Journal of Vascular Surgery
Volume 45, Issue 6, Supplement , Pages A48-A56 , June 2007

The chemokine system in arteriogenesis and hind limb ischemia

  • Paula K. Shireman, MD

      Affiliations

    • Corresponding Author InformationReprint requests: Paula K. Shireman, MD, Associate Professor, Division of Vascular Surgery, MC 7741, 7703 Floyd Curl Dr, San Antonio, TX 78229-3900.

Received 21 December 2006 ,Accepted 11 February 2007.

References 

  1. Charo IF, Taubman MB. Chemokines in the pathogenesis of vascular disease. Circ Res. 2004;95:858–866
  2. Daley GQ, Goodell MA, Snyder EY. Realistic prospects for stem cell therapeutics. Hematology (Am Soc Hematol Educ Program). 2003;398–418
  3. Montgomery SP, Swiecki CW, Shriver CD. The evaluation of casualties from Operation Iraqi Freedom on return to the continental United States from March to June 2003. J Am Coll Surg. 2005;201:7–12discussion 12-3
  4. Marshall TJ. Combat casualty care: the Alpha Surgical Company experience during Operation Iraqi Freedom. Mil Med. 2005;170:469–472
  5. Blaisdell FW. The pathophysiology of skeletal muscle ischemia and the reperfusion syndrome: a review. Cardiovasc Surg. 2002;10:620–630
  6. Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol. 2001;91:534–551
  7. Shireman PK, Quinones MP. Differential necrosis despite similar perfusion in mouse strains after ischemia. J Surg Res. 2005;129:242–250
  8. Shireman PK, Contreras-Shannon V, Reyes-Reyna SM, Robinson SC, McManus LM. MCP-1 parallels inflammatory and regenerative responses in ischemic muscle. J Surg Res. 2006;134:145–157
  9. Scholz D, Thomas S, Sass S, Podzuweit T. Angiogenesis and myogenesis as two facets of inflammatory post-ischemic tissue regeneration. Mol Cell Biochem. 2003;246:57–67
  10. Scholz D, Ziegelhoeffer T, Helisch A, Wagner S, Friedrich C, Podzuweit T, et al. Contribution of arteriogenesis and angiogenesis to postocclusive hindlimb perfusion in mice. J Mol Cell Cardiol. 2002;34:775–787
  11. Heil M, Eitenmuller I, Schmitz-Rixen T, Schaper W. Arteriogenesis versus angiogenesis: similarities and differences. J Cell Mol Med. 2006;10:45–55
  12. Helisch A, Wagner S, Khan N, Drinane M, Wolfram S, Heil M, et al. Impact of mouse strain differences in innate hindlimb collateral vasculature. Arterioscler Thromb Vasc Biol. 2006;26:520–526
  13. Lee CW, Stabile E, Kinnaird T, Shou M, Devaney JM, Epstein SE, et al. Temporal patterns of gene expression after acute hindlimb ischemia in mice: insights into the genomic program for collateral vessel development. J Am Coll Cardiol. 2004;43:474–482
  14. Tang GL, Chang DS, Sarkar R, Wang R, Messina LM. The effect of gradual or acute arterial occlusion on skeletal muscle blood flow, arteriogenesis, and inflammation in rat hindlimb ischemia. J Vasc Surg. 2005;41:312–320
  15. Niiyama H, Kai H, Yamamoto T, Shimada T, Sasaki K, Murohara T, et al. Roles of endogenous monocyte chemoattractant protein-1 in ischemia-induced neovascularization. J Am Coll Cardiol. 2004;44:661–666
  16. Charge SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004;84:209–238
  17. Milkiewicz M, Hudlicka O, Shiner R, Egginton S, Brown MD. VEGF mRNA and protein do not change in parallel during non-inflammatory skeletal muscle ischaemia in rat. J Physiol. 2006;577:671–678
  18. Brown MD, Kent J, Kelsall CJ, Milkiewicz M, Hudlicka O. Remodeling in the microcirculation of rat skeletal muscle during chronic ischemia. Microcirculation. 2003;10:179–191
  19. Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med. 2006;354:610–621
  20. Kim CH. Chemokine-chemokine receptor network in immune cell trafficking. Curr Drug Targets Immune Endocr Metabol Disord. 2004;4:343–361
  21. Olson TS, Ley K. Chemokines and chemokine receptors in leukocyte trafficking. Am J Physiol Regul Integr Comp Physiol. 2002;283:R7–R28
  22. Luster AD. Chemokines—chemotactic cytokines that mediate inflammation. N Engl J Med. 1998;338:436–445
  23. Murphy PM, Baggiolini M, Charo IF, Hebert CA, Horuk R, Matsushima K, et al. International union of pharmacology (XXII. Nomenclature for chemokine receptors). Pharmacol Rev. 2000;52:145–176
  24. Sunderkotter C, Steinbrink K, Goebeler M, Bhardwaj R, Sorg C. Macrophages and angiogenesis. J Leukoc Biol. 1994;55:410–422
  25. Moldovan L, Moldovan NI. Role of monocytes and macrophages in angiogenesis. EXS. 2005;127–146
  26. Tidball JG. Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol. 2005;288:R345–R353
  27. Pimorady-Esfahani A, Grounds MD, McMenamin PG. Macrophages and dendritic cells in normal and regenerating murine skeletal muscle. Muscle Nerve. 1997;20:158–166
  28. Katschke KJ, Rottman JB, Ruth JH, Qin S, Wu L, LaRosa G, et al. Differential expression of chemokine receptors on peripheral blood, synovial fluid, and synovial tissue monocytes/macrophages in rheumatoid arthritis. Arthritis Rheum. 2001;44:1022–1032
  29. Fantuzzi L, Borghi P, Ciolli V, Pavlakis G, Belardelli F, Gessani S. Loss of CCR2 expression and functional response to monocyte chemotactic protein (MCP-1) during the differentiation of human monocytes: role of secreted MCP-1 in the regulation of the chemotactic response. Blood. 1999;94:875–883
  30. Sica A, Saccani A, Borsatti A, Power CA, Wells TN, Luini W, et al. Bacterial lipopolysaccharide rapidly inhibits expression of C-C chemokine receptors in human monocytes. J Exp Med. 1997;185:969–974
  31. Charo IF, Peters W. Chemokine receptor 2 (CCR2) in atherosclerosis, infectious diseases, and regulation of T-cell polarization. Microcirculation. 2003;10:259–264
  32. Heil M, Schaper W. Arteriogenic growth factors, chemokines and proteases as a prerequisite for arteriogenesis. Drug News Perspect. 2005;18:317–322
  33. Unger EF, Sheffield CD, Epstein SE. Heparin promotes the formation of extracardiac to coronary anastomoses in a canine model. Am J Physiol. 1991;260:H1625–H1634
  34. Nagel T, Resnick N, Atkinson WJ, Dewey CF, Gimbrone MA. Shear stress selectively upregulates intercellular adhesion molecule-1 expression in cultured human vascular endothelial cells. J Clin Invest. 1994;94:885–891
  35. Chappell DC, Varner SE, Nerem RM, Medford RM, Alexander RW. Oscillatory shear stress stimulates adhesion molecule expression in cultured human endothelium. Circ Res. 1998;82:532–539
  36. Eischen A, Vincent F, Bergerat JP, Louis B, Faradji A, Bohbot A, et al. Long term cultures of human monocytes in vitro (Impact of GM-CSF on survival and differentiation). J Immunol Methods. 1991;143:209–221
  37. Ito WD, Arras M, Winkler B, Scholz D, Schaper J, Schaper W. Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion. Circ Res. 1997;80:829–837
  38. Hoefer IE, van Royen N, Rectenwald JE, Deindl E, Hua J, Jost M, et al. Arteriogenesis proceeds via ICAM-1/Mac-1- mediated mechanisms. Circ Res. 2004;94:1179–1185
  39. Arras M, Ito WD, Scholz D, Winkler B, Schaper J, Schaper W. Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J Clin Invest. 1998;101:40–50
  40. Scholz D, Ito W, Fleming I, Deindl E, Sauer A, Wiesnet M, et al. Ultrastructure and molecular histology of rabbit hind-limb collateral artery growth (arteriogenesis). Virchows Arch. 2000;436:257–270
  41. Waeckel L, Mallat Z, Potteaux S, Combadiere C, Clergue M, Duriez M, et al. Impairment in postischemic neovascularization in mice lacking the CXC chemokine receptor 3. Circ Res. 2005;96:576–582
  42. Voskuil M, Hoefer IE, van Royen N, Hua J, de Graaf S, Bode C, et al. Abnormal monocyte recruitment and collateral artery formation in monocyte chemoattractant protein-1 deficient mice. Vasc Med. 2004;9:287–292
  43. Shireman PK, Contreras-Shannon V, Ochoa O, Karia BP, Michalek JM, McManus LM. MCP-1 deficiency causes altered inflammation with impaired skeletal muscle regeneration. J Leukoc Biol. 2007;81:775–785
  44. Heil M, Ziegelhoeffer T, Wagner S, Fernandez B, Helisch A, Martin S, et al. Collateral artery growth (arteriogenesis) after experimental arterial occlusion is impaired in mice lacking CC-chemokine receptor-2. Circ Res. 2004;94:671–677
  45. Contreras-Shannon V, Ochoa O, Reyes-Reyna SM, Sun D, Michalek JE, Kuziel WA, et al. Fat accumulation with altered inflammation and regeneration in skeletal muscle of CCR2 -/- mice following ischemic injury. Am J Physiol Cell Physiol. 2007;292:C953–C967
  46. Tang G, Charo DN, Wang R, Charo IF, Messina L. CCR2-/- knockout mice revascularize normally in response to severe hindlimb ischemia. J Vasc Surg. 2004;40:786–795
  47. Schecter AD, Berman AB, Yi L, Ma H, Daly CM, Soejima K, et al. MCP-1-dependent signaling in CCR2(-/-) aortic smooth muscle cells. J Leukoc Biol. 2004;75:1079–1085
  48. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. 2004;25:581–611
  49. Milkiewicz M, Ispanovic E, Doyle JL, Haas TL. Regulators of angiogenesis and strategies for their therapeutic manipulation. Int J Biochem Cell Biol. 2006;38:333–357
  50. Zachary I. VEGF signalling: integration and multi-tasking in endothelial cell biology. Biochem Soc Trans. 2003;31:1171–1177
  51. Tammela T, Enholm B, Alitalo K, Paavonen K. The biology of vascular endothelial growth factors. Cardiovasc Res. 2005;65:550–563
  52. Clauss M, Pipp F, Issbrucker K, Weich H, Heil M, Schaper W. Dissection of monocyte and endothelial activities by using VEGF-receptor specific ligands. Adv Exp Med Biol. 2003;522:75–82
  53. Ferrara N. The role of VEGF in the regulation of physiological and pathological angiogenesis. EXS. 2005;209–231
  54. Anghelina M, Krishnan P, Moldovan L, Moldovan NI. Monocytes and macrophages form branched cell columns in matrigel: implications for a role in neovascularization. Stem Cells Dev. 2004;13:665–676
  55. Anghelina M, Moldovan L, Zabuawala T, Ostrowski MC, Moldovan NI. A subpopulation of peritoneal macrophages form capillarylike lumens and branching patterns in vitro. J Cell Mol Med. 2006;10:708–715
  56. Moldovan NI, Goldschmidt-Clermont PJ, Parker-Thornburg J, Shapiro SD, Kolattukudy PE. Contribution of monocytes/macrophages to compensatory neovascularization: the drilling of metalloelastase-positive tunnels in ischemic myocardium. Circ Res. 2000;87:378–384
  57. Schmeisser A, Graffy C, Daniel WG, Strasser RH. Phenotypic overlap between monocytes and vascular endothelial cells. Adv Exp Med Biol. 2003;522:59–74
  58. Schmeisser A, Strasser RH. Phenotypic overlap between hematopoietic cells with suggested angioblastic potential and vascular endothelial cells. J Hematother Stem Cell Res. 2002;11:69–79
  59. Bernardini G, Ribatti D, Spinetti G, Morbidelli L, Ziche M, Santoni A, et al. Analysis of the role of chemokines in angiogenesis. J Immunol Methods. 2003;273:83–101
  60. Rosenkilde MM, Schwartz TW. The chemokine system—a major regulator of angiogenesis in health and disease. APMIS. 2004;112:481–495
  61. Hwang J, Kim CW, Son KN, Han KY, Lee KH, Kleinman HK, et al. Angiogenic activity of human CC chemokine CCL15 in vitro and in vivo. FEBS Lett. 2004;570:47–51
  62. Addison CL, Daniel TO, Burdick MD, Liu H, Ehlert JE, Xue YY, et al. The CXC chemokine receptor 2, CXCR2, is the putative receptor for ELR+ CXC chemokine-induced angiogenic activity. J Immunol. 2000;165:5269–5277
  63. Yamaguchi J, Kusano KF, Masuo O, Kawamoto A, Silver M, Murasawa S, et al. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation. 2003;107:1322–1328
  64. Kopp HG, Ramos CA, Rafii S. Contribution of endothelial progenitors and proangiogenic hematopoietic cells to vascularization of tumor and ischemic tissue. Curr Opin Hematol. 2006;13:175–181
  65. De Falco E, Porcelli D, Torella AR, Straino S, Iachininoto MG, Orlandi A, et al. SDF-1 involvement in endothelial phenotype and ischemia-induced recruitment of bone marrow progenitor cells. Blood. 2004;104:3472–3482
  66. Weber KS, Nelson PJ, Grone HJ, Weber C. Expression of CCR2 by endothelial cells: implications for MCP-1 mediated wound injury repair and In vivo inflammatory activation of endothelium. Arterioscler Thromb Vasc Biol. 1999;19:2085–2093
  67. Selzman CH, Miller SA, Zimmerman MA, Gamboni-Robertson F, Harken AH, Banerjee A. Monocyte chemotactic protein-1 directly induces human vascular smooth muscle proliferation. Am J Physiol Heart Circ Physiol. 2002;283:H1455–H1461
  68. Streblow DN, Soderberg-Naucler C, Vieira J, Smith P, Wakabayashi E, Ruchti F, et al. The human cytomegalovirus chemokine receptor US28 mediates vascular smooth muscle cell migration. Cell. 1999;99:511–520
  69. Hayes IM, Jordan NJ, Towers S, Smith G, Paterson JR, Earnshaw JJ, et al. Human vascular smooth muscle cells express receptors for CC chemokines. Arterioscler Thromb Vasc Biol. 1998;18:397–403
  70. Hong KH, Ryu J, Han KH. Monocyte chemoattractant protein-1-induced angiogenesis is mediated by vascular endothelial growth factor-A. Blood. 2005;105:1405–1407
  71. Salcedo R, Ponce ML, Young HA, Wasserman K, Ward JM, Kleinman HK, et al. Human endothelial cells express CCR2 and respond to MCP-1: direct role of MCP-1 in angiogenesis and tumor progression. Blood. 2000;96:34–40
  72. Kim MY, Byeon CW, Hong KH, Han KH, Jeong S. Inhibition of the angiogenesis by the MCP-1 (monocyte chemoattractant protein-1) binding peptide. FEBS Lett. 2005;579:1597–1601
  73. Yamada M, Kim S, Egashira K, Takeya M, Ikeda T, Mimura O, et al. Molecular mechanism and role of endothelial monocyte chemoattractant protein-1 induction by vascular endothelial growth factor. Arterioscler Thromb Vasc Biol. 2003;23:1996–2001
  74. Marumo T, Schini-Kerth VB, Busse R. Vascular endothelial growth factor activates nuclear factor-kappaB and induces monocyte chemoattractant protein-1 in bovine retinal endothelial cells. Diabetes. 1999;48:1131–1137
  75. Lakshminarayanan V, Lewallen M, Frangogiannis NG, Evans AJ, Wedin KE, Michael LH, et al. Reactive oxygen intermediates induce monocyte chemotactic protein-1 in vascular endothelium after brief ischemia. Am J Pathol. 2001;159:1301–1311
  76. Goede V, Brogelli L, Ziche M, Augustin HG. Induction of inflammatory angiogenesis by monocyte chemoattractant protein-1. Int J Cancer. 1999;82:765–770
  77. Low QE, Drugea IA, Duffner LA, Quinn DG, Cook DN, Rollins BJ, et al. Wound healing in MIP-1alpha(-/-) and MCP-1(-/-) mice. Am J Pathol. 2001;159:457–463
  78. Dewald O, Zymek P, Winkelmann K, Koerting A, Ren G, Abou-Khamis T, et al. CCL2/monocyte chemoattractant protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circ Res. 2005;96:881–889
  79. Bernardini G, Spinetti G, Ribatti D, Camarda G, Morbidelli L, Ziche M, et al. I-309 binds to and activates endothelial cell functions and acts as an angiogenic molecule in vivo. Blood. 2000;96:4039–4045
  80. Salcedo R, Young HA, Ponce ML, Ward JM, Kleinman HK, Murphy WJ, et al. Eotaxin (CCL11) induces in vivo angiogenic responses by human CCR3+ endothelial cells. J Immunol. 2001;166:7571–7578
  81. Spring H, Schuler T, Arnold B, Hammerling GJ, Ganss R. Chemokines direct endothelial progenitors into tumor neovessels. Proc Natl Acad Sci U S A. 2005;102:18111–18116
  82. Volin MV, Woods JM, Amin MA, Connors MA, Harlow LA, Koch AE. Fractalkine: a novel angiogenic chemokine in rheumatoid arthritis. Am J Pathol. 2001;159:1521–1530
  83. Lee SJ, Namkoong S, Kim YM, Kim CK, Lee H, Ha KS, et al. Fractalkine stimulates angiogenesis by activating the Raf-1/MEK/ERK- and PI3K/Akt/eNOS-dependent signal pathways. Am J Physiol Heart Circ Physiol. 2006;291:H2836–H2846
  84. Sun XT, Zhang MY, Shu C, Li Q, Yan XG, Cheng N, et al. Differential gene expression during capillary morphogenesis in a microcarrier-based three-dimensional in vitro model of angiogenesis with focus on chemokines and chemokine receptors. World J Gastroenterol. 2005;11:2283–2290
  85. Carlson BM, Faulkner JA. The regeneration of skeletal muscle fibers following injury: a review. Med Sci Sports Exerc. 1983;15:187–198
  86. Carlson BM, Gutmann E. Regeneration in free grafts of normal and denervated muscles in the rat: morphology and histochemistry. Anat Rec. 1975;183:47–62
  87. Toumi H, Best TM. The inflammatory response: friend or enemy for muscle injury?. Br J Sports Med. 2003;37:284–286
  88. Teixeira CF, Zamuner SR, Zuliani JP, Fernandes CM, Cruz-Hofling MA, Fernandes I, et al. Neutrophils do not contribute to local tissue damage, but play a key role in skeletal muscle regeneration, in mice injected with Bothrops asper snake venom. Muscle Nerve. 2003;28:449–459
  89. Teixeira CF, Chaves F, Zamuner SR, Fernandes CM, Zuliani JP, Cruz-Hofling MA, et al. Effects of neutrophil depletion in the local pathological alterations and muscle regeneration in mice injected with Bothrops jararaca snake venom. Int J Exp Pathol. 2005;86:107–115
  90. Nguyen HX, Lusis AJ, Tidball JG. Null mutation of myeloperoxidase in mice prevents mechanical activation of neutrophil lysis of muscle cell membranes in vitro and in vivo. J Physiol. 2005;565:403–413
  91. Tidball JG. Inflammatory cell response to acute muscle injury. Med Sci Sports Exerc. 1995;27:1022–1032
  92. DiTirro J, Rhoades ER, Roberts AD, Burke JM, Mukasa A, Cooper AM, et al. Disruption of the cellular inflammatory response to Listeria monocytogenes infection in mice with disruptions in targeted genes. Infect Immun. 1998;66:2284–2289
  93. Grounds MD. Age-associated changes in the response of skeletal muscle cells to exercise and regeneration. Ann N Y Acad Sci. 1998;854:78–91
  94. Goetsch SC, Hawke TJ, Gallardo TD, Richardson JA, Garry DJ. Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration. Physiol Genomics. 2003;14:261–271
  95. Hirata A, Masuda S, Tamura T, Kai K, Ojima K, Fukase A, et al. Expression profiling of cytokines and related genes in regenerating skeletal muscle after cardiotoxin injection: a role for osteopontin. Am J Pathol. 2003;163:203–215
  96. Summan M, McKinstry M, Warren GL, Hulderman T, Mishra D, Brumbaugh K, et al. Inflammatory mediators and skeletal muscle injury: a DNA microarray analysis. J Interferon Cytokine Res. 2003;23:237–245
  97. Paoni NF, Peale F, Wang F, Errett-Baroncini C, Steinmetz H, Toy K, et al. Time course of skeletal muscle repair and gene expression following acute hind limb ischemia in mice. Physiol Genomics. 2002;11:263–272
  98. Yan Z, Choi S, Liu X, Zhang M, Schageman JJ, Lee SY, et al. Highly coordinated gene regulation in mouse skeletal muscle regeneration. J Biol Chem. 2003;278:8826–8836
  99. Sachidanandan C, Sambasivan R, Dhawan J. Tristetraprolin and LPS-inducible CXC chemokine are rapidly induced in presumptive satellite cells in response to skeletal muscle injury. J Cell Sci. 2002;115:2701–2712
  100. Chazaud B, Sonnet C, Lafuste P, Bassez G, Rimaniol AC, Poron F, et al. Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J Cell Biol. 2003;163:1133–1143
  101. Bartoli C, Civatte M, Pellissier JF, Figarella-Branger D. CCR2A and CCR2B, the two isoforms of the monocyte chemoattractant protein-1 receptor are up-regulated and expressed by different cell subsets in idiopathic inflammatory myopathies. Acta Neuropathol (Berl). 2001;102:385–392
  102. Ratajczak MZ, Majka M, Kucia M, Drukala J, Pietrzkowski Z, Peiper S, et al. Expression of functional CXCR4 by muscle satellite cells and secretion of SDF-1 by muscle-derived fibroblasts is associated with the presence of both muscle progenitors in bone marrow and hematopoietic stem/progenitor cells in muscles. Stem Cells. 2003;21:363–371
  103. Warren GL, Hulderman T, Mishra D, Gao X, Millecchia L, O’Farrell L, et al. Chemokine receptor CCR2 involvement in skeletal muscle regeneration. FASEB J. 2005;19:413–415
  104. Warren GL, O’Farrell L, Summan M, Hulderman T, Mishra D, Luster MI, et al. Role of CC chemokines in skeletal muscle functional restoration after injury. Am J Physiol Cell Physiol. 2004;286:C1031–C1036
  105. Summan M, Warren GL, Mercer RR, Chapman R, Hulderman T, Van Rooijen N, et al. Macrophages and skeletal muscle regeneration: a clodronate-containing liposome depletion study. Am J Physiol Regul Integr Comp Physiol. 2006;290:R1488–R1495

 Competition of interest: none.Supported by grants from the National Institutes of Health (HL070158, HL074236) and the Veterans Administration.

PII: S0741-5214(07)00316-3

doi: 10.1016/j.jvs.2007.02.030

Journal of Vascular Surgery
Volume 45, Issue 6, Supplement , Pages A48-A56 , June 2007