Mast cell cathelicidin antimicrobial peptide prevents invasive group A Streptococcus infection of the skin

Journal of Immunology

Volumn 180, Issue 11, 2008, Pages 7565-7573

  Nardo, Anna Di ^a   Yamasaki, Kenshi ^a   Dorschner, Robert A ^a   Lai, Yuping ^a   Gallo, Richard L ^a,b  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHELICIDIN; ANTIMICROBIAL CATIONIC PEPTIDE; CATHELICIDIN ANTIMICROBIAL PEPTIDE;

ARTICLE; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SKIN DEFECT; SKIN INFECTION; STREPTOCOCCUS INFECTION; SURFACE ENHANCED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; ANIMAL; BACTEREMIA; BACTERIAL COUNT; BACTERIAL SKIN DISEASE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOUSE; MOUSE MUTANT; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; SKIN; STREPTOCOCCUS PYOGENES;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTEREMIA; COLONY COUNT, MICROBIAL; MAST CELLS; MICE; MICE, MUTANT STRAINS; NEUTROPHIL INFILTRATION; NEUTROPHILS; SKIN; SKIN DISEASES, BACTERIAL; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES;

EID: 47249165576     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.11.7565     Document Type: Article

References (58)

1. Malaviya, R., T. Ikeda, E. A. Ross, B. A. Jakschik, and S. N. Abraham. 1995. Bacteria: mast cell interactions in inflammatory disease. Am. J. Ther. 2: 787-792.
2. Malaviya, R., and S. N. Abraham. 2001. Mast cell modulation of immune responses to bacteria. Immunol. Rev. 179: 16-24.
3. Di Nardo, A., A. Vitiello, and R. L. Gallo. 2003. Cutting edge: mast cell antimicrobial activity is mediated by expression of cathelicidin antimicrobial peptide. J. Immunol. 170: 2274-2278.
4. Nizet, V., T. Ohtake, X. Lauth, J. Trowbridge. J. Rudisill, R. A. Dorschner, V. Pestonjamasp, J. Piraino, K. Huttner, and R. L. Gallo. 2001. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414: 454-457.
5. Skerlavaj, B., M. Scocchi, R. Gennaro, A. Risso, and M. Zanetti. 2001. Structural and functional analysis of horse cathelicidin peptides. Antimicrob. Agents Che-mother. 45: 715-722.
6. Scocchi, M., D. Bontempo, S. Boscolo, L. Tomasinsig, E. Giulotto, and M. Zanetti. 1999. Novel cathelicidins in horse leukocytes(1). FEBS Lett. 457: 459-464.
7. Zelezetsky, I., A. Pontillo, L. Puzzi, N. Antcheva, L. Segat, S. Pacor, S. Crovella, and A. Tossi. 2006. Evolution of the primate cathelicidin: correlation between structural variations and antimicrobial activity. J. Biol. Chem. 281: 19861-19871.
8. Siebenhaar, R, W. Syska, K. Weller, M. Magerl, T. Zuberbier, M. Metz, and M. Maurer. 2007. Control of Pseudomonas aeruginosa skin infections in mice is mast cell-dependent. Am. J. Pathol. 170: 1910-1916.
9. Xu, X., D. Zhang, N. Lyubynska, P. J. Wolters, N. P. Killeen, P. Baluk, D. M. McDonald, S. Hawgood, and G. H. Caughey. 2006. Mast cells protect mice from Mycoplasma pneumonia. Am. J. Respir. Crit. Care hied. 173: 219-225.
10. Matsui, K., and A. Nishikawa. 2006. Percutaneous application of peptidoglycan from Staphylococcus aureus induces mast cell development in mouse spleen. Int. Arch. Allergy Immunol. 139: 271-278.
11. Carvalho, M., C. Benjamim, F. Santos, S. Ferreira, and F. Cunha. 2005. Effect of mast cells depletion on the failure of neutrophil migration during sepsis. Eur. J. Pharmacol. 525: 161-169.
12. Kanamaru, Y., K. Sumiyoshi, H. Ushio, H. Ogawa, K. Okumura, and A. Nakao. 2005. Smad3 deficiency in mast cells provides efficient host protection against acute septic peritonitis. J. Immunol. 174: 4193-4197.
13. Mallen-St. Clair, J., C. T. Pham, S. A. Villalta, G. H. Caughey, and P. J. Wolters. 2004. Mast cell dipeptidyl peptidase I mediates survival from sepsis. J. Clin. Invest. 113: 628-634.
14. Mercer-Jones, M. A., M. S. Shrotri, M. Heinzelmann, J. C. Peyton, and W. G. Cheadle. 1999. Regulation of early peritoneal neutrophil migration by macrophage inflammatory protein-2 and mast cells in experimental peritonitis. J. Leukocyte Biol. 65: 249-255.
15. McLachlan, J. B., and S. N. Abraham. 2001. Studies of the multifaceted mast cell response to bacteria. Curr. Opin. Microbiol. 4: 260-266.
16. Malaviya, R., Z. Gao, K. Thankavel, P. A. van der Merwe, and S. N. Abraham. 1999. The mast cell tumor necrosis factor α response to FimH-expressing Esch-erichia coli is mediated by the glycosylphosphatidylinositol-anchored molecule CD48. Proc. Natl. Acad. Sci. USA 96: 8110-8115.
17. Dawicki, W., and J. S. Marshall. 2007. New and emerging roles for mast cells in host defence. Curr. Opin. Immunol. 19: 31-38.
18. Feger, F., S. Varadaradjalou, Z. Gao, S. N. Abraham, and M. Arock. 2002. The role of mast cells in host defense and their subversion by bacterial pathogens. Trends Immunol. 23: 151-158.
19. Urban, J. F., Jr., N. Noben-Trauth, L. Schopf. K. B. Madden, and F. D. Finkelman. 2001. Cutting edge: IL-4 receptor expression by non-bone marrow-derived cells is required to expel gastrointestinal nematode parasites. J. Immunol. 167:6078-6081.
20. Malaviya, R., and S. N. Abraham. 2000. Role of mast cell leukotrienes in neutrophil recruitment and bacterial clearance in infectious peritonitis. J. Leukocyte Biol. 67: 841-846.
21. Nizet, V., and R. L. Gallo. 2003. Cathelicidins and innate defense against invasive bacterial infection. Scand. J. Infect. Dis. 35: 670-676.
22. Bals, R., and J. M. Wilson. 2003. Cathelicidins: a family of multifunctional antimicrobial peptides. Cell Mol. Life Sci. 60: 711-720.
23. Zanetti, M., R. Gennaro, B. Skerlavaj, L. Tomasinsig, and R. Circo. 2002. Cathelicidin peptides as candidates for a novel class of antimicrobials. Curr. Pharni. Des. 8: 779-793.
24. Schauber, J., C. Svanholm, S. Termen, K. Iffland, T. Menzel, W. Scheppach, R. Melcher, B. Agerberth, H. Luhrs, and G. H. Gudmundsson. 2003. Expression of the cathelicidin IX-37 is modulated by short chain fatty acids in colonocytes: relevance of signalling pathways. Cut 52: 735-741.
25. Kai-Larsen, Y., G. Bergsson, G. H. Gudmundsson, G. Printz, H. Jornvall, G. Marchini, and B. Agerberth. 2007. Antimicrobial components of the neonatal gut affected upon colonization. Pediatr. Res. 61: 530-536.
26. Schauber, J., F. Weiler, A. Gostner, R. Melcher, T. Kudlich, H. Luhrs, and W. Scheppach. 2006. Human rectal mucosal gene expression after consumption of digestible and non-digestible carbohydrates. Mol. Nutr. Food Res. 50-1006-1012.
27. Bergman, P., L. Johansson, H. Wan, A. Jones, R. L. Gallo, G. H. Gudmundsson, T. Hokfelt, A. B. Jonsson, and B. Agerberth. 2006. Induction of the antimicrobial peptide CRAMP in the blood-brain barrier and meninges after meningococcal infection. Infect. Immun. 74: 6982-6991.
28. Chromek, M., Z. Slamova, P. Bergman, L. Kovacs, L. Podracka, I. Ehren, T. Hokfelt, G. H. Gudmundsson, R. L. Gallo, B. Agerberth, and A. Brauner. 2006. The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat. Med. 12: 636-641.
29. Gennaro, R., M. Scocchi, L. Merluzzi, and M. Zanetti. 1998. Biological characterization of a novel mammalian antimicrobial peptide. Biochim. Biophys. Ada 1425: 361-368.
30. Travis, S. M., N. N. Anderson, W. R. Forsyth, C. Espiritu, B. D. Conway, E. P. Greenberg, P. B. McCray, Jr., R. I. Lehrer, M. J. Welsh, and B. F. Tack. 2000. Bactericidal activity of mammalian calhelicidin-derived peptides. Infect. Immun. 68: 2748-2755.
31. 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.
32. Zanetti, M. 2004. Cathelicidins, multifunctional peptides of the innate immunity. J. Leukocyte Biol. 75: 39-48.
33. Yamasaki, K., J. Schauber, A. Coda, H. Lin, R. A. Dorschner, N. M. Schechter, C. Bonnart, P. Descargues, A. Hovnanian, and R. L. Gallo. 2006. Kallikrein-mediated proteolysis regulates the antimicrobial effects of cathelicidins in skin. FASEB J. 20: 2068-2080.
34. Gallo, R. L., K. J. Kim, M. Bernfield, C. A. Kozak, M. Zanetti, L. Merluzzi, and R. Gennaro. 1997. Identification of CRAMP, a cathelin-related antimicrobial peptide expressed in the embryonic and adult mouse. J. Biol. Chem. 272: 13088-13093.
35. Agerberth, B., J. Charo, J. Werr, B. Olsson, F. Idali, L. Lindbom, R. Kiessling, H. Jornvall, 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.
36. Bowdish, D. M., D. J. Davidson, D. P. Speert, and R. E. Hancock. 2004. The human cationic peptide LL-37 induces activation of the extracellular signal-regulated kinase and p38 kinase pathways in primary human monocytes. J. Immunol. 172: 3758-3765.
37. Braff, M. H., M. A. Hawkins, A. D. Nardo, B. Lopez-Garcia, M. D. Howell, C. Wong, K. Lin, J. E. Streib, R. Dorschner, D. Y. Leung, and R. L. Gallo. 2005. Structure-function relationships among human cathelicidin peptides: dissociation of antimicrobial properties from host immunostimulatory activities. J. Immunol. 174:4271-4278.
38. Murakami, M., B. Lopez-Garcia, M. Braff, R. A. Dorschner, and R. L. Gallo. 2004. Postsecretory processing generates multiple cathelicidins for enhanced topical antimicrobial defense. J. Immunol. 172: 3070-3077.
39. Echtenacher, B., L. Hultner, and D. N. Mannel. 1995. Cellular and molecular mechanisms of TNF protection in septic peritonitis. J. Inflamm. 47: 85-89.
40. Shelley, O., T. Murphy, J. A. Lederer, J. A. Mannick, and M. L. Rodrick. 2003. Mast cells and resistance to peritoneal sepsis after burn injury. Shock 19: 513-518.
41. Besmer, P., K. Manova, R. Duttlinger, E. J. Huang, A. Packer, C. Gyssler, and R. F. Bachvarova. 1993. The kit-ligand (steel factor) and its receptor c-kit/W: pleiotropic roles in gametogenesis and melanogenesis. Development (Suppl.): 125-137.
42. Murakami, M., T. Ohtake, R. A. Dorschner, B. Schittek, C. Garbe, and R. L. Gallo. 2002. Cathelicidin anti-microbial peptide expression in sweat, an innate defense system for the skin. J. Invest. Dermatol. 119: 1090-1095.
43. Porter, E. M., E. van Dam, E. V. Valore, and T. Ganz. 1997. Broad-spectrum antimicrobial activity of human intestinal defensin 5. Infect. Immun. 65: 2396-2401.
44. Yang, Y., S. Xiao, H. Ren, J. Wu, Z. Feng, and P. J. Hotez. 1999. Cutaneous and subcutaneous mast cell and eosinophil responses after challenge in mice vaccinated with living infective third-stage hookworm larvae. Chin. Med. J. 112: 1020-1023
45. Shin, M. H. 1997. Dermal mast cell responses in Paragonimus westermani-infected mice. Korean J. Parasitol. 35: 259-264.
46. Avila, G., L. Aguilar, S. Benitez, L. Yepez-Mulia, I. Lavenat, and A. Flisser. 2002. Inflammatory responses in the intestinal mucosa of gerbils and hamsters experimentally infected with the adult stage of Taenia solium. Int. J. Parasitol. 32: 1301-1308.
47. Sorensen, O. E., P. Follin, A. H. Johnsen, J. Calafat, G. S. Tjabringa, P. S. Hiemstra, and N. Borregaard. 2001. Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with protein-ase 3. Blood 97: 3951-3959
48. Davidson, D. J., A. J. Currie, G. S. Reid, D. M. Bowdish, K. L. MacDonald, R. C. Ma, R. E. Hancock, and D. P. Speert. 2004. The cationic antimicrobial peptide LL-37 modulates dendritic cell differentiation and dendritic cell-induced T cell polarization. J. Immunol. 172: 1146-1156.
49. Di Nardo, A., M. H. Braff, K. R. Taylor, C. Na, R. D. Granstein, J. E. McInturff, S. Krutzik, R. L. Modlin, and R. L. Gallo. 2007. Cathelicidin antimicrobial pep-tides block dendritic cell TLR4 activation and allergic contact sensitization. J. Immunol. 178: 1829-1834.
50. Grimbaldeston, M. A., S. Nakae, J. Kalesnikoff, M. Tsai, and S. J. Galli. 2007. Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat. Immunol. 8: 1095-1104.
51. 1 integrin. Blood 103: 2214-2220.
52. Gallo, R. L., and V. Nizet. 2003. Endogenous production of antimicrobial pep-tides in innate immunity and human disease. Curr. Allergy Asthma Rep. 3: 402-409.
53. De, Y., 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.
54. Kurosaka, K., Q. Chen, F. Yarovinsky, J. J. Oppenheim, and D. Yang. 2005. Mouse cathelin-related antimicrobial peptide chemoattracts leukocytes using formyl peptide receptor-like I/mouse formyl peptide receptor-like 2 as the receptor and acts as an immune adjuvant. J. Immunol. 174: 6257-6265.
55. Arock, M., E. Ross, R. Lai-Kuen, G. Averlant, Z. Gao, and S. N. Abraham. 1998. Phagocytic and tumor necrosis factor a response of human mast cells following exposure to Gram-negative and gram-positive bacteria. Infect. Immun. 66: 6030-6034.
56. von Kockritz-BIickwede, M., O. Goldmann, P. Thulin, K. Heinemann, A. Norrby-Teglund, M. Rohde, and E. Medina. 2008. Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111: 3070-3080.
57. Finkelman, F. D., T. Shea-Donohue, S. C. Morris, L. Gildea, R. Strait, K. B. Madden, L. Schopf, and J. F. Urban, Jr. 2004. Interleukin-4- and interleu-kin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 201: 139-155.
58. Lin, D. A., and J. A. Boyce. 2005. IL-4 regulates MEK expression required for lysophosphatidic acid-mediated chemokine generation by human mast cells. J. Immunol. 175: 5430-5438