Antimicrobial peptide LL-37 promotes bacterial phagocytosis by human macrophages

Journal of Leukocyte Biology

Volumn 95, Issue 6, 2014, Pages 971-981

  Wan, Min ^a   van der Does, Anne M ^a   Tang, Xiao ^a   Lindbom, Lennart ^a   Agerberth, Birgitta ^a   Haeggström, Jesper Z ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Cathelicidin; Fc R; Infection; Innate immunity; TLR

Indexed keywords

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CD11B ANTIGEN; CD14 ANTIGEN; FC RECEPTOR; GLYCOPROTEIN P 15095; IMMUNOGLOBULIN G; TOLL LIKE RECEPTOR 4;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CLEARANCE; CONTROLLED STUDY; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IMMUNOMODULATION; MACROPHAGE; MOUSE; NONHUMAN; OPSONIZATION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

CATHELICIDIN; FCΓR; INFECTION; INNATE IMMUNITY; TLR;

ANIMALS; ANTIGENS, CD14; ANTIMICROBIAL CATIONIC PEPTIDES; CELLS, CULTURED; ESCHERICHIA COLI; HUMANS; IMMUNOGLOBULIN G; MACROPHAGES; MICE; MICE, INBRED C57BL; PHAGOCYTOSIS; RECEPTORS, FORMYL PEPTIDE; RECEPTORS, IGG; TOLL-LIKE RECEPTOR 4;

EID: 84901709779     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0513304     Document Type: Article

References (46)

1. Indik, Z. K., Park, J. G., Hunter, S., Schreiber, A. D. (1995) The molecular dissection of Fc γ receptor mediated phagocytosis. Blood 86, 4389-4399.
2. Fridman, W. H. (1991) Fc receptors and immunoglobulin binding factors. FASEB J. 5, 2684-2690.
3. Peters, B. M., Shirtliff, M. E., Jabra-Rizk, M. A. (2010) Antimicrobial peptides: primeval molecules or future drugs? PLoS Pathog. 6, e1001067.
4. Frohm Nilsson, M., Sandstedt, B., Sorensen, O., Weber, G., Borregaard, N., Stahle-Backdahl, M. (1999) The human cationic antimicrobial protein (hCAP18), a peptide antibiotic, is widely expressed in human squamous epithelia and colocalizes with interleukin-6. Infect. Immun. 67, 2561-2566.
5. Lau, Y. E., Rozek, A., Scott, M. G., Goosney, D. 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.
6. 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.
7. Agerberth, B., Charo, J., Werr, J., Olsson, B., Idali, F., Lindbom, L., Kiessling, R., Jornvall, H., Wigzell, H., Gudmundsson, G. H. (2000) The human antimicrobial and chemotactic peptides LL-37 and α-defensins are expressed by specific lymphocyte and monocyte populations. Blood 96, 3086-3093.
8. 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.
9. Gudmundsson, G. H., Agerberth, B., Odeberg, J., Bergman, T., Olsson, B., Salcedo, R. (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.
10. 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.
11. 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.
12. Bowdish, D. M., Davidson, D. J., Speert, D. P., Hancock, R. E. (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.
13. 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.
14. Davidson, D. J., Currie, A. J., Reid, G. S., Bowdish, D. M., MacDonald, 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.
15. van der Does, A. M., Beekhuizen, H., Ravensbergen, B., Vos, T., Ottenhoff, T. H., van Dissel, J. T., Drijfhout, J. W., Hiemstra, P. S., Nibbering, P. H. (2010) LL-37 directs macrophage differentiation toward macrophages with a proinflammatory signature. J. Immunol. 185, 1442-1449.
16. Wan, M., Sabirsh, A., Wetterholm, A., Agerberth, B., Haeggstrom, J. Z. (2007) Leukotriene B4 triggers release of the cathelicidin LL-37 from human neutrophils: novel lipid-peptide interactions in innate immune responses. FASEB J. 21, 2897-2905.
17. Soehnlein, O., Kai-Larsen, Y., Frithiof, R., Sorensen, O. E., Kenne, E., Scharffetter-Kochanek, K., Eriksson, E. E., Herwald, H., Agerberth, B., Lindbom, L. (2008) Neutrophil primary granule proteins HBP and HNP1-3 boost bacterial phagocytosis by human and murine macrophages. J. Clin. Invest. 118, 3491-3502.
18. 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.
19. Werr, J., Johansson, J., Eriksson, E. E., Hedqvist, P., Ruoslahti, E., Lindbom, L. (2000) Integrin α(2)β(1) (VLA-2) is a principal receptor used by neutrophils for locomotion in extravascular tissue. Blood 95, 1804-1809.
20. Park, B. S., Song, D. H., Kim, H. M., Choi, B. S., Lee, H., Lee, J. O. (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458, 1191-1195.
21. 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.
22. Tokumaru, S., Sayama, K., Shirakata, Y., Komatsuzawa, H., Ouhara, K., Hanakawa, Y., Yahata, Y., Dai, X., Tohyama, M., Nagai, H., Yang, L., Higashiyama, S., Yoshimura, A., Sugai, M., Hashimoto, K. (2005) Induction of keratinocyte migration via transactivation of the epidermal growth factor receptor by the antimicrobial peptide LL-37. J. Immunol. 175, 4662-4668.
23. Huang, L. C., Reins, R. Y., Gallo, R. L., McDermott, A. M. (2007) Cathelicidin-deficient (Cnlp-/-) mice show increased susceptibility to Pseudomonas aeruginosa keratitis. Invest. Ophthalmol. Vis. Sci. 48, 4498-4508.
24. Doring, Y., Drechsler, M., Wantha, S., Kemmerich, K., Lievens, D., Vijayan, S., Gallo, R. L., Weber, C., Soehnlein, O. (2012) Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice. Circ. Res. 110, 1052-1056.
25. Overhage, J., Campisano, A., Bains, M., Torfs, E. C., Rehm, B. H., Hancock, R. E. (2008) Human host defense peptide LL-37 prevents bacterial biofilm formation. Infect. Immun. 76, 4176-4182.
26. Byfield, F. J., Wen, Q., Leszczynska, K., Kulakowska, A., Namiot, Z., Janmey, P. A., Bucki, R. (2011) Cathelicidin LL-37 peptide regulates endothelial cell stiffness and endothelial barrier permeability. Am. J. Physiol. Cell Physiol. 300, C105-C112.
27. 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.
28. Bowdish, D. M., Davidson, D. J., Lau, Y. E., Lee, K., Scott, M. G., Hancock, R. E. (2005) Impact of LL-37 on anti-infective immunity. J. Leukoc. Biol. 77, 451-459.
29. Chen, C. I., Schaller-Bals, S., Paul, K. P., Wahn, U., Bals, R. (2004) β-Defensins and LL-37 in bronchoalveolar lavage fluid of patients with cystic fibrosis. J. Cyst. Fibros. 3, 45-50.
30. Callaghan, M., McClean, S. (2012) Bacterial host interactions in cystic fibrosis. Curr. Opin. Microbiol. 15, 71-77.
31. Holness, C. L., Simmons, D. L. (1993) Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood 81, 1607-1613.
32. Ramprasad, M. P., Terpstra, V., Kondratenko, N., Quehenberger, O., Steinberg, D. (1996) Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotein. Proc. Natl. Acad. Sci. USA 93, 14833-14838.
33. Blander, J. M., Medzhitov, R. (2004) Regulation of phagosome maturation by signals from Toll-like receptors. Science 304, 1014-1018.
34. Doyle, S. E., O'Connell, R. M., Miranda, G. A., Vaidya, S. A., Chow, E. K., Liu, P. T., Suzuki, S., Suzuki, N., Modlin, R. L., Yeh, W. C., Lane, T. F., Cheng, G. (2004) Toll-like receptors induce a phagocytic gene program through p38. J. Exp. Med. 199, 81-90.
35. Sanjuan, M. A., Dillon, C. P., Tait, S. W., Moshiach, S., Dorsey, F., Connell, S., Komatsu, M., Tanaka, K., Cleveland, J. L., Withoff, S., Green, D. R. (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450, 1253-1257.
36. Yoshioka, M., Fukuishi, N., Kubo, Y., Yamanobe, H., Ohsaki, K., Kawasoe, Y., Murata, M., Ishizumi, A., Nishii, Y., Matsui, N., Akagi, M. (2008) Human cathelicidin CAP18/LL-37 changes mast cell function toward innate immunity. Biol. Pharm. Bull. 31, 212-216.
37. van der Does, A. M., Bogaards, S. J., Ravensbergen, B., Beekhuizen, H., van Dissel, J. T., Nibbering, P. H. (2010) Antimicrobial peptide hLF1-11 directs granulocyte-macrophage colony-stimulating factor-driven monocyte differentiation toward macrophages with enhanced recognition and clearance of pathogens. Antimicrob. Agents Chemother. 54, 811-816.
38. Di Nardo, A., Braff, M. H., Taylor, K. R., Na, C., Granstein, R. D., McInturff, J. E., Krutzik, S., Modlin, R. L., Gallo, R. L. (2007) Cathelicidin antimicrobial peptides block dendritic cell TLR4 activation and allergic contact sensitization. J. Immunol. 178, 1829-1834.
39. 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.
40. Mookherjee, N., Brown, K. L., Bowdish, D. M., Doria, S., Falsafi, R., Hokamp, K., Roche, F. M., Mu, R., Doho, G. H., Pistolic, J., Powers, J. P., Bryan, J., Brinkman, F. S., Hancock, R. E. (2006) Modulation of the TLR-mediated inflammatory response by the endogenous human host defense peptide LL-37. J. Immunol. 176, 2455-2464.
41. Mookherjee, N., Wilson, H. L., Doria, S., Popowych, Y., Falsafi, R., Yu, J. J., Li, Y., Veatch, S., Roche, F. M., Brown, K. L., Brinkman, F. S., Hokamp, K., Potter, A., Babiuk, L. A., Griebel, P. J., Hancock, R. E. (2006) Bovine and human cathelicidin cationic host defense peptides similarly suppress transcriptional responses to bacterial lipopolysaccharide. J. Leukoc. Biol. 80, 1563-1574.
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. Ye, R. D., Boulay, F., Wang, J. M., Dahlgren, C., Gerard, C., Parmentier, M., Serhan, C. N., Murphy, P. M. (2009) International Union of Basic and Clinical Pharmacology. LXXIII. Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol. Rev. 61, 119-161.
44. Spurr, L., Nadkarni, S., Pederzoli-Ribeil, M., Goulding, N. J., Perretti, M., D'Acquisto, F. (2011) Comparative analysis of Annexin A1-formyl peptide receptor 2/ALX expression in human leukocyte subsets. Int. Immunopharm. 11, 55-66.
45. Yang, D., Chen, Q., Le, Y., Wang, J. M., Oppenheim, J. J. (2001) Differential regulation of formyl peptide receptor-like 1 expression during the differentiation of monocytes to dendritic cells and macrophages. J. Immunol. 166, 4092-4098.
46. Maderna, P., Cottell, D. C., Toivonen, T., Dufton, N., Dalli, J., Perretti, M., Godson, C. (2010) FPR2/ALX receptor expression and internalization are critical for lipoxin A4 and annexin-derived peptide-stimulated phagocytosis. FASEB J. 24, 4240-4249.