Central lipoprivation-induced suppression of luteinizing hormone pulses is mediated by paraventricular catecholaminergic inputs in female rats

Endocrinology

Volumn 149, Issue 6, 2008, Pages 3016-3024

  Sajapitak, Somchai ^a   Iwata, Kinuyo ^a   Shahab, Mohammad ^a   Uenoyama, Yoshihisa ^a   Yamada, Shunji ^a   Kinoshita, Mika ^a   Bari, Farida Y ^a   I'Anson, Helen ^b   Tsukamura, Hiroko ^a   Maeda, Kei Ichiro ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b WASHINGTON AND LEE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; LUTEINIZING HORMONE; METIROSINE; THIOGLYCOLIC ACID; TRIMETAZIDINE;

ANIMAL EXPERIMENT; ARTICLE; CATECHOLAMINE SYNTHESIS; CATECHOLAMINERGIC SYSTEM; CONTROLLED STUDY; FATTY ACID OXIDATION; FEMALE; GLUCOSE BLOOD LEVEL; MICRODIALYSIS; NONHUMAN; NORADRENALIN RELEASE; OVARIECTOMY; PRIORITY JOURNAL; PULSATILE HORMONE RELEASE; RAT; THALAMUS MIDLINE NUCLEUS;

ANIMALS; CATECHOLAMINES; ESTRADIOL; FEMALE; KINETICS; LIPIDS; LUTEINIZING HORMONE; OVARIECTOMY; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS; RATS, WISTAR; THIOGLYCOLATES; TRIMETAZIDINE;

EID: 44249092535     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0016     Document Type: Article

References (53)

1. Bronson FH 1986 Food-restricted, prepubertal, female rats: rapid recovery of luteinizing hormone pulsing with excess food, and full recovery of pubertal development with gonadotropin-releasing hormone. Endocrinology 118:2483-2487
2. Matsuyama S, Ohkura S, Ichimaru T, Sakurai K, Tsukamura H, Maeda K, Okamura H 2004 Simultaneous observation of the GnRH pulse generator activity and plasma concentrations of metabolites and insulin during fasting and subsequent refeeding periods in Shiba goats. J Reprod Dev 50:697-704
3. Messer NA, I'Anson H 2000 The nature of the metabolic signal that triggers onset of puberty in female rats. Physiol Behav 68:377-382
4. Schneider JE 2004 Energy balance and reproduction. Physiol Behav 81:289-317
5. Tsukamura H, Maeda K-I 2001 Non-metabolic and metabolic factors causing the lactational anestrus: rat models uncovering the neuroendocrine mechanism underlying the suckling-induced changes in the mother. In: Russell JA, Douglas AJ, Windle RJ, Ingram CD, eds. The maternal brain, progress in brain research. Amsterdam: Elsevier; 187-205
6. Wade GN, Jones JE 2004 Neuroendocrinology of nutritional infertility. Am J Physiol Regul Integr Comp Physiol 287:R1277-R1296
7. Wade GN, Schneider JE, Li HY 1996 Control of fertility by metabolic cues. Am J Physiol 270(1 Pt 1):E1-E19
8. Leonhardt S, Shahab M, Luft H, Wuttke W, Jarry H 1999 Reduction of luteinizing hormone secretion induced by long-term feed restriction in male rats is associated with increased expression of GABA-synthesizing enzymes without alterations of GnRH gene expression. J Neuroendocrinol 11:613-619
9. Cagampang FR, Maeda K, Yokoyama A, Ota K 1990 Effect of food deprivation on the pulsatile LH release in the cycling and ovariectomized female rat. Horm Metab Res 22:269-272
10. Maeda K, Tsukamura H 1996 Neuroendocrine mechanism mediating fasting-induced suppression of luteinizing hormone secretion in female rats. Acta Neurobiol Exp (Wars) 56:787-796
11. Cates PS, O'Byrne KT 2000 The area postrema mediates insulin hypoglycaemia-induced suppression of pulsatile LH secretion in the female rat. Brain Res 853:151-155
12. Nagatani S, Bucholtz DC, Murahashi K, Estacio MA, Tsukamura H, Foster DL, Maeda KI 1996 Reduction of glucose availability suppresses pulsatile luteinizing hormone release in female and male rats. Endocrinology 137:1166-1170
13. Schneider JE, Wade GN 1989 Availability of metabolic fuels controls estrous cyclicity of Syrian hamsters. Science 244:1326-1328
14. Levin BE, Routh VH, Kang L, Sanders NM, Dunn-Meynell AA 2004 Neuronal glucosensing: what do we know after 50 years? Diabetes 53:2521-2528
15. Moriyama R, Tsukamura H, Kinoshita M, Okazaki H, Kato Y, Maeda K 2004 In vitro increase in intracellular calcium concentrations induced by low or high extracellular glucose levels in ependymocytes and serotonergic neurons of the rat lower brainstem. Endocrinology 145:2507-2515
16. Ritter S, Calingasan N, Hutton B, Dinh T 1992 Cooperation of vagal and central neural systems in monitoring metabolic events controlling feedback behavior. In: Ritter S, Ritter R, Barnes C, eds. Neuroanatomy and physiology of abdominal vagal afferents. Boca Raton, FL: CRC Press; 249-277
17. Schneider JE, Zhu Y 1994 Caudal brain stem plays a role in metabolic control of estrous cycles in Syrian hamsters. Brain Res 661:70-74
18. Murahashi K, Bucholtz DC, Nagatani S, Tsukahara S, Tsukamura H, Foster DL, Maeda KI 1996 Suppression of luteinizing hormone pulses by restriction of glucose availability is mediated by sensors in the brain stem. Endocrinology 137:1171-1176
19. Nagatani S, Tsukamura H, Murahashi K, Bucholtz DC, Foster DL, Maeda K 1996 Paraventricular norepinephrine release mediates glucoprivic suppression of pulsatile luteinizing hormone secretion. Endocrinology 137:3183-3186
20. Sindelar DK, Ste Marie L, Miura GI, Palmiter RD, McMinn JE, Morton GJ, Schwartz MW 2004 Neuropeptide Y is required for hyperphagic feeding in response to neuroglucopenia. Endocrinology 145:3363-3368
21. Shahab M, Sajapitak S, Tsukamura H, Kinoshita M, Matsuyama S, Ohkura S, Yamada S, Uenoyama Y, I'Anson H, Maeda K 2006 Acute lipoprivation suppresses pulsatile luteinizing hormone secretion without affecting food intake in female rats. J Reprod Dev 52:763:772
22. Cagampang FR, Maeda KI, Tsukamura H, Ohkura S, Ota K 1991 Involvement of ovarian steroids and endogenous opioids in the fasting-induced suppression of pulsatile LH release in ovariectomized rats. J Endocrinol 129:321-328
23. Bauche F, Sabourault D, Giudicelli Y, Nordmann J, Nordmann R 1981 2-Mercaptoacetate administration depresses the β-oxidation pathway through an inhibition of long-chain acyl-CoA dehydrogenase activity. Biochem J 196:803-809
24. Bauche F, Sabourault D, Giudicelli Y, Nordmann J, Nordmann R 1983 Inhibition in vitro of acyl-CoA dehydrogenases by 2-mercaptoacetate in rat liver mitochondria. Biochem J 215:457-464
25. Maeda K, Nagatani S, Estacio MA, Tsukamura H 1996 Novel estrogen feedback sites associated with stress-induced suppression of luteinizing hormone secretion in female rats. Cell Mol Neurobiol 16:311-324
26. Maeda K, Cagampang FR, Coen CW, Tsukamura H 1994 Involvement of the catecholaminergic input to the paraventricular nucleus and of corticotropin-releasing hormone in the fasting-induced suppression of luteinizing hormone release in female rats. Endocrinology 134:1718-1722
27. Merriam GR, Wachter KW 1982 Algorithms for the study of episodic hormone secretion. Am J Physiol 243:E310-E318
28. Maeda KI, Tsukamura H, Uchida E, Ohkura N, Ohkura S, Yokoyama A 1989 Changes in the pulsatile secretion of LH after the removal of and subsequent resuckling by pups in ovariectomized lactating rats. J Endocrinol 121:277-283
29. Kantor PF, Lucien A, Kozak R, Lopaschuk GD 2000 The antianginal drug trimetazidine shifts cardiac energy metabolism from fatty acid oxidation to glucose oxidation by inhibiting mitochondrial long-chain 3-ketoacyl coenzyme A thiolase. Circ Res 86:580-588
30. Li HY, Wade GN, Blaustein JD 1994 Manipulations of metabolic fuel availability alter estrous behavior and neural estrogen receptor immunoreactivity in Syrian hamsters. Endocrinology 135:240-247
31. Schneider JE, Hall AJ, Wade GN 1997 Central vs. peripheral metabolic control of estrous cycles in Syrian hamsters. I. Lipoprivation. Am J Physiol 272(1 Pt 2):R400-R405
32. Ritter RC, Slusser PG, Stone S 1981 Glucoreceptors controlling feeding and blood glucose: location in the hindbrain. Science 213:451-452
33. Maekawa F, Toyoda Y, Torii N, Miwa I, Thompson RC, Foster DL, Tsukahara S, Tsukamura H, Maeda K 2000 Localization of glucokinase-like immunoreactivity in the rat lower brain stem: for possible location of brain glucose-sensing mechanisms. Endocrinology 141:375-384
34. Kinoshita M, I'Anson H, Tsukamura H, Maeda K 2004 Fourth ventricular alloxan injection suppresses pulsatile luteinizing hormone release in female rats. J Reprod Dev 50:279-285
35. Fraley GS, Dinh TT, Ritter S 2002 Immunotoxic catecholamine lesions attenuate 2DG-induced increase of AGRP mRNA. Peptides 23:1093-1099
36. Fraley GS, Ritter S 2003 Immunolesion of norepinephrine and epinephrine afferents to medial hypothalamus alters basal and 2-deoxy-D-glucose-induced neuropeptide Y and agouti gene-related protein messenger ribonucleic acid expression in the arcuate nucleus. Endocrinology 144:75-83
37. Ritter S, Bugarith K, Dinh TT 2001 Immunotoxic destruction of distinct catecholamine subgroups produces selective impairment of glucoregulatory responses and neuronal activation. J Comp Neurol 432:197-216
38. Ritter S, Watts AG, Dinh TT, Sanchez-Watts G, Pedrow C 2003 Immunotoxin lesion of hypothalamically projecting norepinephrine and epinephrine neurons differentially affects circadian and stressor-stimulated corticosterone secretion. Endocrinology 144:1357-1367
39. Ritter S, Dinh TT 1994 2-Mercaptoacetate and 2-deoxy-D-glucose induce Fos-like immunoreactivity in rat brain. Brain Res 641:111-120
40. Cagampang FR, Ohkura S, Tsukamura H, Coen CW, Ota K, Maeda K 1992 α2-Adrenergic receptors are involved in the suppression of luteinizing hormone release during acute fasting in the ovariectomized estradiol-primed rats. Neuroendocrinology 56:724-728
41. Estacio MA, Tsukamura H, Reyes BA, Uenoyama Y, I'Anson H, Maeda K 2004 Involvement of brainstem catecholaminergic inputs to the hypothalamic paraventricular nucleus in estrogen receptor α expression in this nucleus during different stress conditions in female rats. Endocrinology 145:4917-4926
42. I'Anson H, Sundling LA, Roland SM, Ritter S 2003 Immunotoxic destruction of distinct catecholaminergic neuron populations disrupts the reproductive response to glucoprivation in female rats. Endocrinology 144:4325-4331
43. Yoshihara T, Honma S, Honma K 1996 Prefeeding release of paraventricular neuropeptide Y is mediated by ascending noradrenergic neurons in rats. Am J Physiol 270(4 Pt 1):E596-E600
44. Pavia JM, Hastings JA, Morris MJ 1995 Neuropeptide Y potentiation of potassium-induced noradrenaline release in the hypothalamic paraventricular nucleus of the rat in vivo. Brain Res 690:108-111
45. Liposits Z, Paull WK 1989 Association of dopaminergic fibers with corticotropin releasing hormone (CRH)-synthesizing neurons in the paraventricular nucleus of the rat hypothalamus. Histochemistry 93:119-127
46. Bina KG, Cincotta AH 2000 Dopaminergic agonists normalize elevated hypothalamic neuropeptide Y and corticotropin-releasing hormone, body weight gain, and hyperglycemia in ob/ob mice. Neuroendocrinology 71:68-78
47. Tsukahara S, Tsukamura H, Foster DL, Maeda KI 1999 Effect of corticotropin-releasing hormone antagonist on oestrogen-dependent glucoprivic suppression of luteinizing hormone secretion in female rats. J Neuroendocrinol 11:101-105
48. Nagatani S, Tsukamura H, Maeda K 1994 Estrogen feedback needed at the paraventricular nucleus or A2 to suppress pulsatile luteinizing hormone release in fasting female rats. Endocrinology 135:870-875
49. Tsukamura H, Nagatani S, Cagampang FR, Kawakami S, Maeda K 1994 Corticotropin-releasing hormone mediates suppression of pulsatile luteinizing hormone secretion induced by activation of α-adrenergic receptors in the paraventricular nucleus in female rats. Endocrinology 134:1460-1466
50. Estacio MA, Yamada S, Tsukamura H, Hirunagi K, Maeda K 1996 Effect of fasting and immobilization stress on estrogen receptor immunoreactivity in the brain in ovariectomized female rats. Brain Res 717:55-61
51. Reyes BA, Estacio MA, I'Anson H, Tsukamura H, Maeda KI 2001 Glucoprivation increases estrogen receptor α immunoreactivity in the brain catecholaminergic neurons in ovariectomized rats. Neurosci Lett 299:109-112
52. D'Eon TM, Souza SC, Aronovitz M, Obin MS, Fried SK, Greenberg AS 2005 Estrogen regulation of adiposity and fuel partitioning. Evidence of genomic and non-genomic regulation of lipogenic and oxidative pathways. J Biol Chem 280:35983-35991
53. Swanson LW, Sawchenko PE 1983 Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6:269-324