5,676
Views
40
CrossRef citations to date
0
Altmetric
Review

Candida Albicans Interactions With The Host: Crossing The Intestinal Epithelial Barrier”

ORCID Icon, , , ORCID Icon & ORCID Icon
Article: 1612661 | Received 16 Jan 2019, Accepted 24 Apr 2019, Published online: 12 Jun 2019

References

  • Tadec L, Talarmin J-P, Gastinne T, Bretonnière C, Miegeville M, Le Pape P, Morio F. Epidemiology, risk factor, species distribution, antifungal resistance and outcome of Candidemia at a single French hospital: a 7-year study. Mycoses. 2016;59(5):296–303. doi:10.1111/myc.2016.59.issue-5.
  • Horn DL, Neofytos D, Anaissie EJ, Fishman JA, Steinbach WJ, Olyaei AJ, et al. Epidemiology and outcomes of candidemia in 2019 patients: data from the prospective antifungal therapy alliance registry. Clin Infect Dis. 2009;48(12):1695–1703. doi:10.1086/597588.
  • Arendrup MC, Sulim S, Holm A, Nielsen L, Nielsen SD, Knudsen JD, Drenck NE, Christensen JJ, Johansen HK. Diagnostic issues, clinical characteristics and outcome for patients with fungaemia. J Clin Microbiol. 2011;49(9):3300–3308.
  • Gudlaugsson O, Gillespie S, Lee K, Berg JV, Hu J, Messer S, Herwaldt L, Pfaller M, Diekema D. Attributable mortality of nosocomial candidemia, revisited. Clin Infect Dis. 2003;37(9):1172–1177. doi:10.1086/375875.
  • Sheppard DC, Filler SG. Host cell invasion by medically important fungi. Cold Spring Harb Perspect Med. 2014 Nov 3;5(1):a019687. doi:10.1101/cshperspect.a019687.
  • Zhu W, Filler SG. Interactions of Candida albicans with epithelial cells. Cell Microbiol. 2010 Mar;12(3):273–282. doi:10.1111/j.1462-5822.2009.01412.x.
  • Gouba N, Drancourt M. Digestive tract mycobiota: a source of infection. Med Mal Infect. 2015;45(1–2):9–16. doi:10.1016/j.medmal.2015.01.007.
  • Saiman L, Ludington E, Pfaller M, Rangel-Frausto S, Wiblin RT, Dawson J, Blumberg HM, Patterson JE, Rinaldi M, Edwards JE, et al. Risk factors for candidemia in neonatal intensive care unit patients. Pediatr Infect Dis J. 2000;19(4):319–324. doi:10.1097/00006454-200004000-00011.
  • Goyer M, Loiselet A, Bon F, L’Ollivier C, Laue M, Holland G, Bonnin A, Dalle F. Intestinal Cell Tight Junctions Limit Invasion of Candida albicans through Active Penetration and Endocytosis in the Early Stages of the Interaction of the Fungus with the Intestinal Barrier. PLoS One. 2016;11(3):e0149159. doi:10.1371/journal.pone.0149159.
  • Dalle F, Wächtler B, L’Ollivier C, Holland G, Bannert N, Wilson D Labruère C, Bonnin A, Hube B. Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes. Cell Microbiol. 2010 Feb 1;12(2):248–271. doi:10.1111/j.1462-5822.2009.01394.x.
  • Albac S, Schmitz A, Lopez-Alayon C, d’Enfert C, Sautour M, Ducreux A, Labruère-Chazal C, Laue M, Holland G, Bonnin A, et al. Candida albicans is able to use M cells as a portal of entry across the intestinal barrier in vitro. Cell Microbiol. 2016 Feb;18(2):195–210. doi:10.1111/cmi.12570.
  • Perlroth J, Choi B, Spellberg B. Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med Mycol. 2007 Jun;45(4):321–346. doi:10.1080/13693780701218689.
  • Zaborin A, Smith D, Garfield K, Quensen J, Shakhsheer B, Kade M Tirrell M, Tiedje J, Gilbert JA, Zaborina O, et al. Membership and behavior of ultra-low-diversity pathogen communities present in the gut of humans during prolonged critical illness. mBio. 2014 Sep 23;5(5):e01361–01314. doi:10.1128/mBio.01361-14.
  • Koh AY. Murine models of Candida gastrointestinal colonization and dissemination. Eukaryot Cell. 2013 Nov;12(11):1416–1422. doi:10.1128/EC.00196-13.
  • Sokol H, Leducq V, Aschard H, Pham H-P, Jegou S, Landman C, Cohen D, Liguori G, Bourrier A, Nion-Larmurier I, et al. Fungal microbiota dysbiosis in IBD. Gut. 2017;66(6):1039–1048. doi:10.1136/gutjnl-2015-310746.
  • Botschuijver S, Roeselers G, Levin E, Jonkers DM, Welting O, Heinsbroek SEM, de Weerd HH, Boekhout T, Fornai M, Masclee AA, et al. Intestinal Fungal Dysbiosis Is Associated With Visceral Hypersensitivity in Patients With Irritable Bowel Syndrome and Rats. Gastroenterology. 2017;153(4):1026–1039. doi:10.1053/j.gastro.2017.06.004.
  • Wheeler ML, Limon JJ, Bar AS, Leal CA, Gargus M, Tang J, Brown J, Funari VA, Wang HL, Crother TR, et al. Immunological Consequences of Intestinal Fungal Dysbiosis. Cell Host Microbe. 2016 Jun 8;19(6):865–873. doi:10.1016/j.chom.2016.05.003.
  • Standaert-Vitse A, Sendid B, Joossens M, François N, Vandewalle-El Khoury P, Branche J, Van Kruiningen H, Jouault T, Rutgeerts P, Gower-Rousseau C, et al. Candida albicans colonization and ASCA in familial Crohn’s disease. Am J Gastroenterol. 2009 Jul;104(7):1745–1753. doi:10.1038/ajg.2009.225.
  • Chehoud C, Albenberg LG, Judge C, Hoffmann C, Grunberg S, Bittinger K, Baldassano RN, Lewis JD, Bushman FD, Wu GD. Fungal Signature in the Gut Microbiota of Pediatric Patients With Inflammatory Bowel Disease. Inflamm Bowel Dis. 2015 Aug;21(8):1948–1956. doi:10.1097/MIB.0000000000000454.
  • Sommer F, Bäckhed F. The gut microbiota—masters of host development and physiology. Nat Rev Microbiol. 2013;11(4):227. doi:10.1038/nrmicro2974.
  • Limon JJ, Skalski JH, Underhill DM. Commensal Fungi in Health and Disease. Cell Host Microbe. 2017 Aug 9;22(2):156–165. doi:10.1016/j.chom.2017.07.002.
  • Mohajeri MH, Brummer RJM, Rastall RA, Weersma RK, Harmsen HJM, Faas M, Eggersdorfer M. The role of the microbiome for human health: from basic science to clinical applications. Eur J Nutr. 2018 May 10. doi:10.1007/s00394-018-1703-4.
  • Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, Clemente JC, Knight R, Heath AC, Leibel RL, et al. The long-term stability of the human gut microbiota. Science. 2013;341(6141):1237439. doi:10.1126/science.1237439.
  • Sekirov I, Russell SL, Antunes LCM, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90(3):859–904. doi:10.1152/physrev.00045.2009.
  • David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559. doi:10.1038/nature12820.
  • Rolhion N, Chassaing B. When pathogenic bacteria meet the intestinal microbiota. Philos Trans R Soc Lond B Biol Sci. 2016 Nov 5;371:1707. doi:10.1098/rstb.2015.0504.
  • Allaire JM, Crowley SM, Law HT, Chang S-Y, Ko H-J, Vallance BA. The Intestinal Epithelium: central Coordinator of Mucosal Immunity. Trends Immunol. 2018;39(9):677–696.
  • Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis. 2015 Jan 1;26(s2):26191.
  • Cox LM, Weiner HL. Microbiota Signaling Pathways that Influence Neurologic Disease. Neurotherapeutics. 2018 Jan 1;15(1):135–145. doi:10.1007/s13311-017-0598-8.
  • Geuking MB, Köller Y, Rupp S, McCoy KD. The interplay between the gut microbiota and the immune system. Gut Microbes. 2014;5(3):411–418. doi:10.4161/gmic.29330.
  • Rescigno M. Intestinal microbiota and its effects on the immune system. Cell Microbiol. 2014;16(7):1004–1013. doi:10.1111/cmi.2014.16.issue-7.
  • Sittipo P, Lobionda S, Lee YK, Maynard CL. Intestinal microbiota and the immune system in metabolic diseases. J Microbiol. 2018;56(3):154–162. doi:10.1007/s12275-018-7548-y.
  • Hallen-Adams HE, Suhr MJ. Fungi in the healthy human gastrointestinal tract. Virulence. 2017 03;8(3):352–358. doi:10.1080/21505594.2016.1247140.
  • Iliev ID, Leonardi I. Fungal dysbiosis: immunity and interactions at mucosal barriers. Nat Rev Immunol. 2017 Oct;17(10):635–646. doi:10.1038/nri.2017.55.
  • Mar Rodríguez M, Pérez D, Javier Chaves F, Esteve E, Marin-Garcia P, Xifra G, Vendrell J, Jovè M, Pamplona R, Ricart W, et al. Obesity changes the human gut mycobiome. Sci Rep. 2015 Oct;12(5):14600. doi:10.1038/srep14600.
  • Gerbe F, Legraverend C, Jay P. The intestinal epithelium tuft cells: specification and function. Cell Mol Life Sci. 2012;69(17):2907–2917. doi:10.1007/s00018-012-0984-7.
  • Mowat AM. To respond or not to respond — a personal perspective of intestinal tolerance. Nat Rev Immunol. 2018 Jun;18(6):405–415. doi:10.1038/s41577-018-0002-x.
  • Holmes R, Lobley RW. Intestinal brush border revisited. Gut. 1989;30(12):1667. doi:10.1136/gut.30.12.1667.
  • Suzuki T. Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci. 2013 Feb 1;70(4):631–659. doi:10.1007/s00018-012-1070-x.
  • Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol. 2001 Apr;2(4):285–293. doi:10.1038/35067088.
  • Pearce SC, Al-Jawadi A, Kishida K, Yu S, Hu M, Fritzky LF, Edelblum KL, Gao N, Ferraris RP. Marked differences in tight junction composition and macromolecular permeability among different intestinal cell types. BMC Biol. 2018;16(1):19. doi:10.1186/s12915-018-0481-z.
  • Hartsock A, Nelson WJ. Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta BBA-Biomembr. 2008;1778(3):660–669. doi:10.1016/j.bbamem.2007.07.012.
  • Assimakopoulos SF, Papageorgiou I, Charonis A. Enterocytes’ tight junctions: from molecules to diseases. World J Gastrointest Pathophysiol. 2011;2(6):123. doi:10.4291/wjgp.v2.i6.123.
  • Zihni C, Mills C, Matter K, Balda MS. Tight junctions: from simple barriers to multifunctional molecular gates. Nat Rev Mol Cell Biol. 2016;17(9):564–580. doi:10.1038/nrm.2016.80.
  • Bouhet S, Oswald IP. The effects of mycotoxins, fungal food contaminants, on the intestinal epithelial cell-derived innate immune response. Vet Immunol Immunopathol. 2005;108(1–2):199–209. doi:10.1016/j.vetimm.2005.08.010.
  • Lewis SA, Berg JR, Kleine TJ. Modulation of epithelial permeability by extracellular macromolecules. Physiol Rev. 1995 Jul;75(3):561–589. doi:10.1152/physrev.1995.75.3.561.
  • Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC. Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr. 2011 May;141(5):769–776. doi:10.3945/jn.110.135657.
  • Wang W, Uzzau S, Goldblum SE, Fasano A. Human zonulin, a potential modulator of intestinal tight junctions. J Cell Sci. 2000;113:4435–4440.
  • Fasano A. Zonulin, regulation of tight junctions, and autoimmune diseases. Ann N Y Acad Sci. 2012;1258(1):25–33. doi:10.1111/j.1749-6632.2012.06538.x.
  • Martens EC, Neumann M, Desai MS. Interactions of commensal and pathogenic microorganisms with the intestinal mucosal barrier. Nat Rev Microbiol. 2018;16(8):457–470.
  • Tapia R, Kralicek S, Hecht G. EPEC Perturbation of Crb3 and Pals1 Localization Precedes Tight Junction Disruption. Faseb J. 2017;31: 1043–10.
  • Anderson RC, Cookson AL, McNabb WC, Park Z, McCann MJ, Kelly WJ, Roy NC. Lactobacillus plantarum MB452 enhances the function of the intestinal barrier by increasing the expression levels of genes involved in tight junction formation. BMC Microbiol. 2010 Dec 9;10:316. doi:10.1186/1471-2180-10-316.
  • El Asmar R, Panigrahi P, Bamford P, Berti I, Not T, Coppa GV, Catassi C, Fasano A. Host-dependent activation of the zonulin system is involved in the impairment of the gut barrier function following bacterial colonization. Gastroenterology. 2002;123(5):1607–1615. doi:10.1053/gast.2002.36578.
  • Alam A, Neish A. Role of gut microbiota in intestinal wound healing and barrier function. Tissue Barriers. 2018 Jul 3;6(3):1539595. doi:10.1080/21688370.2018.1539595.
  • Awad WA, Hess C, Hess M. Enteric Pathogens and Their Toxin-Induced Disruption of the Intestinal Barrier through Alteration of Tight Junctions in Chickens. Toxins. 2017 Feb 10;9(2):pii: E60.
  • Torres-Flores JM, Arias CF. Tight Junctions Go Viral!. Viruses. 2015 Sep 23;7(9):5145–5154. doi:10.3390/v7092865.
  • Di Genova BM, Tonelli RR. Infection Strategies of Intestinal Parasite Pathogens and Host Cell Responses. Front Microbiol. 2016;7:256. doi:10.3389/fmicb.2016.00256.
  • Hattrup CL, Gendler SJ. Structure and function of the cell surface (tethered) mucins. Annu Rev Physiol. 2008;70:431–457. doi:10.1146/annurev.physiol.70.113006.100659.
  • Deplancke B, Gaskins HR. Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am J Clin Nutr. 2001;73(6):1131S–1141S. doi:10.1093/ajcn/73.6.1131S.
  • Naughton J, Duggan G, Bourke B, Clyne M. Interaction of microbes with mucus and mucins: recent developments. Gut Microbes. 2014;5(1):48–52. doi:10.4161/gmic.26680.
  • Petersson J, Schreiber O, Hansson GC, Gendler SJ, Velcich A, Lundberg JO et al. Importance and regulation of the colonic mucus barrier in a mouse model of colitis. Am J Physiol-Gastrointest Liver Physiol. 2010 Nov 25;300(2):G327–33. doi:10.1152/ajpgi.00422.2010.
  • Kandori H, Hirayama K, Takeda M, Doi K. Histochemical, lectin-histochemical and morphometrical characteristics of intestinal goblet cells of germfree and conventional mice. Exp Anim. 1996;45:155–160.
  • Ishikawa K, Satoh Y, Oomori Y, Yamano M, Matsuda M, Ono K. Influence of conventionalization on cecal wall structure of germ-free Wistar rats: quantitative light and qualitative electron microscopic observations. Anat Embryol (Berl). 1989;180(2):191–198. doi:10.1007/BF00309771.
  • Li H, Limenitakis JP, Fuhrer T, Geuking MB, Lawson MA, Wyss M, Brugiroux S, Keller I, Macpherson JA, Rupp S, et al. The outer mucus layer hosts a distinct intestinal microbial niche. Nat Commun. 2015;6:8292. doi:10.1038/ncomms9292.
  • Ouellette AJ, Darmoul D, Tran D, Huttner KM, Yuan J, Selsted ME. Peptide localization and gene structure of cryptdin 4, a differentially expressed mouse paneth cell alpha-defensin. Infect Immun. 1999 Dec;67(12):6643–6651.
  • Porter EM, Liu L, Oren A, Anton PA, Ganz T. Localization of human intestinal defensin 5 in Paneth cell granules. Infect Immun. 1997 Jun;65(6):2389–2395.
  • Ghoos Y, Vantrappen G. The cytochemical localization of lysozyme in Paneth cell granules. Histochem J. 1971 May;3(3):175–178. doi:10.1007/BF01002560.
  • Longman RJ, Douthwaite J, Sylvester PA, Poulsom R, Corfield AP, Thomas MG, Wright NA. Coordinated localisation of mucins and trefoil peptides in the ulcer associated cell lineage and the gastrointestinal mucosa. Gut. 2000;47(6):792–800.
  • Corfield AP. Mucins: a biologically relevant glycan barrier in mucosal protection. Biochim Biophys Acta BBA-Gen Subj. 2015;1850(1):236–252. doi:10.1016/j.bbagen.2014.05.003.
  • Johansson MEV, Hansson GC. Immunological aspects of intestinal mucus and mucins. Nat Rev Immunol. 2016 Oct;16(10):639–649. doi:10.1038/nri.2016.88.
  • McGuckin MA, Lindén SK, Sutton P, Florin TH. Mucin dynamics and enteric pathogens. Nat Rev Microbiol. 2011 Apr;9(4):265–278. doi:10.1038/nrmicro2538.
  • Corfield AP, Wagner SA, Clamp JR, Kriaris MS, Hoskins LC. Mucin degradation in the human colon: production of sialidase, sialate O-acetylesterase, N-acetylneuraminate lyase, arylesterase, and glycosulfatase activities by strains of fecal bacteria. Infect Immun. 1992;60:3971–3978.
  • Corfield AP, Wagner SA, O’Donnell LJ, Durdey P, Mountford RA, Clamp JR. The roles of enteric bacterial sialidase, sialateO-acetyl esterase and glycosulfatase in the degradation of human colonic mucin. Glycoconj J. 1993;10(1):72–81. doi:10.1007/BF00731190.
  • Haider K, Hossain A, Wanke C, Qadri F, Ali S, Nahar S. Production of mucinase and neuraminidase and binding of Shigella to intestinal mucin. J Diarrhoeal Dis Res. 1993;11(2):88–92.
  • Homer KA, Whiley RA, Beighton D. Production of specific glycosidase activities by Streptococcus intermedius strain UNS35 grown in the presence of mucin. J Med Microbiol. 1994;41(3):184–190. doi:10.1099/00222615-41-3-184.
  • Moncada DM, Kammanadiminti SJ, Chadee K. Mucin and Toll-like receptors in host defense against intestinal parasites. Trends Parasitol. 2003;19(7):305–311. doi:10.1016/S1471-4922(03)00122-3.
  • Lidell ME, Moncada DM, Chadee K, Hansson GC. Entamoeba histolytica cysteine proteases cleave the MUC2 mucin in its C-terminal domain and dissolve the protective colonic mucus gel. Proc Natl Acad Sci. 2006;103(24):9298–9303. doi:10.1073/pnas.0600623103.
  • Cooke CL, An HJ, Kim J, Canfield DR, Torres J, Lebrilla CB, Solnick JV. Modification of gastric mucin oligosaccharide expression in rhesus macaques after infection with Helicobacter pylori. Gastroenterology. 2009;137(3):1061–1071. doi:10.1053/j.gastro.2009.04.014.
  • Skoog EC, Sjöling A, Navabi N, Holgersson J, Lundin SB, Lindén SK. Human gastric mucins differently regulate Helicobacter pylori proliferation, gene expression and interactions with host cells. PloS One. 2012;7:e36378.
  • Tu QV, McGuckin MA, Mendz GL. Campylobacter jejuni response to human mucin MUC2: modulation of colonization and pathogenicity determinants. J Med Microbiol. 2008;57(7):795–802. doi:10.1099/jmm.0.47752-0.
  • Bevins CL, Salzman NH. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol. 2011 May;9(5):356–368. doi:10.1038/nrmicro2546.
  • Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal α-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol. 2000 Aug;1(2):113–118. doi:10.1038/77783.
  • Satoh Y, Habara Y, Ono K, Kanno T. Carbamylcholine- and catecholamine-induced intracellular calcium dynamics of epithelial cells in mouse ileal crypts. Gastroenterology. 1995 May;108(5):1345–1356. doi:10.1016/0016-5085(95)90681-9.
  • Kiyohara H, Egami H, Shibata Y, Murata K, Ohshima S, Ogawa M. Light microscopic immunohistochemical analysis of the distribution of group II phospholipase A2 in human digestive organs. J Histochem Cytochem Off J Histochem Soc. 1992 Nov;40(11):1659–1664. doi:10.1177/40.11.1431054.
  • Lasserre C, Colnot C, Bréchot C, Poirier F. HIP/PAP gene, encoding a C-type lectin overexpressed in primary liver cancer, is expressed in nervous system as well as in intestine and pancreas of the postimplantation mouse embryo. Am J Pathol. 1999 May;154(5):1601–1610. doi:10.1016/S0002-9440(10)65413-2.
  • Holly MK, Smith JG. Paneth Cells during Viral Infection and Pathogenesis. Viruses [Internet]. 2018 Apr 26 [cited 2018 Jul 4];10(5). https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5977218/.
  • Hooper LV, Stappenbeck TS, Hong CV, Gordon JI. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol. 2003 Mar;4(3):269–273. doi:10.1038/ni888.
  • Hase K. Cell Differentiation Is a Key Determinant of Cathelicidin LL-37/Human Cationic Antimicrobial Protein 18 Expression by Human Colon Epithelium. Infect Immun. 2002 Feb 1;70(2):953–963. doi:10.1128/IAI.70.2.953-963.2002.
  • Nakamura K, Sakuragi N, Takakuwa A, Ayabe T. Paneth cell α-defensins and enteric microbiota in health and disease. Biosci Microbiota Food Health. 2016;35(2):57–67. doi:10.12938/bmfh.16-012.
  • Million M, Tomas J, Wagner C, Lelouard H, Raoult D, Gorvel J-P. New insights in gut microbiota and mucosal immunity of the small intestine. Hum Microbiome J. 2018 Apr 1;7–8:23–32. doi:10.1016/j.humic.2018.01.004.
  • Mantis NJ, Rol N, Corthésy B. Secretory IgA’s complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 2011 Nov;4(6):603–611. doi:10.1038/mi.2011.41.
  • Stokes CR, Soothill JF, Turner MW. Immune exclusion is a function of IgA. Nature. 1975 Jun 26;255(5511):745–746. doi:10.1038/255745a0.
  • Pabst O, Cerovic V, Hornef M. Secretory IgA in the Coordination of Establishment and Maintenance of the Microbiota. Trends Immunol. 2016;37(5):287–296. doi:10.1016/j.it.2016.03.002.
  • Forbes SJ, Bumpus T, McCarthy EA, Corthésy B, Mantis NJ. Transient suppression of Shigella flexneri type 3 secretion by a protective O-antigen-specific monoclonal IgA. mBio. 2011;2(3):e00042–00011. doi:10.1128/mBio.00042-11.
  • Vaerman JP, Derijck-Langendries A, Rits M, Delacroix D. Neutralization of cholera toxin by rat bile secretory IgA antibodies. Immunology. 1985 Mar;54(3):601–603.
  • Peterson LW, Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol. 2014 Mar;14(3):141–153. doi:10.1038/nri3608.
  • Howe KL, Reardon C, Wang A, Nazli A, McKay DM. Transforming growth factor-β regulation of epithelial tight junction proteins enhances barrier function and blocks enterohemorrhagic Escherichia coli O157: H7-induced increased permeability. Am J Pathol. 2005;167(6):1587–1597. doi:10.1016/S0002-9440(10)61243-6.
  • Madsen KL, Lewis SA, Tavernini MM, Hibbard J, Fedorak RN. Interleukin 10 prevents cytokine-induced disruption of T84 monolayer barrier integrity and limits chloride secretion. Gastroenterology. 1997;113(1):151–159. doi:10.1016/S0016-5085(97)70090-8.
  • Huttner KM, Bevins CL. Antimicrobial peptides as mediators of epithelial host defense. Pediatr Res. 1999;45(6):785. doi:10.1203/00006450-199906000-00001.
  • Watanabe M, Ueno Y, Yajima T, Iwao Y, Tsuchiya M, Ishikawa H, Aiso S, Hibi T, Ishii H. Interleukin 7 is produced by human intestinal epithelial cells and regulates the proliferation of intestinal mucosal lymphocytes. J Clin Invest. 1995;95(6):2945–2953. doi:10.1172/JCI118002.
  • Dwinell MB, Eckmann L, Leopard JD, Varki NM, Kagnoff MF. Chemokine receptor expression by human intestinal epithelial cells. Gastroenterology. 1999;117(2):359–367. doi:10.1053/gast.1999.0029900359.
  • Jung HC, Eckmann L, Yang S-K, Panja A, Fierer J, Morzycka-Wroblewska E, Kagnoff MF. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest. 1995;95(1):55–65. doi:10.1172/JCI117676.
  • Rooks MG, Garrett WS. Gut microbiota, metabolites and host immunity. Nat Rev Immunol. 2016 Jun;16(6):341–352. doi:10.1038/nri.2016.42.
  • Schoenborn AA, Furstenberg RJ von, Valsaraj S, Hussain Fs, Stein M, Shanahan MT, Henning SJ, Gulati AS. The enteric microbiota regulates jejunal Paneth cell number and function without impacting intestinal stem cells. Gut Microbes. 2019;10(1):45–58.
  • Schoenborn AA, Furstenberg R von, Valsaraj S, Hussain FS, Stein M, Shanahan M, Gulati AS, Henning SJ. The Enteric Microbiota Regulates Paneth Cell Number and Function Without Affecting Intestinal Stem Cells. Gastroenterology. 2017 Apr 1;152(5):S13.
  • Ahluwalia B, Magnusson MK, Öhman L. Mucosal immune system of the gastrointestinal tract: maintaining balance between the good and the bad. Scand J Gastroenterol. 2017 Nov;52(11):1185–1193. doi:10.1080/00365521.2017.1349173.
  • Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336(6086):1268–1273. doi:10.1126/science.1223490.
  • Ohno H. Intestinal M cells. J Biochem (Tokyo). 2015;159(2):151–160. doi:10.1093/jb/mvv121.
  • Chen Y, Chou K, Fuchs E, Havran WL, Boismenu R. Protection of the intestinal mucosa by intraepithelial γδ T cells. Proc Natl Acad Sci. 2002 Oct 29;99(22):14338–14343. doi:10.1073/pnas.212290499.
  • Ismail AS, Severson KM, Vaishnava S, Behrendt CL, Yu X, Benjamin JL, Ruhn KA, Hou B, DeFranco AL, Yarovinsky F, et al. γδ intraepithelial lymphocytes are essential mediators of host–microbial homeostasis at the intestinal mucosal surface. Proc Natl Acad Sci. 2011 May 24;108(21):8743–8748. doi:10.1073/pnas.1019574108.
  • Smith P, Garrett W. The Gut Microbiota and Mucosal T Cells. Front Microbiol [Internet]. 2011 [cited 2019 Mar 7];2. https://www.frontiersin.org/articles/10.3389/fmicb.2011.00111/full.
  • Romani L, Bistoni F, Puccetti P. Adaptation of Candida albicans to the host environment: the role of morphogenesis in virulence and survival in mammalian hosts. Curr Opin Microbiol. 2003;6:338–343.
  • Pearson C, Uhlig HH, Powrie F. Lymphoid microenvironments and innate lymphoid cells in the gut. Trends Immunol. 2012 Jun 1;33(6):289–296. doi:10.1016/j.it.2012.04.004.
  • Kurashima Y, Kiyono H. Mucosal Ecological Network of Epithelium and Immune Cells for Gut Homeostasis and Tissue Healing. Annu Rev Immunol. 2017;35(1):119–147. doi:10.1146/annurev-immunol-051116-052424.
  • Farstad IN, Halstensen TS, Fausa O, Brandtzaeg P. Heterogeneity of M-cell-associated B and T cells in human Peyer’s patches. Immunology. 1994;83:457.
  • Collins JK, Cashman S, Morgan J, O’Sullivan GC. The Gastrointestinal Immune System: recognising Microbes in the Gut.
  • Kanaya T, Hase K, Takahashi D, Fukuda S, Hoshino K, Sasaki I, Hemmi H, Knoop KA, Kumar N, Sato M, et al. The Ets transcription factor Spi-B is essential for the differentiation of intestinal microfold cells. Nat Immunol. 2012 Jun 17;13(8):729–736. doi:10.1038/ni.2352.
  • Sato S, Kaneto S, Shibata N, Takahashi Y, Okura H, Yuki Y, et al. Transcription factor Spi-B-dependent and -independent pathways for the development of Peyer’s patch M cells. Mucosal Immunol. 2013 Jul;6(4):838–846. doi:10.1038/mi.2012.122.
  • Ouzilou L, Caliot E, Pelletier I, Prévost M-C, Pringault E, Colbère-Garapin F. Poliovirus transcytosis through M-like cells. J Gen Virol. 2002;83(9):2177–2182. doi:10.1099/0022-1317-83-9-2177.
  • Jones BD, Ghori N, Falkow S. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer’s patches. J Exp Med. 1994;180:15–23.
  • Schulte R, Kerneis S, Klinke S, Bartels H, Preger S, Kraehenbuhl J-P, Pringault E, Autenrieth IB. Translocation of Yersinia enterocolitica across reconstituted intestinal epithelial monolayers is triggered by Yersinia invasin binding to β1 integrins apically expressed on M-like cells. Cell Microbiol. 2000;2(2):173–185. doi:10.1046/j.1462-5822.2000.00047.x.
  • Tahoun A, Mahajan S, Paxton E, Malterer G, Donaldson DS, Wang D, Tan A, Gillespie TL, O’Shea M, Roe AJ, et al. Salmonella transforms follicle-associated epithelial cells into M cells to promote intestinal invasion. Cell Host Microbe. 2012;12(5):645–656. doi:10.1016/j.chom.2012.10.009.
  • Grassl GA, Bohn E, Müller Y, Bühler OT, Autenrieth IB. Interaction of Yersinia enterocolitica with epithelial cells: invasin beyond invasion. Int J Med Microbiol. 2003;293(1):41–54. doi:10.1078/1438-4221-00243.
  • Clark MA, Jepson MA. Intestinal M cells and their role in bacterial infection. Int J Med Microbiol. 2003;293(1):17–39. doi:10.1078/1438-4221-00242.
  • Calderone RA, Clancy CJ. Candida and candidiasis. American Society for Microbiology Press. 2002; 8(8): 876.
  • Whiteway M, Bachewich C. Morphogenesis in Candida albicans. Annu Rev Microbiol. 2007;61:529–553. doi:10.1146/annurev.micro.61.080706.093341.
  • Navarathna DH, Pathirana RU, Lionakis MS, Nickerson KW, Roberts DD. Candida albicans ISW2 regulates chlamydospore suspensor cell formation and virulence in vivo in a mouse model of disseminated candidiasis. PLoS One. 2016;11(10):e0164449. doi:10.1371/journal.pone.0164449.
  • Slutsky B, Staebell M, Anderson J, Risen L, Pfaller MT, Soll DR. “White-opaque transition”: a second high-frequency switching system in Candida albicans. J Bacteriol. 1987;169:189–197.
  • Ene IV, Lohse MB, Vladu AV, Morschhäuser J, Johnson AD, Bennett RJ. Phenotypic profiling reveals that Candida albicans opaque cells represent a metabolically specialized cell state compared to default white cells. MBio. 2016;7(6):e01269–16. doi:10.1128/mBio.01269-16.
  • Lachke SA, Lockhart SR, Daniels KJ, Soll DR. Skin facilitates Candida albicans mating. Infect Immun. 2003;71(9):4970–4976. doi:10.1128/IAI.71.9.4970-4976.2003.
  • Lohse MB, Johnson AD. Differential phagocytosis of white versus opaque Candida albicans by Drosophila and mouse phagocytes. PLoS One. 2008;3(1):e1473. doi:10.1371/journal.pone.0001473.
  • Lohse MB, Johnson AD. White–opaque switching in Candida albicans. Curr Opin Microbiol. 2009;12(6):650–654. doi:10.1016/j.mib.2009.09.010.
  • Morschhäuser J. Regulation of white-opaque switching in Candida albicans. Med Microbiol Immunol (Berl). 2010;199(3):165–172. doi:10.1007/s00430-010-0147-0.
  • Miller MG, Johnson AD. White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell. 2002;110:293–302.
  • Mallick EM, Bergeron AC, Jones Jr SK, Newman ZR, Brothers KM, Creton R, Wheeler RT, Bennett RJ. Phenotypic plasticity regulates Candida albicans interactions and virulence in the vertebrate host. Front Microbiol. 2016;7:780. doi:10.3389/fmicb.2016.00780.
  • van Burik J-AH, Magee PT. Aspects of fungal pathogenesis in humans. Annu Rev Microbiol. 2001;55(1):743–772. doi:10.1146/annurev.micro.55.1.743.
  • Pande K, Chen C, Noble SM. Passage through the mammalian gut triggers a phenotypic switch that promotes Candida albicans commensalism. Nat Genet. 2013 Sep;45(9):1088–1091. doi:10.1038/ng.2710.
  • Huang G, Wang H, Chou S, Nie X, Chen J, Liu H. Bistable expression of WOR1, a master regulator of white–opaque switching in Candida albicans. Proc Natl Acad Sci. 2006;103(34):12813–12818. doi:10.1073/pnas.0605270103.
  • Srikantha T, Borneman AR, Daniels KJ, Pujol C, Wu W, Seringhaus MR, Gerstein M, Yi S, Snyder M, Soll DR. TOS9 regulates white-opaque switching in Candida albicans. Eukaryot Cell. 2006;5(10):1674–1687. doi:10.1128/EC.00252-06.
  • Zordan RE, Galgoczy DJ, Johnson AD. Epigenetic properties of white–opaque switching in Candida albicans are based on a self-sustaining transcriptional feedback loop. Proc Natl Acad Sci. 2006;103(34):12807–12812. doi:10.1073/pnas.0605138103.
  • Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, Strom SP, Brown J, Becker CA, Fleshner PR, Dubinsky M, et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science. 2012 Jun 8;336(6086):1314–1317. doi:10.1126/science.1221789.
  • Neville BA, d’Enfert C, Bougnoux M-E. Candida albicans commensalism in the gastrointestinal tract. FEMS Yeast Res. 2015;15:7.
  • Fox EP, Cowley ES, Nobile CJ, Hartooni N, Newman DK, Johnson AD. Anaerobic Bacteria Grow within Candida albicans Biofilms and Induce Biofilm Formation in Suspension Cultures. Curr Biol. 2014 Oct 20;24(20):2411–2416. doi:10.1016/j.cub.2014.08.057.
  • Wang ZK, Yang YS, Stefka AT, Sun G, Peng LH. Review article: fungal microbiota and digestive diseases. Aliment Pharmacol Ther. 2014;39(8):751–766. doi:10.1111/apt.12665.
  • Noverr MC, Huffnagle GB. Regulation of Candida albicans Morphogenesis by Fatty Acid Metabolites. Infect Immun. 2004 Nov 1;72(11):6206–6210. doi:10.1128/IAI.72.11.6206-6210.2004.
  • García C, Tebbji F, Daigneault M, Liu N-N, Köhler JR, Allen-Vercoe E, Sellam A. The Human Gut Microbial Metabolome Modulates Fungal Growth via the TOR Signaling Pathway. mSphere. 2017 Dec;2(6)pii: e00555-17.
  • Fitzsimmons N, Berry DR. Inhibition of Candida albicans by Lactobacillus acidophilus: evidence for the involvement of a peroxidase system. Microbios. 1994;80:125–133.
  • Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G, Pieraccini G, Zecchi R, D’Angelo C, Massi-Benedetti C, Fallarino F, et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity. 2013;39(2):372–385. doi:10.1016/j.immuni.2013.05.019.
  • De Luca A, Zelante T, D’angelo C, Zagarella S, Fallarino F, Spreca A, Iannitti RG, Bonifazi P, Renauld JC, Bistoni F. IL-22 defines a novel immune pathway of antifungal resistance. Mucosal Immunol. 2010;3(4):361. doi:10.1038/mi.2009.138.
  • Puel A, Picard C, Cypowyj S, Lilic D, Abel L, Casanova J-L. Inborn errors of mucocutaneous immunity to Candida albicans in humans: a role for IL-17 cytokines?. Curr Opin Immunol. 2010 Aug 1;22(4):467–474. doi:10.1016/j.coi.2010.06.009.
  • Rosenbach A, Dignard D, Pierce JV, Whiteway M, Kumamoto CA. Adaptations of Candida albicans for growth in the mammalian intestinal tract. Eukaryot Cell. 2010;9(7):1075–1086. doi:10.1128/EC.00011-10.
  • White SJ, Rosenbach A, Lephart P, Nguyen D, Benjamin A, Tzipori S, Whiteway M, Mecsas J, Kumamoto CA. Self-regulation of Candida albicans population size during GI colonization. PLoS Pathog. 2007;3(12):e184. doi:10.1371/journal.ppat.0030184.
  • Savage DC. Microbial interference between indigenous yeast and lactobacilli in the rodent stomach. J Bacteriol. 1969;98:1278–1283.
  • Helstrom PB, Balish E. Effect of oral tetracycline, the microbial flora, and the athymic state on gastrointestinal colonization and infection of BALB/c mice with Candida albicans. Infect Immun. 1979;23:764–774.
  • Hummel RP, Oestreicher EJ, Maley MP, Macmillan BG. Inhibition ofCandida albicans by Escherichia coli in vitro and in the germfree mouse. J Surg Res. 1973;15(1):53–58. doi:10.1016/0022-4804(73)90163-7.
  • Zwielehner J, Lassl C, Hippe B, Pointner A, Switzeny OJ, Remely M, Kitzweger E, Ruckser R, Haslberger AG. Changes in human fecal microbiota due to chemotherapy analyzed by TaqMan-PCR, 454 sequencing and PCR-DGGE fingerprinting. PLoS One. 2011;6(12):e28654. doi:10.1371/journal.pone.0028654.
  • Stringer AM, Gibson RJ, Bowen JM, Keefe DM. Chemotherapy-induced modifications to gastrointestinal microflora: evidence and implications of change. Curr Drug Metab. 2009;10(1):79–83. doi:10.2174/138920009787048419.
  • Fan D, Coughlin LA, Neubauer MM, Kim J, Kim MS, Zhan X, Simms-Waldrip TR, Xie Y, Hooper LV, Koh AY. Activation of HIF-1α and LL-37 by commensal bacteria inhibits Candida albicans colonization. Nat Med. 2015;21(7):808. doi:10.1038/nm.3871.
  • Li J, Chen D, Yu B, He J, Zheng P, Mao X, Yu J, Luo J, Tian G, Huang Z, et al. Fungi in Gastrointestinal Tracts of Human and Mice: from Community to Functions. Microb Ecol. 2018 May;75(4):821–829. doi:10.1007/s00248-017-1122-8.
  • Swidergall M, Ernst JF. Interplay between Candida albicans and the antimicrobial peptide armory. Eukaryot Cell. 2014 Jun 20;EC: 00093-14.
  • Chairatana P, Chiang I-L, Nolan EM. Human α-Defensin 6 Self-Assembly Prevents Adhesion and Suppresses Virulence Traits of Candida albicans. Biochemistry. 2017 28;56(8):1033–1041. doi:10.1021/acs.biochem.6b01111.
  • Vandamme D, Landuyt B, Luyten W, Schoofs L. A comprehensive summary of LL-37, the factotum human cathelicidin peptide. Cell Immunol. 2012 Nov;280(1):22–35. doi:10.1016/j.cellimm.2012.11.009.
  • Selsted ME, Ouellette AJ. Mammalian defensins in the antimicrobial immune response. Nat Immunol. 2005 Jun;6(6):551–557. doi:10.1038/ni1206.
  • Moyes DL, Runglall M, Murciano C, Shen C, Nayar D, Thavaraj S, Kohli A, Islam A, Mora-Montes H, Challacombe SJ, et al. A Biphasic Innate Immune MAPK Response Discriminates between the Yeast and Hyphal Forms of Candida albicans in Epithelial Cells. Cell Host Microbe. 2010 Sep 16;8(3):225–235. doi:10.1016/j.chom.2010.08.002.
  • Swidergall M, Ernst AM, Ernst JF. Candida albicans mucin Msb2 is a broad-range protectant against antimicrobial peptides. Antimicrob Agents Chemother. 2013 Jun 3;AAC: 00862-13.
  • Meiller TF, Hube B, Schild L, Shirtliff ME, Scheper MA, Winkler R, Ton A. A novel immune evasion strategy of Candida albicans: proteolytic cleavage of a salivary antimicrobial peptide. PLoS One. 2009;4(4):e5039. doi:10.1371/journal.pone.0005039.
  • Puri S, Kumar R, Chadha S, Tati S, Conti HR, Hube B, Cullen PJ, Edgerton M. Secreted aspartic protease cleavage of Candida albicans Msb2 activates Cek1 MAPK signaling affecting biofilm formation and oropharyngeal candidiasis. PLoS One. 2012;7(11):e46020. doi:10.1371/journal.pone.0046020.
  • Szafranski-Schneider E, Swidergall M, Cottier F, Tielker D, Román E, Pla J, Ernst JF. Msb2 Shedding Protects Candida albicans against Antimicrobial Peptides. PLoS Pathog [Internet], 2012 Feb 2 [cited 2019 Jan 10];8(2). https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3271078/.
  • Argimón S, Fanning S, Blankenship JR, Mitchell AP. Interaction between the Candida albicans High-Osmolarity Glycerol (HOG) Pathway and the Response to Human β-Defensins 2 and 3. Eukaryot Cell. 2011 Feb;10(2):272–275. doi:10.1128/EC.00303-10.
  • Jung S-I, Finkel JS, Solis NV, Chaili S, Mitchell AP, Yeaman MR, Filler SG. Bcr1 Functions Downstream of Ssd1 To Mediate Antimicrobial Peptide Resistance in Candida albicans. Eukaryot Cell. 2013 Mar;12(3):411–419. doi:10.1128/EC.00285-12.
  • Lis M, Liu TT, Barker KS, Rogers PD, Bobek LA. Antimicrobial peptide MUC7 12-mer activates the calcium/calcineurin pathway in Candida albicans. FEMS Yeast Res. 2010 Aug 1;10(5):579–586.
  • Li R, Kumar R, Tati S, Puri S, Edgerton MC. albicans Flu1 mediated efflux of salivary Histatin 5 reduces its cytosolic concentration and fungicidal activity. Antimicrob Agents Chemother. 2013;57(4):1832–1839.
  • Rapala-Kozik M, Bochenska O, Zawrotniak M, Wolak N, Trebacz G, Gogol M, Ostrowska D, Aoki W, Ueda M, Kozik A. Inactivation of the Antifungal and Immunomodulatory Properties of Human Cathelicidin LL-37 by Aspartic Proteases Produced by the Pathogenic Yeast Candida albicans. Infect Immun. 2015 Jun;83(6):2518–2530. doi:10.1128/IAI.00023-15.
  • Alonso-Monge R, Carvaihlo S, Nombela C, Rial E, Pla J. The Hog1 MAP kinase controls respiratory metabolism in the fungal pathogen Candida albicans. Microbiology. 2009;155(2):413–423. doi:10.1099/mic.0.023309-0.
  • Vylkova S, Jang WS, Li W, Nayyar N, Edgerton M. Histatin 5 initiates osmotic stress response in Candida albicans via activation of the Hog1 mitogen-activated protein kinase pathway. Eukaryot Cell. 2007;6(10):1876–1888. doi:10.1128/EC.00039-07.
  • Ostaff MJ, Stange EF, Wehkamp J. Antimicrobial peptides and gut microbiota in homeostasis and pathology. EMBO Mol Med. 2013 Oct;5(10):1465–1483. doi:10.1002/emmm.201201876.
  • Böhringer M, Pohlers S, Schulze S, Albrecht-Eckardt D, Piegsa J, Weber M, Martin R, Hünniger K, Linde J, Guthke R, et al. Candida albicans infection leads to barrier breakdown and a MAPK/NF-κB mediated stress response in the intestinal epithelial cell line C2BBe1. Cell Microbiol. 2016;18(7):889–904.
  • Moyes DL, Shen C, Murciano C, Runglall M, Richardson JP, Arno M Aldecoa-Otalora E, Naglik JR. Protection Against Epithelial Damage During Candida albicans Infection Is Mediated by PI3K/Akt and Mammalian Target of Rapamycin Signaling. J Infect Dis. 2014 Jun 1;209(11):1816–1826. doi:10.1093/infdis/jit541.
  • Allert S, Förster TM, Svensson C-M, Richardson JP, Pawlik T, Hebecker B, Rudolphi S, Juraschitz M, Schaller M, Blagojevic M, et al. Candida albicans-Induced Epithelial Damage Mediates Translocation through Intestinal Barriers. mBio. 2018 May 7;9(3):e00915–18. doi:10.1128/mBio.00915-18.
  • Kavanaugh NL, Zhang AQ, Nobile CJ, Johnson AD, Ribbeck K. Mucins Suppress Virulence Traits of Candida albicans. mBio. 2014 Dec 31;5(6):e01911–14. doi:10.1128/mBio.01911-14.
  • Prieto D, Correia I, Pla J, Román E. Adaptation of Candida albicans to commensalism in the gut. Future Microbiol. 2016 Apr 1;11(4):567–583. doi:10.2217/fmb.16.1.
  • Repentigny L, De, Aumont F, Bernard K, Belhumeur P. Characterization of Binding of Candida albicans to Small Intestinal Mucin and Its Role in Adherence to Mucosal Epithelial Cells. Infect Immun. 2000 Jan 6;68(6):3172–3179. doi:10.1128/IAI.68.6.3172-3179.2000.
  • Böhm L, Torsin S, Tint SH, Eckstein MT, Ludwig T, Pérez JC. The yeast form of the fungus Candida albicans promotes persistence in the gut of gnotobiotic mice. PLoS Pathog [Internet]. 2017 Oct 25 [cited 2018 Jul 17];13(10). https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5673237/.
  • Colina AR, Aumont F, Deslauriers N, Belhumeur P, Repentigny LD. Evidence for degradation of gastrointestinal mucin by Candida albicans secretory aspartyl proteinase. Infect Immun. 1996 Jan 11;64(11):4514–4519.
  • Crowther RS, Roomi NW, Fahim RE, Forstner JF. Vibrio cholerae metalloproteinase degrades intestinal mucin and facilitates enterotoxin-induced secretion from rat intestine. Biochim Biophys Acta BBA-Gen Subj. 1987;924(3):393–402. doi:10.1016/0304-4165(87)90153-X.
  • Mantle M, Husar SD. Adhesion of Yersinia enterocolitica to purified rabbit and human intestinal mucin. Infect Immun. 1993;61:2340–2346.
  • Roberton AM, Stanley RA. In vitro utilization of mucin by Bacteroides fragilis. Appl Environ Microbiol. 1982;43:325–330.
  • Slomiany BL, Murty VLN, Piotrowski J, Liau YH, Sundaram P, Slomiany A. Glycosulfatase activity of Helicobacter pylori toward gastric mucin. Biochem Biophys Res Commun. 1992;183:506–513.
  • Yang Y-L. Virulence factors of Candida species. J Microbiol Immunol Infect. 2003;36:223–228.
  • Modrzewska B, Kurnatowski P. Adherence of Candida sp. to host tissues and cells as one of its pathogenicity features. Ann Parasitol. 2015;61:1.
  • Falgier C, Kegley S, Podgorski H, Heisel T, Storey K, Bendel CM, Gale CA. Candida species differ in their interactions with immature human gastrointestinal epithelial cells. Pediatr Res. 2011 May;69(5 Pt 1):384–389. doi:10.1203/PDR.0b013e31821269d5.
  • Richardson JP, Ho J, Naglik JR. Candida–epithelial Interactions. J Fungi. 2018;4(1):22. doi:10.3390/jof4010022.
  • Zakikhany K, Naglik JR, Schmidt-Westhausen A, Holland G, Schaller M, Hube B. In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell Microbiol. 2007 Dec;9(12):2938–2954. doi:10.1111/j.1462-5822.2007.01009.x.
  • Phan QT, Myers CL, Fu Y, Sheppard DC, Yeaman MR, Welch WH, Ibrahim AS, Edwards JE Jr, Filler SG. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 2007 Mar;5(3):e64. doi:10.1371/journal.pbio.0050064.
  • Ponniah G, Rollenhagen C, Bahn Y-S, Staab JF, Sundstrom P. State of differentiation defines buccal epithelial cell affinity for cross-linking to Candida albicans Hwp1. J Oral Pathol Med. 2007;36(8):456–467. doi:10.1111/j.1600-0714.2007.00565.x.
  • Wiesner SM, Bendel CM, Hess DJ, Erlandsen SL, Wells CL. Adherence of yeast and filamentous forms of Candida albicans to cultured enterocytes. Crit Care Med. 2002 Mar;30(3):677–683. doi:10.1097/00003246-200203000-00030.
  • Sohn K, Senyürek I, Fertey J, Königsdorfer A, Joffroy C, Hauser N, Zelt G, Brunner H, Rupp S. An in vitro assay to study the transcriptional response during adherence of Candida albicans to different human epithelia. FEMS Yeast Res. 2006;6(7):1085–1093. doi:10.1111/j.1567-1364.2006.00130.x.
  • Li X, Yan Z, Xu J. Quantitative variation of biofilms among strains in natural populations of Candida albicans. Microbiology. 2003;149(2):353–362. doi:10.1099/mic.0.25932-0.
  • Höfs S, Mogavero S, Hube B. Interaction of <Emphasis Type=“Italic”>Candida albicans</Emphasis> with host cells: virulence factors, host defense, escape strategies, and the microbiota. J Microbiol. 2016 Mar 1;54(3):149–169.
  • Kojic EM, Darouiche RO. Candida Infections of Medical Devices. Clin Microbiol Rev. 2004 Apr 1;17(2):255–267. doi:10.1128/CMR.17.2.255-267.2004.
  • Sundstrom P. Adhesins in Candida albicans. Curr Opin Microbiol. 1999;2(4):353–357. doi:10.1016/S1369-5274(99)80044-7.
  • de Groot PWJ, Bader O, de Boer AD, Weig M, Chauhan N. Adhesins in human fungal pathogens: glue with plenty of stick. Eukaryot Cell. 2013 Apr;12(4):470–481. doi:10.1128/EC.00364-12.
  • Hebecker B, Naglik JR, Hube B, Jacobsen ID. Pathogenicity mechanisms and host response during oral Candida albicans infections. Expert Rev Anti Infect Ther. 2014;12(7):867–879. doi:10.1586/14787210.2014.916210.
  • Chaffin WL. Candida albicans cell wall proteins. Microbiol Mol Biol Rev. 2008;72(3):495–544. doi:10.1128/MMBR.00032-07.
  • Younes S, Bahnan W, Dimassi HI, Khalaf RA. The Candida albicans Hwp2 is necessary for proper adhesion, biofilm formation and oxidative stress tolerance. Microbiol Res. 2011;166(5):430–436. doi:10.1016/j.micres.2010.08.004.
  • Sandini S, La Valle R, De Bernardis F, Macrì C, Cassone A. The 65 kDa mannoprotein gene of Candida albicans encodes a putative β-glucanase adhesin required for hyphal morphogenesis and experimental pathogenicity. Cell Microbiol. 2007;9(5):1223–1238. doi:10.1111/j.1462-5822.2006.00862.x.
  • Sandini S, Stringaro A, Arancia S, Colone M, Mondello F, Murtas S, Girolamo A, Mastrangelo N, Bernardis FD. The MP65 gene is required for cell wall integrity, adherence to epithelial cells and biofilm formation in Candida albicans. BMC Microbiol. 2011;11(1):106. doi:10.1186/1471-2180-11-106.
  • De Bernardis F, Liu H, O’Mahony R, La Valle R, Bartollino S, Sandini S, Grant S, Brewis N, Tomlinson I, Basset RC, et al. Human domain antibodies against virulence traits of Candida albicans inhibit fungus adherence to vaginal epithelium and protect against experimental vaginal candidiasis. J Infect Dis. 2007 Jan 1;195(1):149–157. doi:10.1086/509891.
  • Gil-Bona A, Amador-García A, Gil C, Monteoliva L. The external face of Candida albicans: A proteomic view of the cell surface and the extracellular environment. J Proteomics. 2018 May;30(180):70–79. doi:10.1016/j.jprot.2017.12.002.
  • Timpel C, Strahl-Bolsinger S, Ziegelbauer K, Ernst JF. Multiple Functions of Pmt1p-mediated ProteinO-Mannosylation in the Fungal Pathogen Candida albicans. J Biol Chem. 1998;273(33):20837–20846. doi:10.1074/jbc.273.33.20837.
  • Dalle F, Jouault T, Trinel PA, Esnault J, Mallet JM, d’Athis P, Poulain D, Bonnin A. Beta-1,2- and alpha-1,2-linked oligomannosides mediate adherence of Candida albicans blastospores to human enterocytes in vitro. Infect Immun. 2003 Dec;71(12):7061–7068. doi:10.1128/IAI.71.12.7061-7068.2003.
  • Lindberg B, Leontein K, Lindquist U, Svenson SB, Wrangsell G, Dell A, Rogers M. Structural studies of the O-antigen polysaccharide of Salmonella thompson, serogroup C1 (6, 7). Carbohydr Res. 1988;174:313–322. doi:10.1016/0008-6215(88)85100-0.
  • Oxley D, Wilkinson SG. Structure of a mannan isolated from the lipopolysaccharide of the reference strain (S3255) for a new serogroup of Serratia marcescens. Carbohydr Res. 1991;212:213–217. doi:10.1016/0008-6215(91)84058-M.
  • Poulain D, Jouault T. Candida albicans cell wall glycans, host receptors and responses: elements for a decisive crosstalk. Curr Opin Microbiol. 2004;7(4):342–349. doi:10.1016/j.mib.2004.06.011.
  • Masuoka J. Surface glycans of Candida albicans and other pathogenic fungi: physiological roles, clinical uses, and experimental challenges. Clin Microbiol Rev. 2004;17(2):281–310. doi:10.1128/CMR.17.2.281-310.2004.
  • Dromer F, Chevalier R, Sendid B, Improvisi L, Jouault T, Robert R, Mallet JM, Poulain D. Synthetic analogues of β-1, 2 oligomannosides prevent intestinal colonization by the pathogenic yeast Candida albicans. Antimicrob Agents Chemother. 2002;46(12):3869–3876. doi:10.1128/AAC.46.12.3869-3876.2002.
  • Wächtler B, Citiulo F, Jablonowski N, Förster S, Dalle F, Schaller M, Wilson D, Hube B. Candida albicans-Epithelial Interactions: dissecting the Roles of Active Penetration, Induced Endocytosis and Host Factors on the Infection Process. PLoS ONE [Internet], 2012 May 14 [cited 2015 Nov 10];7(5). http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3351431/.
  • Santoni G, Spreghini E, Lucciarini R, Amantini C, Piccoli M. Involvement of αvβ3 integrin-like receptor and glycosaminoglycans in Candida albicans germ tube adhesion to vitronectin and to a human endothelial cell line. Microb Pathog. 2001;31(4):159–172. doi:10.1006/mpat.2001.0459.
  • Wächtler B, Wilson D, Haedicke K, Dalle F, Hube B. From Attachment to Damage: defined Genes of Candida albicans Mediate Adhesion, Invasion and Damage during Interaction with Oral Epithelial Cells. PLoS ONE [Internet]. 2011 Feb 23 [cited 2015 Nov 10];6(2). http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3044159/.
  • Park H, Myers CL, Sheppard DC, Phan QT, Sanchez AA, E Edwards J, Filler SG. Role of the fungal Ras-protein kinase A pathway in governing epithelial cell interactions during oropharyngeal candidiasis. Cell Microbiol. 2005;7(4):499–510.
  • Felk A, Kretschmar M, Albrecht A, Schaller M, Beinhauer S, Nichterlein T, Sanglard D, Korting HC, Schäfer W, Hube B. Candida albicans hyphal formation and the expression of the Efg1-regulated proteinases Sap4 to Sap6 are required for the invasion of parenchymal organs. Infect Immun. 2002;70(7):3689–3700. doi:10.1128/IAI.70.7.3689-3700.2002.
  • Gow NA, Brown AJ, Odds FC. Fungal morphogenesis and host invasion. Curr Opin Microbiol. 2002;5:366–371.
  • Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev. 2003;67(3):400–428. doi:10.1128/MMBR.67.3.400-428.2003.
  • Villar CC, Zhao XR. Candida albicans induces early apoptosis followed by secondary necrosis in oral epithelial cells. Mol Oral Microbiol. 2010;25(3):215–225. doi:10.1111/j.2041-1014.2010.00577.x.
  • Villar CC, Kashleva H, Nobile CJ, Mitchell AP, Dongari-Bagtzoglou A. Mucosal tissue invasion by Candida albicans is associated with E-cadherin degradation, mediated by transcription factor Rim101p and protease Sap5p. Infect Immun. 2007 May;75(5):2126–2135. doi:10.1128/IAI.00076-06.
  • Moreno-Ruiz E, Galán-Díez M, Zhu W, Fernández-Ruiz E, d’Enfert C, Filler SG, Cossart P, Veiga E. Candida albicans internalization by host cells is mediated by a clathrin-dependent mechanism. Cell Microbiol. 2009;11(8):1179–1189. doi:10.1111/j.1462-5822.2009.01319.x.
  • Filler SG, Swerdloff JN, Hobbs C, Luckett PM. Penetration and damage of endothelial cells by Candida albicans. Infect Immun. 1995;63:976–983.
  • Sun JN, Solis NV, Phan QT, Bajwa JS, Kashleva H, Thompson A, Liu Y, Dongari-Bagtzoglou A, Edgerton M, Filler SG. Host cell invasion and virulence mediated by Candida albicans Ssa1. PLoS Pathog. 2010 Nov 11;6(11):e1001181. doi:10.1371/journal.ppat.1000975.
  • Phan QT, Fratti RA, Prasadarao NV, Edwards JE, Filler SG. N-cadherin mediates endocytosis of Candida albicans by endothelial cells. J Biol Chem. 2005;280(11):10455–10461. doi:10.1074/jbc.M412592200.
  • Zhu W, Phan QT, Boontheung P, Solis NV, Loo JA, Filler SG. EGFR and HER2 receptor kinase signaling mediate epithelial cell invasion by Candida albicans during oropharyngeal infection. Proc Natl Acad Sci U S A. 2012 Aug 28;109(35):14194–14199. doi:10.1073/pnas.1117676109.
  • Moyes DL, Richardson JP, Naglik JR. Candida albicans-epithelial interactions and pathogenicity mechanisms: scratching the surface. Virulence. 2015 May 19;6(4):338–346. doi:10.1080/21505594.2015.1010982.
  • Rollenhagen C, Wöllert T, Langford GM, Sundstrom P. Stimulation of cell motility and expression of late markers of differentiation in human oral keratinocytes by Candida albicans. Cell Microbiol. 2009 Jun;11(6):946–966. doi:10.1111/j.1462-5822.2009.01303.x.
  • Frank CF, Hostetter MK. Cleavage of E-cadherin: a mechanism for disruption of the intestinal epithelial barrier by Candida albicans. Transl Res J Lab Clin Med. 2007 Apr;149(4):211–222. doi:10.1016/j.trsl.2006.11.006.
  • Gumbiner BM. Cell Adhesion: the Molecular Basis of Tissue Architecture and Morphogenesis. Cell. 1996 Feb 9;84(3):345–357. doi:10.1016/S0092-8674(00)81279-9.
  • Banan A, Choudhary S, Zhang Y, Fields JZ, Keshavarzian A. Ethanol-induced barrier dysfunction and its prevention by growth factors in human intestinal monolayers: evidence for oxidative and cytoskeletal mechanisms. J Pharmacol Exp Ther. 1999;291:1075–1085.
  • Muskett H, Shahin J, Eyres G, Harvey S, Rowan K, Harrison D. Risk factors for invasive fungal disease in critically ill adult patients: a systematic review. Crit Care. 2011;15(6):R287. doi:10.1186/cc10324.
  • Ortega M, Marco F, Soriano A, Almela M, Martínez JA, López J, Pitart C, Mensa J. Candida species bloodstream infection: epidemiology and outcome in a single institution from 1991 to 2008. J Hosp Infect. 2011;77(2):157–161. doi:10.1016/j.jhin.2010.09.026.
  • Moyes DL, Wilson D, Richardson JP, Mogavero S, Tang SX, Wernecke J, Höfs S, Gratacap RL, Robbins J, Runglall M, et al. Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature. 2016;532(7597):64–68. doi:10.1038/nature17625.
  • Wilson D, Naglik JR, Hube B. The Missing Link between Candida albicans Hyphal Morphogenesis and Host Cell Damage. PLoS Pathog. 2016 Oct;12(10):e1005867. doi:10.1371/journal.ppat.1005867.
  • Casadevall A, Pirofski L. Microbiology: ditch the term pathogen. Nature. 2014 Dec 11;516(7530):165–166. doi:10.1038/516165a.
  • Kernéis S, Bogdanova A, Kraehenbuhl J-P, Pringault E. Conversion by Peyer’s patch lymphocytes of human enterocytes into M cells that transport bacteria. Science. 1997;277(5328):949–952. doi:10.1126/science.277.5328.949.
  • Gullberg E, Leonard M, Karlsson J, Hopkins AM, Brayden D, Baird AW, Artursson P. Expression of specific markers and particle transport in a new human intestinal M-cell model. Biochem Biophys Res Commun. 2000;279(3):808–813. doi:10.1006/bbrc.2000.4038.
  • Des Rieux A, Fievez V, Théate I, Mast J, Préat V, Schneider Y-J. An improved in vitro model of human intestinal follicle-associated epithelium to study nanoparticle transport by M cells. Eur J Pharm Sci. 2007;30(5):380–391. doi:10.1016/j.ejps.2006.12.006.
  • Hector RF, Yee E, Collins MS. Use of DBA/2N mice in models of systemic candidiasis and pulmonary and systemic aspergillosis. Infect Immun. 1990 May;58(5):1476–1478.
  • Papadimitriou JM, Ashman RB. The pathogenesis of acute systemic candidiasis in a susceptible inbred mouse strain. J Pathol. 1986;150(4):257–265. doi:10.1002/path.1711500408.
  • MacCallum Donna M, Odds Frank C. Temporal events in the intravenous challenge model for experimental Candida albicans infections in female mice. Mycoses. 2005 Apr 13;48(3):151–161. doi:10.1111/myc.2005.48.issue-3.
  • Spellberg B, Ibrahim AS, Edwards Jr. JE, Filler SG. Mice with Disseminated Candidiasis Die of Progressive Sepsis. J Infect Dis. 2005 Jul 15;192(2):336–343. doi:10.1086/jid.2005.192.issue-2.
  • Samonis G, Anaissie EJ, Rosenbaum B, Bodey GP. A model of sustained gastrointestinal colonization by Candida albicans in healthy adult mice. Infect Immun. 1990 Jan 6;58(6):1514–1517.
  • Clemons KV, Gonzalez GM, Singh G, Imai J, Espiritu M, Parmar R, Stevens DA. Development of an Orogastrointestinal Mucosal Model of Candidiasis with Dissemination to Visceral Organs. Antimicrob Agents Chemother. 2006 Jan 8;50(8):2650–2657. doi:10.1128/AAC.00530-06.
  • Koh AY, Köhler JR, Coggshall KT, Van Rooijen N, Pier GB. Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog. 2008 Feb 8;4(2):e35. doi:10.1371/journal.ppat.0040035.
  • Biasoli MS, Tosello ME, Luque AG, Magaró HM. Adherence, colonization and dissemination of Candida dubliniensis and other Candida species. Med Mycol. 2010 Mar 1;48(2):291–297. doi:10.3109/13693780903114942.
  • de Repentigny L. Animal models in the analysis of Candida host–pathogen interactions. Curr Opin Microbiol. 2004;7(4):324–329. doi:10.1016/j.mib.2004.06.001.
  • Oswald IP. Role of intestinal epithelial cells in the innate immune defence of the pig intestine. Vet Res. 2006;37(3):359–368. doi:10.1051/vetres:2006006.
  • Förster TM, Mogavero S, Dräger A, Graf K, Polke M, Jacobsen ID, Hube B. Enemies and brothers in arms: candida albicans and gram-positive bacteria. Cell Microbiol. 2016 Dec 1;18(12):1709–1715. doi:10.1111/cmi.12570.