Advertisement

The Role of the Mycobiota in the Gut-Liver Axis

  • Maria Camila Alvarez-Silva
  • Thorsten Brach
  • Asker Daniel Brejnrod
  • Manimozhiyan ArumugamEmail author
Chapter
First Online:

Abstract

The human mycobiota, consisting of all the fungi living in and on our body, is an understudied and underestimated part of the human microbiota. Fungal colonization is a well-established cause of human health problems, but for methodological reasons the mycobiota has not been studied as intensely as other constituents of the human microbiota. In this chapter, we highlight the importance of human gut mycobiota and host-fungal homeostasis. We lay out currently proposed mechanisms through which disturbance of host-fungal homeostasis can lead to fungal-related diseases in general as well as liver diseases in particular. We also address the methodological challenges of investigating the fungal component of the human microbiota. While new sequencing technologies have improved our understanding of the human microbiota, investigating and characterizing fungi requires more attention. We draw parallels to the better-established sequencing-based characterization of prokaryotes in the human microbiota, and examine the perspectives for advancing the field of studying fungal communities.

Keywords

Human gut microbiota Human gut mycobiota Human mycobiota Fungal microbiota Fungi Gut-liver axis Liver diseases 
This is a preview of subscription content, log in to check access.

References

  1. 1.
    NIH HMP Working Group TNHW, Peterson J, Garges S, Giovanni M, McInnes P, Wang L, et al. The NIH Human Microbiome Project. Genome Res. 2009;19(12):2317–23.CrossRefGoogle Scholar
  2. 2.
    Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Underhill DM, Iliev ID. The mycobiota: interactions between commensal fungi and the host immune system. Nat Rev Immunol. 2014;14(6):405–16.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Wheeler ML, Limon JJ, Underhill DM. Immunity to commensal fungi: detente and disease. Annu Rev Pathol Mech Dis. 2017;12(1):359–85.CrossRefGoogle Scholar
  5. 5.
    Huffnagle GB, Noverr MC. The emerging world of the fungal microbiome. Trends Microbiol. 2013;21(7):334–41.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Sam QH, Chang MW, Chai LYA. The fungal mycobiome and its interaction with gut bacteria in the host. Int J Mol Sci. 2017;18(2):pii: E330.CrossRefGoogle Scholar
  7. 7.
    Yang AM, Inamine T, Hochrath K, Chen P, Wang L, Llorente C, et al. Intestinal fungi contribute to development of alcoholic liver disease. J Clin Invest. 2017;127(7):2829–41.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Chen Y, Chen Z, Guo R, Chen N, Lu H, Huang S, et al. Correlation between gastrointestinal fungi and varying degrees of chronic hepatitis B virus infection. Diagn Microbiol Infect Dis. 2011;70(4):492–8.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Strati F, Cavalieri D, Albanese D, De Felice C, Donati C, Hayek J, et al. Altered gut microbiota in Rett syndrome. Microbiome. 2016;4(1):41.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Kim SH, Clark ST, Surendra A, Copeland JK, Wang PW, Ammar R, et al. Global analysis of the fungal microbiome in cystic fibrosis patients reveals loss of function of the transcriptional repressor Nrg1 as a mechanism of pathogen adaptation. PLoS Pathog. 2015;11(11):1–26.CrossRefGoogle Scholar
  11. 11.
    Mar Rodríguez M, Pérez D, Javier Chaves F, Esteve E, Marin-Garcia P, Xifra G, et al. Obesity changes the human gut mycobiome. Sci Rep. 2015;5:14600.Google Scholar
  12. 12.
    Hoarau G, Mukherjee PK, Gower-rousseau C, Hager C, Chandra J, Retuerto MA, et al. Bacteriome and mycobiome interactions underscore microbial dysbiosis in familial Crohn’s disease. MBio. 2016;7(October):1–11.Google Scholar
  13. 13.
    Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, Strom SP, et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science. 2012;336(6086):1314–7.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Hager CL, Ghannoum MA. The mycobiome: role in health and disease, and as a potential probiotic target in gastrointestinal disease. Dig Liver Dis. 2017;49(11):1171–6.PubMedCrossRefGoogle Scholar
  15. 15.
    Heisel T, Montassier E, Johnson A, Al-Ghalith G, Lin Y-W, Wei L-N, et al. High-fat diet changes fungal microbiomes and interkingdom relationships in the murine gut. mSphere. 2017;2(5):e00351–17.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Ott SJ, Kühbacher T, Musfeldt M, Rosenstiel P, Hellmig S, Rehman A, et al. Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand J Gastroenterol. 2008;43(7):831–41.PubMedCrossRefGoogle Scholar
  17. 17.
    Kalan L, Loesche M, Hodkinson BP, Heilmann K, Ruthel G, Gardner SE, et al. Redefining the chronic-wound microbiome: fungal communities are prevalent, dynamic, and associated with delayed healing. MBio. 2016;7(5):1–12.CrossRefGoogle Scholar
  18. 18.
    Delhaes L, Monchy S, Fréalle E, Hubans C, Salleron J, Leroy S, et al. The airway microbiota in cystic fibrosis: a complex fungal and bacterial community—implications for therapeutic management. PLoS One. 2012;7(4):e36313.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Sokol H, Leducq V, Aschard H, Pham H, Jegou S, Landman C, et al. Fungal microbiota dysbiosis in IBD. Gut. 2017;66(6):1039–48.PubMedCrossRefGoogle Scholar
  20. 20.
    Sellart-Altisent M, Torres-Rodríguez JM, Gómez de Ana S, Alvarado-Ramírez E. Nasal fungal microbiota in allergic and healthy subjects. Rev Iberoam Micol. 2007;24(2):125–30.PubMedCrossRefGoogle Scholar
  21. 21.
    Limper AH, Adenis A, Le T, Harrison TS. Fungal infections in HIV/AIDS. Lancet Infect Dis. 2017;17(11):e334–43.PubMedCrossRefGoogle Scholar
  22. 22.
    Lionakis MS, Kontoyiannis DP. Glucocorticoids and invasive fungal infections. Lancet. 2003;362(9398):1828–38.PubMedCrossRefGoogle Scholar
  23. 23.
    Fraczek MG, Chishimba L, Niven RM, Bromley M, Simpson A, Smyth L, et al. Corticosteroid treatment is associated with increased filamentous fungal burden in allergic fungal disease. J Allergy Clin Immunol. 2017:pii: S0091-6749(17)31732-3.Google Scholar
  24. 24.
    Ng TTC, Robson GD, Denning DW. Hydrocortisone-enhanced growth of Aspergillus spp.: implications for pathogenesis. Microbiology. 1994;140(9):2475–9.PubMedCrossRefGoogle Scholar
  25. 25.
    Ferwerda B, Ferwerda G, Plantinga TS, Willment JA, van Spriel AB, Venselaar H, et al. Human Dectin-1 deficiency and mucocutaneous fungal infections. N Engl J Med. 2009;361(18):1760–7.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Lamas B, Richard ML, Leducq V, Pham H-P, Michel M-L, Da Costa G, et al. CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat Med. 2016;22(6):598–605.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    GWAS Catalog [Internet]. [cited 2017 Nov 9]. Available from: https://www.ebi.ac.uk/gwas/
  28. 28.
    Cui L, Morris A, Ghedin E. The human mycobiome in health and disease. Genome Med. 2013;5(63):1–12.Google Scholar
  29. 29.
    Hatoum R, Labrie S, Fliss I. Antimicrobial and probiotic properties of yeasts: from fundamental to novel applications. Front Microbiol. 2012;3(December):1–12.Google Scholar
  30. 30.
    Millsap KW, van der Mei HC, Bos R, Busscher HJ. Adhesive interactions between medically important yeasts and bacteria. FEMS Microbiol Rev. 1998;21(4):321–36.PubMedCrossRefGoogle Scholar
  31. 31.
    Rizzetto L, Ifrim DC, Moretti S, Tocci N, Cheng S-C, Quintin J, et al. Fungal chitin induces trained immunity in human monocytes during cross-talk of the host with Saccharomyces cerevisiae. J Biol Chem. 2016;291(15):7961–72.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Hallen-Adams HE, Suhr MJ. Fungi in the healthy human gastrointestinal tract. Virulence. 2017;8(3):352–8.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Suhr MJ, Hallen-Adams HE. The human gut mycobiome: pitfalls and potentials – a mycologists perspective. Mycologia. 2015;107(6):1057–73.PubMedCrossRefGoogle Scholar
  34. 34.
    Hoffmann C, Dollive S, Grunberg S, Chen J, Li H, Wu GD, et al. Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS One. 2013;8(6):e66019.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Mukherjee PK, Sendid B, Hoarau G, Colombel J-F, Poulain D, Ghannoum MA. Mycobiota in gastrointestinal diseases. Nat Rev Gastroenterol Hepatol. 2015;12(2):77–87.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Iliev ID, Leonardi I. Fungal dysbiosis: immunity and interactions at mucosal barriers. Nat Rev Immunol. 2017;7(10):635–47.CrossRefGoogle Scholar
  37. 37.
    Nash AK, Auchtung TA, Wong MC, Smith DP, Gesell JR, Ross MC, et al. The gut mycobiome of the Human Microbiome Project healthy cohort. Microbiome. 2017;5(1):153.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Hallen-Adams HE, Kachman SD, Kim J, Legge RM, Martínez I. Fungi inhabiting the healthy human gastrointestinal tract: a diverse and dynamic community. Fungal Ecol. 2015;15:9–17.CrossRefGoogle Scholar
  39. 39.
    Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, et al. The long-term stability of the human gut microbiota. Science. 2013;341(6141):1237439.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35(21):7188–96.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009;37(Database):D141–5.CrossRefGoogle Scholar
  42. 42.
    Abarenkov K, Henrik Nilsson R, Larsson K-H, Alexander IJ, Eberhardt U, Erland S, et al. The UNITE database for molecular identification of fungi – recent updates and future perspectives. New Phytol. 2010;186(2):281–5.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Irinyi L, Serena C, Garcia-Hermoso D, Arabatzis M, Desnos-Ollivier M, Vu D, et al. International Society of Human and Animal Mycology (ISHAM)-ITS reference DNA barcoding database – the quality controlled standard tool for routine identification of human and animal pathogenic fungi. Med Mycol. 2015;53(4):313–37.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A. 2012;109(16):6241–6.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Herrera ML, Vallor AC, Gelfond JA, Patterson TF, Wickes BL. Strain-dependent variation in 18S ribosomal DNA copy numbers in Aspergillus fumigatus. J Clin Microbiol. 2009;47(5):1325–32.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Stockinger H, Krüger M, Schüßler A. DNA barcoding of arbuscular mycorrhizal fungi. New Phytol. 2010;187(2):461–74.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Bengtsson-Palme J, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A, et al. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol. 2013;4(10):914–9.Google Scholar
  48. 48.
    Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005;71(12):8228–35.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Chen J, Bittinger K, Charlson ES, Hoffmann C, Lewis J, Wu GD, et al. Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics. 2012;28(16):2106–13.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Thorsen J, Brejnrod A, Mortensen M, Rasmussen MA, Stokholm J, Al-Soud WA, et al. Large-scale benchmarking reveals false discoveries and count transformation sensitivity in 16S rRNA gene amplicon data analysis methods used in microbiome studies. Microbiome. 2016;4(1):62.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Gregory Caporaso J, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. Introducing mothur: open-source, platform-independent, community supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75(23):7537–41.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Větrovský T, Baldrian P. Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. Biol Fertil Soils. 2013;49(8):1027–37.CrossRefGoogle Scholar
  54. 54.
    Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R, et al. Fungal community analysis by high-throughput sequencing of amplified markers – a user’s guide. New Phytol. 2013;199(1):288–99.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Llorente C, Schnabl B. The gut microbiota and liver disease. Cell Mol Gastroenterol Hepatol. 2015;1(3):275–84.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Szabo G. Gut-liver axis in alcoholic liver disease. Gastroenterology. 2015;148(1):30–6.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Wang L, Llorente C, Hartmann P, Yang A-M, Chen P, Schnabl B. Methods to determine intestinal permeability and bacterial translocation during liver disease. J Immunol Methods. 2015;421:44–53.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Miele L, Valenza V, La Torre G, Montalto M, Cammarota G, Ricci R, et al. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology. 2009;49(6):1877–87.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Parlesak A, Schäfer C, Schütz T, Bode JC, Bode C. Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. J Hepatol. 2000;32(5):742–7.PubMedCrossRefGoogle Scholar
  60. 60.
    Shrestha R, Shrestha R, Qin X-Y, Kuo T-F, Oshima Y, Iwatani S, et al. Fungus-derived hydroxyl radicals kill hepatic cells by enhancing nuclear transglutaminase. Sci Rep. 2017;7(1):4746.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Ferrier L, Bérard F, Debrauwer L, Chabo C, Langella P, Buéno L, et al. Impairment of the intestinal barrier by ethanol involves enteric microflora and mast cell activation in rodents. Am J Pathol. 2006;168(4):1148–54.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Elamin EE, Masclee AA, Dekker J, Jonkers DM. Ethanol metabolism and its effects on the intestinal epithelial barrier. Nutr Rev. 2013;71(7):483–99.PubMedCrossRefGoogle Scholar
  63. 63.
    Ying W, Jing T, Bing C, Baifang W, Dai Z, Bingyuan W. Effects of alcohol on intestinal epithelial barrier permeability and expression of tight junction-associated proteins. Mol Med Rep. 2014;9(6):2352–6.CrossRefGoogle Scholar
  64. 64.
    Dunagan M, Chaudhry K, Samak G, Rao RK. Acetaldehyde disrupts tight junctions in Caco-2 cell monolayers by a protein phosphatase 2A-dependent mechanism. AJP Gastrointest Liver Physiol. 2012;303(12):G1356–64.CrossRefGoogle Scholar
  65. 65.
    Chen P, Stärkel P, Turner JR, Ho SB, Schnabl B. Dysbiosis-induced intestinal inflammation activates tumor necrosis factor receptor I and mediates alcoholic liver disease in mice. Hepatology. 2015;61(3):883–94.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Rodondo N, Harvey F, Williams R. Fungal infection: a common, unrecognised of acute liver failure complication. J Hepatol. 1991;12:1–9.CrossRefGoogle Scholar
  67. 67.
    Anttila V-J, Elonen E, Nordling S, Sivonen A, Ruutu T, Ruutu P. Hepatosplenic candidiasis in patients with acute leukemia: incidence and prognostic implications. Clin Infect Dis. 1997;24(3):375–80.PubMedCrossRefGoogle Scholar
  68. 68.
    Lorand L, Graham RM. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol. 2003;4(2):140–56.PubMedCrossRefGoogle Scholar
  69. 69.
    Iismaa SE, Mearns BM, Lorand L, Graham RM. Transglutaminases and disease: lessons from genetically engineered mouse models and inherited disorders. Physiol Rev. 2009;89:991–1023.PubMedCrossRefGoogle Scholar
  70. 70.
    Mirza A, Liu SL, Frizell E, Zhu J, Maddukuri S, Martinez J, et al. A role for tissue transglutaminase in hepatic injury and fibrogenesis, and its regulation by NF-kappaB. Am J Phys. 1997;272(2 Pt 1):G281–8.Google Scholar
  71. 71.
    Tatsukawa H, Fukaya Y, Frampton G, Martinez-Fuentes A, Suzuki K, Kuo TF, et al. Role of transglutaminase 2 in liver injury via cross-linking and silencing of transcription factor Sp1. Gastroenterology. 2009;136(5):1783–95.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Wu J, Liu SL, Zhu JL, Norton PA, Nojiri S, Hoek JB, et al. Roles of tissue transglutaminase in ethanol-induced inhibition of hepatocyte proliferation and α1-adrenergic signal transduction. J Biol Chem. 2000;275(29):22213–9.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Kuo TF, Tatsukawa H, Matsuura T, Nagatsuma K, Hirose S, Kojima S. Free fatty acids induce transglutaminase 2-dependent apoptosis in hepatocytes via ER stress-stimulated PERK pathways. J Cell Physiol. 2012;227(3):1130–7.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Lee ZW, Kwon SM, Kim SW, Yi SJ, Kim YM, Ha KS. Activation of in situ tissue transglutaminase by intracellular reactive oxygen species. Biochem Biophys Res Commun. 2003;305(3):633–40.PubMedCrossRefGoogle Scholar
  75. 75.
    Bhatt MP, Lim YC, Hwang J, Na S, Kim YM, Ha KS. C-peptide prevents hyperglycemia-induced endothelial apoptosis through inhibition of reactive oxygen species-mediated transglutaminase 2 activation. Diabetes. 2013;62(1):243–53.PubMedCrossRefGoogle Scholar
  76. 76.
    Schröter C, Hipler UC, Wilmer A, Kunkel W, Wollina U. Generation of reactive oxygen species by Candida albicans in relation to morphogenesis. Arch Dermatol Res. 2000;292(5):260–4.PubMedCrossRefGoogle Scholar
  77. 77.
    Hsu HY, Wen MH. Lipopolysaccharide-mediated reactive oxygen species and signal transduction in the regulation of interleukin-1 gene expression. J Biol Chem. 2002;277(25):22131–9.PubMedCrossRefGoogle Scholar
  78. 78.
    Gross O, Poeck H, Bscheider M, Dostert C, Hannesschläger N, Endres S, et al. Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature. 2009;459(7245):433–6.PubMedCrossRefGoogle Scholar
  79. 79.
    Meyer A, Brach T. Dynamic redox measurements with redox-sensitive GFP in plants by confocal laser scanning microscopy. In: Pfannschmidt T, editor. Plant signal transduction. Methods in molecular biology, vol. 479. Totowa: Humana Press; 2009. p. 479.Google Scholar
  80. 80.
    Tsoni SV, Brown GD. beta-Glucans and dectin-1. Ann N Y Acad Sci. 2008;1143:45–60.PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Reid DM, Gow NA, Brown GD. Pattern recognition: recent insights from Dectin-1. Curr Opin Immunol. 2009;21(1):30–7.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Kankkunen P, Teirila L, Rintahaka J, Alenius H, Wolff H, Matikainen S. (1,3)-beta-glucans activate both Dectin-1 and NLRP3 inflammasome in human macrophages. J Immunol. 2010;184(11):6335–42.PubMedCrossRefGoogle Scholar
  83. 83.
    Dambuza IM, Brown GD. C-type lectins in immunity: recent developments. Curr Opin Immunol. 2015;32:21–7.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Taylor PR, Brown GD, Reid DM, Willment JA, Martinez-Pomares L, Gordon S, et al. beta_Glucans and dectin-1. J Immunol. 2002;169(7):3876–82.PubMedCrossRefGoogle Scholar
  85. 85.
    Bauernfeind FG, Horvath G, Stutz A, Alnemri ES, MacDonald K, Speert D, et al. Cutting edge: NF-B activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol. 2009;183(2):787–91.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Swidergall M, Solis NV, Lionakis MS, Filler SG. EphA2 is an epithelial cell pattern recognition receptor for fungal β-glucans. Nat Microbiol. 2018;3(1):53–61.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Maria Camila Alvarez-Silva
    • 1
  • Thorsten Brach
    • 1
  • Asker Daniel Brejnrod
    • 1
  • Manimozhiyan Arumugam
    • 1
    Email author
  1. 1.Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of CopenhagenCopenhagenDenmark

Personalised recommendations

Cite chapter