Transcriptomic Changes in the Rumen Epithelium of Cattle after the Induction of Acidosis

Document Type: Original Articles

Authors

1 Department of Animal Sciences, Faculty of Animal Sciences and Food technology, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Ahvaz, Iran

2 Department of Tissue Engineering and Applied Cell Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran

3 Department of Medical Biotechnology, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran

Abstract

The transition from normal forage to a highly fermentable diet to achieve rapid weight gain in the cattle industry can induce ruminal acidosis. The molecular host mechanisms that occur in acidosis are largely unknown. Therefore, the histology and transcriptome profiling of rumen epithelium was investigated in normal and acidosis animals to understand the molecular mechanisms involved in the disease. The rumen epithelial transcriptome from acidosis (n=3) and control (n=3) Holstein steers was obtained using RNA-sequencing. The mean values of clean reads were 70,975,460±984,046 and 71,142,189±834,526 in normal and acidosis samples, respectively. In total, 1,074 differentially expressed genes were identified in the two groups (P<0.05), of which 624 and 450 genes were up- and down-regulated in the acidosis samples, respectively. Functional analysis indicated that the majority of the up-regulated genes had a function in filament organization, positive regulation of epithelial and muscle fiber concentration, biomineral tissue development, negative regulation of fat cell differential, regulation of ion transmembrane transport, regulation of cell adhesion and butyrate, as well as short-chain fatty acid absorption that was metabolized as an energy source. Functional analysis of the down-regulated genes revealed effects in immune response, positive regulation of T-cell migration, regulation of metabolic processes, and localization. Furthermore, the results showed a differential expression of genes involved in the Map Kinase and Toll-like receptor signaling pathways. The IL1B, CXCL5, IL36A, and IL36B were significantly down-regulated in acidosis rumen tissue samples. The results suggest that rapid shifts to rich fermentable carbohydrates diets cause an increase in the concentration of ruminal volatile fatty acids, tissue damage, and significant changes in transcriptome profiles of rumen epithelial. 

Keywords


Article Title [French]

Changements Transcriptomiques dans L'épithélium du Rumen des Bovins après L'induction d’uneacidose

Abstract [French]

: La transition d'un fourrage normal à un régime hautement fermentescible pour obtenir un gain de poids rapide chez les bovins peut induire une acidose ruminale. Les mécanismes moléculaires responsables de l'acidose chez les bovins sont encore largement méconnus. Par conséquent, l'histologie et le profilage du transcriptome de l'épithélium du rumen ont été étudiés chez les animaux sainset souffrant d’acidoses pour comprendre les mécanismes moléculaires impliqués dans la maladie. Le transcriptome épithélial du rumen provenant de l'acidose (n=3) et du contrôle (n=3) bouvillons Holstein a été obtenu en utilisant le séquençage d'ARN. Les valeurs moyennes dans les échantillons d’animaux sains et souffrant d'acidose étaient respectivement de 70,975, 460±984,046 et 71,142,189±834,526,. Au total, 1, 074 gènes différentiellement exprimés ont été identifiés dans les deux groupes (P<0.05), dont 624 et 450 gènes étaient respectivement régulés à la hausse et à la baisse dans les échantillons d’animaux souffrant d'acidose. L'analyse fonctionnelle a des gènes régulés à la hausse avaient une fonction dans l'organisation des filaments, la régulation positive de la concentration des fibres épithéliales et musculaires, le développement des tissus biominéraux, la régulation négative du différentiel adipeux, la régulation du transport transmembranaire ionique, la régulation de l'adhésion cellulaire et le butyrate, ainsi que l'absorption des acides gras à chaîne courte métabolisés comme source d'énergie. L'analyse fonctionnelle des gènes régulés à la baisse a révélé des effets sur la réponse immunitaire, la régulation positive de la migration des cellules T, la régulation des processus métaboliques et la localisation. De plus, les résultats ont montré une expression différentielle des gènes impliqués dans les voies de signalisation des récepteurs Map KINASE et Toll-like. Les IL1B, CXCL5, IL36A et IL36B étaient significativement régulés à la baisse dans les échantillons de tissus du rumen avec une acidose. Les résultats suggèrent que des changements rapides vers des régimes riches en glucides fermentescibles provoquent une augmentation de la concentration des acides gras volatils ruminaux, des lésions tissulaires et des changements significatifs dans les profils transcriptomiques de l'épithélium du rumen.

Keywords [French]

  • Acidose
  • Bovins
  • Tissu épithélial ruminal
  • Transcriptome
Alston, J.M., Pardey, P.G., 2014. Agriculture in the global economy. J Econ Perspec 28, 121-146.

Ash, R., Baird, G.D., 1973. Activation of volatile fatty acids in bovine liver and rumen epithelium. Evidence for control by autoregulation. Biochem J 136, 311-319.

Baldwin, R.L.t., Li, R.W., Jia, Y., Li, C.J., 2018. Transcriptomic impacts of rumen epithelium induced by butyrate infusion in dairy cattle in dry period. Gene Regul Syst Bio 12, 1177625018774798.

Blanch, M., Calsamiglia, S., Devant, M., Bach, A., 2010. Effects of acarbose on ruminal fermentation, blood metabolites and microbial profile involved in ruminal acidosis in lactating cows fed a high-carbohydrate ration. J Dairy Res 77, 123-128.

Dionissopoulos, L., AlZahal, O., Steele, M.A., Matthews, J.C., McBride, B.W., 2014. Transcriptomic changes in ruminal tissue induced by the periparturient transition in dairy cows. Am J Anim Vet Sci 9, 36-45.

Durunna, O.N., Mujibi, F.D., Goonewardene, L., Okine, E.K., Basarab, J.A., Wang, Z., et al., 2011. Feed efficiency differences and reranking in beef steers fed grower and finisher diets. J Anim Sci 89, 158-167.

Enemark, J.M., 2008. The monitoring, prevention and treatment of sub-acute ruminal acidosis (SARA): a review. Vet J 176, 32-43.

Gressley, T.F., 2014. Inflammatory responses to sub-acute ruminal acidosis. 25th Annual Florida Ruminant Nutrition Symposium, Florida, USA.

Hernandez, J., Benedito, J.L., Abuelo, A., Castillo, C., 2014. Ruminal acidosis in feedlot: from aetiology to prevention. Sci World J 2014, 702572.

Huang da, W., Sherman, B.T., Lempicki, R.A., 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4, 44-57.

Kahn, L., Cottle, D., 2014. Beef cattle production and trade, Clayton, Australia: Csiro Publishing, p. 221.

Kanehisa, M., Goto, S., 2000. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28, 27-30.

Kanehisa, M., Goto, S., Sato, Y., Kawashima, M., Furumichi, M., Tanabe, M., 2014. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42, 199-205.

Ki, Y.W., Park, J.H., Lee, J.E., Shin, I.C., Koh, H.C., 2013. JNK and p38 MAPK regulate oxidative stress and the inflammatory response in chlorpyrifos-induced apoptosis. Toxicol Lett 218, 235-245.

Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., Salzberg, S.L., 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14, R36.

Kleen, J.L., Hooijer, G.A., Rehage, J., Noordhuizen, J.P., 2003. Subacute ruminal acidosis (SARA): a review. J Vet Med A Physiol Pathol Clin Med 50, 406-414.

Langmead, B., Salzberg, S.L., 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9, 357-359.

Li, S., Khafipour, E., Krause, D.O., Kroeker, A., Rodriguez-Lecompte, J.C., Gozho, G.N., et al., 2012. Effects of subacute ruminal acidosis challenges on fermentation and endotoxins in the rumen and hindgut of dairy cows. J Dairy Sci 95, 294-303.

Li, W., Gelsinger, S., Edwards, A., Riehle, C., Koch, D., 2019. Transcriptome analysis of rumen epithelium and meta-transcriptome analysis of rumen epimural microbial community in young calves with feed induced acidosis. Sci Rep 9, 4744.

Mi, H., Muruganujan, A., Thomas, P.D., 2013. PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Res 41, 377-386.

O'Shea, E., Waters, S.M., Keogh, K., Kelly, A.K., Kenny, D.A., 2016. Examination of the molecular control of ruminal epithelial function in response to dietary restriction and subsequent compensatory growth in cattle. J Anim Sci Biotechnol 7, 53.

Penner, G.B., 2014. Mechanisms of volatile fatty acid absorption and metabolism and maintenance of a stable rumen environment. 25th Florida Ruminant Nutrition Symposium, pp. 92-104.

Penner, G.B., Steele, M.A., Aschenbach, J.R., McBride, B.W., 2011. Ruminant Nutrition Symposium: Molecular adaptation of ruminal epithelia to highly fermentable diets. J Anim Sci 89, 1108-1119.

Sehested, J., Diernaes, L., Moller, P.D., Skadhauge, E., 1999. Ruminal transport and metabolism of short-chain fatty acids (SCFA) in vitro: effect of SCFA chain length and pH. Comp Biochem Physiol A Mol Integr Physiol 123, 359-368.

Steele, M.A., Vandervoort, G., AlZahal, O., Hook, S.E., Matthews, J.C., McBride, B.W., 2011. Rumen epithelial adaptation to high-grain diets involves the coordinated regulation of genes involved in cholesterol homeostasis. Physiol Genomics 43, 308-316.

Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., et al., 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7, 562-578.

Zhao, C., Liu, G., Li, X., Guan, Y., Wang, Y., Yuan, X., et al., 2018. Inflammatory mechanism of Rumenitis in dairy cows with subacute ruminal acidosis. BMC Vet Res 14, 135.