Abstract
In ruminants, the uptake of inorganic phosphate (Pi) across the intestinal mucosa epithelium by Na-dependent and Na-independent mechanisms is a main regulatory factor in P homeostasis. The aim of the study was to elucidate to which extent Na-independent mechanisms, including pH effects or composition of mucosal brush-border membranes, could be involved in positive stimulation of Pi absorptive processes seen under the P deficient condition. Therefore, luminal, surface and intracellular pH of the jejunal epithelial cells in control and P depleted goats were compared and biochemical analyses of membrane phospholipids in the apical membrane of the jejunal epithelium were performed. Dietary P depletion resulted in decreased plasma Pi levels. While pH in jejunal ingesta was not significantly changed, P depletion resulted in a significantly lower surface pH in the crypt region compared to control animals (7.62 ± 0.02 vs. 7.77 ± 0.04, n = 4, P < 0.01). Inhibition of apical Na+/H+-exchange resulted in an increase of the jejunal surface pH in P depleted animals by 0.07 ± 0.01 (n = 6, P < 0.01) and 0.05 ± 0.01 (n = 6, P < 0.01) for the villus and the crypt region, respectively. This increase were inversely correlated with the initial surface pH prior to inhibition. In contrast to surface pH, intracellular pH of the jejunal epithelium and the phospholipid composition of the apical jejunal membrane were not affected by P depletion. Although the data suggest the existence of a Na+/H+-exchange mechanism at the luminal surface of goat jejunum they do not support the hypothesis that adaptational processes of active Pi absorption from goat jejunum in response to low dietary P could be based on “non Pi transporter events”.
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References
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 31:911
Blikslager AT, Roberts MC, Argenzio RA (1999) Prostaglandin-induced recovery of barrier function in porcine ileum is triggered by chloride secretion. Am J Physiol 276:G28–G36
Bode H, Schmitz H, Fromm M, Scholz P, Riecken EO, Schulzke JD (1998) IL-1beta and TNF-alpha, but not IFN-alpha, IFN-gamma, IL-6 or IL-8, are secretory mediators in human distal colon. Cytokine 10:457–465
Boron WF (1986). Intracellular pH regulation in epithelial cells. Annu Rev Physiol 48:377–388
Breves G, Schröder B (1991) Comparative aspects of gastrointestinal phosphorus metabolism. Nutr Res Rev 4:125–140
Busche R, Jeromin A, von Engelhardt W, Rechkemmer G (1993). Basolateral mechanisms of intracellular pH regulation in the colonic epithelial cell line HT29 clone 19A. Pflügers Arch 425:219–224
Busche R, Bartels J, Kirschberger S, von Engelhardt W (2002). Intracellular pH regulation of guinea pig caecal and colonic enterocytes during and after loading with short-chain fatty acids and ammonia. Pflügers Arch 444:785–794
Caboni MF, Menotta S, Lercker G (1996) Separation and analysis of phospholipids with a light-scattering-detector. J Am Oil Chem Soc 73:1561–1566
Daniel H, Rehner G (1986) Effect of metabolizable sugars on the mucosal surface pH of rat intestine. J Nutr 116:768–777
Danisi G, Murer H (1991). Inorganic phosphate absorption in small intestine. In: Schultz SG (ed) Handbook of physiology. The gastrointestinal system IV. Oxford University Press, New York, pp 323–336
Daveloose D, Linard A, Arfi T, Viret J, Christon R (1993) Simultaneous changes in lipid composition, fluidity and enzyme activity in piglet intestinal brush border membrane as affected by dietary polyunsaturated fatty acid deficiency. Biochim Biophys Acta 1166:229–237
Engelmann BE, Bindslev N, Poulsen SS, Hansen MB (2002) Effects of cyclooxygenase and lipoxygenase inhibition on basal- and serotonin-induced ion transport in rat colon. Comp Biochem Physiol C Toxicol Pharmacol 132:37–52
Fuhrmann H, Sallmann HP (1996) Phospholipid fatty acids of brain and liver are modified by alpha-tocopherol and dietary fat in growing chicks. Br J Nutr 76:109–122
Genz AK, von Engelhardt W, Busche R (1999) Maintenance and regulation of the pH-microclimate at the luminal surface of the distal colon of guinea pig. J Physiol (London) 517:507–519
Hilfiker H, Hattenhauer O, Traebert M, Forster I, Murer H, Biber J (1998) Characterization of a murine type II sodium-phosphate cotransporter expressed in mammalian small intestine. Proc Natl Acad Sci USA 95:14564–14569
Huber K, Walter C, Schröder B, Biber J, Murer H, Breves G (2000) Epithelial phosphate transporters in small ruminants. Ann NY Acad Sci 915:95–97
Huber K, Schröder B, Breves G (2002a) Phosphate transport in the duodenum and jejunum of goats and its adaptation by dietary phosphate and calcium. Am J Physiol 283: R296–302
Huber K, Roesler U, Muscher A, Hansen K, Widiyono I, Pfeffer E, Breves G (2002b) Ontogenesis of epithelial phosphate transport systems in goats. Am J Physiol 283:R296–302
Kaluzny MA, Duncan LA, Merritt MV, Epps DE (1985) Rapid separation of lipid classes in high yield and purity using bonded phase columns. J Lipid Res 26:135–140
Katai K, Miyamoto K, Kishida S, Segawa H, Nii T, Tanaka H, Tani Y, Tatsumi S, Morita K, Taketani Y, Takeda E (1999) Regulation of intestinal Na+-dependent phosphate co-transporters by a low-phosphate diet and 1,25-dihydroxyvitamin D3. Biochem J 343:705–712
Kirschberger S, Busche R, von Engelhardt W (1999) Surface-pH at the basolateral membrane of the caecal mucosa of guinea pig. J Membr Biol 169:111–122
Korotkova M, Strandvik B (2000) Essential fatty acid deficiency affects the fatty acid composition of the rat small intestinal and colonic mucosa differently. Biochim Biophys Acta 1487:319–325
Lepage G, Roy CC (1986) Direct transesterification of all classes of lipids in a one-step reaction. J Lipid Res 27:114–120
Markossian S, Kreydiyyeh SI (2005) TNF-alpha down-regulares the Na+–K+ ATPase and the Na+–K+–2Cl-cotransporter in the rat colon via PEG2. Cytokine 30:319–327
McEwan GT, Daniel H, Fett C, Burgess MN, Lucas ML (1988) The effect of Escherichia coli Sta enterotoxin and other secretagogues on mucosal surface pH of rat small intestine in vivo. Proc R Soc London B Biol Sci 234:219–237
Meyer zu Düttingdorf HD, Sallmann HP, Glockenthör U, von Engelhardt W, Busche R (1999) Isolation and lipid composition of apical and basolateral membranes of colonic segments of guinea Pig. Anal Biochem 269:45–53
Pfeffer E, Rodehutscord M, Breves G (1996) Effects of varying dietary calcium and phosphorus on growth and on composition of empty bodies and isolated bones of male kids. Arch Anim Nutr 49:243–252
Schröder B, Breves G (1996). Mechanisms of phosphate uptake into brush-border membrane vesicles from goat jejunum. J Comp Physiol B 166:230–240
Schröder B, Kaune R, Harmeyer J (1991) Effects of calcitriol on stimulation of ion transport in pig jejunal mucosa. J Physiol (London) 433:451–465
Schröder B, Käppner H, Failing K, Pfeffer E, Breves G (1995) Mechanisms of intestinal phosphate transport in small ruminants. Br J Nutr 74:635–648
Schröder B, Hattenhauer O, Breves G (1998) Phosphate transport in pig proximal small intestines during postnatal development: lack of modulation by calcitriol. Endocrinology 139:1500–1507
Schröder B, Walter C, Breves G, Huber K (2000) Comparative studies on Na-dependent Pi transport in ovine, caprine and porcine renal cortex. J Comp Physiol B 170:387–393
Shirazi-Beechey SP, Beechey RB, Penny J, Vayro S, Buchan W, Scott D. (1991) Mechanisms of phosphate transport in sheep intestine and parotid gland: response to variation in dietary phosphate supply. Exp Physiol 76:231–241
Shirazi-Beechey SP, Penny JI, Dyer J, Wood IS, Tarpey PS, Scott D, Buchan W (1996) Epithelial phosphate transport in ruminants, mechanisms and regulation. Kidney Int 49:992–996
Smith PL, Blumberg JB, Stoff JS, Field M (1981). Antisecretory effects of indomethacin on rabbit ileal mucosa in vitro. Gastroenterology 80:356–365
Thwaites DT, McEwan GT, Simmons NL (1995) The role of the proton electrochemical gradient in the transepithelial absorption of amino acids by human intestinal Caco-2 cell monolayers. J Membr Biol 145:245–256
Acknowledgments
We thank Katrin Hansen, Gerhild Becker and Uwe Glockenthör for excellent technical assistance. This study was supported by Deutsche Forschungsgemeinschaft (SFB 280 “Gastrointestinale Barriere”, A1 and A14).
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Communicated by G. Heldmaier.
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Busche, R., Schröder, B., Huber, K. et al. The effects of dietary phosphorus deficiency on surface pH and membrane composition of the mucosa epithelium in caprine jejunum. J Comp Physiol B 177, 135–142 (2007). https://doi.org/10.1007/s00360-006-0118-3
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DOI: https://doi.org/10.1007/s00360-006-0118-3