Effect of Mucine 4 and Fucosyltransferase 1 genetic variants on gut homoeostasis of growing healthy pigs

Diana Luise; Vincenzo Motta; Micol Bertocchi; Chiara Salvarani; Paolo Clavenzani; Flaminia Fanelli; Uberto Pagotto; Paolo Bosi; Paolo Trevisi

doi:10.1111/jpn.13063

Effect of Mucine 4 and Fucosyltransferase 1 genetic variants on gut homoeostasis of growing healthy pigs

J Anim Physiol Anim Nutr (Berl). 2019 May;103(3):801-812. doi: 10.1111/jpn.13063. Epub 2019 Feb 7.

Authors

Diana Luise¹, Vincenzo Motta¹, Micol Bertocchi², Chiara Salvarani¹, Paolo Clavenzani³, Flaminia Fanelli⁴, Uberto Pagotto⁴, Paolo Bosi¹, Paolo Trevisi¹

Affiliations

¹ Department of Agricultural and Food Sciences, University of Bologna, Bologna, Italy.
² Department of Agricultural, Environmental and Food Sciences, University of Molise, Campobasso, Italy.
³ Department of Veterinary Medical Sciences, University of Bologna, Ozzano Emilia, Italy.
⁴ Endocrinology Unit and Center for Applied Biomedical Research, Department of Medical and Surgical Sciences, University of Bologna - S. Orsola-Malpighi Hospital, Bologna, Italy.

PMID: 30734380
DOI: 10.1111/jpn.13063

Abstract

Putative genetic markers have been associated with ETEC F4 (Mucine 4 [MUC4]; MUC4^GG;CG as susceptible; MUC4^CC as resistant) and F18 (Fucosyltransferase 1 [FUT1]; FUT1^GG;AG as susceptible; FUT1^AA as resistant) resistances respectively. In this study, 71 post-weaning pigs were followed from d0 (35 days old) to d42 (77 days of age) to investigate the effect of MUC4 or FUT1 genotypes on the mid-jejunal microbiota composition, pigs expression of genes related to inflammation (IL8, GPX2, REG3G, TFF3, CCL20 and LBPI) and glycomic binding pattern profile (Ulex europaeus agglutinin I [UEA] fucose-binding lectin and peanut agglutinin [PNA] galactose-specific), and on blood plasma targeted metabolomics profile, faecal score and performance parameters of growing healthy pigs. The MUC4 and FUT1 resistant genotypes improved the pigs' growth performance and had firmed faecal score susceptible genotypes in d0-d21 period. Pigs with MUC4^GG genotype had a higher jejunal expression of genes relate to immune function (CCL20 and REG3G) than MUC4^CG and MUC4^CC pigs (p < 0.05). MUC4^CG pigs had higher expression of TFF3 (implicated in mucosal integrity) than MUC4^GG and MUC4^CC (p < 0.05). FUT1 influenced the alpha- and beta-jejunal microbial indices. The FUT1^AA group had a higher number of operational taxonomic units (OTUs) belonging to Lactobacillus genus, while FUT1^GG group had a higher number of OTUs belonging to Veillonella genus. MUC4^CC pigs had lower scores for UEA on brush borders and goblet cells in villi than MUC4^GG (p < 0.05). FUT1^AA pigs had lower UEA positivity and higher PNA positivity on brush borders and goblet cells than FUT1^AG and FUT1^GG (p < 0.05). Both FUT1 and MUC4 influenced the metabolic profile of healthy pigs. Results highlight the role of MUC4 and FUT1 on pig intestinal homoeostasis and improved the knowledge regarding the potential interaction between host genetics, gut microbiota composition and host metabolism in a healthy status.

Keywords: FUT1; MUC4; 16S rRNA; fucose; intestinal mucosa.

MeSH terms

Animals
Bacteria / classification
Female
Fucosyltransferases / genetics
Fucosyltransferases / metabolism*
Galactoside 2-alpha-L-fucosyltransferase
Gastrointestinal Microbiome / physiology*
Gene Expression Regulation
Genetic Variation*
Genotype
Homeostasis / genetics*
Homeostasis / physiology
Male
Mucin-4 / genetics
Mucin-4 / metabolism*
Swine / genetics*
Swine / microbiology
Swine / physiology

Substances

Mucin-4
Fucosyltransferases