Glucose production and substrate cycle activity in a fasting adapted animal, the northern elephant seal

Cory D. Champagne; Dorian S. Houser; Daniel E. Crocker

doi:10.1242/jeb.01476

journal article Mar 01, 2005

Glucose production and substrate cycle activity in a fasting adapted animal, the northern elephant seal

Cory D. Champagne Dorian S. Houser Daniel E. Crocker

Journal of Experimental Biology Vol. 208 No. 5 pp. 859-868 · The Company of Biologists

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Abstract

SUMMARYDuring prolonged fasting physiological mechanisms defend lean tissue from catabolism. In the fasting state, glucose is derived solely from gluconeogenesis, requiring some catabolism of amino acids for gluconeogenic substrates. This creates a conflict in animals undergoing fasts concurrently with metabolically challenging activities. This study investigated glucose metabolism in fasting and developing neonatal elephant seals. Glucose production and glucose cycle activity were measured early (2 weeks) and late(6 weeks) in the postweaning fasting period. Additionally the role of regulatory hormones on glucose production and glucose cycle activity were investigated. Glucose cycle activity was highly variable throughout the study period, did not change over the fasting period, and was not correlated with insulin or glucagon level. Endogenous glucose production (EGP) was 2.80±0.65 mg kg–1 min–1 early and 2.21±0.12 during late fasting. Insulin to glucagon molar ratio decreased while cortisol levels increased over the fast (t=5.27,2.84; P=0.003, 0.04; respectively). There was no relationship between EGP and hormone levels. The glucose production values measured in this study were high and exceeded the estimated gluconeogenic substrate available. These data suggest extensive glucose recycling via Cori cycle activity occurring in northern elephant seals, and we propose a possible justification for this recycling.

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References

56

[1]

Adams, S. H. and Costa, D. P. (1993). Water conservation and protein metabolism in northern elephant seal pups during the postweaning fast. J. Comp. Physiol. B163,367-373. 10.1007/bf00265640

[2]

Castellini, M. A., Costa, D. P. and Huntley, A. C.(1987). Fatty acid metabolism in fasting elephant seal pups. J. Comp. Physiol. B157,445-449. 10.1007/bf00691828

[3]

Castellini, M. J. and Costa, D. P. (1990). Relationships between plasma ketones and fasting duration in neonatal elephant seals. Am. J. Physiol.259,R1086-R1089. 10.1152/ajpregu.1990.259.5.r1086

[4]

Castellini, M. A., Castellini, M. and Kirby, V. L.(1992). Effects of standard anticoagulants and storage procedures on plasma glucose values in seals. J. Am. Vet. Med. Assn.201,145-148. 10.2460/javma.1992.201.01.145

[5]

Cersosimo, E., Judd, R. L. and Miles, J. M.(1994). Insulin regulation of renal glucose metabolism in conscious dogs. J. Clin. Invest.93,2584-2589. 10.1172/jci117270

[6]

Cersosimo, E., Garlick, P. and Ferretti, J.(1999). Insulin regulation of renal glucose metabolism in humans. Am. J. Physiol.276,E78-E84. 10.1152/ajpendo.1999.276.1.e78

[7]

Cherel, Y., Leloup, J. and Le Maho, Y. (1988). Fasting in king penguin. II. Hormonal and metabolic changes during molt. Am. J. Physiol.254,R178-R184.

[8]

Cori, C. F. (1931). Mammalian carbohydrate metabolism. Physiol. Rev.11,143-275. 10.1152/physrev.1931.11.2.143

[9]

Costa, D. P. (1991). Reproductive and foraging energetics of pinnipeds: implications for life history paterns. In The Behavior of Pinnipeds (ed. D. Renouf). London:Chapman and Hall.

[10]

Costa, D. P. and Ortiz, C. L. (1982). Blood chemistry homeostasis during prolonged fasting in the northern elephant seal. Am. J. Physiol.242,R591-R595. 10.1152/ajpregu.1982.242.5.r591

[11]

Cowan, J. S., Vranic, M. and Wrenshall, G. A.(1969). Effects of preceding diet and fasting on glucose turnover in normal dogs. Metabolism18,319-330. 10.1016/0026-0495(69)90053-5

[12]

Dunn, A., Katz, J., Golden, S. and Chenoweth, M.(1976). Estimation of glucose turnover and recycling in rabbits using various [3H, 14C]glucose labels. Am. J. Physiol.230,1159-1162. 10.1152/ajplegacy.1976.230.4.1159

[13]

Felts, P. W., Crofford, O. B. and Park, C. R.(1964). Effect of infused ketone bodies on glucose utilization in the dog. J. Clin. Invest.43,638-646. 10.1172/jci104949

[14]

Friedmann, N., Exton, J. and Park, C. (1967). Interaction of adrenal steroids and glucagon on gluconeogenesis in perfused rat liver. Bioch. Biophys. Res. Commun.29,113-119. 10.1016/0006-291x(67)90550-5

[15]

Goldstein, R. E., Wasserman, D. H., McGuinness, O. P., Lacy, D. B., Cherrington, A. D. and Abumrad, N. N. (1993). Effects of chronic elevation in plasma cortisol on hepatic carbohydrate metabolism. Am. J. Physiol.264,E119-E127. 10.1152/ajpendo.1993.264.1.e119

[16]

Goodman, M. N., Larsen, P. R., Kaplan, M. M., Aoki, T. T.,Young, V. R. and Ruderman, N. B. (1980). Starvation in the rat. II. Effect of age and obesity on protein sparing and fuel metabolism. Am. J. Physiol.239,E277-E286.

[17]

Guinet, C., Servera, N., Mangin, S., Georges, J. Y. and Lacroix,A. (2004). Change in plasma cortisol and metabolites during the attendance period ashore in fasting lactating subantarctic fur seals. Comp. Biochem. Physiol.137A,523-531. 10.1016/j.cbpb.2003.11.006

[18]

Heaney, A. P., Harper, R., Ennis, C., Rooney, D. P., Sheridan,B., Atkinson, A. B. and Bell, P. M. (1997). Insulin action and hepatic glucose cycling in Cushing's syndrome. Clin. Endocrinol.46,735-743. 10.1046/j.1365-2265.1997.2121024.x

[19]

Henry, C. J., Rivers, J. P. and Payne, P. R.(1988). Protein and energy metabolism in starvation reconsidered. Eur. J. Clin. Nutr.42,543-549.

[20]

Hochachka, P. W. (1981). Brain, lung, and heart functions during diving and recovery. Science212,509-514. 10.1126/science.7209545

[21]

Houser, D. S. and Costa, D. P. (2001). Protein catabolism in suckling and fasting northern elephant seal pups (Mirounga angustirostris). J. Comp. Physiol. B171,635-642.

[22]

Houser, D. S. and Crocker, D. E. (2004). Age,sex, and reproductive state influence free amino acid concentrations in the fasting elephant seal. Physiol. Biochem. Zool.77,838-846. 10.1086/422055

[23]

Hue, L. and Hers, H. G. (1974). Utile and futile cycles in the liver. Biochem. Biophys. Res. Commun.58,540-548. 10.1016/s0006-291x(74)80454-7

[24]

Issekutz, B. (1977). Studies on hepatic glucose cycles in normal and methylprednisolone-treated dogs. Metabolism26,157-169. 10.1016/0026-0495(77)90051-8

[25]

Issekutz, B. and Allen, M. (1972). Effect of catecholamines and methylprednisolone on carbohydrate metabolism of dogs. Metabolism21,48-59. 10.1016/0026-0495(72)90019-4

[26]

Jiang, G. and Zhang, B. B. (2003). Glucagon and regulation of glucose metabolism. Am. J. Physiol.284,E671-E678. 10.1152/ajpendo.00492.2002

[27]

Katz, J. and Rognstad, R. (1976). Futile cycles in the metabolism of glucose. In Current Topics in cellular Regulation, vol. 10 (ed. B. L. Horecker and E. R. Stadtman), pp. 237-289. New York: Academic Press. 10.1016/b978-0-12-152810-2.50013-9

[28]

Katz, J. and Tayek, J. A. (1998). Gluconeogenesis and the Cori cycle in 12-, 20-, and 40-h-fasted humans. Am. J. Physiol.275,E537-E542. 10.1152/ajpendo.1998.275.3.e537

[29]

Katz, J., Dunn, A., Chenoweth, M. and Golden, S.(1974). Determination of synthesis, recycling and body mass of glucose in rats and rabbits in vivo 3H- and 14C-labelled glucose. Biochem. J.142,171-183. 10.1042/bj1420171

[30]

Keith, E. O. (1984). Glucose metabolism in fasting northern elephant seal pups. In Biology, pp.101. Santa Cruz: University of California.

[31]

Keith, E. O. and Ortiz, C. L. (1989). Glucose kinetics in neonatal elephant seals during postweaning aphagia. Mar. Mamm. Sci.5,99-115. 10.1111/j.1748-7692.1989.tb00326.x

[32]

Kirby, V. L. and Ortiz, C. L. (1994). Hormones and fuel regulation in fasting elephant seals. In Elephant Seals:Population Ecology, Behavior, and Physiology (ed. B. J. Le Boeuf and L. R. M.), pp. 374-386. Berkeley: University of California Press. 10.1525/9780520328150-023

[33]

Kraus-Friedmann, N. (1984). Hormonal regulation of hepatic gluconeogenesis. Physiol. Rev.64,170-259. 10.1152/physrev.1984.64.1.170

[34]

Landau, B. R. (1993). Measuring glucose and fructose-6-phosphate cycling in liver in vivo. Metabolism42,457-462. 10.1016/0026-0495(93)90103-u

[35]

Marliss, E. B., Aoki, T. T., Unger, R. H., Soeldner, J. S. and Cahill, G. F., Jr (1970). Glucagon levels and metabolic effects in fasting man. J. Clin. Invest.49,2256-2270. 10.1172/jci106445

[36]

Miyoshi, H., Shulman, G. I., Peters, E. J., Wolfe, M. H., Elahi,D. and Wolfe, R. R. (1988). Hormonal control of substrate cycling in humans. J. Clin. Invest.81,1545-1555. 10.1172/jci113487

[37]

Murphy, B., Zapol, W. M. and Hochachka, P. W.(1980). Metabolic activities of heart, lung, and brain during diving and recovery in the Weddell seal. J. Appl. Physiol.48,596-605. 10.1152/jappl.1980.48.4.596

[38]

Neely, R. D., Rooney, D. P., Bell, P. M., Bell, N. P., Sheridan,B., Atkinson, A. B. and Trimble, E. R. (1992). Influence of growth hormone on glucose-glucose 6-phosphate cycle and insulin action in normal humans. Am. J. Physiol.263,E980-E987. 10.1152/ajpendo.1992.263.5.e980

[39]

Nehlig, A. and de Vasconcelos, A. P. (1993). Glucose and ketone body utilization by the brain of neonatal rats. Prog. Neurobiol.40,163-221. 10.1016/0301-0082(93)90022-k

[40]

Newsholme, E. and Crabtree, B. (1976). Substrate cycles in metabolic regulation and in heat generation. Biochem. Soc. Symp.41,61-109.

[41]

Nordøy, E. S. and Blix, A. S. (1991). Glucose and ketone body turnover in fasting grey seal pups. Acta Physiol. Scand.141,563-571. 10.1111/j.1748-1716.1991.tb09118.x

[42]

Opazo, J. C., Soto-Gamboa, M. and Bozinovic, F.(2004). Blood glucose concentration in caviomorph rodents. Comp. Biochem. Physiol. A137, 57-64. 10.1016/j.cbpb.2003.09.007

[43]

Ortiz, C. L., Costa, D. P. and Le Boeuf, B. J.(1978). Water and energy flux in elephant seal pups fasting under natural conditions. Physiol. Zool.51,166-178. 10.1086/physzool.51.2.30157864

[44]

Ortiz, R. M., Wade, C. E. and Ortiz, C. L.(2001). Effects of prolonged fasting on plasma cortisol and TH in postweaned northern elephant seal pups. Am. J. Physiol.280,R790-R795. 10.1152/ajpregu.2001.280.3.r790

[45]

Ortiz, R. M., Noren, D. P., Ortiz, C. L. and Talamantes, F.(2003a). GH and ghrelin increase with fasting in a naturally adapted species, the northern elephant seal (Mirounga angustirostris). J. Endocrinol.178,533-539. 10.1677/joe.0.1780533

[46]

Ortiz, R. M., Houser, D. S., Wade, C. E. and Ortiz, C. L.(2003b). Hormonal changes associated with the transition between nursing and natural fasting in northern elephant seals (Mirounga angustirostris). Gen. Comp. Endocrinol.130, 78-83. 10.1016/s0016-6480(02)00572-5

[47]

Liver and kidney metabolism during prolonged starvation

Oliver E. Owen, PHILIP FELIG, Alfred P. Morgan et al.

Journal of Clinical Investigation 10.1172/jci106016

[48]

Pernia, S. D., Hill, A. and Ortiz, C. L.(1980). Urea turnover during prolonged fasting in the northern elephant seal. Comp. Biochem. Physiol.65B,731-734. 10.1016/0305-0491(80)90188-1

[49]

Reiter, J., Stinson, N. L. and Le Boeuf, B. J.(1978). Northern Elephant Seal Development: The Transition from Weaning to Nutritional Independence. Behav. Ecol. Sociobiol.3,337-367. 10.1007/bf00303199

[50]

Rooney, D. P., Neely, R. D., Ennis, C. N., Bell, N. P.,Sheridan, B., Atkinson, A. B., Trimble, E. R. and Bell, P. M.(1992). Insulin action and hepatic glucose cycling in essential hypertension. Metabolism41,317-324. 10.1016/0026-0495(92)90278-i

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Published: Mar 01, 2005
Vol/Issue: 208(5)
Pages: 859-868

Authors

C

Cory D. Champagne

Department of Biology, Sonoma State University, Rohnert Park, CA 94928, USA

D

Dorian S. Houser

Department of Biology, Sonoma State University, Rohnert Park, CA 94928, USA

D

Daniel E. Crocker

Department of Biology, Sonoma State University, Rohnert Park, CA 94928, USA

Cite This Article

Cory D. Champagne, Dorian S. Houser, Daniel E. Crocker (2005). Glucose production and substrate cycle activity in a fasting adapted animal, the northern elephant seal. Journal of Experimental Biology, 208(5), 859-868. https://doi.org/10.1242/jeb.01476

Glucose production and substrate cycle activity in a fasting adapted animal, the northern elephant seal

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