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Horm Metab Res 2006; 38(9): 607-613
DOI: 10.1055/s-2006-951306
Original Clinical

© Georg Thieme Verlag KG Stuttgart · New York

Diurnal Variation in Insulin-stimulated Systemic Glucose and Amino Acid Utilization in Pigs Fed with Identical Meals at 12-Hour Intervals

S. J. Koopmans 1 , J. van der Meulen 2 , R. Dekker 1 , H. Corbijn 3 , Z. Mroz 1
  • 1Animal Sciences Group, Division of Nutrition and Food, Wageningen University, Edelhertweg, Lelystad, The Netherlands
  • 2Animal Sciences Group, Division of Animal Resources Development, Wageningen University, Edelhertweg, Lelystad, The Netherlands
  • 3Animal Sciences Group, Division of Experimental Animal Services, Wageningen University, Edelhertweg, Lelystad, The Netherlands
Further Information

Publication History

Received 6 February 2006

Accepted after revision 18 April 2006

Publication Date:
18 September 2006 (online)

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Abstract

The diurnal variation in insulin-stimulated systemic glucose and amino acid utilization was investigated in eleven pigs of ∼ 40 kg. Pigs were fed isoenergetic/isoproteinic diets (366 kJ/kg BW0.75 per meal) in two daily rations (06:00 and 18:00 h). After a 3-week habituation period, hyperinsulinemic euglycemic euaminoacidemic clamp studies (by intra-portal insulin, glucose and amino acids infusion and arterial blood sampling) were performed starting at 06:00 or 18:00 h (while skipping the meal), using a cross-over within-animal design. Basal (preclamp) plasma concentrations of insulin, glucose, lactate, individual amino acids and urea were similar in the morning compared to the evening. Insulin-stimulated (∼ 4-fold increase over basal) systemic glucose utilization was similar (17.6±1.4 and 18.9±1.8 mg·kg-1·min-1) but amino acid utilization was 19% greater in the morning vs. the evening (2.37±0.21 vs. 1.99±0.15 mg·kg-1·min-1, p<0.05), respectively. Insulin-stimulated plasma lactate concentrations remained constant in the morning (0.77±0.06 to 0.71±0.04 mmol·l-1) but declined in the evening (0.89±0.09 to 0.65±0.06 mmol·l-1, p<0.05). By contrast, insulin-stimulated plasma urea concentrations declined in the morning (2.48±0.11 to 2.03±0.10 mmol·l-1, p<0.005) but remained constant in the evening (2.18±0.14 to 2.12±0.12 mmol·l-1). In conclusion, pigs fed identical meals at 12-hour intervals follow a clear diurnal biorhythm in protein anabolism, with greater insulin-stimulated systemic amino acid utilization and lower plasma urea response in the morning compared to the evening.

Key words

Insulin sensitivity - circadian rhythm - protein anabolism - autonomic nervous system - urea - lactate - swine

References

  • 1 Service FJ, Hall LD, Westland RE, O'Brien PC, Go VLW, Haymond MW, Rizza RA. Effects of size, time of day and sequence of meal ingestion on carbohydrate tolerance in normal subjects.  Diabetologia. 1983;  25 316-321
    PubMedGoogle Scholar
  • 2 Leighton B, Kowalchuk JM, Challiss RAJ, Newsholm EA. Circadian rhythm in sensitivity of glucose metabolism to insulin in rat soleus muscle.  Am J Physiol. 1988;  255 E41-E45
    PubMedGoogle Scholar
  • 3 Lesault A, Elchinger B, Desbals B. Circadian rhythms of food intake, plasma glucose and insulin levels in fed and fasted rabbits.  Horm Metab Res. 1991;  23 515-516
    PubMedGoogle Scholar
  • 4 Strubbe JH. Circadian rhythms of food intake. In: Westerterp-Plantenga MS, Fredrix EWHM, Steffens AB (eds). Food intake and energy expenditure. London CRC Press 1994: 155-174
    Google Scholar
  • 5 Koopmans SJ, Mandarino L, DeFronzo RA. Time course of insulin action on tissue-specific intracellular glucose metabolism in normal rats.  Am J Physiol. 1998;  274 E642-E650
    PubMedGoogle Scholar
  • 6 Bellinger LL, Mendel VE, Moberg GP. Circadian insulin, GH, prolactin, corticosterone and glucose rhythms in fed and fasted rats.  Horm Metab Res. 1975;  7 132-135
    PubMedGoogle Scholar
  • 7 Strubbe JH, Alingh Prins AJ, Bruggink J, Steffens AB. Daily variation of food-induced changes in blood glucose and insulin in the rat and the control by the suprachiasmatic nucleus and the vagus nerve.  J Autonom Nerv Syst. 1987;  20 113-119
    CrossrefPubMedGoogle Scholar
  • 8 Kalsbeek A, Strubbe JH. Circadian control of insulin secretion is independent of the temporal distribution of feeding.  Physiol Behav. 1998;  63 553-558
    CrossrefPubMedGoogle Scholar
  • 9 Buijs RM, Kalsbeek A. Hypothalamic integration of central and peripheral clocks.  Nature Rev. 2001;  2 521-526
    CrossrefPubMedGoogle Scholar
  • 10 Frape DL, Williams NR, Scriven AJ, Palmer CR, O'Sullivan K, Fletcher RJ. Diurnal trends in responses of blood plasma concentrations of glucose, insulin, and C-peptide following high- and low-fat meals and their relation to fat metabolism in healthy middle-aged volunteers.  Br J Nutr. 1997;  77 523-535
    CrossrefPubMedGoogle Scholar
  • 11 Squibb RL. Diurnal rhythm of tissue components related to protein metabolism in normal and virus infected chicks.  J Nutr. 1966;  90 71-76
    PubMedGoogle Scholar
  • 12 Rapoport MI, Beisel WR. Circadian periodicity of tryptophan metabolism.  J Clin Invest. 1968;  47 934-939
    PubMedGoogle Scholar
  • 13 Feigin RD, Klainer AS, Beisel WR. Circadian periodicity of blood amino acids in adult man.  Nature. 1976;  215 512-514
    PubMedGoogle Scholar
  • 14 De Boer SF, Van der Gugten J. Daily variations in plasma noradrenaline, adrenaline and corticosterone concentrations in rats.  Physiol Behav. 1986;  40 323-328
    PubMedGoogle Scholar
  • 15 Van Cauter E, Shapiro ET, Tillil H, Polonsky KS. Circadian modulation of glucose and insulin responses to meals: relationship to cortisol rhythm.  Am J Physiol. 1992;  262 E467-E475
    PubMedGoogle Scholar
  • 16 Kraetzl WD, Schams D, Brem G. Secretory patterns of porcine growth hormone and insulin-like growth-factor-1 in growing pigs.  J Anim Physiol Anim Nutr. 1994;  71 1-14
    PubMedGoogle Scholar
  • 17 Koopmans SJ, Van der Meulen J, Dekker R, Corbijn H, Mroz Z. Diurnal rhythms in plasma cortisol, insulin, glucose, lactate and urea in pigs fed identical meals at 12-hourly intervals.  Physiol Behav. 2005;  84 497-503
    CrossrefPubMedGoogle Scholar
  • 18 Newsholm EA, Leech AR. Biochemistry for the Medical Sciences. John Wiley & Sons Ltd. UK 1983
    Google Scholar
  • 19 DeFronzo RA. The triumvirate: beta-cell, muscle, liver. A collusion responsible for NIDDM.  Diabetes. 1987;  37 667-687
    PubMedGoogle Scholar
  • 20 Donaghue KM, Badger TM, Miljard WJ, Frisch LS, Russell WE. Absence of ultradian rhythm or diurnal variation in insulin-like growth factor-I in rats.  Neuroendocrinology. 1990;  52 1-8
    PubMedGoogle Scholar
  • 21 DeFronzo RA, Ferrannini E. Insulin actions in vivo: Protein Metabolism. In: Alberti, KGMM (ed). International Textbook of diabetes mellitus. John Wiley & Sons Ltd 1992: 467-511
    Google Scholar
  • 22 Van Cauter E, Polonsky KS, Scheen AJ. Roles of circadian rhythmicity and sleep in human glucose regulation.  Endocr Rev. 1997;  18 716-738
    CrossrefPubMedGoogle Scholar
  • 23 Southorn BG, Palmer RM, Garlick PJ. Acute effects of corticosterone on tissue protein synthesis and insulin-sensitivity in rats in vivo.  Biochem J. 1990;  272 187-191
    PubMedGoogle Scholar
  • 24 Goldstein RE, Reed GW, Wasserman DH, Williams PE, Lacy DB, Buckspan R, Abumrad NN, Cherrington AD. The effects of acute elevations in plasma cortisol levels on alanine metabolism in the conscious dog.  Metabolism. 1992;  41 1295-1303
    CrossrefPubMedGoogle Scholar
  • 25 Strack AM, Sebastian RJ, Schwartz MW, Dallman MF. Glucocorticoids and insulin: reciprocal signals for energy balance.  Am J Physiol. 1995;  268 R142-R149
    PubMedGoogle Scholar
  • 26 Bratusch-Marrain PR. Insulin-counteracting hormones: their impact on glucose metabolism.  Diabetologia. 1983;  24 74-79
    CrossrefPubMedGoogle Scholar
  • 27 Millward DJ. The hormonal control of protein turnover.  Clin Nutr. 1990;  9 115-126
    CrossrefPubMedGoogle Scholar
  • 28 Sacca L, Morrone G, Cicala M, Corso G, Ungaro B. Influence of epinephrine, norepinephrine, and isoproterenol on glucose homeostasis in normal man.  J Clin Endocrinol Metab. 1980;  50 680-684
    PubMedGoogle Scholar
  • 29 Baron AD, Wallace P, Brechtel G. In vivo regulation of non-insulin-mediated and insulin-mediated glucose uptake by cortisol.  Diabetes. 1987;  36 1230-1237
    PubMedGoogle Scholar
  • 30 Almdal TP, Vilstrup H. Exogenous hyperglucagonaemia in insulin controlled diabetic rats increases urea excretion and nitrogen loss from organs.  Diabetologia. 1988;  31 836-841
    PubMedGoogle Scholar
  • 31 Wolfe RR. Radioactive and stable isotope tracers in biomedicine. Principles and practice of kinetic analysis. New York: Wiley-Liss, Inc. Publication 1992
    Google Scholar
  • 32 Tumbleson ME, Schook LB. Advances in swine in biomedical research. Volume 1 & 2. Plenum Press, New York, USA 1996
    Google Scholar
  • 33 Koopmans SJ, Mroz Z, Dekker R, Corbijn H, Wijdenes J, Van der Crabben S, Ackermans M, Sauerwein HP. Insulin-stimulated net utilization of plasma glucose and amino acids in growing pigs. In: Souffrant WB, Metges CC (eds). Progress in research on energy and protein metabolism. 2003 109: 197-200
    Google Scholar
  • 34 Wray-Cahen D, Beckett PR, Nguyen HV, Davis TA. Insulin-stimulated amino acid utilization during glucose and amino acid clamps decreases with development.  Am J Physiol. 1997;  273 E305-E314
    PubMedGoogle Scholar
  • 35 Jonge de LH, Breuer M. Modification of the analysis of amino acids in pig plasma.  J Chromatography B. 1994;  652 90-96
    PubMedGoogle Scholar
  • 36 Gutmann I, Bergmeyer HU. Urea. In: Bergmeyer HU (ed). Methods of enzymatic analyses. 2nd Edition. New York and London: Verlag Chemie Weinheim and Academic Press Inc 1974: 1791
    Google Scholar
  • 37 Payne RW, Lane PW, Ainsley AE, Bicknell KE, Digby PGN, Harding SA, Leech PK, Simpson HR, Todd AD, Verrier PJ, White RP. Genstat 5 reference Manual. Oxford, U.K: Oxford University Press 1987
    Google Scholar
  • 38 Liu SM, Lobley GE, Macleod NA, Kyle DJ, Chen XB, Ørskov ER. Effects of long-term protein excess or deficiency on whole-body protein turnover in sheep nourished by intragastric infusion of nutrients.  Br J Nutr. 1995;  73 829-839
    CrossrefPubMedGoogle Scholar
  • 39 Ferrannini E. Metabolic interactions of amino acids and glucose in healthy humans.  Diab Nutr Metab. 1988;  3 176-186
    PubMedGoogle Scholar
  • 40 Randle PJ, Garland PB, Hales CN, Newsholme EA. The glucose-fatty acid cycle: its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus.  Lancet. 1963;  1 785-789
    PubMedGoogle Scholar

Correspondence

S. J. Koopmans

Animal Sciences Group·Division of Nutrition and Food·Wageningen University

Edelhertweg 15·P.O. Box 65·8200 AB Lelystad·The Netherlands

Phone: +31/320/23 73 27

Fax: +31/320/23 73 20

Email: sietse-jan.koopmans@wur.nl

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