Flow-induced neointimal regression in baboon polytetrafluoroethylene grafts is associated with decreased cell proliferation and increased apoptosis

Journal of Vascular Surgery

Volumn 36, Issue 6, 2002, Pages 1248-1255

  Berceli, Scott A ^a   Davies, Mark G ^b   Kenagy, Richard D ^c   Clowes, Alexander W ^c,d  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CYCLIC GMP; N(G) NITRO DEXTRO ARGININE METHYL ESTER; N(G) NITROARGININE METHYL ESTER; NITRATE; NITRIC OXIDE; NITRITE; POLITEF;

ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTERIOVENOUS FISTULA; ARTERY GRAFT; ARTICLE; ATROPHY; BABOON; BLOOD FLOW; BLOOD FLOW VELOCITY; CELL GROWTH; CELL INFILTRATION; CELL PROLIFERATION; CONTROLLED STUDY; GROWTH REGULATION; HEMODYNAMICS; INTIMA; MACROPHAGE; MALE; MODULATION; NICK END LABELING; NONHUMAN; POLITEF IMPLANT; PRIORITY JOURNAL; SHEAR STRESS; VASCULAR SMOOTH MUSCLE;

EID: 0037000886     PISSN: 07415214     EISSN: None     Source Type: Journal    
DOI: 10.1067/mva.2002.128295     Document Type: Article

References (46)

1. Gibbons GH, Dzau VJ. The emerging concept of vascular remodeling. N Engl J Med 1994;330:1431-8.
2. Glagov S, Weisenberg E, Zarins CK, Stankunavicius R, Kolettis GJ. Compensator enlargement of human atherosclerotic coronary arteries. N Engl J Med 1987;316:1371-5.
3. Langille BL, O'Donnell F. Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science 1986;231(4736):405-7.
4. Ward MR, Pasterkamp G, Ycung AC, Borst C. Arterial remodeling. Mechanisms and clinical implications. Circulation 2000;102:1186-91.
5. Wentzel JJ, Krams R, Schuurbiers JC, Oomen JA, Kloet J, Der Giessen WJ, et al. Relationship between neointimal thickness and shear stress after Wallstent implantation in human coronary arteries. Circulation 2001;103:1740-5.
6. Geary RL, Kohler TR, Vergel S, Kirkman TR, Clowes AW. Time course of flow-induced smooth muscle cell proliferation and intimal thickening in endothelialized baboon vascular grafts. Circ Res 1994;74:14-23.
7. Kraiss LW, Geary RL, Mattsson EJ, Vergel S, Au YP, Clowes AW. Acute reductions in blood flow and shear stress induce platelet-derived growth factor-A expression in baboon prosthetic grafts. Circ Res 1996;79:45-53.
8. Mattsson EJ, Kohler TR, Vergel SM, Clowes AW. Increased blood flow induces regression of intimal hyperplasia. Arterioscler Thromb Vasc Biol 1997;17:2245-9.
9. Cho A, Courtman DW, Langille BL. Apoptosis (programmed cell death) in arteries of the neonatal lamb. Circ Res 1995;76:168-75.
10. Cho A, Mitchell L, Koopmans D, Langille BL. Effects of changes in blood flow rate on cell death and cell proliferation in carotid arteries of immature rabbits. Circ Res 1997;81:328-37.
11. Fisher SA, Langille BL, Srivastava D. Apoptosis during cardiovascular development. Circ Res 2000;87:856-64.
12. Chen L, Daum G, Forough R, Clowes M, Walter U, Clowes AW. Overexpression of human endothelial nitric oxide synthase in rat vascular smooth muscle cells and in balloon-injured carotid artery. Circ Res 1998;82:862-70.
13. Iwashina M, Shichiri M, Marumo F, Hirata Y. Transfection of inducible nitric oxide synthase gene causes apoptosis in vascular smooth muscle cells. Circulation 1998;98:1212-8.
14. Kibbe MR, Li J, Nie S, Watkins SC, Lizonova A, Kovesdi I, et al. Inducible nitric oxide synthase (iNOS) expression upregulates p21 and inhibits vascular smooth muscle cell proliferation through p42/44 mitogen-activated protein kinase activation and independent of p53 and cyclic guanosine monophosphate. J Vasc Surg 2000;31:1214-28.
15. Mattsson EJ, Geary RL, Kraiss LW, Vergel S, Liao JK, Corson MA, et al. Is smooth muscle growth in primate arteries regulated by endothelial nitric oxide synthase? J Vasc Surg 1998;28:514-21.
16. Gratzner HG. Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 1982; 218(4571):474-5.
17. Gavrieli Y, Sherman Y, Ben Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992;119:493-501.
18. Mallat Z, Ohan J, Leseche G, Tedgui A. Colocalization of CPP-32 with apoptotic cells in human atherosclerotic plaques. Circulation 1997;96:424-8.
19. Ellenby MI, Ernst CB, Carretero OA, Scicli AG. Role of nitric oxide in the effect of blood flow on neointima formation. J Vasc Surg 1996;23:314-22.
20. Kung CF, Moreau P, Takase H, Luscher TF. L-NAME hypertension alters endothelial and smooth muscle function in rat aorta. Prevention by trandolapril and verapamil. Hypertension 1995;26:744-51.
21. Luvara G, Pueyo ME, Philippe M, Mandet C, Savoie F, Henrion D, et al. Chronic blockade of NO synthase activity induces a proinflammatory phenotype in the arterial wall: prevention by angiotensin II antagonism. Arterioscler Thromb Vasc Biol 1998;18:1408-16.
22. Bosmans JM, Vrints CJ, Kockx MM, Bult H, Cromheeke KM, Herman AG. Continuous perivascular L-arginine delivery increases total vessel area and reduces neointimal thickening after experimental balloon dilatation. Arterioscler Thromb Vasc Biol 1999;19:767-76.
23. Cayarte AJ, Palacino JJ, Horten K, Cohen RA. Chronic inhibition of nitric oxide production accelerates neointima formation and impairs endothelial function in hypercholesterolemic rabbits. Arterioscler Thromb 1994;14:753-9.
24. Navarro-Cid J, Maeso R, Rodrigo E, Munoz-Garcia K, Ruilope LM, Lahera V, et al. Renal and vascular consequences of the chronic nitric oxide synthase inhibition. Effects of antihypertensive drugs. Am J Hypertens 1996;9:1077-83.
25. Krejcy K, Schwarzacher S, Raberger G. Distribution and metabolism of NG-nitro-L-arginine and NG-nitro-L-arginine methylester in canine blood in vitro. Naunyn Schmiedebergs Arch Pharmacol 1993;347:342-5.
26. Piotrovskij VK, Kallay Z, Krejcy K, Horecky J, Trnovec T, Raberger G. NG-nitro-L-arginine pharmacokinetics in rats after a single intravascutar and oral dose: an appearance of secondary concentration time peaks. Drug Metab Dispos 1993;21:962-4.
27. Tabrizi-Fard MA, Fung HL. Pharmacokinetics, plasma protein binding and urinary excretion of N omega-nitro-L-arginine in rats. Br J Pharmacol 1994;111:394-6.
28. Watanabe H, Kakihana M, Ohtsuka S, Enomoto T, Yasui K, Sugishita Y. Platelet cyclic GMP. A potentially useful indicator to evaluate the effects of nitroglycerin and nitrate tolerance. Circulation 1993;88:29-36.
29. Guevara I, Iwanejko J, Dembinska-Kiec A, Pankiewicz J, Wanat A, Anna P, et al. Determination of nitrite/nitrate in human biological material by the simple Griess reaction. Clin Chim Acta 1998;274:177-88.
30. Kenagy RD, Fischer JW, Davies MG, Berceli SA, Hawkins SM, Wight TN, et al. Increased plasmin and serine proteinase activity during flow-induced intimal atrophy in baboon PTFE grafts. Arterioscler Thromb Vase Biol 2002;22:400-4.
31. Han DK, Haudenschild CC, Hong MK, Tinkle BT, Leon MB, Liau G. Evidence for apoptosis in human atherogenesis and in a rat vascular injury model. Am J Pathol 1995;147:267-77.
32. Bauriedel G, Schluckebier S, Hurter K, Welsch U, Kandolf R, Luderitz B, et al. Apoptosis in restenosis versus stable-angina atherosclerosis: implications for the pathogenesis of restenosis. Arterioscler Thromb Vase Biol 1998;18:1132-9.
33. Kollum M, Kaiser S, Kinscherf R, Metz J, Kubler W, Hehrlein C. Apoptosis after stent implantation compared with balloon angioplasty in rabbits. Role of macrophages. Arterioscler Thromb Vase Biol 1997; 17:2383-8.
34. Schaub FJ, Han DK, Liles WC, Adams LD, Coats SA, Ramachandran RK, et al. Fas/FADD-mediated activation of a specific program of inflammatory gene expression in vascular smooth muscle cells. Nat Med 2000;6:790-6.
35. Clowes AW, Berceli SA. Mechanisms of vascular atrophy and fibrous cap disruption. Ann N Y Acad Sci 2000;902:153-61.
36. Kawashima S, Yamashita T, Ozaki M, Ohashi Y, Azumi H, Inoue N, et al. Endothelial NO synthase overexpression inhibits lesion formation in mouse model of vascular remodeling. Arterioscler Thromb Vasc Biol 2001;21:201-7.
37. Shears LL, Kibbe MR, Murdock AD, Billiar TR, Lizonova A, Kovesdi I, et al. Efficient inhibition of intimal hyperplasia by adenovirus-mediated inducible nitric oxide synthase gene transfer to rats and pigs in vivo. J Am Coll Surg 1998;187:295-306.
38. Calvo WJ, Hajduczok G, Russell JA, Diamond SL. Inhibition of nitric oxide but not prostacyclin prevents poststenotic dilatation in rabbit femoral artery. Circulation 1999;99:1069-76.
39. Guzman RJ, Abe K, Zarins CK. Flow-induced arterial enlargement is inhibited by suppression of nitric oxide synthase activity in vivo. Surgery 1997;122:273-9.
40. Tronc F, Wassef M, Esposito B, Henrion D, Glagov S, Tedgui A. Role of NO in flow-induced remodeling of the rabbit common carotid artery. Arterioscler Thromb Vasc Biol 1996;16:1256-62.
41. Yogo K, Shimokawa H, Funakoshi H, Kandabashi T, Miyata K, Okamoto S, et al. Different vasculoprotective roles of NO synthase isoforms in vascular lesion formation in mice. Arterioscler Thromb Vasc Biol 2000;20:E96-100.
42. Ceiler DL, De Mey JG. Chronic N(G)-nitro-L-arginine methyl ester treatment does not prevent flow-induced remodeling in mesentric feed arteries and arcading arterioles. Arterioscler Thromb Vasc Biol 2000; 20:2057-63.
43. Nishiyama A, Kimura S, Fukui T, Rahman M, Yoneyama H, Kosaka H, et al. Blood flow-dependent changes in renal interstitial guanosine 3′,5′- cyclic monophosphate in rabbits. Am J Physiol Renal Physiol 2002;282:F238-44.
44. Akiyama M, Eguchi D, Weiler D, O'Brien T, Kovesdi I, Scotland RS, et al. Expression and function of recombinant S1179D endothelial nitric oxide synthase in canine cerebral arteries. Stroke 2002;33:1071-6.
45. Southan GJ, Szabo C. Selective pharmacological inhibition of distinct nitric oxide synthase isoforms. Biochem Pharmacol 1996;51:383-94.
46. Miller MJ, Thompson JH, Liu X, Eloby-Childress S, Sadowska-Krowicka H, Zhang XJ, et al. Failure of L-NAME to cause inhibition of nitric oxide synthesis: role of inducible nitric oxide synthase. Inflamm Res 1996;45:272-6.