Gluten-free diet affects fecal small non-coding RNA profiles and microbiome composition in celiac disease supporting a host-gut microbiota crosstalk
ABSTRACTCurrent treatment for celiac disease (CD) is adhering to a gluten-free diet (GFD), although its long-term molecular effects are still undescribed. New molecular features detectable in stool may improve and facilitate noninvasive clinical management of CD. For this purpose, fecal small non-co...
| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Taylor & Francis Group
2023-12-01
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| Series: | Gut Microbes |
| Subjects: | |
| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2023.2172955 |
| _version_ | 1827303779855237120 |
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| author | Antonio Francavilla Giulio Ferrero Barbara Pardini Sonia Tarallo Laura Zanatto Gian Paolo Caviglia Sabina Sieri Sara Grioni Giulia Francescato Francesco Stalla Cristina Guiotto Lucia Crocella Marco Astegiano Mauro Bruno Pier Luigi Calvo Paolo Vineis Davide Giuseppe Ribaldone Alessio Naccarati |
| author_facet | Antonio Francavilla Giulio Ferrero Barbara Pardini Sonia Tarallo Laura Zanatto Gian Paolo Caviglia Sabina Sieri Sara Grioni Giulia Francescato Francesco Stalla Cristina Guiotto Lucia Crocella Marco Astegiano Mauro Bruno Pier Luigi Calvo Paolo Vineis Davide Giuseppe Ribaldone Alessio Naccarati |
| author_sort | Antonio Francavilla |
| collection | DOAJ |
| description | ABSTRACTCurrent treatment for celiac disease (CD) is adhering to a gluten-free diet (GFD), although its long-term molecular effects are still undescribed. New molecular features detectable in stool may improve and facilitate noninvasive clinical management of CD. For this purpose, fecal small non-coding RNAs (sncRNAs) and gut microbiome profiles were concomitantly explored in CD subjects in relation to strict (or not) GFD adherence over time. In this observational study, we performed small RNA and shotgun metagenomic sequencing in stool from 63 treated CD (tCD) and 3 untreated subjects as well as 66 sex- and age-matched healthy controls. tCD included 51 individuals on strict GFD and with negative transglutaminase (TG) serology (tCD-TG-) and 12 symptomatic with not strict/short-time of GFD adherence and positive TG serology (tCD-TG+). Samples from additional 40 healthy adult individuals and a cohort of 19 untreated pediatric CD subjects and 19 sex/age matched controls were analyzed to further test the outcomes. Several miRNA and microbial profiles were altered in tCD subjects (adj. p < .05). Findings were validated in the external group of adult controls. In tCD-TG-, GFD duration correlated with five miRNA levels (p < .05): for miR-4533-3p and miR-2681-3p, the longer the diet adherence, the less the expression differed from controls. tCD-TG+ and untreated pediatric CD patients showed a similar miRNA dysregulation. Immune-response, trans-membrane transport and cell death pathways were enriched in targets of identified miRNAs. Bifidobacterium longum, Ruminococcus bicirculans, and Haemophilus parainfluenzae abundances shifted (adj. p < .05) with a progressive reduction of denitrification pathways with GFD length. Integrative analysis highlighted 121 miRNA-bacterial relationships (adj. p < .05). Specific molecular patterns in stool characterize CD subjects, reflecting either the long-term GFD effects or the gut inflammatory status, in case of a not strict/short-time adherence. Our findings suggest novel host-microbial interplays and could help the discovery of biomarkers for GFD monitoring over time. |
| first_indexed | 2024-03-11T14:20:05Z |
| format | Article |
| id | doaj.art-1b4eb8277e3d413d95b823eb3dcd1c08 |
| institution | Directory Open Access Journal |
| issn | 1949-0976 1949-0984 |
| language | English |
| last_indexed | 2024-04-24T17:06:54Z |
| publishDate | 2023-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj.art-1b4eb8277e3d413d95b823eb3dcd1c082024-03-28T22:38:20ZengTaylor & Francis GroupGut Microbes1949-09761949-09842023-12-0115110.1080/19490976.2023.2172955Gluten-free diet affects fecal small non-coding RNA profiles and microbiome composition in celiac disease supporting a host-gut microbiota crosstalkAntonio Francavilla0Giulio Ferrero1Barbara Pardini2Sonia Tarallo3Laura Zanatto4Gian Paolo Caviglia5Sabina Sieri6Sara Grioni7Giulia Francescato8Francesco Stalla9Cristina Guiotto10Lucia Crocella11Marco Astegiano12Mauro Bruno13Pier Luigi Calvo14Paolo Vineis15Davide Giuseppe Ribaldone16Alessio Naccarati17Molecular and Genetic Epidemiology, Italian Institute for Genomic Medicine (IIGM), Torino, ItalyDepartment of Computer Sciences, University of Torino, Torino, ItalyMolecular and Genetic Epidemiology, Italian Institute for Genomic Medicine (IIGM), Torino, ItalyMolecular and Genetic Epidemiology, Italian Institute for Genomic Medicine (IIGM), Torino, ItalyMolecular and Genetic Epidemiology, Italian Institute for Genomic Medicine (IIGM), Torino, ItalyDivision of Gastroenterology, Department of Medical Sciences, University of Torino, Torino, ItalyEpidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milano, ItalyEpidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milano, ItalyMolecular and Genetic Epidemiology, Italian Institute for Genomic Medicine (IIGM), Torino, ItalyGastroenterology and Digestive Endoscopy Unit, “Città della Salute e della Scienza” Hospital, Torino, ItalyGastroenterology, Hospital Mauriziano Umberto I, Torino, ItalyGastroenterology, Hospital Mauriziano Umberto I, Torino, ItalyGastroenterology and Digestive Endoscopy Unit, “Città della Salute e della Scienza” Hospital, Torino, ItalyGastroenterology and Digestive Endoscopy Unit, “Città della Salute e della Scienza” Hospital, Torino, ItalyPediatric Gastroenterology Unit, Department of Pediatrics, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di, Torino, ItalySchool of Public Health, Imperial College London, London, UKDivision of Gastroenterology, Department of Medical Sciences, University of Torino, Torino, ItalyMolecular and Genetic Epidemiology, Italian Institute for Genomic Medicine (IIGM), Torino, ItalyABSTRACTCurrent treatment for celiac disease (CD) is adhering to a gluten-free diet (GFD), although its long-term molecular effects are still undescribed. New molecular features detectable in stool may improve and facilitate noninvasive clinical management of CD. For this purpose, fecal small non-coding RNAs (sncRNAs) and gut microbiome profiles were concomitantly explored in CD subjects in relation to strict (or not) GFD adherence over time. In this observational study, we performed small RNA and shotgun metagenomic sequencing in stool from 63 treated CD (tCD) and 3 untreated subjects as well as 66 sex- and age-matched healthy controls. tCD included 51 individuals on strict GFD and with negative transglutaminase (TG) serology (tCD-TG-) and 12 symptomatic with not strict/short-time of GFD adherence and positive TG serology (tCD-TG+). Samples from additional 40 healthy adult individuals and a cohort of 19 untreated pediatric CD subjects and 19 sex/age matched controls were analyzed to further test the outcomes. Several miRNA and microbial profiles were altered in tCD subjects (adj. p < .05). Findings were validated in the external group of adult controls. In tCD-TG-, GFD duration correlated with five miRNA levels (p < .05): for miR-4533-3p and miR-2681-3p, the longer the diet adherence, the less the expression differed from controls. tCD-TG+ and untreated pediatric CD patients showed a similar miRNA dysregulation. Immune-response, trans-membrane transport and cell death pathways were enriched in targets of identified miRNAs. Bifidobacterium longum, Ruminococcus bicirculans, and Haemophilus parainfluenzae abundances shifted (adj. p < .05) with a progressive reduction of denitrification pathways with GFD length. Integrative analysis highlighted 121 miRNA-bacterial relationships (adj. p < .05). Specific molecular patterns in stool characterize CD subjects, reflecting either the long-term GFD effects or the gut inflammatory status, in case of a not strict/short-time adherence. Our findings suggest novel host-microbial interplays and could help the discovery of biomarkers for GFD monitoring over time.https://www.tandfonline.com/doi/10.1080/19490976.2023.2172955Stool microRNAsgut microbiotaceliac diseasegluten-free diet |
| spellingShingle | Antonio Francavilla Giulio Ferrero Barbara Pardini Sonia Tarallo Laura Zanatto Gian Paolo Caviglia Sabina Sieri Sara Grioni Giulia Francescato Francesco Stalla Cristina Guiotto Lucia Crocella Marco Astegiano Mauro Bruno Pier Luigi Calvo Paolo Vineis Davide Giuseppe Ribaldone Alessio Naccarati Gluten-free diet affects fecal small non-coding RNA profiles and microbiome composition in celiac disease supporting a host-gut microbiota crosstalk Gut Microbes Stool microRNAs gut microbiota celiac disease gluten-free diet |
| title | Gluten-free diet affects fecal small non-coding RNA profiles and microbiome composition in celiac disease supporting a host-gut microbiota crosstalk |
| title_full | Gluten-free diet affects fecal small non-coding RNA profiles and microbiome composition in celiac disease supporting a host-gut microbiota crosstalk |
| title_fullStr | Gluten-free diet affects fecal small non-coding RNA profiles and microbiome composition in celiac disease supporting a host-gut microbiota crosstalk |
| title_full_unstemmed | Gluten-free diet affects fecal small non-coding RNA profiles and microbiome composition in celiac disease supporting a host-gut microbiota crosstalk |
| title_short | Gluten-free diet affects fecal small non-coding RNA profiles and microbiome composition in celiac disease supporting a host-gut microbiota crosstalk |
| title_sort | gluten free diet affects fecal small non coding rna profiles and microbiome composition in celiac disease supporting a host gut microbiota crosstalk |
| topic | Stool microRNAs gut microbiota celiac disease gluten-free diet |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2023.2172955 |
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