Journal of Comparative Physiology B

, Volume 177, Issue 1, pp 135–142 | Cite as

The effects of dietary phosphorus deficiency on surface pH and membrane composition of the mucosa epithelium in caprine jejunum

  • R. Busche
  • B. Schröder
  • K. Huber
  • H. P. Sallmann
  • G. Breves
Original Paper
First Online:
Received:
Revised:
Accepted:
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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”.

Keywords

Jejunum Surface pH P deficiency Caprine jejunum 
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Notes

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).

References

  1. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 31:911Google Scholar
  2. 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–G36PubMedGoogle Scholar
  3. 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 10:457–465PubMedCrossRefGoogle Scholar
  4. Boron WF (1986). Intracellular pH regulation in epithelial cells. Annu Rev Physiol 48:377–388PubMedCrossRefGoogle Scholar
  5. Breves G, Schröder B (1991) Comparative aspects of gastrointestinal phosphorus metabolism. Nutr Res Rev 4:125–140CrossRefPubMedGoogle Scholar
  6. 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 425:219–224PubMedCrossRefGoogle Scholar
  7. 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 444:785–794PubMedCrossRefGoogle Scholar
  8. Caboni MF, Menotta S, Lercker G (1996) Separation and analysis of phospholipids with a light-scattering-detector. J Am Oil Chem Soc 73:1561–1566CrossRefGoogle Scholar
  9. Daniel H, Rehner G (1986) Effect of metabolizable sugars on the mucosal surface pH of rat intestine. J Nutr 116:768–777PubMedGoogle Scholar
  10. 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 323–336Google Scholar
  11. 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 1166:229–237PubMedGoogle Scholar
  12. 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 132:37–52PubMedCrossRefGoogle Scholar
  13. 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 76:109–122PubMedCrossRefGoogle Scholar
  14. 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) 517:507–519CrossRefGoogle Scholar
  15. 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 95:14564–14569PubMedCrossRefGoogle Scholar
  16. Huber K, Walter C, Schröder B, Biber J, Murer H, Breves G (2000) Epithelial phosphate transporters in small ruminants. Ann NY Acad Sci 915:95–97PubMedCrossRefGoogle Scholar
  17. 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: R296–302Google Scholar
  18. 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:R296–302Google Scholar
  19. 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 26:135–140PubMedGoogle Scholar
  20. 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 343:705–712PubMedCrossRefGoogle Scholar
  21. Kirschberger S, Busche R, von Engelhardt W (1999) Surface-pH at the basolateral membrane of the caecal mucosa of guinea pig. J Membr Biol 169:111–122PubMedCrossRefGoogle Scholar
  22. 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 1487:319–325PubMedGoogle Scholar
  23. Lepage G, Roy CC (1986) Direct transesterification of all classes of lipids in a one-step reaction. J Lipid Res 27:114–120PubMedGoogle Scholar
  24. 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 30:319–327PubMedCrossRefGoogle Scholar
  25. 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 234:219–237CrossRefGoogle Scholar
  26. 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 269:45–53PubMedCrossRefGoogle Scholar
  27. 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 49:243–252CrossRefGoogle Scholar
  28. Schröder B, Breves G (1996). Mechanisms of phosphate uptake into brush-border membrane vesicles from goat jejunum. J Comp Physiol B 166:230–240PubMedCrossRefGoogle Scholar
  29. Schröder B, Kaune R, Harmeyer J (1991) Effects of calcitriol on stimulation of ion transport in pig jejunal mucosa. J Physiol (London) 433:451–465Google Scholar
  30. Schröder B, Käppner H, Failing K, Pfeffer E, Breves G (1995) Mechanisms of intestinal phosphate transport in small ruminants. Br J Nutr 74:635–648PubMedCrossRefGoogle Scholar
  31. 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 PubMedCrossRefGoogle Scholar
  32. 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 170:387–393PubMedCrossRefGoogle Scholar
  33. 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 76:231–241PubMedGoogle Scholar
  34. 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 49:992–996PubMedGoogle Scholar
  35. Smith PL, Blumberg JB, Stoff JS, Field M (1981). Antisecretory effects of indomethacin on rabbit ileal mucosa in vitro. Gastroenterology 80:356–365PubMedGoogle Scholar
  36. 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 145:245–256PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • R. Busche
    • 1
  • B. Schröder
    • 2
  • K. Huber
    • 2
  • H. P. Sallmann
    • 3
  • G. Breves
    • 2
  1. 1.Clinic for CattleSchool of Veterinary MedicineHannoverGermany
  2. 2.Department of PhysiologySchool of Veterinary MedicineHannoverGermany
  3. 3.Department of Physiological ChemistrySchool of Veterinary MedicineHannoverGermany

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