Angiotensin-converting enzyme inhibition prevents the release of monocytes from their splenic reservoir in mice with myocardial infarction

Circulation Research

Volumn 107, Issue 11, 2010, Pages 1364-1373

  Leuschner, Florian ^a   Panizzi, Peter ^a   Chico Calero, Isabel ^a   Lee, Won Woo ^a   Ueno, Takuya ^a   Cortez Retamozo, Virna ^a   Waterman, Peter ^a   Gorbatov, Rostic ^a   Marinelli, Brett ^a   Iwamoto, Yoshiko ^a   Chudnovskiy, Aleksey ^a   Figueiredo, Jose Luiz ^a   Sosnovik, David E ^a   Pittet, Mikael J ^a   Swirski, Filip K ^a   Weissleder, Ralph ^a   Nahrendorf, Matthias ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

ACE inhibitor; Heart failure; Monocyte; Myocardial infarction; Spleen

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; BIOLOGICAL MARKER; ENALAPRIL; HYDRALAZINE;

ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CARDITIS; CELL MIGRATION; CELL MOTILITY; COMPUTER ASSISTED TOMOGRAPHY; CORONARY ARTERY LIGATION; ENZYME INHIBITION; FEMALE; FLOW CYTOMETRY; FLUORESCENCE IMAGING; HEART EJECTION FRACTION; HEART INFARCTION; HEART INFARCTION SIZE; HEART MUSCLE ISCHEMIA; INTRACELLULAR SIGNALING; MICROSCOPY; MONOCYTE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN DEGRADATION; REPERFUSION INJURY; SPLEEN; SPLENECTOMY; TISSUE REPAIR; WESTERN BLOTTING; X RAY FLUORESCENCE;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; CELL MOVEMENT; ENALAPRIL; FEMALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MONOCYTES; MYOCARDIAL INFARCTION; SPLEEN;

EID: 78650418632     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.227454     Document Type: Article

References (52)

1. Antman EM, Anbe DT, Armstrong PW, Bates ER, Green LA, Hand M, Hochman JS, Krumholz HM, Kushner FG, Lamas GA, Mullany CJ,Ornato JP, Pearle DL, Sloan MA, Smith SCJ, Alpert JS, Anderson JL, Faxon DP, Fuster V, Gibbons RJ, Gregoratos G, Halperin JL, Hiratzka LF, Hunt SA, Jacobs AK. CC/AHA uidelines for the management of patients with ST-elevation myocardial infarction: A report of the American ollege of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee to Revise he 1999 Guidelines for the Management of Patients with Acute Myocardial Infarction). Circulation. 2004;110:e82-e292.
2. Pfeffer MA, Braunwald E, Moye LA, Basta L, Brown EJ Jr, Cuddy TE, Davis BR, Geltman EM, oldman S, Flaker GC, Klein M, Lamas GA, Packer M, Rouleau J, Rouleau JL, Rutherford J, Wertheimer H, Hawkins CM, on behalf of the SAVE Investigators. Effect of captopril on mortality and morbidity in atients with left ventricular dysfunction after myocardial infarction. Results of the survival and ventricular nlargement trial. The SAVE Investigators. N Engl J Med. 1992;327:669-677.
3. Pfeffer MA, Braunwald E. Ventricular remodeling after myocardial infarction. Experimental bservations nd clinical implications. Circulation. 1990;81:1161-1172.
4. Dzau VJ, Bernstein K, Celermajer D, Cohen J, Dahlof B, Deanfield J, Diez J, Drexler H, Ferrari R, Van ilst W, Hansson L, Hornig B, Husain A, Johnston C, Lazar H, Lonn E, Luscher T, Mancini J, Mimran A, Pepine C, Rabelink T, Remme W, Ruilope L, Ruzicka M, Schunkert H, Swedberg K, Unger T, Vaughan D, eber M. Pathophysiologic and therapeutic importance of tissue ACE: A consensus report. CardiovascDrugs Ther. 2002;16:149-160.
5. Platten M, Youssef S, Hur EM, Ho PP, Han MH, Lanz TV, Phillips LK, Goldstein MJ, Bhat R, Raine S, Sobel RA, Steinman L. Blocking angiotensin-converting enzyme induces potent regulatory T cells and modulates TH1- and TH17-mediated autoimmunity. Proc Natl Acad Sci U S A. 2009;106:14948-14953.
6. Swirski F, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo J, Kohler R, Chudnovskiy A, Waterman P, Aikawa E, Mempel T, Libby P, Weissleder R, Pittet M. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 2009;325:612-616.
7. Tsubakimoto Y, Yamada H, Yokoi H, Kishida S, Takata H, Kawahito H, Matsui A, Urao N, Nozawa Y, Hirai H, Imanishi J, Ashihara E, Maekawa T, Takahashi T, Okigaki M, Matsubara H. Bone marrow angiotensin AT1 receptor regulates differentiation of monocyte lineage progenitors from hematopoietic stem cells. Arterioscler Thromb Vasc Biol. 2009;29: 1529-1536.
8. Blais CJ, Lapointe N, Rouleau JL, Clement R, Bachvarov DR, Adam A. Effects of captopril and omapatrilat on early post-myocardial infarction survival and cardiac hemodynamics in rats: Interaction with cardiac cytokine expression. Can J Physiol Pharmacol. 2002;80:48-58. (Pubitemid 34194286)
9. Peng H, Carretero OA, Vuljaj N, Liao TD, Motivala A, Peterson EL, Rhaleb NE. Angiotensin-converting enzyme inhibitors: A new mechanism of action. Circulation. 2005;112:2436-2445.
10. Young JB. Angiotensin-converting enzyme inhibitors and cytokines in heart failure: Dose and effect? J Am Coll Cardiol. 1999;34:2068 -2071.
11. Bujak M, Frangogiannis NG. The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc Res. 2007;74: 184-195.
12. Dewald O, Zymek P, Winkelmann K, Koerting A, Ren G, Abou-Khamis T, Michael LH, Rollins BJ, Entman ML, Frangogiannis NG. CCL2/ monocyte chemoattractant protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circ Res. 2005;96:881-889.
13. Cleutjens JP, Blankesteijn WM, Daemen MJ, Smits JF. The infracted myocardium: Simply dead tissue, or a lively target for therapeutic interventions. Cardiovasc Res. 1999;44:232-241.
14. Frangogiannis NG, Smith CW, Entman ML. The inflammatory response in myocardial infarction. Cardiovasc Res. 2002;53:31-47.
15. Frantz S, Bauersachs J, Ertl G. Post-infarct remodelling: Contribution of wound healing and inflammation. Cardiovasc Res. 2009;81:474-481.
16. French BA, Kramer CM. Mechanisms of post-infarct left ventricular remodeling. Drug Discov Today Dis Mech. 2007;4:185-196.
17. Panizzi P, Swirski FK, Figueiredo JL, Waterman P, Sosnovik DE, Aikawa E, Libby P, Pittet M, Weissleder R, Nahrendorf M. Impaired infarct healing in atherosclerotic mice with Ly-6C(hi) monocytosis. J Am Coll Cardiol. 2010;55:1629-1638.
18. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL, Libby P, Weissleder R, Pittet MJ. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med. 2007;204:3037-3047.
19. Maekawa Y, Anzai T, Yoshikawa T, Asakura Y, Takahashi T, Ishikawa S, Mitamura H, Ogawa S. Prognostic significance of peripheral monocytosis after reperfused acute myocardial infarction: A possible role for left ventricular remodeling. J Am Coll Cardiol. 2002;39:241-246.
20. Mariani M, Fetiveau R, Rossetti E, Poli A, Poletti F, Vandoni P, D'Urbano M, Cafiero F, Mariani G, Klersy C, De Servi S. Significance of total and differential leucocyte count in patients with acute myocardialinfarction treated with primary coronary angioplasty. Eur Heart J. 2006; 27:2511-2515.
21. Tsujioka H, Imanishi T, Ikejima H, Kuroi A, Takarada S, Tanimoto T, Kitabata H, Okochi K, Arita Y, Ishibashi K, Komukai K, Kataiwa H, Nakamura N, Hirata K, Tanaka A, Akasaka T. Impact of heterogeneity of human peripheral blood monocyte subsets on myocardial salvage in patients with primary acute myocardial infarction. J Am Coll Cardiol. 2009;54:130-138.
22. Luster AD, Alon R, von Andrian UH. Immune cell migration in inflammation: Present and future therapeutic targets. Nat Immunol. 2005;6: 1182-1190.
23. Nahrendorf M, Hu K, Frantz S, Jaffer FA, Tung CH, Hiller KH, Voll S, Nordbeck P, Sosnovik D, Gattenlöhner S, Novikov M, Dickneite G, Reed GL, Jakob P, Rosenzweig A, Bauer WR, Weissleder R, Ertl G. Factor XIII deficiency causes cardiac rupture, impairs wound healing, and aggravates cardiac remodeling in mice with myocardial infarction. Circulation. 2006;113:1196-1202.
24. Gard PR, Mandy A, Sutcliffe MA. Evidence of a possible role of altered angiotensin function in the treatment, but not etiology, of depression. Biol Psychiatry. 1999;45:1030-1034.
25. Nascimben L, Friedrich J, Liao R, Pauletto P, Pessina AC, Ingwall JS. Enalapril treatment increases cardiac performance and energy reserve via the creatine kinase reaction in myocardium of Syrian myopathic hamsters with advanced heart failure. Circulation. 1995;91:1824-1833.
26. Liu YH, Xu J, Yang XP, Yang F, Shesely E, Carretero OA. Effect of ACE inhibitors and angiotensin II type 1 receptor antagonists on endothelial NO synthase knockout mice with heart failure. Hypertension. 2002;39: 375-381.
27. Xu J, Carretero OA, Liu YH, Shesely EG, Yang F, Kapke A, Yang XP. Role of AT2 receptors in the cardioprotective effect of AT1 antagonists in mice. Hypertension. 2002;40:244-250.
28. Kanamori H, Takemura G, Li Y, Okada H, Maruyama R, Aoyama T, Miyata S, Esaki M, Ogino A, Nakagawa M, Ushikoshi H, Kawasaki M, Minatoguchi S, Fujiwara H. Inhibition of Fas-associated apoptosis in granulation tissue cells accompanies attenuation of postinfarction left ventricular remodeling by olmesartan. Am J Physiol Heart Circ Physiol. 2007;292:H2184-H2194.
29. Dunay IR, Damatta RA, Fux B, Presti R, Greco S, Colonna M, Sibley LD. Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity. 2008;29:306-317.
30. Nahrendorf M, Waterman P, Thurber G, Groves K, Rajopadhye M, Panizzi P, Marinelli B, Aikawa E, Pittet MJ, Swirski FK, Weissleder R. Hybrid in vivo FMT-CT imaging of protease activity in atherosclerosis with customized nanosensors. Arterioscler Thromb Vasc Biol. 2009;29: 1444-1451. .
31. Nahrendorf M, Sosnovik DE, Waterman P, Swirski FK, Pande AN, Aikawa E, Figueiredo JL, Pittet MJ, Weissleder R. Dual channel optical tomographic imaging of leukocyte recruitment and protease activity in the healing myocardial infarct. Circ Res. 2007;100:1218-1225. .
32. Daugherty A, Rateri D, Hong L, Balakrishnan A. Measuring blood pressure in mice using volume pressure recording, a tail-cuff method. J Vis Exp. 2009;15:1291.
33. AbdAlla S, Lother H, Langer A, Faramawy Y, Quitterer U. Factor XIIIA transglutaminase crosslinks AT1 receptor dimers of monocytes at the onset of atherosclerosis. Cell. 2004;119:343-354. .
34. Nahrendorf M, Pittet MJ, Swirski FK. Monocytes: Protagonists of infarct inflammation and repair after myocardial infarction. Circulation. 2010; 121:2437-2445. .
35. Nahrendorf M, Badea C, Hedlund LW, Figueiredo JL, Sosnovik DE, Johnson GA, Weissleder R. High-resolution imaging of murine myocardial infarction with delayed-enhancement cine micro-CT. Am J Physiol Heart Circ Physiol. 2007;292:H3172-H3178. .
36. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger V, Rosamond W, Sacco R, Sorlie P, Stafford R, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J. Heart Disease and Stroke Statistics-2010 Update. A Report From the American Heart Association. Circulation. 2010;121:e46-e215.
37. Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, Weissleder R, Pittet MJ. Ly-6Chi monocytes dominate hypercholesterolemiaassociated monocytosis and give rise to macrophages in atheromata. J Clin Invest. 2007;117:195-205.
38. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868-874.
39. Swirski FK, Pittet MJ, Kircher MF, Aikawa E, Jaffer FA, Libby P, Weissleder R. Monocyte accumulation in mouse atherogenesis is progressive and proportional to extent of disease. Proc Natl Acad Sci U S A. 2006;103:10340-10345.
40. Mulder P, Devaux B, Richard V, Henry JP, Wimart MC, Thibout E, Mace B, Thuillez C. Early versus delayed angiotensin-converting enzyme inhibition in experimental chronic heart failure. Effects on survival, hemodynamics, and cardiovascular remodeling. Circulation. 1997;95: 1314-1319. .
41. Wollert KC, Studer R, Doerfer K, Schieffer E, Holubarsch C, Just H, Drexler H. Differential effects of kinins on cardiomyocyte hypertrophy and interstitial collagen matrix in the surviving myocardium after myocardial infarction in the rat. Circulation. 1997;95:1910-1917.
42. Jugdutt BI, Lucas A, Khan MI. Effect of angiotensin-converting enzyme inhibition on infarct collagen deposition and remodelling during healing after transmural canine myocardial infarction. Can J Cardiol. 1997;13: 657-668.
43. Jugdutt BI. Ventricular remodeling after infarction and the extracellular collagen matrix: When is enough enough? Circulation. 2003;108: 1395-1403.
44. Zughaib ME, Sun JZ, Bolli R. Effect of angiotensin-converting enzyme inhibitors on myocardial ischemia/reperfusion injury: An overview. Basic Res Cardiol. 1993;88(Suppl 1):155-167. .
45. Przyklenk K, Kloner RA. Relationships between structure and effects of ACE inhibitors: Comparative effects in myocardial ischaemic/reperfusion injury. Br J Clin Pharmacol. 1989;28(Suppl 2):167S-175S. .
46. Lazar HL, Bao Y, Rivers S, Colton T, Bernard SA. High tissue affinity angiotensin-converting enzyme inhibitors improve endothelial function and reduce infarct size. Ann Thorac Surg. 2001;72:548-553.
47. Robinette CD, Fraumeni JFJ. Splenectomy and subsequent mortality in veterans of the 1939-45 war. Lancet. 1977;2:127-129.
48. Pfeffer MA, Greaves SC, Arnold JM, Glynn RJ, LaMotte FS, Lee RT, Menapace FJJ, Rapaport E, Ridker PM, Rouleau JL, Solomon SD, Hennekens CH. Early versus delayed angiotensin-converting enzyme inhibition therapy in acute myocardial infarction. The healing and early afterload reducing therapy trial. Circulation. 1997;95:2643-2651.
49. Ambrosioni E, Borghi C, Magnani B. The effect of the angiotensinconverting- enzyme inhibitor zofenopril on mortality and morbidity after anterior myocardial infarction. The Survival of Myocardial Infarction Long-Term Evaluation (SMILE) Study Investigators. N Engl J Med. 1995;332:80-85.
50. Sosnovik DE, Nahrendorf M, Weissleder R. Molecular magnetic resonance imaging in cardiovascular medicine. Circulation. 2007;115:2076-2086. . (Pubitemid 46625959)
51. Swirski FK, Wildgruber M, Ueno T, Figueiredo JL, Panizzi P, Iwamoto Y, Zhang E, Stone JR, Rodriguez E, Chen JW, Pittet MJ, Weissleder R, Nahrendorf M. Myeloperoxidase-rich Ly-6C+ myeloid cells infiltrate allografts and contribute to an imaging signature of organ rejection in mice. J Clin Invest. 2010;120:2627-2634. .
52. Su H, Spinale FG, Dobrucki LW, Song J, Hua J, Sweterlitsch S, Dione DP, Cavaliere P, Chow C, Bourke BN, Hu XY, Azure M, Yalamanchili P, Liu R, Cheesman EH, Robinson S, Edwards DS, Sinusas AJ. Noninvasive targeted imaging of matrix metalloproteinase activation in a murine model of postinfarction remodeling. Circulation. 2005;112:3157-3167.