Journal of Vascular Surgery
Volume 48, Issue 6 , Pages 1546-1558 , December 2008

Cellular and molecular mechanism regulating blood flow recovery in acute versus gradual femoral artery occlusion are distinct in the mouse

  • Yagai Yang, PhD

      Affiliations

    • Department of Medicine, Division of Cardiology, University of California, San Francisco, Calif
    • ,
  • Gale Tang, MD

      Affiliations

    • Division of Vascular Surgery, Northwestern University, Chicago, Ill
    • ,
  • Jinglian Yan, PhD

      Affiliations

    • Division of Vascular Surgery, University of Massachusetts Medical School, Worcester, Mass
    • ,
  • Brian Park, MD

      Affiliations

    • Division of Vascular Surgery, University of Massachusetts Medical School, Worcester, Mass
    • ,
  • Ari Hoffman, MD

      Affiliations

    • School of Medicine, University of California, San Francisco, Calif
    • ,
  • Guodong Tie, PhD

      Affiliations

    • Division of Vascular Surgery, University of Massachusetts Medical School, Worcester, Mass
    • ,
  • Rong Wang, PhD

      Affiliations

    • Pacific Vascular Research Laboratory, Division of Vascular Surgery, Department of Surgery, University of California, San Francisco, Calif
    • ,
  • Louis M. Messina, MD

      Affiliations

    • Department of Medicine, Division of Cardiology, University of California, San Francisco, Calif
    • Corresponding Author InformationReprint requests: Louis M. Messina, MD, Division of Vascular Surgery, University of Massachusetts Medical School, 55 Lake Avenue North, Worcester, MA 01655

Received 16 May 2008 ,Accepted 21 July 2008.

References 

  1. Schainfeld RM, Isner JM. Critical limb ischemia: nothing to give at the office?. Ann Intern Med. 1999;130:442–444
  2. Baffour R, Garb JL, Kaufman J, Berman J, Rhee SW, Norris MA, et al. Angiogenic therapy for the chronically ischemic lower limb in a rabbit model. J Surg Res. 2000;93:219–229
  3. 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
  4. Helisch A, Schaper W. Arteriogenesis: the development and growth of collateral arteries. Microcirculation. 2003;10:83–97
  5. Schaper W, Scholz D. Factors regulating arteriogenesis. Arterioscler Thromb Vasc Biol. 2003;23:1143–1151
  6. 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
  7. Cooke JP. Flow, NO, and atherogenesis. Proc Natl Acad Sci U S A. 2003;100:768–770
  8. Pipp F, Boehm S, Cai WJ, Adili F, Ziegler B, Karanovic G, et al. Elevated fluid shear stress enhances postocclusive collateral artery growth and gene expression in the pig hind limb. Arterioscler Thromb Vasc Biol. 2004;24:1664–1668
  9. Topper JN, Gimbrone MA. Blood flow and vascular gene expression: fluid shear stress as a modulator of endothelial phenotype. Mol Med Today. 1999;5:40–46
  10. van Royen N, Hoefer I, Buschmann I, Kostin S, Voskuil M, Bode C, et al. Effects of local MCP-1 protein therapy on the development of the collateral circulation and atherosclerosis in Watanabe hyperlipidemic rabbits. Cardiovasc Res. 2003;57:178–185
  11. Voskuil M, van Royen N, Hoefer IE, Seidler R, Guth BD, Bode C, et al. Modulation of collateral artery growth in a porcine hindlimb ligation model using MCP-1. Am J Physiol Heart Circ Physiol. 2003;284:H1422–H1428
  12. Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S, et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res. 2004;94:678–685
  13. Jin DK, Shido K, Kopp HG, Petit I, Shmelkov SV, Young LM, et al. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med. 2006;12:557–567
  14. Szmitko PE, Fedak PW, Weisel RD, Stewart DJ, Kutryk MJ, Verma S. Endothelial progenitor cells: new hope for a broken heart. Circulation. 2003;107:3093–3100
  15. Brevetti LS, Paek R, Brady SE, Hoffman JI, Sarkar R, Messina LM. Exercise-induced hyperemia unmasks regional blood flow deficit in experimental hindlimb ischemia. J Surg Res. 2001;98:21–26
  16. Deindl E, Boengler K, van Royen N, Schaper W. Differential expression of GAPDH and beta3-actin in growing collateral arteries. Mol Cell Biochem. 2002;236:139–146
  17. Jacobi J, Tam BY, Wu G, Hoffman J, Cooke JP, Kuo CJ. Adenoviral gene transfer with soluble vascular endothelial growth factor receptors impairs angiogenesis and perfusion in a murine model of hindlimb ischemia. Circulation. 2004;110:2424–2429
  18. Tuomisto TT, Rissanen TT, Vajanto I, Korkeela A, Rutanen J, Yla-Herttuala S. HIF-VEGF-VEGFR-2, TNF-alpha and IGF pathways are upregulated in critical human skeletal muscle ischemia as studied with DNA array. Atherosclerosis. 2004;174:111–120
  19. Witt KA, Mark KS, Huber J, Davis TP. Hypoxia-inducible factor and nuclear factor kappa-B activation in blood-brain barrier endothelium under hypoxic/reoxygenation stress. J Neurochem. 2005;92:203–214
  20. Schalch P, Patejunas G, Retuerto M, Sarateanu S, Milbrandt J, Thakker G, et al. Homozygous deletion of early growth response 1 gene and critical limb ischemia after vascular ligation in mice: evidence for a central role in vascular homeostasis. J Thorac Cardiovasc Surg. 2004;128:595–601
  21. Tousoulis D, Davies GJ, Asimakopoulos G, Homaei H, Zouridakis E, Ahmed N, et al. Vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 serum level in patients with chest pain and normal coronary arteries (syndrome X). Clin Cardiol. 2001;24:301–304
  22. Signorelli SS, Malaponte G, Di Pino L, Digrandi D, Pennisi G, Mazzarino MC. Effects of ischemic stress on leukocyte activation processes in patients with chronic peripheral occlusive arterial disease: role of L-propionyl carnitine administration. Pharmacol Res. 2001;44:305–309
  23. Ley K, Gaehtgens P, Fennie C, Singer MS, Lasky LA, Rosen SD. Lectin-like cell adhesion molecule 1 mediates leukocyte rolling in mesenteric venules in vivo. Blood. 1991;77:2553–2555
  24. Panettieri RA, Lazaar AL, Pure E, Albelda SM. Activation of cAMP-dependent pathways in human airway smooth muscle cells inhibits TNF-alpha-induced ICAM-1 and VCAM-1 expression and T lymphocyte adhesion. J Immunol. 1995;154:2358–2365
  25. Bao X, Lu C, Frangos JA. Temporal gradient in shear but not steady shear stress induces PDGF-A and MCP-1 expression in endothelial cells: role of NO, NF kappa B, and Egr-1. Arterioscler Thromb Vasc Biol. 1999;19:996–1003
  26. Chiu JJ, Wung BS, Hsieh HJ, Lo LW, Wang DL. Nitric oxide regulates shear stress-induced early growth response-1 (Expression via the extracellular signal-regulated kinase pathway in endothelial cells). Circ Res. 1999;85:238–246
  27. 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
  28. Garcia-Cardena G, Comander J, Anderson KR, Blackman BR, Gimbrone MA. Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc Natl Acad Sci U S A. 2001;98:4478–4485
  29. Kuchan MJ, Jo H, Frangos JA. Role of G proteins in shear stress-mediated nitric oxide production by endothelial cells. Am J Physiol. 1994;267:C753–C758
  30. Tsao PS, Buitrago R, Chan JR, Cooke JP. Fluid flow inhibits endothelial adhesiveness (Nitric oxide and transcriptional regulation of VCAM-1). Circulation. 1996;94:1682–1689
  31. Tsao PS, Lewis NP, Alpert S, Cooke JP. Exposure to shear stress alters endothelial adhesiveness (Role of nitric oxide). Circulation. 1995;92:3513–3519
  32. Uematsu M, Ohara Y, Navas JP, Nishida K, Murphy TJ, Alexander RW, et al. Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. Am J Physiol. 1995;269:C1371–C1378
  33. 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
  34. Palmer-Kazen U, Wariaro D, Luo F, Wahlberg E. Vascular endothelial cell growth factor and fibroblast growth factor 2 expression in patients with critical limb ischemia. J Vasc Surg. 2004;39:621–628
  35. Werner GS, Jandt E, Krack A, Schwarz G, Mutschke O, Kuethe F, et al. Growth factors in the collateral circulation of chronic total coronary occlusions: relation to duration of occlusion and collateral function. Circulation. 2004;110:1940–1945
  36. Lee CW, Kinnaird T, Shou M, Devaney JM, Epstein SE, Burnett MS. Temporal patterns of gene expression after acute hindlimb ischemia in mice: insights into the genomic program for collateral vessel development. SE J Am Coll Cardiol. 2004;43:474–482
  37. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med. 2003;9:702–712
  38. Zernecke A, Schober A, Bot I, von Hundelshausen P, Liehn EA, Mopps B, et al. SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circ Res. 2005;96:784–791
  39. Ratajczak MZ, Zuba-Surma E, Kucia M, Reca R, Wojakowski W, Ratajczak J. The pleiotropic effects of the SDF-1-CXCR4 axis in organogenesis, regeneration and tumorigenesis. Leukemia. 2006;20:1915–1924
  40. Pituch-Noworolska A, Majka M, Janowska-Wieczorek A, Baj-Krzyworzeka M, Urbanowicz B, Malec E, et al. Circulating CXCR4-positive stem/progenitor cells compete for SDF-1-positive niches in bone marrow, muscle and neural tissues: an alternative hypothesis to stem cell plasticity. Folia Histochem Cytobiol. 2003;41:13–21

 Supported by the National Institutes of Health Grant HL75353 (L.M.M.) and Pacific Vascular Research Institute.

 Competition of interest: none.

 Additional material for this article may be found online at www.jvascsurg.org

PII: S0741-5214(08)01222-6

doi: 10.1016/j.jvs.2008.07.063

Journal of Vascular Surgery
Volume 48, Issue 6 , Pages 1546-1558 , December 2008

Article Tools

* Image Usage & Resolution