Complement component 3 is necessary to preserve myocardium and myocardial function in chronic myocardial infarction

Stem Cells

Volumn 32, Issue 9, 2014, Pages 2502-2515

  Wysoczynski, Marcin ^a   Solanki, Mitesh ^a   Borkowska, Sylwia ^b   Van Hoose, Patrick ^a   Brittian, Kenneth R ^a   Prabhu, Sumanth D ^a,c   Ratajczak, Mariusz Z ^b   Rokosh, Gregg ^a  

^a University of Louisville School of Medicine   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

Complement component C3; Mobilization; Myocardial infarction; Myocardial regeneration; Stem cells

Indexed keywords

ACTIN; BROXURIDINE; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C5; TRANSCRIPTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BLOOD CELL COUNT; CAPILLARY DENSITY; CFU COUNTING; COMPLEMENT ACTIVATION; CONTROLLED STUDY; CORONARY ARTERY LIGATION; DISEASE EXACERBATION; DNA REPLICATION; ECHOCARDIOGRAPHY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FOLLOW UP; HEART DISEASE; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE CAPILLARY; HEMATOPOIETIC STEM CELL; HISTOPATHOLOGY; IN VIVO STUDY; INFLAMMATION; MORPHOMETRICS; MOUSE; NICK END LABELING; NONHUMAN; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCAR; SCAR FORMATION; SHAM PROCEDURE; STEM CELL; STEM CELL MOBILIZATION; SYSTOLE; ANIMAL; C57BL MOUSE; CELL PROLIFERATION; DISEASE MODEL; ECHOGRAPHY; GENETICS; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; REGENERATION;

ANIMALS; CELL PROLIFERATION; COMPLEMENT C3; DISEASE MODELS, ANIMAL; ECHOCARDIOGRAPHY; FEMALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL INFARCTION; MYOCARDIUM; REGENERATION; VENTRICULAR FUNCTION, LEFT;

EID: 84906217707     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1743     Document Type: Article

References (67)

1. Arumugam TV, Magnus T, Woodruff TM, et al. Complement mediators in ischemia-reperfusion injury. Clin Chim Acta 2006; 374: 33-45.
2. Amara U, Rittirsch D, Flierl M, et al. Interaction between the coagulation and complement system. Adv Exp Med Biol 2008; 632: 71-79.
3. Hill JH, Ward PA,. The phlogistic role of C3 leukotactic fragments in myocardial infarcts of rats. J Exp Med 1971; 133: 885-900.
4. Crawford MH, Grover FL, Kolb WP, et al. Complement and neutrophil activation in the pathogenesis of ischemic myocardial injury. Circulation 1988; 78: 1449-1458.
5. Vakeva AP, Agah A, Rollins SA, et al. Myocardial infarction and apoptosis after myocardial ischemia and reperfusion: Role of the terminal complement components and inhibition by anti-C5 therapy. Circulation 1998; 97: 2259-2267.
6. De Vries B, Matthijsen RA, Wolfs TG, et al. Inhibition of complement factor C5 protects against renal ischemia-reperfusion injury: Inhibition of late apoptosis and inflammation. Transplantation 2003; 75: 375-382.
7. Vakeva A, Morgan BP, Tikkanen I, et al. Time course of complement activation and inhibitor expression after ischemic injury of rat myocardium. Am J Pathol 1994; 144: 1357-1368.
8. Busche MN, Stahl GL,. Role of the complement components C5 and C3a in a mouse model of myocardial ischemia and reperfusion injury. Ger Med Sci 2010; 8.
9. Maroko PR, Carpenter CB, Chiariello M, et al. Reduction by cobra venom factor of myocardial necrosis after coronary artery occlusion. J Clin Invest 1978; 61: 661-670.
10. Granger CB, Mahaffey KW, Weaver WD, et al. Pexelizumab, an anti-C5 complement antibody, as adjunctive therapy to primary percutaneous coronary intervention in acute myocardial infarction: The COMplement inhibition in Myocardial infarction treated with Angioplasty (COMMA) trial. Circulation 2003; 108: 1184-1190.
11. Mahaffey KW, Granger CB, Nicolau JC, et al. Effect of pexelizumab, an anti-C5 complement antibody, as adjunctive therapy to fibrinolysis in acute myocardial infarction: The COMPlement inhibition in myocardial infarction treated with thromboLYtics (COMPLY) trial. Circulation 2003; 108: 1176-1183.
12. Martel C, Granger CB, Ghitescu M, et al. Pexelizumab fails to inhibit assembly of the terminal complement complex in patients with ST-elevation myocardial infarction undergoing primary percutaneous coronary intervention. Insight from a substudy of the Assessment of Pexelizumab in Acute Myocardial Infarction (APEX-AMI) trial. Am Heart J 2012; 164: 43-51.
13. Smith PK, Shernan SK, Chen JC, et al. Effects of C5 complement inhibitor pexelizumab on outcome in high-risk coronary artery bypass grafting: Combined results from the PRIMO-CABG I and II trials. J Thorac Cardiovasc Surg 2011; 142: 89-98.
14. Ignatius A, Ehrnthaller C, Brenner RE, et al. The anaphylatoxin receptor C5aR is present during fracture healing in rats and mediates osteoblast migration in vitro. J Trauma 2011; 71: 952-960.
15. Kimura Y, Madhavan M, Call MK, et al. Expression of complement 3 and complement 5 in newt limb and lens regeneration. J Immunol 2003; 170: 2331-2339.
16. Markiewski MM, Mastellos D, Tudoran R, et al. C3a and C3b activation products of the third component of complement (C3) are critical for normal liver recovery after toxic injury. J Immunol 2004; 173: 747-754.
17. Mastellos D, Papadimitriou JC, Franchini S, et al. A novel role of complement: Mice deficient in the fifth component of complement (C5) exhibit impaired liver regeneration. J Immunol 2001; 166: 2479-2486.
18. Reca R, Mastellos D, Majka M, et al. Functional receptor for C3a anaphylatoxin is expressed by normal hematopoietic stem/progenitor cells, and C3a enhances their homing-related responses to SDF-1. Blood 2003; 101: 3784-3793.
19. Schoengraf P, Lambris JD, Recknagel S, et al. Does complement play a role in bone development and regeneration? Immunobiology 2012; 218: 1-9.
20. Shinjyo N, Stahlberg A, Dragunow M, et al. Complement-derived anaphylatoxin C3a regulates in vitro differentiation and migration of neural progenitor cells. Stem Cells 2009; 27: 2824-2832.
21. Strey CW, Markiewski M, Mastellos D, et al. The proinflammatory mediators C3a and C5a are essential for liver regeneration. J Exp Med 2003; 198: 913-923.
22. Brennan FH, Anderson AJ, Taylor SM, et al. Complement activation in the injured central nervous system: Another dual-edged sword? J Neuroinflammation 2012; 9: 137.
23. Janowska-Wieczorek A, Marquez-Curtis LA, Shirvaikar N, et al. The role of complement in the trafficking of hematopoietic stem/progenitor cells. Transfusion (Paris) 2012; 52: 2706-2716.
24. Kim CH, Wu W, Wysoczynski M, et al. Conditioning for hematopoietic transplantation activates the complement cascade and induces a proteolytic environment in bone marrow: A novel role for bioactive lipids and soluble C5b-C9 as homing factors. Leukemia 2012; 26: 106-116.
25. Ratajczak MZ, Reca R, Wysoczynski M, et al. Transplantation studies in C3-deficient animals reveal a novel role of the third complement component (C3) in engraftment of bone marrow cells. Leukemia 2004; 18: 1482-1490.
26. Ratajczak MZ, Reca R, Wysoczynski M, et al. Modulation of the SDF-1-CXCR4 axis by the third complement component (C3)-Implications for trafficking of CXCR4+ stem cells. Exp Hematol 2006; 34: 986-995.
27. Reca R, Wysoczynski M, Yan J, et al. The role of third complement component (C3) in homing of hematopoietic stem/progenitor cells into bone marrow. Adv Exp Med Biol. 2006; 586: 35-51.
28. Wysoczynski M, Reca R, Lee H, et al. Defective engraftment of C3aR-/- hematopoietic stem progenitor cells shows a novel role of the C3a-C3aR axis in bone marrow homing. Leukemia 2009; 23: 1455-1461.
29. Dai S, Yuan F, Mu J, et al. Chronic AMD3100 antagonism of SDF-1alpha-CXCR4 exacerbates cardiac dysfunction and remodeling after myocardial infarction. J Mol Cell Cardiol 2010; 49: 587-597.
30. Hamid T, Gu Y, Ortines RV, et al. Divergent tumor necrosis factor receptor-related remodeling responses in heart failure: Role of nuclear factor-kappaB and inflammatory activation. Circulation 2009; 119: 1386-1397.
31. Tang XL, Rokosh G, Sanganalmath SK, et al. Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation 2010; 121: 293-305.
32. Beltrami AP, Barlucchi L, Torella D, et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003; 114: 763-776.
33. Fransioli J, Bailey B, Gude NA, et al. Evolution of the c-kit-positive cell response to pathological challenge in the myocardium. Stem Cells 2008; 26: 1315-1324.
34. Loffredo FS, Steinhauser ML, Gannon J, et al. Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell 2011; 8: 389-398.
35. Suzuki G, Iyer V, Lee TC, et al. Autologous mesenchymal stem cells mobilize cKit+ and CD133+ bone marrow progenitor cells and improve regional function in hibernating myocardium. Circ Res 2011; 109: 1044-1054.
36. Senyo SE, Steinhauser ML, Pizzimenti CL, et al. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013; 493: 433-436.
37. Wyderka R, Wojakowski W, Jadczyk T, et al. Mobilization of CD34+CXCR4+ stem/progenitor cells and the parameters of left ventricular function and remodeling in 1-year follow-up of patients with acute myocardial infarction. Mediators Inflamm 2012; 2012: 564027.
38. Kucia M, Dawn B, Hunt G, et al. Cells expressing early cardiac markers reside in the bone marrow and are mobilized into the peripheral blood after myocardial infarction. Circ Res 2004; 95: 1191-1199.
39. Kucia M, Reca R, Campbell FR, et al. A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia 2006; 20: 857-869.
40. Wojakowski W, Tendera M,. Mobilization of bone marrow-derived progenitor cells in acute coronary syndromes. Folia Histochem Cytobiol 2005; 43: 229-232.
41. Wojakowski W, Tendera M, Michalowska A, et al. Mobilization of CD34/CXCR4+, CD34/CD117+, c-met+ stem cells, and mononuclear cells expressing early cardiac, muscle, and endothelial markers into peripheral blood in patients with acute myocardial infarction. Circulation 2004; 110: 3213-3220.
42. Orlic D, Kajstura J, Chimenti S, et al. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci USA 2001; 98: 10344-10349.
43. Buerke M, Murohara T, Lefer AM,. Cardioprotective effects of a C1 esterase inhibitor in myocardial ischemia and reperfusion. Circulation 1995; 91: 393-402.
44. Buerke M, Prufer D, Dahm M, et al. Blocking of classical complement pathway inhibits endothelial adhesion molecule expression and preserves ischemic myocardium from reperfusion injury. J Pharmacol Exp Ther 1998; 286: 429-438.
45. Buerke M, Schwertz H, Seitz W, et al. Novel small molecule inhibitor of C1s exerts cardioprotective effects in ischemia-reperfusion injury in rabbits. J Immunol 2001; 167: 5375-5380.
46. Walsh MC, Bourcier T, Takahashi K, et al. Mannose-binding lectin is a regulator of inflammation that accompanies myocardial ischemia and reperfusion injury. J Immunol 2005; 175: 541-546.
47. Weisman HF, Bartow T, Leppo MK, et al. Soluble human complement receptor type 1: In vivo inhibitor of complement suppressing post-ischemic myocardial inflammation and necrosis. Science 1990; 249: 146-151.
48. Busche MN, Pavlov V, Takahashi K, et al. Myocardial ischemia and reperfusion injury is dependent on both IgM and mannose-binding lectin. Am J Physiology Heart Circ Physiol 2009; 297: H1853-H1859.
49. Landmesser U, Engberding N, Bahlmann FH, et al. Statin-induced improvement of endothelial progenitor cell mobilization, myocardial neovascularization, left ventricular function, and survival after experimental myocardial infarction requires endothelial nitric oxide synthase. Circulation 2004; 110: 1933-1939.
50. Takahashi T, Kalka C, Masuda H, et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 1999; 5: 434-438.
51. Kocher AA, Schuster MD, Szabolcs MJ, et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 2001; 7: 430-436.
52. Yamaguchi J, Kusano KF, Masuo O, et al. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 2003; 107: 1322-1328.
53. Jujo K, Hamada H, Iwakura A, et al. CXCR4 blockade augments bone marrow progenitor cell recruitment to the neovasculature and reduces mortality after myocardial infarction. Proc Natl Acad Sci USA 2010; 107: 11008-11013.
54. Riley RD, Sato H, Zhao ZQ, et al. Recombinant human complement C5a receptor antagonist reduces infarct size after surgical revascularization. J Thorac Cardiovasc Surg 2000; 120: 350-358.
55. Pawlinski R, Tencati M, Hampton CR, et al. Protease-activated receptor-1 contributes to cardiac remodeling and hypertrophy. Circulation 2007; 116: 2298-2306.
56. Kajstura J, Urbanek K, Perl S, et al. Cardiomyogenesis in the adult human heart. Circ Res 2010; 107: 305-315.
57. Schraufstatter IU, Discipio RG, Zhao M, et al. C3a and C5a are chemotactic factors for human mesenchymal stem cells, which cause prolonged ERK1/2 phosphorylation. J Immunol 2009; 182: 3827-3836.
58. Del Rio-Tsonis K, Tsonis PA, Zarkadis IK, et al. Expression of the third component of complement, C3, in regenerating limb blastema cells of urodeles. J Immunol 1998; 161: 6819-6824.
59. Abdel-Latif A, Bolli R, Tleyjeh IM, et al. Adult bone marrow-derived cells for cardiac repair: A systematic review and meta-analysis. Arch Intern Med 2007; 167: 989-997.
60. Zuba-Surma EK, Guo Y, Taher H, et al. Transplantation of expanded bone marrow-derived very small embryonic-like stem cells (VSEL-SCs) improves left ventricular function and remodelling after myocardial infarction. J Cell Mol Med 2011; 15: 1319-1328.
61. Wojakowski W, Tendera M, Kucia M, et al. Mobilization of bone marrow-derived Oct-4+ SSEA-4+ very small embryonic-like stem cells in patients with acute myocardial infarction. J Am Coll Cardiol 2009; 53: 1-9.
62. Lee HM, Wysoczynski M, Liu R, et al. Mobilization studies in complement-deficient mice reveal that optimal AMD3100 mobilization of hematopoietic stem cells depends on complement cascade activation by AMD3100-stimulated granulocytes. Leukemia 2010; 24: 573-582.
63. Lee HM, Wu W, Wysoczynski M, et al. Impaired mobilization of hematopoietic stem/progenitor cells in C5-deficient mice supports the pivotal involvement of innate immunity in this process and reveals novel promobilization effects of granulocytes. Leukemia 2009; 23: 2052-2062.
64. Ratajczak J, Reca R, Kucia M, et al. Mobilization studies in mice deficient in either C3 or C3a receptor (C3aR) reveal a novel role for complement in retention of hematopoietic stem/progenitor cells in bone marrow. Blood 2004; 103: 2071-2078.
65. Pfister O, Mouquet F, Jain M, et al. CD31- but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 2005; 97: 52-61.
66. Oyama T, Nagai T, Wada H, et al. Cardiac side population cells have a potential to migrate and differentiate into cardiomyocytes in vitro and in vivo. J Cell Biol 2007; 176: 329-341.
67. Nahrendorf M, Swirski FK, Aikawa E, et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 2007; 204: 3037-3047.