Uremic serum and solutes increase post-vascular interventional thrombotic risk through altered stability of smooth muscle cell tissue factor

Circulation

Volumn 127, Issue 3, 2013, Pages 365-376

  Chitalia, Vipul C ^a,b   Shivanna, Sowmya ^a,b   Martorell, Jordi ^a,d   Balcells, Mercedes ^a,d   Bosch, Irene ^a,e   Kolandaivelu, Kumaran ^a,c   Edelman, Elazer R ^a,c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d INSTITUT QUÍMIC DE SARRIÀ   (Spain)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

angioplasty; coagulation; coronary stent; kidney; risk factors; thrombus; tissue

Indexed keywords

CREATININE; CRESOL; GLUCOSE; HOMOCYSTEINE; INDICAN; INDOLEACETIC ACID; NEUTRALIZING ANTIBODY; OXALIC ACID; THROMBOPLASTIN; UREA; URIC ACID;

ADULT; AGED; ARTICLE; BLOOD CLOTTING; CELL CULTURE; CLINICAL ARTICLE; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; CREATININE BLOOD LEVEL; DIABETES MELLITUS; ETHNICITY; FEMALE; GLUCOSE BLOOD LEVEL; HEMODIALYSIS; HUMAN; HUMAN CELL; HYPERTENSION; KIDNEY FAILURE; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN STABILITY; SMOOTH MUSCLE FIBER; THROMBOGENICITY; THROMBOSIS; UBIQUITINATION; UREA NITROGEN BLOOD LEVEL; UREMIA; VASCULAR SMOOTH MUSCLE FIBER;

ADULT; AGED; CELL LINE; CORONARY VESSELS; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; INDICAN; INDOLEACETIC ACIDS; KIDNEY FAILURE, CHRONIC; MALE; MIDDLE AGED; MYOCYTES, SMOOTH MUSCLE; RENAL DIALYSIS; RISK FACTORS; SERUM; STENTS; THROMBOPLASTIN; THROMBOSIS; UBIQUITINATION; UREMIA;

EID: 84872678251     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.112.118174     Document Type: Article

References (39)

1. Butenas S, Orfeo T, Mann KG. Tissue factor in coagulation: which? where? when? Arterioscler Thromb Vasc Biol. 2009;29:1989-1996.
2. Cimmino G, D'Amico C, Vaccaro V, D'Anna M, Golino P. The missing link between atherosclerosis, infammation and thrombosis: is it tissue factor? Expert Rev Cardiovasc Ther. 2011;9:517-523.
3. Westrick RJ, Bodary PF, Xu Z, Shen YC, Broze GJ, Eitzman DT. De-fciency of tissue factor pathway inhibitor promotes atherosclerosis and thrombosis in mice. Circulation. 2001;103:3044-3046.
4. Gomez K, McVey JH. Tissue factor initiated blood coagulation. Front Biosci. 2006;11:1349-1359.
5. Hasenstab D, Lea H, Hart CE, Lok S, Clowes AW. Tissue factor overex-pression in rat arterial neointima models thrombosis and progression of advanced atherosclerosis. Circulation. 2000;101:2651-2657.
6. Steffel J, Lüscher TF, Tanner FC. Tissue factor in cardiovascular diseases: molecular mechanisms and clinical implications. Circulation. 2006;113:722-731.
7. Motovska Z, Knot J, Widimsky P. Stent thrombosis: risk assessment and prevention. Cardiovasc Ther. 2010;28:e92-100.
8. Stähli BE, Camici GG, Tanner FC. Drug-eluting stent thrombosis. Ther Adv Cardiovasc Dis. 2009;3:45-52.
9. Park DW, Park SW, Park KH, Lee BK, Kim YH, Lee CW, Hong MK, Kim JJ, Park SJ. Frequency of and risk factors for stent thrombosis after drug-eluting stent implantation during long-term follow-up. Am J Cardiol. 2006;98:352-356.
10. Iakovou I, Schmidt T, Bonizzoni E, Ge L, Sangiorgi GM, Stankovic G, Airoldi F, Chieffo A, Montorfano M, Carlino M, Michev I, Corvaja N, Briguori C, Gerckens U, Grube E, Colombo A. Incidence, predictors, and outcome of thrombosis after successful implantation of drug-eluting stents. JAMA. 2005;293:2126-2130.
11. Kimura T, Morimoto T, Kozuma K, Honda Y, Kume T, Aizawa T, Mit-sudo K, Miyazaki S, Yamaguchi T, Hiyoshi E, Nishimura E, Isshiki T; RESTART Investigators. Comparisons of baseline demographics, clinical presentation, and long-term outcome among patients with early, late, and very late stent thrombosis of sirolimus-eluting stents: observations from the Registry of Stent Thrombosis for Review and Reevaluation (RESTART). Circulation. 2010;122:52-61.
12. Lasala JM, Cox DA, Dobies D, Baran K, Bachinsky WB, Rogers EW, Breall JA, Lewis DH, Song A, Starzyk RM, Mascioli SR, Dawkins KD, Baim DS; ARRIVE 1 and ARRIVE 2 Participating Physicians. Drug-elut-ing stent thrombosis in routine clinical practice: two-year outcomes and predictors from the TAXUS ARRIVE registries. Circ Cardiovasc Interv. 2009;2:285-293.
13. Lambert ND, Sacrinty MT, Ketch TR, Turner SJ, Santos RM, Daniel KR, Applegate RJ, Kutcher MA, Sane DC. Chronic kidney disease and dipstick proteinuria are risk factors for stent thrombosis in patients with myo-cardial infarction. Am Heart J. 2009;157:688-694.
14. Ting HH, Tahirkheli NK, Berger PB, McCarthy JT, Timimi FK, Mathew V, Rihal CS, Hasdai D, Holmes DR Jr. Evaluation of long-term survival after successful percutaneous coronary intervention among patients with chronic renal failure. Am J Cardiol. 2001;87:630-633, A9.
15. Mercier E, Branger B, Vecina F, Al-Sabadani B, Berlan J, Dauzat M, Four-cade J, Gris JC. Tissue factor coagulation pathway and blood cells activation state in renal insuffciency. Hematol J. 2001;2:18-25.
16. Dubin R, Cushman M, Folsom AR, Fried LF, Palmas W, Peralta CA, Was-sel C, Shlipak MG. Kidney function and multiple hemostatic markers: cross sectional associations in the multi-ethnic study of atherosclerosis. BMC Nephrol. 2011;12:3.
17. Serradell M, Díaz-Ricart M, Cases A, Zurbano MJ, Aznar-Salatti J, López-Pedret J, Ordinas A, Escolar G. Uremic medium disturbs the he-mostatic balance of cultured human endothelial cells. Thromb Haemost. 2001;86:1099-1105.
18. Kario K, Matsuo T, Matsuo M, Koide M, Yamada T, Nakamura S, Sakata T, Kato H, Miyata T. Marked increase of activated factor VII in uremic patients. Thromb Haemost. 1995;73:763-767.
19. Vanholder R, Argilés A, Baurmeister U, Brunet P, Clark W, Cohen G, De Deyn PP, Deppisch R, Descamps-Latscha B, Henle T, Jorres A, Massy ZA, Rodriguez M, Stegmayr B, Stenvinkel P, Wratten ML. Uremic toxic-ity: present state of the art. Int J Artif Organs. 2001;24:695-725.
20. Dou L, Bertrand E, Cerini C, Faure V, Sampol J, Vanholder R, Berland Y, Brunet P. The uremic solutes p-cresol and indoxyl sulfate inhibit endothe-lial proliferation and wound repair. Kidney Int. 2004;65:442-451.
21. Kolandaivelu K, Swaminathan R, Gibson WJ, Kolachalama VB, Nguy-en-Ehrenreich KL, Giddings VL, Coleman L, Wong GK, Edelman ER. Stent thrombogenicity early in high-risk interventional settings is driven by stent design and deployment and protected by polymer-drug coatings. Circulation. 2011;123:1400-1409.
22. Balcells M, Martorell J, Olivé C, Santacana M, Chitalia V, Cardoso AA, Edelman ER. Smooth muscle cells orchestrate the endothelial cell response to fow and injury. Circulation. 2010;121:2192-2199.
23. Chitalia VC, Murikipudi S, Indolf L, Rabadi L, Valdez R, Franses JW, Edelman ER. Matrix-embedded endothelial cells are protected from the uremic milieu. Nephrol Dial Transplant. 2011;26:3858-3865.
24. Schecter AD, Giesen PL, Taby O, Rosenfeld CL, Rossikhina M, Fyfe BS, Kohtz DS, Fallon JT, Nemerson Y, Taubman MB. Tissue factor expression in human arterial smooth muscle cells: TF is present in three cellular pools after growth factor stimulation. J Clin Invest. 1997;100:2276-2285.
25. Butenas S, Orfeo T, Mann KG. Tissue factor activity and function in blood coagulation. Thromb Res. 2008;122 (suppl 1):S42-S46.
26. Bogdanov VY, Osterud B. Cardiovascular complications of diabetes mel-litus: the tissue factor perspective. Thromb Res. 2010;125:112-118.
27. Marmur JD, Rossikhina M, Guha A, Fyfe B, Friedrich V, Mendlowitz M, Nemerson Y, Taubman MB. Tissue factor is rapidly induced in arterial smooth muscle after balloon injury. J Clin Invest. 1993;91:2253-2259.
28. Staub O, Rotin D. Role of ubiquitylation in cellular membrane transport. Physiol Rev. 2006;86:669-707.
29. Chitalia VC, Foy RL, Bachschmid MM, Zeng L, Panchenko MV, Zhou MI, Bharti A, Seldin DC, Lecker SH, Dominguez I, Cohen HT. Jade-1 inhibits Wnt signalling by ubiquitylating beta-catenin and mediates Wnt pathway inhibition by pVHL. Nat Cell Biol. 2008;10:1208-1216.
30. Ocak G, Verduijn M, Vossen CY, Lijfering WM, Dekker FW, Rosend-aal FR, Gansevoort RT, Mahmoodi BK. Chronic kidney disease stages 1-3 increase the risk of venous thrombosis. J Thromb Haemost. 2010;8:2428-2435.
31. London GM. Vascular disease and atherosclerosis in uremia. Nefrologia. 2005;25(suppl 2):91-95.
32. Brunet P, Gondouin B, Duval-Sabatier A, Dou L, Cerini C, Dignat-George F, Jourde-Chiche N, Argiles A, Burtey S. Does uremia cause vascular dysfunction? Kidney Blood Press Res. 2011;34:284-290.
33. Fort J. Chronic renal failure: a cardiovascular risk factor. Kidney Int Suppl. 2005;99:S25-S29.
34. Vanholder R, Van Laecke S, Glorieux G. The middle-molecule hypothesis 30 years after: lost and rediscovered in the universe of uremic toxicity? J Nephrol. 2008;21:146-160.
35. Feig DI, Kang DH, Johnson RJ. Uric acid and cardiovascular risk. N Engl J Med. 2008;359:1811-1821.
36. Neri L, Rocca Rey LA, Lentine KL, Hinyard LJ, Pinsky B, Xiao H, Dukes J, Schnitzler MA. Joint association of hyperuricemia and reduced GFR on cardiovascular morbidity: a historical cohort study based on laboratory and claims data from a national insurance provider. Am J Kidney Dis. 2011;58:398-408.
37. Rubenstein MH, Sheynberg BV, Harrell LC, Schunkert H, Bazari H, Pa-lacios IF. Effectiveness of and adverse events after percutaneous coronary intervention in patients with mild versus severe renal failure. Am J Car-diol. 2001;87:856-860.
38. Hakim RM, Himmelfarb J. Hemodialysis access failure: a call to action: revisited. Kidney Int. 2009;76:1040-1048.
39. Lee T, Roy-Chaudhury P. Advances and new frontiers in the pathophysiol-ogy of venous neointimal hyperplasia and dialysis access stenosis. Adv Chronic Kidney Dis. 2009;16:329-338.