Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-19T20:26:19.135Z Has data issue: false hasContentIssue false

Urea nitrogen salvage mechanisms and their relevance to ruminants, non-ruminants and man

Published online by Cambridge University Press:  14 December 2007

Gavin S. Stewart
Affiliation:
School of Biological Sciences, Stopford Building, University of Manchester, Oxford Road, Manchester M13 9PT, UK
Craig P. Smith*
Affiliation:
School of Biological Sciences, Stopford Building, University of Manchester, Oxford Road, Manchester M13 9PT, UK
*
*Corresponding author: Dr Craig Smith, fax +44 161 275 5600, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Maintaining a correct balance of N is essential for life. In mammals, the major sources of N in the diet are amino acids and peptides derived from ingested proteins. The immediate endproduct of mammalian protein catabolism is ammonia, which is toxic to cells if allowed to accumulate. Therefore, amino acids are broken down in the liver as part of the ornithine–urea cycle, which results in the formation of urea – a highly soluble, biochemically benign molecule. Mammals cannot break down urea, which is traditionally viewed as a simple waste product passed out in the urine. However, urea from the bloodstream can pass into the gastrointestinal tract, where bacteria expressing urease cleave urea into ammonia and carbon dioxide. The bacteria utilise the ammonia as an N source, producing amino acids and peptides necessary for growth. Interestingly, these microbial products can be reabsorbed back into the host mammalian circulation and used for synthetic processes. This entire process is known as ‘urea nitrogen salvaging’ (UNS). In this review we present evidence supporting a role for this process in mammals – including ruminants, non-ruminants and man. We also explore the possible mechanisms involved in UNS, including the role of specialised urea transporters.

Type
Research Articles
Copyright
Copyright © The Authors 2005

References

Al-Dehneh, A, Huber, JT, Wandeley, R, Theurer, CB, Pessarakli, M & de Young, D (1997) Incorporation of recycled urea-N into ruminal bacteria flowing to the small intestine of dairy cows fed a high-grain or high-forage diet. Animal Feed Science and Technology 68, 327388.Google Scholar
Archibeque, SL, Burns, JC & Huntington, GB (2001) Urea flux in beef steers: effects of forage species and nitrogen fertilization. Journal of Animal Science 79, 19371943.Google Scholar
Bagnasco, SM, Jackson, S, Vikulina, T, Kim, D-G, Hennigar, RA & Inoue, H (2003) The UT-B urea transporter is expressed in colon mucosa. Journal of American Society of Nephrology Proceeding Abstract F-P0043.Google Scholar
Bagnasco, SM, Peng, T, Janech, MG, Karakashian, A & Sands, JM (2001) Cloning and characterization of the human urea transporter UT-A1 and mapping of the human Slc14a2 gene. American Journal of Physiology 281, F400–F406.Google Scholar
Bankir, L (1996) Urea and the kidney. In The Kidney, chapter 14 pp.571606. [Brenner, BM, editor]. Philadelphia: WB Saunders.Google Scholar
Benlamlih, S & de Pomyers, H (1989) Changes in endogenous urea recycling and the handling of renal urea in pregnant and lactating Sardi sheep kept on a constant feeding level. Reproductive Nutritional Development 29, 129137.Google Scholar
Berger, UV, Tsukaguchi, H & Hediger, MA (1998) Distribution of mRNA for the facilitated urea transporter UT3 in the rat nervous system. Anatomical Embryology 197, 405414.Google Scholar
Bochroder, B, Schubert, R & Bodeker, D (1994) Studies on the transport in vitro of lysine, histidine, arginine and ammonium across the mucosa of the equine colon. Equine Veterinary Journal 26, 131133.Google Scholar
Bodeker, D & Kemkowski, J (1996) Participation of NH 4 + in total ammonia absorption across the rumen epithelium of sheep ( Ovis aries ). Comparative Biochemical and Physiological Animal Physiology 114, 305310.CrossRefGoogle Scholar
Bodeker, D, Shen, Y, Kemkowski, J & Holler, H (1992) Influence of short chain fatty acids on ammonia absorption across the rumen wall in sheep. Experimental Physiology 77, 369376.CrossRefGoogle ScholarPubMed
Boll, M, Foltz, M, Rubio-Aliaga, I, Kottra, G, Daniel, H (2002) Functional characterization of two novel mammalian electrogenic proton-dependent amino acid cotransporters. Journal of Biological Chemistry 277, 2296622973.Google Scholar
Bown, RL, Gibson, JA, Fenton, JC, Snedden, W, Clark, ML & Sladen, GE (1975) Ammonia and urea transport by the excluded human colon. Clinical Science of Molecular Medicine 48, 279287.Google Scholar
Buddington, RK (1996) Postnatal changes in bacterial populations in the gastro-intestinal tract of dogs. American Journal of Veterinary Research 64, 646651.Google Scholar
Bunting, LD, Boling, JA, MacKown, CT (1989 a) Effect of dietary protein level on nitrogen metabolism in the growing bovine: I Nitrogen recycling and intestinal protein supply in calves. Journal of Animal Science 67, 810819.Google Scholar
Bunting, LD, Boling, JA, MacKown, CT, Davenport, GM (1989 b) Effect of dietary protein level on nitrogen metabolism in the growing bovine: 2 Diffusion into and utilization of endogenous urea nitrogen in the rumen. Journal of Animal Science 67, 820826.Google Scholar
Chen, H, Wong, EA & Webb, KEJ (1999) Tissue distribution of a peptide transporter mRNA in sheep, dairy cows, pigs and chickens. Journal of Animal Science 77, 12771283.Google Scholar
Correa, P (1996) Human gastric carcinogenesis: a multistep and multifactorial process. Cancer Research 52, 67356740.Google Scholar
Danielsen, M & Jackson, AA (1992) Limits of adaptation to a diet low in protein in normal man: urea kinetics. Clinical Science 83, 103108.Google Scholar
Donovan, SM & Lonnerdal, B (1989) Non-protein nitrogen and true protein in infant formulas. Acta Paediatrica Scandinavica 78, 497504.Google Scholar
Doran, JJ, Gunn, RB, Sands, JM & Timmer, RT (1999) Urea transporter (UT-A) mRNA isoforms are expressed in rat extra-renal tissues. Journal of the American Society of Nephrology 10, 14A, A0069.Google Scholar
Doring, F, Walter, J, Will, J, Focking, M, Boll, M, Amasheh, S, Clauss, W & Daniel, H (1998) Delta-aminolevulinic acid transport by intestinal and renal peptide transporters and its physiological and clinical implications. Journal of Clinical Investigation 101, 27612767.Google Scholar
Echevarria, M & Ilundain, AA (1998) Aquaporins. Journal of Physiological Biochemistry 54, 107118.Google Scholar
el-Khoury, AE, Fugakawa, NF, Sanchez, M, Tsay, RH, Gleason, RE, Chapman, TE & Young, VR (1994) Validation of the tracer-balance concept with reference to leucine: 24-h intravenous tracer studies with L-[1-13C]leucine and [15N-15N]urea. American Journal of Clinical Nutrition 59, 10001011.Google Scholar
Ergene, N & Pickering, EC (1978) The effects of reducing dietary nitrogen and of increasing sodium chloride intake on urea excretion and reabsorption and on urine osmolality in sheep. Quarterly Journal of Experimental Physiology 63, 6776.Google Scholar
Faber, P, Faber, P, Johnstone, AM, Gibney, ER, Elia, M, Stubbs, RJ, Roger, PL, Milne, E, Buchan, W & Lobley, GE (2003) The effect of rate and extent of weight loss on urea salvage in obese male subjects. British Journal of Nutrition 90, 221231.Google Scholar
Fenton, RA, Cooper, GJ, Morris, ID & Smith, CP (2002) Coordinated expression of UT-A and UT-B urea transporters in testis. American Journal of Physiology 282, C1492–C1501.Google Scholar
Ferraris, RP (1996) Dietary and developmental regulation of intestinal sugar transport. Biochemical Journal 360, 265276.Google Scholar
Fihn, BM & Jodal, M (2001) Permeability of the proximal and distal rat colon crypt and surface epithelium to hydrophilic molecules. Pflugers Archives – European Journal of Physiology 441, 656662.CrossRefGoogle ScholarPubMed
Ford, D, Howard, A & Hirst, BH (2003) Expression of the peptide transporter hPepT1 in human colon: a potential route for colonic protein nitrogen and drug absorption. Histochemistry and Cell Biology 119, 3743.Google Scholar
Forrester, T, Badaloo, A, Persaud, C & Jackson, AA (1994) Urea production and salvage during pregnancy in normal Jamaican women. American Journal of Clinical Nutrition 60, 341346.CrossRefGoogle ScholarPubMed
Forsum, E & Lonnerdal, B (1980) Effect of protein intake on protein and nitrogen composition of breast milk. American Journal of Clinical Nutrition 33, 18091813.Google Scholar
Fuller, MF & Reeds, PJ (1998) Nitrogen recycling in the gut. Annual Reviews of Nutrition 18, 385411.Google Scholar
Galluci, E, Micelli, S & Lippe, C (1971) Non-electrolyte permeability across thin lipid membranes. Archives of Integrative Physiology and Biochemistry 79, 881887.Google Scholar
Gibson, GR, Mountzouris, KC, McCartney, AL & Gibson, GR (2002) Intestinal microflora of human infants and current trends for its nutritional modulation. British Journal of Nutrition 87, 405420.Google Scholar
Harada, K, Murawaki, Y & Hirayama, C (1985) Comparative studies in nicotinohydroxamic acid and neomycin in ammonia and urea metabolism in rats. Research Communications in Chemical Pathology and Pharmacology 49, 309312.Google Scholar
Harmeyer, J & Martens, H (1980) Aspects of urea metabolism in ruminants with reference to the goat. Journal of Dairy Science 63, 17071728.Google Scholar
Hatanaka, T, Huang, W, Nakanishi, T, Bridges, CC, Smith, SB, Prasad, PD, Ganapathy, ME & Ganapathy, V (2002) Transport of D-serine via the amino acid transporter ATB0,+ expressed in the colon. Biochemical and Biophysical Research Communications 291, 291295.Google Scholar
Heine, W, Mohr, C, Wutzke, K & Radke, M (1991) Symbiotic interactions between colonic microflora and protein metabolism in infants. Acta Paediatrica Scandinavica 80, 712.Google Scholar
Heine, W, Wutzke, KD, Richter, I, Walther, F & Plath, C (1987) Evidence for colonic absorption of protein nitrogen in infants. Acta Paediatrica Scandinavica 76, 741744.CrossRefGoogle ScholarPubMed
Herrera-Ruiz, D, Wang, O, Gudmundsson, OS, Cook, TJ, Smith, RL, Faria, TN & Knipp, GT (2001) Spatial expression patterns of peptide transporters in the human and rat gastrointestinal tracts, Caco-2 in vitro cell culture model, and multiple human tissues. AAPS Pharmacological Science 3, E9.Google Scholar
Hill, MJ & Cook, AR (1986) Nitrogen metabolism in the animal gut. Society of Applied Bacteriology Symposium 13, 287301.Google Scholar
Hinnebusch, BF, Meng, S, Wu, JT, Archer, SY & Hodin, RA (2002) The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. Journal of Nutrition 132, 10121017.CrossRefGoogle ScholarPubMed
Hobson, PN & Wallace, RJ (1982) Microbial ecology and activities in the rumen. Part I. Critical Review in Microbiology 9, 165225.Google Scholar
Hooper, LV, Wong, MH, Thelin, A, Hansson, L, Falk, PG & Gordon, JI (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291, 881884.Google Scholar
Houpt, TR & Houpt, KA (1968) Transfer of urea nitrogen across the rumen wall. American Journal of Physiology 214, 12961303.Google Scholar
Howell, JA, Matthews, AD, Swanson, KC, Harmon, DL & Matthews, JC (2001) Molecular identification of high affinity glutamate transporters in sheep and cattle forestomach, intestine, liver, kidney, pancreas. Journal of Animal Science 79, 13291336.Google Scholar
Huntington, GB (1996) Uptake and transport of non-protein nitrogen by the ruminal gut. Federation Proceedings 45, 22722276.Google Scholar
Inoue, H, Jackson, SD, Vikulina, T, Klein, JD, Tomita, K & Bagnasco, SM (2004) Identification and characterization of a Kidd antigen/UT-B urea transporter expressed in human colon. American Journal of Physiology 287, C30–C35.Google Scholar
Isolauri, E, Kirjavainen, PV & Salminen, S (2002) Probiotics: a role in the treatment of intestinal infection and inflammation? Gut 50, 354359.Google Scholar
Isozaki, T, Gillin, AG, Swanson, CE & Sands, JM (1994) Protein restriction sequentially induces new urea transport processes in rat initial IMCD. American Journal of Physiology 266, F756–F761.Google Scholar
Isozaki, T, Verlander, JW & Sands, JM (1993) Low protein diet alters urea transport and cell structure in rat initial inner medullary collecting duct. Journal of Clinical Investigation 92, 24482457.CrossRefGoogle ScholarPubMed
Jackson, AA (1996) Urea as a nutrient: bioavailability and role in nitrogen economy. Archives of Diseases in Childhood 70, 34.Google Scholar
Jackson, AA (1996) Salvage of urea-nitrogen and protein requirements. Proceedings of the Nutrition Society 54, 535547.Google Scholar
Jackson, AA (1996) Salvage of urea-nitrogen in the large bowel: functional significance in metabolic control and adaptation. Biochemical Society Transactions 26, 231236.CrossRefGoogle Scholar
Kato, A & Sands, JM (1998) Evidence for sodium-dependent active urea secretion in the deepest subsegment of the rat inner medullary collecting duct. Journal of Clinical Investigation 101, 423428.Google Scholar
Koenig, KM, Newbold, CJ, McIntosh, FM & Rode, LM (2000) Effects of protozoa on bacterial nitrogen recycling in the rumen. Journal of Animal Science 78, 24312445.Google Scholar
Koster, HH, Woods, BC, Cochran, RC, Vanzant, ES, Titgemeyer, EC, Grieger, DM, Olson, KC & Stokka, G (2002) Effect of increasing proportion of supplemental N from urea in prepartum supplements on range beef cow performance and on forage intake and digestibility by steers fed low-quality forage. Journal of Animal Science 80, 16521662.CrossRefGoogle ScholarPubMed
Langran, M, Moran, BJ, Murphy, JL & Jackson, AA (1992) Adaptation to a diet low in protein: effect of complex carbohydrate upon urea kinetics in normal man. Clinical Science 82, 191198.Google Scholar
Lapierre, H & Lobley, GE (2001) Nitrogen recycling in the ruminant: a review. Journal of Dairy Science 84, Suppl., E223–E236.Google Scholar
Leng, L, Szanyiova, M & Boda, K (1985) The renal response of sheep to a low dietary nitrogen intake. Physiologia Bohemoslovaca 35, 147154.Google Scholar
Leung, DW, Loo, DD, Hariyama, BA, Zeuthen, T & Wright, EM (2000) Urea transport by cotransporters. Journal of Physiology 528, 251257.Google Scholar
LeVeen, EG, Falk, G, Ip, M, Mazzapica, N & LeVeen, HH (1978) Urease as a contributing factor in ulcerative lesions of the colon. American Journal of Surgery 135, 5356.Google Scholar
Long, CL, Jeevanandam, M & Kinney, JM (1978) Metabolism and recycling of urea in man. American Journal of Clinical Nutrition 31, 13671382.Google Scholar
Ma, T & Verkman, A (1999) Aquaporin channels in gastrointestinal physiology. Journal of Physiology 517, 317326.Google Scholar
MacAulay, N, Gether, U, Klaeke, DA & Zeuthen, T (2002) Passive water and urea permeability of a human Na + glutamate cotransporter expressed in Xenopus oocytes. Journal of Physiology 542, 817828.Google Scholar
McClelland, IS, Persaud, C & Jackson, AA (1997) Urea kinetics in healthy women during normal pregnancy. British Journal of Nutrition 77, 165181.Google Scholar
Maekawa, M, Beauchemin, KA & Christensen, DA (2002) Chewing activity, saliva production and ruminal pH of primiparous and multiparous lactating dairy cows. Journal of Dairy Science 85, 11761182.Google Scholar
Marini, JC, Van Amburgh, ME (2003) Nitrogen metabolism and recycling in Holstein heifers. Journal of Animal Science 81, 545552.Google Scholar
Marini, JC, Klein, JD, Sands, JM, Van Amburgh, ME (2004) Effect of nitrogen intake on nitrogen recycling and urea transporter abundance in lambs. Journal of Animal Science 82, 11571164.CrossRefGoogle ScholarPubMed
Marsh, MJ & Knepper, MA (1992) Renal handling of urea. In Handbook of Physiology, Renal Physiology pp.13171347 [Windhager, EE]. Oxford: Oxford University Press.Google Scholar
Martin, RG, McMeniman, NP, Norton, BW & Dowsett, KF (1996) Utilization of endogenous and dietary urea in the large intestine of the mature horse. British Journal of Nutrition 76, 373386.Google Scholar
Mason, VC (1996) Metabolism of nitrogenous compounds in the large gut. Proceedings of the Nutrition Society 43, 4553.Google Scholar
Meakins, TS & Jackson, AA (1996) Salvage of exogenous urea nitrogen enhances nitrogen balance in normal men consuming marginally inadequate protein diets. Clinical Science 90, 215225.Google Scholar
Merlin, D, Si-Tahar, M, Sitaraman, SV, Eastburn, K, Williams, I, Liu, X, Hediger, MA, Madara, JL (2001) Colonic epithelial hPepT1 expression occurs in inflammatory bowel disease: transport of bacterial peptides influences expression of MHC class 1 molecules. Gastroenterology 120, 16661679.Google Scholar
Metges, CC (2000) Contribution of microbial amino acids to amino acids homeostasis of the host. Journal of Nutrition 130, 1857S–1864S.Google Scholar
Metges, CC, Petzke, KJ, el-Khoury, AE, Henneman, L, Grant, I, Bedri, S, Regan, MM, Fuller, MF, Young, VR (1999) Incorporation of urea and ammonia nitrogen into ileal and fecal microbial proteins and plasma free amino acids in normal men and ilestomates. American Journal of Clinical Nutrition 70, 10461058.Google Scholar
Millward, DJ, Forrester, T, Ah-Sing, E, Yeboah, N, Gibson, N, Badaloo, A, Boyne, M, Reade, M, Persaud, C & Jackson, AA (2000) The transfer of 15N from urea to lysine in the human infant. British Journal of Nutrition 83, 505512.Google Scholar
Moran, BJ & Jackson, AA (1990) 15N urea metabolism in the functioning human colon: luminal hydrolysis and mucous permeability. Gut 31, 454457.Google Scholar
Mousa, HM, Ali, KE & Hume, ID (1983) Effects of water deprivation on urea metabolism in camels, desert sheep and desert goats fed dry desert grass. Comparative Biochemical and Physiological Anatomy 74, 715720.Google Scholar
Ogihara, H, Suzuki, T, Nagamachi, Y, Inui, K & Takata, K (1999) Peptide transporter in the rat small intestine: ultrastructural localization and the effect of starvation and administration of amino acids. Histochemical Journal 31, 169174.Google Scholar
Olives, B, Martial, S, Mattei, M-G, Matassi, G, Rousselet, G, Ripoche, P, Cartron, J-P & Bailly, P (1996) Molecular characterization of a new urea transporter in the human kidney. FEBS Letters 386, 156160.Google Scholar
Olives, B, Neau, P, Bailly, P, Hediger, MA, Rousselet, G, Cartron, JP & Ripoche, P (1994) Cloning and functional expression of a urea transporter from human bone marrow cells. Journal of Biological Chemistry 269, 3164931652.Google Scholar
Packett, LV & Groves, TDD (1965) Urea recycling in the ovine. Journal of Animal Science 24, 341346.Google Scholar
Potter, GD, Schmidt, KL & Lester, R (1983) Glucose absorption by an in vitro perfused colon of the fetal rat. American Journal of Physiology 245, G424–G430.Google Scholar
Puga, DC, Galina, HM, Perez-Gil, RF, Sangines, GL, Aquilera, BA, Haenlein, GF, Barajas, CR & Herrera, HJ (2001) Effect of a controlled-release urea supplementation on feed intake, digestibility, nitrogen balance and ruminal kinetics of sheep fed low quality tropical forage. Small Ruminant Research 41, 918.Google Scholar
Ramirez, M, Fernandez, R & Malnic, G (1999) Permeation of NH3/NH4 + and cell pH in colonic crypts of the rat. Pflugers Archives – European Journal of Physiology 438, 508515.Google Scholar
Richards, P (1996) Nutritional potential of nitrogen recycling in man. American Journal of Clinical Nutrition 25, 615625.Google Scholar
Ritzhaupt, A, Breves, G, Schroder, B, Winckler, CG & Shirazi-Beechey, SP (1997) Urea transport in gastrointestinal tract of ruminants: effect of dietary nitrogen. Biochemical Society Transactions 25, S122.Google Scholar
Ritzhaupt, A, Wood, IS, Jackson, AA, Moran, BJ & Shirazi-Beechey, SP (1998) Isolation of a RT-PCR fragment from human colon and sheep rumen RNA with nucleotide sequence similarity to human and rat urea transporter isoforms. Biochemical Society Transactions 26, S40.Google Scholar
Russell, K, Lobley, GE, Rawlings, J, Millward, DJ & Harper, EJ (2000) Urea kinetics of a carnivore, Felis silvestris catus. British Journal of Nutrition 84, 597604.Google Scholar
Sands, JM (1996) Molecular mechanisms of urea transport. Journal of Membrane Biology 191, 149163.Google Scholar
Sarraseca, A, Milne, E, Metcalf, MJ & Lobley, GE (1998) Urea recycling in sheep: effects of intake. British Journal of Nutrition 79, 7988.Google Scholar
Shen, H, Smith, DE & Brosius, FC (2001) Developmental expression of PEPT1 and PEPT2 in rat small intestine, colon and kidney. Pediatric Research 49, 789795.Google Scholar
Singh, SK, Binder, HJ, Giebel, JP & Boron, WF (1995) An apical permeability barrier to NH3/NH4 + in isoloated, perfused colon crypts. Proceedings of the National Academy of Science USA 92, 1157311577.Google Scholar
Smith, CP, Lee, W-S, Martial, S, Knepper, MA, You, G, Sands, JM & Hediger, MA (1995) Cloning and regulation of expression of the rat kidney urea transporter (rUT2). Journal of Clinical Investigation 96, 15561563.Google Scholar
Smith, CP, Potter, EA, Fenton, RA & Stewart, GS (2004) Characterization of a human colonic cDNA encoding a structurally novel urea transporter, hUT-A6. American Journal of Physiology 287, C1087–C1093.Google Scholar
Smith, CP & Rousselet, G (2001) Urea transporters. Journal of Membrane Biology 183, 114.Google Scholar
Steinbrecher, HA, Griffiths, DM & Jackson, AA (1996) Urea production in normal breast-fed infants measured with primed/ intermittent oral doses of 15N15N urea. Acta Paediatrica 85, 656662.Google Scholar
Stewart, GS, Fenton, RA, Thevenod, F & Smith, CP (2004) Urea movement across mouse colonic plasma membranes is mediated by UT-A urea transporters. Gastroenterology 126, 765773.Google Scholar
Tanaka, N, Kubo, K, Shiraki, K, Koishi, H & Yoshimura, H (1980) A pilot study on protein metabolism in the Papua New Guinea highlanders. Journal of Nutritional Science and Vitaminology 26, 247259.Google Scholar
Tebot, I, Britos, A, Godeau, JM & Cirio, A (2002) Microbial protein production determined by urinary allantoin and renal urea sparing in normal and low protein fed Corriedale sheep. Veterinary Research 33, 101106.Google Scholar
Theurer, CB, Huntington, GB, Huber, JT, Swingle, RS & Moore, JA (2002) 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. Journal of Animal Science 80, 525532.Google Scholar
Timmer, RT, Klein, JD, Bagnasco, SM, Doran, JJ, Verlander, JW, Gunn, RB & Sands, JM (2001) Localization of the urea transporter UT-B protein in human and rat erythrocytes and tissues. American Journal of Physiology 281, C1318–C1325.Google Scholar
Tombola, F, Morbiato, L, Del Giudice, G, Rappuoli, R, Zoratti, M & Papini, E (2001) The Helicobacter pylori VacA toxin is a urea permease that promotes urea diffusion across epithelia. Journal of Clinical Investigation 108, 929937.CrossRefGoogle ScholarPubMed
Torrallardona, D, Harris, CI, Coates, ME & Fuller, MF (1996 a) Microbial amino acid synthesis and utilization in rats: incorporation of 15N from 15NH4Cl into lysine in the tissues of germ-free and conventional rats. British Journal of Nutrition 76, 689700.Google Scholar
Torrallardona, D, Harris, CI & Fuller, MF (1996 b) Microbial amino acid synthesis and utilization in rats: the role of coprophagy. British Journal of Nutrition 76, 701709.Google Scholar
Torrallardona, D, Harris, CI & Fuller, MF (2003) Pigs' gastrointestinal microflora provide them with essential amino acids. Journal of Nutrition 133, 11271131.Google Scholar
Ugawa, S, Sunouchi, Y, Ueda, T, Takahashi, E, Saishin, Y & Shimada, S (2001) Characterization of a mouse colonic system B(0+) amino acid transporter related to amino acid absorption in colon. American Journal of Physiology 281, G365–G370.Google Scholar
Vaira, D, Holton, J, Dowsett, J, Oderda, G & Barbera, L (1990) Helicobacter pylori – its role in gastric disease. Digestive Diseases 8, 322326.Google Scholar
Varady, J, Tashenov, KT, Boda, K, Fejes, J & Kosta, K (1979) Endogenous urea secretion into the sheep gastrointestinal tract. Physiologia Bohemoslov 28, 551559.Google Scholar
Walser, M & Bondenlos, LJ (1959) Urea metabolism in man. Journal of Clinical Investigation 38, 16171626.Google Scholar
Waterlow, JC (1999) The mysteries of nitrogen balance. Nutrition Research Reviews 12, 2554.Google Scholar
Wheeler, RA, Jackson, AA & Griffiths, DM (1991) Urea production and recycling in neonates. Journal of Pediatric Surgery 26, 575577.Google Scholar
Wiklund, L, George, M, Nord, CE, Ronquist, G & Saldeen, T (1998) Sudden infant death syndrome and nitrogen metabolism: further development of a hypothesis. European Journal of Clinical Investigation 28, 958968.Google Scholar
Wolfe, RR (1981) Measurement of urea kinetics in vivo by means of a constant tracer infusion of di-15N-urea. American Journal of Physiology 240, E428–E434.Google Scholar
Wolpert, E, Phillips, SF & Summerskill, WH (1971) Transport of urea and ammonia production in the human colon. Lancet ii, 13871390.Google Scholar
Wrong, OM (1967) The metabolism of urea and ammonium in the healthy and uraemic colon. Medical Journal of Australia 12, 281283.Google Scholar
Wrong, OM (1971) Intestinal handling of urea and ammonium. Proceedings of the Royal Society of Medicine 64, 10251026.Google Scholar
Wrong, OM (1978) Nitrogen metabolism in the gut. American Journal of Clinical Nutrition 31, 15871593.Google Scholar
Wu, ZC, Chijang, CC, Lau, BH, Hwang, B, Sugawara, M & Idota, T (2000) Crude protein content and amino acid composition in Taiwanese human milk. Journal of Science and Vitaminology 46, 246251.Google Scholar
You, G, Smith, CP, Kanai, Y, Lee, W, Stelzner, M & Hediger, M (1993) Cloning and characterization of the vasopressin-regulated urea transporter. Nature 365, 844847.Google Scholar
Younes, H, Demigne, C, Behr, SR, Garleb, KA & Remesy, C (1996) A blend of dietary fibers increases urea disposal in the large intestine and lowers urinary nitrogen excretion in rats fed a low protein diet. Nutritional Biochemistry 7, 474480.Google Scholar
Ziegler, TR, Fernandez-Estivariz, C, Gu, LH, Bazargan, N, Umeakunne, K, Wallace, TM, Diaz, EE, Rosado, KE, Pascal, RR, Galloway, JR, Wilcox, JN & Leader, LM (2002) Distribution of the H + /peptide transporter PepT1 in human intestine: upregulated expression in the colonic mucosa of patients with short-bowel syndrome. American Journal of Clinical Nutrition 75, 922930.Google Scholar