IL-17 Receptor Signaling in Oral Epithelial Cells Is Critical for Protection against Oropharyngeal Candidiasis

Cell Host and Microbe

Volumn 20, Issue 5, 2016, Pages 606-617

  Conti, Heather R ^a,b   Bruno, Vincent M ^c   Childs, Erin E ^a   Daugherty, Sean ^c   Hunter, Joseph P ^b   Mengesha, Bemnet G ^b   Saevig, Danielle L ^b   Hendricks, Matthew R ^a   Coleman, Bianca M ^a   Brane, Lucas ^a   Solis, Norma ^d   Cruz, J Agustin ^a   Verma, Akash H ^a   Garg, Abhishek V ^a   Hise, Amy G ^e,f   Richardson, Jonathan P ^g   Naglik, Julian R ^g   Filler, Scott G ^d   Kolls, Jay K ^h   Sinha, Satrajit ⁱ   Gaffen, Sarah L ^a,g   more..

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TOLEDO   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d HARBOR UCLA MEDICAL CENTER   (United States)

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

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

^g KING'S COLLEGE LONDON   (United Kingdom)

^h CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

ⁱ UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA DEFENSIN 3; INTERLEUKIN 17 RECEPTOR; LACTATE DEHYDROGENASE; BETA DEFENSIN; BETA-DEFENSIN 3, MOUSE; IL17R PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIFUNGAL ACTIVITY; ARTICLE; CANDIDA ALBICANS; CANDIDIASIS; CELL PROTECTION; ENZYME RELEASE; EPITHELIUM CELL; FLOW CYTOMETRY; GENE EXPRESSION; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; LIMIT OF DETECTION; MOUSE; MOUTH MUCOSA; NEUTROPHIL; NONHUMAN; ORAL EPITHELIAL CELL; OROPHARYNX CANDIDIASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIATION CHIMERA; WEIGHT REDUCTION; ANIMAL; CANDIDA; CELL LINE; DEFICIENCY; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; SIGNAL TRANSDUCTION; THRUSH;

ANIMALS; BETA-DEFENSINS; CANDIDA; CANDIDIASIS, ORAL; CELL LINE; EPITHELIAL CELLS; HUMANS; MICE; MICE, KNOCKOUT; MOUTH MUCOSA; RECEPTORS, INTERLEUKIN-17; SIGNAL TRANSDUCTION;

EID: 84994719165     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.10.001     Document Type: Article

References (60)

1. Aujla, S.J., Dubin, P.J., Kolls, J.K., Th17 cells and mucosal host defense. Semin. Immunol. 19 (2007), 377–382.
2. Bär, E., Gladiator, A., Bastidas, S., Roschitzki, B., Acha-Orbea, H., Oxenius, A., LeibundGut-Landmann, S., A novel Th cell epitope of Candida albicans mediates protection from fungal infection. J. Immunol. 188 (2012), 5636–5643.
3. Bär, E., Whitney, P.G., Moor, K., Reis e Sousa, C., LeibundGut-Landmann, S., IL-17 regulates systemic fungal immunity by controlling the functional competence of NK cells. Immunity 40 (2014), 117–127.
4. Boisson, B., Wang, C., Pedergnana, V., Wu, L., Cypowyj, S., Rybojad, M., Belkadi, A., Picard, C., Abel, L., Fieschi, C., et al. An ACT1 mutation selectively abolishes interleukin-17 responses in humans with chronic mucocutaneous candidiasis. Immunity 39 (2013), 676–686.
5. Brown, G.D., Denning, D.W., Gow, N.A., Levitz, S.M., Netea, M.G., White, T.C., Hidden killers: human fungal infections. Sci. Transl. Med., 4, 2012, 165rv13.
6. Chen, K., Trevejo-Nunez, G., Way, E., Elsegeiny, W., Ricks, D., Garg, A., Wang, T., Gaffen, S.L., Kolls, J., Epithelial IL-17R signaling is required for mucosal chemokine gradients and pulmonary host defense against K. pneumoniae. Cell Host Microbe 20 (2016), 596–605 this issue.
7. Conti, H.R., Gaffen, S.L., IL-17-mediated immunity to the opportunistic fungal pathogen Candida albicans. J. Immunol. 195 (2015), 780–788.
8. Conti, H.R., Shen, F., Nayyar, N., Stocum, E., Sun, J.N., Lindemann, M.J., Ho, A.W., Hai, J.H., Yu, J.J., Jung, J.W., et al. Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J. Exp. Med. 206 (2009), 299–311.
9. Conti, H.R., Baker, O., Freeman, A.F., Jang, W.S., Holland, S.M., Li, R.A., Edgerton, M., Gaffen, S.L., New mechanism of oral immunity to mucosal candidiasis in hyper-IgE syndrome. Mucosal Immunol. 4 (2011), 448–455.
10. Conti, H.R., Peterson, A.C., Brane, L., Huppler, A.R., Hernández-Santos, N., Whibley, N., Garg, A.V., Simpson-Abelson, M.R., Gibson, G.A., Mamo, A.J., et al. Oral-resident natural Th17 cells and γδ T cells control opportunistic Candida albicans infections. J. Exp. Med. 211 (2014), 2075–2084.
11. Conti, H.R., Whibley, N., Coleman, B.M., Garg, A.V., Jaycox, J.R., Gaffen, S.L., Signaling through IL-17C/IL-17RE is dispensable for immunity to systemic, oral and cutaneous candidiasis. PLoS ONE, 10, 2015, e0122807.
12. Cua, D.J., Tato, C.M., Innate IL-17-producing cells: the sentinels of the immune system. Nat. Rev. Immunol. 10 (2010), 479–489.
13. Dickson, M.A., Hahn, W.C., Ino, Y., Ronfard, V., Wu, J.Y., Weinberg, R.A., Louis, D.N., Li, F.P., Rheinwald, J.G., Human keratinocytes that express hTERT and also bypass a p16(INK4a)-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics. Mol. Cell. Biol. 20 (2000), 1436–1447.
14. Edgerton, M., Koshlukova, S.E., Araujo, M.W., Patel, R.C., Dong, J., Bruenn, J.A., Salivary histatin 5 and human neutrophil defensin 1 kill Candida albicans via shared pathways. Antimicrob. Agents Chemother. 44 (2000), 3310–3316.
15. Ferreira, M.C., Whibley, N., Mamo, A.J., Siebenlist, U., Chan, Y.R., Gaffen, S.L., Interleukin-17-induced protein lipocalin 2 is dispensable for immunity to oral candidiasis. Infect. Immun. 82 (2014), 1030–1035.
16. Fidel, P.L. Jr., Candida-host interactions in HIV disease: implications for oropharyngeal candidiasis. Adv. Dent. Res. 23 (2011), 45–49.
17. Gaffen, S.L., Jain, R., Garg, A.V., Cua, D.J., The IL-23-IL-17 immune axis: from mechanisms to therapeutic testing. Nat. Rev. Immunol. 14 (2014), 585–600.
18. Gladiator, A., Wangler, N., Trautwein-Weidner, K., LeibundGut-Landmann, S., Cutting edge: IL-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J. Immunol. 190 (2013), 521–525.
19. Glocker, E., Grimbacher, B., Chronic mucocutaneous candidiasis and congenital susceptibility to Candida. Curr. Opin. Allergy Clin. Immunol. 10 (2010), 542–550.
20. Ha, H.L., Wang, H., Pisitkun, P., Kim, J.C., Tassi, I., Tang, W., Morasso, M.I., Udey, M.C., Siebenlist, U., IL-17 drives psoriatic inflammation via distinct, target cell-specific mechanisms. Proc. Natl. Acad. Sci. USA 111 (2014), E3422–E3431.
21. Hernández-Santos, N., Gaffen, S.L., Th17 cells in immunity to Candida albicans. Cell Host Microbe 11 (2012), 425–435.
22. Hernández-Santos, N., Huppler, A.R., Peterson, A.C., Khader, S.A., McKenna, K.C., Gaffen, S.L., Th17 cells confer long-term adaptive immunity to oral mucosal Candida albicans infections. Mucosal Immunol. 6 (2013), 900–910.
23. Ho, A.W., Shen, F., Conti, H.R., Patel, N., Childs, E.E., Peterson, A.C., Hernández-Santos, N., Kolls, J.K., Kane, L.P., Ouyang, W., Gaffen, S.L., IL-17RC is required for immune signaling via an extended SEF/IL-17R signaling domain in the cytoplasmic tail. J. Immunol. 185 (2010), 1063–1070.
24. Huppler, A.R., Conti, H.R., Hernández-Santos, N., Darville, T., Biswas, P.S., Gaffen, S.L., Role of neutrophils in IL-17-dependent immunity to mucosal candidiasis. J. Immunol. 192 (2014), 1745–1752.
25. Huppler, A.R., Verma, A.H., Conti, H.R., Gaffen, S.L., Neutrophils do not express IL-17A in the context of acute oropharyngeal candidiasis. Pathogens 4 (2015), 559–572.
26. Ibrahim, A.S., Luo, G., Gebremariam, T., Lee, H., Schmidt, C.S., Hennessey, J.P. Jr., French, S.W., Yeaman, M.R., Filler, S.G., Edwards, J.E. Jr., NDV-3 protects mice from vulvovaginal candidiasis through T- and B-cell immune response. Vaccine 31 (2013), 5549–5556.
27. Ishigame, H., Kakuta, S., Nagai, T., Kadoki, M., Nambu, A., Komiyama, Y., Fujikado, N., Tanahashi, Y., Akitsu, A., Kotaki, H., et al. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30 (2009), 108–119.
28. Jia, H.P., Wowk, S.A., Schutte, B.C., Lee, S.K., Vivado, A., Tack, B.F., Bevins, C.L., McCray, P.B. Jr., A novel murine β -defensin expressed in tongue, esophagus, and trachea. J. Biol. Chem. 275 (2000), 33314–33320.
29. Joly, S., Maze, C., McCray, P.B. Jr., Guthmiller, J.M., Human β-defensins 2 and 3 demonstrate strain-selective activity against oral microorganisms. J. Clin. Microbiol. 42 (2004), 1024–1029.
30. Kagami, S., Rizzo, H.L., Kurtz, S.E., Miller, L.S., Blauvelt, A., IL-23 and IL-17A, but not IL-12 and IL-22, are required for optimal skin host defense against Candida albicans. J. Immunol. 185 (2010), 5453–5462.
31. Kamai, Y., Kubota, M., Kamai, Y., Hosokawa, T., Fukuoka, T., Filler, S.G., New model of oropharyngeal candidiasis in mice. Antimicrob. Agents Chemother. 45 (2001), 3195–3197.
32. Kao, C.Y., Chen, Y., Thai, P., Wachi, S., Huang, F., Kim, C., Harper, R.W., Wu, R., IL-17 markedly up-regulates β-defensin-2 expression in human airway epithelium via JAK and NF-kappaB signaling pathways. J. Immunol. 173 (2004), 3482–3491.
33. Kisand, K., Bøe Wolff, A.S., Podkrajsek, K.T., Tserel, L., Link, M., Kisand, K.V., Ersvaer, E., Perheentupa, J., Erichsen, M.M., Bratanic, N., et al. Chronic mucocutaneous candidiasis in APECED or thymoma patients correlates with autoimmunity to Th17-associated cytokines. J. Exp. Med. 207 (2010), 299–308.
34. Kuestner, R.E., Taft, D.W., Haran, A., Brandt, C.S., Brender, T., Lum, K., Harder, B., Okada, S., Ostrander, C.D., Kreindler, J.L., et al. Identification of the IL-17 receptor related molecule IL-17RC as the receptor for IL-17F. J. Immunol. 179 (2007), 5462–5473.
35. Kumar, P., Monin, L., Castillo, P., Elsegeiny, W., Horne, W., Eddens, T., Vikram, A., Good, M., Schoenborn, A.A., Bibby, K., et al. Intestinal interleukin-17 receptor signaling mediates reciprocal control of the gut microbiota and autoimmune inflammation. Immunity 44 (2016), 659–671.
36. Ling, Y., Cypowyj, S., Aytekin, C., Galicchio, M., Camcioglu, Y., Nepesov, S., Ikinciogullari, A., Dogu, F., Belkadi, A., Levy, R., et al. Inherited IL-17RC deficiency in patients with chronic mucocutaneous candidiasis. J. Exp. Med. 212 (2015), 619–631.
37. Liu, Y., Shetty, A.C., Schwartz, J.A., Bradford, L.L., Xu, W., Phan, Q.T., Kumari, P., Mahurkar, A., Mitchell, A.P., Ravel, J., et al. New signaling pathways govern the host response to C. albicans infection in various niches. Genome Res. 25 (2015), 679–689.
38. Lubberts, E., Schwarzenberger, P., Huang, W., Schurr, J.R., Peschon, J.J., van den Berg, W.B., Kolls, J.K., Requirement of IL-17 receptor signaling in radiation-resistant cells in the joint for full progression of destructive synovitis. J. Immunol. 175 (2005), 3360–3368.
39. Milner, J.D., Holland, S.M., The cup runneth over: lessons from the ever-expanding pool of primary immunodeficiency diseases. Nat. Rev. Immunol. 13 (2013), 635–648.
40. Moyes, D.L., Richardson, J.P., Naglik, J.R., Candida albicans-epithelial interactions and pathogenicity mechanisms: scratching the surface. Virulence 6 (2015), 338–346.
41. Moyes, D.L., Wilson, D., Richardson, J.P., Mogavero, S., Tang, S.X., Wernecke, J., Höfs, S., Gratacap, R.L., Robbins, J., Runglall, M., et al. Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature 532 (2016), 64–68.
42. Parikh, N., Nagarajan, P., Sei-ichi, M., Sinha, S., Garrett-Sinha, L.A., Isolation and characterization of an immortalized oral keratinocyte cell line of mouse origin. Arch. Oral Biol. 53 (2008), 1091–1100.
43. Pietrella, D., Rachini, A., Pines, M., Pandey, N., Mosci, P., Bistoni, F., d'Enfert, C., Vecchiarelli, A., Th17 cells and IL-17 in protective immunity to vaginal candidiasis. PLoS ONE, 6, 2011, e22770.
44. Presland, R.B., Dale, B.A., Epithelial structural proteins of the skin and oral cavity: function in health and disease. Crit. Rev. Oral Biol. Med. 11 (2000), 383–408.
45. Puel, A., Döffinger, R., Natividad, A., Chrabieh, M., Barcenas-Morales, G., Picard, C., Cobat, A., Ouachée-Chardin, M., Toulon, A., Bustamante, J., et al. Autoantibodies against IL-17A, IL-17F, and IL-22 in patients with chronic mucocutaneous candidiasis and autoimmune polyendocrine syndrome type I. J. Exp. Med. 207 (2010), 291–297.
46. Puel, A., Cypowyj, S., Bustamante, J., Wright, J.F., Liu, L., Lim, H.K., Migaud, M., Israel, L., Chrabieh, M., Audry, M., et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332 (2011), 65–68.
47. Sanford, M., McKeage, K., Secukinumab: first global approval. Drugs 75 (2015), 329–338.
48. Shen, F., Hu, Z., Goswami, J., Gaffen, S.L., Identification of common transcriptional regulatory elements in interleukin-17 target genes. J. Biol. Chem. 281 (2006), 24138–24148.
49. Simpson-Abelson, M.R., Childs, E.E., Ferreira, M.C., Bishu, S., Conti, H.R., Gaffen, S.L., C/EBPβ promotes immunity to oral candidiasis through regulation of β-defensins. PLoS ONE, 10, 2015, e0136538.
50. Solis, N.V., Filler, S.G., Mouse model of oropharyngeal candidiasis. Nat. Protoc. 7 (2012), 637–642.
51. Taylor, P.R., Leal, S.M. Jr., Sun, Y., Pearlman, E., Aspergillus and Fusarium corneal infections are regulated by Th17 cells and IL-17-producing neutrophils. J. Immunol. 192 (2014), 3319–3327.
52. Tomalka, J., Azodi, E., Narra, H.P., Patel, K., O'Neill, S., Cardwell, C., Hall, B.A., Wilson, J.M., Hise, A.G., β-defensin 1 plays a role in acute mucosal defense against Candida albicans. J. Immunol. 194 (2015), 1788–1795.
53. Whibley, N., Gaffen, S.L., Gut-busters: IL-17 ain't afraid of no IL-23. Immunity 43 (2015), 620–622.
54. Whibley, N., Tritto, E., Traggiai, E., Kolbinger, F., Moulin, P., Brees, D., Coleman, B.M., Mamo, A.J., Garg, A.V., Jaycox, J.R., et al. Antibody blockade of IL-17 family cytokines in immunity to acute murine oral mucosal candidiasis. J. Leukoc. Biol. 99 (2016), 1153–1164.
55. Yamazaki, T., Yang, X.O., Chung, Y., Fukunaga, A., Nurieva, R., Pappu, B., Martin-Orozco, N., Kang, H.S., Ma, L., Panopoulos, A.D., et al. CCR6 regulates the migration of inflammatory and regulatory T cells. J. Immunol. 181 (2008), 8391–8401.
56. Yang, D., Chen, Q., Hoover, D.M., Staley, P., Tucker, K.D., Lubkowski, J., Oppenheim, J.J., Many chemokines including CCL20/MIP-3α display antimicrobial activity. J. Leukoc. Biol. 74 (2003), 448–455.
57. Yano, J., Noverr, M.C., Fidel, P.L. Jr., Cytokines in the host response to Candida vaginitis: identifying a role for non-classical immune mediators, S100 alarmins. Cytokine 58 (2012), 118–128.
58. Yao, Z., Fanslow, W.C., Seldin, M.F., Rousseau, A.-M., Painter, S.L., Comeau, M.R., Cohen, J.I., Spriggs, M.K., Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3 (1995), 811–821.
59. Ye, P., Rodriguez, F.H., Kanaly, S., Stocking, K.L., Schurr, J., Schwarzenberger, P., Oliver, P., Huang, W., Zhang, P., Zhang, J., et al. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194 (2001), 519–527.
60. Zhu, W., Phan, Q.T., Boontheung, P., Solis, N.V., Loo, J.A., Filler, S.G., EGFR and HER2 receptor kinase signaling mediate epithelial cell invasion by Candida albicans during oropharyngeal infection. Proc. Natl. Acad. Sci. USA 109 (2012), 14194–14199.