(Circulation. 1997;95:684-692.)
© 1997 American Heart Association, Inc.
Articles |
Complement C5a, TGF-ß1, and MCP-1, in Sequence, Induce Migration of Monocytes Into Ischemic Canine Myocardium Within the First One to Five Hours After Reperfusion
the Immunology Research Laboratory and the Research Center for AIDS and HIV Infections at the Houston Veterans Affairs Medical Center (H.H.B., D.M.G., J.T., R.D.R.); Section of Cardiovascular Sciences and DeBakey Heart Center, Methodist Hospital, Houston (K.A.Y., L.H.M., M.L.E.); Speros P. Martel Laboratory of Leukocyte Biology at Texas Children's Hospital, Houston (A.R.B., C.W.S.); Department of Pathology, University of Texas Medical Branch, Galveston (H.K.H.); Immunology Department, Leuko Site, Inc, Cambridge, Mass (C.R.M., G.J.L.); and the Departments of Otorhinolaryngology (H.H.B., D.M.G.), Medicine (J.T., K.A.Y., L.H.M., M.L.E., R.D.R.), Microbiology (H.H.B., C.W.S., R.D.R.), and Pediatrics (A.R.B., C.W.S.), Baylor College of Medicine, Houston, Tex.
Correspondence to Holly H. Birdsall, MD, PhD, Bldg 109, Room 230, Veterans Affairs Medical Center, 2002 Holcombe Blvd, Houston, TX 77030. E-mail birdsall@bcm.tmc.edu.
Background Recent studies suggest that reperfusion promotes healing of formerly ischemic heart tissue even when myocardial salvage is no longer possible. Since monocyte-macrophage infiltration is the hallmark of the healing infarct, we have attempted to identify mechanisms that attract monocytes into the heart after reperfusion of ischemic canine myocardium.
Methods and Results Isolated autologous 99mTc-labeled mononuclear leukocytes injected into the left atrium localized preferentially in previously ischemic myocardium within the first hour after reperfusion. Histological studies revealed CD64+ monocytes in small venules and the perivascular connective tissue within the first hour after reperfusion. Flow cytometric analysis of cells in cardiac lymph showed systematically increasing numbers of neutrophils and monocytes between 1 and 4 hours after reperfusion; monocyte enrichment was eventually greater than neutrophil enrichment. Monocyte chemotactic activity in cardiac lymph collected in the first hour after reperfusion was wholly attributable to C5a. Transforming growth factor (TGF)-ß1 contributed significantly to this chemotactic activity after 60 to 180 minutes, and after 180 minutes, monocyte chemotactic activity in lymph was largely dependent on monocyte chemoattractant protein (MCP)-1 acting in concert with TGF-ß1.
Conclusions Beginning in the first 60 minutes after reperfusion, C5a, TGF-ß1, and MCP-1, acting sequentially, promote infiltration of monocytes into formerly ischemic myocardium. These events may promote the healing of myocardial injury facilitated by reperfusion.
Key Words: leukocytes • blood cells • immune system • ischemia • reperfusion
This article has been cited by other articles:
 |
|
 |
|
  D. Chen, A. Carpenter, J. Abrahams, R. C. Chambers, R. I. Lechler, J. H. McVey, and A. Dorling Protease-activated receptor 1 activation is necessary for monocyte chemoattractant protein 1-dependent leukocyte recruitment in vivo J. Exp. Med., July 7, 2008; (2008) jem.20071427. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Fraccarollo, P. Galuppo, S. Schraut, S. Kneitz, N. van Rooijen, G. Ertl, and J. Bauersachs Immediate Mineralocorticoid Receptor Blockade Improves Myocardial Infarct Healing by Modulation of the Inflammatory Response Hypertension, April 1, 2008; 51(4): 905 - 914. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Natarajan, F. N. Salloum, B. J. Fisher, E. D. Ownby, R. C. Kukreja, and A. A. Fowler 3rd Activation of hypoxia-inducible factor-1 via prolyl-4 hydoxylase-2 gene silencing attenuates acute inflammatory responses in postischemic myocardium Am J Physiol Heart Circ Physiol, September 1, 2007; 293(3): H1571 - H1580. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Bujak and N. G. Frangogiannis The role of TGF-{beta} signaling in myocardial infarction and cardiac remodeling Cardiovasc Res, May 1, 2007; 74(2): 184 - 195. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Z. Yang, Y.-J. Day, M.-C. Toufektsian, Y. Xu, S. I. Ramos, M. A. Marshall, B. A. French, and J. Linden Myocardial Infarct-Sparing Effect of Adenosine A2A Receptor Activation Is due to Its Action on CD4+ T Lymphocytes Circulation, November 7, 2006; 114(19): 2056 - 2064. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Iwama, S. Uemura, N. Naya, K.-i. Imagawa, Y. Takemoto, O. Asai, K. Onoue, S. Okayama, S. Somekawa, Y. Kida, et al. Cardiac Expression of Placental Growth Factor Predicts the Improvement of Chronic Phase Left Ventricular Function in Patients With Acute Myocardial Infarction J. Am. Coll. Cardiol., April 18, 2006; 47(8): 1559 - 1567. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Xu, Y. Huo, M.-C. Toufektsian, S. I. Ramos, Y. Ma, A. D. Tejani, B. A. French, and Z. Yang Activated platelets contribute importantly to myocardial reperfusion injury Am J Physiol Heart Circ Physiol, February 1, 2006; 290(2): H692 - H699. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. A. Reichel, A. Khandoga, H.-J. Anders, D. Schlondorff, B. Luckow, and F. Krombach Chemokine receptors Ccr1, Ccr2, and Ccr5 mediate neutrophil migration to postischemic tissue J. Leukoc. Biol., January 1, 2006; 79(1): 114 - 122. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Banz, O. M. Hess, S. C. Robson, D. Mettler, P. Meier, A. Haeberli, E. Csizmadia, E. Y. Korchagina, N. V. Bovin, and R. Rieben Locally targeted cytoprotection with dextran sulfate attenuates experimental porcine myocardial ischaemia/reperfusion injury Eur. Heart J., November 1, 2005; 26(21): 2334 - 2343. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Sano, A. Tessitore, A. Ingrassia, and A. d'Azzo Chemokine-induced recruitment of genetically modified bone marrow cells into the CNS of GM1-gangliosidosis mice corrects neuronal pathology Blood, October 1, 2005; 106(7): 2259 - 2268. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Trial, R. D. Rossen, J. Rubio, and A. A. Knowlton Inflammation and Ischemia: Macrophages Activated by Fibronectin Fragments Enhance the Survival of Injured Cardiac Myocytes Experimental Biology and Medicine, June 1, 2004; 229(6): 538 - 545. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Vinten-Johansen Involvement of neutrophils in the pathogenesis of lethal myocardial reperfusion injury Cardiovasc Res, February 15, 2004; 61(3): 481 - 497. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y.-J. Day, M. A. Marshall, L. Huang, M. J. McDuffie, M. D. Okusa, and J. Linden Protection from ischemic liver injury by activation of A2A adenosine receptors during reperfusion: inhibition of chemokine induction Am J Physiol Gastrointest Liver Physiol, February 1, 2004; 286(2): G285 - G293. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. G. Frangogiannis, L. H. Mendoza, G. Ren, S. Akrivakis, P. L. Jackson, L. H. Michael, C. W. Smith, and M. L. Entman MCSF expression is induced in healing myocardial infarcts and may regulate monocyte and endothelial cell phenotype Am J Physiol Heart Circ Physiol, July 11, 2003; 285(2): H483 - H492. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. A. de Lemos, D. A. Morrow, M. S. Sabatine, S. A. Murphy, C. M. Gibson, E. M. Antman, C. H. McCabe, C. P. Cannon, and E. Braunwald Association Between Plasma Levels of Monocyte Chemoattractant Protein-1 and Long-Term Clinical Outcomes in Patients With Acute Coronary Syndromes Circulation, February 11, 2003; 107(5): 690 - 695. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. de Zwaan, A.H. Kleine, J.H.C. Diris, J.F.C. Glatz, H.J.J. Wellens, P.F.W. Strengers, M. Tissing, C.E. Hack, M.P. van Dieijen-Visser, and W.T. Hermens Continuous 48-h C1-inhibitor treatment, following reperfusion therapy, in patients with acute myocardial infarction Eur. Heart J., November 1, 2002; 23(21): 1670 - 1677. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. H.M. Lopes, S. S. Vasudevan, D. Gregg, B. Selvakumar, P. J. Pagano, H. Kovacic, and P. J. Goldschmidt-Clermont Rac-Dependent Monocyte Chemoattractant Protein-1 Production Is Induced by Nutrient Deprivation Circ. Res., November 1, 2002; 91(9): 798 - 805. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. K. D. Ng, S. S. Deshpande, K. Irani, and B. R. Alevriadou Adhesion of flowing monocytes to hypoxia-reoxygenation-exposed endothelial cells: role of Rac1, ROS, and VCAM-1 Am J Physiol Cell Physiol, July 1, 2002; 283(1): C93 - C102. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Zhang, L. L. McCormick, S. R. Desai, C. Wu, and A. C. Gilliam Murine Sclerodermatous Graft-Versus-Host Disease, a Model for Human Scleroderma: Cutaneous Cytokines, Chemokines, and Immune Cell Activation J. Immunol., March 15, 2002; 168(6): 3088 - 3098. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. O. Nossuli, N. G. Frangogiannis, P. Knuefermann, V. Lakshminarayanan, O. Dewald, A. J. Evans, J. Peschon, D. L. Mann, L. H. Michael, and M. L. Entman Brief murine myocardial I/R induces chemokines in a TNF-alpha -independent manner: role of oxygen radicals Am J Physiol Heart Circ Physiol, December 1, 2001; 281(6): H2549 - H2558. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. Lakshminarayanan, M. Lewallen, N. G. Frangogiannis, A. J. Evans, K. E. Wedin, L. H. Michael, and M. L. Entman Reactive Oxygen Intermediates Induce Monocyte Chemotactic Protein-1 in Vascular Endothelium after Brief Ischemia Am. J. Pathol., October 1, 2001; 159(4): 1301 - 1311. [Abstract] [Full Text]
|
|
|
|
|
|
M. Bhatia, A. K. Saluja, V. P. Singh, J.-L. Frossard, H.-S. Lee, L. Bhagat, C. Gerard, and M. L. Steer Complement factor C5a exerts an anti-inflammatory effect in acute pancreatitis and associated lung injury Am J Physiol Gastrointest Liver Physiol, May 1, 2001; 280(5): G974 - G978. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. H. Erlich, E. M. Boyle, J. Labriola, J. C. Kovacich, R. A. Santucci, C. Fearns, E. N. Morgan, W. Yun, T. Luther, O. Kojikawa, et al. Inhibition of the Tissue Factor-Thrombin Pathway Limits Infarct Size after Myocardial Ischemia-Reperfusion Injury by Reducing Inflammation Am. J. Pathol., December 1, 2000; 157(6): 1849 - 1862. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. G. Frangogiannis, L. H. Michael, and M. L. Entman Myofibroblasts in reperfused myocardial infarcts express the embryonic form of smooth muscle myosin heavy chain (SMemb) Cardiovasc Res, October 1, 2000; 48(1): 89 - 100. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-S. Silvestre, Z. Mallat, M. Duriez, R. Tamarat, M. F. Bureau, D. Scherman, N. Duverger, D. Branellec, A. Tedgui, and B. I. Levy Antiangiogenic Effect of Interleukin-10 in Ischemia-Induced Angiogenesis in Mice Hindlimb Circ. Res., September 15, 2000; 87(6): 448 - 452. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. G. Frangogiannis, L. H. Mendoza, M. L. Lindsey, C. M. Ballantyne, L. H. Michael, C. W. Smith, and M. L. Entman IL-10 Is Induced in the Reperfused Myocardium and May Modulate the Reaction to Injury J. Immunol., September 1, 2000; 165(5): 2798 - 2808. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. O. Nossuli, V. Lakshminarayanan, G. Baumgarten, G. E. Taffet, C. M. Ballantyne, L. H. Michael, and M. L. Entman A chronic mouse model of myocardial ischemia-reperfusion: essential in cytokine studies Am J Physiol Heart Circ Physiol, April 1, 2000; 278(4): H1049 - H1055. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. A. Youker, J. Beirne, J. Lee, L. H. Michael, C. W. Smith, and M. L. Entman Time-Dependent Loss of Mac-1 from Infiltrating Neutrophils in the Reperfused Myocardium J. Immunol., March 1, 2000; 164(5): 2752 - 2758. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. H. Michael, C. M. Ballantyne, J. P. Zachariah, K. E. Gould, J. S. Pocius, G. E. Taffet, C. J. Hartley, T. T. Pham, S. L. Daniel, E. Funk, et al. Myocardial infarction and remodeling in mice: effect of reperfusion Am J Physiol Heart Circ Physiol, August 1, 1999; 277(2): H660 - H668. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. G. Simms and K. R. Walley Activated macrophages decrease rat cardiac myocyte contractility: importance of ICAM-1-dependent adhesion Am J Physiol Heart Circ Physiol, July 1, 1999; 277(1): H253 - H260. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Tritto and G. Ambrosio Spotlight on microcirculation: an update Cardiovasc Res, June 1, 1999; 42(3): 600 - 606. [Full Text] [PDF]
|
|
|
|
|
|
H. J. Geissler, K. L. Davis, G. A. Laine, M. L. Brennan, U. Mehlhorn, and S. J. Allen Contamination of lymph from the major prenodal cardiac lymphatic in dogs Am J Physiol Heart Circ Physiol, May 1, 1999; 276(5): H1795 - H1800. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Gwechenberger, L. H. Mendoza, K. A. Youker, N. G. Frangogiannis, C. W. Smith, L. H. Michael, and M. L. Entman Cardiac Myocytes Produce Interleukin-6 in Culture and in Viable Border Zone of Reperfused Infarctions Circulation, February 2, 1999; 99(4): 546 - 551. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. A Woodcock, S. J Matkovich, and O. Binah Ins(1,4,5)P3 and cardiac dysfunction Cardiovasc Res, November 1, 1998; 40(2): 251 - 256. [Full Text] [PDF]
|
|
|
|
|
|
D. M. Green, J. Trial, and H. H. Birdsall TNF-{alpha} Released by Comigrating Monocytes Promotes Transendothelial Migration of Activated Lymphocytes J. Immunol., September 1, 1998; 161(5): 2481 - 2489. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. G. Frangogiannis, J. L. Perrard, L. H. Mendoza, A. R. Burns, M. L. Lindsey, C. M. Ballantyne, L. H. Michael, C. W. Smith, and M. L. Entman Stem Cell Factor Induction Is Associated With Mast Cell Accumulation After Canine Myocardial Ischemia and Reperfusion Circulation, August 18, 1998; 98(7): 687 - 698. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Aukrust, T. Ueland, F. Muller, A. K. Andreassen, I. Nordoy, H. Aas, J. Kjekshus, S. Simonsen, S. S. Froland, and L. Gullestad Elevated Circulating Levels of C-C Chemokines in Patients With Congestive Heart Failure Circulation, March 31, 1998; 97(12): 1136 - 1143. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. G. Kumar, C. M. Ballantyne, L. H. Michael, G. L. Kukielka, K. A. Youker, M. L. Lindsey, H. K. Hawkins, H. H. Birdsall, C. R. MacKay, G. J. LaRosa, et al. Induction of Monocyte Chemoattractant Protein-1 in the Small Veins of the Ischemic and Reperfused Canine Myocardium Circulation, February 4, 1997; 95(3): 693 - 700. [Abstract] [Full Text]
|
|