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Folia Microbiologica

, Volume 64, Issue 4, pp 555–566 | Cite as

Heat-killed Candida albicans augments synthetic bacterial component-induced proinflammatory cytokine production

  • Riyoko TamaiEmail author
  • Yusuke Kiyoura
Original Article
  • 115 Downloads

Abstract

Candida albicans can enhance the invasion of oral epithelial cells by Porphyromonas gingivalis, although the fungus is not a periodontal pathogen. In this study, we investigated whether C. albicans augments proinflammatory cytokine production by mouse macrophage-like J774.1 cells incubated with synthetic bacterial components. Mouse macrophage-like J774.1 cells, mouse primary splenocytes, human THP-1 cells, and A549 cells were pretreated with or without heat-killed C. albicans (HKCA) or substitutes for C. albicans cell wall components in 96-well flat-bottomed plates. Cells were then washed and incubated with Pam3CSK4, a Toll-like receptor (TLR) 2 ligand, or lipid A, a TLR4 ligand. Culture supernatants were analyzed by ELISA for secreted IL-6, MCP-1, TNF-α, and IL-8. HKCA augmented TLR ligand-induced proinflammatory cytokine production by J774.1 cells, mouse splenocytes, and THP-1 cells, but not A549 cells. However, IL-6, MCP-1, and TNF-α production induced by Pam3CSK4 or lipid A was not augmented when cells were pretreated with curdlan, a dectin-1 ligand, or mannan, a dectin-2 ligand. In contrast, pretreatment of cells with TLR ligands upregulated the production of IL-6 and TNF-α, but not MCP-1, induced by Pam3CSK4 or lipid A. The results suggest that C. albicans augments synthetic bacterial component-induced cytokine production by J774.1 cells via the TLR pathway, but not the dectin-1 or dectin-2 pathway.

Notes

Funding information

This study was supported by a Grant-in-Aid for Scientific Research from the Ohu University School of Dentistry.

Compliance with ethical standards

Ethics statement

All animals were handled and cared for according to guidelines for the proper conduct of animal experiments (Japan) published by the Science Council of Japan. All procedures were approved by the Institutional Animal Care and Use Committee of Ohu University.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Akagawa G, Abe S, Yamaguchi H (1995) Mortality of Candida albicans-infected mice is facilitated by superinfection of Escherichia coli or administration of its lipopolysaccharide. J Infect Dis 171:1539–1544CrossRefGoogle Scholar
  2. Biondo C, Malara A, Costa A, Signorino G, Cardile F, Midiri A, Galbo R, Papasergi S, Domina M, Pugliese M, Teti G, Mancuso G, Beninati C (2012) Recognition of fungal RNA by TLR7 has a nonredundant role in host defense against experimental candidiasis. Eur J Immunol 42:2632–2643CrossRefGoogle Scholar
  3. Brown BR, Lee EJ, Snow PE, Vance EE, Iwakura Y, Ohno N, Miura N, Lin X, Brown GD, Wells CA, Smith JR, Caspi RR, Rosenzweig HL (2017) Fungal-derived cues promote ocular autoimmunity through a Dectin-2/Card9-mediated mechanism. Clin Exp Immunol 190:293–303CrossRefGoogle Scholar
  4. Charo IF, Taubman MB (2004) Chemokines in the pathogenesis of vascular disease. Circ Res 95:858–866CrossRefGoogle Scholar
  5. Choteau L, Vancraeyneste H, Le Roy D, Dubuquoy L, Romani L, Jouault T, Poulain D, Sendid B, Calandra T, Roger T, Jawhara S (2017) Role of TLR1, TLR2 and TLR6 in the modulation of intestinal inflammation and Candida albicans elimination. Gut Pathog 9:9CrossRefGoogle Scholar
  6. Esteban A, Popp MW, Vyas VK, Strijbis K, Ploegh HL, Fink GR (2011) Fungal recognition is mediated by the association of dectin-1 and galectin-3 in macrophages. Proc Natl Acad Sci 108:14270–14275CrossRefGoogle Scholar
  7. Feinberg H, Jegouzo SAF, Rex MJ, Drickamer K, Weis WI, Taylor ME (2017) Mechanism of pathogen recognition by human dectin-2. J Biol Chem 292:13402–13414CrossRefGoogle Scholar
  8. Ferwerda G, Meyer-Wentrup F, Kullberg BJ, Netea MG, Adema GJ (2008) Dectin-1 synergizes with TLR2 and TLR4 for cytokine production in human primary monocytes and macrophages. Cell Microbiol 10:2058–2066CrossRefGoogle Scholar
  9. Fowler M, Thomas RJ, Atherton J, Roberts IS, High NJ (2006) Galectin-3 binds to Helicobacter pylori O-antigen: it is upregulated and rapidly secreted by gastric epithelial cells in response to H. pylori adhesion. Cell Microbiol 8:44–54CrossRefGoogle Scholar
  10. Fradin C, Poulain D, Jouault T (2000) β-1,2-linked oligomannosides from Candida albicans bind to a 32-kilodalton macrophage membrane protein homologous to the mammalian lectin galectin-3. Infect Immun 68:4391–4398CrossRefGoogle Scholar
  11. Garcia-Valtanen P, Guzman-Genuino RM, Williams DL, Hayball JD, Diener KR (2017) Evaluation of trained immunity by β-1, 3 (D)-glucan on murine monocytes in vitro and duration of response in vivo. Immunol Cell Biol 95:601–610CrossRefGoogle Scholar
  12. Han C, Jin J, Xu S, Liu H, Li N, Cao X (2010) Integrin CD11b negatively regulates TLR-triggered inflammatory responses by activating Syk and promoting degradation of MyD88 and TRIF via Cbl-b. Nat Immunol 11:734–742CrossRefGoogle Scholar
  13. Harokopakis E, Hajishengallis G (2005) Integrin activation by bacterial fimbriae through a pathway involving CD14, Toll-like receptor 2, and phosphatidylinositol-3-kinase. Eur J Immunol 35:1201–1210CrossRefGoogle Scholar
  14. Heinsbroek SE, Taylor PR, Martinez FO, Martinez-Pomares L, Brown GD, Gordon S (2008) Stage-specific sampling by pattern recognition receptors during Candida albicans phagocytosis. PLoS Pathog 4:e1000218CrossRefGoogle Scholar
  15. Heyl KA, Klassert TE, Heinrich A, Muller MM, Klaile E, Dienemann H, Grunewald C, Bals R, Singer BB, Slevogt H (2014) Dectin-1 is expressed in human lung and mediates the proinflammatory immune response to nontypeable Haemophilus influenzae. MBio 5:e01492–e01414CrossRefGoogle Scholar
  16. Hojo K, Tamai R, Kobayashi-Sakamoto M, Kiyoura Y (2017) Etidronate down-regulates Toll-like receptor (TLR) 2 ligand-induced proinflammatory cytokine production by inhibiting NF-κB activation. Pharmacol Rep 69:773–778CrossRefGoogle Scholar
  17. Hwang G, Liu Y, Kim D, Li Y, Krysan DJ, Koo H (2017) Candida albicans mannans mediate Streptococcus mutans exoenzyme GtfB binding to modulate cross-kingdom biofilm development in vivo. PLoS Pathog 13:e1006407CrossRefGoogle Scholar
  18. Ifrim DC, Joosten LA, Kullberg BJ, Jacobs L, Jansen T, Williams DL, Gow NA, van der Meer JW, Netea MG, Quintin J (2013) Candida albicans primes TLR cytokine responses through a Dectin-1/Raf-1-mediated pathway. J Immunol 190:4129–4135CrossRefGoogle Scholar
  19. Jouault T, El Abed-El Behi M, Martinez-Esparza M, Breuilh L, Trinel PA, Chamaillard M, Trottein F, Poulain D (2006) Specific recognition of Candida albicans by macrophages requires galectin-3 to discriminate Saccharomyces cerevisiae and needs association with TLR2 for signaling. J Immunol 177:4679–4687CrossRefGoogle Scholar
  20. Kamagata-Kiyoura Y, Abe S, Yamaguchi H, Nitta T (2004a) Protective effects of human saliva on experimental murine oral candidiasis. J Infect Chemother 10:253–255CrossRefGoogle Scholar
  21. Kamagata-Kiyoura Y, Abe S, Yamaguchi H, Nitta T (2004b) Reduced activity of Candida detachment factors in the saliva of the elderly. J Infect Chemother 10:59–61CrossRefGoogle Scholar
  22. Kobayashi-Sakamoto M, Tamai R, Isogai E, Kiyoura Y (2018) Gastrointestinal colonisation and systemic spread of Candida albicans in mice treated with antibiotics and prednisolone. Microb Pathog 117:191–199CrossRefGoogle Scholar
  23. Kohatsu L, Hsu DK, Jegalian AG, Liu FT, Baum LG (2006) Galectin-3 induces death of Candida species expressing specific β-1,2-linked mannans. J Immunol 177:4718–4726CrossRefGoogle Scholar
  24. Kuhn DM, Vyas VK (2012) The Candida glabrata adhesin Epa1p causes adhesion, phagocytosis, and cytokine secretion by innate immune cells. FEMS Yeast Res 12:398–414CrossRefGoogle Scholar
  25. Kumar PS, Griffen AL, Moeschberger ML, Leys EJ (2005) Identification of candidate periodontal pathogens and beneficial species by quantitative 16S clonal analysis. J Clin Microbiol 43:3944–3955CrossRefGoogle Scholar
  26. Kushida T, Makino T, Tomomura M, Tomomura A, Sakagami H (2011) Enhancement of Dectin-2 gene expression by lignin-carbohydrate complex from Lentinus edodes mycelia extract (LEM) in a mouse macrophage-like cell line. Anticancer Res 31:1241–1248Google Scholar
  27. Lee J, Lee S, Zhang H, Hill MA, Zhang C, Park Y (2017) Interaction of IL-6 and TNF-α contributes to endothelial dysfunction in type 2 diabetic mouse hearts. PLoS One 12:e0187189CrossRefGoogle Scholar
  28. Lee WJ, Liao YC, Wang YF, Lin IF, Wang SJ, Fuh JL (2018) Plasma MCP-1 and cognitive decline in patients with Alzheimer’s disease and mild cognitive impairment: a two-year follow-up study. Sci Rep 8:1280CrossRefGoogle Scholar
  29. Li X, Qin L, Bergenstock M, Bevelock LM, Novack DV, Partridge NC (2007) Parathyroid hormone stimulates osteoblastic expression of MCP-1 to recruit and increase the fusion of pre/osteoclasts. J Biol Chem 282:33098–33106CrossRefGoogle Scholar
  30. Li Y, Komai-Koma M, Gilchrist DS, Hsu DK, Liu FT, Springall T, Xu D (2008) Galectin-3 is a negative regulator of lipopolysaccharide-mediated inflammation. J Immunol 181:2781–2789CrossRefGoogle Scholar
  31. Li X, Utomo A, Cullere X, Choi MM, Milner DA Jr, Venkatesh D, Yun SH, Mayadas TN (2011) The β-glucan receptor Dectin-1 activates the integrin mac-1 in neutrophils via Vav protein signaling to promote Candida albicans clearance. Cell Host Microbe 10:603–615CrossRefGoogle Scholar
  32. Linden JR, De Paepe ME, Laforce-Nesbitt SS, Bliss JM (2013) Galectin-3 plays an important role in protection against disseminated candidiasis. Med Mycol 51:641–651CrossRefGoogle Scholar
  33. Makimura Y, Asai Y, Taiji Y, Sugiyama A, Tamai R, Ogawa T (2006) Correlation between chemical structure and biological activities of Porphyromonas gingivalis synthetic lipopeptide derivatives. Clin Exp Immunol 146:159–168CrossRefGoogle Scholar
  34. Martin M, Katz J, Vogel SN, Michalek SM (2001) Differential induction of endotoxin tolerance by lipopolysaccharides derived from Porphyromonas gingivalis and Escherichia coli. J Immunol 167:5278–5285CrossRefGoogle Scholar
  35. Masuda T, Deng X, Tamai R (2009) Mouse macrophages primed with alendronate down-regulate monocyte chemoattractant protein-1 (MCP-1) and macrophage inflammatory protein-1α (MIP-1α) production in response to Toll-like receptor (TLR) 2 and TLR4 agonist via Smad3 activation. Int Immunopharmacol 9:1115–1121CrossRefGoogle Scholar
  36. McKenzie CG, Koser U, Lewis LE, Bain JM, Mora-Montes HM, Barker RN, Gow NA, Erwig LP (2010) Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages. Infect Immun 78:1650–1658CrossRefGoogle Scholar
  37. Miyazato A, Nakamura K, Yamamoto N, Mora-Montes HM, Tanaka M, Abe Y, Tanno D, Inden K, Gang X, Ishii K, Takeda K, Akira S, Saijo S, Iwakura Y, Adachi Y, Ohno N, Mitsutake K, Gow NA, Kaku M, Kawakami K (2009) Toll-like receptor 9-dependent activation of myeloid dendritic cells by deoxynucleic acids from Candida albicans. Infect Immun 77:3056–3064CrossRefGoogle Scholar
  38. Naik S, Larsen SB, Gomez NC, Alaverdyan K, Sendoel A, Yuan S, Polak L, Kulukian A, Chai S, Fuchs E (2017) Inflammatory memory sensitizes skin epithelial stem cells to tissue damage. Nature 550:475–480CrossRefGoogle Scholar
  39. Netea MG, van de Veerdonk F, Verschueren I, van der Meer JW, Kullberg BJ (2008) Role of TLR1 and TLR6 in the host defense against disseminated candidiasis. FEMS Immunol Med Microbiol 52:118–123CrossRefGoogle Scholar
  40. Netea MG, Joosten LA, Latz E, Mills KH, Natoli G, Stunnenberg HG, O’Neill LA, Xavier RJ (2016) Trained immunity: a program of innate immune memory in health and disease. Science 352:aaf1098CrossRefGoogle Scholar
  41. Nomura F, Akashi S, Sakao Y, Sato S, Kawai T, Matsumoto M, Nakanishi K, Kimoto M, Miyake K, Takeda K, Akira S (2000) Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J Immunol 164:3476–3479CrossRefGoogle Scholar
  42. O’Brien XM, Heflin KE, Lavigne LM, Yu K, Kim M, Salomon AR, Reichner JS (2012) Lectin site ligation of CR3 induces conformational changes and signaling. J Biol Chem 287:3337–3348CrossRefGoogle Scholar
  43. Pietrella D, Pandey N, Gabrielli E, Pericolini E, Perito S, Kasper L, Bistoni F, Cassone A, Hube B, Vecchiarelli A (2013) Secreted aspartic proteases of Candida albicans activate the NLRP3 inflammasome. Eur J Immunol 43:679–692CrossRefGoogle Scholar
  44. Pinke KH, Freitas P, Viera NA, Honorio HM, Porto VC, Lara VS (2016) Decreased production of proinflammatory cytokines by monocytes from individuals presenting Candida-associated denture stomatitis. Cytokine 77:145–151CrossRefGoogle Scholar
  45. Plantinga TS, Johnson MD, Scott WK, van de Vosse E, Velez Edwards DR, Smith PB, Alexander BD, Yang JC, Kremer D, Laird GM, Oosting M, Joosten LA, van der Meer JW, van Dissel JT, Walsh TJ, Perfect JR, Kullberg BJ, Netea MG (2012) Toll-like receptor 1 polymorphisms increase susceptibility to candidemia. J Infect Dis 205:934–943CrossRefGoogle Scholar
  46. Quintin J, Saeed S, Martens JHA, Giamarellos-Bourboulis EJ, Ifrim DC, Logie C, Jacobs L, Jansen T, Kullberg BJ, Wijmenga C, Joosten LAB, Xavier RJ, van der Meer JWM, Stunnenberg HG, Netea MG (2012) Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 12:223–232CrossRefGoogle Scholar
  47. Reynaud AH, Nygaard-Ostby B, Boygard GK, Eribe ER, Olsen I, Gjermo P (2001) Yeasts in periodontal pockets. J Clin Periodontol 28:860–864CrossRefGoogle Scholar
  48. Saijo S, Ikeda S, Yamabe K, Kakuta S, Ishigame H, Akitsu A, Fujikado N, Kusaka T, Kubo S, Chung SH, Komatsu R, Miura N, Adachi Y, Ohno N, Shibuya K, Yamamoto N, Kawakami K, Yamasaki S, Saito T, Akira S, Iwakura Y (2010) Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 32:681–691CrossRefGoogle Scholar
  49. Samaranayake LP, Holmstrup P (1989) Oral candidiasis and human immunodeficiency virus infection. J Oral Pathol Med 18:554–564CrossRefGoogle Scholar
  50. Samaranayake LP, Lamb AB, Lamey PJ, MacFarlane TW (1989) Oral carriage of Candida species and coliforms in patients with burning mouth syndrome. J Oral Pathol Med 18:233–235CrossRefGoogle Scholar
  51. Schulert GS, Allen LA (2006) Differential infection of mononuclear phagocytes by Francisella tularensis: role of the macrophage mannose receptor. J Leukoc Biol 80:563–571CrossRefGoogle Scholar
  52. Slots J, Rams TE, Listgarten MA (1988) Yeasts, enteric rods and pseudomonads in the subgingival flora of severe adult periodontitis. Oral Microbiol Immunol 3:47–52CrossRefGoogle Scholar
  53. Tamai R, Kiyoura Y (2014) Candida albicans and Candida parapsilosis rapidly up-regulate galectin-3 secretion by human gingival epithelial cells. Mycopathologia 177:75–79CrossRefGoogle Scholar
  54. Tamai R, Kiyoura Y (2018) Alendronate augments lipid A-induced IL-1β release and Smad3/NLRP3/ASC-dependent cell death. Life Sci 198:8–17CrossRefGoogle Scholar
  55. Tamai R, Deng X, Kiyoura Y (2009) Porphyromonas gingivalis with either Tannerella forsythia or Treponema denticola induces synergistic IL-6 production by murine macrophage-like J774.1 cells. Anaerobe 15:87–90CrossRefGoogle Scholar
  56. Tamai R, Sugamata M, Kiyoura Y (2011) Candida albicans enhances invasion of human gingival epithelial cells and gingival fibroblasts by Porphyromonas gingivalis. Microb Pathog 51:250–254CrossRefGoogle Scholar
  57. Tanne A, Ma B, Boudou F, Tailleux L, Botella H, Badell E, Levillain F, Taylor ME, Drickamer K, Nigou J, Dobos KM, Puzo G, Vestweber D, Wild MK, Marcinko M, Sobieszczuk P, Stewart L, Lebus D, Gicquel B, Neyrolles O (2009) A murine DC-SIGN homologue contributes to early host defense against Mycobacterium tuberculosis. J Exp Med 206:2205–2220CrossRefGoogle Scholar
  58. Thein ZM, Samaranayake YH, Samaranayake LP (2006) Effect of oral bacteria on growth and survival of Candida albicans biofilms. Arch Oral Biol 51:672–680CrossRefGoogle Scholar
  59. Underhill DM (2007) Collaboration between the innate immune receptors dectin-1, TLRs, and nods. Immunol Rev 219:75–87CrossRefGoogle Scholar
  60. Waltimo TM, Sen BH, Meurman JH, Orstavik D, Haapasalo MP (2003) Yeasts in apical periodontitis. Crit Rev Oral Biol Med 14:128–137CrossRefGoogle Scholar
  61. Wang S, Xu M, Li F, Wang X, Bower KA, Frank JA, Lu Y, Chen G, Zhang Z, Ke Z, Shi X, Luo J (2012) Ethanol promotes mammary tumor growth and angiogenesis: the involvement of chemoattractant factor MCP-1. Breast Cancer Res Treat 133:1037–1048CrossRefGoogle Scholar
  62. Wang W, Li Z, Han Q, Guo Y, Zhang B, D’Inca R (2016) Dietary live yeast and mannan-oligosaccharide supplementation attenuate intestinal inflammation and barrier dysfunction induced by Escherichia coli in broilers. Br J Nutr 116:1878–1888CrossRefGoogle Scholar
  63. Wang J, Huang J, Wang L, Chen C, Yang D, Jin M, Bai C, Song Y (2017) Urban particulate matter triggers lung inflammation via the ROS-MAPK-NF-κB signaling pathway. J Thorac Dis 9:4398–4412CrossRefGoogle Scholar
  64. Wellington M, Dolan K, Krysan DJ (2009) Live Candida albicans suppresses production of reactive oxygen species in phagocytes. Infect Immun 77:405–413CrossRefGoogle Scholar
  65. Wirnsberger G, Zwolanek F, Asaoka T, Kozieradzki I, Tortola L, Wimmer RA, Kavirayani A, Fresser F, Baier G, Langdon WY, Ikeda F, Kuchler K, Penninger JM (2016) Inhibition of CBLB protects from lethal Candida albicans sepsis. Nat Med 22:915–923CrossRefGoogle Scholar
  66. Wu SY, Huang JH, Chen WY, Chan YC, Lin CH, Chen YC, Liu FT, Wu-Hsieh BA (2017) Cell intrinsic galectin-3 attenuates neutrophil ROS-dependent killing of Candida by modulating CR3 downstream Syk activation. Front Immunol 8:48Google Scholar
  67. Xiao Y, Tang J, Guo H, Zhao Y, Tang R, Ouyang S, Zeng Q, Rappleye CA, Rajaram MV, Schlesinger LS, Tao L, Brown GD, Langdon WY, Li BT, Zhang J (2016) Targeting CBLB as a potential therapeutic approach for disseminated candidiasis. Nat Med 22:906–914CrossRefGoogle Scholar
  68. Xiaoyan Z, Xinyi W, Li G (2011) Pretreatment with lipopolysaccharide modulates innate immunity in corneal fibroblasts challenged with Aspergillus fumigatus. Innate Immun 17:237–244CrossRefGoogle Scholar
  69. Xie Y, Xu M, Xiao Y, Liu Z, Jiang C, Kuang X, Wang C, Wu H, Peng J, Li C, Wang Y, Liu H, Liu B, Zhang X, Zhao F, Zeng T, Liu S, Wu Y (2017) Treponema pallidum flagellin FlaA2 induces IL-6 secretion in THP-1 cells via the Toll-like receptor 2 signaling pathway. Mol Immunol 81:42–51CrossRefGoogle Scholar
  70. Yee NK, Hamerman JA (2013) β2 integrins inhibit TLR responses by regulating NF-κB pathway and p38 MAPK activation. Eur J Immunol 43:779–792CrossRefGoogle Scholar
  71. Zaric SS, Coulter WA, Shelburne CE, Fulton CR, Zaric MS, Scott A, Lappin MJ, Fitzgerald DC, Irwin CR, Taggart CC (2011) Altered Toll-like receptor 2-mediated endotoxin tolerance is related to diminished interferon β production. J Biol Chem 286:29492–29500CrossRefGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i. 2019

Authors and Affiliations

  1. 1.Department of Oral Medical ScienceOhu University School of DentistryKoriyamaJapan

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