Histochemistry and Cell Biology

, Volume 132, Issue 5, pp 559–565

Fibulin-1 and fibrinogen in human atherosclerotic lesions

  • W. Scott Argraves
  • Asashi Tanaka
  • Elizabeth P. Smith
  • Waleed O. Twal
  • Kelley M. Argraves
  • Daping Fan
  • Christian C. Haudenschild
Original Paper

Abstract

Fibulin-1 is a fibrinogen-binding blood protein and a component of many extracellular matrices (ECM) including those of blood vessels. In this study, the deposition patterns of fibulin-1 and fibrinogen were examined in human coronary artery atherosclerotic lesions excised by atherectomy from 20 patients. Fibulin-1 deposition was found to be closely overlapping with fibrinogen located within the atherosclerotic lesions and in regions containing fresh thrombi. Pronounced intracellular fibulin-1 immunostaining was apparent in lesion areas rich in macrophages and foam cells, although THP-1 macrophages and foam cells were found not to express fibulin-1. Strong ECM deposition of fibulin-1 was observed in acellular atheromatous and myxomatous regions. By contrast, fibulin-1 was present at relatively low levels in the ECM associated with smooth muscle cells within and outside of lesions and was not detected in sclerotic regions. These results reveal the pattern of fibulin-1 within human atherosclerotic lesions and highlight the potential for fibulin-1, perhaps derived from the blood and acting in conjunction with fibrinogen, to play a role in the etiology and cardiovascular disease progression, particularly with respect to thrombotic aspects of atherosclerosis.

Keywords

Fibulin-1 Fibrinogen Extracellular matrix Atherosclerosis 

References

  1. Abrignani MG, Novo G, Di Girolamo A, Caruso R, Tantillo R, Braschi A, Braschi GB, Strano A, Novo S (1999) Increased plasma levels of fibrinogen in acute and chronic ischemic coronary syndromes. Cardiologia 44:1047–1052PubMedGoogle Scholar
  2. Argraves WS, Tran H, Burgess WH, Dickerson K (1990) Fibulin is an extracellular matrix and plasma glycoprotein with repeated domain structure. J Cell Biol 111:3155–3164CrossRefPubMedGoogle Scholar
  3. Auwerx J (1991) The human leukemia cell line, THP-1: a multifacetted model for the study of monocyte-macrophage differentiation. Experientia 47:22–31CrossRefPubMedGoogle Scholar
  4. Balbona K, Tran H, Godyna S, Ingham KC, Strickland DK, Argraves WS (1992) Fibulin binds to itself and to the carboxyl-terminal heparin-binding region of fibronectin. J Biol Chem 267:20120–20125PubMedGoogle Scholar
  5. Basu SK, Goldstein JL, Anderson GW, Brown MS (1976) Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc Natl Acad Sci USA 73:3178–3182CrossRefPubMedGoogle Scholar
  6. Bini A, Fenoglio JJ Jr, Mesa-Tejada R, Kudryk B, Kaplan KL (1989) Identification and distribution of fibrinogen, fibrin, and fibrin(ogen) degradation products in atherosclerosis. Use of monoclonal antibodies. Arteriosclerosis 9:109–121PubMedGoogle Scholar
  7. Ge M, Ryan TJ, Lum H, Malik AB (1991) Fibrinogen degradation product fragment D increases endothelial monolayer permeability. Am J Physiol 261:L283–L289PubMedGoogle Scholar
  8. Godyna S, Diaz-Ricart M, Argraves WS (1996) Fibulin-1 mediates platelet adhesion via a bridge of fibrinogen. Blood 88:2569–2577PubMedGoogle Scholar
  9. Gonda SR, Shainoff JR (1982) Adsorptive endocytosis of fibrin monomer by macrophages: evidence of a receptor for the amino terminus of the fibrin alpha chain. Proc Natl Acad Sci USA 79:4565–4569CrossRefPubMedGoogle Scholar
  10. Jonsson-Rylander AC, Nilsson T, Fritsche-Danielson R, Hammarstrom A, Behrendt M, Andersson JO, Lindgren K, Andersson AK, Wallbrandt P, Rosengren B, Brodin P, Thelin A, Westin A, Hurt-Camejo E, Lee-Sogaard CH (2005) Role of ADAMTS-1 in atherosclerosis: remodeling of carotid artery, immunohistochemistry, and proteolysis of versican. Arterioscler Thromb Vasc Biol 25:180–185PubMedGoogle Scholar
  11. Kadish JL, Butterfield CE, Folkman J (1979) The effect of fibrin on cultured vascular endothelial cells. Tissue Cell 11:99–108CrossRefPubMedGoogle Scholar
  12. Kannel WB, D’Agostino RB, Belanger AJ (1992) Update on fibrinogen as a cardiovascular risk factor. Ann Epidemiol 2:457–466PubMedCrossRefGoogle Scholar
  13. Kaplan JE, Cardarelli PM, Rourke FJ, Weston LK, Moon DG, Blumenstock FA (1989) Fibronectin augments binding of fibrin to macrophages. J Lab Clin Med 113:168–176PubMedGoogle Scholar
  14. Kawata K, Tanaka A, Arai M, Argraves WS, Fukutake K (2001) Alteration of plasma fibulin-1 concentrations in ischemic heart diseases. Jpn J Thromb Hemost 12:126–132CrossRefGoogle Scholar
  15. Koenig W (1999) Fibrinogen and coronary risk. Curr Cardiol Rep 1:112–118CrossRefPubMedGoogle Scholar
  16. Lee NV, Rodriguez-Manzaneque JC, Thai SN, Twal WO, Luque A, Lyons KM, Argraves WS, Iruela-Arispe ML (2005) Fibulin-1 acts as a cofactor for the matrix metalloprotease ADAMTS-1. J Biol Chem 280:34796–34804CrossRefPubMedGoogle Scholar
  17. Lendrum AC, Fraser DS, Slidders W, Henderson R (1962) Studies on the character of staining of fibrin. J Clin Pathol 15:401–413CrossRefPubMedGoogle Scholar
  18. Lien E, Means TK, Heine H, Yoshimura A, Kusumoto S, Fukase K, Fenton MJ, Oikawa M, Qureshi N, Monks B, Finberg RW, Ingalls RR, Golenbock DT (2000) Toll-like receptor 4 imparts ligand-specific recognition of bacterial lipopolysaccharide. J Clin Invest 105:497–504CrossRefPubMedGoogle Scholar
  19. Lou XJ, Boonmark NW, Horrigan FT, Degen JL, Lawn RM (1998) Fibrinogen deficiency reduces vascular accumulation of apolipoprotein(a) and development of atherosclerosis in apolipoprotein(a) transgenic mice. Proc Natl Acad Sci USA 95:12591–12595CrossRefPubMedGoogle Scholar
  20. Luna LG (1968) Manual of histological staining methods of the Armed Forces Institute of Pathology. McGraw-Hill, New YorkGoogle Scholar
  21. Meade TW, North WR, Chakrabarti R, Stirling Y, Haines AP, Thompson SG, Brozovie M (1980) Haemostatic function and cardiovascular death: early results of a prospective study. Lancet 1:1050–1054CrossRefPubMedGoogle Scholar
  22. Nomura H, Naito M, Iguchi A, Thompson WD, Smith EB (1999) Fibrin gel induces the migration of smooth muscle cells from rabbit aortic explants. Thromb Haemost 82:1347–1352PubMedGoogle Scholar
  23. Prandoni P, Bilora F, Marchiori A, Bernardi E, Petrobelli F, Lensing AW, Prins MH, Girolami A (2003) An association between atherosclerosis and venous thrombosis. N Engl J Med 348:1435–1441CrossRefPubMedGoogle Scholar
  24. Roark EF, Keene DR, Haudenschild CC, Godyna S, Little CD, Argraves WS (1995) The association of human fibulin-1 with elastic fibers: an immunohistological, ultrastructural, and RNA study. J Histochem Cytochem 43:401–411PubMedGoogle Scholar
  25. Sasaki T, Gohring W, Miosge N, Abrams WR, Rosenbloom J, Timpl R (1999) Tropoelastin binding to fibulins, nidogen-2 and other extracellular matrix proteins. FEBS Lett 460:280–284CrossRefPubMedGoogle Scholar
  26. Sueishi K, Ichikawa K, Kato K, Nakagawa K, Chen YX (1998) Atherosclerosis: coagulation and fibrinolysis. Semin Thromb Hemost 24:255–260CrossRefPubMedGoogle Scholar
  27. Tjurmin AV, Ananyeva NM, Smith EP, Gao Y, Hong MK, Leon MB, Haudenschild CC (1999) Studies on the histogenesis of myxomatous tissue of human coronary lesions. Arterioscler Thromb Vasc Biol 19:83–97PubMedGoogle Scholar
  28. Tran H, Tanaka A, Litvinovich SV, Medved LV, Haudenschild CC, Argraves WS (1995) The interaction of fibulin-1 with fibrinogen. A potential role in hemostasis and thrombosis. J Biol Chem 270:19458–19464CrossRefPubMedGoogle Scholar
  29. Tran H, Mattei M, Godyna S, Argraves WS (1997) Human fibulin-1D: molecular cloning, expression and similarity with S1-5 protein, a new member of the fibulin gene family. Matrix Biol 15:479–493CrossRefPubMedGoogle Scholar
  30. Twal WO, Czirok A, Hegedus B, Knaak C, Chintalapudi MR, Okagawa H, Sugi Y, Argraves WS (2001) Fibulin-1 suppression of fibronectin-regulated cell adhesion and motility. J Cell Sci 114:4587–4598PubMedGoogle Scholar
  31. Wang MD, Kiss RS, Franklin V, McBride HM, Whitman SC, Marcel YL (2007) Different cellular traffic of LDL-cholesterol and acetylated LDL-cholesterol leads to distinct reverse cholesterol transport pathways. J Lipid Res 48:633–645CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • W. Scott Argraves
    • 1
  • Asashi Tanaka
    • 2
  • Elizabeth P. Smith
    • 3
  • Waleed O. Twal
    • 1
  • Kelley M. Argraves
    • 1
  • Daping Fan
    • 4
  • Christian C. Haudenschild
    • 5
  1. 1.Department of Regenerative Medicine and Cell BiologyMedical University of South CarolinaCharlestonUSA
  2. 2.Department of Clinical Laboratory MedicineHachioji Medical Center of Tokyo Medical UniversityTokyoJapan
  3. 3.Center for Vascular and Inflammatory DiseasesUniversity of Maryland School of MedicineBaltimoreUSA
  4. 4.Department of Cell Biology and Anatomy, School of MedicineUniversity of South CarolinaColumbiaUSA
  5. 5.Department of PathologyGeorge Washington University Medical CenterWashingtonUSA

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