Identification and characterization of intestinal lactobacilli strains capable of degrading immunotoxic peptides present in gluten

Journal of Applied Microbiology

Volumn 118, Issue 2, 2015, Pages 515-527

  Duar, R M ^a,b   Clark, K J ^a   Patil, P B ^a,c   Hernandez C ^a   Bruning S ^a   Burkey, T E ^a   Madayiputhiya, N ^a   Taylor, S L ^a   Walter, Jens ^a,b  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

Author keywords

Coeliac; Epitopes; Gliadin; Gluten; Lactobacillus; Peptidase; Probiotics

Indexed keywords

BACTERIA; BIODEGRADATION; DEGRADATION; EPITOPES; MASS SPECTROMETRY;

CELIAC; CELIAC DISEASE; GASTROINTESTINAL TRACT; GLIADIN; GLUTEN; GLUTEN PEPTIDES; LACTOBACILLUS; LACTOBACILLUS STRAINS; PEPTIDASE; PROBIOTICS;

PEPTIDES;

GLIADIN; GLUTEN; PEPTIDE; PROTEINASE; EPITOPE; PEPTIDE HYDROLASE; PROBIOTIC AGENT;

ENZYME ACTIVITY; HYDROLYSIS; IDENTIFICATION KEY; MICROBIAL ACTIVITY; PEPTIDE; PIG; SPECIES DIVERSITY;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; CELIAC DISEASE; CONTROLLED STUDY; ENZYME SYNTHESIS; HYDROLYSIS; IMMUNOTOXICITY; INTESTINE FLORA; LACTOBACILLUS; LACTOBACILLUS AMYLOVORUS; LACTOBACILLUS JOHNSONII; LACTOBACILLUS RUMINIS; LACTOBACILLUS SALIVARIUS; LIQUID CHROMATOGRAPHY; NONHUMAN; PROTEIN DEGRADATION; SMALL INTESTINE; TANDEM MASS SPECTROMETRY; ANIMAL; BACTERIUM; CHEMISTRY; ENZYMOLOGY; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PIG;

LACTOBACILLUS; LACTOBACILLUS AMYLOVORUS; LACTOBACILLUS JOHNSONII; LACTOBACILLUS RUMINIS; LACTOBACILLUS SALIVARIUS; SUIDAE;

ANIMALS; BACTERIA; CELIAC DISEASE; EPITOPES; GLIADIN; GLUTENS; INTESTINE, SMALL; LACTOBACILLUS; PEPTIDE HYDROLASES; PEPTIDES; PROBIOTICS; SWINE;

EID: 84921505663     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12687     Document Type: Article

References (55)

1. Alvarez-Sieiro, P., Martin, M.C., Redruello, B., Del Rio, B., Ladero, V., Palanski, B.A., Khosla, C., Fernandez, M. et al. (2014) Generation of food-grade recombinant Lactobacillus casei delivering Myxococcus xanthus prolyl endopeptidase. Appl Microbiol Biotechnol 98, 6689-6700.
2. Arentz-Hansen, H., Körner, R., Molberg, O., Quarsten, H., Vader, W., Kooy, Y.M., Lundin, K.E., Koning, F. et al. (2000) The intestinal T cell response to alpha-gliadin in adult celiac disease is focused on a single deamidated glutamine targeted by tissue transglutaminase. J Exp Med 191, 603-612.
3. Berntsson, R.P.A., Doeven, M.K., Fusetti, F., Duurkens, R.H., Sengupta, D., Marrink, S.J., Thunnissen, A.M.W.H., Poolman, B. et al. (2009) The structural basis for peptide selection by the transport receptor OppA. EMBO J 28, 1332-1340.
4. Bethune, M.T. and Khosla, C. (2012) Oral enzyme therapy for celiac sprue. Methods Enzymol 502, 241-271.
5. Caminero, A., Herrán, A.R., Nistal, E., Pérez-Andrés, J., Vaquero, L., Vivas, S., Ruiz de Morales, J.M.G., Albillos, S.M. et al. (2014) Diversity of the cultivable human gut microbiome involved in gluten metabolism: isolation of microorganisms with potential interest for coeliac disease. FEMS Microbiol Ecol 88, 309-319.
6. Castillo, M., Skene, G., Roca, M., Anguita, M., Badiola, I., Duncan, S.H., Flint, H.J. and Martín-Orúe, S.M. (2007) Application of 16S rRNA gene-targetted fluorescence in situ hybridization and restriction fragment length polymorphism to study porcine microbiota along the gastrointestinal tract in response to different sources of dietary fibre. FEMS Microbiol Ecol 59, 138-146.
7. Christensen, J.E., Dudley, E.G., Pederson, J.A. and Steele, J.L. (1999) Peptidases and amino acid catabolism in lactic acid bacteria. Antonie Van Leeuwenhoek 76, 217-246.
8. Daniel, C., Roussel, Y., Kleerebezem, M. and Pot, B. (2011) Recombinant lactic acid bacteria as mucosal biotherapeutic agents. Trends Biotechnol 29, 499-508.
9. Davila, A.M., Blachier, F., Gotteland, M., Andriamihaja, M., Benetti, P.H., Sanz, Y. and Tomé, D. (2013) Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host. Pharmacol Res 68, 95-107.
10. De Angelis, M., Rizzello, C.G., Fasano, A., Clemente, M.G., De Simone, C., Silano, M., De Vincenzi, M., Losito, I. et al. (2006) VSL#3 probiotic preparation has the capacity to hydrolyze gliadin polypeptides responsible for celiac sprue. Biochim Biophys Acta 1762, 80-93.
11. De Angelis, M., Cassone, A., Rizzello, C.G., Gagliardi, F., Minervini, F., Calasso, M., Di Cagno, R., Francavilla, R. et al. (2010) Mechanism of degradation of immunogenic gluten epitopes from Triticum turgidum L. var. durum by sourdough lactobacilli and fungal proteases. Appl Environ Microbiol 76, 508-518.
12. De Sousa Moraes, L.F., Grzeskowiak, L.M., de Sales Teixeira, T.F. and Gouveia Peluzio, Mdo.C. (2014) Intestinal microbiota and probiotics in celiac disease. Clin Microbiol Rev 27, 482-489.
13. Di Sabatino, A. and Corazza, G.R. (2009) Coeliac disease. Lancet 373, 1480-1493.
14. Elli, M., Zink, R., Rytz, A., Reniero, R. and Morelli, L. (2000) Iron requirement of Lactobacillus spp. in completely chemically defined growth media. J Appl Microbiol 88, 695-703.
15. Fernández, M. and Zúñiga, M. (2006) Amino acid catabolic pathways of lactic acid bacteria. Crit Rev Microbiol 32, 155-183.
16. Fernandez-Feo, M., Wei, G., Blumenkranz, G., Dewhirst, F.E., Schuppan, D., Oppenheim, F.G. and Helmerhorst, E.J. (2013) The cultivable human oral gluten-degrading microbiome and its potential implications in coeliac disease and gluten sensitivity. Clin Microbiol Infect 19, E386-E394.
17. Gass, J., Bethune, M.T., Siegel, M., Spencer, A. and Khosla, C. (2007) Combination enzyme therapy for gastric digestion of dietary gluten in patients with celiac sprue. Gastroenterology 133, 472-480.
18. Gobbetti, M., Giuseppe Rizzello, C., Di Cagno, R. and De Angelis, M. (2007) Sourdough lactobacilli and celiac disease. Food Microbiol 24, 187-196.
19. Green, P.H.R. and Cellier, C. (2007) Celiac disease. N Engl J Med 357, 1731-1743.
20. Heinritz, S.N., Mosenthin, R. and Weiss, E. (2013) Use of pigs as a potential model for research into dietary modulation of the human gut microbiota. Nutr Res Rev 26, 191-209.
21. Jacobsen, C.N., Rosenfeldt Nielsen, V., Hayford, A.E., Moller, P.L., Michaelsen, K.F., Parregaard, A., Sandstrom, B., Tvede, M. et al. (1999) Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol 65, 4949-4956.
22. Kaukinen, K., Lindfors, K. and Mäki, M. (2014) Advances in the treatment of coeliac disease: an immunopathogenic perspective. Nat Rev Gastroenterol Hepatol 11, 36-44.
23. Lähdeaho, M.L., Kaukinen, K., Laurila, K., Vuotikka, P., Koivurova, O.P., Kärjä-Lahdensuu, T., Marcantonio, A., Adelman, D.C. et al. (2014) Glutenase ALV003 attenuates gluten-induced mucosal injury in patients with celiac disease. Gastroenterology 146, 1649-1658.
24. Laparra, J.M. and Sanz, Y. (2010) Bifidobacteria inhibit the inflammatory response induced by gliadins in intestinal epithelial cells via modifications of toxic peptide generation during digestion. J Cell Biochem 109, 801-807.
25. Leser, T.D., Amenuvor, J.Z., Jensen, T.K., Lindecrona, R.H., Boye, M. and Moller, K. (2002) Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68, 673-690.
26. Lindfors, K., Blomqvist, T., Juuti-Uusitalo, K., Stenman, S., Venäläinen, J., Mäki, M. and Kaukinen, K. (2008) Live probiotic Bifidobacterium lactis bacteria inhibit the toxic effects induced by wheat gliadin in epithelial cell culture. Clin Exp Immunol 152, 552-558.
27. Liu, M., Bayjanov, J.R., Renckens, B., Nauta, A. and Siezen, R.J. (2010) The proteolytic system of lactic acid bacteria revisited: a genomic comparison. BMC Genom 11, 36.
28. Louis, P., Scott, K.P., Duncan, S.H. and Flint, H.J. (2007) Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol 102, 1197-1208.
29. Ludvigsson, J.F., Rubio-Tapia, A., van Dyke, C.T., Melton, L.J., Zinsmeister, A.R., Lahr, B.D. and Murray, J.A. (2013) Increasing incidence of celiac disease in a north american population. Am J Gastroenterol 108, 818-824.
30. Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N. et al. (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103, 15611-15616.
31. Martínez, I., Wallace, G., Zhang, C., Legge, R., Benson, A.K., Carr, T.P., Moriyama, E.N. and Walter, J. (2009) Diet-induced metabolic improvements in a hamster model of hypercholesterolemia are strongly linked to alterations of the gut microbiota. Appl Environ Microbiol 75, 4175-4184.
32. Meroth, C.B., Walter, J., Hertel, C., Brandt, M.J. and Hammes, W.P. (2003) Monitoring the bacterial population dynamics in sourdough fermentation processes by using PCR-denaturing gradient gel electrophoresis. Appl Environ Microbiol 69, 475-482.
33. Mitea, C., Havenaar, R., Drijfhout, J.W., Edens, L., Dekking, L. and Koning, F. (2008) Efficient degradation of gluten by a prolyl endoprotease in a gastrointestinal model: implications for coeliac disease. Gut 57, 25-32.
34. Nadal, I., Donat, E., Donant, E., Ribes-Koninckx, C., Calabuig, M. and Sanz, Y. (2007) Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J Med Microbiol 56, 1669-1674.
35. Neish, A.S. (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136, 65-80.
36. Oh, P.L., Benson, A.K., Peterson, D.A., Patil, P.B., Moriyama, E.N., Roos, S. and Walter, J. (2010) Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. ISME J 4, 377-387.
37. Piper, J.L., Gray, G.M. and Khosla, C. (2004) Effect of prolyl endopeptidase on digestive-resistant gliadin peptides in vivo. J Pharmacol Exp Ther 311, 213-219.
38. Rizzello, C.G., De Angelis, M., Di Cagno, R., Camarca, A., Silano, M., Losito, I., De Vincenzi, M., De Bari, M.D. 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.
39. Rollán, G., De Angelis, M., Gobbetti, M. and de Valdez, G.F. (2005) Proteolytic activity and reduction of gliadin-like fractions by sourdough lactobacilli. J Appl Microbiol 99, 1495-1502.
40. Sanz, Y., Sánchez, E., Marzotto, M., Calabuig, M., Torriani, S. and Dellaglio, F. (2007) Differences in faecal bacterial communities in coeliac and healthy children as detected by PCR and denaturing gradient gel electrophoresis. FEMS Immunol Med Microbiol 51, 562-568.
41. Shan, L., Molberg, Ø., Parrot, I., Hausch, F., Filiz, F., Gray, G.M., Sollid, L.M. and Khosla, C. (2002) Structural basis for gluten intolerance in celiac sprue. Science 297, 2275-2279.
42. Shan, L., Marti, T., Sollid, L.M., Gray, G.M. and Khosla, C. (2004) Comparative biochemical analysis of three bacterial prolyl endopeptidases: implications for coeliac sprue. Biochem J 383, 311-318.
43. Shan, L., Qiao, S.W., Arentz-hansen, H., Molberg, Ø., Gray, G.M., Sollid, L.M., Khosla, C. and California, S. (2005) Identification and analysis of multivalent proteolytically resistant peptides from gluten : implications for celiac sprue. J Proteome Res 4, 1732-1741.
44. Siegel, M., Bethune, M.T., Gass, J., Ehren, J., Xia, J., Johannsen, A., Stuge, T.B., Gray, G.M. et al. (2006) Rational design of combination enzyme therapy for celiac sprue. Chem Biol 13, 649-658.
45. Siegel, M., Garber, M.E., Spencer, A.G., Botwick, W., Kumar, P., Williams, R.N., Kozuka, K., Shreeniwas, R. et al. (2012) Safety, tolerability, and activity of ALV003: results from two phase 1 single, escalating-dose clinical trials. Dig Dis Sci 57, 440-450.
46. Sollid, L.M. (2002) Coeliac disease: dissecting a complex inflammatory disorder. Nat Rev Immunol 2, 647-655.
47. Sollid, L.M. and Khosla, C. (2005) Future therapeutic options for celiac disease. Nat Clin Pract Gastroenterol Hepatol 2, 140-147.
48. Sollid, L.M., Qiao, S.W., Anderson, R.P., Gianfrani, C. and Koning, F. (2012) Nomenclature and listing of celiac disease relevant gluten T-cell epitopes restricted by HLA-DQ molecules. Immunogenetics 64, 455-460.
49. Stepniak, D., Spaenij-Dekking, L., Mitea, C., Moester, M., de Ru, A., Baak-Pablo, R., van Veelen, P., Edens, L. 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-G629.
50. Tack, G.J., van de Water, J.M.W., Bruins, M.J., Kooy-Winkelaar, E.M.C., van Bergen, J., Bonnet, P., Vreugdenhil, A.C.E., Korponay-Szabo, I. et al. (2013) Consumption of gluten with gluten-degrading enzyme by celiac patients: a pilot-study. World J Gastroenterol 19, 5837-5847.
51. Tjellström, B., Stenhammar, L., Högberg, L., Fälth-Magnusson, K., Magnusson, K.E., Midtvedt, T., Sundqvist, T. and Norin, E. (2005) Gut microflora associated characteristics in children with celiac disease. Am J Gastroenterol 100, 2784-2788.
52. Tye-Din, J.A., Stewart, J.A., Dromey, J.A., Beissbarth, T., van Heel, D.A., Tatham, A., Henderson, K., Mannering, S.I. et al. (2010) Comprehensive, quantitative mapping of T cell epitopes in gluten in celiac disease. Sci Transl Med 2, 41ra51.
53. Walter, J. (2008) Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol 74, 4985-4996.
54. Wells, J.M. and Mercenier, A. (2008) Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat Rev Microbiol 6, 349-362.
55. Zamakhchari, M., Wei, G., Dewhirst, F., Lee, J., Schuppan, D., Oppenheim, F.G. and Helmerhorst, E.J. (2011) Identification of Rothia bacteria as gluten-degrading natural colonizers of the upper gastro-intestinal tract. Roop, R.M. ed. PLoS One 6, e24455.