Deriving a cardiac ageing signature to reveal MMP-9-dependent inflammatory signalling in senescence

Cardiovascular Research

Volumn 106, Issue 3, 2015, Pages 421-431

  Ma, Yonggang ^a,b   Chiao, Ying Ann ^a,c   Clark, Ryan ^a,b   Flynn, Elizabeth R ^a,b   Yabluchanskiy, Andriy ^a,b   Ghasemi, Omid ^a,d   Zouein, Fouad ^a,b   Lindsey, Merry L ^a,b,e   Jin, Yu Fang ^a,d  

^a San Antonio Cardiovascular Proteomics Center   (United States)

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

^c UNIVERSITY OF WASHINGTON   (United States)

^d The University of Texas at San Antonio   (United States)

^e G V SONNY MONTGOMERY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cardiac ageing; Inflammation; Macrophage polarization; MMP 9; Proteomics

Indexed keywords

BIOLOGICAL MARKER; C REACTIVE PROTEIN; CXCL13 CHEMOKINE; EOTAXIN 2; GELATINASE B; INTERLEUKIN 4; PROTEIN BCL 6; AUTACOID; MMP9 PROTEIN, MOUSE;

ADULT; AGED; AGING; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTERIAL WALL THICKNESS; ARTICLE; CELL POLARITY; DIASTOLIC DYSFUNCTION; FLOW CYTOMETRY; HEART LEFT VENTRICLE; HEART MUSCLE FIBROSIS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; SENESCENCE; AGE; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE CELL; CELL AGING; CELL COMMUNICATION; DEFICIENCY; DIASTOLE; ENZYMOLOGY; FEMALE; FIBROSIS; GENE EXPRESSION PROFILING; GENETICS; HEART LEFT VENTRICLE FUNCTION; HEART VENTRICLE REMODELING; HYPERTROPHY, LEFT VENTRICULAR; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; SIGNAL TRANSDUCTION;

AGE FACTORS; AGING; ANIMALS; CELL AGING; CELL COMMUNICATION; DIASTOLE; FEMALE; FIBROSIS; GENE EXPRESSION PROFILING; HYPERTROPHY, LEFT VENTRICULAR; INFLAMMATION MEDIATORS; MACROPHAGES; MALE; MATRIX METALLOPROTEINASE 9; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCYTES, CARDIAC; PHENOTYPE; SIGNAL TRANSDUCTION; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 84930328812     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv128     Document Type: Article

References (38)

1. Boon RA, Iekushi K, Lechner S, Seeger T, Fischer A, Heydt S, Kaluza D, Treguer K, Carmona G, Bonauer A, Horrevoets AJ, Didier N, Girmatsion Z, Biliczki P, Ehrlich JR, Katus HA, Muller OJ, Potente M, Zeiher AM, Hermeking H, Dimmeler S. MicroRNA-34a regulates cardiac ageing and function. Nature 2013;495:107-110.
2. Jackson SH,Weale MR,Weale RA. Biological age-what is it and can it be measured? Arch Gerontol Geriatr 2003;36:103-115.
3. Lin J, Lopez EF, Jin Y, Van Remmen H, Bauch T, Han HC, Lindsey ML. Age-related cardiac muscle sarcopenia: combining experimental and mathematical modeling to identify mechanisms. Exp Gerontol 2008;43:296-306.
4. Dutta D, Calvani R, Bernabei R, Leeuwenburgh C, Marzetti E. Contribution of impaired mitochondrial autophagy to cardiac aging: mechanisms and therapeutic opportunities. Circ Res 2012;110:1125-1138.
5. Chiao YA, Ramirez TA, Zamilpa R, Okoronkwo SM, Dai Q, Zhang J, Jin YF, Lindsey ML. Matrix metalloproteinase-9 deletion attenuates myocardial fibrosis and diastolic dysfunction in ageing mice. Cardiovasc Res 2012;96:444-455.
6. Baylis D, Bartlett DB, Patel HP, Roberts HC. Understanding how we age: insights into inflammaging. Longev Healthspan 2013;2:8.
7. Chiao YA, Dai Q, Zhang J, Lin J, Lopez EF, Ahuja SS, Chou YM, Lindsey ML, Jin YF. Multianalyte profiling reveals matrix metalloproteinase-9 and monocyte chemotactic protein-1 as plasma biomarkers of cardiac aging. Circ Cardiovasc Genet 2011;4:455-462.
8. Xia Y, Frangogiannis NG. MCP-1/CCL2 as a therapeutic target in myocardial infarction and ischemic cardiomyopathy. Inflamm Allergy Drug Targets 2007;6:101-107.
9. Han L, Li M, Liu Y, Han C, Ye P. Atorvastatin may delay cardiac aging by upregulating peroxisome proliferator-activated receptors in rats. Pharmacology 2012;89:74-82.
10. Mercken EM, Crosby SD, Lamming DW, JeBailey L, Krzysik-Walker S, Villareal DT, Capri M, Franceschi C, Zhang Y, Becker K, Sabatini DM, de Cabo R, Fontana L. Calorie restriction in humans inhibits the PI3K/AKTpathway and induces a younger transcription profile. Aging Cell 2013;12:645-651.
11. Lindsey ML, Escobar GP, Dobrucki LW, Goshorn DK, Bouges S, Mingoia JT, McClister DM Jr, Su H, Gannon J, MacGillivray C, Lee RT, Sinusas AJ, Spinale FG. Matrix metalloproteinase-9 gene deletion facilitates angiogenesis after myocardial infarction. Am J Physiol Heart Circ Physiol 2006;290:H232-H239.
12. Ducharme A, Frantz S, Aikawa M, Rabkin E, Lindsey M, Rohde LE, Schoen FJ, Kelly RA, Werb Z, Libby P, Lee RT. Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J Clin Invest 2000;106:55-62.
13. Yabluchanskiy A, Ma Y, Chiao YA, Lopez EF, Voorhees AP, Toba H, Hall ME, Han HC, Lindsey ML, Jin YF. Cardiac aging is initiated by matrix metalloproteinase-9 mediated endothelial dysfunction. Am J Physiol Heart Circ Physiol 2014;306:H1398-H1407.
14. Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, Hanahan D, Shapiro SD, Senior RM, Werb Z. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 1998;93:411-422.
15. Martin MD, Carter KJ, Jean-Philippe SR, Chang M, Mobashery S, Thiolloy S, Lynch CC, Matrisian LM, Fingleton B. Effect of ablation or inhibition of stromal matrix metalloproteinase-9 on lung metastasis in a breast cancer model is dependent on genetic background. Cancer Res 2008;68:6251-6259.
16. Ma Y, Halade GV, Zhang J, Ramirez TA, Levin D, Voorhees A, Jin YF, Han HC, Manicone AM, Lindsey ML. Matrix metalloproteinase-28 deletion exacerbates cardiac dysfunction and rupture after myocardial infarction in mice by inhibiting m2 macrophage activation. Circ Res 2013;112:675-688.
17. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, PfafflMW, Shipley GL, Vandesompele J, WittwerCT. The MIQE guidelines: minimum information for publication of quantitative real-timePCR experiments. Clin Chem 2009;55: 611-622.
18. Ghasemi O, Nguyen N, RamirezTA, Zhang J, Lindsey ML, Jin Y-F.Abiclustering approach to analyze drug effects on extracellular matrix remodeling post-myocardial infarction. In 2012 IEEE International Conference on Bioinformatics and Biomedicine Workshops (BIBMW 2012). Philadelphia, USA: ; 2012. p. 143-150.
19. Ma Y, Chiao YA, Zhang J, Manicone AM, Jin YF, LindseyML. Matrix metalloproteinase-28 deletion amplifies inflammatory and extracellular matrix responses to cardiac aging. Microsc Microanal 2012;18:81-90.
20. Zamilpa R, Ibarra J, de CastroBras LE, RamirezTA, Nguyen N, HaladeGV, Zhang J, Dai Q, Dayah T, Chiao YA, LowellW, Ahuja SS, D'Armiento J, Jin YF, Lindsey ML. Transgenic overexpression of matrix metalloproteinase-9 in macrophages attenuates the inflammatory response and improves left ventricular function post-myocardial infarction. J Mol Cell Cardiol 2012;53:599-608.
21. Yan X, Anzai A, Katsumata Y, Matsuhashi T, Ito K, Endo J, Yamamoto T, Takeshima A, Shinmura K, Shen W, Fukuda K, Sano M. Temporal dynamics of cardiac immune cell accumulation following acute myocardial infarction. J Mol Cell Cardiol 2013;62:24-35.
22. Shebl FM, Pinto LA, Garcia-Pineres A, Lempicki R, Williams M, Harro C, Hildesheim A. Comparison of mRNA and protein measures of cytokines following vaccination with human papillomavirus-16 L1 virus-like particles. Cancer Epidemiol Biomarkers Prev 2010;19:978-981.
23. Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J,Wolf J, ChenW, Selbach M. Global quantification of mammalian gene expression control. Nature 2011;473: 337-342.
24. Heidt T, Courties G, Dutta P, Sager HB, Sebas M, Iwamoto Y, Sun Y, Da Silva N, Panizzi P, van der Lahn AM, Swirski FK,Weissleder R, Nahrendorf M. Differential contribution of monocytes to heart macrophages in steady-state and after myocardial infarction. Circ Res 2014;115:284-295.
25. Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA, Jones PA. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 2006;9:435-443.
26. Chen J,Wang M, Guo M, Xie Y, Cong YS. miR-127 regulates cell proliferation and senescence by targeting BCL6. PLoS ONE 2013;8:e80266.
27. Patel VP, Kreider BL, Li Y, Li H, Leung K, Salcedo T, Nardelli B, Pippalla V, Gentz S, Thotakura R, Parmelee D, Gentz R, Garotta G. Molecular and functional characterization of two novel human C-C chemokines as inhibitors of two distinct classes of myeloid progenitors. J Exp Med 1997;185:1163-1172.
28. Kim HD, Yu SJ, Kim HS, Kim YJ, Choe JM, Park YG, Kim J, Sohn J. Interleukin-4 induces senescence in human renal carcinoma cell lines through STAT6 and p38 MAPK. J Biol Chem 2013;288:28743-28754.
29. HartatikT, Okada S, Okabe S, Arima M, Hatano M, TokuhisaT. Binding of BAZFand Bc16 to STAT6-binding DNA sequences. Biochem Biophys Res Commun 2001;284:26-32.
30. Swirski FK, Nahrendorf M. Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure. Science 2013;339:161-166.
31. Aurora AB, Porrello ER, Tan W, Mahmoud AI, Hill JA, Bassel-Duby R, Sadek HA, Olson EN. Macrophages are required for neonatal heart regeneration. J Clin Invest 2014;124:1382-1392.
32. Bailey-Downs LC, Tucsek Z, Toth P, Sosnowska D, Gautam T, Sonntag WE, Csiszar A, Ungvari Z. Aging exacerbates obesity-induced oxidative stress and inflammation in perivascular adipose tissue in mice: a paracrine mechanism contributing to vascular redox dysregulation and inflammation. J Gerontol A Biol Sci Med Sci 2013;68:780-792.
33. Biswas SK, Chittezhath M, Shalova IN, Lim JY. Macrophage polarization and plasticity in health and disease. Immunol Res 2012;53:11-24.
34. Nahrendorf M. Macrophages in the infarct: fiery friends or friendly fire? J Mol Cell Cardiol 2012;53:591-592.
35. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008;8:958-969.
36. Brown BN, Ratner BD, Goodman SB, Amar S, Badylak SF. Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine. Biomaterials 2012;33:3792-3802.
37. Marchetti V, Yanes O, Aguilar E,Wang M, Friedlander D, Moreno S, Storm K, Zhan M, Naccache S, Nemerow G, Siuzdak G, Friedlander M. Differential macrophage polarization promotes tissue remodeling and repair in a model of ischemic retinopathy. Sci Rep 2011;1:76.
38. Pinto AR, Godwin JW, Chandran A, Hersey L, Ilinykh A, Debuque R, Wang L, Rosenthal NA. Age-related changes in tissue macrophages precede cardiac functional impairment. Aging (Albany NY) 2014;6:399-413.