Sex differences in the neuroendocrine response to short-term fasting in rhesus macaques

Journal of Neuroendocrinology

Volumn 17, Issue 7, 2005, Pages 435-444

  Lado Abeal, J ^a,c   Robert McComb, J ^a   Qian, X P ^a   Leproult, R ^b   Van Cauter, E ^b   Norman, Reid L ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

Cortisol; Fasting; GH; LH; Primate; Reproduction

Indexed keywords

CORTICOTROPIN; GLUCOSE; GONADOTROPIN; GROWTH HORMONE; HYDROCORTISONE; LUTEINIZING HORMONE;

ANIMAL EXPERIMENT; ARTICLE; CALORIC RESTRICTION; CIRCADIAN RHYTHM; CONTROLLED STUDY; CORTICOTROPIN RELEASE; DIET RESTRICTION; FEMALE; FOOD INTAKE; GONADOTROPIN RELEASE; GROWTH HORMONE RELEASE; HORMONE RELEASE; LUTEINIZING HORMONE RELEASE; MACACA; MALE; MAMMAL; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; PULSATILE HORMONE RELEASE; SEX DIFFERENCE; TIME;

ANIMALS; BLOOD GLUCOSE; FASTING; FEMALE; FOLLICULAR PHASE; GROWTH HORMONE; HYDROCORTISONE; LUTEINIZING HORMONE; MACACA MULATTA; MALE; NEUROSECRETORY SYSTEMS; SEX CHARACTERISTICS;

EID: 21044443313     PISSN: 09538194     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2005.01323.x     Document Type: Article

References (61)

1. Schwartz MW, Seeley RJ. Neuroendocrine responses to starvation and weight loss. N Engl J Med 1997; 336: 1802-1811.
2. Cameron JL, Nobisch C. Suppression of pulsatile luteinizing hormone and testosterone secretion during short-term food restriction in the adult male rhesus monkey (Macaca mulatto) Endocrinology 1991; 128: 1532-1540.
3. Lado-Abeal J, Hickox JR, Cheung TL, Veldhuis JD, Hardy DM, Norman RL. Neuroendocrine consequences of fasting in adult male macaques: effects of recombinant rhesus macaque leptin infusion. Neuroendocrinology 2000; 71: 196-208.
4. Rojdmark S. Influence of short-term fasting on pituitary-testicular axis in normal men. Horm Res 1987; 25: 140-146.
5. Cameron JL, Weltzin TE, McConaha C, Helmreich DL, Kaye WH. Slowing of pulsatile luteinizing hormone secretion in men after forty-eight hours of fasting. J Clin Endocrinol Metab 1991; 73: 35-41.
6. Veldhuis JD, Iranmanesh A, Evans WS, Lizarralde G, Thorner MO, Vance ML. Amplitude suppression of the pulsatile mode of immunoradiometric luteinizing hormone release in fasting-induced hypoandrogenemia in normal men. J Clin Endocrinol Metab 1993; 76: 587-593.
7. Aloi JA, Bergendahl M, Iranmanesh A, Veldhuis JD. Pulsatile intravenous gonadotropin-releasing hormone administration averts fasting-induced hypogonadotropism and hypoandrogenemia in healthy, normal weight men. J Clin Endocrinol Metab 1997; 82: 1543-1548.
8. Williams NI, Lancas MJ, Cameron JL. Stimulation of luteinizing hormone secretion by food intake: evidence against a role for insulin. Endocrinology 1996; 137: 2565-2571.
9. Helmreich DL, Cameron JL. Suppression of luteinizing hormones secretion during food restriction in male rhesus monkeys (Macaca mulatta): failure of naloxone to restore normal pulsatility. Neuroendocrinol 1992; 56: 464-473.
10. Lado-Abeal J, Lukyanenko YO, Swamy S, Hermida RC, Hutson JC, Norman RL. Short-term leptin infusion does not affect circulating levels of LH, testosterone or cortisol in food-restricted pubertal male rhesus macaques. Clin Endocrinol 1999; 51: 41-51.
11. Schreihofer DA, Parfiit DB, Cameron JL. Suppression of luteinizing hormone secretion during short-term fasting in male rhesus monkeys: the role of metabolic versus stress signals. Endocrinology 1993; 132: 1881-1889.
12. Olster DH, Ferin M. Corticotropin-releasing hormone inhibits gonadotropin secretion in the ovariectomized rhesus monkey. J Clin Endocrinol Metab 1987; 65: 262-267.
13. Schreihofer DA, Amico JA, Cameron JL. Reversal of fasting-induced suppression of luteinizing hormone (LH) secretion in male rhesus monkeys by intragastric nutrient infusion: evidence for a rapid stimulation of LH by nutritional signals. Endocrinology 1993; 132: 1890-1897.
14. Lado Abeal J, Veldhuis JD, Norman RL. Glucose relays information regarding nutritional status to the neural circuits that control the somatotropic, corticotropic, and gonadotropic axes in adult male rhesus macaques. Endocrinology 2002; 143: 403-410.
15. Zubiran S, Gomez-Mont F. Endocrine disturbances in chronic human malnutrition. Vitam Horm 1953; 11: 97-132.
16. Van der Spuy ZM. Nutrition and reproduction. Clin Obstet Gynaecol 1985; 12: 579-604.
17. Warren MP. Effects of undernutrition on reproductive function in the human. Endocr Rev 1983; 4: 363-377.
18. Boyar RM, Katz J, Finkelstein JW, Kapen S, Weiner H, Weitzman ED, Hellman L. Anorexia nervosa. Immaturity of the 24-hour luteinizing hormone secretory pattern. N Engl J Med 1975; 291: 861-865.
19. Soules MR, Merriggiola MC, Steiner RA, Clifton DK, Toivola B, Bremner WJ. Short-term fasting in normal women: absence of effects on gonadotrophin secretion and the menstrual cycle. Clin Endocrinol 1994; 40: 725-731.
20. Berga SL, Tammy LL, Cameron JL. Endocrine and chronobiological effects of fasting in women. Fert Steril 2001; 75: 926-932.
21. Cagampang FRA, Maeda K-I, Yokoyama A, Ota K. Effect of food deprivation on the pulsatile LH release in the cycling and ovariectomized female rat. Horm Res 1990; 22: 269-272.
22. Wade GN, Schneider JE, Li H-Y. Control of fertility by metabolic cues. Am J Physiol Endocrinol Metab 1996; 270: E1-E19.
23. Ho KY, Evans WS, Blizzard RM, Veldhuis JD, Merriam GR, Samojlik E, Furlanetto R, Rogol AD, Kaiser DL, Thorner MO. Effects of sex and age on the 24-h profile of growth hormone secretion in man: importance of exogenous estradiol concentrations. J Clin Endocrinol Metab 1987; 64: 51-58.
24. Weltman A, Weltman JY, Hartman ML, Abbott RD, Rogol AD, Evans WS, Veldhuis JD. Relationship between age, percentage of body fat, fitness and 24-h growth hormone release in healthy young adults: effect of gender. J Clin Endocrinol Metab 1994; 78: 543-548.
25. Bray MJ, Vick TM, Shah N, Anderson SM, Rice LW, Iranmanesh A, Evans WS, Veldhuis JD. Short-term estradiol replacement in postmenopausal women selectively mutes somatostatin's dose-dependent inhibition of fasting growth hormone secretion. J Clin Endocrinol Metab 2001; 86: 3143-3149.
26. Ho KY, Veldhuis JD, Johnson ML, Furlanetto R, Evans WS, Alberti KG, Thorner MO. Fasting enhances growth hormone secretion and amplifies the complex rhythms of growth hormone secretion in man. J Clin Invest 1988; 81: 968-975.
27. Norrelund H, Nair KS, Jorgensen JO, Christiansen JS, Moller N. The protein-retaining effects of growth hormone during fasting involve inhibition of muscle-protein breakdown. Diabetes 2001; 50: 96-104.
28. Maccario M, Aimaretti G, Corneli G, Gauna C, Grottoli S, Bidlingmaier M, Strasburger CJ, Dieguez C, Casanueva FF, Ghigo E. Short-term fasting abolishes the sex-related difference in GH and leptin secretion in humans. Am J Physiol Endocrinol Metab 2000; 279: E411-E416.
29. Hojlund K, Wildner-Christensen M, Eshoj O, Skjaerbaek C, Holst JJ, Koldkjaer O, Moller Jensen D, Beck-Nielsen H. Reference intervals for glucose, beta-cell polypeptides, and counterregulatory factors during prolonged fasting. Am J Physiol Endocrinol Metab 2001; 280: E50-E58.
30. Hartman ML, Veldhuis JD, Johnson ML, Lee MM, Alberti KG, Samojlik E, Thorner MO. Augmented growth hormone (GH) secretory burst frequency and amplitude mediate enhanced GH secretion during a two-day fast in normal men. J Clin Endocrinol Metab 1992; 74: 757-765.
31. Giustina A, Veldhuis JD. Pathophysiology of the neuroregulation of growth hormone secretion in experimental animals and the human. Endocr Rev 1998; 19: 717-797.
32. Horrocks PM, Jones AF, Ratcliffe WA, Holder G, White A, Holder R, Ratcliffe JG, London DR. Patterns of ACTH and cortisol pulsatility over twenty-four hours in normal males and females. Clin Endocrinol (Oxf) 1990; 32: 127-134.
33. Van Cauter E, Leproult R, Kupfer DJ. Effects of gender and age on the levels and circadian rhythmicity of plasma cortisol. J Clin Endocrinol Metab 1996; 81: 2468-2473.
34. Bergendahl M, Vance ML, Iranmanesh A, Thorner MO, Veldhuis JD. 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 Endocrinol Metab 1996; 81: 692-699.
35. Bergendahl M, Iranmanesh A, Pastor C, Evans WS, Veldhuis JD. Homeostatic joint amplification of pulsatile and 24-hour rhythmic cortisol secretion by fasting stress in midluteal phase women. concurrent disruption of cortisol-growth hormone, cortisol luteinizing hormone, and cortisol-leptin synchrony. J Clin Endocrinol Metab 2000; 85: 4028-4035.
36. Smith CJ, Norman RL. Circadian periodicity in circulating cortisol is absent after orchidectomy in rhesus macaques. Endocrinology 1987; 121: 2186-2191.
37. Smith CJ, Norman RL. Influence of the gonads on cortisol secretion in female rhesus macaques. Endocrinology 1987; 121: 2192-2198.
38. Norman RL, Lindstrom SA, Bangsberg D, Ellinwood WE, Gliessman P, Spies HG. Pulsatile secretion of luteinizing hormone during the menstrual cycle of rhesus macaques. Endocrinology 1984; 115: 261-266.
39. Ellinwood WE, Norman RL, Spies HG. Changing frequency of pulsatile luteinizing hormone and progesterone secretion during the luteal phase of the menstrual cycle of rhesus macaques. Biol Reprod 1984; 31: 714-722.
40. Van Cauter E. Estimating false-positive and false-negative errors in analyses of hormonal pulsatility. Am J Physiol Endocrinol Metab 1991; 254: E786-E794.
41. Van Cauter E, Kerkhofs M, Caufriez A, Van Onderbergen A, Thorner MO, Copinschi G. A quantitative estimation of GH secretion in normal man: reproducibility and relation to sleep and time of day. J Clin Endocrinol Metab 1992; 74: 1441-1450.
42. Refetoff S, Sonksen PH. Disappearance rate of endogenous and exogenous human growth hormone in man. J Clin Endocrinol Metab 1970; 30: 386-392.
43. Van Cauter E, Mestrez F, Sturis J, Polonsky DS. Estimation of insulin secretion rates from C-peptide levels. Comparison of individual and standard kinetic parameters for C-peptide clearance. Diabetes 1992; 41: 368-377.
44. Feng YJ, Shalts E, Xia LN, Rivier J, Rivier C, Vale W, Ferin M. An inhibitory effect of interleukin-1α on basal gonadotropin release in the ovariectomized rhesus monkey: reversal by a corticotropin-releasing factor antagonist. Endocrinology 1991; 128: 2077-2082.
45. Xiao E, Xia L, Shanen D, Khabele D, Ferin M. Stimulatory effects of interleukin-induced activation of the hypothalamo-pituitary-adrenal axis on gonadotropin secretion in ovariectomized monkeys replaced with estradiol. Endocrinology 1994; 135: 2093-2098.
46. Xiao E, Xia-Zhang L, Thornell D, Ferin M. Interleukin-1 stimulates luteinizing hormone release during the midfollicular phase in the rhesus monkey: a novel way in which stress may influence the menstrual cycle. J Clin Endocrinol Metab 1996; 81: 2136-2141.
47. Maeda K, Nagatani S, Estacio MA, Tsukamura H. Novel estrogen feedback sites associated with stress-induced suppression of luteinizing hormone secretion in female rats. Cell Mol Neurobiol 1996; 16: 311-324.
48. Cagampang FR, Maeda K, Yokoyama A, Ota K. Effect of food deprivation on the pulsatile LH release in the cycling and ovariectomized female rat. Horm Metab Res 1990; 22: 269-272.
49. Cahill GF Jr, Herrera MG, Morgan AP, Soeldner JS, Steinke J, Levy PL, Reichard GA Jr, Kipnis DM. Hormone-fuel interrelationships during fasting. J Clin Invest 1966; 45: 1751-1769.
50. Owen OE, Morgan AP, Kemp HG, Sullivan JM, Herrera MG, Cahill GF Jr. Brain metabolism during fasting. J Clin Invest 1967; 46: 1589-1595.
51. Carlson MG, Snead WL, Campbell PJ. Fuel and energy metabolism in fasting humans. Am J Clin Nutr 1994; 60: 29-36.
52. Merimee TJ, Misbin RI, Pulkkinen AJ. Sex variations in free fatty acids and ketones during fasting: evidence for a role of glucagon. J Clin Endocrinol Metab 1978; 46: 414-419.
53. Suryanarayana BV, Kent JR, Meister L, Parlow AF. Pituitary-gonadal axis during prolonged total starvation in obese men. Am J Clin Nutr 1969; 22: 767-770.
54. Klibanski A, Beitins IZ, Badger T, Little R, McArthur JW. Reproductive function during fasting in men. J Clin Endocrinol Metab 1981; 53: 258-263.
55. Drezgic M, Penezic Z, Zarkovic M, Vujovic S, Ciric J, Trbojevic B, Bogdanovic AD, Nesovic M. Influence of three-week fasting on gonadotropin pulsatility in obese menstruating women. Int J Obes Relat Metab Disord 1996; 20: 608-612.
56. Alvero R, Kimzey L, Sebring N, Reynolds J, Loughran M, Nieman L, Olson BR. Effects of fasting on neuroendocrine function and follicle development in lean women. J Clin Endocrinol Metab 1998; 83: 76-80.
57. Bradbury MJ, McBurnie MI, Denton DA, Lee KF, Vale WW. Modulation of urocortin-induced hypophagia and weight loss by corticotropin-releasing factor receptor 1 deficiency in mice. Endocrinology 2000; 141: 2715-2724.
58. Ferin M. Clinical review 105: stress and the reproductive cycle. J Clin Endocrinol Metab 1999; 84: 1768-1774.
59. Jeong KH, Jacobson L, Widmaier EP, Majzoub JA. Normal suppression of the reproductive axis following stress in corticotropin-releasing hormone-deficient mice. Endocrinology 1999; 140: 1702-1708.
60. Laugero KD, Bell ME, Bhatnagar S, Soriano L, Dallman MF. Sucrose ingestion normalizes central expression of corticotropin-releasing-factor messenger ribonucleic acid and energy balance in adrenalectomized rats: a glucocorticoid-metabolic-brain axis. Endocrinology 2001; 142: 2796-2804.
61. Bronson FH. Puberty and energy balance. A walk on the wild side; . In: Wallen K, Schneider JE, eds. Reproduction in Context: Social and Environmental Influences on Reproduction. Cambridge, MA: MIT Press, 2000: 15-33.