Hormone and metabolite changes associated with extended breeding fasts in male northern elephant seals (Mirounga angustirostris)

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 161, Issue 4, 2012, Pages 388-394

  Crocker, Daniel E ^a   Ortiz, Rudy M ^b   Houser, Dorian S ^c   Webb, Paul M ^d   Costa, Daniel P ^e  

^a SONOMA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL MARINE MAMMAL FOUNDATION   (United States)

^d ROGER WILLIAMS UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adipose tissue; Cortisol; DDE; Deiondination; Elephant seal; Fasting; Ghrelin; Leptin; Thyroxine

Indexed keywords

FATTY ACID; GHRELIN; GLUCAGON; GLUCOSE; GROWTH HORMONE; HYDROCORTISONE; INSULIN; LEPTIN; LIOTHYRONINE; OXOACID; SOMATOMEDIN C; THYROXINE;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY MASS; BREEDING; DECREASED APPETITE; DEIODINATION; DIET RESTRICTION; ELEPHANT; ENERGY EXPENDITURE; FATTY ACID BLOOD LEVEL; FEMALE; GLUCAGON BLOOD LEVEL; GLUCOSE BLOOD LEVEL; GROWTH HORMONE BLOOD LEVEL; HOMEOSTASIS; HYDROCORTISONE BLOOD LEVEL; INSULIN BLOOD LEVEL; LIOTHYRONINE BLOOD LEVEL; MALE; MIROUNGA ANGUSTIROSTRIS; NONHUMAN; PROTEIN DEGRADATION; THYROXINE BLOOD LEVEL; UREA NITROGEN BLOOD LEVEL;

MAMMALIA; MIROUNGA; MIROUNGA ANGUSTIROSTRIS;

EID: 84857370622     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2011.12.013     Document Type: Article

References (79)

1. Ahima R.S., Prabakaran D., Mantzoros C., Qu D., Lowell B., Maratos-Flier E., Flier J.S. Role of leptin in the neuroendocrine response to fasting. Nature 1996, 382:250-252.
2. Anderson S.S., Fedak M.A. Grey seal males: energetic and behavioural links between size and sexual success. Anim. Behav. 1985, 33:829-838.
3. Baumber J., South F.E., Ferren L., Zatzman M.L. A possible basis for periodic arousals during hibernation: accumulation of ketone bodies. Life Sci. 1971, 10:463-467.
4. Bennett K.A., Moss S.E.W., Pomeroy P., Speakman J.R., Fedak M.A. Effects of handling regime and sex on changes in cortisol, thyroid hormones and body mass in fasting grey seal pups. Com. Biochem. Phys. A 2012, 161:69-76.
5. Berelowitz M., Szabo M., Frohman L.A., Firestone S., Chu L., Hintz R.L. Somatomedin-C mediates growth hormone negative feedback by effects on both the hypothalamus and the pituitary. Science 1981, 212:1279-1281.
6. Bergendahl M., Vance M.L., Iranmanesh A., Thorner M.O., Veldhuis J.D. Fasting as a metabolic stress paradigm selectively amplifies cortisol secretory burst mass and delays the time of maximal nyctohemeral cortisol concentrations in healthy men. J. Clin. Endocrin. Metab. 1996, 81:692-699.
7. Blake N.G., Eckland D.J., Foster O.J., Lightman S.L. Inhibition of hypothalamic thyrotropin-releasing hormone messenger ribonucleic acid during food deprivation. Endocrinology 1991, 129:2714-2718.
8. Boden G., Chen X., Mozzoli M., Ryan I. Effect of fasting on serum leptin in normal human subjects. J. Clin. Endocrinol. Metab. 1996, 81:3419-3423.
9. Boelen A., Wiersinga W.M., Fliers E. Fasting-induced changes in the hypothalamus-pituitary-thyroid axis. Thyroid 2008, 18:123-129.
10. Boily P. Metabolic and hormonal changes during the molt of captive gray seals, Halichoerus grypus. Am. J. Physiol. 1996, 270:R1051-R1058.
11. Bowen W.D., Iverson S.J. Estimation of total body water in pinnipeds using hydrogen-isotope dilution. Physiol. Biochem. Zool. 1998, 71:329-332.
12. Boyle P.J., Shah S.D., Cryer P.E. Insulin, glucagon and catecholamines in prevention of hypoglycemia during fasting. Am. J. Physiol. 1989, 256:E651-E661.
13. Broglio F., Arvat E., Benso A., Gottero C., Muccioli G., Papotti M., van der Lely A.J., Deghenghi R., Ghigo E. Ghrelin, a Natural GH Secretagogue Produced by the Stomach, Induces Hyperglycemia and Reduces Insulin Secretion in Humans. J. Clin. Endocrin. Metab. 2001, 86:5083-5086.
14. Cahill G.F. Famine symposium: physiology of acute starvation in man. Ecolog. Food Nutr. 1978, 6:221-230.
15. Castellini M.A., Costa D.P. Relationships between plasma ketones and fasting duration in neonatal elephant seals. Am. J. Physiol. 1990, 259:R1086-R1089.
16. Castellini M.A., Rea L.D. The biochemistry of natural fasting at its limits. Cell. Mol. Life Sci. 1992, 48:575-582.
17. Champagne C.D., Houser D.S., Crocker D.E. Glucose production and substrate cycle activity in a fasting adapted animal, the northern elephant seal. J. Exp. Biol. 2005, 208:859-868.
18. Champagne C.D., Houser D.S., Crocker D.E. Glucose metabolism during lactation in a fasting animal, the northern elephant seal. Am. J. Physiol. 2006, 291:R1129-R1137.
19. Cherel Y., LeMaho Y. Five months of fasting in king penguin chicks: body mass loss and fuel metabolism. Am. J. Physiol. 1985, 249:R387-R392.
20. Cherel Y., LeMaho Y. Changes in body mass and plasma metabolites during short-term fasting in the king penguin. Condor 1988, 90:257-258.
21. Cherel Y., Robin J.P., Walch O., Karmann H., Netchitailo P., Le Maho Y. Fasting in king penguin. I. Hormonal and metabolic changes during breeding. Am. J. Physiol. 1988, 254:R170-177.
22. Cherel Y., Robin J.P., Heitz A., Calgari C., Le Maho Y. Relationships between lipid availability and protein utilization during prolonged fasting. J. Comp. Physiol. B 1992, 162:305-311.
23. Cherel Y., Omari B.E., Le Maho Y., Sabourea M. Protein and lipid utilization during fasting with shallow and deep hypothermia in the European hedgehog (Erinaceus europaeus). J. Comp. Physiol. B 1995, 164:653-658.
24. Costa D.P. Isotopic methods for quantifying material and energy intake of free-ranging marine mammals. Approaches to Marine Mammal Energetics 1987, 43-66. Society for Marine Mammalogy. A.C. Huntley, D.P. Costa, G.A.J. Worthy, M.A. Castellini (Eds.).
25. Crocker D.E., Webb P.M., Costa D.P., Le Boeuf B.J. Protein catabolism and renal function in lactating northern elephant seals. Physiol. Zool. 1998, 71:485-491.
26. Crocker D.E., Houser D.S., Webb P.M. Impact of body reserves on energy expenditure, water flux, and mating success in breeding male northern elephant seals. Physiol. Biochem. Zool. 2012, 85:11-20.
27. Cuendet G.S., Loten E.G., Cameron D.P., Renold A.E., Marliss E.B. Hormone-substrate responses to total fasting in lean and obese mice. Am. J. Phys. 1975, 228:276-283.
28. Deutsch C.J., Haley M.P., Le Boeuf B.J. Reproductive effort of male northern elephant seals: estimates from mass loss. Can. J. Zool. 1990, 68:2580-2593.
29. Deutsch C., Costa D.P., Le Boeuf B.J. Sex differences in reproductive effort in northern elephant seals. Elephant Seals: Population Ecology, Behavior, and Physiology 1994, 169-210. University of California Press, Berkeley. B.J. Le Boeuf, R.M. Laws (Eds.).
30. Donahue S.W., Galley S.A., Vaughan M.R., Patterson-Buckendahl P., Demers L.M., Vance J.L., McGee M.E. Parathyroid hormone may maintain bone formation in hibernating black bears, Ursus americanus to prevent disuse osteoperosis. J. Exp. Biol. 2006, 209:1630-1638.
31. Florant G.L., Hoo-Paris R., Castex C., Bauman W.A., Sutter B.C. Pancreatic A and B cell stimulation in euthermic and hibernating marmots, Marmota flaviventris: effects of glucose and arginine administration. J. Comp. Physiol. B 1986, 156:309-314.
32. Fowler M.A., Champagne C.D., Houser D.S., Crocker D.E. Hormonal regulation of glucose clearance in lactating northern elephant seals (Mirounga angustirostris). J. Exp. Biol. 2008, 211:2943-2949.
33. Fuglei E., Mustonen A.-M., Nieminen P. Effects of season, food deprivation and re-feeding on leptin, ghrelin and growth hormone in arctic foxes, Alopex lagopus on Svalbard, Norway. J. Comp. Physiol. B 2004, 174:157-162.
34. Goldberg A.L., Tischler M., DeMartino G., Griffin G. Hormonal regulation of protein degradation and synthesis in skeletal muscle. Fed. Proc. 1980, 39:31-36.
35. Goodman H.G., Grumbach M.M., Kaplan S.L. Growth and growth hormone - a comparison of isolated growth-hormone deficiency and multiple pituitary-hormone deficiencies in 35 patients with idiopathic hypopituitary dwarfism. N. Engl. J. Med. 1968, 278:57-68.
36. Goodman M.N., Larsen P.R., Kaplan M.M., Aoki T.T., Young V.R., Ruderman N.B. Starvation in the rat. II. Effect of age and obesity on protein sparing and fuel metabolism. Am. J. Physiol. 1980, 239:E277-E286.
37. Haley M.P., Deutsch C.J., Le Boeuf B.J. Size, dominance and copulatory success in male northern elephant seals, Mirounga angustirostris. Anim. Behav. 1994, 48:1249-1260.
38. Haulena M., St.Aubin D., Duignan P.J. Thyroid hormone dynamics during the nursing period in harbour seals, Phoca vitulina. Can. J. Zool. 1998, 76:48-55.
39. Hazelwood R.L. Pancreatic hormones, insulin/glucagon molar ratios, and somatostatin as determinants of avian carbohydrate metabolism. J. Exp. Zool. 1984, 232:647-652.
40. Henry C.J., Rivers J.P., Payne P.R. Protein and energy metabolism in starvation reconsidered. Eur. J. Clin. Nutr. 1988, 42:543-549.
41. Houser D.S., Costa D.P. Protein catabolism in suckling and fasting northern elephant seal pups, Mirounga angustirostris. J. Comp. Physiol. B 2001, 171:635-642.
42. Houser D.S., Champagne C.D., Crocker D.E. Lipolysis and glycerol gluconeogenesis in simultaneously fasting and lactating northern elephant seals. Am. J. Physiol. 2007, 293:R2376-R2381.
43. Iverson S.J., Bowen W.D., Boness D.J., Oftedal O.T. The effect of maternal size and milk energy output on pup growth in grey seals, Halichoerus grypus. Physiol. Zool. 1993, 66:61-88.
44. Kersten S. Mechanisms of nutritional and hormonal regulation of lipogenesis. EMBO Rep. 2001, 21:282-286.
45. Kirby V.L., Ortiz C.L. Hormones and fuel regulation in fasting elephant seals. Elephant Seals: Population Ecology, Behavior, and Physiology 1994, 374-386. University of California Press, Berkeley. B.J. Le Boeuf, R.M. Laws (Eds.).
46. Koea J.B., Doublas R.G., Breier B.H., Shaw J.H., Gluckman P.D. Synergistic effect of insulin-like growth factor-I administration on the protein-sparing effects of total parenteral nutrition in fasted lambs. Endocrinology 1992, 131:643-648.
47. Kojima M., Hosoda H., Date Y., Nakazato M., Matsuo H., Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1999, 402:656-660.
48. Kolaczynski J.W., Considine R.V., Ohannesian J., Marco C., Opentanova I., Nyce M.R., Myint M., Caro J.F. Responses of leptin to short-term fasting and refeeding in humans: a link with ketogenesis but not ketone themselves. Diabetes 1996, 45:1511-1515.
49. Korbonits M., Blaine D., Elia M., Powell-Tuck J. Metabolic and hormonal changes during the refeeding period of prlonged fasting. Eur. J. Endocrinol. 2007, 157:157-166.
50. Le Boeuf B.J. Male-male competition and reproductive success in elephant seals. Am. Zool. 1974, 14:163-176.
51. Lidgard D.C., Boness D.J., Bowen W.D., McMillan J.I. State-dependent male mating tactics in the grey seal: the importance of body size. Behav. Ecol. 2005, 16:541-549.
52. Mustonen A.-M., Saarela S., Pyykönen T., Nieminen P. Endocrinologic adaptations to wintertime fasting in the male American mink, Mustela vison. Exp. Biol. Med. 2005, 230:612-620.
53. Nakazato M., Murakami N., Date Y. A role for ghrelin in the central regulation of feeding. Nature 2001, 409:194-198.
54. Nieminen P., Asikainen J., Hyvärinen H. Effects of seasonality and fasting on the plasma leptin and thyroxin levels of the raccoon dog, Nyctereutes procyonoides and the blue fox, Alopex lagopus. J. Exp. Zool. 2001, 289:109-118.
55. Nieminen P., Mustonen A.-M., Asikainen J., Hyvärinen H. Seasonal weight regulation of the raccon dog, Nyctereutes procyonoides: interactions between melatonin, leptin, ghrelin and growth hormone. J. Biol. Rhythms 2002, 17:155-163.
56. Nordøy E.S., Blix A.S. Glucose and ketone body turnover in fasting grey seal pups. Acta Physiol. Scand. 1991, 141:563-571.
57. Norrelund H. The metabolic role of growth hormone in humans with particular reference to fasting. Growth Hor. IGF Res. 2005, 15:95-122.
58. Nørrelund H., Fisker S., Vahl N., Børglum J., Richelsen B.J.S., Christiansen J.S., Jørgensen J.O.L. Evidence supporting a direct suppressive effect of growth hormone on serum IGFBP-1 levels. Experimental studies in normal, obese and GH-deficient adults. Growth Horm. IGF Res. 1999, 9:52-60.
59. Ortiz C.L., Costa D., Le Boeuf B.J. Water and energy flux in elephant seal pups fasting under natural conditions. Physiol. Zool. 1978, 51:166-178.
60. Ortiz R.M., Crocker D.E., Houser D.S., Webb P.M. Angiotensin II and Aldosterone increase with fasting in breeding adult male northern elephant seals (Mirounga angustirostris). Physiol. Biochem. Zool. 2006, 79:1106-1112.
61. Ortiz R.M., Noren D.P., Litz B., Ortiz C.L. A new perspective on adiposity in a naturally obese mammal. Am. J. Physiol. 2001, 281:E1347-E1351.
62. Ortiz R.M., Wade C.E., Ortiz C.L. Effects of prolonged fasting on plasma cortisol and TH in postweaned northern elephant seal pups. Am. J. Physiol. 2001, 280:R790-R795.
63. Ortiz R.M., Houser D.S., Wade C.E., Ortiz C.L. Hormonal changes associated with the transition between nursing and natural fasting in northern elephant seals, Mirounga angustirostris. Gen. Comp. Endocrinol. 2003, 130:78-83.
64. Sakharova A.A., Horowitz J.F., Surya S., Goldenberg N., Harber M.P., Symons K., Barkan A. Role of growth hormone in regulating lipolysis, proteolysis, and hepatic glucose production during fasting. J. Clin. Endocrinol. Metab. 2008, 93:2755-2759.
65. Saltiel A.R., Kahn C.R. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001, 414:799-806.
66. Shintani M., Ogawa Y., Ebihara K., Aizawa-Abe M., Miyanaga F., Takaya K., Hayashi T., Inoue G., Hosoda K., Kojima M., et al. Ghrelin, an endogenous growth hormone secretagogue, is a novel orexigenic peptide that antagonizes leptin action through the activation of hypothalamic neuropeptide Y/Y1 receptor pathway. Diabetes 2001, 50:227-232.
67. Sormo E.G., Jussi I., Jussi M., Braathen M., Skaare J.U., Jenssen B.M. Thyroid hormone status in gray seal, Halichoerus grypus pups from the Baltic Sea and the Atlantic Ocean in relation to organochlorine pollutants. Virus Res. 2005, 108:83-87.
68. Spencer C.A., Lum S.M.C., Wilber J.F., Kaptein E.M., Nicoloff J.T. Dynamics of serum thyrotropin and thyroid hormone changes in fasting. J. Clin. Endocrinol. Metab. 1983, 56:883-888.
69. Stokkan K.A., Vaughan M.K., Beiter R.J., Folkow L.P., Martensson P.E., Sager G., Lydersen C., Blix A.S. Pineal and thyroid functions in newborn seals. Gen. Comp. Endocrinol. 1995, 98:321-331.
70. Straus D.S., Takemoto C.D. Effect of fasting on insulin-like growth factor-I (IGF-I) and growth hormone receptor mRNA levels and IGF-I gene transcription in rat liver. Mol. Endocrinol. 1990, 4:91-100.
71. Viscarra J., Champagne C.D., Crocker D.E., Ortiz R.M. 5-AMP-activated protein kinase activity is increased in adipose tissue of northern elephant seal pups during prolonged fasting-induced insulin resistance. J. Endocrinol. 2011, 209:317-325.
72. Viscarra J., Vazquez-Medina J.P., Crocker D.E., Ortiz R.M. Glut4 is upregulated despite decreased insulin signaling during prolonged fasting in northern elephant seal pups. Am. J. Physiol. 2011, 300:R1501-R.
73. Vuagnat B.A.M., Pierroz D.D., Lalaoui M., Englaro P., Pralong F.P., Blum W.F., Aubert M.L. Evidence for a leptin-neuropeptide Y axis for the regulation of growth hormone secretion in the rat. Neuroendocrinology 1998, 67:291-300.
74. Weigle D.S., Duell P.B., Connor W.E., Steiner R.A., Soules M.R., Kuijper J.L. Effect of fasting, refeeding, and dietary fat restriction on plasma leptin levels. J. Clin. Endocrinol. Metab. 1997, 82:561-565.
75. Williams G., Cai X.J., Elliott J.C., Harrold J.A. Anabolic neuropeptides. Physiol. Behav. 2004, 81:211-222.
76. Woldstad S., Jenssen B.M. Thyroid hormones in grey seal pups, Halichoerus grypus. Comp. Biochem. Physiol. A: Comp Physiol. 1999, 122:157-162.
77. Yochem P.K., Gulland F.M.D., Stewart B.S., Haulena M., Mazet J.A.K., Boyce W.M. Thyroid function testing in elephant seals in health and disease. Gen. Comp. Endocrinol. 2008, 155:627-632.
78. Yosefi S., Hen G., Rosenblum C.I., Cerasale D.J., Beauulieu M., Criscuolo F., Fridman-Einat M. Lack of leptin activity in blood samples of Adelie penguin and bar-tailed godwit. J. Endocrinol. 2010, 207:113-122.
79. Yu L., Jin W., Zhang X., Wang D., Zheng J., Tang G., Xu S., Cho S., Zhang Y. Evidence for positive selection on the leptin gene in cetacea and pinnipedia. PLoS One 2011, 6(10):e26579.