Discovery of a novel and rich source of gluten-degrading microbial enzymes in the oral cavity

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Helmerhorst, Eva J ^a   Zamakhchari, Maram ^a   Schuppan, Detlef ^b   Oppenheim, Frank G ^a  

^a BOSTON UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANILIDE; GLIADIN; GLUTEN; MICROBIAL ENZYME; ENZYME;

ARTICLE; BACTERIAL METABOLISM; CELIAC DISEASE; CONTROLLED STUDY; DIETARY INTAKE; ENZYME SUBSTRATE; HUMAN; ISOELECTRIC POINT; MOLECULAR WEIGHT; MOUTH CAVITY; MOUTH FLORA; NONHUMAN; PROTEIN DEGRADATION; PROTEIN HYDROLYSIS; TOOTH PLAQUE; UPPER GASTROINTESTINAL TRACT; ZYMOGRAPHY; AMINO ACID SEQUENCE; CHEMISTRY; ELECTROSPRAY MASS SPECTROMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; ISOELECTRIC FOCUSING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MOUTH; PH; SEQUENCE HOMOLOGY; TANDEM MASS SPECTROMETRY;

BACTERIA (MICROORGANISMS);

AMINO ACID SEQUENCE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ENZYMES; GLIADIN; GLUTENS; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; ISOELECTRIC FOCUSING; MOLECULAR SEQUENCE DATA; MOUTH; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 78149423735     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013264     Document Type: Article

References (35)

1. DeSesso JM, Jacobson CF (2001) Anatomical and physiological parameters affecting gastrointestinal absorption in humans and rats. Food Chem Toxicol 39: 209-228.
2. 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.
3. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, et al. (2001) Bacterial diversity in human subgingival plaque. J Bacteriol 183: 3770-3783.
4. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, et al. (2005) Diversity of the human intestinal microbial flora. Science 308: 1635-1638.
5. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, et al. (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 104: 13780-13785.
6. Camp JG, Kanther M, Semova I, Rawls JF (2009) Patterns and scales in gastrointestinal microbial ecology. Gastroenterology 136: 1989-2002.
7. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, et al. (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027-1031.
8. Daniel H (2004) Molecular and integrative physiology of intestinal peptide transport. Annu Rev Physiol 66: 361-384.
9. Wieser H (2007) Chemistry of gluten proteins. Food Microbiol 24: 115-119.
10. 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.
11. Koning F, Schuppan D, Cerf-Bensussan N, Sollid LM (2005) Pathomechanisms in celiac disease. Best Pract Res Clin Gastroenterol 19: 373-387.
12. Jabri B, Sollid LM (2006) Mechanisms of disease: immunopathogenesis of celiac disease. Nat Clin Pract Gastroenterol Hepatol 3: 516-525.
13. Schuppan D, Junker Y, Barisani D (2009) Celiac disease: from pathogenesis to novel therapies. Gastroenterology 137: 1912-1933.
14. 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.
15. Abe T, Chung SI, DiAugustine RP, Folk JE (1977) Rabbit liver transglutaminase: physical, chemical, and catalytic properties. Biochemistry 16: 5495-5501.
16. Messana I, Cabras T, Pisano E, Sanna MT, Olianas A, et al. (2008) Trafficking and postsecretory events responsible for the formation of secreted human salivary peptides: a proteomics approach. Mol Cell Proteomics 7: 911-926.
17. 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.
18. 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.
19. Sun X, Salih E, Oppenheim FG, Helmerhorst EJ (2009) Kinetics of histatin proteolysis in whole saliva and the effect on bioactive domains with metalbinding, antifungal, and wound-healing properties. Faseb J 23: 2691-2701.
20. Zhou M, Lucas DA, Chan KC, Issaq HJ, Petricoin EF, 3rd, et al. (2004) An investigation into the human serum "interactome". Electrophoresis 25: 1289-1298.
21. Koning F (2003) The molecular basis of celiac disease. J Mol Recognit 16: 333-336.
22. 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.
23. Troncone R, Auricchio R, Granata V (2008) Issues related to gluten-free diet in coeliac disease. Curr Opin Clin Nutr Metab Care 11: 329-333.
24. 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.
25. Stenman SM, Venalainen JI, Lindfors K, Auriola S, Mauriala T, et al. (2009) Enzymatic detoxification of gluten by germinating wheat proteases: implications for new treatment of celiac disease. Ann Med 41: 390-400.
26. 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.
27. Gass J, Khosla C (2007) Prolyl endopeptidases. Cell Mol Life Sci 64: 345-355.
28. 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.
29. Fleckenstein B, Qiao SW, Larsen MR, Jung G, Roepstorff P, et al. (2004) Molecular characterization of covalent complexes between tissue transglutaminase and gliadin peptides. J Biol Chem 279: 17607-17616.
30. Tollefsen S, Arentz-Hansen H, Fleckenstein B, Molberg O, Raki M, et al. (2006) HLA-DQ2 and -DQ8 signatures of gluten T cell epitopes in celiac disease. J Clin Invest 116: 2226-2236.
31. Biagi F, Corazza GR (2001) Defining gluten refractory enteropathy. Eur J Gastroenterol Hepatol 13: 561-565.
32. Maeda N, Kim HS, Azen EA, Smithies O (1985) Differential RNA splicing and post-translational cleavages in the human salivary proline-rich protein gene system. J Biol Chem 260: 11123-11130.
33. Koning F, Vader W (2003) Gluten peptides and celiac disease. Science 299: 513-515. author reply 513-515.
34. 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.
35. Lamkin MS, Oppenheim FG (1993) Structural features of salivary function. Crit Rev Oral Biol Med 4: 251-259.