The cultivable human oral gluten-degrading microbiome and its potential implications in coeliac disease and gluten sensitivity

Coeliac disease is characterized by intestinal inflammation caused by gluten, proteins which are widely contained in the Western diet. Mammalian digestive enzymes are only partly capable of cleaving gluten, and fragments remain that induce toxic responses in patients with coeliac disease. We found t...

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Published in:	Clinical microbiology and infection Vol. 19; no. 9; pp. E386 - E394
Main Authors:	Fernandez-Feo, M., Wei, G., Blumenkranz, G., Dewhirst, F.E., Schuppan, D., Oppenheim, F.G., Helmerhorst, E.J.
Format:	Journal Article
Language:	English
Published:	England Elsevier Ltd 01-09-2013 Elsevier Limited
Subjects:	Actinomyces - enzymology Actinomyces - isolation & purification Actinomyces odontolyticus Bacteria - enzymology Bacteria - isolation & purification Capnocytophaga Capnocytophaga - enzymology Capnocytophaga - isolation & purification Celiac Disease - drug therapy Celiac Disease - enzymology Coeliac disease degradation Dental Plaque - microbiology gliadin Gliadin - chemistry Gliadin - metabolism Glutens - immunology Glutens - metabolism Humans Microbiota Neisseria Neisseria mucosa - enzymology Neisseria mucosa - isolation & purification oral bacteria proteases Saliva - microbiology Streptococcus Streptococcus - enzymology Streptococcus - isolation & purification Streptococcus mitis oral bacteria degradation Coeliac disease gliadin proteases
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Summary:	Coeliac disease is characterized by intestinal inflammation caused by gluten, proteins which are widely contained in the Western diet. Mammalian digestive enzymes are only partly capable of cleaving gluten, and fragments remain that induce toxic responses in patients with coeliac disease. We found that the oral microbiome is a novel and rich source of gluten-degrading organisms. Here we report on the isolation and characterization of the cultivable resident oral microbes that are capable of cleaving gluten, with special emphasis on the immunogenic domains. Bacteria were obtained by a selective culturing approach and enzyme activities were characterized by: (i) hydrolysis of paranitroanilide-derivatized gliadin-derived tripeptide substrates; (ii) gliadin degradation in-gel (gliadin zymography); (iii) gliadin degradation in solution; (iv) proteolysis of the highly immunogenic α-gliadin-derived 33-mer peptide. For selected strains pH activity profiles were determined. The culturing strategy yielded 87 aerobic and 63 anaerobic strains. Species with activity in at least two of the four assays were typed as: Rothia mucilaginosa HOT-681, Rothia aeria HOT-188, Actinomyces odontolyticus HOT-701, Streptococcus mitis HOT-677, Streptococcus sp. HOT-071, Neisseria mucosa HOT-682 and Capnocytophaga sputigena HOT-775, with Rothia species being active in all four assays. Cleavage specificities and substrate preferences differed among the strains identified. The approximate molecular weights of the enzymes were ~75 kD (Rothia spp.), ~60 kD (A. odontolyticus) and ~150 kD (Streptococcus spp.). In conclusion, this study identified new gluten-degrading microorganisms in the upper gastrointestinal tract. A cocktail of the most active oral bacteria, or their isolated enzymes, may offer promising new treatment modalities for coeliac disease.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	1198-743X 1469-0691
DOI:	10.1111/1469-0691.12249