Secreted protein acidic and rich in cysteine facilitates age-related cardiac inflammation and macrophage M1 polarization

American Journal of Physiology - Cell Physiology

Volumn 308, Issue 12, 2015, Pages C972-C982

  Toba, Hiroe ^a,b   de Castro Brás, Lisandra E ^a,c   Baicu, Catalin F ^d   Zile, Michael R ^d,e,f   Bradshaw, Amy D ^d,e  

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

^b KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

^c EAST CAROLINA UNIVERSITY   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e RALPH H JOHNSON VA MEDICAL CENTER   (United States)

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

Author keywords

Aging; Heart; Inflammation; Macrophage; Secreted protein acidic and rich in cysteine

Indexed keywords

CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CXCR3; FRACTALKINE; MACROPHAGE MIGRATION INHIBITION FACTOR; OSTEONECTIN; RANTES; AUTACOID; CCL5 PROTEIN, MOUSE; CCR2 PROTEIN, MOUSE; CX3CL1 PROTEIN, MOUSE; CXCR3 PROTEIN, MOUSE; MESSENGER RNA; SPARC PROTEIN, MOUSE;

ADULT; AGE; AGE RELATED CARDIAC INFLAMMATION; ANIMAL CELL; ARTICLE; CARDIAC STRUCTURE; CARDIOVASCULAR PARAMETERS; CARDITIS; CELL INFILTRATION; CELL SIZE; CELL STIMULATION; CONTROLLED STUDY; DOWN REGULATION; ECHOCARDIOGRAPHY; FEMALE; GENE DELETION; GENE EXPRESSION ASSAY; GENOTYPE; HEART EJECTION FRACTION; HEART LEFT VENTRICLE FUNCTION; HEART LEFT VENTRICLE HYPERTROPHY; HEART MUSCLE CONTRACTILITY; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MALE; MIDDLE AGED; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; THICKNESS; UPREGULATION; VEIN DILATATION; AGING; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMOTAXIS; COMPARATIVE STUDY; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; HEART MUSCLE; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MYOCARDITIS; PATHOLOGY; PATHOPHYSIOLOGY; PERITONEUM MACROPHAGE; PHENOTYPE;

MUS;

AGE FACTORS; AGING; ANIMALS; CELLS, CULTURED; CHEMOKINE CCL5; CHEMOKINE CX3CL1; CHEMOTAXIS; GENE EXPRESSION REGULATION; INFLAMMATION MEDIATORS; MACROPHAGES, PERITONEAL; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDITIS; MYOCARDIUM; OSTEONECTIN; PHENOTYPE; RECEPTORS, CCR2; RECEPTORS, CXCR3; RNA, MESSENGER; VENTRICULAR FUNCTION, LEFT;

EID: 84931096289     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00402.2014     Document Type: Article

References (58)

1. Altin SE, Schulze PC. Fractalkine: a novel cardiac chemokine? Cardio-vasc Res 92: 361–362, 2011.
2. Arnold SA, Rivera LB, Miller AF, Carbon JG, Dineen SP, Xie Y, Castrillon DH, Sage EH, Puolakkainen P, Bradshaw AD, Brekken RA. Lack of host SPARC enhances vascular function and tumor spread in an orthotopic murine model of pancreatic carcinoma. Dis Model Mech 3: 57–72, 2010.
3. Ballou SP, Lozanski FB, Hodder S, Rzewnicki DL, Mion LC, Sipe JD, Ford AB, Kushner I. Quantitative and qualitative alterations of acute-phase proteins in healthy elderly persons. Age Ageing 25: 224–230, 1996.
4. Bradshaw AD. The role of SPARC in extracellular matrix assembly. J Cell Commun Signal 3: 239–246, 2009.
5. Bradshaw AD, Baicu CF, Rentz TJ, Van Laer AO, Bonnema DD, Zile MR. Age-dependent alterations in fibrillar collagen content and myocar-dial diastolic function: role of SPARC in postsynthetic procollagen processing. Am J Physiol Heart Circ Physiol 298: H614–H622, 2010.
6. Bradshaw AD, Sage EH. SPARC, a matricellular protein that functions in cellular differentiation and tissue response to injury. J Clin Invest 107: 1049–1054, 2001.
7. Brekken RA, Sage EH. SPARC, a matricellular protein: at the crossroads of cell-matrix. Matrix Biol 19: 569–580, 2000.
8. Bruunsgaard H, Pedersen BK. Age-related inflammatory cytokines and disease. Immunol Allergy Clin North Am 23: 15–39, 2003.
9. Calandra T, Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 3: 791–800, 2003.
10. Cheitlin MD. Cardiovascular physiology-changes with aging. Am J Geri-atr Cardiol 12: 9–13, 2003.
11. Chen J, Rider DA, Ruan R. Identification of valid housekeeping genes and antioxidant enzyme gene expression change in the aging rat liver. J Gerontol A Biol Sci Med Sci 61: 20–27, 2006.
12. 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 96: 444–455, 2012.
13. Chung HY, Cesari M, Anton S, Marzetti E, Giovannini S, Seo AY, Carter C, Yu BP, Leeuwenburgh C. Molecular inflammation: underpinnings of aging and age-related diseases. Ageing Res Rev 8: 18–30, 2009.
14. Dawson J, Miltz W, Mir AK, Wiessner C. Targeting monocyte che-moattractant protein-1 signaling in disease. Expert Opin Ther Targets 7: 35–48, 2003.
15. De la Fuente M, Miquel J. An update of the oxidation-inflammation theory of aging: the involvement of the immune system in oxi-inflamm-aging. Curr Pharm Des 15: 3003–3026, 2009.
16. Ershler WB, Sun WH, Binkley N, Gravenstein S, Volk MJ, Kamoske G, Klopp RG, Roecker EB, Daynes RA, Weindruch R. Interleukin-6 and aging: blood levels and mononuclear cell production increase with advancing age and in vitro production is modifiable by dietary restriction. Lymphokine Cytokine Res 12: 225–230, 1993.
17. Ferrandi C, Ardissone V, Ferro P, Ruckle T, Zaratin P, Ammannati E, Hauben E, Rommel C, Cirillo R. Phosphoinositide 3-kinase gamma inhibition plays a crucial role in early steps of inflammation by blocking neutrophil recruitment. J Pharmacol Exp Ther 322: 923–930, 2007.
18. Ferrari AU, Radaelli A, Centola M. Invited review: aging and the cardiovascular system. J Appl Physiol (1985) 95: 2591–2597, 2003.
19. Goldblum SE, Ding X, Funk SE, Sage EH. SPARC (secreted protein acidic and rich in cysteine) regulates endothelial cell shape and barrier function. Proc Natl Acad Sci USA 91: 3448–3452, 1994.
20. Groom JR, Luster AD. CXCR3 in T cell function. Exp Cell Res 317: 620–631, 2011.
21. Horn MA, Graham HK, Richards MA, Clarke JD, Greensmith DJ, Briston SJ, Hall MC, Dibb KM, Trafford AW. Age-related divergent remodeling of the cardiac extracellular matrix in heart failure: collagen accumulation in the young and loss in the aged. J Mol Cell Cardiol 53: 82–90, 2012.
22. Houard X, Touat Z, Ollivier V, Louedec L, Philippe M, Sebbag U, Meilhac O, Rossignol P, Michel JB. Mediators of neutrophil recruitment in human abdominal aortic aneurysms. Cardiovasc Res 82: 532–541, 2009.
23. Jacob MP. Extracellular matrix remodeling and matrix metalloproteinases in the vascular wall during aging and in pathological conditions. Biomed Pharmacother 57: 195–202, 2003.
24. Kelly KA, Allport JR, Yu AM, Sinh S, Sage EH, Gerszten RE, Weissleder R. SPARC is a VCAM-1 counter-ligand that mediates leukocyte transmigration. J Leukoc Biol 81: 748–756, 2007.
25. Koga K, Kenessey A, Powell SR, Sison CP, Miller EJ, Ojamaa K. Macrophage migration inhibitory factor provides cardioprotection during ischemia/reperfusion by reducing oxidative stress. Antioxid Redox Signal 14: 1191–1202, 2011.
26. Krishnamurthy J, Torrice C, Ramsey MR, Kovalev GI, Al-Regaiey K, Su L, Sharpless NE. Ink4a/Arf expression is a biomarker of aging. J Clin Invest 114: 1299–1307, 2004.
27. Kzhyshkowska J, Gratchev A, Goerdt S. Stabilin-1, a homeostatic scavenger receptor with multiple functions. J Cell Mol Med 10: 635–649, 2006.
28. Kzhyshkowska J, Workman G, Cardo-Vila M, Arap W, Pasqualini R, Gratchev A, Krusell L, Goerdt S, Sage EH. Novel function of alternatively activated macrophages: stabilin-1-mediated clearance of SPARC. J Immunol 176: 5825–5832, 2006.
29. Lakatta EG, Levy D. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises. Part I. Aging arteries: a “set up” for vascular disease. Circulation 107: 139–146, 2003.
30. Lakatta EG, Levy D. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises. Part II: The aging heart in health: links to heart disease. Circulation 107: 346–354, 2003.
31. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, Sutton MS, Stewart WJ. Recommendations for chamber quantification: a report from the American Society of Ech-ocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr 18: 1440–1463, 2005.
32. 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 43: 296–306, 2008.
33. Loetscher M, Gerber B, Loetscher P, Jones SA, Piali L, Clark-Lewis I, Baggiolini M, Moser B. Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. J Exp Med 184: 963–969, 1996.
34. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117: 175–184, 2007.
35. 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 112: 675–688, 2013.
36. Mansfield AS, Nevala WK, Dronca RS, Leontovich AA, Shuster L, Markovic SN. Normal ageing is associated with an increase in Th2 cells, MCP-1 (CCL1) and RANTES (CCL5), with differences in sCD40L and PDGF-AA between sexes. Clin Exp Immunol 170: 186–193, 2012.
37. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25: 677–686, 2004.
38. Martos R, Baugh J, Ledwidge M, O’Loughlin C, Conlon C, Patle A, Donnelly SC, McDonald K. Diastolic heart failure: evidence of increased myocardial collagen turnover linked to diastolic dysfunction. Circulation 115: 888–895, 2007.
39. Ng YL, Klopcic B, Lloyd F, Forrest C, Greene W, Lawrance IC. Secreted protein acidic and rich in cysteine (SPARC) exacerbates colonic inflammatory symptoms in dextran sodium sulphate-induced murine colitis. PLos One 8: e77575, 2013.
40. Norose K, Clark JI, Syed NA, Basu A, Heber-Katz E, Sage EH, Howe CC. SPARC deficiency leads to early-onset cataractogenesis. Invest Oph-thalmol Vis Sci 39: 2674–2680, 1998.
41. Prockop DJ, Kivirikko KI. Collagens: molecular biology, diseases, and potentials for therapy. Annu Rev Biochem 64: 403–434, 1995.
42. Qi D, Hu X, Wu X, Merk M, Leng L, Bucala R, Young LH. Cardiac macrophage migration inhibitory factor inhibits JNK pathway activation and injury during ischemia/reperfusion. J Clin Invest 119: 3807–3816, 2009.
43. Rammos C, Hendgen-Cotta UB, Pohl J, Totzeck M, Luedike P, Schulze VT, Kelm M, Rassaf T. Modulation of circulating macrophage migration inhibitory factor in the elderly. Biomed Res Int 2014: 582586, 2014.
44. Rempel SA, Hawley RC, Gutierrez JA, Mouzon E, Bobbitt KR, Lemke N, Schultz CR, Schultz LR, Golembieski W, Koblinski J, VanOsdol S, Miller CG. Splenic and immune alterations of the Sparc-null mouse accompany a lack of immune response. Genes Immun 8: 262–274, 2007.
45. Rentz TJ, Poobalarahi F, Bornstein P, Sage EH, Bradshaw AD. SPARC regulates processing of procollagen I and collagen fibrillogenesis in dermal fibroblasts. J Biol Chem 282: 22062–22071, 2007.
46. Salmi M, Koskinen K, Henttinen T, Elima K, Jalkanen S. CLEVER-1 mediates lymphocyte transmigration through vascular and lymphatic en-dothelium. Blood 104: 3849–3857, 2004.
47. Sangaletti S, Tripodo C, Cappetti B, Casalini P, Chiodoni C, Piconese S, Santangelo A, Parenza M, Arioli I, Miotti S, Colombo MP. SPARC oppositely regulates inflammation and fibrosis in bleomycin-induced lung damage. Am J Pathol 179: 3000–3010, 2011.
48. Sikora E, Arendt T, Bennett M, Narita M. Impact of cellular senescence signature on ageing research. Ageing Res Rev 10: 146–152, 2011.
49. Socha MJ, Manhiani M, Said N, Imig JD, Motamed K. Secreted protein acidic and rich in cysteine deficiency ameliorates renal inflammation and fibrosis in angiotensin hypertension. Am J Pathol 171: 1104–1112, 2007.
50. Wei J, Xu H, Davies JL, Hemmings GP. Increase of plasma IL-6 concentration with age in healthy subjects. Life Sci 51: 1953–1956, 1992.
51. Westermann D, Lindner D, Kasner M, Zietsch C, Savvatis K, Escher F, von Schlippenbach J, Skurk C, Steendijk P, Riad A, Poller W, Schultheiss HP, Tschope C. Cardiac inflammation contributes to changes in the extracellular matrix in patients with heart failure and normal ejection fraction. Circ Heart Fail 4: 44–52, 2011.
52. Wilke A, Schonian U, Herzum M, Hengstenberg C, Hufnagel G, Brilla CG, Maisch B. [The extracellular matrix and cytoskeleton of the myocardium in cardiac inflammatory reaction]. Herz 20: 95–108, 1995.
53. Workman G, Sage EH. Identification of a sequence in the matricellular protein SPARC that interacts with the scavenger receptor stabilin-1. J Cell Biochem 112: 1003–1008, 2011.
54. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol 214: 199–210, 2008.
55. Xu L, Ping F, Yin J, Xiao X, Xiang H, Ballantyne CM, Wu H, Li M. Elevated plasma SPARC levels are associated with insulin resistance, dyslipidemia, and inflammation in gestational diabetes mellitus. PLos One 8: e81615, 2013.
56. 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 306: H1398–H1407, 2014.
57. Zamilpa R, Ibarra J, de Castro Bras LE, Ramirez TA, Nguyen N, Halade GV, Zhang J, Dai Q, Dayah T, Chiao YA, Lowell W, 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 postmyocardial infarction. J Mol Cell Cardiol 53: 599–608, 2012.
58. Zile MR, Baicu CF, Stroud RE, Van Laer AO, Jones JA, Patel R, Mukherjee R, Spinale FG. Mechanistic relationship between membrane type-1 matrix metalloproteinase and the myocardial response to pressure overload. Circ Heart Fail 7: 340–350, 2014.