Cathepsin G-regulated release of formyl peptide receptor agonists modulate neutrophil effector functions

Journal of Biological Chemistry

Volumn 287, Issue 41, 2012, Pages 34101-34109

  Woloszynek, Josh C ^a   Hu, Ying ^a   Pham, Christine T N ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANNEXINS; ANTIMICROBIAL PEPTIDE; CHEMOKINES; DOSE-DEPENDENT MANNER; ELASTASE; EXTRACELLULAR; FORMYL PEPTIDE RECEPTOR; IMMUNE COMPLEX; IN-VITRO; IN-VIVO; INFLAMMATORY MEDIATORS; N-TERMINALS; PROTEOMIC APPROACHES; REACTIVE OXYGEN SPECIES; SERINE PROTEASE;

AMINO ACIDS; DEFECTS; ENZYME ACTIVITY; PEPTIDES;

POLYPEPTIDES;

CATHELIN RELATED ANTIMICROBIAL PEPTIDE; CATHEPSIN G; CXCL2 CHEMOKINE; FORMYLPEPTIDE RECEPTOR; LEUKOCYTE ELASTASE; LIPOCORTIN 1; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEOMICS; SIGNAL TRANSDUCTION;

ANIMALS; ANNEXIN A1; CATHELICIDINS; CATHEPSIN G; CHEMOKINE CXCL2; CHEMOTACTIC FACTORS; MICE; MICE, MUTANT STRAINS; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEUTROPHILS; OLIGOPEPTIDES; PROTEOLYSIS; REACTIVE OXYGEN SPECIES; RECEPTORS, FORMYL PEPTIDE;

EID: 84867248955     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.394452     Document Type: Article

References (54)

1. Pham, C. (2006) Neutrophil serine proteases: Specific regulators of inflammation. Nat. Rev. Immunol. 6, 541-550
2. Adkison, A. M., Raptis, S. Z., Kelley, D. G., and Pham, C. T. (2002) Dipeptidyl peptidase I activates neutrophil-derived serine proteases and regulates the development of acute experimental arthritis. J. Clin. Invest. 109, 363-371 (Pubitemid 34141810)
3. Remijsen, Q., Kuijpers, T. W., Wirawan, E., Lippens, S., Vandenabeele, P., and Vanden Berghe, T. (2011) Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ. 18, 581-588
4. Owen, C. A., Campbell, M. A., Sannes, P. L., Boukedes, S. S., and Campbell, E. J. (1995) Cell surface-bound elastase and cathepsin G on human neutrophils: A novel, non-oxidative mechanism by which neutrophils focus and preserve catalytic activity of serine proteinases. J. Cell Biol. 131, 775-789
5. Raptis, S. Z., Shapiro, S. D., Simmons, P. M., Cheng, A. M., and Pham, C. T. (2005) Serine protease cathepsinGregulates adhesion-dependent neutrophil effector functions by modulating integrin clustering. Immunity 22, 679-691 (Pubitemid 40814499)
6. Belaaouaj, A., McCarthy, R., Baumann, M., Gao, Z., Ley, T. J., Abraham, S. N., and Shapiro, S. D. (1998) Mice lacking neutrophil elastase reveal impaired host defense against gram negative bacterial sepsis. Nat. Med. 4, 615-618 (Pubitemid 28237363)
7. MacIvor, D. M., Shapiro, S. D., Pham, C. T., Belaaouaj, A., Abraham, S. N., and Ley, T. J. (1999) Normal neutrophil function in cathepsin G-deficient mice. Blood 94, 4282-4293
8. Bredemeyer, A. J., Lewis, R. M., Malone, J. P., Davis, A. E., Gross, J., Townsend, R. R., and Ley, T. J. (2004) A proteomic approach for the discovery of protease substrates. Proc. Natl. Acad. Sci. U.S.A. 101, 11785-11790 (Pubitemid 39095372)
9. Tsunezumi, J., Yamamoto, K., Higashi, S., and Miyazaki, K. (2008) Matrilysin (matrix metalloprotease-7) cleaves membrane-bound annexin II and enhances binding of tissue-type plasminogen activator to cancer cell surfaces. FEBS J. 275, 4810-4823
10. Zanetti, M., Litteri, L., Gennaro, R., Horstmann, H., and Romeo, D. (1990) Bactenecins, defense polypeptides of bovine neutrophils, are generated from precursor molecules stored in the large granules. J. Cell Biol. 111, 1363-1371
11. Sørensen, O. E., Follin, P., Johnsen, A. H., Calafat, J., Tjabringa, G. S., Hiemstra, P. S., and Borregaard, N. (2001) Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 97, 3951-3959
12. Perretti, M., and Dalli, J. (2009) Exploiting the annexin A1 pathway for the development of novel anti-inflammatory therapeutics. Br. J. Pharmacol. 158, 936-946
13. Huang, K. S., McGray, P., Mattaliano, R. J., Burne, C., Chow, E. P., Sinclair, L. K., and Pepinsky, R. B. (1987) Purification and characterization of proteolytic fragments of lipocortin I that inhibit phospholipase A2. J. Biol. Chem. 262, 7639-7645
14. Rescher, U., Goebeler, V., Wilbers, A., and Gerke, V. (2006) Proteolytic cleavage of annexin 1 by human leukocyte elastase. Biochim. Biophys. Acta 1763, 1320-1324 (Pubitemid 44779860)
15. Vong, L., D'Acquisto, F., Pederzoli-Ribeil, M., Lavagno, L., Flower, R. J., Witko-Sarsat, V., and Perretti, M. (2007) Annexin 1 cleavage in activated neutrophils: A pivotal role for proteinase 3. J. Biol. Chem. 282, 29998-30004 (Pubitemid 350035249)
16. Cirino, G., Cicala, C., Sorrentino, L., Ciliberto, G., Arpaia, G., Perretti, M., and Flower, R. (1993) Anti-inflammatory actions of an N-terminal peptide from human lipocortin 1. Br. J. Pharmacol. 108, 573-574 (Pubitemid 23067918)
17. Pepinsky, R. B., Sinclair, L. K., Browning, J. L., Mattaliano, R. J., Smart, J. E., Chow, E. P., Falbel, T., Ribolini, A., Garwin, J. L., and Wallner, B. P. (1986) Purification and partial sequence analysis of a 37-kDa protein that inhibits phospholipase A2 activity from rat peritoneal exudates. J. Biol. Chem. 261, 4239-4246 (Pubitemid 17198864)
18. Pestonjamasp, V. K., Huttner, K. H., and Gallo, R. L. (2001) Processing site and gene structure for the murine antimicrobial peptide CRAMP. Peptides 22, 1643-1650 (Pubitemid 32918243)
19. Li, Y., Cai, L., Wang, H., Wu, P., Gu, W., Chen, Y., Hao, H., Tang, K., Yi, P., Liu, M., Miao, S., and Ye D (2011) Pleiotropic regulation of macrophage polarization and tumorigenesis by formyl peptide receptor-2. Oncogene 30, 3887-3899
20. Ernst, S., Lange, C., Wilbers, A., Goebeler, V., Gerke, V., and Rescher, U. (2004) An annexin 1 N-terminal peptide activates leukocytes by triggering different members of the formyl peptide receptor family. J. Immunol. 172, 7669-7676 (Pubitemid 38747633)
21. Kurosaka, K., Chen, Q., Yarovinsky, F., Oppenheim, J. J., and Yang, D. (2005) Mouse cathelin-related antimicrobial peptide chemoattracts leukocytes using formyl peptide receptor-like 1/mouse formyl peptide receptor-like 2 as the receptor and acts as an immune adjuvant. J. Immunol. 174, 6257-6265 (Pubitemid 40663818)
22. Gao, J. L., Guillabert, A., Hu, J., Le, Y., Urizar, E., Seligman, E., Fang, K. J., Yuan, X., Imbault, V., Communi, D., Wang, J. M., Parmentier, M., Murphy, P. M., and Migeotte, I. (2007) F2L, a peptide derived from hemebinding protein, chemoattracts mouse neutrophils by specifically activating Fpr2, the low-affinity N-formylpeptide receptor. J. Immunol. 178, 1450-1456 (Pubitemid 46154616)
23. Zheng Y, Niyonsaba F, Ushio H, Nagaoka I, Ikeda S, Okumura K, Ogawa H. (2007) Cathelicidin LL-37 induces the generation of reactive oxygen species and release of human α-defensins from neutrophils. Br. J. Dermatol. 157, 1124-1131 (Pubitemid 350115677)
24. Alalwani, S. M., Sierigk, J., Herr, C., Pinkenburg, O., Gallo, R., Vogelmeier, C., and Bals, R. (2010) The antimicrobial peptide LL-37 modulates the inflammatory and host defense response of human neutrophils. Eur. J. Immunol. 40, 1118-1126
25. Yang, Y., Leech, M., Hutchinson, P., Holdsworth, S. R., and Morand, E. F. (1997) Antiinflammatory effect of lipocortin 1 in experimental arthritis. Inflammation 21, 583-596 (Pubitemid 28026329)
26. Xu, L. M., Jin, S. W., Zhou, X. Y., Wu, P., Li, Y. S., Zhang, L., Lin, Y. Y., Chen, Y., and Ye, D. Y. (2009) Effects of exogenous annexin-1 on lipopolysaccharide-induced proliferation and reactive oxygen species production partially through modulation of CRAC channels but independent of NF-κB pathway. Inflamm. Res. 58, 921-930
27. Sun, R., Iribarren, P., Zhang, N., Zhou, Y., Gong, W., Cho, E. H., Lockett, S., Chertov, O., Bednar, F., Rogers, T. J., Oppenheim, J. J., and Wang, J. M. (2004) Identification of neutrophil granule protein cathepsin G as a novel chemotactic agonist for the G protein-coupled formyl peptide receptor. J. Immunol. 173, 428-436 (Pubitemid 38797369)
28. Williams, S. L., Milne, I. R., Bagley, C. J., Gamble, J. R., Vadas, M. A., Pitson, S. M., and Khew-Goodall, Y. (2010) A proinflammatory role for proteolytically cleaved annexin A1 in neutrophil transendothelial migration. J. Immunol. 185, 3057-3063
29. Smith, S. F., Tetley, T. D., Guz, A., and Flower, R. J. (1990) Detection of lipocortin 1 in human lung lavage fluid: Lipocortin degradation as a possible proteolytic mechanism in the control of inflammatory mediators and inflammation. Environ. Health Perspect. 85, 135-144 (Pubitemid 20315292)
30. Tsao, F. H., Meyer, K. C., Chen, X., Rosenthal, N. S., and Hu, J. (1998) Degradation of annexin I in bronchoalveolar lavage fluid from patients with cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 18, 120-128 (Pubitemid 128355354)
31. Vishwanatha, J. K., Davis, R. G., Rubinstein, I., and Floreani, A. (1998) Annexin I degradation in bronchoalveolar lavage fluids from healthy smokers: A possible mechanism of inflammation. Clin. Cancer Res. 4, 2559-2564 (Pubitemid 28477925)
32. Perretti, M., Getting, S. J., Solito, E., Murphy, P. M., and Gao, J. L. (2001) Involvement of the receptor for formylated peptides in the in vivo antimigratory actions of annexin 1 and its mimetics. Am. J. Pathol. 158, 1969-1973 (Pubitemid 32545181)
33. La, M., D'Amico, M., Bandiera, S., Di Filippo, C., Oliani, S. M., Gavins, F. N., Flower, R. J., and Perretti, M. (2001) Annexin 1 peptides protect against experimental myocardial ischemia-reperfusion: Analysis of their mechanism of action. FASEB J. 15, 2247-2256 (Pubitemid 32927943)
34. Hong, S. H., Won, J. H., Yoo, S. A., Auh, C. K., and Park, Y. M. (2002) Effect of annexin I on insulin secretion through surface binding sites in rat pancreatic islets. FEBS Lett. 532, 17-20 (Pubitemid 35375859)
35. Won, J. H., Kang, N. N., Auh, C. K., and Park, Y. M. (2003) The surface receptor is involved in annexin I-stimulated insulin secretion in MIN6N8a cells. Biochem. Biophys. Res. Commun. 307, 389-394 (Pubitemid 36818883)
36. Tagoe, C. E., Marjanovic, N., Park, J. Y., Chan, E. S., Abeles, A. M., Attur, M., Abramson, S. B., and Pillinger, M. H. (2008) Annexin-1 mediates TNF-α-stimulated matrix metalloproteinase secretion from rheumatoid arthritis synovial fibroblasts. J. Immunol. 181, 2813-2820
37. Cederlund, A., Gudmundsson, G. H., and Agerberth, B. (2011) Antimicrobial peptides important in innate immunity. FEBS J. 278, 3942-3951
38. Zarember, K. A., Katz, S. S., Tack, B. F., Doukhan, L., Weiss, J., and Elsbach, P. (2002) Host defense functions of proteolytically processed and parent (unprocessed) cathelicidins of rabbit granulocytes. Infect. Immun. 70, 569-576 (Pubitemid 34086921)
39. Verbanac, D., Zanetti, M., and Romeo, D. (1993) Chemotactic and protease-inhibiting activities of antibiotic peptide precursors. FEBS Lett. 317, 255-258 (Pubitemid 23045800)
40. De Yang, Chen, Q., Schmidt, A. P., Anderson, G. M., Wang, J. M., Wooters, J., Oppenheim, J. J., and Chertov, O. (2000) LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J. Exp. Med. 192, 1069-1074
41. Zuyderduyn, S., Ninaber, D. K., Hiemstra, P. S., and Rabe, K. F. (2006) The antimicrobial peptide LL-37 enhances IL-8 release by human airway smooth muscle cells. J. Allergy Clin. Immunol. 117, 1328-1335 (Pubitemid 43795721)
42. Nagaoka, I., Tamura, H., and Hirata, M. (2006) An antimicrobial cathelicidin peptide, human CAP18/LL-37, suppresses neutrophil apoptosis via the activation of formyl-peptide receptor-like 1 and P2X7. J. Immunol. 176, 3044-3052
43. Zhang, Z., Cherryholmes, G., Chang, F., Rose, D. M., Schraufstatter, I., and Shively, J. E. (2009) Evidence that cathelicidin peptide LL-37 may act as a functional ligand for CXCR2 on human neutrophils. Eur. J. Immunol. 39, 3181-3194
44. Subramanian, H., Gupta, K., Guo, Q., Price, R., and Ali, H. (2011) Masrelated gene X2 (MrgX2) is a novel G protein-coupled receptor for the antimicrobial peptide LL-37 in human mast cells: Resistance to receptor phosphorylation, desensitization, and internalization. J. Biol. Chem. 286, 44739-44749
45. Girnita, A., Zheng, H., Grönberg, A., Girnita, L., and Ståhle, M. (2012) Identification of the cathelicidin peptide LL-37 as agonist for the type I insulin-like growth factor receptor. Oncogene 31, 352-365
46. Tjabringa, G. S., Aarbiou, J., Ninaber, D. K., Drijfhout, J. W., Sørensen, O. E., Borregaard, N., Rabe, K. F., Hiemstra, P. S. (2003) The antimicrobial peptide LL-37 activates innate immunity at the airway epithelial surface by transactivation of the epidermal growth factor receptor. J. Immunol. 171, 6690-6696 (Pubitemid 37532101)
47. Malm, J., Sørensen, O., Persson, T., Frohm-Nilsson, M., Johansson, B., Bjartell, A., Lilja, H., Ståhle-Bäckdahl, M., Borregaard, N., and Egesten A. (2000) The human cationic antimicrobial protein (hCAP-18) is expressed in the epithelium of human epididymis, is present in seminal plasma at high concentrations, and is attached to spermatozoa. Infect. Immun. 68, 4297-4302 (Pubitemid 30434586)
48. Bylund, J., Christophe, T., Boulay, F., Nyström, T., Karlsson, A., and Dahlgren, C. (2001) Proinflammatory activity of a cecropin-like antibacterial peptide from Helicobacter pylori. Antimicrob. Agents Chemother. 45, 1700-1704 (Pubitemid 32466337)
49. Bjerknes, R., Vesterhus, P., and Aarskog, D. (1997) Increased neutrophil insulin-like growth factor-I (IGF-I) receptor expression and IGF-I-induced functional capacity in patients with untreated Laron syndrome. Eur. J. Endocrinol. 136, 92-95 (Pubitemid 27090686)
50. Lewkowicz, P., Tchórzewski, H., Dytnerska, K., Banasik, M., and Lewkowicz, N. (2005) Epidermal growth factor enhances TNF-α-induced priming of human neutrophils. Immunol. Lett. 96, 203-210 (Pubitemid 39600776)
51. Zughaier, S. M., Shafer, W. M., and Stephens, D. S. (2005) Antimicrobial peptides and endotoxin inhibit cytokine and nitric oxide release but amplify respiratory burst response in human and murine macrophages. Cell. Microbiol. 7, 1251-1262 (Pubitemid 41179418)
52. Chertov, O., Ueda, H., Xu, L. L., Tani, K., Murphy, W. J., Wang, J. M., Howard, O. M., Sayers, T. J., and Oppenheim J. J. (1997) Identification of human neutrophil-derived cathepsin G and azurocidin/CAP37 as chemoattractants for mononuclear cells and neutrophils. J. Exp. Med. 186, 739-747 (Pubitemid 27381538)
53. Rafiq, K., Hanscom, M., Valerie, K., Steinberg, S. F., and Sabri, A. (2008) Novel mode for neutrophil protease cathepsin G-mediated signaling: Membrane shedding of epidermal growth factor is required for cardiomyocyte anoikis. Circ. Res. 102, 32-41
54. Stie, J., Jesaitis, A. V., Lord, C. I., Gripentrog, J. M., Taylor, R. M., Burritt, J. B., and Jesaitis, A. J. (2007) Localization of hCAP-18 on the surface of chemoattractant-stimulated human granulocytes: Analysis using two novel hCAP-18-specific monoclonal antibodies. J. Leukoc. Biol. 82, 161-172 (Pubitemid 47026428)