Differences in gluten metabolism among healthy volunteers, coeliac disease patients and first-degree relatives
Open accessAbstract
Coeliac disease (CD) is an immune-mediated enteropathy resulting from exposure to gluten in genetically predisposed individuals. Gluten proteins are partially digested by human proteases generating immunogenic peptides that cause inflammation in patients carrying HLA-DQ2 and DQ8 genes. Although intestinal dysbiosis has been associated with patients with CD, bacterial metabolism of gluten has not been studied in depth thus far. The aim of this study was to analyse the metabolic activity of intestinal bacteria associated with gluten intake in healthy individuals, CD patients and first-degree relatives of CD patients. Faecal samples belonging to twenty-two untreated CD patients, twenty treated CD patients, sixteen healthy volunteers on normal diet, eleven healthy volunteers on gluten-free diet (GFD), seventy-one relatives of CD patients on normal diet and sixty-nine relatives on GFD were tested for several proteolytic activities, cultivable bacteria involved in gluten metabolism, SCFA and the amount of gluten in faeces. We detected faecal peptidasic activity against the gluten-derived peptide 33-mer. CD patients showed differences in faecal glutenasic activity (FGA), faecal tryptic activity (FTA), SCFA and faecal gluten content with respect to healthy volunteers. Alterations in specific bacterial groups metabolising gluten such as Clostridium or Lactobacillus were reported in CD patients. Relatives showed similar parameters to CD patients (SCFA) and healthy volunteers (FTA and FGA). Our data support the fact that commensal microbial activity is an important factor in the metabolism of gluten proteins and that this activity is altered in CD patients.
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An increase in proteolytic activity towards gluten proteins has been observed in the duodenum and feces of celiac disease patients.
“an increase in proteolytic activity towards gluten proteins has been observed in the duodenum and feces of CeD patients.41,42”
From The emerging roles of bacterial proteases in intestinal diseases (2023) · cites this paper as [42]
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Cites
Diversity, stability and resilience of the human gut microbiota
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K., & Knight, R. (2012) · Nature · doi:10.1038/nature11550 · Cited by 5,533 · see citing works
The Oslo definitions for coeliac disease and related terms
Ludvigsson, J. F., Leffler, D. A., Bai, J. C., Biagi, F., Fasano, A., Green, P. H. R., Hadjivassiliou, M., Kaukinen, K., Kelly, C. P., Leonard, J. N., et al. (2013) · Gut · doi:10.1136/gutjnl-2011-301346 · Cited by 1,721 · see citing works
Structural Basis for Gluten Intolerance in Celiac Sprue
Shan, L., Molberg, Ø., Parrot, I., Hausch, F., Filiz, F., Gm, G., Sollid, L. M., & Khosla, C. (2002) · Science · doi:10.1126/science.1074129 · Cited by 1,576 · see citing works
The influence of diet on the gut microbiota
Scott, K. P., Gratz, S. W., Sheridan, P. O., Flint, H. J., & Duncan, S. H. (2013) · Pharmacological Research · doi:10.1016/j.phrs.2012.10.020 · Cited by 1,052 · see citing works
Intestinal luminal nitrogen metabolism: Role of the gut microbiota and consequences for the host
Davila, A.-M., Blachier, F., Gotteland, M., Andriamihaja, M., Benetti, P.-H., Sanz, Y., & Tomé, D. (2013) · Pharmacological Research · doi:10.1016/j.phrs.2012.11.005 · Cited by 548 · see citing works
Zhao, G., NYMAN, M. E., & Jönsson, J. Å. (2005) · Biomedical Chromatography · doi:10.1002/bmc.580 · Cited by 531 · see citing works
Celiac disease: pathogenesis of a model immunogenetic disease
Kagnoff, M. F. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30253 · Cited by 385 · see citing works
Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease
Collado, M. C., Donat, E., Ribes-Koninckx, C., Calabuig, M., & Sanz, Y. (2009) · Journal of Clinical Pathology · doi:10.1136/jcp.2008.061366 · Cited by 354 · see citing works
De Palma, G., Nadal, I., Medina, M., Donat, E., Ribes-Koninckx, C., Calabuig, M., & Sanz, Y. (2010) · BMC Microbiology · doi:10.1186/1471-2180-10-63 · Cited by 330 · see citing works
New chromogenic substrates for X-prolyl dipeptidyl-aminopeptidase
Nagatsu, T., Hino, M., Fuyamada, H., Hayakawa, T., Sakakibara, S., Nakagawa, Y., & Takemoto, T. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90227-x · Cited by 306 · see citing works
Shan, L., Qiao, S., Arentz–Hansen, H., Molberg, Ø., Gm, G., Sollid, L. M., & Khosla, C. (2005) · Journal of Proteome Research · doi:10.1021/pr050173t · Cited by 274 · see citing works
Contribution of the microflora to proteolysis in the human large intestine
Macfarlane, G. T., Allison, C., Gibson, S. A. W., & Cummings, J. H. (1988) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1988.tb02427.x · Cited by 237 · see citing works
Davila, A.-M., Blachier, F., Gotteland, M., Andriamihaja, M., Benetti, P.-H., Sanz, Y., & Tomé, D. (2013) · Pharmacological Research · doi:10.1016/j.phrs.2013.01.003 · Cited by 231 · see citing works
Collado, M. C., Donat, E., Ribes-Koninckx, C., Calabuig, M., & Sanz, Y. (2008) · BMC Microbiology · doi:10.1186/1471-2180-8-232 · Cited by 220 · see citing works
Comino, I., Real, A., Vivas, S., Siglez, M. Á., Caminero, A., Nistal, E., Casqueiro, J., Rodríguez‐Herrera, A., Cebolla, Á., & Sousa, C. (2012) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.026708 · Cited by 188 · see citing works
Self-citationNistal, E., Caminero, A., Vivas, S., Morales, J., de Miera, L. E. S., Rodrı́guez-Aparicio, L. B., & Casqueiro, J. (2012) · Biochimie · doi:10.1016/j.biochi.2012.03.025 · Cited by 173 · see citing works
Self-citationCaminero, A., Herrán, A. R., Nistal, E., Pérez-Andrés, J., Vaquero, L. M., Vivas, S., de Morales, J. M. G. R., Albillos, S. M., & Casqueiro, J. (2014) · FEMS Microbiology Ecology · doi:10.1111/1574-6941.12295 · Cited by 155 · see citing works
Self-citationUnraveling the Ties between Celiac Disease and Intestinal Microbiota
Sanz, Y., Palma, G. D., & Laparra, J. M. (2011) · International Reviews of Immunology · doi:10.3109/08830185.2011.599084 · Cited by 141 · see citing works
Gut Microflora Associated Characteristics in Children with Celiac Disease
Tjellström, B., Stenhammar, L., Högberg, L., Fälth‐Magnusson, K., Magnusson, K., Midtvedt, T., Sundqvist, T., & Norin, E. L. (2005) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2005.00313.x · Cited by 137 · see citing works
Richardson, A. J., McKain, N., & Wallace, R. J. (2013) · BMC Microbiology · doi:10.1186/1471-2180-13-6 · Cited by 134 · see citing works
Laparra, J. M., & Sanz, Y. (2010) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22459 · Cited by 131 · see citing works
Zamakhchari, M., Wei, G., Dewhirst, F. E., Lee, J., Schuppan, D., Oppenheim, F. G., & Helmerhorst, E. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024455 · Cited by 121 · see citing works
Fernandez-Feo, M., Wei, G., Blumenkranz, G., Dewhirst, F. E., Schuppan, D., Oppenheim, F. G., & Helmerhorst, E. J. (2013) · Clinical Microbiology and Infection · doi:10.1111/1469-0691.12249 · Cited by 110 · see citing works
Discerning the Role of Bacteroides fragilis in Celiac Disease Pathogenesis
Sánchez, E., Laparra, J. M., & Sanz, Y. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.00563-12 · Cited by 101 · see citing works
Bernardo, D., Garrote, J. A., Nadal, I., León, A. J., Calvo, C., Fernández-Salazar, L., Blanco-Quirós, A., Sanz, Y., & Arranz, E. (2009) · Gut · doi:10.1136/gut.2008.167296 · Cited by 98 · see citing works
Discovery of a Novel and Rich Source of Gluten-Degrading Microbial Enzymes in the Oral Cavity
Helmerhorst, E. J., Zamakhchari, M., Schuppan, D., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013264 · Cited by 93 · see citing works
Fasano, A. (2009) · Scientific American · doi:10.1038/scientificamerican0809-54 · Cited by 82 · see citing works
Fecal Protease Activity Is Associated with Compositional Alterations in the Intestinal Microbiota
Carroll, I. M., Ringel‐Kulka, T., Ferrier, L., Wu, M. C., Siddle, J. P., Bueno, L. P., & Ringel, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078017 · Cited by 70 · see citing works
Dipeptidyl peptidase IV and adenosine deaminase activity
Elgün, S., Keskinege, A., & Kumbasar, H. (1999) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(99)00039-6 · Cited by 62 · see citing works
Camarca, A., Mastro, A. D., & Gianfrani, C. (2012) · Endocrine Metabolic & Immune Disorders - Drug Targets · doi:10.2174/187153012800493549 · Cited by 53 · see citing works
Midtvedt, T., Zabarovsky, E. R., Norin, E. L., Bark, J., Gizatullin, R. Z., Kashuba, V. I., Ljungqvist, O. H., Zabarovska, V. I., Möllby, R., & Ernberg, I. T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066074 · Cited by 49 · see citing works
A sensitive method for the assay of serum prolyl endopeptidase.
Goossens, F., Meester, I. D., Vanhoof, G., et al. (1992) · PubMed · Cited by 43 · see citing works
Douglas, A. P., & Booth, C. C. (1970) · Clinical Science · doi:10.1042/cs0380011 · Cited by 42 · see citing works
A gluten metabolism study in healthy individuals shows the presence of faecal glutenasic activity
Caminero, A., Nistal, E., Arias, L., Vivas, S., Comino, I., Real, A., Sousa, C., Morales, J., Ferrero, M. Á. M., Rodrı́guez-Aparicio, L. B., et al. (2011) · European Journal of Nutrition · doi:10.1007/s00394-011-0214-3 · Cited by 41 · see citing works
Self-citationBreakdown of gliadin peptides by intestinal brush borders from coeliac patients.
Bruce, G., Woodley, J. F., & Swan, C. H. J. (1984) · Gut · doi:10.1136/gut.25.9.919 · Cited by 32 · see citing works
Ranilla, M. J., Carro, M. D., López, S., et al. (2001) · British Journal Of Nutrition · doi:10.1079/bjn2001475 · Cited by 26 · see citing works
Intestinal peptidases and sucrase in coeliac disease
Sjöström, H., Norén, O., Krasilnikoff, P. A., et al. (1981) · Clinica Chimica Acta · doi:10.1016/0009-8981(81)90136-4 · Cited by 23 · see citing works
Non-dietary forms of treatment for adult celiac disease
Freeman, H. J. (2013) · World Journal of Gastrointestinal Pharmacology and Therapeutics · doi:10.4292/wjgpt.v4.i4.108 · Cited by 15 · see citing works
Digestion of Gliadin Peptides by Intestinal Mucosa from Control or Coeliac Children
Carchon, H. A., Serrus, M., & Eggermont, E. (2009) · Digestion · doi:10.1159/000198315 · Cited by 11 · see citing works
Verdu, E. F. (2012) · The American Journal of Gastroenterology · doi:10.1038/ajg.2012.291 · Cited by 10 · see citing works
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Research works printed but not linked: 1
- Caminero A, Nistal E, Herrán A, et al. (2013) Gluten metabolism in humans: involvement of the gut microbiota. In Whole Wheat and Rice in Disease pp. 157-170 [RR Watson, VR Preedy and S Zibadi, editors]. Amsterdam: Elsevier.
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Koppel, N., Maini Rekdal, V., & Balskus, E. P. (2017) · Science · doi:10.1126/science.aag2770 · Cited by 1,080 · see citing works
Caminero, A., Galipeau, H. J., McCarville, J. L., Johnston, C. W., Bernier, S. P., Russell, A. K., Jury, J., Herran, A. R., Casqueiro, J., Tye-Din, J. A., et al. (2016) · Gastroenterology · doi:10.1053/j.gastro.2016.06.041 · Cited by 250 · see citing works
Self-citationCaminero, A., McCarville, J. L., Galipeau, H. J., Deraison, C., Bernier, S. P., Constante, M., Rolland, C., Meisel, M., Murray, J. A., Yu, X. B., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09037-9 · Cited by 139 · see citing works
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Caminero, A., Guzman, M., Libertucci, J., & Lomax, A. E. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2181922 · Cited by 92 · see citing works
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- Authors
- Caminero, A., Nistal, E., Herrán, A. R., Pérez-Andrés, J., Ferrero, M. A., Vaquero Ayala, L., Vivas, S., Ruiz de Morales, J. M. G., Albillos, S. M., & Casqueiro, F. J.
- Affiliations
- Universidad de León (ES)
- Hospital Universitario de León (ES)
- Instituto de Biotecnología de León (ES)
- Corresponding author
- Caminero, Alberto
- Venue
- British Journal of Nutrition
- Publisher
- Cambridge University Press (CUP)
- Published
- 2015-08-26
- Volume
- 114
- Issue
- 8
- Pages
- 1157-1167
- ISSN
- 0007-1145 (ISSN-L)
- 1475-2662
- OpenAlex
- W1841699601
- Cited by
- 70
- References
- 40
- Citations by year
- 2025: 7 · 2024: 7 · 2023: 8 · 2022: 8 · 2021: 8 · 2020: 9 · 2019: 11 · 2018: 3 · 2017: 7 · 2016: 2
- FWCI
- 4.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- British Journal Of Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministerio de Educación, Cultura y Deporte
- Junta de Castilla y León
- Instituto de Salud Carlos III (FIS PI10/02447)
- European Social Fund
- Topics
- Health Sciences › Medicine › Gastroenterology › Celiac Disease Research and Management
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- celiac disease, intestinal bacteria, tryptic activity, short-chain fatty acids, gluten-free diet, first-degree relatives, Clostridium, Lactobacillus, gut dysbiosis
- MeSH terms
- Bacillota, Adolescent, Adult, Alleles, Caproates, Celiac Disease, Feces, Glutens, HLA-DQ Antigens, Humans, Intestinal Mucosa, Intestines, Middle Aged, Pentanoic Acids, Propionates, Acetic Acid, Butyric Acid, Proteobacteria, Actinobacteria, Diet, Gluten-Free, Young Adult, Healthy Volunteers
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