Identification of rothia bacteria as gluten-degrading natural colonizers of the upper gastro-intestinal tract

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Zamakhchari, Maram ^a   Wei, Guoxian ^a   Dewhirst, Floyd ^b   Lee, Jaeseop ^a   Schuppan, Detlef ^c,d   Oppenheim, Frank G ^a   Helmerhorst, Eva J ^a  

^a BOSTON UNIVERSITY   (United States)

^b FORSYTH INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR; DNA 16S; DNA FRAGMENT; EPITOPE; GLIADIN; GLUTEN; ANILINE DERIVATIVE; NITROANILINE; PEPTIDE FRAGMENT;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; CARBOXY TERMINAL SEQUENCE; CELL SUSPENSION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE; GENE SEQUENCE; INCUBATION TIME; MASS SPECTROMETRY; MOUTH FLORA; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ROTHIA; ROTHIA AERIA; ROTHIA MUCILAGINOSA; SPECIES DIFFERENTIATION; UPPER GASTROINTESTINAL TRACT; ZYMOGRAPHY; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; CLASSIFICATION; ENZYME SPECIFICITY; ENZYMOLOGY; HUMAN; HYDROLYSIS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MICROCOCCACEAE; MOLECULAR GENETICS; MOLECULAR WEIGHT; SALIVA; SOLUTION AND SOLUBILITY; TOOTH PLAQUE;

BACTERIA (MICROORGANISMS); HORDEUM; MAMMALIA; ROTHIA; ROTHIA AERIA; ROTHIA MUCILAGINOSA; SECALE CEREALE; TRITICUM AESTIVUM;

AMINO ACID SEQUENCE; ANILINE COMPOUNDS; BINDING SITES; DENTAL PLAQUE; GLIADIN; GLUTENS; HUMANS; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; MICROCOCCACEAE; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PEPTIDE FRAGMENTS; PROTEOLYSIS; SALIVA; SOLUTIONS; SUBSTRATE SPECIFICITY; UPPER GASTROINTESTINAL TRACT;

EID: 80053038305     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024455     Document Type: Article

References (41)

1. Koning F, Schuppan D, Cerf-Bensussan N, Sollid LM, (2005) Pathomechanisms in celiac disease. Best Pract Res Clin Gastroenterol 19: 373-387.
2. Rubio-Tapia A, Murray JA, (2010) Celiac disease. Curr Opin Gastroenterol 26: 116-122.
3. Green PH, Jabri B, (2006) Celiac disease. Annu Rev Med 57: 207-221.
4. Schuppan D, Junker Y, Barisani D, (2009) Celiac disease: from pathogenesis to novel therapies. Gastroenterology 137: 1912-1933.
5. Wieser H, (1995) The precipitating factor in coeliac disease. Baillieres Clin Gastroenterol 9: 191-207.
6. Shan L, Molberg O, Parrot I, Hausch F, Filiz F, et al. (2002) Structural basis for gluten intolerance in celiac sprue. Science 297: 2275-2279.
7. Hausch F, Shan L, Santiago NA, Gray GM, Khosla C, (2002) Intestinal digestive resistance of immunodominant gliadin peptides. Am J Physiol Gastrointest Liver Physiol 283: G996-G1003.
8. Shan L, Qiao SW, Arentz-Hansen H, Molberg O, Gray GM, et al. (2005) Identification and analysis of multivalent proteolytically resistant peptides from gluten: implications for celiac sprue. J Proteome Res 4: 1732-1741.
9. Molberg O, McAdam SN, Korner R, Quarsten H, Kristiansen C, et al. (1998) Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease. Nat Med 4: 713-717.
10. Sollid LM, Khosla C, (2005) Future therapeutic options for celiac disease. Nat Clin Pract Gastroenterol Hepatol 2: 140-147.
11. Shan L, Marti T, Sollid LM, Gray GM, Khosla C, (2004) Comparative biochemical analysis of three bacterial prolyl endopeptidases: implications for coeliac sprue. Biochem J 383: 311-318.
12. Stepniak D, Spaenij-Dekking L, Mitea C, Moester M, de Ru A, et al. (2006) Highly efficient gluten degradation with a newly identified prolyl endoprotease: implications for celiac disease. Am J Physiol Gastrointest Liver Physiol 291: G621-629.
13. Bethune MT, Strop P, Tang Y, Sollid LM, Khosla C, (2006) Heterologous expression, purification, refolding, and structural-functional characterization of EP-B2, a self-activating barley cysteine endoprotease. Chem Biol 13: 637-647.
14. Siegel M, Bethune MT, Gass J, Ehren J, Xia J, et al. (2006) Rational design of combination enzyme therapy for celiac sprue. Chem Biol 13: 649-658.
15. Gass J, Bethune MT, Siegel M, Spencer A, Khosla C, (2007) Combination enzyme therapy for gastric digestion of dietary gluten in patients with celiac sprue. Gastroenterology 133: 472-480.
16. Gass J, Vora H, Bethune MT, Gray GM, Khosla C, (2006) Effect of barley endoprotease EP-B2 on gluten digestion in the intact rat. J Pharmacol Exp Ther 318: 1178-1186.
17. Mitea C, Havenaar R, Drijfhout JW, Edens L, Dekking L, et al. (2008) Efficient degradation of gluten by a prolyl endoprotease in a gastrointestinal model: implications for coeliac disease. Gut 57: 25-32.
18. Marti T, Molberg O, Li Q, Gray GM, Khosla C, et al. (2005) Prolyl endopeptidase-mediated destruction of T cell epitopes in whole gluten: chemical and immunological characterization. J Pharmacol Exp Ther 312: 19-26.
19. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, et al. (2006) Metagenomic analysis of the human distal gut microbiome. Science 312: 1355-1359.
20. Hooper LV, Midtvedt T, Gordon JI, (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22: 283-307.
21. Helmerhorst EJ, Sun X, Salih E, Oppenheim FG, (2008) Identification of Lys-Pro-Gln as a novel cleavage site specificity of saliva-associated proteases. J Biol Chem 283: 19957-19966.
22. Helmerhorst EJ, Zamakhchari M, Schuppan D, Oppenheim FG, (2010) Discovery of a novel and rich source of gluten-degrading microbial enzymes in the oral cavity. PLoS One 5: e13264.
23. Campese M, Sun X, Bosch JA, Oppenheim FG, Helmerhorst EJ, (2009) Concentration and fate of histatins and acidic proline-rich proteins in the oral environment. Arch Oral Biol 54: 345-353.
24. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE, (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43: 5721-5732.
25. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, et al. (2001) Bacterial diversity in human subgingival plaque. J Bacteriol 183: 3770-3783.
26. Sun X, Salih E, Oppenheim FG, Helmerhorst EJ, (2009) Kinetics of histatin proteolysis in whole saliva and the effect on bioactive domains with metal-binding, antifungal, and wound-healing properties. Faseb J 23: 2691-2701.
27. Arentz-Hansen H, McAdam SN, Molberg O, Fleckenstein B, Lundin KE, et al. (2002) Celiac lesion T cells recognize epitopes that cluster in regions of gliadins rich in proline residues. Gastroenterology 123: 803-809.
28. Camp JG, Kanther M, Semova I, Rawls JF, (2009) Patterns and scales in gastrointestinal microbial ecology. Gastroenterology 136: 1989-2002.
29. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, et al. (2007) The human microbiome project. Nature 449: 804-810.
30. Chen T, Yu WH, Izard J, Baranova OV, Lakshmanan A, et al. (2010) The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford) 2010: baq013.
31. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, et al. (2010) The human oral microbiome. J Bacteriol 192: 5002-5017.
32. Li Y, Kawamura Y, Fujiwara N, Naka T, Liu H, et al. (2004) Rothia aeria sp. nov., Rhodococcus baikonurensis sp. nov. and Arthrobacter russicus sp. nov., isolated from air in the Russian space laboratory Mir. Int J Syst Evol Microbiol 54: 827-835.
33. Kazor CE, Mitchell PM, Lee AM, Stokes LN, Loesche WJ, et al. (2003) Diversity of bacterial populations on the tongue dorsa of patients with halitosis and healthy patients. J Clin Microbiol 41: 558-563.
34. Collins MD, Hutson RA, Baverud V, Falsen E, (2000) Characterization of a Rothia-like organism from a mouse: description of Rothia nasimurium sp. nov. and reclassification of Stomatococcus mucilaginosus as Rothia mucilaginosa comb. nov. Int J Syst Evol Microbiol 50 Pt 3: 1247-1251.
35. Zaura E, Keijser BJ, Huse SM, Crielaard W, (2009) Defining the healthy "core microbiome" of oral microbial communities. BMC Microbiol 9: 259.
36. Ou G, Hedberg M, Horstedt P, Baranov V, Forsberg G, et al. (2009) Proximal small intestinal microbiota and identification of rod-shaped bacteria associated with childhood celiac disease. Am J Gastroenterol 104: 3058-3067.
37. Rizzello CG, De Angelis M, Di Cagno R, Camarca A, Silano M, et al. (2007) Highly efficient gluten degradation by lactobacilli and fungal proteases during food processing: new perspectives for celiac disease. Appl Environ Microbiol 73: 4499-4507.
38. Matysiak-Budnik T, Candalh C, Cellier C, Dugave C, Namane A, et al. (2005) Limited efficiency of prolyl-endopeptidase in the detoxification of gliadin peptides in celiac disease. Gastroenterology 129: 786-796.
39. Vader LW, de Ru A, van der Wal Y, Kooy YM, Benckhuijsen W, et al. (2002) Specificity of tissue transglutaminase explains cereal toxicity in celiac disease. J Exp Med 195: 643-649.
40. Dieterich W, Ehnis T, Bauer M, Donner P, Volta U, et al. (1997) Identification of tissue transglutaminase as the autoantigen of celiac disease. Nat Med 3: 797-801.
41. Tian N, Wei G, Schuppan D, Oppenheim FG, Helmerhorst EJ, (2011) Proteolytic degradation of immunogenic 33-mer and 26-mer gliadin-derived peptides by oral bacteria reduces tissue transglutaminase recognition in vitro. 14th International Celiac Disease Symposium, Oslo, Norway, Abstract #220.