Treatment of sepsis-induced acquired protein C deficiency reverses angiotensin-converting enzyme-2 inhibition and decreases pulmonary inflammatory response

Journal of Pharmacology and Experimental Therapeutics

Volumn 325, Issue 1, 2008, Pages 17-26

  Richardson, Mark A ^a   Gupta, Akanksha ^a   O'Brien, Lee A ^a   Berg, David T ^a   Gerlitz, Bruce ^a   Syed, Samreen ^a   Sharma, Ganesh R ^a   Cramer, Martin S ^a   Heuer, Josef G ^a   Galbreath, Elizabeth J ^a   Grinnell, Brian W ^a  

^a ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED PROTEIN C; ANGIOTENSIN; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN II; CHEMOKINE; ENDOTHELIAL PROTEIN C RECEPTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; MACROPHAGE INFLAMMATORY PROTEIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN C; THYMUS AND ACTIVATION REGULATED CHEMOKINE;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CECUM; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG MECHANISM; ENZYME INHIBITION; IMMUNE RESPONSE; LIGATION; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN C DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FAMILY; PUNCTURE; RAT; RECEPTOR UPREGULATION; SEPSIS; SIGNAL TRANSDUCTION;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; GENE EXPRESSION REGULATION; MACROPHAGE INFLAMMATORY PROTEINS; NITRIC OXIDE SYNTHASE TYPE II; PEPTIDYL-DIPEPTIDASE A; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN C DEFICIENCY; RATS; RESPIRATORY DISTRESS SYNDROME, ADULT; SEPSIS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

EID: 41149176563     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.107.130609     Document Type: Article

References (41)

1. Abraham E (2005) Effects of recombinant human activated protein C in human models of endotoxin administration. Proc Am Thorac Soc 2:243-247.
2. Arndt P, Young S, Poch K, Nick J, Falk S, Schrier R, and Worthen G (2006) Systemic inhibition of the angiotensin-converting enzyme limits lipopolysaccharide-induced lung neutrophil recruitment through both bradykinin and angiotensin II-regulated pathways. J Immunol 177:7233-7241.
3. Bastarache J, Ware L, and Bernard G (2006) The role of the coagulation cascade in the continuum of sepsis and acute lung injury and acute respiratory distress syndrome. Semin Respir Crit Care Med 27:365-376.
4. Berg D, Gerlitz B, Sharma G, Richardson M, Stephens E, Grubbs R, Holmes K, Montani D, Zhang T, Cramer M, et al. (2006) FoxA2 involvement in suppression of protein C, an outcome predictor in experimental sepsis. Clinical Vaccine Immunol 13:426-432.
5. Bernard G, Vincent J, Laterre P, LaRosa S, Dhainaut J, Lopez-Rodriguez A, Steingrub J, Garber G, Helterbrand J, Ely E, et al. (2001) Efficacy and safety of recombinant human activated protein C for severe sepsis. New Engl J Med 344:699-705.
6. Bonville C, Bennett N, Koehnlein M, Haines D, Ellis J, DelVecchio A, Rosenberg H, and Domachowske J (2006) Respiratory dysfunction and proinflammatory chemokines in the pneumonia virus of mice (PVM) model of viral bronchiolitis. Virology 349:87-95.
7. Dahlbäck B and Villoutreix B (2005) The anticoagulant protein C pathway. FEBS Lett 579:3310-3316.
8. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, Donovan M, Woolf B, Robison K, Jeyaseelan R, et al. (2000) A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res 87:E1-E9.
9. Ferrario CM, Trask AJ, and Jessup JA (2005) Advances in biochemical and functional roles of angiotensin-converting enzyme 2 and angiotensin-(1-7) in regulation of cardiovascular function. Am J Physiol Heart Circ Physiol 289:H2281-H2290.
10. Fujii Y, Goldberg P, and Hussain SN (1998) Contribution of macrophages to pulmonary nitric oxide production in septic shock. Am J Respir Crit Care Med 157:1645-1651.
11. 37-39 in human protein C inhibits activation by the thrombomodulin-thrombin complex without affecting activation by free thrombin. J Biol Chem 271:22285-22288.
12. Gupta A, Berg D, Gerlitz B, Sharma G, Syed S, Richardson M, Sandusky G, Heuer J, Galbreath E, and Grinnell B (2007) Role of protein C in renal dysfunction after polymicrobial sepsis. J Am Soc Nephrol 18:860-867.
13. Hardaway R (2006) A brief overview of acute respiratory distress syndrome. World J Surg 30:1829-1834.
14. Heuer JG, Sharma GR, Gerlitz B, Zhang T, Bailey DL, Ding C, Berg DT, Perkins D, Stephens EJ, Holmes KC, et al. (2004) Evaluation of protein C and other biomarkers as predictors of mortality in a rat cecal ligation and puncture model of sepsis. Crit Care Med 32:1570-1578.
15. Imai Y, Kuba K, Rao S, Huan Y, Guo F, Guan B, Yang P, Sarao R, Wada T, Leong-Poi H, et al. (2005) Angiotensin-converting enzyme 2 protects from severe acute lung failure. Nature 436:112-116.
16. Institute of Laboratory Animal Resources (1996) Guide for the Care and Use of Laboratory Animals 7th ed. Institute of Laboratory Animal Resources, Commission on Life Sciences, National Research Council, Washington DC.
17. Kerschen E, Fernandez J, Cooley B, Yang X, Sood R, Mosnier L, Castellino F, Mackman N, Griffin J, and Weiler H (2007) Endotoxemia and sepsis mortality reduction by non-anticoagulant activated protein C. J Exp Med 204:2439-2448.
18. Kim JY, Kim D, Lee EM, Choi I, Park CG, Kim KS, Ha J, Kim SJ, Yang J, Kim YS, et al. (2003) Inducible nitric oxide synthase inhibitors prolonged the survival of skin xenografts through selective down-regulation of pro-inflammatory cytokine and CC-chemokine expressions. Transpl Immunol 12:63-72.
19. Kuba K, Imai Y, and Penninger J (2006) Angiotensin-converting enzyme 2 in lung diseases. Curr Opin Pharmacol 6:271-276.
20. Macias WL and Nelson DR (2004) Severe protein C deficiency predicts early death in severe sepsis. Crit Care Med 32:S223-S228.
21. Manabe K, Nishioka Y, Kishi J, Inayama M, Aono Y, Nakamura Y, Ogushi F, Bando H, Tani K, and Sone S (2005) Elevation of macrophage-derived chemokine in eosinophilic pneumonia: a role of alveolar macrophages. J Med Invest 52:85-92.
22. Martin EL, Moyer BZ, Pape MC, Starcher B, Leco KJ, and Veldhuizen RA (2003) Negative impact of tissue inhibitor of metalloproteinase-3 null mutation on lung structure and function in response to sepsis. Am J Physiol Lung Cell Mol Physiol 285:L1222-L1232.
23. Mosnier L, Zlokovic B, and Griffin J (2007) The cytoprotective protein C pathway. Blood 109:3161-3172.
24. Nabah YN, Mateo T, Estelles R, Mata M, Zagorski J, Sarau H, Cortijo J, Morcillo EJ, Jose PJ, and Sanz MJ (2004) Angiotensin II induces neutrophil accumulation in vivo through generation and release of CXC chemokines. Circulation 110:3581-3586.
25. Nick JA, Coldren CD, Geraci MW, Poch KR, Fouty BW, O'Brien J, Gruber M, Zarini S, Murphy RC, Kuhn K, et al. (2004) Recombinant human activated protein C reduces human endotoxin-induced pulmonary inflammation via inhibition of neutrophil chemotaxis. Blood 104:3878-3885.
26. O'Brien L, Gupta A, and Grinnell B (2006) Activated protein C and sepsis. Front Biosci 11:676-698.
27. Orinska Z, Maurer M, Mirghomizadeh F, Bulanova E, Metz M, Nashkevich N, Schiemann F, Schulmistrat J, Budagian V, Giron-Michel J, et al. (2007) IL-15 constrains mast cell-dependent antibacterial defenses by suppressing chymase activities. Nat Med 13:927-934.
28. Ritter M, Mennerich D, Weith A, and Seither P (2005) Characterization of Toll-like receptors in primary lung epithelial cells: strong impact of the TLR3 ligand poly(I:C) on the regulation of Toll-like receptors, adaptor proteins and inflammatory response. J Inflamm (Lond) 29:16.
29. Robriquet L, Collet F, Tournoys A, Prangere T, Neviere R, Fourrier F, and Guery BP (2006) Intravenous administration of activated protein C in Pseudomonas-induced lung injury: impact on lung fluid balance and the inflammatory response. Respir Res 7:41.
30. Schultz M, Haitsma J, Zhang H, and Slutsky A (2006) Pulmonary coagulopathy as a new target in therapeutic studies of acute lung injury or pneumonia: a review. Crit Care Med 34:871-877.
31. Shin H, Kitajima I, Nakajima T, Shao Q, Tokioka T, Takasaki I, Hanyu N, Kubo T, and Maruyama I (1999) Thrombin receptor mediated signals induce expressions of interleukin 6 and granulocyte colony stimulating factor via NF-kappa B activation in synovial fibroblasts. Ann Rheum Dis 58:55-60.
32. Su C, Yang F, and Chen H (2007) Inhibition of inducible nitric oxide synthase attenuates acute endotoxin-induced lung injury in rats. Clin Exp Pharmacol Physiol 34:339-346.
33. + Th cells. Infect Immun 74:5943-5954.
34. van der Poll T, Levi M, Nick JA, and Abraham E (2005) Activated protein C inhibits local coagulation after intrapulmonary delivery of endotoxin in humans. Am J Respir Crit Care Med 171:1125-1128.
35. Vincent J and Zambon M (2006) Why do patients who have acute lung injury/acute respiratory distress syndrome die from multiple organ dysfunction syndrome? Implications for management. Clin Chest Med 27:725-731.
36. Vincent JL, Sakr Y, and Ranieri VM (2003) Epidemiology and outcome of acute respiratory failure in intensive care unit patients. Crit Care Med 31:S296-S299.
37. Wang H, Yi T, Zheng Y, and He S (2007a) Induction of monocyte chemoattractant protein-1 release from A549 cells by agonists of protease-activated receptor-1 and -2. Eur J Cell Biol 86:233-242.
38. Wang LF, Patel M, Razavi H, Weicker, Joseph M, McCormack D, and Mehta S (2002) Role of inducible nitric oxide synthase in pulmonary microvascular protein leak in murine sepsis. Am J Respir Crit Care Med 165:1634-1639.
39. Wang Z, Su F, Rogiers P, and Vincent J (2007b) Beneficial effects of recombinant human activated protein C in a ewe model of septic shock. Crit Care Med Sep 35:2594-2600.
40. Ware LB, Camerer E, Welty-Wolf K, Schultz MJ, and Matthay MA (2006) Bench to bedside: targeting coagulation and fibrinolysis in acute lung injury. Am J Physiol Lung Cell Mol Physiol 291:L307-L311.
41. Xia Z, Wang X, Chen X, and Xia Z (2007) Effect of NO donor sodium nitroprusside on lipopolysaccharide induced acute lung injury in rats. Injury 38:53-59.