β-defensin 1 plays a role in acute mucosal defense against Candida albicans

Journal of Immunology

Volumn 194, Issue 4, 2015, Pages 1788-1795

  Tomalka, Jeffrey ^a   Azodi, Elaheh ^a,b   Narra, Hema P ^a   Patel, Krupen ^a   O'Neill, Samantha ^a   Cardwell, Cisley ^a   Hall, Brian A ^a   Wilson, James M ^c   Hise, Amy G ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA DEFENSIN; BETA DEFENSIN 1; BETA DEFENSIN 2; BETA DEFENSIN 3; BETA DEFENSIN 4; CYTOKINE; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; POLYPEPTIDE ANTIBIOTIC AGENT; DEFB1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; CYTOKINE PRODUCTION; FUNGUS IDENTIFICATION; HOST RESISTANCE; IMMUNE RESPONSE; INFLAMMATORY CELL; INNATE IMMUNITY; MOLECULAR DYNAMICS; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; THRUSH; ANIMAL; C57BL MOUSE; IMMUNOLOGY; KNOCKOUT MOUSE; MUCOSAL IMMUNITY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; BETA-DEFENSINS; CANDIDA ALBICANS; CANDIDIASIS, ORAL; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84922572847     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203239     Document Type: Article

References (52)

1. Wisplinghoff, H., T. Bischoff, S. M. Tallent, H. Seifert, R. P. Wenzel, and M. B. Edmond. 2004. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39: 309-317.
2. Fraser, V. J., M. Jones, J. Dunkel, S. Storfer, G. Medoff, and W. C. Dunagan. 1992. Candidemia in a tertiary care hospital: epidemiology, risk factors, and predictors of mortality. Clin. Infect. Dis. 15: 414-421.
3. Brogden, K. A. 2005. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3: 238-250.
4. Schroeder, B. O., Z. Wu, S. Nuding, S. Groscurth, M. Marcinowski, J. Beisner, J. Buchner, M. Schaller, E. F. Stange, and J. Wehkamp. 2011. Reduction of disulphide bonds unmasks potent antimicrobial activity of human β-defensin 1. Nature 469: 419-423.
5. Wang, Y., Y. Jiang, T. Gong, X. Cui, W. Li, Y. Feng, B. Wang, Z. Jiang, and M. Li. 2010. High-level expression and novel antifungal activity of mouse beta defensin-1 mature peptide in Escherichia coli. Appl. Biochem. Biotechnol. 160: 213-221.
6. Hassan, S. A. 2005. Amino acid side chain interactions in the presence of salts. J. Phys. Chem. B 109: 21989-21996.
7. Vylkova, S., X. S. Li, J. C. Berner, and M. Edgerton. 2006. Distinct antifungal mechanisms: beta-defensins require Candida albicans Ssa1 protein, while Trk1p mediates activity of cysteine-free cationic peptides. Antimicrob. Agents Che-mother. 50: 324-331.
8. Vylkova, S., N. Nayyar, W. Li, and M. Edgerton. 2007. Human beta-defensins kill Candida albicans in an energy-dependent and salt-sensitive manner without causing membrane disruption. Antimicrob. Agents Chemother. 51: 154-161.
9. Scudiero, O., S. Galdiero, M. Cantisani, R. Di Noto, M. Vitiello, M. Galdiero, G. Naclerio, J. J. Cassiman, C. Pedone, G. Castaldo, and F. Salvatore. 2010. Novel synthetic, salt-resistant analogs of human beta-defensins 1 and 3 endowed with enhanced antimicrobial activity. Antimicrob. Agents Chemother. 54: 2312-2322.
10. Lee, J. K., Y. J. Park, K. Y. Kum, S. H. Han, S. W. Chang, B. Kaufman, J. Jiang, Q. Zhu, K. Safavi, and L. Spangberg. 2013. Antimicrobial efficacy of a human β-defensin-3 peptide using an Enterococcus faecalis dentine infection model. Int. Endod. J. 46: 406-412.
11. Argimón, S., S. Fanning, J. R. Blankenship, and A. P. Mitchell. 2011. Interaction between the Candida albicans high-osmolarity glycerol (HOG) pathway and the response to human beta-defensins 2 and 3. Eukaryot. Cell 10: 272-275.
12. Bals, R., M. J. Goldman, and J. M. Wilson. 1998. Mouse beta-defensin 1 is a salt-sensitive antimicrobial peptide present in epithelia of the lung and urogenital tract. Infect. Immun. 66: 1225-1232.
13. Hinrichsen, K., R. Podschun, S. Schubert, J. M. Schröder, J. Harder, and E. Proksch. 2008. Mouse beta-defensin-14, an antimicrobial ortholog of human beta-defensin-3. Antimicrob. Agents Chemother. 52: 1876-1879.
14. Röhrl, J., D. Yang, J. J. Oppenheim, and T. Hehlgans. 2008. Identification and biological characterization of mouse beta-defensin 14, the orthologue of human beta-defensin 3. J. Biol. Chem. 283: 5414-5419.
15. Jia, H. P., S. A. Wowk, B. C. Schutte, S. K. Lee, A. Vivado, B. F. Tack, C. L. Bevins, and P. B. McCray, Jr. 2000. A novel murine beta - defensin expressed in tongue, esophagus, and trachea. J. Biol. Chem. 275: 33314-33320.
16. Moser, C., D. J. Weiner, E. Lysenko, R. Bals, J. N. Weiser, and J. M. Wilson. 2002. beta-Defensin 1 contributes to pulmonary innate immunity in mice. Infect. Immun. 70: 3068-3072.
17. Tanida, T., T. Okamoto, A. Okamoto, H. Wang, T. Hamada, E. Ueta, and T. Osaki. 2003. Decreased excretion of antimicrobial proteins and peptides in saliva of patients with oral candidiasis. J. Oral Pathol. Med. 32: 586-594.
18. Ryan, L. K., K. B. Freeman, J. A. Masso-Silva, K. Falkovsky, A. Aloyouny, K. Markowitz, A. G. Hise, M. Fatahzadeh, R. W. Scott, and G. Diamond. 2014. Activity of potent and selective host defense peptide mimetics in mouse models of oral candidiasis. Antimicrob. Agents Chemother. 58: 3820-3827.
19. Jiang, Y., X. Yi, M. Li, T. Wang, T. Qi, and X. She. 2012. Antimicrobial activities of recombinant mouse β-defensin 3 and its synergy with antibiotics. J. Mater. Sci. Mater. Med. 23: 1723-1728.
20. Krishnakumari, V., N. Rangaraj, and R. Nagaraj. 2009. Antifungal activities of human beta-defensins HBD-1 to HBD-3 and their C-terminal analogs Phd1 to Phd3. Antimicrob. Agents Chemother. 53: 256-260.
21. Hise, A. G., J. Tomalka, S. Ganesan, K. Patel, B. A. Hall, G. D. Brown, and K. A. Fitzgerald. 2009. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 5: 487-497.
22. Dwivedi, P., A. Thompson, Z. Xie, H. Kashleva, S. Ganguly, A. P. Mitchell, and A. Dongari-Bagtzoglou. 2011. Role of Bcr1-activated genes Hwp1 and Hyr1 in Candida albicans oral mucosal biofilms and neutrophil evasion. PLoS ONE 6: e16218.
23. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
24. Howell, M. D., J. F. Jones, K. O. Kisich, J. E. Streib, R. L. Gallo, and D. Y. Leung. 2004. Selective killing of vaccinia virus by LL-37: implications for eczema vaccinatum. J. Immunol. 172: 1763-1767.
25. López-García, B., P. H. Lee, K. Yamasaki, and R. L. Gallo. 2005. Anti-fungal activity of cathelicidins and their potential role in Candida albicans skin infection. J. Invest. Dermatol. 125: 108-115.
26. Bals, R., X. Wang, M. Zasloff, and J. M. Wilson. 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.
27. Tomalka, J., S. Ganesan, E. Azodi, K. Patel, P. Majmudar, B. A. Hall, K. A. Fitzgerald, and A. G. Hise. 2011. A novel role for the NLRC4 inflam-masome in mucosal defenses against the fungal pathogen Candida albicans. PLoS Pathog. 7: e1002379.
28. Conti, H. R., F. Shen, N. Nayyar, E. Stocum, J. N. Sun, M. J. Lindemann, A. W. Ho, J. H. Hai, J. J. Yu, J. W. Jung, et al. 2009. Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J. Exp. Med. 206: 299-311.
29. Huang, W., L. Na, P. L. Fidel, and P. Schwarzenberger. 2004. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 190: 624-631.
30. van de Veerdonk, F. L., R. J. Marijnissen, B. J. Kullberg, H. J. Koenen, S. C. Cheng, I. Joosten, W. B. van den Berg, D. L. Williams, J. W. van der Meer, L. A. Joosten, and M. G. Netea. 2009. The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell Host Microbe 5: 329-340.
31. Zelante, T., A. De Luca, P. Bonifazi, C. Montagnoli, S. Bozza, S. Moretti, M. L. Belladonna, C. Vacca, C. Conte, P. Mosci, et al. 2007. IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur. J. Immunol. 37: 2695-2706.
32. Gross, O., H. Poeck, M. Bscheider, C. Dostert, N. Hannesschläger, S. Endres, G. Hartmann, A. Tardivel, E. Schweighoffer, V. Tybulewicz, et al. 2009. Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 459: 433-436.
33. Joly, S., N. Ma, J. J. Sadler, D. R. Soll, S. L. Cassel, and F. S. Sutterwala. 2009. Cutting edge: Candida albicans hyphae formation triggers activation of the Nlrp3 inflammasome. J. Immunol. 183: 3578-3581.
34. Kumar, H., Y. Kumagai, T. Tsuchida, P. A. Koenig, T. Satoh, Z. Guo, M. H. Jang, T. Saitoh, S. Akira, and T. Kawai. 2009. Involvement of the NLRP3 inflammasome in innate and humoral adaptive immune responses to fungal beta-glu-can. J. Immunol. 183: 8061-8067.
35. Ameen, M. 2010. Epidemiology of superficial fungal infections. Clin. Dermatol. 28: 197-201.
36. Azie, N., D. Neofytos, M. Pfaller, H. U. Meier-Kriesche, S. P. Quan, and D. Horn. 2012. The PATH (Prospective Antifungal Therapy) Alliance® registry and invasive fungal infections: update 2012. Diagn. Microbiol. Infect. Dis. 73: 293-300.
37. Pfaller, M., D. Neofytos, D. Diekema, N. Azie, H. U. Meier-Kriesche, S. P. Quan, and D. Horn. 2012. Epidemiology and outcomes of candidemia in 3648 patients: data from the Prospective Antifungal Therapy (PATH Alliance®) registry, 2004-2008. Diagn. Microbiol. Infect. Dis. 74: 323-331.
38. Pfaller, M. A. 2012. Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am. J. Med. 125(1, Suppl)S3-S13.
39. Schofield, D. A., C. Westwater, and E. Balish. 2004. beta-Defensin expression in immunocompetent and immunodeficient germ-free and Candida albicans-monoassociated mice. J. Infect. Dis. 190: 1327-1334.
40. Schofield, D. A., C. Westwater, and E. Balish. 2005. Divergent chemokine, cytokine and beta-defensin responses to gastric candidiasis in immunocompetent C57BL/6 and BALB/c mice. J. Med. Microbiol. 54: 87-92.
41. Deng, L. X., G. X. Wu, Y. Cao, B. Fan, X. Gao, X. H. Tang, and N. Huang. 2012. The chromosomal protein HMGN2 mediates the LPS-induced expression of β-defensins in mice. Inflammation 35: 456-473.
42. Yuan, X., X. Hua, and K. R. Wilhelmus. 2010. The corneal expression of antimicrobial peptides during experimental fungal keratitis. Curr. Eye Res. 35: 872-879.
43. Chang, H. T, P. W. Tsai, H. H. Huang, Y S. Liu, T. S. Chien, and C. Y. Lan. 2012. LL37 and hBD-3 elevate the β-1, 3-exoglucanase activity of Candida albicans Xog1p, resulting in reduced fungal adhesion to plastic. Biochem. J. 441: 963-970.
44. Niyonsaba, F., H. Ushio, M. Hara, H. Yokoi, M. Tominaga, K. Takamori, N. Kajiwara, H. Saito, I. Nagaoka, H. Ogawa, and K. Okumura. 2010. Antimicrobial peptides human beta-defensins and cathelicidin LL-37 induce the secretion of a pruritogenic cytokine IL-31 by human mast cells. J. Immunol. 184: 3526-3534.
45. Niyonsaba, F., H. Ushio, I. Nagaoka, K. Okumura, and H. Ogawa. 2005. The human beta-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.
46. Niyonsaba, F, H. Ushio, N. Nakano, W. Ng, K. Sayama, K. Hashimoto, I. Nagaoka, K. Okumura, and H. Ogawa. 2007. Antimicrobial peptides human beta-defensins stimulate epidermal keratinocyte migration, proliferation and production of proinflammatory cytokines and chemokines. J. Invest. Dermatol. 127: 594-604.
47. Conti, H. R., O. Baker, A. F. Freeman, W. S. Jang, S. M. Holland, R. A. Li, M. Edgerton, and S. L. Gaffen. 2011. New mechanism of oral immunity to mucosal candidiasis in hyper-IgE syndrome. Mucosal Immunol. 4: 448-455.
48. Kobayashi, Y 2008. The role of chemokines in neutrophil biology. Front. Biosci. 13: 2400-2407.
49. Martinon, F, K. Burns, and J. Tschopp. 2002. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell 10: 417-426.
50. Hoover, D. M., C. Boulegue, D. Yang, J. J. Oppenheim, K. Tucker, W. Lu, and J. Lubkowski. 2002. The structure of human macrophage inflammatory protein-3alpha /CCL20. Linking antimicrobial and CC chemokine receptor-6-binding activities with human beta-defensins. J. Biol. Chem. 277: 37647-37654.
51. Yang, D., Q. Chen, D. M. Hoover, P. Staley, K. D. Tucker, J. Lubkowski, and J. J. Oppenheim. 2003. Many chemokines including CCL20/MIP-3alpha display antimicrobial activity. J. Leukoc. Biol. 74: 448-455.
52. Cole, A. M., and T Ganz. 2001. Human antimicrobial peptides: analysis and application. Nat. Med. 7: 158-159.