An antimicrobial cathelicidin peptide, human CAP18/LL-37, suppresses neutrophil apoptosis via the activation of formyl-peptide receptor-like 1 and P2X7

Journal of Immunology

Volumn 176, Issue 5, 2006, Pages 3044-3052

  Nagaoka, Isao ^a   Tamura, Hiroshi ^b   Hirata, Michimasa ^c  

^a JUNTENDO UNIVERSITY   (Japan)

^b Insititute of Ohtaka Enzyme ^*

^c Ohtaka Enzyme Co Ltd   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CATHELICIDIN; CHEMOATTRACTANT; FORMYLPEPTIDE RECEPTOR; FORMYLPEPTIDE RECEPTOR LIKE 1; HUMAN CATIONIC ANTIBACTERIAL PROTEIN OF 18 KDA; INHIBITOR OF APOPTOSIS PROTEIN; LL 37; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN BCL XL; PURINE P2X7 RECEPTOR; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; APOPTOSIS; ARTICLE; BACTERIAL INFECTION; BACTERICIDAL ACTIVITY; CELL STRUCTURE; CONTROLLED STUDY; DRUG POTENCY; DRUG RECEPTOR BINDING; ENZYME PHOSPHORYLATION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HORMONAL REGULATION; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; LIFESPAN; NEUTROPHIL; NORMAL HUMAN; PRIORITY JOURNAL;

EID: 33644511380     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.5.3044     Document Type: Article

References (65)

1. Smith, J. A. 1994. Neutrophils, host defense, and inflammation: a double-edged sword. J. Leukocyte Biol. 56: 672-686.
2. Whyte, M., S. Renshaw, R. Lawson, and C. Bingle. 1999. Apoptosis and the regulation of neutrophil life span. Biochem. Soc. Trans. 27: 802-807.
3. Keel, M., U. Ungethüm, U. Steckholzer, E. Niedere, T. Hartung, O. Trentz, and W. Ertel. 1997. Interleukin-10 counterregulates proinflammatory cytokine-induced inhibition of neutrophil apoptosis during severe sepsis. Blood 90: 3356-3363.
4. Jimenez, M. F., R. W. G. Watson, J. Parodo, D. Evans, D. Foster, M. Steinberg, O. D. Rotstein, and J. C. Marshall. 1997. Dysregulated expression of neutrophil apoptosis in the systemic inflammatory response syndrome. Arch. Surg. 132: 1263-1269.
5. Matute-Bello, G., W. C. Liles, F. Radella II, K. P. Steinberg, J. T. Ruzinski, M. Jonas, E. Y. Chi, L. D. Hudson, and T. R. Martin. 1997. Neutrophil apoptosis in the acute respiratory distress syndrome. Am. J. Respir. Crit. Care Med. 156: 1969-1977.
6. Colotta, F., F. Re, N. Polentarutti, S. Sozzani, and A. Mantovani. 1992. Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 80: 2012-2020.
7. Akgul, C., D. A. Moulding, and S. W. Edwards. 2001. Molecular control of neutrophil apoptosis. FEBS Lett. 487: 318-322.
8. Oberholzer, C., A. Oberholzer, M. Clare-Salzler, and L. L. Moldawer. 2001. Apoptosis in sepsis: a new target for therapeutic exploration. FASEB J. 15: 879-892.
9. Cohen, J. 2002. The immunopathogenesis of sepsis. Nature 420: 885-891.
10. Liles, W. C., P. A. Kiener, J. A. Ledbetter, A. Aruffo, and S. J. Klebanoff. 1996. Differential expression of Fas (CD95) and Fas ligand on normal human phagocytes: implications for the regulation of apoptosis in neutrophils. J. Exp. Med. 184: 429-440.
11. Kasahara, Y., K. Iwai, A. Yachie, K. Ohta, A. Konno, H. Seki, T. Miyawaki, and N. Taniguchi. 1997. Involvement of reactive oxygen intermediates in spontaneous and CD95 (Fas/APO-1)-mediated apoptosis of neutrophils. Blood 89: 1748-1753.
12. Gamberale, R., M. Giordano, A. S. Trevani, G. Andonegui, and J. R. Geffner. 1998. Modulation of human neutrophil apoptosis by immune complexes. J. Immunol. 161: 3666-3674.
13. Usher, L. R., R. A. Lawson, I. Geary, C. J. Taylor, C. D. Bingle, G. W. Taylor, and M. K. B. Whyte. 2002. Induction of neutrophil apoptosis by the Pseudomonas aeruginosa exotoxin pyocyanin: a potential mechanism of persistent infection. J. Immunol. 168: 1861-1868.
14. Martin, E., T. Ganz, and R. I. Lehrer. 1995. Defensins and other endogenous peptide antibiotics of vertebrates. J. Leukocyte Biol. 58: 128-136.
15. Hancock, R. E. W., and G. Diamond. 2000. The role of cationic antimicrobial peptides in innate host defenses. Trends Microbiol. 8: 402-410.
16. Selsted, M. E., and A. J. Quellette. 2005. Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 6: 551-557.
17. Levy, O. 2004. Antimicrobial proteins and peptides: anti-infective molecules of mammalian leukocytes. J. Leukocyte Biol. 76: 909-925.
18. Gennaro, R., and M. Zanetti. 2000. Structural features and biological activities of the cathelicidin-derived antimicrobial peptides. Biopolymers 55: 31-49.
19. Larrick, J. W., M. Hirata, R. F. Balint, J. Lee, J. Zhong, and S. Wright. 1995. Human CAP18: a novel antimicrobial lipopolysaccharide-binding protein. Infec. Immun. 63: 1291-1297.
20. Gudmundsson, G. H., B. Agerberth, J. Odeberg, T. Bergman, B. Olsson, and R. Salcedo. 1996. The human gene FALL39 and processing of the cathelin precursor to the antibacterial peptide LL-37 in granulocytes. Eur. J. Biochem. 238: 325-332.
21. Turner, J., Y. Cho, N. N. Dinh, A. J. Waring, and R. I. Lehrer. 1998. Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob. Agents Chemother. 42: 2206-2214.
22. + cells. J. Immunol. 167: 3329-3338.
23. Yang, D., Q. Chen, A. P. Schmidt, G. M. Anderson, J. M. Wang, J. Wooters, J. J. Oppenheim, and O. Chertov. 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.
24. 7 receptor activator, the human cathelicidin-derived peptide LL-37, induces IL-1β processing and release. J. Immunol. 172: 4987-4994.
25. Yang, D., O. Chertov, and J. J. Oppenheim. 2001. Participation of mammalian defensins and cathelicidins in anti-microbial immunity: receptors and activities of human defensins and cathelicidin (LL-37). J. Leukocyte Biol. 69: 691-697.
26. Bowdish, D. M. E., D. J. Davidson, Y. E. Lau, M. G. Scott, and R. E. K. Hancock. 2005. Impact of LL-37 on anti-infective immunity. J. Leukocyte Biol. 77: 451-459.
27. Bae, Y. S., H. Y. Lee, E. J. Jo, J. I. Kim, H. K. Kang, R. D. Ye, J. Y. Kwak, and S. H. Ryu. 2004. Identification of peptides that antagonize formyl peptide receptor-like 1-mediated signaling. J. Immunol. 173: 607-614.
28. Le, Y., P. M. Murphy, and J. M. Wang. 2002. Formyl-peptide receptors revised. Trends Immunol. 23: 541-548.
29. Nagaoka, I., S. Yomogida, H. Tamura, and M. Hirata. 2004. Antibacterial cathelicidin peptide CAP11 inhibits the lipopolysaccharide (LPS)-induced suppression of neutrophil apoptosis by blocking the binding of LPS to target cells. Inflamm. Res. 53: 609-622.
30. North, R. A., and A. Surprenant. 2000. Pharmacology of cloned P2X receptors. Annu. Rev. Pharmacol. Toxicol. 40: 563-580.
31. 7 receptor. Curr. Top. Med. Chem. 4: 1707-1717.
32. Fan, G. H., L. Z. Wang, H. C. Qiu, L. Ma, and G. Pei. 1999. Inhibition of calcium/calmodulin-dependent protein kinase II in rat hippocampus attenuates morphine tolerance and dependence. Mol. Pharmacol. 56: 39-45.
33. Majewska, E., Z. Sulowska, and Z. Baj. 2000. Spontaneous apoptosis of neutrophils in whole blood and its relation to apoptosis gene proteins. Scand. J. Immunol. 52: 496-501.
34. Vermes, I., C. Haanen, and C. Reutelingsperger. 2000. Flow cytometry of apoptotic cell death. J. Immunol. Methods 243: 167-190.
35. Hua, J., S. Suguro, K. Iwabuchi, Y. Tsutsumi-Ishii, K. Sakamoto, and I. Nagaoka. 2004. Glucosamine, a naturally occurring amino monosaccharide, suppresses the ADP-mediated platelet activation in humans. Inflamm. Res. 53: 680-688.
36. Hengartner, M. O. 2000. The biochemistry of apoptosis. Nature 407: 770-776.
37. Nolan, B., A. Duffy, L. Faquin, M. De, H. Collette, C. M. Graziano, and P. Bankey. 1999. Mitogen-activated protein kinases signal inhibition of apoptosis in lipopolysaccharide-stimulated neutrophils. Surgery 126: 406-412.
38. L- and Bax-α-mediated regulation of apoptosis of human neutrophils via caspase-3. Blood 93: 3106-3115.
39. L up-regulation via inhibition of caspase activities in erythropoietin signaling. J. Cell. Physiol. 195: 290-297.
40. 2 or lipoxin A4 in human neutrophils. Mol. Pharmacol. 64: 721-730.
41. Pfeiffer, Z. A., M. Aga, U. Prabhu, J. J. Watters, D. J. Hall, and P. J. Bertics. 2004. The nucleotide receptor P2X7 mediates actin reorganization and membrane blebbing in RAW264.7 macrophages via p38 MAP kinase and Rho. J. Leukocyte Biol. 75: 1173-1182.
42. Matsuzaki, K. 1999. Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta 1462: 1-10.
43. Tossi, A., L. Sandri, and A. Giangaspero. 2000. Amphipathic, α-helical antimicrobial peptides. Biopolymers 55: 4-30.
44. Yang, D., O. Chertov, S. N. Bykovskaia, Q. Chen, M. J. Buffo, J. Shogan, M. Anderson, J. M. Schröder, J. M. Wang, O. M. Z. Howard, and J. J. Oppenheim. 1999. β-Defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286: 425-528.
45. Niyonsaba, F., H. Ogawa, and I. Nagaoka. 2004. Human β-defensin-2 functions as a chemotactic agent for tumor necrosis factor-α-treated human neutrophils. Immunology 111: 273-281.
46. Khine, A. A., L. del Sorbo, A. S. Slutsky, and H. Zhang. 2004. Human neutrophil-peptides-induced interleukin-8 production by P2 receptor-nucleotide signaling in lung epithelial cells. Am. J. Respir. Crit. Care Med. 169: A806.
47. 7 receptor. Neuropharmacology 36: 1277-1283.
48. Tjabringa, G. S., J. Aarbiou, D. K. Ninaber, J. W. Drijfhout, O. E. Sørensen, N. Borregaard, K. F. Rabe, and P. S. Hiemstra. 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.
49. 7 receptor activation. J. Immunol. 173: 1202-1208.
50. North, R. A. 2002. Molecular physiology of P2X receptors. Physiol. Rev. 82: 1013-1067.
51. 7 contains multiple protein- and lipid-interaction motifs including a potential binding site for bacterial lipopolysaccharide. J. Immunol. 167: 1871-1876.
52. 2Z receptor. J. Biol. Chem. 268: 8199-8203.
53. Gudmundsson, G. H., and B. Agerberth. 1999. Neutrophil antibacterial peptides, multifunctional effector molecules in the mammalian immune system. J. Immunol. Methods 232: 45-54.
54. Agerberth, B., J. Charo, J. Werr, B. Olsson, F. Idali, L. Lindbom, R. Kiessling, H. Jörnvall, H. Wigzell, and G. H. Gudmundsson. 2000. The human antimicrobial and chemotactic peptides LL-37 and α-defensins are expressed by specific lymphocyte and monocyte populations. Blood 96: 3086-3093.
55. Nardo, A. D., A. Vitiello, and R. L. Gallo. 2003. Mast cell antimicrobial activity is mediated by expression of cathelicidin antimicrobial peptide. J. Immunol. 170: 2274-2278.
56. Bowdish, D. M. E., D. J. Davidson, and R. E. W. Hancock. 2005. A re-evaluation of the role of host defense peptides in mammalian immunity. Curr. Protein Pept. Sci. 6: 35-51.
57. Chen, C. I. U., S. Schaller-Bals, K. P. Paul, U. Wahn, and R. Bals. 2004. β-Defensins and LL-37 in bronchoalveolar lavage fluid of patients with cystic fibrosis. J. Cyst. Fibros. 3: 45-50.
58. Sørensen, O., J. B. Cowland, J. Askaa, and B. Borregaard. 1997. An ELISA for hCAP18, the cathelicidin present in human neutrophils and plasma. J. Immunol. Methods 206: 53-59.
59. Theilgaard-Mönch, K., S. Knudsen, P. Follin, and N. Borregaard. 2004. The transcriptional activation program of human neutrophils in skin lesions supports their important role in wound healing. J. Immunol. 172: 7684-7693.
60. Zychlinsky, A., and P. Sansonetti. 1997. Apoptosis in bacterial pathogenesis. J. Clin. Invest. 100: 493-496.
61. Allen, L., D. H. Dockrell, T. Pattery, D. G. Lee, P. Cornelis, P. G. Hellewell, and M. K. B. Whyte. 2005. Pyocyanin production by Pseudomonas aeruginosa induces neutrophil apoptosis and impairs neutrophil-mediated host defenses in vivo. J. Immunol. 174: 3643-3649.
62. Ramanathan, B., H. Wu, C. R. Ross, and F. Blecha. 2004. PR-39, a porcine antimicrobial peptide, inhibits apoptosis: involvement of caspase-3. Dev. Comp. Immunol. 28: 163-169.
63. Risso, A., M. Zanetti, and R. Gennaro. 1998. Cytotoxicity and apoptosis mediated by two peptides of innate immunity. Cell. Immunol. 189: 107-115.
64. Okumura, K., A. Itoh, E. Isogai, K. Hirose, Y. Hosokawa, Y. Abiko, T. Shibata, M. Hirata, and H. Isogai. 2004. C-terminal domain of human CAP18 antimicrobial peptide induces apoptosis in oral squamous cell carcinoma SAS-H1 cells. Cancer Lett. 212: 185-194.
65. Kirikae, T., M. Hirata, H. Yamasu, F. Kirikae, H. Tamura, F. Kayama, K. Nakatsuka, T. Yokochi, and M. Nakano. 1998. Protective effects of a human 18-kilodalton cationic antimicrobial protein (CAP18)-derived peptide against murine endotoxemia. Infect. Immun. 66: 1861-1868.