects against oxidative stress possibly through the Nrf2 signaling pathway and inhibits inflammation in daunorubicin-induced nephrotoxicity in rats. Int Immunopharmacol. 2014; 18(2):282-9. doi: 10.1016/j.intimp.2013.11.018 PMID: 24291173.
11. Ma Y, Chiao YA, Clark R, Flynn ER, Yabluchanskiy A, Ghasemi O, et al. Deriving a cardiac ageing signature to reveal MMP-9-dependent inflammatory signalling in senescence. Cardiovasc Res. 2015; 106 (3):421-31. doi: 10.1093/cvr/cvv128 PMID: 25883218; PubMed Central PMCID: PMC4498140.
12. Karuppagounder V, Arumugam S, Thandavarayan RA, Pitchaimani V, Sreedhar R, Afrin R, et al. Resveratrol attenuates HMGB1 signaling and inflammation in house dust mite-induced atopic dermatitis in mice. Int Immunopharmacol. 2014; 23(2):617-23. doi: 10.1016/j.intimp.2014.10.014 PMID: 25466270.
13. Karuppagounder V, Arumugam S, Thandavarayan RA, Pitchaimani V, Sreedhar R, Afrin R, et al. Modulation of HMGB1 translocation and RAGE/NFkappaB cascade by quercetin treatment mitigates atopic dermatitis in NC/Nga transgenic mice. Exp Dermatol. 2015; 24(6):418-23. doi: 10.1111/exd.12685 PMID: 25739980.
14. Takeda T, Hosokawa M, Takeshita S, Irino M, Higuchi K, Matsushita T, et al. A new murine model of accelerated senescence. Mech Ageing Dev. 1981; 17(2):183-94. PMID: 7311623.
15. Shioi T, Inuzuka Y. Aging as a substrate of heart failure. J Cardiol. 2012; 60(6):423-8. doi: 10.1016/j. jjcc.2012.07.015 PMID: 23068289.
16. Reed AL, Tanaka A, Sorescu D, Liu H, Jeong EM, Sturdy M, et al. Diastolic dysfunction is associated with cardiac fibrosis in the senescence-accelerated mouse. Am J Physiol Heart Circ Physiol. 2011; 301 (3):H824-31. doi: 10.1152/ajpheart.00407.2010 PMID: 21724869; PubMed Central PMCID: PMC3191096.
17. Gan W, Nie B, Shi F, Xu XM, Qian JC, Takagi Y, et al. Age-dependent increases in the oxidative damage of DNA, RNA, and their metabolites in normal and senescence-accelerated mice analyzed by LCMS/MS: Urinary 8-oxoguanosine as a novel biomarker of aging. Free Radic Biol Med. 2012; 52 (9):1700-7. doi: 10.1016/j.freeradbiomed.2012.02.016 PMID: 22348977.
18. Forman K, Vara E, Garcia C, Kireev R, Cuesta S, Escames G, et al. Effect of a combined treatment with growth hormone and melatonin in the cardiological aging on male SAMP8 mice. J Gerontol A Biol Sci Med Sci. 2011; 66(8):823-34. doi: 10.1093/gerona/glr083 PMID: 21665987.
19. Ranganathan PV, Jayakumar C, Ramesh G. Netrin-1-treated macrophages protect the kidney against ischemia-reperfusion injury and suppress inflammation by inducing M2 polarization. Am J Physiol Renal Physiol. 2013; 304(7):F948-57. doi: 10.1152/ajprenal.00580.2012 PMID: 23408164; PubMed Central PMCID: PMC3625850.
20. Cucak H, Nielsen Fink L, Hojgaard Pedersen M, Rosendahl A. Enalapril treatment increases T cell number and promotes polarization towards M1-like macrophages locally in diabetic nephropathy. Int Immunopharmacol. 2015; 25(1):30-42. doi: 10.1016/j.intimp.2015.01.003 PMID: 25598292.
21. Azzawi M, Kan SW, Hillier V, Yonan N, Hutchinson IV, Hasleton PS. The distribution of cardiac macrophages in myocardial ischaemia and cardiomyopathy. Histopathology. 2005; 46(3):314-9. doi: 10. 1111/j.1365-2559.2005.02075.x PMID: 15720417.
22. Gullestad L, Ueland T, Vinge LE, Finsen A, Yndestad A, Aukrust P. Inflammatory cytokines in heart failure: Mediators and markers. Cardiology. 2012; 122(1):23-35. doi: 10.1159/000338166 PMID: 22699305.
23. Saito H, Papaconstantinou J. Age-associated differences in cardiovascular inflammatory gene induction during endotoxic stress. J Biol Chem. 2001; 276(31):29307-12. doi: 10.1074/jbc.M103740200 PMID: 11382779.
24. Qin YH, Dai SM, Tang GS, Zhang J, Ren D, Wang ZW, et al. HMGB1 enhances the proinflammatory activity of lipopolysaccharide by promoting the phosphorylation of MAPK p38 through receptor for advanced glycation end products. J Immunol. 2009; 183(10):6244-50. doi: 10.4049/jimmunol.0900390 PMID: 19890065.
25. Karuppagounder V, Arumugam S, Thandavarayan RA, Pitchaimani V, Sreedhar R, Afrin R, et al. Modulation of HMGB1 translocation and RAGE/NFkappaB cascade by quercetin treatment mitigates atopic dermatitis in NC/Nga transgenic mice. Exp Dermatol. 2015. doi: 10.1111/exd.12685 PMID: 25739980.
26. Xu H, Su Z, Wu J, Yang M, Penninger JM, Martin CM, et al. The alarmin cytokine, high mobility group box 1, is produced by viable cardiomyocytes and mediates the lipopolysaccharide-induced myocardial dysfunction via a TLR4/phosphatidylinositol 3-kinase gamma pathway. J Immunol. 2010; 184(3):1492-8. doi: 10.4049/jimmunol.0902660 PMID: 20028656.
27. Wang WK, Lu QH, Zhang JN, Wang B, Liu XJ, An FS, et al. HMGB1 mediates hyperglycaemia-induced cardiomyocyte apoptosis via ERK/Ets-1 signalling pathway. J Cell Mol Med. 2014; 18(11):2311-20. doi: 10.1111/jcmm.12399 PMID: 25210949; PubMed Central PMCID: PMC4224563.
28. Van Beijnum JR, Buurman WA, Griffioen AW. Convergence and amplification of toll-like receptor (TLR) and receptor for advanced glycation end products (RAGE) signaling pathways via high mobility group B1 (HMGB1). Angiogenesis. 2008; 11(1):91-9. doi: 10.1007/s10456-008-9093-5 PMID: 18264787.
29. De Haan JJ, Smeets MB, Pasterkamp G, Arslan F. Danger signals in the initiation of the inflammatory response after myocardial infarction. Mediators Inflamm. 2013; 2013:206039. doi: 10.1155/2013/206039 PMID: 24363498; PubMed Central PMCID: PMC3864081.
30. Favre J, Musette P, Douin-Echinard V, Laude K, Henry JP, Arnal JF, et al. Toll-like receptors 2-deficient mice are protected against postischemic coronary endothelial dysfunction. Arterioscler Thromb Vasc Biol. 2007; 27(5):1064-71. doi: 10.1161/ATVBAHA.107.140723 PMID: 17332486.
31. Oyama J, Blais C Jr., Liu X, Pu M, Kobzik L, Kelly RA, et al. Reduced myocardial ischemia-reperfusion injury in toll-like receptor 4-deficient mice. Circulation. 2004; 109(6):784-9. doi: 10.1161/01.CIR. 0000112575.66565.84 PMID: 14970116.
32. Andrassy M, Volz HC, Igwe JC, Funke B, Eichberger SN, Kaya Z, et al. High-mobility group box-1 in ischemia-reperfusion injury of the heart. Circulation. 2008; 117(25):3216-26. doi: 10.1161/CIRCULATIONAHA.108.769331 PMID: 18574060.
33. Qiu Y, Yang J, Wang W, Zhao W, Peng F, Xiang Y, et al. HMGB1-promoted and TLR2/4-dependent NK cell maturation and activation take part in rotavirus-induced murine biliary atresia. PLoS pathogens. 2014; 10(3):e1004011. doi: 10.1371/journal.ppat.1004011 PMID: 24651485; PubMed Central PMCID: PMC3961347.
34. Tang D, Kang R, Zeh HJ 3rd, Lotze MT. High-mobility group box 1, oxidative stress, and disease. Antioxid Redox Signal. 2011; 14(7):1315-35. doi: 10.1089/ars.2010.3356 PMID: 20969478; PubMed Central PMCID: PMC3048826.
35. Hao Q, Chen X, Wang X, Dong B, Yang C. Curcumin Attenuates Angiotensin II-Induced Abdominal Aortic Aneurysm by Inhibition of Inflammatory Response and ERK Signaling Pathways. Evid Based Complement Alternat Med. 2014; 2014:270930. doi: 10.1155/2014/270930 PMID: 25431606; PubMed Central PMCID: PMC4241315.
36. Csiszar A, Ungvari Z, Edwards JG, Kaminski P, Wolin MS, Koller A, et al. Aging-induced phenotypic changes and oxidative stress impair coronary arteriolar function. Circ Res. 2002; 90(11):1159-66. PMID: 12065318.
37. Csiszar A, Wang M, Lakatta EG, Ungvari Z. Inflammation and endothelial dysfunction during aging: Role of NF-kappaB. J Appl Physiol (1985). 2008; 105(4):1333-41. doi: 10.1152/japplphysiol.90470.2008 PMID: 18599677; PubMed Central PMCID: PMC2576023.
38. Chinetti-Gbaguidi G, Staels B. Macrophage polarization in metabolic disorders: Functions and regulation. Current opinion in lipidology. 2011; 22(5):365-72. doi: 10.1097/MOL.0b013e32834a77b4 PMID: 21825981; PubMed Central PMCID: PMC3565956.
39. Han X, Kitamoto S, Wang H, Boisvert WA. Interleukin-10 overexpression in macrophages suppresses atherosclerosis in hyperlipidemic mice. FASEB journal: Official publication of the Federation of American Societies for Experimental Biology. 2010; 24(8):2869-80. doi: 10.1096/fj.09-148155 PMID: 20354139; PubMed Central PMCID: PMC2909283.
40. Jackaman C, Radley-Crabb HG, Soffe Z, Shavlakadze T, Grounds MD, Nelson DJ. Targeting macrophages rescues age-related immune deficiencies in C57BL/6J geriatric mice. Aging cell. 2013; 12 (3):345-57. doi: 10.1111/acel.12062 PMID: 23442123.