Proteinase-activated receptor-1, CCL2, and CCL7 regulate acute neutrophilic lung inflammation

American Journal of Respiratory Cell and Molecular Biology

Volumn 50, Issue 1, 2014, Pages 144-157

  Mercer, Paul F ^a   Williams, Andrew E ^a   Scotton, Christopher J ^a   José, Ricardo J ^a   Sulikowski, Michal ^a   Moffatt, James D ^b   Murray, Lynne A ^c   Chambers, Rachel C ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^c Department of Immunobiology Centocor Research and Development ^*  (United States)

Author keywords

Chemokine; Inflammation; Lung; Neutrophil; Proteinase activated receptor 1

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; PROTEINASE ACTIVATED RECEPTOR 1; RECOMBINANT CYTOKINE; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; LEUKOCYTE; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; MOUSE; NEUTROPHIL; NONHUMAN; PNEUMONIA; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; CHEMOKINE CCL2; CHEMOKINE CCL7; CHEMOKINES; EPITHELIAL CELLS; FEMALE; LEUKOCYTES; LUNG; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED BALB C; NEUTROPHILS; PNEUMONIA; PULMONARY ALVEOLI; RECEPTOR, PAR-1; RECEPTORS, CHEMOKINE; RECEPTORS, INTERLEUKIN-8B;

EID: 84891817128     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0142OC     Document Type: Article

References (49)

1. Grommes J, Soehnlein O. Contribution of neutrophils to acute lung injury. Mol Med 2011; 17: 293-307.
2. Chambers RC. Procoagulant signalling mechanisms in lung inflammation and fibrosis: novel opportunities for pharmacological intervention? Br J Pharmacol 2008; 153: S367-S378. (Pubitemid 351340998)
3. Howell DC, Laurent GJ, Chambers RC. Role of thrombin and its major cellular receptor, protease-activated receptor-1, in pulmonary fibrosis. Biochem Soc Trans 2002; 30: 211-216.
4. Jenkins RG, Su X, Su G, Scotton CJ, Camerer E, Laurent GJ, Davis GE, Chambers RC, Matthay MA, Sheppard D. Ligation of proteaseactivated receptor 1 enhances alpha(v)beta6 integrin-dependent TGFbeta activation and promotes acute lung injury. J Clin Invest 2006; 116: 1606-1614.
5. Scotton CJ, Krupiczojc MA, Konigshoff M, Mercer PF, Lee YC, Kaminski N, Morser J, Post JM, Maher TM, Nicholson AG, et al. Increased local expression of coagulation factor X contributes to the fibrotic response in human and murine lung injury. J Clin Invest 2009; 119: 2550-2563.
6. Tressel SL, Kaneider NC, Kasuda S, Foley C, Koukos G, Austin K, Agarwal A, Covic L, Opal SM, Kuliopulos A. A matrix metalloprotease-PAR1 system regulates vascular integrity, systemic inflammation and death in sepsis. EMBO Mol Med 2011; 3: 370-384.
7. Levitt JE, Gould MK, Ware LB, Matthay MA. The pathogenetic and prognostic value of biologic markers in acute lung injury. J Intensive Care Med 2009; 24: 151-167.
8. Chambers RC. Role of coagulation cascade proteases in lung repair and fibrosis. Eur Respir J Suppl 2003; 44: 33s-35s. (Pubitemid 37222060)
9. Chignard M, Balloy V. Neutrophil recruitment and increased permeability during acute lung injury induced by lipopolysaccharide. Am J Physiol Lung Cell Mol Physiol 2000; 279: L1083-L1090. (Pubitemid 32009494)
10. Miller EJ, Cohen AB, Nagao S, Griffith D, Maunder RJ, Martin TR, Weiner-Kronish JP, Sticherling M, Christophers E, Matthay MA. Elevated levels of NAP-1/interleukin-8 are present in the airspaces of patients with the adult respiratory distress syndrome and are associated with increased mortality. Am Rev Respir Dis 1992; 146: 427-432.
11. Balamayooran G, Batra S, Balamayooran T, Cai S, Jeyaseelan S. Monocyte chemoattractant protein 1 regulates pulmonary host defense via neutrophil recruitment during Escherichia coli infection. Infect Immun 2011; 79: 2567-2577.
12. Balamayooran G, Batra S, Theivanthiran B, Cai S, Pacher P, Jeyaseelan S. Intrapulmonary G-CSF rescues neutrophil recruitment to the lung and neutrophil release to blood in gram-negative bacterial infection in MCP-12/2 mice. J Immunol 2012; 189: 5849-5859.
13. Crane MJ, Hokeness-Antonelli KL, Salazar-Mather TP. Regulation of inflammatory monocyte/macrophage recruitment from the bone marrow during murine cytomegalovirus infection: role for type i interferons in localized induction of CCR2 ligands. J Immunol 2009; 183: 2810-2817.
14. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, Mack M, Charo IF. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 2007; 117: 902-909. (Pubitemid 46556746)
15. Jia T, Serbina NV, Brandl K, Zhong MX, Leiner IM, Charo IF, Pamer EG. Additive roles for MCP-1 and MCP-3 in CCR2-mediated recruitment of inflammatory monocytes during Listeria monocytogenes infection. J Immunol 2008; 180: 6846-6853.
16. Winter C, Herbold W, Maus R, Langer F, Briles DE, Paton JC, Welte T, Maus UA. Important role for CC chemokine ligand 2-dependent lung mononuclear phagocyte recruitment to inhibit sepsis in mice infected with Streptococcus pneumoniae. J Immunol 2009; 182: 4931-4937.
17. Kurihara T, Warr G, Loy J, Bravo R. Defects in macrophage recruitment and host defense in mice lacking the CCR2 chemokine receptor. J Exp Med 1997; 186: 1757-1762. (Pubitemid 27506288)
18. Zhang HC, Derian CK, Andrade-Gordon P, Hoekstra WJ, McComsey DF, White KB, Poulter BL, Addo MF, Cheung WM, Damiano BP, et al. Discovery and optimization of a novel series of thrombin receptor (PAR-1) antagonists: potent, selective peptide mimetics based on indole and indazole templates. J Med Chem 2001; 44: 1021-1024. (Pubitemid 32852127)
19. Damiano BP, Derian CK, Maryanoff BE, Zhang HC, Gordon PA. RWJ- 58259: a selective antagonist of protease activated receptor-1. Cardiovasc Drug Rev 2003; 21: 313-326. (Pubitemid 38029966)
20. Andrade-Gordon P, Derian CK, Maryanoff BE, Zhang HC, Addo MF, Cheung W, Damiano BP, D'Andrea MR, Darrow AL, Garavilla L, et al. Administration of a potent antagonist of protease-activated receptor- 1 (PAR-1) attenuates vascular restenosis following balloon angioplasty in rats. J Pharmacol Exp Ther 2001; 298: 34-42. (Pubitemid 32574507)
21. Derian CK, Damiano BP, Addo MF, Darrow AL, D'Andrea MR, Nedelman M, Zhang HC, Maryanoff BE, Andrade-Gordon P. Blockade of the thrombin receptor protease-activated receptor-1 with a small-molecule antagonist prevents thrombus formation and vascular occlusion in nonhuman primates. J Pharmacol Exp Ther 2003; 304: 855-861. (Pubitemid 36152366)
22. Ramachandran R, Noorbakhsh F, Defea K, Hollenberg MD. Targeting proteinase-activated receptors: therapeutic potential and challenges. Nat Rev Drug Discov 2011; 11: 69-86.
23. Howell DC, Johns RH, Lasky JA, Shan B, Scotton CJ, Laurent GJ, Chambers RC. Absence of proteinase-activated receptor-1 signaling affords protection from bleomycin-induced lung inflammation and fibrosis. Am J Pathol 2005; 166: 1353-1365. (Pubitemid 40586507)
24. Summers C, Rankin SM, Condliffe AM, Singh N, Peters AM, Chilvers ER. Neutrophil kinetics in health and disease. Trends Immunol 2010; 31: 318-324.
25. Ma L, Dorling A. The roles of thrombin and protease-activated receptors in inflammation. Semin Immunopathol 2012; 34: 63-72.
26. Sadik CD, Kim ND, Luster AD. Neutrophils cascading their way to inflammation. Trends Immunol 2011; 32: 452-460.
27. Matute-Bello G, Downey G, Moore BB, Groshong SD, Matthay MA, Slutsky AS, Kuebler WM. An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. Am J Respir Cell Mol Biol 2011; 44: 725-738.
28. Maus U, von Grote K, Kuziel WA, Mack M, Miller EJ, Cihak J, Stangassinger M, Maus R, Schlöndorff D, Seeger W, et al. The role of CC chemokine receptor 2 in alveolar monocyte and neutrophil immigration in intact mice. Am J Respir Crit Care Med 2002; 166: 268-273. (Pubitemid 34864412)
29. Wiedermann FJ, Mayr AJ, Kaneider NC, Fuchs D, Mutz NJ, Schobersberger W. Alveolar granulocyte colony-stimulating factor and alpha-chemokines in relation to serum levels, pulmonary neutrophilia, and severity of lung injury in ARDS. Chest 2004; 125: 212-219. (Pubitemid 38114585)
30. Aggarwal A, Baker CS, Evans TW, Haslam PL. G-CSF and IL-8 but not GM-CSF correlate with severity of pulmonary neutrophilia in acute respiratory distress syndrome. Eur Respir J 2000; 15: 895-901. (Pubitemid 30321847)
31. Matthay MA. Cellular basis for injury and repair in the adult respiratory distress syndrome. West J Med 1985; 143: 665-667.
32. Suzuki T, Yamashita C, Zemans RL, Briones N, Van LA, Downey GP. Leukocyte elastase induces lung epithelial apoptosis via a PAR-1-, NF-kappaB-, and P53-dependent pathway. Am J Respir Cell Mol Biol 2009; 41: 742-755.
33. Wang L, Luo J, Fu Y, He S. Induction of interleukin-8 secretion and activation of ERK1/2, p38 MAPK signaling pathways by thrombin in dermal fibroblasts. Int J Biochem Cell Biol 2006; 38: 1571-1583. (Pubitemid 43729306)
34. Scholz M, Vogel JU, Hover G, Kotchetkov R, Cinatl J, Doerr HW, Cinatl J. Thrombin stimulates IL-6 and IL-8 expression in cytomegalovirusinfected human retinal pigment epithelial cells. Int J Mol Med 2004; 13: 327-331.
35. Asokananthan N, Graham PT, Fink J, Knight DA, Bakker AJ, McWilliam AS, Thompson PJ, Stewart GA. Activation of protease-activated receptor (PAR)-1, PAR-2, and PAR-4 stimulates IL-6, IL-8, and prostaglandin E2 release from human respiratory epithelial cells. J Immunol 2002; 168: 3577-3585. (Pubitemid 34250428)
36. Deng X, Mercer PF, Scotton CJ, Gilchrist A, Chambers RC. Thrombin induces fibroblast CCL2/JE production and release via coupling of PAR1 to Galphaq and cooperation between ERK1/2 and Rho kinase signaling pathways. Mol Biol Cell 2008; 19: 2520-2533.
37. Goodman RB, Pugin J, Lee JS, Matthay MA. Cytokine-Mediated Inflammation in Acute Lung Injury. Cytokine Growth Factor Rev 2003; 14: 523-535. (Pubitemid 37296025)
38. Pease JE, Sabroe I. The role of interleukin-8 and its receptors in inflammatory lung disease: implications for therapy. Am J Respir Med 2002; 1: 19-25. (Pubitemid 37038920)
39. Mukaida N. Pathophysiological roles of interleukin-8/CXCL8 in pulmonary diseases. Am J Physiol Lung Cell Mol Physiol 2003; 284: L566-L577. (Pubitemid 36343304)
40. Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, Matsushima K. Essential involvement of interleukin-8 (IL-8) in acute inflammation. J Leukoc Biol 1994; 56: 559-564. (Pubitemid 24348812)
41. Ichikawa A, Kuba K, Morita M, Chida S, Tezuka H, Hara H, Sasaki T, Ohteki T, Ranieri VM, Dos Santos CC, et al. CXCL10-CXCR3 enhances the development of neutrophil-mediated fulminant lung injury of viral and nonviral origin. Am J Respir Crit Care Med 2013; 187: 65-77.
42. Bozic CR, Gerard NP, Gerard C. Receptor binding specificity and pulmonary gene expression of the neutrophil-activating peptide ENA-78. Am J Respir Cell Mol Biol 1996; 14: 302-308. (Pubitemid 126439825)
43. Mercer PF, Johns RH, Scotton CJ, Krupiczojc MA, Konigshoff M, Howell DC, McAnulty RJ, Das A, Thorley AJ, Tetley TD, et al. Pulmonary epithelium is a prominent source of proteinase-activated receptor-1-inducible CCL2 in pulmonary fibrosis. Am J Respir Crit Care Med 2009; 179: 414-425.
44. Menten P, Wuyts A, Van DJ. Monocyte chemotactic protein-3. Eur Cytokine Netw 2001; 12: 554-560. (Pubitemid 34062141)
45. Van DJ, Proost P, Lenaerts JP, Opdenakker G. Structural and functional identification of two human, tumor-derived monocyte chemotactic proteins (MCP-2 and MCP-3) belonging to the chemokine family. J Exp Med 1992; 176: 59-65.
46. Saban R, D'Andrea MR, Andrade-Gordon P, Derian CK, Dozmorov I, Ihnat MA, Hurst RE, Simpson C, SabanMR. Regulatory network of inflammation downstream of proteinase-activated receptors. BMC Physiol 2007; 7: 3.
47. Maus UA, Waelsch K, Kuziel WA, Delbeck T, Mack M, Blackwell TS, Christman JW, Schlondorff D, Seeger W, Lohmeyer J. Monocytes are potent facilitators of alveolar neutrophil emigration during lung inflammation: role of the CCL2-CCR2 axis. J Immunol 2003; 170: 3273-3278. (Pubitemid 36302205)
48. TRA*CER Executive and Steering Committees. The Thrombin Receptor Antagonist for Clinical Event Reduction in Acute Coronary Syndrome (TRA*CER) trial: study design and rationale. Am Heart J 2009; 158: 327-334.
49. Morrow DA, Scirica BM, Fox KA, Berman G, Strony J, Veltri E, Bonaca MP, Fish P, McCabe CH, Braunwald E. Evaluation of a novel antiplatelet agent for secondary prevention in patients with a history of atherosclerotic disease: design and rationale for the Thrombin-Receptor Antagonist in Secondary Prevention of Atherothrombotic Ischemic Events (TRA 2 Degrees P)-TIMI 50 trial. Am Heart J 2009; 158: 335-341.