Age-dependent vulnerability to endotoxemia is associated with reduction of anticoagulant factors activated protein C and thrombomodulin

Blood

Volumn 115, Issue 23, 2010, Pages 4886-4893

  Starr, Marlene E ^a,b,c   Ueda, Junji ^a   Takahashi, Hitoshi ^a,b,c   Weiler, Hartmut ^d   Esmon, Charles T ^e   Evers, B Mark ^a,b,c,f   Saito, Hiroshi ^a,b,c  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d BLOOD RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^f UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED PROTEIN C; BACTERIUM LIPOPOLYSACCHARIDE; FIBRIN; THROMBOMODULIN; LIPOPOLYSACCHARIDE; PROTEIN C;

AGE DISTRIBUTION; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CLOTTING; CONTROLLED STUDY; ENDOTOXEMIA; FIBRIN FORMATION; MALE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SURVIVAL; THROMBOSIS; WILD TYPE; ANIMAL; CHEMICALLY INDUCED DISORDER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT; TRANSGENIC MOUSE;

AGING; ANIMALS; ENDOTOXEMIA; FIBRIN; GENE EXPRESSION REGULATION; LIPOPOLYSACCHARIDES; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; PROTEIN C; THROMBOMODULIN; THROMBOSIS;

EID: 77954738683     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-10-246678     Document Type: Article

References (50)

1. Levy MM, Fink MP, Marshall JC, et al. 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med. 2003;31(4):1250- 1256.
2. Bone RC, Balk RA, Cerra FB, et al. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee: American College of Chest Physicians/Society of Critical Care Medicine. Chest. 1992;101(6):1644-1655.
3. Davies MG, Hagen PO. Systemic inflammatory response syndrome. Br J Surg. 1997;84(7):920-935.
4. Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med. 2003;348(16):1546-1554.
5. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med. 2001;29(7):1303-1310. (Pubitemid 32641789)
6. Podnos YD, Jimenez JC, Wilson SE. Intra-abdominal sepsis in elderly persons. Clin Infect Dis. 2002;35(1):62-68.
7. Martin GS, Mannino DM, Moss M. The effect of age on the development and outcome of adult sepsis. Crit Care Med. 2006;34(1):15-21.
8. Gorina Y, Hoyert D, Lentzner H, Goulding M. Trends in causes of death among older persons in the United States. Aging Trends. 2005;(6):1-12.
9. Esmon CT. Inflammation and thrombosis. J Thromb Haemost. 2003;1(7):1343-1348.
10. Levi M, de Jonge E, van der Poll T, ten Cate H. Disseminated intravascular coagulation. Thromb Haemost. 1999;82(2):695-705.
11. Philippart F, Dinarello C. Inflammatory mediators. In: Cavaillon J-M, ed. Sepsis and Non-infectious Systemic Inflammation: From Biology to Critical Care. Weinheim, Germany: Wiley-VCH Verlag; 2009:177-204.
12. Hamzaoui O. Organ Dysfunctions during severe sepsis and septic-like syndromes: epidemiology, classification, and mechanisms. In: Cavaillon J-M, ed. Sepsis and Non-infectious Systemic Inflammation: From Biology to Critical Care. Weinheim, Germany: Wiley-VCH Verlag; 2009:57-76.
13. Esmon CT. Inflammation and the activated protein C anticoagulant pathway. Semin Thromb Hemost. 2006;32(suppl 1):49-60.
14. Toltl LJ, Swystun LL, Pepler L, Liaw PC. Protective effects of activated protein C in sepsis. Thromb Haemost. 2008;100(4):582-592.
15. Van de Wouwer M, Collen D, Conway EM. Thrombomodulin-protein C-EPCR system: integrated to regulate coagulation and inflammation. Arterioscler Thromb Vasc Biol. 2004;24(8):1374-1383. (Pubitemid 39050428)
16. Stearns-Kurosawa DJ, Kurosawa S, Mollica JS, Ferrell GL, Esmon CT. The endothelial cell protein C receptor augments protein C activation by the thrombin-thrombomodulin complex. Proc Natl Acad Sci U S A. 1996;93(19):10212- 10216. (Pubitemid 26314601)
17. Dittman WA, Majerus PW. Structure and function of thrombomodulin: a natural anticoagulant. Blood. 1990;75(2):329-336.
18. Faust SN, Levin M, Harrison OB, et al. Dysfunction of endothelial protein C activation in severe meningococcal sepsis. N Engl J Med. 2001;345(6):408-416. (Pubitemid 32747604)
19. Terada Y, Eguchi Y, Nosaka S, Toba T, Nakamura T, Shimizu Y. Capillary endothelial thrombomodulin expression and fibrin deposition in rats with continuous and bolus lipopolysaccharide administration. Lab Invest. 2003;83(8):1165-1173.
20. Esmon CT. Coagulation inhibitors in inflammation. Biochem Soc Trans. 2005;33(2):401-405.
21. Delvaeye M, Noris M, De Vriese A, et al. Thrombomodulin mutations in atypical hemolytic-uremic syndrome. N Engl J Med. 2009;361(4):345-357.
22. Chorinchath BB, Kong LY, Mao L, McCallum RE. Age-associated differences in TNF-alpha and nitric oxide production in endotoxic mice. J Immunol. 1996;156(4):1525-1530. (Pubitemid 26065864)
23. Tateda K, Matsumoto T, Miyazaki S, Yamaguchi K. Lipopolysaccharide- induced lethality and cytokine production in aged mice. Infect Immun. 1996;64(3):769-774.
24. Saito H, Sherwood ER, Varma TK, Evers BM. Effects of aging on mortality, hypothermia, and cytokine induction in mice with endotoxemia or sepsis. Mech Ageing Dev. 2003;124(10):1047-1058.
25. Weiler-Guettler H, Christie PD, Beeler DL, et al. A targeted point mutation in thrombomodulin generates viable mice with a prethrombotic state. J Clin Invest. 1998;101(9):1983-1991. (Pubitemid 28226118)
26. Weiler H, Lindner V, Kerlin B, et al. Characterization of a mouse model for thrombomodulin deficiency. Arterioscler Thromb Vasc Biol. 2001;21(9):1531-1537.
27. Cleuren AC, van Vlijmen BJ, Reitsma PH. Transgenic mouse models of venous thrombosis: fulfilling the expectations? Semin Thromb Hemost. 2007;33(6):610-616.
28. Weiler H, Kerlin B, Lytle MC. Factor V Leiden polymorphism modifies sepsis outcome: evidence from animal studies. Crit Care Med. 2004;32(5 suppl):S233-S238.
29. Ueda J, Starr ME, Takahashi H, et al. Decreased pulmonary extracellular superoxide dismutase during systemic inflammation. Free Radic Biol Med. 2008;45(6):897-904.
30. Runge MS, Bode C, Matsueda GR, Haber E. Antibody-enhanced thrombolysis: targeting of tissue plasminogen activator in vivo. Proc Natl Acad Sci U S A. 1987;84(21):7659-7662.
31. Li W, Zheng X, Gu J, et al. Overexpressing endothelial cell protein C receptor alters the hemostatic balance and protects mice from endotoxin. J Thromb Haemost. 2005;3(7):1351-1359.
32. Starr ME, Evers BM, Saito H. Age-associated increase in cytokine production during systemic inflammation: adipose tissue as a major source of IL-6. J Gerontol A Biol Sci Med Sci. 2009;64(7):723-730.
33. Ely EW, Angus DC, Williams MD, Bates B, Qualy R, Bernard GR. Drotrecogin alfa (activated) treatment of older patients with severe sepsis. Clin Infect Dis. 2003;37(2):187-195. (Pubitemid 36930348)
34. Borgel D, Bornstain C, Reitsma PH, et al. A comparative study of the protein C pathway in septic and nonseptic patients with organ failure. Am J Respir Crit Care Med. 2007;176(9):878-885.
35. Hanson SR, Griffin JH, Harker LA, Kelly AB, Esmon CT, Gruber A. Antithrombotic effects of thrombin-induced activation of endogenous protein C in primates. J Clin Invest. 1993;92(4):2003-2012.
36. Rijneveld AW, Weijer S, Florquin S, et al. Thrombomodulin mutant mice with a strongly reduced capacity to generate activated protein C have an unaltered pulmonary immune response to respiratory pathogens and lipopolysaccharide. Blood. 2004;103(5):1702-1709.
37. Sohn RH, Deming CB, Johns DC, et al. Regulation of endothelial thrombomodulin expression by inflammatory cytokines is mediated by activation of nuclear factor-kappa B. Blood. 2005;105(10):3910-3917.
38. Kume M, Hayashi T, Yuasa H, et al. Bacterial lipopolysaccharide decreases thrombomodulin expression in the sinusoidal endothelial cells of rats: a possible mechanism of intrasinusoidal microthrombus formation and liver dysfunction. J Hepatol. 2003;38(1):9-17.
39. Bergh N, Ulfhammer E, Glise K, Jern S, Karlsson L. Influence of TNF-alpha and biomechanical stress on endothelial anti- and prothrombotic genes. Biochem Biophys Res Commun. 2009;385(3):314-318.
40. Fukudome K, Esmon CT. Identification, cloning, and regulation of a novel endothelial cell protein C/activated protein C receptor. J Biol Chem. 1994;269(42):26486-26491. (Pubitemid 24328474)
41. Conway EM, Rosenberg RD. Tumor necrosis factor suppresses transcription of the thrombomodulin gene in endothelial cells. Mol Cell Biol. 1988;8(12):5588-5592.
42. Yamamoto K, Shimokawa T, Yi H, et al. Aging accelerates endotoxin-induced thrombosis: increased responses of plasminogen activator inhibitor-1 and lipopolysaccharide signaling with aging. Am J Pathol. 2002;161(5):1805-1814. (Pubitemid 35265538)
43. Saito H, Papaconstantinou J. Age-associated differences in cardiovascular inflammatory gene induction during endotoxic stress. J Biol Chem. 2001;276(31):29307-29312.
44. Zelko IN, Folz RJ. Myeloid zinc finger (MZF)-like, Kruppel-like and Ets families of transcription factors determine the cell-specific expression of mouse extracellular superoxide dismutase. Biochem J. 2003;369(2):375-386.
45. Hamik A, Lin Z, Kumar A, et al. Kruppel-like factor 4 regulates endothelial inflammation. J Biol Chem. 2007;282(18):13769-13779.
46. Lin Z, Kumar A, SenBanerjee S, et al. Kruppel-like factor 2 (KLF2) regulates endothelial thrombotic function. Circ Res. 2005;96(5):e48-e57.
47. Yuksel M, Okajima K, Uchiba M, Horiuchi S, Okabe H. Activated protein C inhibits lipopolysaccharide-induced tumor necrosis factor-alpha production by inhibiting activation of both nuclear factor-kappa B and activator protein-1 in human monocytes. Thromb Haemost. 2002;88(2):267-273.
48. Liaw PC, Esmon CT, Kahnamoui K, et al. Patients with severe sepsis vary markedly in their ability to generate activated protein C. Blood. 2004;104(13):3958-3964.
49. Esmon CT. New mechanisms for vascular control of inflammation mediated by natural anticoagulant proteins. J Exp Med. 2002;196(5):561-564.
50. Xu J, Zhang X, Pelayo R, et al. Extracellular histones are major mediators of death in sepsis. Nat Med. 2009;15(11):1318-1321.