Cardiac macrophages promote diastolic dysfunction

Journal of Experimental Medicine

Volumn 215, Issue 2, 2018, Pages 423-440

  Hulsmans, Maarten ^a   Sager, Hendrik B ^a   Roh, Jason D ^a   Valero Muñoz, María ^b   Houstis, Nicholas E ^a   Iwamoto, Yoshiko ^a   Sun, Yuan ^a   Wilson, Richard M ^b   Wojtkiewicz, Gregory ^a   Tricot, Benoit ^a   Osborne, Michael T ^a   Hung, Judy ^a   Vinegoni, Claudio ^a   Naxerova, Kamila ^a,c   Sosnovik, David E ^a   Zile, Michael R ^d   Bradshaw, Amy D ^d   Liao, Ronglih ^c   Tawakol, Ahmed ^a   Weissleder, Ralph ^a,e   Rosenzweig, Anthony ^a   Swirski, Filip K ^a   Sam, Flora ^b   Nahrendorf, Matthias ^a   more..

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; COLLAGEN TYPE 1; INTERLEUKIN 10; IL10 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CARDIAC MUSCLE; CELL ACTIVATION; CELL AGING; CELL DENSITY; CELL EXPANSION; CLINICAL ARTICLE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; DIASTOLIC DYSFUNCTION; ECHOCARDIOGRAPHY; FEMALE; FIBROBLAST; HEART MUSCLE COMPLIANCE; HEART MUSCLE FIBROSIS; HEART MUSCLE RELAXATION; HEMATOPOIESIS; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERTENSION; MACROPHAGE; MALE; MIDDLE AGED; MONOCYTE; MOUSE; MYELOPOIESIS; NONHUMAN; POSITRON EMISSION TOMOGRAPHY-COMPUTED TOMOGRAPHY; PRIORITY JOURNAL; SPLEEN; AGED; AGING; ANIMAL; C57BL MOUSE; DEFICIENCY; DIASTOLE; GENETICS; HEART; HEART FAILURE; HEART STROKE VOLUME; HOMEOSTASIS; KNOCKOUT MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADULT; AGED; AGING; ANIMALS; DIASTOLE; FEMALE; FIBROBLASTS; HEART; HEART FAILURE; HEMATOPOIESIS; HOMEOSTASIS; HUMANS; HYPERTENSION; INTERLEUKIN-10; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; MONOCYTES; MYOCARDIUM; STROKE VOLUME;

EID: 85041385587     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20171274     Document Type: Article

References (52)

1. Alili, L., M. Sack, K. Puschmann, and P. Brenneisen. 2014. Fibroblast-tomyofibroblast switch is mediated by NAD(P)H oxidase generated reactive oxygen species. Biosci. Rep. 34:00089. https ://doi. org /10. 1042 /BSR20130091
2. Ather, S., W. Chan, B. Bozkurt, D. Aguilar, K. Ramasubbu, A.A. Zachariah, X.H. Wehrens, and A. Deswal. 2012. Impact of noncardiac comorbidities on morbidity and mortality in a predominantly male population with heart failure and preserved versus reduced ejection fraction. J. Am. Coll. Cardiol. 59:998-1005. https ://doi. org /10. 1016 /j. jacc. 2011. 11. 040
3. Beerman, I., D. Bhattacharya, S. Zandi, M. Sigvardsson, I.L. Weissman, D. Bryder, and D.J. Rossi. 2010. Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proc. Natl. Acad. Sci. USA. 107:5465-5470. https ://doi. org /10. 1073 /pnas. 1000834107
4. Beerman, I., C. Bock, B.S. Garrison, Z.D. Smith, H. Gu, A. Meissner, and D.J. Rossi. 2013. Proliferation-dependent alterations of the DNA methylation landscape underlie hematopoietic stem cell aging. Cell Stem Cell. 12:413-425. https ://doi. org /10. 1016 /j. stem. 2013. 01. 017
5. Dykstra, B., S. Olthof, J. Schreuder, M. Ritsema, and G. de Haan. 2011. Clonal analysis reveals multiple functional defects of aged murine hematopoietic stem cells. J. Exp. Med. 208:2691-2703. https ://doi. org /10. 1084 /jem. 20111490
6. Eisenberg, T., M. Abdellatif, S. Schroeder, U. Primessnig, S. Stekovic, T. Pendl, A. Harger, J. Schipke, A. Zimmermann, A. Schmidt, et al. 2016. Cardioprotection and lifespan extension by the natural polyamine spermidine. Nat. Med. 22:1428-1438. https ://doi. org /10. 1038 /nm. 4222
7. Emami, H., P. Singh, M. MacNabb, E. Vucic, Z. Lavender, J.H. Rudd, Z.A. Fayad, J. Lehrer-Graiwer, M. Korsgren, A.L. Figueroa, et al. 2015. Splenic metabolic activity predicts risk of future cardiovascular events: demonstration of a cardiosplenic axis in humans. JACC Cardiovasc. Imaging. 8:121-130. https ://doi. org /10. 1016 /j. jcmg. 2014. 10. 009
8. Epelman, S., K.J. Lavine, A.E. Beaudin, D.K. Sojka, J.A. Carrero, B. Calderon, T. Brija, E.L. Gautier, S. Ivanov, A.T. Satpathy, et al. 2014. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity. 40:91-104. https ://doi. org /10. 1016 /j. immuni. 2013. 11. 019
9. Francis, G.S. 2011. Neurohormonal control of heart failure. Cleve. Clin. J. Med. 78(Suppl. 1):S75-S79. https ://doi. org /10. 3949 /ccjm. 78. s1. 13
10. Hartupee, J., and D.L. Mann. 2016. Role of inflammatory cells in fibroblast activation. J. Mol. Cell. Cardiol. 93:143-148. https ://doi. org /10. 1016 /j. yjmcc. 2015. 11. 016
11. Heart Failure Society of America, J. Lindenfeld, N.M. Albert, J.P. Boehmer, S.P. Collins, J.A. Ezekowitz, M.M. Givertz, S.D. Katz, M. Klapholz, D.K. Moser, J.G. Rogers, et al. 2010. HFSA 2010 Comprehensive Heart Failure Practice Guideline. J. Card. Fail. 16:e1-e194. https ://doi. org /10. 1016 /j. cardfail. 2010. 04. 004
12. Heidt, T., G. Courties, P. Dutta, H.B. Sager, M. Sebas, Y. Iwamoto, Y. Sun, N. Da Silva, P. Panizzi, A.M. van der Laan, et al. 2014. Differential contribution of monocytes to heart macrophages in steady-state and after myocardial infarction. Circ. Res. 115:284-295. https ://doi. org /10. 1161 /CIR CRE SAHA. 115. 303567
13. Hulsmans, M., F. Sam, and M. Nahrendorf. 2016. Monocyte and macrophage contributions to cardiac remodeling. J. Mol. Cell. Cardiol. 93:149-155. https ://doi. org /10. 1016 /j. yjmcc. 2015. 11. 015
14. Hulsmans, M., S. Clauss, L. Xiao, A.D. Aguirre, K.R. King, A. Hanley, W.J. Hucker, E.M. Wülfers, G. Seemann, G. Courties, et al. 2017. Macrophages facilitate electrical conduction in the heart. Cell. 169:510-522.e20. https ://doi. org /10. 1016 /j. cell. 2017. 03. 050
15. Jaiswal, S., P. Fontanillas, J. Flannick, A. Manning, P.V. Grauman, B.G. Mar, R.C. Lindsley, C.H. Mermel, N. Burtt, A. Chavez, et al. 2014. Age-related clonal hematopoiesis associated with adverse outcomes. N. Engl. J. Med. 371:2488-2498. https ://doi. org /10. 1056 /NEJMoa1408617
16. Kalogeropoulos, A., V. Georgiopoulou, B.M. Psaty, N. Rodondi, A.L. Smith, D.G. Harrison, Y. Liu, U. Hoffmann, D.C. Bauer, A.B. Newman, et al. Health ABC Study Investigators. 2010. Inflammatory markers and incident heart failure risk in older adults: The Health ABC (Health, Aging, and Body Composition) study. J. Am. Coll. Cardiol. 55:2129-2137. https ://doi. org /10. 1016 /j. jacc. 2009. 12. 045
17. Kasner, M., D. Westermann, B. Lopez, R. Gaub, F. Escher, U. Kühl, H.P. Schultheiss, and C. Tschöpe. 2011. Diastolic tissue Doppler indexes correlate with the degree of collagen expression and cross-linking in heart failure and normal ejection fraction. J. Am. Coll. Cardiol. 57:977-985. https ://doi. org /10. 1016 /j. jacc. 2010. 10. 024
18. Kong, P., P. Christia, and N.G. Frangogiannis. 2014. The pathogenesis of cardiac fibrosis. Cell. Mol. Life Sci. 71:549-574. https ://doi. org /10. 1007 /s00018-013-1349-6
19. Lenga, Y., A. Koh, A.S. Perera, C.A. McCulloch, J. Sodek, and R. Zohar. 2008. Osteopontin expression is required for myofibroblast differentiation. Circ. Res. 102:319-327. https ://doi. org /10. 1161 /CIR CRE SAHA. 107. 160408
20. Liu, Y. 2009. Clinical significance of diffusely increased splenic uptake on FDG-PET. Nucl. Med. Commun. 30:763-769. https ://doi. org /10. 1097 / MNM. 0b013e32832fa254
21. Ma, Y., Y.A. Chiao, R. Clark, E.R. Flynn, A. Yabluchanskiy, O. Ghasemi, F. Zouein, M.L. Lindsey, and Y.F. Jin. 2015. Deriving a cardiac ageing signature to reveal MMP-9-dependent inflammatory signalling in senescence. Cardiovasc. Res. 106:421-431. https ://doi. org /10. 1093 /cvr /cvv128
22. Mallat, Z., S. Besnard, M. Duriez, V. Deleuze, F. Emmanuel, M.F. Bureau, F. Soubrier, B. Esposito, H. Duez, C. Fievet, et al. 1999. Protective role of interleukin-10 in atherosclerosis. Circ. Res. 85:e17-e24. https ://doi. org /10. 1161 /01. RES. 85. 8. e17
23. McMurray, J.J., P.E. Carson, M. Komajda, R. McKelvie, M.R. Zile, A. Ptaszynska, C. Staiger, J.M. Donovan, and B.M. Massie. 2008. Heart failure with preserved ejection fraction: Clinical characteristics of 4133 patients enrolled in the I-PRE SER VE trial. Eur. J. Heart Fail. 10:149-156. https ://doi. org /10. 1016 /j. ejheart. 2007. 12. 010
24. Moore, K.W., R. de Waal Malefyt, R.L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19:683-765. https ://doi. org /10. 1146 /annurev. immunol. 19. 1. 683
25. Mozaffarian, D., E.J. Benjamin, A.S. Go, D.K. Arnett, M.J. Blaha, M. Cushman, S.R. Das, S. de Ferranti, J.P. Després, H.J. Fullerton, et al. 2016. Executive Summary: Heart Disease and Stroke Statistics-2016 Update: A report from the American Heart Association. Circulation. 133:447-454. https :// doi. org /10. 1161 /CIR. 0000000000000366
26. Mulder, W.J., F.A. Jaffer, Z.A. Fayad, and M. Nahrendorf. 2014. Imaging and nanomedicine in inflammatory atherosclerosis. Sci. Transl. Med. 6:239sr1. https ://doi. org /10. 1126 /scitranslmed. 3005101
27. Murray, P.J., and T.A. Wynn. 2011. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11:723-737. https ://doi. org /10. 1038 /nri3073
28. Nagueh, S.F., O.A. Smiseth, C.P. Appleton, B.F. Byrd III, H. Dokainish, T. Edvardsen, F.A. Flachskampf, T.C. Gillebert, A.L. Klein, P. Lancellotti, et al. 2016. Recommendations for the evaluation of left ventricular diastolic function by echocardiography: An update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J. Am. Soc. Echocardiogr. 29:277-314. https ://doi. org /10. 1016 /j. echo. 2016. 01. 011
29. Ohtsu, H., G.D. Frank, H. Utsunomiya, and S. Eguchi. 2005. Redoxdependent protein kinase regulation by angiotensin II: Mechanistic insights and its pathophysiology. Antioxid. Redox Signal. 7:1315-1326. https ://doi. org /10. 1089 /ars. 2005. 7. 1315
30. Owan, T.E., D.O. Hodge, R.M. Herges, S.J. Jacobsen, V.L. Roger, and M.M. Redfield. 2006. Trends in prevalence and outcome of heart failure with preserved ejection fraction. N. Engl. J. Med. 355:251-259. https ://doi. org /10. 1056 /NEJMoa052256
31. Paulus, W.J., and C. Tschöpe. 2013. A novel paradigm for heart failure with preserved ejection fraction: Comorbidities drive myocardial dysfunction and remodeling through coronary microvascular endothelial inflammation. J. Am. Coll. Cardiol. 62:263-271. https ://doi. org /10. 1016 /j. jacc. 2013. 02. 092
32. Paulus, W.J., C. Tschöpe, J.E. Sanderson, C. Rusconi, F.A. Flachskampf, F.E. Rademakers, P. Marino, O.A. Smiseth, G. De Keulenaer, A.F. Leite-Moreira, et al. 2007. How to diagnose diastolic heart failure: A consensus statement on the diagnosis of heart failure with normal left ventricular ejection fraction by the Heart Failure and Echocardiography Associations of the European Society of Cardiology. Eur. Heart J. 28:2539-2550. https ://doi. org /10. 1093 /eurheartj /ehm037
33. Pinto, A.R., J.W. Godwin, A. Chandran, L. Hersey, A. Ilinykh, R. Debuque, L. Wang, and N.A. Rosenthal. 2014. Age-related changes in tissue macrophages precede cardiac functional impairment. Aging (Albany N.Y.). 6:399-413. https ://doi. org /10. 18632 /aging. 100669
34. Pinto, A.R., A. Ilinykh, M.J. Ivey, J.T. Kuwabara, M.L. D'Antoni, R. Debuque, A. Chandran, L. Wang, K. Arora, N.A. Rosenthal, and M.D. Tallquist. 2016. Revisiting cardiac cellular composition. Circ. Res. 118:400-409. https ://doi. org /10. 1161 /CIR CRE SAHA. 115. 307778
35. Roers, A., L. Siewe, E. Strittmatter, M. Deckert, D. Schlüter, W. Stenzel, A.D. Gruber, T. Krieg, K. Rajewsky, and W. Müller. 2004. T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J. Exp. Med. 200:1289-1297. https ://doi. org /10. 1084 /jem. 20041789
36. Sager, H.B., M. Hulsmans, K.J. Lavine, M.B. Moreira, T. Heidt, G. Courties, Y. Sun, Y. Iwamoto, B. Tricot, O.F. Khan, et al. 2016. Proliferation and recruitment contribute to myocardial macrophage expansion in chronic heart failure. Circ. Res. 119:853-864. https ://doi. org /10. 1161 /CIR CRE SAHA. 116. 309001
37. Schulz, C., E. Gomez Perdiguero, L. Chorro, H. Szabo-Rogers, N. Cagnard, K. Kierdorf, M. Prinz, B. Wu, S.E. Jacobsen, J.W. Pollard, et al. 2012. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science. 336:86-90. https ://doi. org /10. 1126 /science. 1219179
38. Sharma, K., and D.A. Kass. 2014. Heart failure with preserved ejection fraction: Mechanisms, clinical features, and therapies. Circ. Res. 115:79-96. https ://doi. org /10. 1161 /CIR CRE SAHA. 115. 302922
39. Shiraishi, M., Y. Shintani, Y. Shintani, H. Ishida, R. Saba, A. Yamaguchi, H. Adachi, K. Yashiro, and K. Suzuki. 2016. Alternatively activated macrophages determine repair of the infarcted adult murine heart. J. Clin. Invest. 126:2151-2166. https ://doi. org /10. 1172 /JCI85782
40. Signore, S., A. Sorrentino, G. Borghetti, A. Cannata, M. Meo, Y. Zhou, R. Kannappan, F. Pasqualini, H. O'Malley, M. Sundman, et al. 2015. Late Na(+) current and protracted electrical recovery are critical determinants of the aging myopathy. Nat. Commun. 6:8803. https ://doi. org /10. 1038 /ncomms9803
41. Subramanian, A., P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, E.S. Lander, and J.P. Mesirov. 2005. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA. 102:15545-15550. https ://doi. org /10. 1073 /pnas. 0506580102
42. Sun, L., M.C. Louie, K.M. Vannella, C.A. Wilke, A.M. LeVine, B.B. Moore, and T.P. Shanley. 2011. New concepts of IL-10-induced lung fibrosis: Fibrocyte recruitment and M2 activation in a CCL2/CCR2 axis. Am. J. Physiol. Lung Cell. Mol. Physiol. 300:L341-L353. https ://doi. org /10. 1152 /ajplung. 00122. 2010
43. Tawakol, A., Z.A. Fayad, R. Mogg, A. Alon, M.T. Klimas, H. Dansky, S.S. Subramanian, A. Abdelbaky, J.H. Rudd, M.E. Farkouh, et al. 2013. Intensification of statin therapy results in a rapid reduction in atherosclerotic inflammation: Results of a multicenter fluorodeoxyglucose-positron emission tomography/computed tomography feasibility study. J. Am. Coll. Cardiol. 62:909-917. https ://doi. org /10. 1016 /j. jacc. 2013. 04. 066
44. Troidl, C., H. Möllmann, H. Nef, F. Masseli, S. Voss, S. Szardien, M. Willmer, A. Rolf, J. Rixe, K. Troidl, et al. 2009. Classically and alternatively activated macrophages contribute to tissue remodelling after myocardial infarction. J. Cell. Mol. Med. 13(9b, 9B):3485-3496. https ://doi. org /10. 1111 /j. 1582-4934. 2009. 00707. x
45. Valero-Muñoz, M., S. Li, R.M. Wilson, M. Hulsmans, T. Aprahamian, J.J. Fuster, M. Nahrendorf, P.E. Scherer, and F. Sam. 2016. Heart failure with preserved ejection fraction induces beiging in adipose tissue. Circ Heart Fail. 9:e002724. https ://doi. org /10. 1161 /CIR CHE ART FAI LURE. 115. 002724
46. Vasan, R.S., M.G. Larson, E.J. Benjamin, J.C. Evans, C.K. Reiss, and D. Levy. 1999. Congestive heart failure in subjects with normal versus reduced left ventricular ejection fraction: Prevalence and mortality in a population-based cohort. J. Am. Coll. Cardiol. 33:1948-1955. https ://doi. org /10. 1016 /S0735-1097(99)00118-7
47. Verma, S.K., P. Krishnamurthy, D. Barefield, N. Singh, R. Gupta, E. Lambers, M. Thal, A. Mackie, E. Hoxha, V. Ramirez, et al. 2012. Interleukin-10 treatment attenuates pressure overload-induced hypertrophic remodeling and improves heart function via signal transducers and activators of transcription 3-dependent inhibition of nuclear factor-κB. Circulation. 126:418-429. https ://doi. org /10. 1161 /CIR CUL ATI ONA HA. 112. 112185
48. Westermann, D., D. Lindner, M. Kasner, C. Zietsch, K. Savvatis, F. Escher, J. von Schlippenbach, C. Skurk, P. Steendijk, A. Riad, et al. 2011. Cardiac inflammation contributes to changes in the extracellular matrix in patients with heart failure and normal ejection fraction. Circ Heart Fail. 4:44-52. https ://doi. org /10. 1161 /CIR CHE ART FAI LURE. 109. 931451
49. Wick, G., C. Grundtman, C. Mayerl, T.F. Wimpissinger, J. Feichtinger, B. Zelger, R. Sgonc, and D. Wolfram. 2013. The immunology of fibrosis. Annu. Rev. Immunol. 31:107-135. https ://doi. org /10. 1146 /annurev-immunol-032712-095937
50. Yancy, C.W., M. Jessup, B. Bozkurt, J. Butler, D.E. Casey Jr., M.M. Colvin, M.H. Drazner, G. Filippatos, G.C. Fonarow, M.M. Givertz, et al. WRI TING COM MIT TEE MEM BERS. 2016. 2016 ACC/AHA/ HFSA Focused Update on New Pharmacological Therapy for Heart Failure: An Update of the 2013 ACCF/AHA Guideline for the Management of Heart Failure: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines and the Heart Failure Society of America. Circulation. 134:e282-e293. https ://doi. org /10. 1161 /CIR. 0000000000000435
51. Yona, S., K.W. Kim, Y. Wolf, A. Mildner, D. Varol, M. Breker, D. Strauss-Ayali, S. Viukov, M. Guilliams, A. Misharin, et al. 2013. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity. 38:79-91. https ://doi. org /10. 1016 /j. immuni. 2012. 12. 001
52. Zile, M.R., C.F. Baicu, J.S. Ikonomidis, R.E. Stroud, P.J. Nietert, A.D. Bradshaw, R. Slater, B.M. Palmer, P. Van Buren, M. Meyer, et al. 2015. Myocardial stiffness in patients with heart failure and a preserved ejection fraction: Contributions of collagen and titin. Circulation. 131:1247-1259. https :// doi. org /10. 1161 /CIR CUL ATI ONA HA. 114. 013215