The role of salivary histatin and the human cathelicidin LL-37 in wound healing and innate immunity

Biological Chemistry

Volumn 391, Issue 5, 2010, Pages 541-548

  Oudhoff, Menno J ^a   Blaauboer, Marjolein E ^a,b   Nazmi, Kamran ^a   Scheres, Nina ^a   Bolscher, Jan G M ^a   Veerman, Enno C I ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b TNO   (Netherlands)

Author keywords

Antimicrobial peptides; Candida albicans; Cell migration; Fibrosis; Gingival fibroblasts; Saliva

Indexed keywords

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CHEMOKINE; CYTOKINE; HISTATIN; HISTATIN 2; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; UNCLASSIFIED DRUG;

ANTIFUNGAL ACTIVITY; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DOSE RESPONSE; FIBROBLAST; FIBROSIS; GINGIVA; HUMAN; HUMAN CELL; IMMUNOMODULATION; INNATE IMMUNITY; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALIVA LEVEL; WOUND HEALING;

AMINO ACID SEQUENCE; ANTIFUNGAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; CANDIDA ALBICANS; CATHELICIDINS; CELL DEATH; CELL DIFFERENTIATION; CELL MOVEMENT; FIBROBLASTS; FIBROSIS; GINGIVA; HISTATINS; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-8; LIPOPOLYSACCHARIDES; MOLECULAR SEQUENCE DATA; WOUND HEALING;

CANDIDA ALBICANS;

EID: 77952791627     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2010.057     Document Type: Article

References (45)

1. Aarbiou, J., Tjabringa, G.S., Verhoosel, R.M., Ninaber, D.K., White, S.R., Peltenburg, L.T., Rabe, K.F., and Hiemstra, P.S. (2006). Mechanisms of cell death induced by the neutrophil antimicrobial peptides a-defensins and LL-37. Inflamm. Res. 55, 119-127.
2. Barlow, P.G., Li, Y., Wilkinson, T.S., Bowdish, D.M., Lau, Y.E., Cosseau, C., Haslett, C., Simpson, A.J., Hancock, R.E., and Davidson, D.J. (2006). The human cationic host defense peptide LL-37 mediates contrasting effects on apoptotic pathways in different primary cells of the innate immune system. J. Leukoc. Biol. 80, 509-520.
3. Bringardner, B.D., Baran, C.P., Eubank, T.D., and Marsh, C.B. (2008). The role of inflammation in the pathogenesis of idiopathic pulmonary fibrosis. Antioxid. Redox Signal. 10, 287-301.
4. Carretero, M., Escamez, M.J., Garcia, M., Duarte, B., Holguin, A., Retamosa, L., Jorcano, J.L., Rio, M.D., and Larcher, F. (2008). In vitro and in vivo wound healing-promoting activities of human cathelicidin LL-37. J. Invest. Dermatol. 128, 223-236.
5. Chamorro, C.I., Weber, G., Gronberg, A., Pivarcsi, A., and Stahle, M. (2009). The human antimicrobial peptide LL-37 suppresses apoptosis in keratinocytes. J. Invest. Dermatol. 129, 937-944.
6. Chen, Q., Wade, D., Kurosaka, K., Wang, Z.Y., Oppenheim, J.J., and Yang, D. (2004). Temporin A and related frog antimicrobial peptides use formyl peptide receptor-like 1 as a receptor to chemoattract phagocytes. J. Immunol. 173, 2652-2659.
7. De, Y., Chen, G., 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.
8. de Vries, T.J., Schoenmaker, T., Wattanaroonwong, N., van den Hoonaard, M., Nieuwenhuijse, A., Beertsen, W., and Everts, V. (2006). Gingival fibroblasts are better at inhibiting osteoclast formation than periodontal ligament fibroblasts. J. Cell. Biochem. 98, 370-382.
9. Elssner, A., Duncan, M., Gavrilin, M., and Wewers, M.D. (2004). A novel P2X7 receptor activator, the human cathelicidin-derived peptide LL37, induces IL-1b processing and release. J. Immunol. 172, 4987-4994.
10. Gautier, R., Douguet, D., Antonny, B., and Drin, G. (2008). HELIQUEST: a web server to screen sequences with specific a-helical properties. Bioinformatics 24, 2101-2102.
11. Helmerhorst, E.J., Van't Hof, W., Veerman, E.C., Simoons-Smit, I., and Nieuw Amerongen, A.V. (1997). Synthetic histatin analogues with broad-spectrum antimicrobial activity. Biochem. J. 326, 39-45.
12. Imamura, Y., Fujigaki, Y., Oomori, Y., Usui, S., and Wang, P.L. (2009). Cooperation of salivary protein histatin 3 with heat shock cognate protein 70 relative to the G1/S transition in human gingival fibroblasts. J. Biol. Chem. 284, 14316-14325.
13. Koczulla, R., von Degenfeld, G., Kupatt, C., Krotz, F., Zahler, S., Gloe, T., Issbrucker, K., Unterberger, P., Zaiou, M., Lebherz, C., et al. (2003). An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J. Clin. Invest. 111, 1665-1672.
14. Kuijpers, T.W., van Bruggen, R., Kamerbeek, N., Tool, A.T., Hicsonmez, G., Gurgey, A., Karow, A., Verhoeven, A.J., Seeger, K., Sanal, O., et al. (2007). Natural history and early diagnosis of LAD-1/variant syndrome. Blood 109, 3529-3537.
15. Lai, Y. and Gallo, R.L. (2009). AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol. 30, 131-141.
16. Mochon, A.B. and Liu, H. (2008). The antimicrobial peptide histatin-5 causes a spatially restricted disruption on the Candida albicans surface, allowing rapid entry of the peptide into the cytoplasm. PLoS Pathog. 4, e1000190.
17. Molhoek, E.M., den Hertog, A.L., de Vries, A.M., Nazmi, K., Veerman, E.C., Hartgers, F.C., Yazdanbakhsh, M., Bikker, F.J., and van der Kleij, D. (2009). Structure-function relationship of the human antimicrobial peptide LL-37 and LL-37 fragments in the modulation of TLR responses. Biol. Chem. 390, 295-303.
18. Mookherjee, N., Brown, K.L., Bowdish, D.M., Doria, S., Falsafi, R., Hokamp, K., Roche, F.M., Mu, R., Doho, G.H., Pistolic, J., et al. (2006). Modulation of the TLR-mediated inflammatory response by the endogenous human host defense peptide LL-37. J. Immunol. 176, 2455-2464.
19. Mookherjee, N., Lippert, D.N., Hamill, P., Falsafi, R., Nijnik, A., Kindrachuk, J., Pistolic, J., Gardy, J., Miri, P., Naseer, M., et al. (2009). Intracellular receptor for human host defense peptide LL-37 in monocytes. J. Immunol. 183, 2688-2696.
20. Niyonsaba, F., Ushio, H., Nagaoka, I., Okumura, K., and Ogawa, H. (2005). The human b-defensins (-1, -2, -3, -4) and cathelicidin LL-37 induce IL-18 secretion through p38 and ERK MAPK activation in primary human keratinocytes. J. Immunol. 175, 1776-1784.
21. Niyonsaba, F., Ushio, H., Nakano, N., Ng, W., Sayama, K., Hashimoto, K., Nagaoka, I., Okumura, K., and Ogawa, H. (2007). Antimicrobial peptides human beta-defensins stimulate epidermal keratinocyte migration, proliferation and production of proinflammatory cytokines and chemokines. J. Invest. Dermatol. 127, 594-604.
22. Nunes, I., Shapiro, R.L., and Rifkin, D.B. (1995). Characterization of latent TGF-b activation by murine peritoneal macrophages. J. Immunol. 155, 1450-1459.
23. Oppenheim, J.J. and Yang, D. (2005). Alarmins: chemotactic activators of immune responses. Curr. Opin. Immunol. 17, 359-365.
24. Oudhoff, M.J., Bolscher, J.G., Nazmi, K., Kalay, H., van't Hof, W., Amerongen, A.V., and Veerman, E.C. (2008). Histatins are the major wound-closure stimulating factors in human saliva as identified in a cell culture assay. FASEB J. 22, 3805-3812.
25. Oudhoff, M.J., Kroeze, K.L., Nazmi, K., van den Keijbus, P.A., van't Hof, W., Fernandez-Borja, M., Hordijk, P.L., Gibbs, S., Bolscher, J.G., and Veerman, E.C. (2009a). Structure-activity analysis of histatin, a potent wound healing peptide from human saliva: cyclization of histatin potentiates molar activity 1000-fold. FASEB J. 23, 3928-3935.
26. Oudhoff, M.J., van den Keijbus, P.A., Kroeze, K.L., Nazmi, K., Gibbs, S., Bolscher, J.G., and Veerman, E.C. (2009b). Histatins enhance wound closure with oral and non-oral cells. J. Dent. Res. 88, 846-850.
27. Park, H.J., Cho, D.H., Kim, H.J., Lee, J.Y., Cho, B.K., Bang, S.I., Song, S.Y., Yamasaki, K., Di Nardo, A., and Gallo, R.L. (2009). Collagen synthesis is suppressed in dermal fibroblasts by the human antimicrobial peptide LL-37. J. Invest. Dermatol. 129, 843-850.
28. Rappolee, D.A. and Werb, Z. (1992). Macrophage-derived growth factors. Curr. Top. Microbiol. Immunol. 181, 87-140.
29. Scheres, N., Laine, M.L., de Vries, T.J., Everts, V., and van Winkelhoff, A.J. (2009). Gingival and periodontal ligament fibroblasts differ in their inflammatory response to viable Porphyromonas gingivalis. J. Periodontal Res., Epub ahead of print; DOI: 10.1111/j.1600-0765.2009.01229.x.
30. Schiemann, F., Brandt, E., Gross, R., Lindner, B., Mittelstadt, J., Sommerhoff, C.P., Schulmistrat, J., and Petersen, F. (2009). The cathelicidin LL-37 activates human mast cells and is degraded by mast cell tryptase: counter-regulation by CXCL4. J. Immunol. 183, 2223-2231.
31. Scott, M.G., Davidson, D.J., Gold, M.R., Bowdish, D., and Hancock, R.E. (2002). The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J. Immunol. 169, 3883-3891.
32. Tjabringa, G.S., Aarbiou, J., Ninaber, D.K., Drijfhout, J.W., Sorensen, O.E., Borregaard, N., Rabe, K.F., and 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.
33. Tjabringa, G.S., Ninaber, D.K., Drijfhout, J.W., Rabe, K.F., and Hiemstra, P.S. (2006). Human cathelicidin LL-37 is a chemoattractant for eosinophils and neutrophils that acts via formyl-peptide receptors. Int. Arch. Allergy Immunol. 140, 103-112.
34. Tokumaru, S., Sayama, K., Shirakata, Y., Komatsuzawa, H., Ouhara, K., Hanakawa, Y., Yahata, Y., Dai, X., Tohyama, M., Nagai, H., et al. (2005). Induction of keratinocyte migration via transactivation of the epidermal growth factor receptor by the antimicrobial peptide LL-37. J. Immunol. 175, 4662-4668.
35. Tomasek, J.J., Gabbiani, G., Hinz, B., Chaponnier, C., and Brown, R.A. (2002). Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3, 349-363.
36. Tomasinsig, L., Pizzirani, C., Skerlavaj, B., Pellegatti, P., Gulinelli, S., Tossi, A., Di Virgilio, F., and Zanetti, M. (2008). The human cathelicidin LL-37 modulates the activities of the P2X7 receptor in a structure-dependent manner. J. Biol. Chem. 283, 30471-30481.
37. Turner, J., Cho, Y., Dinh, N.N., Waring, A.J., and Lehrer, R.I. (1998). Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob. Agents Chemother. 42, 2206-2214.
38. van Wetering, S., Tjabringa, G.S., and Hiemstra, P.S. (2005). Interactions between neutrophil-derived antimicrobial peptides and airway epithelial cells. J. Leukoc. Biol. 77, 444-450.
39. Veerman, E.C., Valentijn-Benz, M., Nazmi, K., Ruissen, A.L., Walgreen-Weterings, E., van Marle, J., Doust, A.B., van't Hof, W., Bolscher, J.G., and Nieuw Amerongen, A.V. (2007). Energy depletion protects Candida albicans against antimicrobial peptides by rigidifying its cell membrane. J. Biol. Chem. 282, 18831-18841.
40. von Haussen, J., Koczulla, R., Shaykhiev, R., Herr, C., Pinkenburg, O., Reimer, D., Wiewrodt, R., Biesterfeld, S., Aigner, A., Czubayko, F., and Bals, R. (2008). The host defence peptide LL-37/ hCAP-18 is a growth factor for lung cancer cells. Lung Cancer 59, 12-23.
41. Xu, T., Telser, E., Troxler, R.F., and Oppenheim, F.G. (1990). Primary structure and anticandidal activity of the major histatin from parotid secretion of the subhuman primate, Macaca fascicularis. J. Dent. Res. 69, 1717-1723.
42. Yang, D., de la Rosa, G., Tewary, P., and Oppenheim, J.J. (2009). Alarmins link neutrophils and dendritic cells. Trends Immunol. 30, 531-537.
43. Zasloff, M. 2002. Antimicrobial peptides of multicellular organisms. Nature 415, 389-395.
44. 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.
45. 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.