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Intestinal handling of a glucose gavage by the rat

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Abstract

An oral gavage of either 3, 1 or 0.1 mmoles of 14C-labelled glucose was given to rats under standard feeding conditions or food deprived for 24 hr. The fate of the glucose label was determined at 10, 15, 30 and 60 min after gavage; at 60 min 40% of the glucose was absorbed in fed rats (60% in food deprived). The portal vein blood flows were determined and the levels of glucose, lactate, alanine and pyruvate, and their radioactivity, as well as that of CO, were measured in both portal and arterial blood.

The net computed glucose and 3-carbon carriers (lactate, alanine and pyruvate) actually released into the portal system by the intestine was lower than the amount of glucose taken up from the intestinal lumen in one hour. Oxidation to 14CO2 accounted for a 12–15% of the absorbed glucose. The size of the gavage deeply affected the proportion of glucose released into the portal blood (c. 50% with a 3 mmoles gavage and practically nil with a 0.1 mmoles gavage), but it affected much less the generation of lactate and other 3 C carriers. In fed rats, the net intestinal balance of non-radioactive glucose was negative, and that of lactate positive; when radioactive glucose was considered, the pattern was inverted. In starved rats, both glucose and lactate were released in large proportions by the intestine, but alanine efflux was lower.

It can be concluded that the intestine consumes a considerable proportion of glucose in the fed state. Glucose handling by the intestine is compartmentalized in two functional circuits: glucose is taken up from the arterial blood and used for intestinal metabolism and lactate production, luminal glucose is absorbed mainly unaltered and transferred to the portal blood. Thus, the generation of lactate is mainly related to the availability of arterial glucose. In addition to the release of the ingested glucose as 3 C carriers or glucose, an extraportal pathway for glucose transfer into the bloodstream is postulated.

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References

  1. McGarry JD, Kuwajima M, Newgard CB, Foster DW, Katz J: From dietary glucose to liver glycogen: the full circle round. Annu Rev Nutr 7: 51–73, 1987

    Google Scholar 

  2. Watford M: What is the metabolic fate of dietary glucose? Trends Biochem Sci 13: 329–330, 1988

    Google Scholar 

  3. Katz LD, Glickman MG, Rapoport S, Ferrannini E, DeFronzo RA: Splanchnic and peripheral disposal of oral glucose in man. Diabetes 32: 675–679, 1983

    Google Scholar 

  4. Smadja C, Morin J, Ferré P, Girard J: Metabolic fate of a gastric glucose load in unrestrained rats bearing a portal vein catheter. Am J Physiol 254: E407-E413, 1988

    Google Scholar 

  5. Madison LL: Role of insulin in the hepatic handling of glucose. Arch Intern Med 123: 284–292, 1969

    Google Scholar 

  6. Felig P, Wahren J, Hendler R: Influence of oral glucose ingestion on splanchnic glucose and gluconeogenic substrate metabolism in man. Diabetes 24: 468–475, 1975

    Google Scholar 

  7. Newgard CB, Hirsch LJ, Foster DW, McGarry JD: Studies on the mechanism by which exogenous glucose is converted into liver glycogen in the rat. J Biol Chem 258: 8046–8052, 1983

    Google Scholar 

  8. Katz J, Kuwajima M, Foster DW, McGarry JD: The glucose paradox: new perspectives on hepatic carbohydrate metabolism. Trends Biochem Sci 11: 136–140, 1986

    Google Scholar 

  9. Pilkis SJ, El-Maghrabi MR, Claus TH: Hormonal regulation of hepatic gluconeogenesis and glycolysis. Annu Rev Biochem 57: 755–783, 1988

    Google Scholar 

  10. Shikama H, Ui M: Glucose load diverts hepatic gluconeogenic product from glucose to glycogen in vivo. Am J Physiol 235: E354-E360, 1978

    Google Scholar 

  11. Radziuk J: Sources of carbon in hepatic glycogen synthesis during absorption of an oral glucose load in humans. Fed Proc 41: 110–116, 1982

    Google Scholar 

  12. Huang MT, Veech RL: Role of the direct and indirect pathways for glycogen synthesis in rat liver in the postprandial state. J Clin Invest 81: 872–878, 1988

    Google Scholar 

  13. Sugden MC, Watts DI, Palmer TN, Myles DD: Direction of carbon flux in starvation and after refeeding: in vitro and in vivo effects of 3-mercaptopicolinate. Biochem Int 7: 329–337, 1983

    Google Scholar 

  14. Kuwajima M, Golden S, Katz J, Unger RH, Foster DW, McGarry JD: Active hepatic glycogen synthesis from gluconeogenic precursors despite high tissue levels of fructose 26-bisphosphate. J Biol Chem 261: 2632–2637, 1986

    Google Scholar 

  15. Windmueller HG, Spaeth AE: Respiratory fuels and nitrogen metabolism in vivo in small intestine of fed rats. Quantitative importance of glutamine glutamate and aspartate. J Biol Chem 255: 107–112, 1980

    Google Scholar 

  16. Nicholls TJ, Leese HJ, Bronk R: Transport and metabolism of glucose by rat small intestine. Biochem J 212: 183–187, 1983

    Google Scholar 

  17. Rich-Denson C, Kimura RE: Evidence in vivo that most of the intraluminally absorbed glucose is absorbed intact into the portal vein and not metabolized to lactate. Biochem J 254: 931–934, 1988

    Google Scholar 

  18. Aikawa T, Matsutaka H, Yamamoto H, Okuda T, Ishikawa E, Kawano T, Matsumura E: Gluconeogenesis and amino acid metabolism. II. Inter-organal relations and roles of glutamine and alanine in the amino acid metabolism of fasted rats. J Biochem 74: 1003–1017, 1973

    Google Scholar 

  19. Felig P, Pozefsky T, Marliss E. Cahill GF: Alanine: key role in gluconeogenesis. Science 167: 1003–1004, 1970

    Google Scholar 

  20. De Fronzo RA, Ferrannini E, Hendler R, Wahren J, Felig P: Influence of hyperinsulinemia hyperglycemia and the route of glucose administration on splanchnic glucose exchange. Proc Natl Acad Sci USA 75: 5173–5177, 1978

    Google Scholar 

  21. Schuster LT, Go VLM, Rizza RA, O'Brien PC, Service FJ: Incretin effect due to increased secretion and decreased clearance of insulin normal humans. Diabetes 37: 200–203, 1988

    Google Scholar 

  22. Bergman RN, Beir JR, Hourigan PM: Intraportal glucose infusion matched to oral glucose absorption Lack of evidence for ‘gut factor’ involvement in hepatic glucose storage. Diabetes 31: 27–35, 1982

    Google Scholar 

  23. Lang CH, Bagby GJ, Blakesley HL, Johnson JL, Spitzer JJ: Plasma glucose concentration determines direct versus indirect liver glycogen synthesis. Am J Physiol 251: E584-E590, 1986

    Google Scholar 

  24. Pénicaud L, Ferré P, Kande J, Leturque A, Issad T, Girard J: Effect of anesthesia on glucose production and utilization in rats. Am J Physiol 252: E365-E369, 1987

    Google Scholar 

  25. Jackson RA, Blix PM, Matthews JA, Morgan LM, Rubenstein AH, Nabarro JDN: Comparison of peripheral glucose uptake after oral glucose loading and a mixed meal. Metabolism 32: 706–710, 1983

    Google Scholar 

  26. Casado FJ, Fernández-López JA, Argilés JM, Alemany M: Role of the rat liver in the disposal of a glucose gavage. Mol Cell Biochem 113; 33–41, 1992

    Google Scholar 

  27. Katz ML, Bergman EN: Simultaneous measurement of hepatic and portal venous flow in the sheep and dog. Am J Physiol 216: 946–952, 1969

    Google Scholar 

  28. Casado J, Pastor-Anglada M, Remesar X: Hepatic uptake of amino acids at mid-lactation in the rat. Biochem J 245: 297–300, 1987

    Google Scholar 

  29. Barrowman JA, Granger DN: Effects of experimental cirrhosis on splanchnic microvascular fluid and solute exchange in the rat. Gastroenterology 87: 165–172, 1984

    Google Scholar 

  30. Peng CT: Sample preparation in liquid scintillation counting. Amersham International, Amersham, pp 47–48, 1977

    Google Scholar 

  31. Heding LG: Determination of total serum insulin (IRI) in insulin-treated diabetic patients. Diabetologia 8: 260–266, 1972

    Google Scholar 

  32. Trinder P: Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann Clin Biochem 6: 24–27, 1969

    CAS  Google Scholar 

  33. Gutmann I, Wahlefeld AW: in Methods of enzymatic analysis, second edition. Bergmeyer ed, pp 1464–1468. Academic Press, New York-London, 1974

  34. Passoneau JV, Lowry OH: in Methods of enzymatic analysis, second edition. Bergmeyer ed, pp 1452–1456. Academic Press, New York-London, 1974

  35. Williamson DH: in Methods of enzymatic analysis, second edition. Bergmeyer ed, pp 1679–1682. Academic Press, New York-London, 1974

  36. Golden S, Chenoweth M, Dunn A, Okajima F, Katz J: Metabolism of tritium- and 14-labelled alanine in rats. Am J Physiol 241: E121-E128, 1981

    Google Scholar 

  37. Casado J, Fernández-López JA, Argilés JM, Alemany M: A nondestructive method for the measurement of radioactive 14CO2 in blood. Anal Biochem 172: 509–513. 1988

    Google Scholar 

  38. Rémesy C, Demigné C: Changes in availability of gluconeogenic and ketogenic substrates and liver metabolism in fed or starved rats. Ann Nutr Metab 27: 57–70, 1983

    Google Scholar 

  39. Tuma RF, Vasthare US, Irion GL, Wiedeman MP: Considerations in use of microspheres for flow measurements in anaesthetized rats. Am J Physiol 250: H137-H143, 1986

    Google Scholar 

  40. Arola L, Palou A, Remesar X, Herrera E, Alemany M: Effect of ether sodium pentobarbital and chloral hydrate anesthesia on rat plasma metabolite concentrations. Rev Esp Fisiol 37: 379–386, 1981

    Google Scholar 

  41. Allison SP, Prowse K, Chamberlain MJ: Failure of insulin response to glucose load during operation and after myocardial infarction. Lancet i: 478–481, 1967

    Google Scholar 

  42. Casado J, Fernández-López JA, Esteve M, Rafecas I, Argilés JM, Alemany M: Rat spanchnic net oxygen consumption. Energetic implications. J Physiol-London 431: 557–569, 1990

    Google Scholar 

  43. Felig P, Owen OF, Wahren J, Cahill GF: Amino acid metabolism during prolonged starvation. J Clin Invest 48: 584–594, 1969

    Google Scholar 

  44. Palen A, Remesar X, Arola LI, Herrera E, Alemany M: Metabolic effects of short term food deprivation in the rat. Horm Metabol Res 13: 326–330, 1981

    Google Scholar 

  45. Leese HJ, Bronk JR: Lactate formation by rat small intestine in vitro. Biochim Biophys Acta 404: 40–48, 1975

    Google Scholar 

  46. Hanson PJ, Parsons DS: The utilization of glucose and production of lactate by in vitro preparation of rat small intestine: effect of vascular perfusion. J Physiol (Lond) 255: 775–795, 1976

    Google Scholar 

  47. Porteous JW: Glucoses as a fuel from small intestine. Biochem Soc Trans 6: 534–539, 1978

    Google Scholar 

  48. Abumrad NN, Cherrington AD, Williams PE, Lacy WW, Rabin D: Absorption and disposition of a glucose load in the conscious dog. Am J Physiol 242: E398-E406, 1982

    Google Scholar 

  49. Lee JS: Lymph flow during fluid absorption from rat jejunum. Am J Physiol 240: G312-G316, 1981

    Google Scholar 

  50. Argilés JM, Fernández-López JA, Casado J, Alemany M: Is there a role for limph in intestinal glucose absorption? Med Hyp 33: 169–171, 1990

    Google Scholar 

  51. Fernández-López JA, Casado J, Argilés M, Alemany M: In the rat, intestinal lymph carries a significant amount of ingested glucose into the bloodstream. Arch Int Physiol Biochim Biophys. In the press, 1992

  52. Bisgaier CL, Glickman RM: Intestinal synthesis secretion and transport of lipoproteins. Annu Rev Biochem 45: 625–636, 1983

    Google Scholar 

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Fernández-López, J.A., Casado, J., Argilés, J.M. et al. Intestinal handling of a glucose gavage by the rat. Mol Cell Biochem 113, 43–53 (1992). https://doi.org/10.1007/BF00230884

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