Impact of LL-37 on anti-infective immunity

Journal of Leukocyte Biology

Volumn 77, Issue 4, 2005, Pages 451-459

  Bowdish, Dawn M E ^a   Davidson, Donald J ^a,d   Lau, Y Elaine ^a   Lee, Ken ^b   Scott, Monisha G ^b   Hancock, Robert E W ^a,c  

^a Centre for Microbial Diseases and Immunity Research   (Canada)

^b Inimex Pharmaceuticals Inc   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cathelicidin; Host defense peptide; Immunomodulator; Innate immunity

Indexed keywords

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; MITOGEN ACTIVATED PROTEIN KINASE; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; CELL DIFFERENTIATION; CELL INTERACTION; CELL SPECIFICITY; CELL TYPE; CONFERENCE PAPER; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG MECHANISM; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOMODULATION; MONOCYTE; PEPTIDE ANALYSIS; PLEIOTROPY; PRIORITY JOURNAL; SALMONELLA; STAPHYLOCOCCUS AUREUS; TH1 CELL; TISSUE CULTURE;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; GENE EXPRESSION REGULATION; HUMANS; INFECTION; MONOCYTES; NEUTROPHILS; SALMONELLA INFECTIONS, ANIMAL; STAPHYLOCOCCAL INFECTIONS;

ANIMALIA; SALMONELLA; STAPHYLOCOCCUS AUREUS;

EID: 16844381376     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0704380     Document Type: Conference Paper

References (66)

1. Tjabringa, G. S., Aarbiou, J., Ninaber, D. K., Drijfhout, J. W., Sorensen, 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.
2. Koczulla, R., von Degenfeld, G., Kupatt, C., Krotz, F., Zahler, S., Gloe, T., Issbrucker, K., Unterberger, P., Zaiou, M., Lebherz, C., Karl, A., Raake, P., Pfosser, A., Boekstegers, P., Welsch, U., Hiemstra, P. S., Vogelmeier, C., Gallo, R. L., Clauss, M., Bals, R. (2003) An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J. Clin. Invest. 111, 1665-1672.
3. Heilborn, J. D., Nilsson, M. F., Kratz, G., Weber, G., Sorensen, O., Borregaard, N., Stahle-Backdahl, M. (2003) The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J. Invest. Dermatol. 120, 379-389.
4. Scott, M. G., Davidson, D. J., Gold, M. R., Bowdish, D., Hancock, R. E. (2002) The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J. Immunol. 169, 3883-3891.
5. Bowdish, D. M. E., Davidson, D. J., Speert, D. P., Hancock, R. E. W. (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.
6. Bowdish, D. M. E., Davidson, D. J., Hancock, R. E. W. (2004) A re-evaluation of the role of host defense peptides in mammalian immunity. Comb. Chem. High Throughput Screen., In press.
7. Hase, K., Eckmann, L., Leopard, J. D., Varki, N., Kagnoff, M. F. (2002) Cell differentiation is a key determinant of cathelicidin LL-37/human cationic antimicrobial protein 18 expression by human colon epithelium. Infect. Immun. 70, 953-963.
8. Erdag, G., Morgan, J. R. (2002) Interleukin-1α and interleukin-6 enhance the antibacterial properties of cultured composite keratinocyte grafts. Ann. Surg. 235, 113-124.
9. Dorschner, R. A., Pestonjamasp, V. K., Tamakuwala, S., Ohtake, T., Rudisill, J., Nizet, V., Agerberth, B., Gudmundsson, G. H., Gallo, R. L. (2001) Cutaneous injury induces the release of cathelicidin anti-microbial peptides active against group A Streptococcus. J. Invest. Dermatol. 117, 91-97.
10. Sorensen, O., Arnljots, K., Cowland, J. B., Bainton, D. F., Borregaard, N. (1997) The human antibacterial cathelicidin, hCAP-18, is synthesized in myelocytes and metamyelocytes and localized to specific granules in neutrophils. Blood 90, 2796-2803.
11. Wilson, C. L., Ouellette, A. J., Satchell, D. P., Ayabe, T., Lopez-Boado, Y. S., Stratman, J. L., Hultgren, S. J., Matrisian, L. M., Parks, W. C. (1999) Regulation of intestinal α-defensin activation by the metalloproteinase matrilysin in innate host defense. Science 286, 113-117.
12. Nizet, V., Ohtake, T., Lauth, X., Trowbridge, J., Rudisill, J., Dorschner, R. A., Pestonjamasp, V., Piraino, J., Huttner, K., Gallo, R. L. (2001) Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414, 454-457.
13. Bals, R., Wang, X., Zasloff, M., Wilson, J. M. (1998) The peptide antibiotic LL-37/hCAP-18 is expressed in epithelia of the human lung where it has broad antimicrobial activity at the airway surface. Proc. Natl. Acad. Sci. USA 95, 9541-9546.
14. Turner, J., Cho, Y., Dinh, N. N., Waring, A. J., Lehrer, R. I. (1998) Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob. Agents Chemother. 42, 2206-2214.
15. Bals, R., Goldman, M. J., Wilson, J. M. (1998) Mouse β-clefensin 1 is a salt-sensitive antimicrobial peptide present in epithelia of the lung and urogenital tract. Infect. Immun. 66, 1225-1232.
16. Bals, R., Wang, X., Wu, Z., Freeman, T., Bafna, V., Zasloff, M., Wilson, J. M. (1998) Human β-defensin 2 is a salt-sensitive peptide antibiotic expressed in human lung. J. Clin. Invest. 102, 874-880.
17. Garcia, J. R., Krause, A., Schulz, S., Rodriguez-Jimenez, F. J., Kluver, E., Adermann, K., Forssmann, U., Frimpong-Boateng, A., Bals, R., Forssmann, W. G. (2001) Human β-defensin 4: a novel inclucible peptide with a specific salt-sensitive spectrum of antimicrobial activity. FASEB J. 15, 1819-1821.
18. Friedrich, C., Scott, M. G., Karunaratne, N., Yan, H., Hancock, R. E. (1999) Salt-resistant α-helical cationic antimicrobial peptides. Antimicrob. Agents Chemother. 43, 1542-1548.
19. Halmerbauer, G., Arri, S., Schierl, M., Strauch, E., Koller, D. Y. (2000) The relationship of eosinophil granule proteins to ions in the sputum of patients with cystic fibrosis. Clin. Exp. Allergy 30, 1771-1776.
20. Baconnais, S., Tirouvanziam, R., Zahm, J. M., de Bentzmann, S., Peault, B., Balossier, G., Puchelle, E. (1999) Ion composition and rheology of airway liquid from cystic fibrosis fetal tracheal xenografts. Am. J. Respir. Cell Mol. Biol. 20, 605-611.
21. Hoshino, K., Ogawa, K., Hishitani, T., Kitazawa, R. (2003) Influence of heart surgery on magnesium concentrations in pediatric patients. Pediatr. Int. 45, 39-44.
22. Salzman, N. H., Ghosh, D., Huttner, K. M., Paterson, Y., Bevins, C. L. (2003) Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature 422, 522-526.
23. Sawa, T., Kurahashi, K., Ohara, M., Gropper, M. A., Doshi, V., Larrick, J. W., Wiener-Kronish, J. P. (1998) Evaluation of antimicrobial and lipopolysaccharide-neutralizing effects of a synthetic CAP18 fragment against Pseudomonas aeruginosa in a mouse model. Antimicrob. Agents Chemother. 42, 3269-3275.
24. Tomita, T., Hitomi, S., Nagase, T., Matsui, H., Matsuse, T., Kimura, S., Ouchi, Y. (2000) Effect of ions on antibacterial activity of human β defensin 2. Microbiol. Immunol. 44, 749-754.
25. Scott, M. G., Gold, M. R., Hancock, R. E. (1999) Interaction of cationic peptides with lipoteichoic acid and gram-positive bacteria. Infect. Immun. 67, 6445-6453.
26. Niyonsaba, F., Iwabuchi, K., Someya, A., Hirata, M., Matsuda, H., Ogawa, H., Nagaoka, I. (2002) A cathelicidin family of human antibacterial peptide LL-37 induces mast cell chemotaxis. Immunology 106, 20-26.
27. De, Y., Chen, Q., Schmidt, A. P., Anderson, G. M., Wang, J. M., Wooters, J., Oppenheim, J. J., 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.
28. Niyonsaba, F., Someya, A., Hirata, M., Ogawa, H., Nagaoka, I. (2001) Evaluation of the effects of peptide antibiotics human β-defensins-1/-2 and LL-37 on histamine release and prostaglandin D(2) production from mast cells. Eur. J. Immunol. 31, 1066-1075.
29. Biragyn, A., Ruffini, P. A., Leifer, C. A., Klyushnenkova, E., Shakhov, A., Chertov, O., Shirakawa, A. K., Farber, J. M., Segal, D. M., Oppenheim, J. J., Kwak, L. W. (2002) Toll-like receptor 4-dependent activation of dendritic cells by β-defensin 2. Science 298, 1025-1029.
30. Sorensen, O., Cowland, J. B., Askaa, J., Borregaard, N. (1997) An ELISA for hCAP-18, the cathelicidin present in human neutrophils and plasma. J. Immunol. Methods 206, 53-59.
31. Agerberth, B., Gunne, H., Odeberg, J., Kogner, P., Boman, H. G., Gudmundsson, G. H. (1995) FALL-39, a putative human peptide antibiotic, is cysteine-free and expressed in bone marrow and testis. Proc. Natl. Acad. Sci. USA 92, 195-199.
32. Sorensen, O. E., Follin, P., Johnsen, A. H., Calafat, J., Tjabringa, G. S., Hiemstra, P. S., 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.
33. Putsep, K., Carlsson, G., Boman, H. G., Andersson, M. (2002) Deficiency of antibacterial peptides in patients with morbus Kostmann: an observation study. Lancet 360, 1144-1149.
34. Dale, B. A., Kimball, J. R., Krisanaprakornkit, S., Roberts, F., Robinovitch, M., O'Neal, R., Valore, E. V., Ganz, T., Anderson, G. M., Weinberg, A. (2001) Localized antimicrobial peptide expression in human gingiva. J. Periodontal Rex. 36, 285-294.
35. Hase, K., Murakami, M., Iimura, M., Cole, S. P., Horibe, Y., Ohtake, T., Obonyo, M., Gallo, R. L., Eckmann, L., Kagnoff, M. F. (2003) Expression of LL-37 by human gastric epithelial cells as a potential host defense mechanism against Helicobacter pylori. Gastroenterology 125, 1613-1625.
36. Frohm, M., Agerberth, B., Ahangari, G., Stahle-Backdahl, M., Liden, S., Wigzell, H., Gudmundsson, G. H. (1997) The expression of the gene coding for the antibacterial peptide LL-37 is induced in human keratinocytes during inflammatory disorders. J. Biol. Chem. 272, 15258-15263.
37. Agerberth, B., Grunewald, J., Castanos-Velez, E., Olsson, B., Jornvall, H., Wigzell, H., Eklund, A., Gudmundsson, G. H. (1999) Antibacterial components in bronchoalveolar lavage fluid from healthy individuals and sarcoidosis patients. Am. J. Respir. Crit. Care Med. 160, 283-290.
38. Elssner, A., Duncan, M., Gavrilin, M., Wewers, M. D. (2004) A novel P2X7 receptor activator, the human cathelicidin-derived peptide LL37, induces IL-1 β processing and release. J. Immunol. 172, 4987-4994.
39. Lau, Y. E., Scott, M. G., Goosney, G. L., Davidson, D. J., Hancock, R. E. (2005) Interaction and cellular localization of the human host defense peptide LL-37 with lung epithelial cells. Infect. Immun. 73, 583-591.
40. Witte, M. B., Barbul, A. (1997) General principles of wound healing. Surg. Clin. North Am. 77, 509-528.
41. Nagaoka, I., Hirota, S., Niyonsaba, F., Hirata, M., Adachi, Y., Tamura, H., Tanaka, S., Heumann, D. (2002) Augmentation of the lipopolysaccharide- neutralizing activities of human cathelicidin CAP18/LL-37-derived antimicrobial peptides by replacement with hydrophobic and cationic amino acid residues. Clin. Diagn. Lab. Immunol. 9, 972-982.
42. Scott, M. G., Vreugdenhil, A. C., Buurman, W. A., Hancock, R. E., Gold, M. R. (2000) Cutting edge: cationic antimicrobial peptides block the binding of lipopolysaccharide (LPS) to LPS binding protein. J. Immunol. 164, 549-553.
43. Liu, Y. J. (2001) Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 106, 259-262.
44. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y. J., Pulendran, B., Palucka, K. (2000) Immunobiology of dendritic cells. Annu. Rev. Immunol. 18, 767-811.
45. Lanzavecchia, A., Sallusto, F. (2001) Regulation of T cell immunity by dendritic cells. Cell 106, 263-266.
46. Davidson, D. J., Currie, A. J., Reid, G. S., Bowdish, D. M., Mac-Donald, K. L., Ma, R. C., Hancock, R. E., Speert, D. P. (2004) The cationic antimicrobial peptide LL-37 modulates dendritic cell differentiation and dendritic cell-induced T cell polarization. J. Immunol. 172, 1146-1156.
47. Schaller-Bals, S., Schulze, A., Bals, R. (2002) Increased levels of antimicrobial peptides in tracheal aspirates of newborn infants during infection. Am. J. Respir. Crit. Care Med. 165, 992-995.
48. Ong, P. Y., Ohtake, T., Brandt, C. Strickland, I., Boguniewicz, M., Ganz, T., Gallo, R. L., Leung, D. Y. (2002) Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N. Engl. J. Med. 347, 1151-1160.
49. Biragyn, A., Surenhu, M., Yang, D., Ruffini, P. A., Haines, B. A., Klyushnenkova, E., Oppenheim, J. J., Kwak, L. W. (2001) Mediators of innate immunity that target immature, but not mature, dendritic cells induce antitumor immunity when genetically fused with nonimmunogenic tumor antigens. J. Immunol. 167, 6644-6653.
50. Kalinski, P., Hilkens, C. M., Snijders, A., Snijdewint, F. G., Kapsenberg, M. L. (1997) IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells. J. Immunol. 159, 28-35.
51. Steinbrink, K., Wolfl, M., Jonuleit, H., Knop, J., Enk, A. H. (1997) Induction of tolerance by IL-10-treated dendritic cells. J. Immunol. 159, 4772-4780.
52. Widdicombe, J. H. (2002) Regulation of the depth and composition of airway surface liquid. J. Anal. 201, 313-318.
53. Singh, P. K., Tack, B. F., McCray Jr., P. B., Welsh, M. J. (2000) Synergistic and additive killing by antimicrobial factors found in human airway surface liquid. Am. J. Physiol. Lung Cell. Mol. Physiol. 279, L799-L805.
54. Barreda, D. R., Hanington, P. C., Belosevic, M. (2004) Regulation of myeloid development and function by colony stimulating factors. Dev. Comp. Immunol. 28, 509-554.
55. Xu, H., Okamoto, A., Ichikawa, J., Ando, T., Tasaka, K., Masuyama, K., Ogawa, H., Yagita, H., Okumura, K., Nakao, A. (2004) TWEAK/Fn14 interaction stimulates human bronchial epithelial cells to produce IL-8 and GM-CSF. Biochem. Biophys. Res. Commun. 318, 422-427.
56. Saba, S., Soong, G., Greenberg, S., Prince, A. (2002) Bacterial stimulation of epithelial G-CSF and GM-CSF expression promotes PMN survival in CF airways. Am. J. Respir. Cell Mol. Biol. 27, 561-567.
57. Nieda, M., Tomiyama, M., Egawa, K. (2003) Ex vivo enhancement of antigen-presenting function of dendritic cells and its application for DC-based immunotherapy. Hum. Cell 16, 199-204.
58. Campbell, J. R., Edwards, M. S. (2000) Cytokines enhance opsonophagocytosis of type III group B Streptococcus. J. Perinatol. 20, 225-230.
59. Ottonello, L., Epstein, A. L., Mancini, M., Tortolina, G., Dapino, P., Dallegri, F. (2001) Chimaeric Lym-1 monoclonal antibody-mediated cytolysis by neutrophils from G-CSF-treated patients: stimulation by GM-CSF and role of Fc γ-receptors. Br. J. Cancer 85, 463-469.
60. Dissemond, J., Weimann, T. K., Schneider, L. A., Schneeberger, A., Scharffetter-Kochanek, K., Goos, M., Wagner, S. N. (2003) Activated neutrophils exert antitumor activity against human melanoma cells: reactive oxygen species-induced mechanisms and their modulation by granulocyte-macrophage- colony-stimulating factor. J. Invest. Dermatol. 121, 936-938,
61. Li, H., Cheung, W., Choo, H. H. Chan, J. H., Lai, P. S. Fred Wong, W. S. (2003) IL-10 synergistically enhances GM-CSF-induced CCR1 expression in myelomonocytic cells. Biochem. Biophys. Res. Commun. 304, 417-424.
62. Kumagai, M., Imaizumi, T., Suzuki, K., Yoshida, H., Takanashi, S., Okumura, K., Sugawarai, K., Satoh, K. (2004) 15-Deoxy-δ(12,14)- prostaglandin J2 inhibits the IL-1β-induced expression of granulocyte-macrophage colony-stimulating factor in BEAS-2B bronchial epithelial cells. Tohoku J. Exp. Med. 202, 69-76.
63. Sha, Q., Truong-Tran, A. Q., Plitt, J. R., Beck, L. A., Schleimer, R. P. (2004) Activation of airway epithelial cells by Toll-like receptor agonists. Am. J. Respir. Cell Mol. Biol. 31, 358-364.
64. Chambers, C. A., Allison, J. P. (1999) Costimulatory regulation of T cell function. Curr. Opin. Cell Biol. 11, 203-210.
65. Kiefer, F., Vogel, W. F., Arnold, R. (2002) Signal transduclion and co-stimulatory pathways. Transpl. Immunol. 9, 69-82.
66. Ciornei, C. D., Egesten, A., Bodelsson, M. (2003) Effects of human cathelicidin antimicrobial peptide LL-37 on lipopolysaccharide-induced nitric oxide release from rat aorta in vitro. Acta Anaesthesiol. Scand. 47, 213-220.