CoChat
Sign Up
Cited by 66Animal Nutrition and PhysiologyGut microbiota and healthGastrointestinal motility and disorders

The Olfactory Receptor OR51E1 Is Present along the Gastrointestinal Tract of Pigs, Co-Localizes with Enteroendocrine Cells and Is Modulated by Intestinal Microbiota

Open access
Priori, Davide, Colombo, Michela, Clavenzani, Paolo, Jansman, Alfons J. M., Lallès, Jean-Paul, Trevisi, Paolo, Bosi, Paolo·2015·PLOS ONE
DOI 10.1371/journal.pone.0129501PMC PMC4468170
Open this paper in CoChat — free accountOpen PDF

Abstract

UNLABELLED: The relevance of the butyrate-sensing olfactory receptor OR51E1 for gastrointestinal (GIT) functioning has not been considered so far. We investigated in young pigs the distribution of OR51E1 along the GIT, its relation with some endocrine markers, its variation with age and after interventions affecting the gut environment and intestinal microbiota. Immuno-reactive cells for OR51E1 and chromogranin A (CgA) were counted in cardial (CA), fundic (FU), pyloric (PL) duodenal (DU), jejunal (JE), ileal (IL), cecal (CE), colonic (CO) and rectal (RE) mucosae. OR51E1 co-localization with serotonin (5HT) and peptide YY (PYY) were evaluated in PL and CO respectively. FU and PL tissues were also sampled from 84 piglets reared from sows receiving either or not oral antibiotics (amoxicillin) around parturition, and sacrificed at days 14, 21, 28 (weaning) and 42 of age. JE samples were also obtained from 12 caesarean-derived piglets that were orally associated with simple (SA) or complex (CA) microbiota in the postnatal phase, and of which on days 26-37 of age jejunal loops were perfused for 8 h with enterotoxigenic Escherichia coli F4 (ETEC), Lactobacillus amylovorus or saline (CTRL). Tissue densities of OR51E1+ cells were in decreasing order: PL=DU>FU=CA>JE=IL=CE=CO=RE. OR51E1+ cells showed an enteroendocrine nature containing gastrointestinal hormones such as PYY or 5HT. OR51E1 gene expression in PL and FU increased during and after the suckling period (p<0.05). It was marginally reduced in offspring from antibiotic-treated sows (tendency, p=0.073), vs. CONTROL: Jejunal OR51E1 gene expression was reduced in piglets early associated with SA, compared with CA, and in ETEC-perfused loops vs. CTRL (p<0.01). Our results indicate that OR51E1 is related to GIT enteroendocrine activity. Moreover age, pathogen challenge and dietary manipulations influencing the gastrointestinal luminal microenvironment significantly affect the OR51E1 gene expression in GIT tissues presumably in association with the release of microbial metabolites.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0129501

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Butyrate activates the niacin receptor hydroxycarboxylic acid receptor 2 and the olfactory receptor OR51E1.

    “A lesser-known colonic GPCR activated by butyrate is the receptor for niacin: hydroxycarboxylic acid receptor 2 (Thangaraju et al., 2009).Another receptor activated by butyrate is the olfactory receptor family 51 subfamily E member 1 (OR51E1 for humans, olfactory receptor 558 -Olfr558 for mice) (Priori et al., 2015).”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Priori et al., 2015

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 48

  1. [1]Flegel C, Manteniotis S, Osthold S, Hatt H, Gisselmann G. Expression profile of ectopic olfactory receptors determined by deep sequencing. PLOS ONE, 2013; 8(2): e55368 10.1371/journal.pone.0055368 23405139 PMC3566163 · DOI
  2. [2]Braun T, Voland P, Kunz L, Prinz C, Gratzl M. Enterochromaffin cells of the human gut: sensors for spices and odorants. Gastroenterology, 2007; 132: 1890– 1901. 17484882
  3. [3]Foster SR, Roura E, Thomas WG. Extrasensory perception: Odorant and taste receptors beyond the nose and mouth. Pharmacol Therapeut, 2014; 142: 41– 61. 24280065
  4. [4]Colombo M, Priori D, Trevisi P, Bosi P. Differential gene expression in the oxyntic and pyloric mucosa of the young pig. PLOS ONE, 2014; 9(10): e111447 10.1371/journal.pone.0111447 25357124 PMC4214732 · DOI
  5. [5]Fujita Y, Takahashi T, Suzuki A, Kawashima K, Nara F, Koishi R. Deorphanization of Dresden G protein-coupled receptor for an odorant receptor. J Recept Sig Transd, 2007; 27: 323– 334. 17885925
  6. [6]Li YR, Matsunami H M. Activation state of the M3 muscarinic acetylcholine receptor modulates mammalian odorant receptor signaling. Sci Signal, 2011; 4(155): ra1 10.1126/scisignal.2001230 21224444 PMC3034603 · DOI
  7. [7]Adipietro KA, Mainland JD, Matsunami H. Functional evolution of mammalian odorant receptors. PLOS Genet, 2012; 8(7): e1002821 10.1371/journal.pgen.1002821 22807691 PMC3395614 · DOI
  8. [8]Canani RB, Costanzo MD, Leone L, Pedata M., Meli R., Calignano A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol, 2011; 17: 1519– 1528. 10.3748/wjg.v17.i12 21472114 PMC3070119 · DOI
  9. [9]Leja J, Essaghir A, Essand M, Wester K. Novel markers for enterochromaffin cells and gastrointestinal neuroendocrine carcinomas. Modern Pathol; 2011; 22: 261– 272. 18953328
  10. [10]Thompson CL, Wang B, Holmes AJ. The immediate environment during postnatal development has long-term impact on gut community structure in pigs. ISME J, 2008; 2: 739– 748. 10.1038/ismej.2008.29 18356821 · DOI
  11. [11]Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, et al Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc. P Natl Acad Sci USA, 2010; 107: 18933– 18938. 10.1073/pnas.1007028107 20937875 PMC2973891 · DOI · Paper page
  12. [12]Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett C, Knight R, Gordon JI. The human microbiome project: exploring the microbial part of ourselves in a changing world. Nature, 2007; 449: 804– 810. 17943116 PMC3709439
  13. [14]Longo WE, Ballantyne GH, Savoca PE, Adrian TE, Bilchik AJ, Modlin IM. Short-chain fatty acid release of peptide YY in the isolated rabbit distal colon. Scand J Gastroenterol, 1991; 26: 442– 448. 2034997
  14. [15]Berge RD, Savage D. Immune responses of specific pathogen-free and gnotobiotic mice to antigens of indigenous and nonindigenous microorganisms. Infect Immun, 1975; 11: 320– 329. 1089600 PMC415064
  15. [16]Dibner JJ, Richards JD, Knight CD. Microbial imprinting in gut development and health. J Appl Poult Res, 2008; 17: 174– 188.
  16. [18]Arnal ME, Zhang J, Messori S, Bosi P, Smidt H, Lallès JP. Early changes in microbial colonization selectively modulate intestinal enzymes, but not inducible heat shock proteins in young adult swine. PLOS ONE, 2014; 9(2), e87967 10.1371/journal.pone.0087967 24505340 PMC3913709 · DOI
  17. [19]Arnal ME, Zhang J, Erridge C, Smidt H, Lallès JP. Maternal Antibiotic-Induced Early Changes in Microbial Colonization Selectively Modulate Colonic Permeability and Inducible Heat Shock Proteins, and Digesta Concentrations of Alkaline Phosphatase and TLR-Stimulants in Swine Offspring. PLOS ONE, 2015; 10(2), e0118092 10.1371/journal.pone.0118092 25689154 PMC4331088 · DOI
  18. [20]Schumann A, Nutten S, Donnicola D, Comelli EM, Mansourian R, et al Neonatal antibiotic treatment alters gastrointestinal tract developmental gene expression and intestinal barrier transcriptome. Physiol Genomics, 2005; 23: 235– 245. 16131529
  19. [21]Nutten S, Schumann A, Donnicola D, Mercenier A, Rami S, et al Antibiotic administration early in life impairs specific humoral responses to an oral antigen and increases intestinal mast cell numbers and mediator concentrations. Clin Vaccine Immunol, 2007; 14: 190– 197. 17151185 PMC1797787
  20. [22]Godden S, McMartin S, Feirtag J, Stabel J, Bey R, Goyal S, et al Heat treatment of bovine colostrum. II. Effects of heating duration on pathogen viability and IgG. J Dairy Sci, 2006; 89: 3476– 3483. 16899682
  21. [23]Elizondo-Salazar JA, Heinrichs AJ. Feeding heat-treated colostrum or unheated colostrum with two different bacterial concentrations to neonatal dairy calves. J Dairy Sci, 2009; 92: 4565– 4571. 10.3168/jds.2009-2188 19700719 · DOI
  22. [24]Laycock G, Sait L, Inman C, Lewis M, Smidt H, van Diemen P, et al A defined intestinal colonization microbiota for gnotobiotic pigs. Vet Immunol Immunopathol, 2012; 149: 216– 224. 10.1016/j.vetimm.2012.07.004 22868203 · DOI
  23. [25]Nabuurs MJ, Hoogendoorn A, van Zijderveld FG, van der Klis JD. A long-term perfusion test to measure net absorption in the small intestine of weaned pigs. Res Vet Sci, 1993; 55: 108– 114. 8378603
  24. [26]Nabuurs MJ, Hoogendoorn A, van Zijderveld FG. Effects of weaning and enterotoxigenic Escherichia coli on net absorption in the small intestine of pigs. Res Vet Sci, 1994; 56: 379– 385. 8073191
  25. [27]Mazzoni M, De Giorgio R, Latorre R, Vallorani C, Bosi P, Trevisi P et al Expression and regulation of alpha-transducin in the pig gastrointestinal tract. J Cell Mol Med, 2013; 17: 466– 474. 10.1111/jcmm.12026 23414137 PMC3640731 · DOI
  26. [28]Trevisi P, Gandolfi G, Priori D, Messori S, Colombo M, et al Age-related expression of the polymeric immunoglobulin receptor (pIgR) in the gastric mucosa of young pigs. PLOS ONE, 2013; 8: e81473 10.1371/journal.pone.0081473 24236214 PMC3827463 · DOI
  27. [29]Nygard AB, Jørgensen CB, Cirera S, Fredholm M. Selection of reference genes for gene expression studies in pig tissues using SYBR green qPCR. BMC Mol Biol, 2007; 8: 67 17697375 PMC2000887
  28. [30]Glusman G, Yanai I, Rubin I, Lancet D. The complete human olfactory subgenome. Genome Res, 2001; 11: 685– 702. 11337468
  29. [31]Zhang X, Firestein S. The olfactory receptor gene superfamily of the mouse. Nat Neurosci, 2002; 5: 124– 133. 11802173
  30. [32]Nguyen DT, Lee K, Choi H, Choi MK, Le MT, Song N,. et al The complete swine olfactory subgenome: expansion of the olfactory gene repertoire in the pig genome. BMC Genomics, 2006; 13: 584. PMC3499278 23153364
  31. [33]Lee K, Nguyen DT, Choi M, Cha SY, Kim JH, Dadi H, et al Analysis of cattle olfactory subgenome: the first detail study on the characteristics of the complete olfactory receptor repertoire of a ruminant. BMC Genomics, 2013; 14: 596 10.1186/1471-2164-14-596 24004971 PMC3766653 · DOI
  32. [34]Feldmesser E, Olender T, Khen M, Yanai I, Ophir R, Lancet D. Widespread ectopic expression of olfactory receptor genes. BMC Genomics, 2006; 7: 121 16716209 PMC1508154
  33. [35]Kang N, Koo J. Olfactory receptors in non-chemosensory tissues. BMB Rep, 2012; 45: 612– 622. 23186999 PMC4133803
  34. [37]Gershon MD. 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract. Curr Opin Endocrinol Diabetes Obes, 2013; 20: 14– 21. 10.1097/MED.0b013e32835bc703 23222853 PMC3708472 · DOI · Paper page
  35. [38]Li N, Ghia JE, Wang H, McClemens J, Cote F, Suehiro Y, et al Serotonin activates dendritic cell function in the context of gut inflammation. Am J Pathol, 2011; 178: 662– 671. 10.1016/j.ajpath.2010.10.028 21281798 PMC3069907 · DOI
  36. [39]Gu X, Karp PH, Brody SL, Pierce RA, Welsh MJ, Holtzman MJ, et al Chemosensory Functions for Pulmonary Neuroendocrine Cells. Am J Respir Cell Mol Biol, 2014; 50: 637– 646. 10.1165/rcmb.2013-0199OC 24134460 PMC4068934 · DOI
  37. [40]Theodorakis MJ, Carlson O, Michopoulos S, Doyle ME, Juhaszova M, Petraki K, et al Human duodenal enteroendocrine cells: source of both incretin peptides, GLP-1 and GIP. Am J Physiol-Endoc M, 2006; 290: E550– E559. 16219666
  38. [41]Cherbut C, Ferrier L, Rozé C, Anini Y, Blottière H, Lecannu G, et al Short-chain fatty acids modify colonic motility through nerves and polypeptide YY release in the rat. Am J Physiol, 1988; 275: G1415– G1422. 9843779
  39. [42]Karaki SI, Tazoe H, Hayashi H, Kashiwabara H, Tooyama K, Suzuki Y, et al Expression of the short-chain fatty acid receptor, GPR43, in the human colon. J Mol Histol, 2008; 39: 135– 142. 17899402
  40. [43]Tazoe H, Otomo Y, Karaki SI, Kato I, Fukami Y, Terasaki M, et al Expression of short-chain fatty acid receptor GPR41 in the human colon. Biomed Res, 2009; 30: 149– 156. 19574715
  41. [44]Tajima K, Ohmori H, Aminov RI, Kobashi Y, Kawashima T. Fermented liquid feed enhances bacterial diversity in piglet intestine. Anaerobe, 2010; 16: 6– 11. 10.1016/j.anaerobe.2009.04.002 19393756 · DOI
  42. [45]Metzler‐Zebeli BU, Zijlstra RT, Mosenthin R, Gänzle MG. Dietary calcium phosphate content and oat β‐glucan influence gastrointestinal microbiota, butyrate‐producing bacteria and butyrate fermentation in weaned pigs. FEMS Microbiol Ecol, 2011; 75: 402– 413. 10.1111/j.1574-6941.2010.01017.x 21166688 · DOI
  43. [46]Zentek J, Buchheit-Renko S, Männer K, Pieper R, Vahjen W. Intestinal concentrations of free and encapsulated dietary medium-chain fatty acids and effects on gastric microbial ecology and bacterial metabolic products in the digestive tract of piglets. Arch Anim Nutr, 2012; 66: 14– 26. 22397093
  44. [48]Levine UY, Looft T, Allen HK, Stanton TB. Butyrate-producing bacteria, including mucin degraders, from the swine intestinal tract. Appl Environ Microb, 2013; 79: 3879– 3881. 10.1128/AEM.00589-13 23584773 PMC3675948 · DOI
  45. [49]Jansman A JM, Zhang J, Koopmans SJ, Dekker RA, Smidt H. Effects of a simple or a complex starter microbiota on intestinal microbiota composition in caesarean derived piglets. J Anim Sci, 2012; 90(Suppl.4): 433– 435. 10.2527/jas.53850 23365401 · DOI
  46. [50]Priori D, Colombo M, Koopmans SJ, Jansman AJM, Schiavo G, Trevisi P, et al Effects of a simple or a complex starter microbiota on the gastric transcriptome profile of caesarean derived piglets In: Energy and protein metabolism and nutrition in sustainable animal production. Wageningen Academic Publishers, The Netherlands; 2013 pp. 295– 296.
  47. [51]Kiers JL, Nout MJ, Rombouts FM, van Andel EE, Nabuurs MJ, van der Meulen J. Effect of processed and fermented soyabeans on net absorption in enterotoxigenic Escherichia coli-infected piglet small intestine. Brit J Nutr, 2006; 95: 1193– 1198. 16768844
  48. [52]Bosi P, Casini L, Finamore A, Cremokolini C, Merialdi G, Trevisi P, et al Spray-dried plasma improves growth performance and reduces inflammatory status of weaned pigs challenged with enterotoxigenic Escherichia coli K88. J Anim Sci, 2004; 82: 1764– 1772. 15217004

Cited by

Sorted by citations

Authors
Priori, D., Colombo, M., Clavenzani, P., Jansman, A. J. M., Lallès, J.-P., Trevisi, P., & Bosi, P.
Affiliations
  • University of Bologna (IT)
  • Wageningen University & Research (NL)
  • Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
Corresponding author
Bosi, Paolo
ORCID
Venue
PLOS ONE
Publisher
Public Library of Science (PLoS)
Published
2015-06-15
Volume
10
Issue
6
Pages
e0129501
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0129501
PMC
PMC4468170
OpenAlex
W1515656431
Cited by
66
References
4
Citations by year
2026: 1 · 2025: 5 · 2024: 8 · 2023: 8 · 2022: 7 · 2021: 11 · 2020: 2 · 2019: 8 · 2018: 6 · 2017: 5 · 2016: 3 · 2015: 1
FWCI
7.07
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • Socio-Environmental Systems Modeling (submittedVersion, cc-by)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders
European Commission (227549)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords
olfactory receptors, enteroendocrine cells, gastrointestinal tract, pigs, gut microbiota, peptide YY, serotonin, chromogranin A, antibiotic exposure, enterotoxigenic Escherichia coli, Lactobacillus amylovorus, gastrointestinal hormones, age-related gene expression
MeSH terms
Gastrointestinal Microbiome, Animals, Anti-Bacterial Agents, Swine, Gene Expression, Receptors, Odorant, Enteroendocrine Cells, Gastrointestinal Tract

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review