Gut fungal microbiota: The Yin and Yang of inflammatory bowel disease

Inflammatory Bowel Diseases

Volumn 21, Issue 3, 2015, Pages 656-665

  Richard, Mathias L ^a,b   Lamas, Bruno ^b,c   Liguori, Giuseppina ^d   Hoffmann, Thomas W ^a,b   Sokol, Harry ^a,b,c,e  

^a UMR1319 MICALIS   (France)

^b HÔPITAL SAINT ANTOINE   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITY OF BOLOGNA   (Italy)

^e ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

Author keywords

fungi; inflammatory bowel disease; microbiota

Indexed keywords

CHINESE MEDICINE; FUNGUS; FUNGUS IMMUNITY; GUT FUNGAL MICROBIOTA; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; MICROBIAL DIVERSITY; MICROBIAL POPULATION DYNAMICS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES BOULARDII; ANIMAL; GASTROINTESTINAL TRACT; IMMUNOLOGY; MICROBIOLOGY; MICROFLORA;

ANIMALS; FUNGI; GASTROINTESTINAL TRACT; HUMANS; INFLAMMATORY BOWEL DISEASES; MICROBIOTA;

EID: 84923468750     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000261     Document Type: Review

References (78)

1. Khor B, Gardet A, Xavier RJ. Genetics and pathogenesis of inflammatory bowel disease. Nature. 2011; 474: 307-317.
2. Manichanh C, Borruel N, Casellas F, et al. The gut microbiota in IBD. Nat Rev Gastroenterol Hepatol. 2012; 9: 599-608.
3. Sokol H, Seksik P, Furet JP, et al. Low counts of faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis. 2009; 15: 1183-1189.
4. Willing BP, Dicksved J, Halfvarson J, et al. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology. 2010; 139: 1844-1854. e1841.
5. Sommer F, Backhed F. The gut microbiota: masters of host development and physiology. Nat Rev Microbiol. 2013; 11: 227-238.
6. Bultman SJ. Emerging roles of the microbiome in cancer. Carcinogenesis. 2014; 35: 249-255.
7. Martin R, Miquel S, Langella P, et al. The role of metagenomics in understanding the human microbiome in health and disease. Virulence. 2014; 5: 413-423.
8. Montiel-Castro AJ, Gonzalez-Cervantes RM, et al. The microbiota-gut-brain axis: neurobehavioral correlates, health and sociality. Front Integr Neurosci. 2013; 7: 70.
9. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010; 464: 59-65.
10. Huffnagle GB, Noverr MC. The emerging world of the fungal microbiome. Trends Microbiol. 2013; 21: 334-341.
11. Findley K, Oh J, Yang J, et al. Topographic diversity of fungal and bacterial communities in human skin. Nature. 2013; 498: 367-370.
12. Paulino LC, Tseng CH, Strober BE, et al. Molecular analysis of fungal microbiota in samples from healthy human skin and psoriatic lesions. J Clinical Microbiol. 2006; 44: 2933-2941.
13. Drell T, Lillsaar T, Tummeleht L, et al. Characterization of the vaginal micro-And mycobiome in asymptomatic reproductive-Age Estonian Women. PloS One. 2013; 8: e54379.
14. Zheng NN, Guo XC, Lv W, et al. Characterization of the vaginal fungal flora in pregnant diabetic women by 18S rRNA sequencing. Eur J Clin Microbiol Infect Dis. 2013; 32: 1031-1040.
15. Ghannoum MA, Jurevic RJ, Mukherjee PK, et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathogens. 2010; 6: e1000713.
16. Gouba N, Raoult D, Drancourt M. Plant and fungal diversity in gut microbiota as revealed by molecular and culture investigations. PLoS One. 2013; 8: e59474.
17. Schoch CL, Seifert KA, Huhndorf S, 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: 6241-6246.
18. Delhaes L, Monchy S, Frealle E, et al. The airway microbiota in cystic fibrosis: a complex fungal and bacterial community: implications for therapeutic management. PLoS One. 2012; 7: e36313.
19. Dollive S, Peterfreund GL, Sherrill-Mix S, et al. A tool kit for quantifying eukaryotic rRNA gene sequences from human microbiome samples. Genome Biol. 2012; 13: R60.
20. White JR, Maddox C, White O, et al. CloVR-ITS: automated internal transcribed spacer amplicon sequence analysis pipeline for the characterization of fungal microbiota. Microbiome. 2013; 1: 6.
21. Scanlan PD, Marchesi JR. Micro-eukaryotic diversity of the human distal gut microbiota: qualitative assessment using culture-dependent and-independent analysis of faeces. ISME J. 2008; 2: 1183-1193.
22. Kuhbacher T, Ott SJ, Helwig U, et al. Bacterial and fungal microbiota in relation to probiotic therapy (VSL#3) in pouchitis. Gut. 2006; 55: 833-841.
23. Chen Y, Chen Z, Guo R, et al. Correlation between gastrointestinal fungi and varying degrees of chronic hepatitis B virus infection. Diagn Microbiol Infect Dis. 2011; 70: 492-498.
24. Li Q, Wang C, Tang C, et al. Dysbiosis of gut fungal microbiota is associated with mucosal inflammation in Crohn's disease. J Clin Gastroenterol. 2013; 48: 513-523.
25. Li Q, Wang C, Zhang Q, et al. Use of 18S ribosomal DNA polymerase chain reaction-denaturing gradient gel electrophoresis to study composition of fungal community in 2 patients with intestinal transplants. Hum Pathol. 2012; 43: 1273-1281.
26. Ott SJ, Kuhbacher T, Musfeldt M, et al. Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand J Gastroenterol. 2008; 43: 831-841.
27. Pandey PK, Siddharth J, Verma P, et al. Molecular typing of fecal eukaryotic microbiota of human infants and their respective mothers. J Biosci. 2012; 37: 221-226.
28. Ukhanova M, Wang X, Baer DJ, et al. Effects of almond and pistachio consumption on gut microbiota composition in a randomised cross-over human feeding study. Br J Nutr. 2014; 111: 2146-2152.
29. von Rosenvinge EC, Song Y, White JR, et al. Immune status, antibiotic medication and pH are associated with changes in the stomach fluid microbiota. ISME J. 2013; 7: 1354-1366.
30. Hamad I, Sokhna C, Raoult D. Molecular detection of eukaryotes in a single human stool sample from Senegal. PloS One. 2012; 7: e40888.
31. Hoffmann C, Dollive S, Grunberg S, et al. Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PloS One. 2013; 8: e66019.
32. Mason KL, Erb Downward JR, Mason KD, et al. Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy. Infect Immun. 2012; 80: 3371-3380.
33. Garcia-Vidal C, Viasus D, Carratala J. Pathogenesis of invasive fungal infections. Curr Opin Infect Dis. 2013; 26: 270-276.
34. McKay AH, Forster H, Adaskaveg JE. Distinguishing galactomyces citriaurantii from G. geotrichum and characterizing population structure of the two postharvest sour rot pathogens of fruit crops in California. Phytopathology. 2012; 102: 528-538.
35. Waghmode TR, Kurade MB, Kabra A, et al. Biodegradation of Rubine GFL by Galactomyces geotrichum MTCC 1360 and subsequent toxicological analysis by using cytotoxicity, genotoxicity and oxidative stress studies. Microbiology. 2012; 158: 2344-2352.
36. Gaitanis G, Velegraki A, Mayser P, et al. Skin diseases associated with Malassezia yeasts: facts and controversies. Clin Dermatol. 2013; 31: 455-463.
37. Yang CS, Li DW. Ecology of fungi in the indoor environment. In: Yang CS, Heinsohn PA, eds. Sampling and Analysis of Indoor Microorganisms. Hoboken, NJ: John Wiley &Sons; 2007; 191-214.
38. Charlson ES, Diamond JM, Bittinger K, et al. Lung-enriched organisms and aberrant bacterial and fungal respiratory microbiota after lung transplant. Am J Respir Crit Care Med. 2012; 186: 536-545.
39. Scupham AJ, Presley LL, Wei B, et al. Abundant and diverse fungal microbiota in the murine intestine. Appl Environment Microbiol. 2006; 72: 793-801.
40. Dollive S, Chen YY, Grunberg S, et al. Fungi of the murine gut: episodic variation and proliferation during antibiotic treatment. PLoS One. 2013; 8: e71806.
41. Iliev ID, Funari VA, Taylor KD, et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science. 2012; 336: 1314-1317.
42. Sokol H, Seksik P. The intestinal microbiota in inflammatory bowel diseases: time to connect with the host. Curr Opin Gastroenterol. 2010; 26: 327-331.
43. Jostins L, Ripke S, Weersma RK, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012; 491: 119-124.
44. Morgan XC, Tickle TL, Sokol H, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012; 13: R79.
45. Sokol H, Lay C, Seksik P, et al. Analysis of bacterial bowel communities of IBD patients: what has it revealed. Inflamm Bowel Dis. 2008; 14: 858-867.
46. McKenzie H, Main J, Pennington C, et al. Antibody to selected strains of Saccharomyces cerevisiae (baker's and brewer's yeast) and Candida albicans in Crohn's disease. Gut. 1990; 31: 536-538.
47. Vermeire S, Peeters M, Vlietinck R, et al. Anti-saccharomyces cerevisiae antibodies (ASCA), phenotypes of IBD, and intestinal permeability: a study in IBD families. Inflamm Bowel Dis. 2001; 7: 8-15.
48. Quinton JF, Sendid B, Reumaux D, et al. Anti-saccharomyces cerevisiae mannan antibodies combined with antineutrophil cytoplasmic autoantibodies in inflammatory bowel disease: prevalence and diagnostic role. Gut. 1998; 42: 788-791.
49. Dotan I, Fishman S, Dgani Y, et al. Antibodies against laminaribioside and chitobioside are novel serologic markers in Crohn's disease. Gastroenterology. 2006; 131: 366-378.
50. Landers CJ, Cohavy O, Misra R, et al. Selected loss of tolerance evidenced by Crohn's disease-Associated immune responses to auto-And microbial antigens. Gastroenterology. 2002; 123: 689-699.
51. Sendid B, Quinton JF, Charrier G, et al. Anti-Saccharomyces cerevisiae mannan antibodies in familial Crohn's disease. Am J Gastroenterol. 1998; 93: 1306-1310.
52. Calich VL, Pina A, Felonato M, et al. Toll-like receptors and fungal infections: the role of TLR2, TLR4 and MyD88 in paracoccidioidomycosis. FEMS Immunol Med Microbiol. 2008; 53: 1-7.
53. Gross O, Gewies A, Finger K, et al. Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature. 2006; 442: 651-656.
54. Romani L. Immunity to fungal infections. Nat Rev Immunol. 2011; 11: 275-288.
55. Standaert-Vitse A, Sendid B, Joossens M, et al. Candida albicans colonization and ASCA in familial Crohn's disease. Am J Gastroenterol. 2009; 104: 1745-1753.
56. Zwolinska-Wcislo M, Brzozowski T, Budak A, et al. Effect of Candida colonization on human ulcerative colitis and the healing of inflammatory changes of the colon in the experimental model of colitis ulcerosa. J Physiol Pharmocol. 2009; 60: 107-118.
57. Hueber W, Sands BE, Lewitzky S, et al. Secukinumab, a human anti-IL-17A monoclonal antibody, for moderate to severe Crohn's disease: unexpected results of a randomised, double-blind placebo-controlled trial. Gut. 2012; 61: 1693-1700.
58. Samuel S, Loftus EV Jr, Sandborn WJ. The effects of itraconazole on inflammatory bowel disease activity in patients treated for histoplasmosis. Aliment Pharmacol Ther. 2010; 32: 1207-1209.
59. Jawhara S, Thuru X, Standaert-Vitse A, et al. Colonization of mice by Candida albicans is promoted by chemically induced colitis and augments inflammatory responses through galectin-3. J Infect Dis. 2008; 197: 972-980.
60. Sokol H, Conway KL, Zhang M, et al. Card9 mediates intestinal epithelial cell restitution, T-helper 17 responses, and control of bacterial infection in mice. Gastroenterology. 2013; 145: 591-601: e593.
61. Edwards-Ingram L, Gitsham P, Burton N, et al. Genotypic and physiological characterization of Saccharomyces boulardii, the probiotic strain of Saccharomyces cerevisiae. Appl Environ Microbiol. 2007; 73: 2458-2467.
62. McFarland LV. Systematic review and meta-Analysis of Saccharomyces boulardii in adult patients. World J Gastroenterol. 2010; 16: 2202-2222.
63. Wu X, Vallance BA, Boyer L, et al. Saccharomyces boulardii ameliorates Citrobacter rodentium-induced colitis through actions on bacterial virulence factors. Am J Physiol Gastrointest Liver Physiol. 2008; 294: G295-G306.
64. Murzyn A, Krasowska A, Augustyniak D, et al. The effect of Saccharomyces boulardii on Candida albicans-infected human intestinal cell lines Caco-2 and Intestin 407. FEMS Microbiol Lett. 2010; 310: 17-23.
65. Murzyn A, Krasowska A, Stefanowicz P, et al. Capric acid secreted by S. boulardii inhibits C. albicans filamentous growth, adhesion and biofilm formation. PLoS One. 2010; 5: e12050.
66. Krasowska A, Murzyn A, Dyjankiewicz A, et al. The antagonistic effect of Saccharomyces boulardii on Candida albicans filamentation, adhesion and biofilm formation. FEMS Yeast Res. 2009; 9: 1312-1321.
67. Chen X, Yang G, Song JH, et al. Probiotic yeast inhibits VEGFR signaling and angiogenesis in intestinal inflammation. PloS One. 2013; 8: e64227.
68. Jawhara S, Poulain D. Saccharomyces boulardii decreases inflammation and intestinal colonization by Candida albicans in a mouse model of chemically-induced colitis. Med Mycol. 2007; 45: 691-700.
69. Samonis G, Falagas ME, Lionakis S, et al. Saccharomyces boulardii and Candida albicans experimental colonization of the murine gut. Med Mycol. 2011; 49: 395-399.
70. Rajput IR, Li LY, Xin X, et al. Effect of Saccharomyces boulardii and Bacillus subtilis B10 on intestinal ultrastructure modulation and mucosal immunity development mechanism in broiler chickens. Poult Sci. 2013; 92: 956-965.
71. Chen X, Kokkotou EG, Mustafa N, et al. Saccharomyces boulardii inhibits ERK1/2 mitogen-Activated protein kinase activation both in vitro and in vivo and protects against Clostridium difficile toxin A-induced enteritis. J Biol Chem. 2006; 281: 24449-24454.
72. Sougioultzis S, Simeonidis S, Bhaskar KR, et al. Saccharomyces boulardii produces a soluble anti-inflammatory factor that inhibits NF-kappaBmediated IL-8 gene expression. Biochem Biophys Res Commun. 2006; 343: 69-76.
73. Dalmasso G, Cottrez F, Imbert V, et al. Saccharomyces boulardii inhibits inflammatory bowel disease by trapping T cells in mesenteric lymph nodes. Gastroenterology. 2006; 131: 1812-1825.
74. Canonici A, Pellegrino E, Siret C, et al. Saccharomyces boulardii improves intestinal epithelial cell restitution by inhibiting alpha vbeta5 integrin activation state. PLoS One. 2012; 7: e45047.
75. Canonici A, Siret C, Pellegrino E, et al. Saccharomyces boulardii improves intestinal cell restitution through activation of the alpha 2 beta 1 integrin collagen receptor. PLoS One. 2011; 6: e18427.
76. Ruland J. CARD9 signaling in the innate immune response. Ann New York Acad Sci. 2008; 1143: 35-44.
77. Mukherjee PK, Chandra J, Retuerto M, et al. Oral mycobiome analysis of HIV-infected patients: identification of Pichia as an antagonist of opportunistic fungi. PLoS Pathogens. 2014; 10: e1003996.
78. Zelante T, Iannitti RG, Cunha C, et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity. 2013; 39: 372-385.