Mycobiota in gastrointestinal diseases

Nature Reviews Gastroenterology and Hepatology

Volumn 12, Issue 2, 2015, Pages 77-87

  Mukherjee, Pranab K ^a   Sendid, Boualem ^b   Hoarau, Gautier ^b   Colombel, Jean Frédéric ^c   Poulain, Daniel ^b   Ghannoum, Mahmoud A ^a  

^a UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^b UNIV LILLE   (France)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER;

BACTERIAL STRAIN; CLADISTICS; CROHN DISEASE; DISEASE SEVERITY; DISEASE TRANSMISSION; FUNGAL COLONIZATION; FUNGAL COMMUNITY; FUNGAL DETECTION; FUNGAL GENETICS; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS IDENTIFICATION; GASTROINTESTINAL DISEASE; GRAFT VERSUS HOST REACTION; HEPATITIS; HOST PARASITE INTERACTION; HUMAN; IMMUNE RESPONSE; INFECTION RISK; INFLAMMATION; INTESTINE FLORA; MICROBIAL DIVERSITY; MICROBIOME; MOUTH FLORA; NONHUMAN; PATHOGENESIS; POPULATION ABUNDANCE; PRIORITY JOURNAL; REVIEW; TH1 CELL; TH2 CELL; ULCERATIVE COLITIS; BACTERIAL PHENOMENA AND FUNCTIONS; COMPLICATION; FUNGUS; GASTROINTESTINAL TRACT; HOST PATHOGEN INTERACTION; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; MYCOSIS; ORGANISMAL INTERACTION; PHYSIOLOGY;

BACTERIAL PHYSIOLOGICAL PHENOMENA; FUNGI; GASTROINTESTINAL DISEASES; GASTROINTESTINAL TRACT; HOST-PATHOGEN INTERACTIONS; HUMANS; MICROBIAL INTERACTIONS; MICROBIOTA; MYCOSES;

EID: 84926080075     PISSN: 17595045     EISSN: 17595053     Source Type: Journal    
DOI: 10.1038/nrgastro.2014.188     Document Type: Review

References (96)

1. Odds, F. C. in Candida and Candidosis 156-163 (Bailliere Tindall, 1988).
2. Parrot, J. Note sur un cas de muguet du gros intestin. Archives de Physiologie Normale et Pathologique 3, 621-625 (1870).
3. Parrot, J. Du muguet gastrique et de quelques autres localisations de ce parasite. Archives de Physiologie Normale et Pathologique 2, 579-599 (1869).
4. Ludlam, G. & Henderson, J. Neonatal thrush in a maternity hospital. Lancet 239, 64-70 (1942).
5. Goodrich, J. K. et al. Conducting a Microbiome Study. Cell 158, 250-262 (2014).
6. Norman, J. M., Handley, S. A. & Virgin, H. W. Kingdom?agnostic metagenomics and the importance of complete characterization of enteric microbial communities. Gastroenterology 146, 1459-1469 (2014).
7. Morgan, X. C. & Huttenhower, C. Chapter 12: Human microbiome analysis. PLoS Comput. Biol. 8, e1002808 (2012).
8. Gencosmanoglu, R. et al. Mid?esophageal ulceration and candidiasis?associated distal esophagitis as two distinct clinical patterns of tetracycline or doxycycline?induced esophageal injury. J. Clin. Gastroenterol. 38, 484-489 (2004).
9. Sano, T., Ozaki, K., Kodama, Y., Matsuura, T. & Narama, I. Antimicrobial agent, tetracycline, enhanced upper alimentary tract Candida albicans infection and its related mucosal proliferation in alloxan?induced diabetic rats. Toxicol. Pathol. 40, 1014-1019 (2012).
10. Wiesner, S. M., Jechorek, R. P., Garni, R. M., Bendel, C. M. & Wells, C. L. Gastrointestinal colonization by Candida albicans mutant strains in antibiotic?treated mice. Clin. Diagn. Lab. Immunol. 8, 192-195 (2001).
11. Mellado, E. et al. Sustained gastrointestinal colonization and systemic dissemination by Candida albicans, Candida tropicalis and Candida parapsilosis in adult mice. Diagn. Microbiol. Infect. Dis. 38, 21-28 (2000).
12. DeMaria, A., Buckley, H. & von Lichtenberg, F. Gastrointestinal candidiasis in rats treated with antibiotics, cortisone, and azathioprine. Infect. Immun. 13, 1761-1770 (1976).
13. Helstrom, P. B. & 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. 23, 764-774 (1979).
14. Clark, J. D. Influence of antibiotics or certain intestinal bacteria on orally administered Candida albicans in germ?free and conventional mice. Infect. Immun. 4, 731-737 (1971).
15. Dollive, S. et al. Fungi of the murine gut: episodic variation and proliferation during antibiotic treatment. PLoS ONE 8, e71806 (2013).
16. Faust, K. et al. Microbial co?occurrence relationships in the human microbiome. PLoS Comput. Biol. 8, e1002606 (2012).
17. Mukherjee, P. K. et al. Oral mycobiome analysis of HIV?infected patients: identification of Pichia as an antagonist of opportunistic fungi. PLoS Pathog. 10, e1003996 (2014).
18. Navazesh, M. et al. The effect of HAART on salivary microbiota in the Women's Interagency HIV Study (WIHS). Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 100, 701-708 (2005).
19. Cruz, M. R., Graham, C. E., Gagliano, B. C., Lorenz, M. C. & Garsin, D. A. Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans. Infect. Immun. 81, 189-200 (2012).
20. Mondot, S. et al. Highlighting new phylogenetic specificities of Crohn's disease microbiota. Inflamm Bowel Dis. 17, 185-192 (2011).
21. Kang, S. et al. Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray. Inflamm. Bowel Dis. 16, 2034-2042 (2010).
22. Workman, S. N., Been, F. E., Crawford, S. R. & Lavoie, M. C. Bacteriocin?like inhibitory substances from Campylobacter spp. Antonie Van Leeuwenhoek 93, 435-436 (2008).
23. Ghannoum, M. A. et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog. 6, e1000713 (2010).
24. Jawhara, S. et al. Modulation of intestinal inflammation by yeasts and cell wall extracts: strain dependence and unexpected antiinflammatory role of glucan fractions. PLoS ONE 7, e40648 (2012).
25. Jawhara, S. & Poulain, D. Saccharomyces boulardii decreases inflammation and intestinal colonization by Candida albicans in a mouse model of chemically?induced colitis. Med. Mycol. 45, 691-700 (2007).
26. Samonis, G. et al. Saccharomyces boulardii and Candida albicans experimental colonization of the murine gut. Med. Mycol. 49, 395-399 (2011).
27. Demirel, G. et al. Prophylactic Saccharomyces boulardii versus nystatin for the prevention of fungal colonization and invasive fungal infection in premature infants. Eur. J. Pediatr. 172, 1321-1326 (2013).
28. Nasidze, I., Li, J., Quinque, D., Tang, K. & Stoneking, M. Global diversity in the human salivary microbiome. Genome Res. 19, 636-643 (2009).
29. Dollive, S. et al. A tool kit for quantifying eukaryotic rRNA gene sequences from human microbiome samples. Genome Biol. 13, R60 (2012).
30. Hoffmann, C. et al. Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS ONE 8, e66019 (2013).
31. Sartor, R. B. Gut microbiota: Diet promotes dysbiosis and colitis in susceptible hosts. Nat. Rev. Gastroenterol. Hepatol. 9, 561-562 (2012).
32. Goldsmith, J. R. & Sartor, R. B. The role of diet on intestinal microbiota metabolism: downstream impacts on host immune function and health, and therapeutic implications. J. Gastroenterol. 49, 785-798 (2014).
33. Angebault, C. et al. Candida albicans is not always the preferential yeast colonizing humans: a study in Wayampi Amerindians. J. Infect. Dis. 208, 1705-1716 (2013).
34. Ott, S. J. et al. Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand. J. Gastroenterol. 43, 831-841 (2008).
35. Ramaswamy, K., Correa, M. & Koshy, A. Nonhealing gastric ulcer associated with Candida infection. Indian J. Med. Microbiol. 25, 57-58 (2007).
36. Santelmann, H. & Howard, J. M. Yeast metabolic products, yeast antigens and yeasts as possible triggers for irritable bowel syndrome. Eur. J. Gastroenterol. Hepatol. 17, 21-26 (2005).
37. Krause, R. & Reisinger, E. C. Candida and antibiotic?associated diarrhoea. Clin. Microbiol. Infect. 11, 1-2 (2005).
38. Stringer, A. M. et al. Gastrointestinal microflora and mucins may play a critical role in the development of 5?Fluorouracil?induced gastrointestinal mucositis. Exp. Biol. Med. (Maywood) 234, 430-441 (2009).
39. Cominelli, F. Inhibition of leukocyte trafficking in inflammatory bowel disease. N. Engl. J. Med. 369, 775-776 (2013).
40. Nielsen, O. H. & Ainsworth, M. A. Tumor necrosis factor inhibitors for inflammatory bowel disease. N. Engl. J. Med. 369, 754-762 (2013).
41. Abraham, C. & Cho, J. H. Inflammatory bowel disease. N. Engl. J. Med. 361, 2066-2078 (2009).
42. McKenzie, H., Main, J., Pennington, C. R. & Parratt, D. Antibody to selected strains of Saccharomyces cerevisiae (baker's and brewer's yeast) and Candida albicans in Crohn's disease. Gut 31, 536-538 (1990).
43. Poulain, D. et al. Yeasts: neglected pathogens. Dig. Dis. 27 (Suppl. 1), 104-110 (2009).
44. Colombel, J. F., Sendid, B., Jouault, T. & Poulain, D. Secukinumab failure in Crohn's disease: the yeast connection? Gut 62, 800-801 (2013).
45. Sendid, B. et al. Anti?Saccharomyces cerevisiae mannan antibodies in familial Crohn's disease. Am. J. Gastroenterol. 93, 1306-1310 (1998).
46. Standaert?Vitse, A. et al. Candida albicans colonization and ASCA in familial Crohn's disease. Am. J. Gastroenterol. 104, 1745-1753 (2009).
47. Sendid, B. et al. Antibodies against glucan, chitin, and Saccharomyces cerevisiae mannan as new biomarkers of Candida albicans infection that complement tests based on, C. albicans mannan. Clin. Vaccine Immunol. 15, 1868-1877 (2008).
48. Vasseur, F. et al. Variants of NOD1 and NOD2 genes display opposite associations with familial risk of Crohn's disease and antisaccharomyces cerevisiae antibody levels. Inflamm. Bowel Dis. 18, 430-438 (2012).
49. Standaert?Vitse, A. et al. Candida albicans is an immunogen for anti?Saccharomyces cerevisiae antibody markers of Crohn's disease. Gastroenterology 130, 1764-1775 (2006).
50. Quinton, J. F. et al. Anti?Saccharomyces cerevisiae mannan antibodies combined with antineutrophil cytoplasmic autoantibodies in inflammatory bowel disease: prevalence and diagnostic role. Gut 42, 788-791 (1998).
51. Seow, C. H. et al. Novel anti?glycan antibodies related to inflammatory bowel disease diagnosis and phenotype. Am. J. Gastroenterol. 104, 1426-1434 (2009).
52. Dotan, I. et al. Antibodies against laminaribioside and chitobioside are novel serologic markers in Crohn's disease. Gastroenterology 131, 366-378 (2006).
53. Ferrante, M. et al. New serological markers in inflammatory bowel disease are associated with complicated disease behaviour. Gut 56, 1394-1403 (2007).
54. Kaul, A. et al. Serum anti?glycan antibody biomarkers for inflammatory bowel disease diagnosis and progression: a systematic review and meta?analysis. Inflamm. Bowel Dis. 18, 1872-1884 (2012).
55. Jawhara, S. et al. Colonization of mice by Candida albicans is promoted by chemically induced colitis and augments inflammatory responses through galectin?3. J. Infect. Dis. 197, 972-980 (2008).
56. Trojanowska, D. et al. The role of Candida in inflammatory bowel disease. Estimation of transmission of C. albicans fungi in gastrointestinal tract based on genetic affinity between strains. Med. Sci. Monit. 16, 451-457 (2010).
57. Iliev, I. D. et al. Interactions between commensal fungi and the C?type lectin receptor dectin?1 influence colitis. Science 336, 1314-1317 (2012).
58. Brown, G. D. et al. Dectin?1 mediates the biological effects of beta?glucans. J. Exp. Med. 197, 1119-1124 (2003).
59. Marr, K. A. et al. Prolonged fluconazole prophylaxis is associated with persistent protection against candidiasis?related death in allogeneic marrow transplant recipients: long?term follow?up of a randomized, placebocontrolled trial. Blood 96, 2055-2061 (2000).
60. de Vries, H. S. et al. Genetic association analysis of the functional c.714T>G. polymorphism and mucosal expression of dectin?1 in inflammatory bowel disease. PLoS ONE 4, e7818 (2009).
61. Iliev, I. D., Mileti, E., Matteoli, G., Chieppa, M. & Rescigno, M. Intestinal epithelial cells promote colitis?protective regulatory T?cell differentiation through dendritic cell conditioning. Mucosal Immunol. 2, 340-350 (2009).
62. Penack, O., Holler, E. & van den Brink, M. R. Graft?versus?host disease: regulation by microbeassociated molecules and innate immune receptors. Blood 115, 1865-1872 (2010).
63. Shlomchik, W. D. Graft?versus?host disease. Nat. Rev. Immunol. 7, 340-352 (2007).
64. van der Velden, W. J. et al. Role of the mycobiome in human acute graft?versus?host disease. Biol. Blood Marrow Transplant 19, 329-332 (2013).
65. Tawara, I. et al. Influence of donor microbiota on the severity of experimental graft?versushost?disease. Biol. Blood Marrow Transplant 19, 164-168 (2013).
66. Holler, E. et al. Metagenomic analysis of the stool microbiome in patients receiving allogeneic stem cell transplantation: loss of diversity is associated with use of systemic antibiotics and more pronounced in gastrointestinal graft?versus?host disease. Biol. Blood Marrow Transplant 20, 640-645 (2014).
67. Chen, Y. et al. Correlation between gastrointestinal fungi and varying degrees of chronic hepatitis B virus infection. Diagn. Microbiol. Infect. Dis. 70, 492-498 (2011).
68. Brown, K. S., Ryder, S. D., Irving, W. L., Sim, R. B. & Hickling, T. P. Mannan binding lectin and viral hepatitis. Immunol. Lett. 108, 34-44 (2007).
69. Knoke, M. Gastrointestinal microecology of humans and Candida [German]. Mycoses 42 (Suppl. 1), 30-34 (1999).
70. Thomas, H. C. et al. Mutation of gene of mannose?binding protein associated with chronic hepatitis B viral infection. Lancet 348, 1417-1419 (1996).
71. Romani, L. Immunity to fungal infections. Nat. Rev. Immunol. 11, 275-288 (2011).
72. Ashman, R. B. & Papadimitriou, J. M. Production and function of cytokines in natural and acquired immunity to Candida albicans infection. Microbiol. Rev. 59, 646-672 (1995).
73. Romani, L. Immunity to Candida albicans: Th1, Th2 cells and beyond. Curr. Opin. Microbiol. 2, 363-367 (1999).
74. Nelson, R. D., Shibata, N., Podzorski, R. P. & Herron, M. J. Candida mannan: chemistry, suppression of cell?mediated immunity, and possible mechanisms of action. Clin. Microbiol. Rev. 4, 1-19 (1991).
75. Quintin, J. et al. Differential role of NK cells against Candida albicans infection in immunocompetent or immunocompromised mice. Eur. J. Immunol. 44, 2405-2414 (2014).
76. Netea, M. G., Brown, G. D., Kullberg, B. J. & Gow, N. A. An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 6, 67-78 (2008).
77. Hernandez?Santos, N. et al. Th17 cells confer long?term adaptive immunity to oral mucosal Candida albicans infections. Mucosal Immunol. 6, 900-910 (2013).
78. Zelante, T. et al. Sensing of mammalian IL?17A regulates fungal adaptation and virulence. Nat. Commun. 3, 683 (2012).
79. Dominguez?Villar, M. & Hafler, D. A. An Innate Role for IL?17. Science 332, 47-48 (2011).
80. Puel, A. et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin?17 immunity. Science 332, 65-68 (2011).
81. Underhill, D. M. & Iliev, I. D. The mycobiota: interactions between commensal fungi and the host immune system. Nat. Rev. Immunol. 14, 405-416 (2014).
82. Romani, L. et al. Indoleamine 2, 3?dioxygenase (IDO) in inflammation and allergy to Aspergillus. Med. Mycol. 47 (Suppl. 1), 154-161 (2009).
83. Zelante, T., Fallarino, F., Bistoni, F., Puccetti, P. & Romani, L. Indoleamine 2, 3?dioxygenase in infection: the paradox of an evasive strategy that benefits the host. Microbes Infect. 11, 133-141 (2009).
84. Bonifazi, P. et al. Balancing inflammation and tolerance in vivo through dendritic cells by the commensal Candida albicans. Mucosal Immunol. 2, 362-374 (2009).
85. Sendid, B. et al. Anti?glycan antibodies establish an unexpected link between C. albicans and Crohn disease [French]. Med. Sci. (Paris) 25, 473-481 (2009).
86. Gerard, R., Sendid, B., Colombel, J. F., Poulain, D. & Jouault, T. An immunological link between Candida albicans colonization and Crohn's disease. Crit. Rev. Microbiol. http://dx.doi.org/10.3109/1040841X.2013.810587.
87. Mora?Montes, H. M. et al. Recognition and blocking of innate immunity cells by Candida albicans chitin. Infect. Immun. 79, 1961-1970 (2011).
88. Boudeau, J., Glasser, A. L., Masseret, E., Joly, B. & Darfeuille?Michaud, A. Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect. Immun. 67, 4499-4509 (1999).
89. Barnich, N. & Darfeuille?Michaud, A. Adherent?invasive Escherichia coli and Crohn's disease. Curr. Opin. Gastroenterol. 23, 16-20 (2007).
90. Clarke, D. J. et al. Complete genome sequence of the Crohn's disease?associated adherentinvasive Escherichia coli strain HM605. J. Bacteriol. 193, 4540 (2011).
91. Mpofu, C. M. et al. Microbial mannan inhibits bacterial killing by macrophages: a possible pathogenic mechanism for Crohn's disease. Gastroenterology 133, 1487-1498 (2007).
92. d'Ostiani, C. F. et al. Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans. Implications for initiation of T helper cell immunity in vitro and in vivo. J. Exp. Med. 191, 1661-1674 (2000).
93. Acosta?Rodriguez, E. V. et al. Surface phenotype and antigenic specificity of human interleukin 17?producing T helper memory cells. Nat. Immunol. 8, 639-646 (2007).
94. Monk, C. E., Hutvagner, G. & Arthur, J. S. Regulation of miRNA transcription in macrophages in response to Candida albicans. PLoS ONE 5, e13669 (2010).
95. Nemeth, T. et al. Transcriptome profile of the murine macrophage cell response to Candida parapsilosis. Fungal Genet. Biol. 65, 48-56 (2014).
96. Ghannoum, M. A. & Mukherjee, P. K. The microbiome: more than bacteria (letter). Microbe 5, 459 (2010).