A matched cross-sectional study of the association between circulating tissue factor activity, immune activation and advanced liver fibrosis in hepatitis C infection

BMC Infectious Diseases

Volumn 15, Issue 1, 2015, Pages

  Hodowanec, Aimee C ^a,b   Lee, Rebecca D ^c   Brady, Kirsten E ^b   Gao, Weihua ^d   Kincaid, Stacey ^a   Plants, Jill ^b   Bahk, Mieoak ^a   Mackman, Nigel ^c   Landay, Alan L ^b   Huhn, Gregory D ^a,b  

^a Ruth M Rothstein CORE Center   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Cirrhosis; Coagulation; Fibrosis; Hepatitis C; HIV; Immune activation; Tissue factor; Viral hepatitis

Indexed keywords

BIOLOGICAL MARKER; THROMBOPLASTIN;

ADULT; BLOOD; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; COINFECTION; COMPLICATION; CROSS-SECTIONAL STUDY; CYTOLOGY; DIAGNOSTIC IMAGING; ECHOGRAPHY; FEMALE; FLOW CYTOMETRY; HEPATITIS C; HEPATITIS C, CHRONIC; HIV INFECTIONS; HUMAN; IMMUNOLOGY; LIVER; LIVER CIRRHOSIS; MALE; MIDDLE AGED; PATHOLOGY;

ADULT; BIOMARKERS; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; COINFECTION; CROSS-SECTIONAL STUDIES; FEMALE; FLOW CYTOMETRY; HEPATITIS C; HEPATITIS C, CHRONIC; HIV INFECTIONS; HUMANS; LIVER; LIVER CIRRHOSIS; MALE; MIDDLE AGED; THROMBOPLASTIN; ULTRASONOGRAPHY;

EID: 84928556929     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/s12879-015-0920-1     Document Type: Article

References (50)

1. Weber R, Sabin CA, Friis-Møller N, Reiss P, El-Sar WM, Kirk O, et al. Liver Related Deaths in Persons Infected with the HIV Virus: The D-A-D Study. Ann Intern Med. 2006;166:1632-41.
2. Graham CS, Baden LR, Yu E, Mrus JM, Carnie J, Heeren T, et al. Influence of human immunodeficiency virus infection on the course of hepatitis C virus infection: a meta-analysis. Clin Infect Dis. 2001;33:562-9.
3. Soto B, Sanchez-Quijano A, Rodrigo L, Del Olmo JA, García-Bengoechea M, Hernández-Quero J, et al. Human immunodeficiency virus infection modifies the natural history of chronic parenterally-acquired hepatitis C with an unusually rapid progression to cirrhosis. J Hepatol. 1997;26(1):1-5.
4. Di Martino V, Rufat P, Boyer N, Renard P, Degos F, Martinot-Peignoux M, et al. The influence of human immunodeficiency virus coinfection on chronic hepatitis C in injection drug users: a long-term retrospective cohort study. Hepatology. 2001;34(6):1193-9.
5. Monto A, Kakar S, Dove LM, Bostrom A, Miller EL, Wright TL. Contributions to hepatic fibrosis in HIV-HCV coinfected and HCV monoinfected patients. Am J Gastroenterol. 2006;101:1509-15.
6. Baker JV. Chronic. HIV disease and activation of the coagulation system. Thromb Res. 2013;132(5):495-9.
7. Baker JV, Hullsiek KH, Bradford RL, Prosser R, Tracy RP, Key NS. Circulating levels of tissue factor microparticle procoagulant activity are reduced with antiretroviral therapy and are associated with persistent inflammation and coagulation activation among HIV positive patients. J Acquir Immune Defic Syndr. 2013;63:367-71.
8. Coughlin SR. Thrombin signaling and protease-activated receptors. Nature. 2000;407:258-64.
9. Key NS. Analysis of tissue factor positive microparticles. Thromb Res. 2010;125 Suppl 1:S42-5.
10. Morel O, Jesel L, Freyssinet JM, Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol. 2011;31:15-26.
11. Chu AJ. Tissue factor, blood coagulation, and beyond: An overview. International J Inflammation 2011:367284. Epub.
12. Stravitz RT, Bowling R, Bradford RL, Key NS, Glover S, Thacker LR, et al. Role of procoagulant microparticles in mediating complications and coutcome of acute liver injury/acute liver failure. Hepatology. 2013;58:304-13.
13. Meziani F, Delabranche X, Asfar P, Toti F. Bench-to-bedside review: circulating microparticles-a new player in sepsis? Crit Care. 2010;14:236.
14. Funderburg NT, Mayne E, Sieg SF, Asaad R, Jiang W, Kalinowska M, et al. Increased tissue factor expression on circulating monocytes in chronic HIV infection: relationship to in vivo coagulation and immune activation. Blood. 2010;115(2):161-7.
15. Sandrin L, Tanter M, Catheline S, Fink M. Shear modulus imaging with 2-D transient elastography. IEEE Trans Ultrason Ferroelectr Freq Control. 2002;49(4):426-35.
16. Sandrin L, Tanter M, Gennisson JL, Catheline S, Fink M. Shear elasticity probe for soft tissues with 1-D transient elastography. IEEE Trans Ultrason Ferroelectr Freq Control. 2002;49(4):436-46.
17. Kirk GD, Astemborski J, Mehta SH, Spoler C, Fisher C, Allen D, et al. Assessment of liver fibrosis by transient elastography in persons with hepatitis C virus infection or HIV-hepatitis C virus coinfection. Clin Infect Dis. 2009;48(7):963-72.
18. Khorana AA, Francis CW, Menzies KE, Wang JG, Hyrien O, Hathcock J, et al. Plasma tissue factor may be predictive of venous thromboembolism in pancreatic cancer. J Thromb Haemost. 2008;6:1983-5.
19. Hodowanec A, Brady K, Gao W, Kincaid S, Plants J, Bahk M, et al. Differences in CD4+ T-Cell Immune Activation in HIV, HCV, and HIV/HCV Coinfection are Influenced by HIV and HCV Infection Status. J Aquir Immune Defic Syndr. 2013;64:232-40.
20. Catalfamo M, Wilhelm C, Tcheung L, Proschan M, Friesen T, Park JH, et al. CD4 and CD8 T Cell Immune Activation during Chronic HIV Infection; roles of Homeostasis, HIV, Type I IFN, IL-7. J Immunol. 2011;186:2106-16.
21. Hurley AH, Smith M, Karpova T, Hasley RB, Belkina N, Shaw S, et al. Enhanced Effector Function of CD8+ T Cells From Healthy Controls and HIV-infected Patients Occurs through Thrombin Activation of Protease-Activated Receptor 1. J Infect Dis. 2013;207:638-50.
22. Balagopal A, Philp FH, Astemborski J, Block TM, Mehta A, Long R, et al. Human immunodeficiency virus-related microbial translocation and progression of hepatitis C. Gastroenterology. 2008;135(1):226-33.
23. Rasaratnam B, Kaye D, Jennings G, Dudley F, Chin-Dusting J, et al. The effect of selective intestinal decontamination on the hyperdynamic circulatory state in cirrhosis. A randomized trial. Ann Intern Med. 2003;139:186-93.
24. Gauley J, Pisetsky DS. The release of microparticles by RAW 264.7 macrophage cells stimulated with TLR ligands. J Leukoc Biol. 2010;87:1115-23.
25. Kornek M, Popov Y, Libermann TA, Afdhal NH, Schuppan D. Human T cell microparticles circulate in blood of hepatitis patients and induce fibrolytic activation of hepatic stellate cells. Hepatology. 2011;53:230-42.
26. Gonzalez SA, Fiel MI, Sauk J, Canchis PW, Liu RC, Chiriboga L, et al. Inverse association between hepatic stellate cell apoptosis and fibrosis in chronic hepatitis C virus infection. J Viral Hepat. 2009;16(2):141-8.
27. Friedman SL. Molecular regulation of hepatic fibrosis, and integrated cellular response to tissue injury. J Biol Chem. 2000;22:136-44.
28. Canbay A, Friedman S, Gores GJ. Apoptosis: the nexus of liver injury and fibrosis. Hepatology. 2004;39:273-8.
29. Baker AK, Wang R, Mackman N, Luyendyk JP. Rapamycin enhances LPS induction of tissue factor and tumor necrosis factor-alpha expression in macrophages by reducing IL-10 expression. Mol Immunol. 2009;46:2249-55.
30. Antoniak S, Owens 3rd AP, Baunacke M, Williams JC, Lee RD, Weithäuser A, et al. PAR-1 contributes to the innate immune response during viral infection. J Clin Invest. 2013;123(3):1310-22.
31. Petts G, Dhar A, Kudo H, Sadiq F, Anstee QM, Kallis YN, et al. Targeted. inhibition of tissue factor suppresses hepatic fibrosis in CCL4 treated mice. Gut. 2012;61:A28-8.
32. Martinelli A, Knapp S, Anstee Q, Worku M, Tommasi A, Zucoloto S, et al. Effect of a thrombin receptor (protease-activated receptor 1, PAR-1) gene polymorphism in chronic hepatitis C liver fibrosis. J Gastroenterol Hepatol. 2008;23(9):1403-9.
33. Anstee QM, Goldin RD, Wright M, Martinelli A, Cox R, Thursz MR. Coagulation status modulates murine hepatic fibrogenesis: implications for the development of novel therapies. J Thromb Haemost. 2008;6(8):1336-43.
34. Butt AA, Xiaoqiang W, Budoff M, Leaf D, Kuller LH, Justice AC. Hepatitis C Virus Infection and the Risk of Coronary Disease. Clin Infect Dis. 2009;49:225-32.
35. Petta S, Torres D, Fazio G, Cammà C, Cabibi D, Di Marco V, et al. Carotid Atherosclerosis and Chronic Hepatitis C: A Prospective Study of Risk Associations. Hepatology. 2012;55:1317-23.
36. Vassalle, Masini S, Bianchi F, Zucchelli GC. Evidence for association between hepatitis C virus seropositivity and coronary artery disease. Heart. 2004;90:565-6.
37. Alyan O, Kacmaz F, Ozdemir O, Deveci B, Astan R, Celebi AS, et al. Hepatitis C Infection is associated with increased coronary artery atherosclerosis defined by Modified Reardon Severity Score System. Circ J. 2008;72:1960-5.
38. Boddi M, Abbate R, Chellini B, Giusti B, Giannini C, Pratesi G, et al. Hepatitis C virus RNA localization in human carotid plaques. J Clin Virol. 2010;47:72-5.
39. Talal AH, Feron-Rigodon M, Madere J, Subramanian GM. Simtuzumab, an Antifibrotic Monoclonal Antibody Against Lysyl Oxidase-Like 2 (LOXL2) Enzyme, Is Safe and Well Tolerated in Patients with Liver Disease. 2013 European Association of the Study of the Liver Conference. Abstract 1319.
40. Owens AP, Mackman N. Microparticles in hemostasis and thrombosis. Circ Res. 2011;108:1284-97.
41. Lee RD, Barcel DA, Williams JC, Wang JG, Boles JC, Manly DA, et al. Pre-analytical and analytical variables affecting the measurement of plasma-derived microparticle tissue factor activity. Thromb Res. 2012;129:80-5.
42. Auwerda JJ, Yuana Y, Osanto S, de Maat MP, Sonneveld P, Bertina RM. Microparticle-associated tissue factor activity and venous thrombosis in multiple myeloma. Thromb Haemost. 2011;105:14-20.
43. Parhami-Seren B, Butenas S, Krudysz-Ambio J, Mann KG. Immunologic quantitation of tissue factor. J Thromb Haemost. 2006;4:1747-55.
44. Key NS, Mackman N. Tissue factor and its measurements in whole blood, plasma, and microparticles. Semin Thromb Hemost. 2010;36:865-75.
45. Satta N, Toti F, Feugeas O, Bohbot A, Dachary-Prignet J, Eschwege V, et al. Monocyte vesiculation is is a possible mechanism for dissemination of membrane-associated procoagulant activities and adhesion molecules after stimulation by lipopolysaccaride. J Immunol. 1994;153:3245-55.
46. Dasgupta SK, Abdel-Monem H, Niravath P, et al. Lactadherin and clearance of platelet-derived microvesicles. Blood. 2009;113:1332-9.
47. Willekens FL, Werre JM, Kruijt JK, Le A, Bellera RV, Langlois K, et al. Liver Kupffer cells rapidly remove red blood cell-derived vesicles from the circulation by scavenger receptors. Blood. 2005;105:2141-5.
48. Al Faraj A, Gazeau F, Wilhelm C, Devue C, Guérin CL, Péchoux C, et al. Endothelial cell-derived microparticles loaded with iron oxide nanoparticles: feasibility of MR imaging monitoring in mice. Radiology. 2012;263:169-78.
49. Rautou PE, Vion AC, Amabile N, Chironi G, Simon A, Tedgui A, et al. Microparticles, vascular function, and atherothrombosis. Circ Res. 2011;109:593-606.
50. Thabut D, Tazi KA, Bonnefont-Rousselot D, Aller M, Farges O, Guimont MC, et al. High-density lipoprotein administration attenuates liver proinflammatory response, restores liver endothelial nitric oxide synthase activity, and lowers portal pressure in cirrhotic rats. Hepatology. 2007;46:1893-906.