Epithelial response to high-grain diets involves alteration in nutrient transporters and Na+/K+-ATPase mRNA expression in rumen and colon of goats

Journal of Animal Science

Volumn 91, Issue 9, 2013, Pages 4256-4266

  Metzler Zebeli, B U ^a   Hollmann, M ^a   Sabitzer, S ^a   Podstatzky Lichtenstein, L ^b   Klein, D ^a   Zebeli, Q ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b Institute for Organic Farming and Biodiversity   (Austria)

Author keywords

Colon; Epithelium; Gene expression; Goat; Grain; Rumen

Indexed keywords

CAPRA HIRCUS; HORDEUM;

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CARRIER PROTEIN; GLUCOSE; MESSENGER RNA; VOLATILE FATTY ACID;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ARTICLE; COLON; DIET; DRUG EFFECT; EPITHELIUM; FERMENTATION; GENE EXPRESSION REGULATION; GENETICS; GOAT; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; HOMEOSTASIS; MALE; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; RANDOMIZATION; RUMINANT STOMACH;

ANIMAL FEED; ANIMALS; COLON; DIET; EPITHELIUM; FATTY ACIDS, VOLATILE; FERMENTATION; GENE EXPRESSION REGULATION; GLUCOSE; GOATS; HOMEOSTASIS; MALE; MEMBRANE TRANSPORT PROTEINS; POLYMERASE CHAIN REACTION; RANDOM ALLOCATION; RNA, MESSENGER; RUMEN; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 85047688794     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2012-5570     Document Type: Article

References (45)

1. Albrecht, E., M. Kolisek, T. Viergutz, R. Zitnan, and M. Schweigel. 2008. Molecular identification, immunolocalization, and functional activity of a vacuolar-type H1-ATPase in bovine rumen epithelium. J. Comp. Physiol. B 178:285-295.
2. Ametaj, B. N., Q. Zebeli, F. Saleem, N. Psychogios, M. Lewis, S. M. Dunn, J. Xia, and D. Wishart. 2010. Metabolomics reveals unhealthy alterations in rumen metabolism with increased proportion of cereal grain in the diet of dairy cows. Metabolomics 6:583-594.
3. Aschenbach, J. R., G. B. Penner, R. Stumpff, and G. Gäbel. 2011. Ruminant Nutrition Symposium: Role of fermentation acid absorption in the regulation of ruminal pH. J. Anim. Sci. 89:1092-1107.
4. Bergman, E. N. 1990. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol. Rev. 70:567-590.
5. Bondzio, A., C. Gabler, B. Badewien-Rentzsch, P. Schulze, H. Martens, and R. Einspanier. 2011. Identification of differentially expressed proteins in ruminal epithelium in response to a concentrate supplemented diet. Am. J. Physiol. Gastrointest. Liver Physiol. 301:G260-G268.
6. Connor, E. E., R. W. Li, R. L. Baldwin VI, and C. Li. 2010. Gene expression in the digestive tissues of ruminants and their relationships with feeding and digestive processes. Animal 4:993-1007.
7. Cuff, M. A., D. W. Lambert, and S. R. Shirazi-Beechey. 2002. Substrate-induced regulation of the human colonic monocarboxylate transporter, MCT1. J. Physiol. 539:361-371.
8. Cresci, G. A., M. Thangaraju, J. Mellinger, K. Liu, and V. Ganapathy. 2010. Colonic gene expression in conventional and germ-free mice with a focus on the butyrate receptor GPR109A and the butyrate transporter SLC5A8. J. Gastrointest. Surg. 14:449-461.
9. Delezay, O., B. Verrier, K. Mabrouk, J. van Rietschoten, J. Fantini, J. Mauchamp, and C. Gerard. 1995. Characterization of an electrogenic sodium/glucose cotransporter in a human colon epithelial cell line. J. Cell. Physiol. 163:120-128.
10. Durand, T., J. L. Gallis, S. Masson, P. J. Cozzone, and P. Canioni. 1993. pH regulation in perfused rat liver: Respective role of Na(+)-H+ exchanger and Na(+)-HCO3-cotransport. Am. J. Physiol. 265:G43-G50.
11. Erwin, E. S., G. J. Marco, and E. M. Emery. 1961. Volatile fatty acids analysis of blood and rumen fluid by gas chromatography. J. Dairy Sci. 44:1768-1771.
12. Gäbel, G., and J. R. Aschenbach. 2004. Adaptation und Regulation resorptiver Prozesse im Gastrointestinaltrakt von Wiederkäuern. Übers. Tierernährg. 32:149-181.
13. Gesellschaft für Ernährungsphysiologie. 2003. Recommendations for the Supply of Energy and Nutrients to Goats. DLG-Verlag, Frankfurt am Main, Germany.
14. Gorka, P., Z. M. Kowalski, P. Pietrzak, A. Kotunia, R. Kiljanczyk, J. Flaga, J. J. Holst, P. Guilloteau, and R. Zabielski. 2009. Effects of sodium butyrate supplementation in milk replacer and starter diet on rumen development in calves. J. Physiol. Pharmacol. 60:47-53.
15. Graham, C., I. Gatherar, I. Haslam, M. Glanville, and N. L. Simmons. 2007. Expression and localization of monocarboxylate transporters and sodium/proton exchangers in bovine rumen epithelium. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292:R997-R1007.
16. Gressley, T. F., M. B. Hall, and L. E. Armentano. 2011. Ruminant nutrition symposium: Productivity, digestion, and health responses to hindgut acidosis in ruminants. J. Anim. Sci. 89:1120-1130.
17. +/glucose cotransporter (SGLT1). J. Biol. Chem. 269:21407-21410.
18. Jais, A., D. Klein, B. Wolfesberger, and I. Walter. 2011. Gene expression profile of vascular endothelial growth factor and its receptors in various cell types of the canine lymph node (using laser capture microdissection). Vet. Immunol. Immunopathol. 140:207-214.
19. Kirat, D., J. Masuoka, H. Hayashi, H. Iwano, H. Yokota, H. Taniyama, and S. Kato. 2006. Monocarboxylate transporter 1 (MCT1) plays a direct role in short-chain fatty acids absorption in caprine rumen. J. Physiol. 576:635-647.
20. Kirat, D., Y. Matsuda, N. Yamashiki, H. Hayashi, and S. Kato. 2007. Expression, cellular localization, and functional role of monocarboxylate transporter 4 (MCT4) in the gastrointestinal tract of ruminants. Gene 391:140-149.
21. Klein, D. 2002. Quantification using real-time PCR technology: Applications and limitations. Trends Mol. Med. 8:257-260.
22. Klein, D., P. Janda, R. Steinborn, M. Müller, B. Salmons, and W.H. Günzburg. 1999. Proviral load determination of different feline immunodeficiency virus isolates using real-time polymerase chain reaction: Influence of mismatches on quantification. Electrophoresis 20:291-299.
23. Koho, N., V. Maijala, H. Norberg, M. Nieminen, and A. R. Pösö. 2005. Expression of MCT1, MCT2 and MCT4 in the rumen, small intestine and liver of reindeer (Rangifer tarandus tarandus L.). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 141:29-34.
24. Kolm, G., E. Knapp, R. Wagner, and D. Klein. 2006. Increased interleukin-1beta mRNA expression in skin biopsies of horses with Culicoides hypersensitivity following challenge with Culicoides nubeculosus extract. Vet. Immunol. Immunopathol. 113:90-98.
25. +-ATPase expression plays a role in rumen epithelium adaptation in sheep fed hay ad libitum or a mixed hay/concentrate diet. Vet. Med. Czech. 56:35-47.
26. Laverty, G., V. S. Elbrønd, S. S. Árnason, and E. Skadhauge. 2006. Endocrine regulation of ion transport in the avian lower intestine. Gen. Comp. Endocrinol. 147:70-77.
27. Li, S., E. Khafipour, D. O. Krause, A. Kroeker, J. C. Rodriguez-Lecompte, G. N. Gozho, and J. C. Plaizier. 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.
28. Liao, S. F., D. L. Harmon, E. S. Vanzant, K. R. McLeod, J. A. Boling, and J. C. Matthews. 2010. The small intestinal epithelia of beef steers differentially express sugar transporter messenger ribonucleic acid in response to abomasal versus ruminal infusion of starch hydrolysate. J. Anim. Sci. 88:306-314.
29. Mentschel, J., C. Leiser, C. Mülling, C. Pfarrer, and R. Claus. 2001. Butyric acid stimulates rumen mucosa development in the calf mainly by a reduction of apoptosis. Arch. Anim. Nutr. 55:85-102.
30. Metzler-Zebeli, B. U., M. G. Gänzle, R. Mosenthin, and R. T. Zijlstra. 2012. Oat β-glucan and dietary calcium and phosphorus differentially modify intestinal expression of pro-inflammatory cytokines and monocarboxylate transporter 1 and cecal morphology in weaned pigs. J. Nutr. 142:668-674.
31. Metzler-Zebeli, B. U., R. T. Zijlstra, R. Mosenthin, and M. G. Gänzle. 2011. Dietary calcium phosphate content and oat β-glucan influence gastrointestinal microbiota, butyrate-producing bacteria and butyrate fermentation in weaned pigs. FEMS Microbiol. Ecol. 75:402-413.
32. Penner, G. B., M. A. Steele, J. R. Aschenbach, and B. W. Bride. 2011. Ruminant nutrition symposium: Molecular adaptation of ruminal epithelia to highly fermentable diets. J. Anim. Sci. 89:1108-1119.
33. Rodenburg, W., J. Keijer, E. Kramer, C. Vinc, R. van der Meer, and I. M. Bovee-Oudenhoven. 2008. Impaired barrier function by dietary fructo-oligosaccharides (FOS) in rats is accompanied by increased colonic mitochondrial gene expression. BMC Genomics 9:144-159.
34. Schroeder, A., O. Mueller, S. Stocker, R. Salowsky, M. Leiber, M. Grassmann, S. Lightfoot, W. Menzel, M. Granzow, and T. Ragg. 2006. The RIN: An RNA integrity number for assigning integrity values to RNA measurements. BMC Mol. Biol. 7:3.
35. Shabi, Z., I. Bruckental, S. Zamwell, H. Tagari, and A. Arieli. 1999. Effects of extrusion of grain and feeding frequency on rumen fermentation, nutrient digestibility, and milk yield and composition in dairy cows. J. Dairy Sci. 82:1252-1260.
36. Shen, Z., H.-M. Seyfert, B. Löhrke, F. Schneider, R. Zitnan, A. Chudy, S. Kuhla, H. M. Hammon, J. W. Blum, H. Martens, H. Hagemeister, and J. Voigt. 2004. An energy-rich diet causes rumen papillae proliferation associated with more IGF type 1 receptors and increased plasma IGF-1 concentrations in young goats. J. Nutr. 134:11-17.
37. Steele, M. A., L. Dionissopoulos, O. AlZahal, J. Doelman, and B. W. McBride. 2012. Rumen epithelial adaptation to ruminal acidosis in lactating cattle involves the coordinated expression of insulinlike growth factor-binding proteins and a cholesterolgenic enzyme. J. Dairy Sci. 95:318-327.
38. St-Pierre, N. R. 2001. Invited review: Integrating quantitative findings from multiple studies using mixed model methodology. J. Dairy Sci. 84:741-755.
39. Tsukahara, T., Y. Iwasaki, K. Nakayama, and K. Ushida. 2003. Stimulation of butyrate production in the large intestine of weaning piglets by dietary fructooligosaccharides and its influence on the histological variables of the large intestinal mucosa. J. Nutr. Sci. Vitaminol. (Tokyo) 49:414-421.
40. Vandesompele, J., K. De Preter, F. Pattyn, B. Poppe, N. van Roy, A. de Paepe, and F. Speleman. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:RESEARCH0034.
41. VDLUFA. 1976. Methodenbuch. Buch III: Die chemische Untersuchung von Futtermitteln. 3rd ed. VDLUFA-Verlag, Darmstadt, Germany.
42. + exchanger isoform 1 and 3 messenger RNA in rumen epithelium of goat. J. Anim. Sci. 90:307-317.
43. Zebeli, Q., J.R. Aschenbach, M. Tafaj, J. Boghun, B. N. Ametaj, and W. Drochner. 2012. Invited review: Role of physically effective fiber and estimation of dietary fiber adequacy in high-producing dairy cattle. J. Dairy Sci. 95:1041-1056.
44. Zebeli, Q., M. Tafaj, I. Weber, J. Dijkstra, H. Steingass, and W. Drochner. 2007. Effects of varying dietary forage particle size in two concentrate levels on chewing activity, ruminal mat characteristics, and passage in dairy cows. J. Dairy Sci. 90:1929-1942.
45. Zouzoulas, A., P. B. Dunham, and R. Blostein. 2005. The effect of the gamma modulator on Na/K pump activity of intact mammalian cells. J. Membr. Biol. 204:49-56.