Serosal-to-mucosal urea flux across the isolated ruminal epithelium is mediated via urea transporter-B and aquaporins when Holstein calves are abruptly changed to a moderately fermentable diet

Journal of Dairy Science

Volumn 98, Issue 2, 2015, Pages 1204-1213

  Walpole, M E ^a   Schurmann, B L ^a   Gorka P ^b   Penner, G B ^a   Loewen, M E ^c   Mutsvangwa, T ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF AGRICULTURE IN KRAKOW   (Poland)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Aquaporin; Ruminal epithelium; Urea transporter; Ussing chamber

Indexed keywords

ANIMALIA; HORDEUM;

AQUAPORIN; CARBOHYDRATE DIET; CARRIER PROTEIN; MESSENGER RNA; MINERAL; NICKEL; NICKEL CHLORIDE; PHLORETIN; UREA; UREA TRANSPORTER; VITAMIN;

ADMINISTRATION AND DOSAGE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOREACTOR; BOVINE; CARBOHYDRATE DIET; CEREAL; DIET; DIET SUPPLEMENTATION; EPITHELIUM; FERMENTATION; GENETICS; MALE; METABOLISM; MUCOSA; RUMINANT STOMACH; TRANSPORT AT THE CELLULAR LEVEL; VETERINARY;

ANIMALS; AQUAPORINS; BIOLOGICAL TRANSPORT; BIOREACTORS; CATTLE; CEREALS; DIET; DIETARY CARBOHYDRATES; DIETARY SUPPLEMENTS; EPITHELIUM; FERMENTATION; MALE; MEMBRANE TRANSPORT PROTEINS; MINERALS; MUCOUS MEMBRANE; NICKEL; PHLORETIN; RNA, MESSENGER; RUMEN; UREA; VITAMINS;

EID: 84922334945     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2014-8757     Document Type: Article

References (48)

1. 2. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298:G190-G202.
2. Abdoun K., Stumpff F., Martens H. Ammonia and urea transport across the rumen epithelium: A review. Anim. Health Res. Rev. 2006, 7:43-59.
3. Bagnasco S.M. Role and regulation of urea transporters. Pflugers Arch. 2005, 450:217-226.
4. Broderick G.A., Kang J.H. Automated simultaneous determination of ammonia and total amino acids in ruminal fluid and in vitro media. J. Dairy Sci. 1980, 63:64-75.
5. Cheng K.J., Wallace R.J. The mechanism of passage of endogenous urea through the rumen wall and the role of ureolytic epithelial bacteria in the urea flow. Br. J. Nutr. 1979, 42:553-557.
6. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
7. Delgado-Elorduy A., Theurer C.B., Huber J.T., Alio A., Lozano O., Sadik M., Cuneo P., De Young H.D., Simas I.J., Santos J.E.P., Nussio L., Nussio C., Webb K.E., Tagari H. Splanchnic and mammary nitrogen metabolism by dairy cows fed steam-rolled or steam-flaked corn. J. Dairy Sci. 2002, 85:160-168.
8. Doranalli K., Penner G.B., Mutsvangwa T. Feeding oscillating dietary crude protein concentrations increases nitrogen utilization in growing lambs and this response is partly attributable to increased urea transfer to the rumen. J. Nutr. 2011, 141:560-567.
9. Egan A.R., Boda K., Varady J. Regulation of nitrogen metabolism and recycling. Control of Digestion and Metabolism in Ruminants 1986, 386-402. Prentice-Hall, Englewood Cliffs, NJ. L.P. Milligan, W.L. Grovum, A. Dobson (Eds.).
10. Fuller M.F., Reeds P.J. Nitrogen recycling in the gut. Annu. Rev. Nutr. 1998, 18:385-411.
11. Gozho G.N., Hobin M.R., Mutsvangwa T. Interactions between barley grain processing and source of supplemental dietary fat on nitrogen metabolism and urea-nitrogen recycling in dairy cows. J. Dairy Sci. 2008, 91:247-259.
12. Grether-Beck S., Felsner I., Brenden H., Kohne Z., Majora M., Marini A., Jaenicke T., Rodriguez-Martin M., Trullas C., Hupe M., Elias P.M., Krutmann J. Urea uptake enhances barrier function and antimicrobial defense in humans by regulating epidermal gene expression. J. Invest. Dermatol. 2012, 132:1561-1572.
13. Harmeyer J., Martens H. Aspects of urea metabolism in ruminants with reference to the goat. J. Dairy Sci. 1980, 63:1707-1728.
14. Huntington G.B. Hepatic urea synthesis and site and rate of urea removal from blood of beef steers fed alfalfa hay or a high concentrate diet. Can. J. Anim. Sci. 1989, 69:215-223.
15. Huntington G.B., Archibeque S.L. Practical aspects of urea and ammonia metabolism in ruminants. J. Anim. Sci. 1999, 78:742-749.
16. Ishibashi K., Sasaki S., Fushimi K., Yamamoto T., Kuwahara M., Marumo F. Immunolocalization and effect of dehydration on AQP3, a basolateral water channel of kidney collecting ducts. Am. J. Physiol. 1997, 272:F235-F241.
17. Johnston H., Koukoulas I., Jeyaseelan K., Armugam A., Earnest L., Baird R., Dawson N., Ferraro T., Wintour E.M. Ontogeny of aquaporins 1 and 3 in ovine placenta and fetal membranes. Placenta 2000, 21:88-99.
18. Kennedy P.M., Milligan L.P. The degradation and utilization of endogenous urea in the gastrointestinal tract of ruminants: a review. Can. J. Anim. Sci. 1980, 60:205-221.
19. Kristensen N.B., Storm A.C., Larsen M. Effect of dietary nitrogen content and intravenous urea infusion on ruminal and portal-drained visceral extraction of arterial urea in lactating Holstein cows. J. Dairy Sci. 2010, 93:2670-2683.
20. Lapierre H., Lobley G.E. Nitrogen recycling in the ruminant: A review. J. Dairy Sci. 2001, 84(E. Suppl.):E223-E226.
21. -δδCT method. Methods 2001, 25:402-408.
22. Lobley G.E., Bremner D.M., Zuur G. Effects of diet quality on urea fates in sheep as assessed by refined, non-invasive [15N 15N] urea kinetics. Br. J. Nutr. 2000, 84:459-468.
23. Ludden P.A., Stohrer R.M., Austin K.J., Atkinson R.L., Belden E.L., Harlow H.J. Effect of protein supplementation on expression and distribution of urea transporter-B in lambs fed low-quality forage. J. Anim. Sci. 2009, 87:1354-1365.
24. Ma T., Verkman A.S. Aquaporin water channels in gastrointestinal physiology. J. Physiol. 1999, 517:317-326.
25. MacIver B., Cutler C.P., Yin J., Hill M.G., Zeidel M.L., Hill W.G. Expression and functional characterization of four aquaporin water channels from the European eel (Anguilla anguilla). J. Exp. Biol. 2009, 212:2856-2863.
26. Marini J.C., Klein J.M., Sands J.M., Van Amburgh M.E. Effect of nitrogen intake on nitrogen recycling and urea transporter abundance in lambs. J. Anim. Sci. 2004, 82:1157-1164.
27. Marini J.C., Van Amburgh M.E. Nitrogen metabolism and recycling in Holstein heifers. J. Anim. Sci. 2003, 81:545-552.
28. Marsh W.H., Fingerhunt B., Kirsch E. Determination of urea N with the diacetyl method and an automatic dialyzing apparatus. Am. J. Clin. Pathol. 1957, 28:681-688.
29. Muscher A.S., Schroder B., Breves G., Huber K. Dietary nitrogen reduction enhances urea transport across goat rumen epithelium. J. Anim. Sci. 2010, 88:3390-3398.
30. Ontsouka E.C., Korczak B., Harmon H.M., Blum J.W. Real-time PCR quantification of bovine lactase mRNA localization in the gastrointestinal tract of milk-fed calves. J. Dairy Sci. 2004, 87:4230-4237.
31. Owens F.N., Secrist D.S., Hill W.J., Gill D.R. Acidosis in cattle: A review. J. Anim. Sci. 1998, 76:275-286.
32. Rémond D., Meschy F., Boivin R. Metabolites, water and mineral exchanges cross the rumen wall: Mechanisms and regulation. Ann. Zootech. 1996, 45:97-119.
33. Reynolds C.K., Kristensen N.B. Nitrogen recycling through the gut and the nitrogen economy of ruminants: An asynchronous symbiosis. J. Anim. Sci. 2008, 86(E. Suppl.):E293-E305.
34. Ritzhaupt A., Breves G., Schroder B., Winckler C.G., Shirazi-Beechey S.P. Urea transport in gastrointestinal tract of ruminants: effect of dietary nitrogen. Biochem. Soc. Trans. 1997, 25:S490. (Abstr.).
35. Ritzhaupt A., Wood I.S., Jackson A.A., Moran B.J., Shirazi-Beechey S.P. Isolation of RT-PCR fragment from human colon and sheep rumen RNA with nucleotide sequence similarity to human and rat urea transporter isoforms. Biochem. Soc. Trans. 1998, 26:S122. (Abstr.).
36. Robertson G.L., Athar S. The interaction of blood osmolality and blood volume in regulating plasma vasopressin in man. J. Clin. Endocrinol. Metab. 1976, 42:613-620.
37. Robinson P.H., Gill M., Kennelly J.J. Influence of time of feeding a protein meal on ruminal fermentation and forestomach digestion in dairy cows. J. Dairy Sci. 1997, 80:1366-1373.
38. Rojek A., Praetorius J., Frøkiaer J., Nielsen S., Fenton R.A. A current view of mammalian aquaglyceroporins. Annu. Rev. Physiol. 2008, 70:301-327.
39. Røjen B.A., Poulsen S.B., Theil P.K., Fenton R.A., Kristensen N.B. Effects of dietary nitrogen concentration on messenger RNA expression and protein abundance of urea transporter-B and aquaporins in ruminal papillae from lactating Holstein cows. J. Dairy Sci. 2011, 94:2587-2591.
40. Røjen B.A., Theil P.K., Larsen M., Kristensen N.B. Correlation between UT-B mRNA abundance in ruminant epithelia and net portal flux of urea in transition dairy cows. J. Anim. Sci. 2008, 86(E-Suppl. 2):T260. (Abstr.).
41. Schurmann B.L. Functional adaptation of the ruminal epithelium. MSc Thesis 2014, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.
42. Siddons R.C., Nolan J.V., Beever D.E., MacRae J.C. Nitrogen digestion and metabolism in sheep consuming diets containing contrasting forms and levels of N. Br. J. Nutr. 1985, 54:175-187.
43. Simmons N.L., Chaudhry A.S., Graham C., Scriven E.S., Thistelthwaite A., Smith C.P., Stewart G.S. Dietary regulation of ruminal bovine UT-B urea transporter expression and localization. J. Anim. Sci. 2009, 87:3288-3299.
44. Stewart G.S., Graham C., Cattell S., Smith T.P.L., Simmons N.L., Smith C.P. UT-B is expressed in the bovine rumen: Potential role in ruminal urea transport. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289:R605-R612.
45. Sunny N.E., Owens S.L., Baldwin R.L., El-Kadi S.W., Kohn R.A., Bequette B.J. Salvage of blood urea nitrogen in sheep is highly dependent upon plasma urea concentration and the efficiency of capture within the digestive tract. J. Anim. Sci. 2007, 85:1006-1013.
46. Theurer C.B., Huntington G.B., Huber J.T., Swingle R.S., Moore J.A. Net absorption and utilization of nitrogenous compounds across ruminal, intestinal, and hepatic tissues of growing beef steers fed dry-rolled or steam-flaked sorghum grain. J. Anim. Sci. 2002, 80:525-532.
47. Vercoe J.E. The transfer of nitrogen from the blood to the rumen of cattle. Aust. J. Agric. Res. 1969, 20:191-197.
48. Zhao D., Bankir L., Qian L., Yang D., Yang B. Urea and urine concentrating ability in mice lacking AQP 1 and 3. Am. J. Physiol. Renal Physiol. 2006, 291:F429-F438.