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Horm Metab Res 2014; 46(03): 187-192
DOI: 10.1055/s-0033-1363263
Endocrine Research
© Georg Thieme Verlag KG Stuttgart · New York

Primate HPT Axis Response to the Peripheral Kisspeptin Challenge Under Different Time Periods of Food Restriction in Monkeys

F. Wahab
1   Laboratory of Reproductive Neuroendocrinology, Department of Animal Sciences, Faculty of Biological Sciences, Quaid-i-Azam University, 45320 Islamabad, Pakistan
2   Department of Physiology, Institute of Basic Medical Sciences, Khyber Medical University, Peshawar, KPK, Pakistan
,
B. Atika
1   Laboratory of Reproductive Neuroendocrinology, Department of Animal Sciences, Faculty of Biological Sciences, Quaid-i-Azam University, 45320 Islamabad, Pakistan
,
T. Huma
1   Laboratory of Reproductive Neuroendocrinology, Department of Animal Sciences, Faculty of Biological Sciences, Quaid-i-Azam University, 45320 Islamabad, Pakistan
,
M. Shahab
1   Laboratory of Reproductive Neuroendocrinology, Department of Animal Sciences, Faculty of Biological Sciences, Quaid-i-Azam University, 45320 Islamabad, Pakistan
› Author Affiliations
Further Information

Publication History

received 21 June 2013

accepted 28 November 2013

Publication Date:
05 February 2014 (online)

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Abstract

Metabolism and reproduction are closely linked. Both long- and short-term fasting-induced metabolic deficiency suppresses reproductive function in mammals. Recently, we have shown that 48-h fasting-induced metabolic deficiency attenuates the reproductive axis responsiveness to peripheral kisspeptin injection in the sexually mature monkeys. But currently there is no data to show whether shorter time periods of fasting also alter the reproductive axis responsiveness to kisspeptin. Therefore, this study was aimed to examine the reproductive axis responsiveness to kisspeptin administration in the adult male rhesus monkey fasted for 12-, 18-, and 24h. Intravenous boli of vehicle (1ml) and human kisspeptin-10 (KP10; 50μg) were given to 5 intact sexually mature male rhesus monkeys in both fasting (12-, 18-, 24-h) and ad libitum feeding conditions. Specific immunoassays were used to determine plasma hormones concentrations. KP10 injection highly stimulated testosterone secretion in all conditions. However, mean testosterone concentrations in 3-h post-KP10 injection period were significantly (p<0.01) decreased in 18- and 24-h fasted monkeys when compared to 12-h fasted and fed monkeys. Moreover, 18- and 24-h fasting conditions also significantly (p<0.05) delayed the duration to the first significant increase in T levels after KP10 injection. Vehicle injection did not alter these parameters in any conditions. Present results indicate that 18- and 24-h fasting conditions suppressed the testosterone response to KP10 administration both in initiation and quantity. These results suggest that 18- and 24-h fasting-induced inhibition of the reproductive functions in the mature male macaque may partly involve attenuation in the reproductive axis responsiveness to endogenous kisspeptin stimulation.

Key words

fasting - HPT axis - GnRH - Kiss1 - Kiss1r - testosterone - monkey
 

  • References

  • 1 Schneider JE. Energy balance and reproduction. Physiol Behav 2004; 81: 289-317
    CrossrefPubMedGoogle Scholar
  • 2 Evans JJ, Anderson GM. Balancing ovulation and anovulation: integration of the reproductive and energy balance axes by neuropeptides. Hum Reprod Update 2012; 18: 313-332
    CrossrefPubMedGoogle Scholar
  • 3 Wade GN, Jones JE. Neuroendocrinology of nutritional infertility. Am J Physiol Regul Integr Comp Physiol 2004; 287: R1277-R1296
    CrossrefPubMedGoogle Scholar
  • 4 Wahab F, Atika B, Shahab M. Kisspeptin as a link between metabolism and reproduction: Evidences from rodent and primate studies. Metabolism 2013; 62: 898-910
    CrossrefPubMedGoogle Scholar
  • 5 Kumar S, Kaur G. Intermittent fasting dietary restriction regimen negatively influences reproduction in young rats: a study of hypothalamo-hypophysial-gonadal axis. Plos One 2013; 8: e52416
    CrossrefPubMedGoogle Scholar
  • 6 Wahab F, Aziz F, Irfan S, Zaman W-U, Shahab M. Short-term fasting attenuates the response of the HPG axis to kisspeptin challenge in the adult male rhesus monkey (Macaca mulatta). Life Sci 2008; 83: 633-637
    CrossrefPubMedGoogle Scholar
  • 7 Wahab F, Zaman W, Shahab M. Differential response of the primate HPG axis to N-methyl-D, L-aspartate, but not to Kisspeptin challenge under euglycemic and hypoglycemic conditions. Horm Metab Res 2012; 44: 451-457
    Article in Thieme ConnectPubMedGoogle Scholar
  • 8 Lado-Abeal J, Clapper JA, Chen Zhu B, Hough CM, Syapin PJ, Norman RL. Hypoglycemia-induced suppression of luteinizing hormone (LH) secretion in intact female rhesus macaques: role of vasopressin and endogenous opioids. Stress Amst Neth 2002; 5: 113-119
    PubMedGoogle Scholar
  • 9 Sexton WJ, Jarow JP. Effect of diabetes mellitus upon male reproductive function. Urology 1997; 49: 508-513
    CrossrefPubMedGoogle Scholar
  • 10 Lado-Abeal J, Robert-McComb JJ, Qian X-P, Leproult R, Van Cauter E, Norman RL. Sex differences in the neuroendocrine response to short-term fasting in rhesus macaques. J Neuroendocrinol 2005; 17: 435-444
    CrossrefPubMedGoogle Scholar
  • 11 Gill CJ, Rissman EF. Female sexual behavior is inhibited by short- and long-term food restriction. Physiol Behav 1997; 61: 387-394
    CrossrefPubMedGoogle Scholar
  • 12 Cameron JL. Regulation of reproductive hormone secretion in primates by short-term changes in nutrition. Rev Reprod 1996; 1: 117-126
    CrossrefPubMedGoogle Scholar
  • 13 Cameron JL, Helmreich DL, Schreihofer DA. Modulation of reproductive hormone secretion by nutritional intake: stress signals versus metabolic signals. Hum Reprod Oxf Engl 1993; 8 (Suppl. 02) 162-167
    PubMedGoogle Scholar
  • 14 Cameron JL, Nosbisch C. Suppression of pulsatile luteinizing hormone and testosterone secretion during short term food restriction in the adult male rhesus monkey (Macaca mulatta). Endocrinology 1991; 128: 1532-1540
    CrossrefPubMedGoogle Scholar
  • 15 Bergendahl M, Perheentupa A, Huhtaniemi I. Starvation-induced suppression of pituitary-testicular function in rats is reversed by pulsatile gonadotropin-releasing hormone substitution. Biol Reprod 1991; 44: 413-419
    CrossrefPubMedGoogle Scholar
  • 16 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
    CrossrefPubMedGoogle Scholar
  • 17 Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena-Sempere M. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev 2012; 92: 1235-1316
    CrossrefPubMedGoogle Scholar
  • 18 Han S-K, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci Off J Soc Neurosci 2005; 25: 11349-11356
    CrossrefPubMedGoogle Scholar
  • 19 Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci USA 2005; 102: 2129-2134
    CrossrefPubMedGoogle Scholar
  • 20 Terasawa E, Guerriero KA, Plant TM. Kisspeptin and puberty in mammals. Adv Exp Med Biol 2013; 784: 253-273
    PubMedGoogle Scholar
  • 21 Elizur A. The KiSS1/GPR54 system in fish. Peptides 2009; 30: 164-170
    CrossrefPubMedGoogle Scholar
  • 22 Tena-Sempere M, Felip A, Gómez A, Zanuy S, Carrillo M. Comparative insights of the kisspeptin/kisspeptin receptor system: lessons from non-mammalian vertebrates. Gen Comp Endocrinol 2012; 175: 234-243
    CrossrefPubMedGoogle Scholar
  • 23 Castellano JM, Tena-Sempere M. Metabolic regulation of kisspeptin. Adv Exp Med Biol 2013; 784: 363-383
    PubMedGoogle Scholar
  • 24 Wahab F, Ullah F, Chan Y-M, Seminara SB, Shahab M. Decrease in hypothalamic Kiss1 and Kiss1r expression: a potential mechanism for fasting-induced suppression of the HPG axis in the adult male rhesus monkey (Macaca mulatta). Horm Metab Res 2011; 43: 81-85
    Article in Thieme ConnectPubMedGoogle Scholar
  • 25 Wahab F, Salahuddin H, Anees M, Leprince J, Vaudry H, Tena-Sempere M, Shahab M. Study of the effect of 26RF- and 43RF-amides on testosterone and prolactin secretion in the adult male rhesus monkey (Macaca mulatta). Peptides 2012; 36: 23-28
    CrossrefPubMedGoogle Scholar
  • 26 Wahab F, Zaman W, Shahab M. Differential response of the primate HPG axis to N-methyl-D, L-aspartate, but not to Kisspeptin challenge under euglycemic and hypoglycemic conditions. Horm Metab Res 2012; 44: 451-457
    Article in Thieme ConnectPubMedGoogle Scholar
  • 27 Wahab F, Bano R, Jabeen S, Irfan S, Shahab M. Effect of peripheral kisspeptin administration on adiponectin, leptin, and resistin secretion under fed and fasting conditions in the adult male rhesus monkey (Macaca mulatta). Horm Metab Res Horm 2010; 42: 570-574
    PubMedGoogle Scholar
  • 28 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
    CrossrefPubMedGoogle Scholar
  • 29 Shahab M, Zaman W, Bashir K, Arslan M. Fasting-induced suppression of hypothalamic-pituitary-gonadal axis in the adult rhesus monkey: evidence for involvement of excitatory amino acid neurotransmitters. Life Sci 1997; 61: 1293-1300
    CrossrefPubMedGoogle Scholar
  • 30 Castellano JM, Navarro VM, Fernández-Fernández R, Nogueiras R, Tovar S, Roa J, Vazquez MJ, Vigo E, Casanueva FF, Aguilar E, Pinilla L, Dieguez C, Tena-Sempere M. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology 2005; 146: 3917-3925
    CrossrefPubMedGoogle Scholar
  • 31 Castellano JM, Navarro VM, Fernández-Fernández R, Roa J, Vigo E, Pineda R, Dieguez C, Aguilar E, Pinilla L, Tena-Sempere M. Expression of hypothalamic KiSS-1 system and rescue of defective gonadotropic responses by kisspeptin in streptozotocin-induced diabetic male rats. Diabetes 2006; 55: 2602-2610
    CrossrefPubMedGoogle Scholar
  • 32 Luque RM, Kineman RD, Tena-Sempere M. Regulation of hypothalamic expression of KiSS-1 and GPR54 genes by metabolic factors: analyses using mouse models and a cell line. Endocrinology 2007; 148: 4601-4611
    CrossrefPubMedGoogle Scholar
  • 33 Yamada S, Uenoyama Y, Kinoshita M, Iwata K, Takase K, Matsui H, Adachi S, Inoue K, Maeda KI, Tsukamura H. Inhibition of metastin (kisspeptin-54)-GPR54 signaling in the arcuate nucleus-median eminence region during lactation in rats. Endocrinology 2007; 148: 2226-2232
    CrossrefPubMedGoogle Scholar
  • 34 Chan Y-M. Effects of kisspeptin on hormone secretion in humans. Adv Exp Med Biol 2013; 784: 89-112
    PubMedGoogle Scholar
  • 35 Abbara A, Ratnasabapathy R, Jayasena CN, Dhillo WS. The Effects of Kisspeptin on Gonadotropin Release in Non-human Mammals. Adv Exp Med Biol 2013; 784: 63-87
    PubMedGoogle Scholar
  • 36 Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004; 145: 4073-4077
    CrossrefPubMedGoogle Scholar
  • 37 Navarro VM, Castellano JM, Fernández-Fernández R, Tovar S, Roa J, Mayen A, Nogueiras R, Vazquez MJ, Barreiro ML, Magni P, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 2005; 146: 156-163
    CrossrefPubMedGoogle Scholar
  • 38 Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2004; 80: 264-272
    CrossrefPubMedGoogle Scholar
  • 39 Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 2005; 102: 1761-1766
    CrossrefPubMedGoogle Scholar
  • 40 Patterson M, Murphy KG, Thompson EL, Patel S, Ghatei MA, Bloom SR. Administration of kisspeptin-54 into discrete regions of the hypothalamus potently increases plasma luteinising hormone and testosterone in male adult rats. J Neuroendocrinol 2006; 18: 349-354
    CrossrefPubMedGoogle Scholar
  • 41 Grachev P, Li XF, O’Byrne K. Stress regulation of kisspeptin in the modulation of reproductive function. Adv Exp Med Biol 2013; 784: 431-454
    PubMedGoogle Scholar
  • 42 Wang O. Glucocorticoids Regulate Kisspeptin Neurons during Stress and Contribute to Infertility and Obesity in Leptin-Deficient Mice. 2012 http://nrs.harvard.edu/urn-3:HUL.InstRepos:9453704
    PubMedGoogle Scholar
  • 43 Kinoshita M, Moriyama R, Tsukamura H, Maeda K-I. A rat model for the energetic regulation of gonadotropin secretion: role of the glucose-sensing mechanism in the brain. Domest Anim Endocrinol 2003; 25: 109-120
    CrossrefPubMedGoogle Scholar
  • 44 Lado-Abeal J, Norman RL. Leptin and reproductive function in males. Semin Reprod Med 2002; 20: 145-151
    Article in Thieme ConnectPubMedGoogle Scholar
  • 45 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
    CrossrefPubMedGoogle Scholar
  • 46 Scheid JL, De Souza MJ, Hill BR, Leidy HJ, Williams NI. Decreased luteinizing hormone pulse frequency is associated with elevated 24-hour ghrelin after calorie restriction and exercise in premenopausal women. Am J Physiol Endocrinol Metab 2013; 304: E109-E116
    CrossrefPubMedGoogle Scholar