Estradiol alters body temperature regulation in the female mouse

References

• Kronenberg F. Menopausal hot flashes: a review of physiology and biosociocultural perspective on methods of assessment. J Nutr. 2010;140:1380S-1385S. doi:10.3945/jn.109.120840
   PubMed Web of Science ®Google Scholar
• Freedman RR. Physiology of hot flashes. Am J Human Biol. 2001;13:453-464. doi:10.1002/ajhb.1077
   PubMed Web of Science ®Google Scholar
• Rance NE, Young WS, III. Hypertrophy and increased gene expression of neurons containing neurokinin-B and substance-P messenger ribonucleic acids in the hypothalami of postmenopausal women. Endocrinology. 1991;128:2239-2247. doi:10.1210/endo-128-5-2239
   PubMed Web of Science ®Google Scholar
• Sandoval-Guzmán T, Stalcup ST, Krajewski SJ, Voytko ML, Rance NE. Effects of ovariectomy on the neuroendocrine axes regulating reproduction and energy balance in young cynomolgus macaques. J Neuroendocrinol. 2004;16:146-153. doi:10.1111/j.0953-8194.2004.01143.x
   PubMed Web of Science ®Google Scholar
• Rometo AM, Krajewski SJ, Voytko ML, Rance NE. Hypertrophy and increased kisspeptin gene expression in the hypothalamic infundibular nucleus of postmenopausal women and ovariectomized monkeys. J Clin Endocrinol Metab. 2007;92:2744-2750. doi:10.1210/jc.2007-0553
   PubMed Web of Science ®Google Scholar
• Rance NE. Menopause and the human hypothalamus: evidence for the role of kisspeptin/neurokinin B neurons in the regulation of estrogen negative feedback. Peptides. 2009;30:111-122. doi:10.1016/j.peptides.2008.05.016
   PubMed Web of Science ®Google Scholar
• Dacks PA, Krajewski SJ, Rance NE. Activation of neurokinin 3 receptors in the median preoptic nucleus decreases core temperature in the rat. Endocrinology. 2011;152:4894-4905. doi:10.1210/en.2011-1492
   PubMed Web of Science ®Google Scholar
• Mittelman-Smith MA, Williams H, Krajewski-Hall SJ, McMullen NT, Rance NE. Role for kisspeptin/neurokinin B/dynorphin (KNDy) neurons in cutaneous vasodilatation and the estrogen modulation of body temperature. Proc Natl Acad Sci U S A. 2012;109:19846-19851. doi:10.1073/pnas.1211517109
   PubMed Web of Science ®Google Scholar
• Rance NE, Dacks PA, Mittelman-Smith MA, Romanovsky AA, Krajewski-Hall SJ. Modulation of body temperature and LH secretion by hypothalamic KNDy (kisspeptin, neurokinin B and dynorphin) neurons: A novel hypothesis on the mechanism of hot flushes. Front Neuroendocrinol. 2013;34:211-227. doi:10.1016/j.yfrne.2013.07.003
   PubMed Web of Science ®Google Scholar
• Mittelman-Smith MA, Krajewski-Hall SJ, McMullen NT, Rance NE. Neurokinin 3 receptor-expressing neurons in the median preoptic nucleus modulate heat-dissipation effectors in the female rat. Endocrinology. 2015;156:2552-2562. doi:10.1210/en.2014-1974
   PubMed Web of Science ®Google Scholar
• Jayasena CN, Comninos AN, Stefanopoulou E, Buckley A, Narayanaswamy S, Izzi-Engbeaya C, Abbara A, Ratnasabapathy R, Mogford J, Ng N, et al. Neurokinin B administration induces hot flushes in women. Scientific Reports. 2015;5:8466. doi:10.1038/srep08466 PMID:25683060
   PubMed Web of Science ®Google Scholar
• Crandall CJ, Manson JE, Hohensee C, Horvath S, Wactawski-Wende J, LeBlanc ES, Vitolins MZ, Nassir R, Sinsheimer JS. Association of genetic variation in the tachykinin receptor 3 locus with hot flashes and night sweats in the Women's Health Initiative Study. Menopause. 2017;24:252-261. doi:10.1097/GME.0000000000000763
   PubMed Web of Science ®Google Scholar
• Prague JK, Roberts RE, Comninos AN, Clarke S, Jayasena CN, Nash Z, Doyle C, Papadopoulou DA, Bloom SR, Mohideen P, et al. Neurokinin 3 receptor antagonism as a novel treatment for menopausal hot flushes: a phase 2, randomised, double-blind, placebo-controlled trial. Lancet. 2017;389:1809-1820. doi:10.1016/S0140-6736(17)30823-1
   PubMed Web of Science ®Google Scholar
• Fraser GL, Depypere H, Timmerman D, Donders G, Sieprath P, Ramael S, Combalbert J, Hoveyda HR. Clinical Evaluation of the NK3 Receptor Antagonist Fezolinetant (a.k.a. ESN364) for the Treatment of Menopausal Hot Flashes. Endocrine Soc Abstr. 2017;38:OR16-5.
   Google Scholar
• Skorupskaite K, George JT, Veldhuis JD, Millar RP, Anderson RA. Neurokinin 3 Receptor Antagonism Reveals Roles for Neurokinin B in the Regulation of Gonadotropin Secretion and Hot Flashes in Postmenopausal Women. Neuroendocrinology. 2017; In press: doi:10.1159/000473893 PMID:28380486
   PubMed Web of Science ®Google Scholar
• Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA. Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci. 2009;29:11859-11866. doi:10.1523/JNEUROSCI.1569-09.2009
   PubMed Web of Science ®Google Scholar
• Burke MC, Letts PA, Krajewski SJ, Rance NE. Coexpression of dynorphin and neurokinin B immunoreactivity in the rat hypothalamus: morphologic evidence of interrelated function within the arcuate nucleus. J Comp Neurol. 2006;498:712-726. doi:10.1002/cne.21086
   PubMed Web of Science ®Google Scholar
• True C, Kirigiti M, Ciofi P, Grove KL, Smith MS. Characterisation of arcuate nucleus kisspeptin/neurokinin B neuronal projections and regulation during lactation in the rat. J Neuroendocrinol. 2011;23:52-64. doi:10.1111/j.1365-2826.2010.02076.x
   PubMed Web of Science ®Google Scholar
• Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda K-I, et al. Neurokinin B and dynorphin A in kisspeptin neurons of the arcuate nucleus participate in generation of periodic oscillation of neural activity driving pulsatile gonadotropin-releasing hormone secretion in the goat. J Neurosci. 2010;30:3124-3132. doi:10.1523/JNEUROSCI.5848-09.2010
   PubMed Web of Science ®Google Scholar
• Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CVR, Jafarzadehshirazi MR, Pereira A, Iqbal J, Caraty A, Ciofi P, et al. Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology. 2007;148:5752-5760. doi:10.1210/en.2007-0961
   PubMed Web of Science ®Google Scholar
• Lehman MN, Merkley CM, Coolen LM, Goodman RL. Anatomy of the kisspeptin neural network in mammals. Brain Res. 2010;1364:90-102. doi:10.1016/j.brainres.2010.09.020
   PubMed Web of Science ®Google Scholar
• Abel TW, Voytko ML, Rance NE. The effects of hormone replacement therapy on hypothalamic neuropeptide gene expression in a primate model of menopause. J Clin Endocrinol Metab. 1999;84:2111-2118. doi:10.1210/jc.84.6.2111 10.1210/jcem.84.6.5689
   PubMed Web of Science ®Google Scholar
• Ramaswamy S, Seminara SB, Ali B, Ciofi P, Amin NA, Plant TM. Neurokinin B stimulates GnRH release in the male monkey (Macaca mulatta) and is colocalized with kisspeptin in the arcuate nucleus. Endocrinology. 2010;151:4494-4503. doi:10.1210/en.2010-0223
   PubMed Web of Science ®Google Scholar
• Rometo AM, Rance NE. Changes in prodynorphin gene expression and neuronal morphology in the hypothalamus of postmenopausal women. J Neuroendocrinol. 2008;20:1376-1381. doi:10.1111/j.1365-2826.2008.01796.x
   PubMed Web of Science ®Google Scholar
• Hrabovszky E, Borsay BA, Racz K, Herczeg L, Ciofi P, Bloom SR, Ghatei MA, Dhillo WS, Liposits Z. Substance p immunoreactivity exhibits frequent colocalization with kisspeptin and neurokinin B in the human infundibular region. PloS one. 2013;8:e72369. doi:10.1371/journal.pone.0072369 PMID:23977290
   PubMed Web of Science ®Google Scholar
• Romanovsky AA, Ivanov AI, Shimansky YP. Selected contribution: ambient temperature for experiments in rats: a new method for determining the zone of thermal neutrality. J Appl Physiol. 2002;92:2667-2679. doi:10.1152/japplphysiol.01173.2001
   PubMed Web of Science ®Google Scholar
• Gordon CJ, Puckett E, Padnos B. Rat tail skin temperature monitored noninvasively by radiotelemetry: characterization by examination of vasomotor responses to thermomodulatory agents. J Pharmacol Toxicol Methods. 2002;47:107-114. doi:10.1016/S1056-8719(02)00219-8
   PubMed Web of Science ®Google Scholar
• Dacks PA, Rance NE. Effects of estradiol on the thermoneutral zone and core temperature in ovariectomized rats. Endocrinology. 2010;151:1187-1193. doi:10.1210/en.2009-1112
   PubMed Web of Science ®Google Scholar
• Williams H, Dacks PA, Rance NE. An improved method for recording tail skin temperature in the rat reveals changes during the estrous cycle and effects of ovarian steroids. Endocrinology. 2010;151:5389-5394. doi:10.1210/en.2010-0630
   PubMed Web of Science ®Google Scholar
• Dacks PA, Krajewski SJ, Rance NE. Ambient temperature and 17β-estradiol modify fos immunoreactivity in the median preoptic nucleus, a putative regulator of skin vasomotion. Endocrinology. 2011;152:2750-2759. doi:10.1210/en.2010-1230
   PubMed Web of Science ®Google Scholar
• Krajewski SJ, Burke MC, Anderson MJ, McMullen NT, Rance NE. Forebrain projections of arcuate neurokinin B neurons demonstrated by anterograde tract-tracing and monosodium glutamate lesions in the rat. Neuroscience. 2010;166:680-697. doi:10.1016/j.neuroscience.2009.12.053
   PubMed Web of Science ®Google Scholar
• Meyer CW, Ootsuka Y, Romanovsky AA. Body Temperature Measurements for Metabolic Phenotyping in Mice. Front Physiol. 2017;8:520. doi:10.3389/fphys.2017.00520 PMID:28824441
   PubMed Web of Science ®Google Scholar
• Cholanian M, Krajewsk-Hall SJ, Levine RB, McMullen NT, Rance NE. Electrophysiology of Arcuate Neurokinin B Neurons in Female Tac2-EGFP Transgenic Mice. Endocrinology. 2014;155:2555-2565. doi:10.1210/en.2014-1065
   PubMed Web of Science ®Google Scholar
• Berendsen HHG, Kloosterboer HJ. Oestradiol and mirtazapine restore the disturbed tail-temperature of oestrogen-deficient rats. Eur J Pharmacol. 2003;482:329-333. doi:10.1016/j.ejphar.2003.09.061
   PubMed Web of Science ®Google Scholar
• Bowe J, Li XF, Kinsey-Jones J, Heyerick A, Brain S, Milligan S, O'Byrne K. The hop phytoestrogen, 8-prenylnaringenin, reverses the ovariectomy-induced rise in skin temperature in an animal model of menopausal hot flushes. J Endocrinol. 2006;191:399-405. doi:10.1677/joe.1.06919
   PubMed Web of Science ®Google Scholar
• Stoessl AJ, Dourish CT, Iversen SD. The NK-3 tachykinin receptor agonist senktide elicits 5-HT-mediated behaviour following central or peripheral administration in mice and rats. Br J Pharmacol. 1988;94:285-287. doi:10.1111/j.1476-5381.1988.tb11527.x
   PubMed Web of Science ®Google Scholar
• Ström JO, Theodorsson E, Theodorsson A. Order of magnitude differences between methods for maintaining physiological 17beta-oestradiol concentrations in ovariectomized rats. Scand J Clin Lab Invest. 2008;68:814-822. doi:10.1080/00365510802409703
   PubMed Web of Science ®Google Scholar
• Kanosue K, Crawshaw LI, Nagashima K, Yoda T. Concepts to utilize in describing thermoregulation and neurophysiological evidence for how the system works. Eur J Appl Physiol. 2010;109:5-11. doi:10.1007/s00421-009-1256-6
   PubMed Web of Science ®Google Scholar
• Mauvais-Jarvis F, Clegg DJ, Hevener AL. The role of estrogens in control of energy balance and glucose homeostasis. Endocr Rev. 2013;34:309-338. doi:10.1210/er.2012-1055
   PubMed Web of Science ®Google Scholar
• Zhu L, Zou F, Yang Y, Xu P, Saito K, Othrell Hinton A, Jr., Yan X, Ding H, Wu Q, Fukuda M, et al. Estrogens prevent metabolic dysfunctions induced by circadian disruptions in female mice. Endocrinology. 2015;156:2114-2123. doi:10.1210/en.2014-1922
   PubMed Web of Science ®Google Scholar
• Xu P, Zhu L, Saito K, Yang Y, Wang C, He Y, Yan X, Hyseni I, Tong Q, Xu Y. Melanocortin 4 receptor is not required for estrogenic regulations on energy homeostasis and reproduction. Metabolism. 2017;70:152-159. doi:10.1016/j.metabol.2016.12.004
   PubMed Web of Science ®Google Scholar
• Saito K, He Y, Yang Y, Zhu L, Wang C, Xu P, Hinton AO, Yan X, Zhao J, Fukuda M, et al. PI3K in the ventromedial hypothalamic nucleus mediates estrogenic actions on energy expenditure in female mice. Scientific reports. 2016;6:23459. doi:10.1038/srep23459 PMID:26988598
   PubMed Web of Science ®Google Scholar
• Paul KN, Laposky AD, Turek FW. Reproductive hormone replacement alters sleep in mice. Neurosci Lett. 2009;463:239-243. doi:10.1016/j.neulet.2009.07.081
   PubMed Web of Science ®Google Scholar
• Martinez de Morentin PB, Gonzalez-Garcia I, Martins L, Lage R, Fernandez-Mallo D, Martinez-Sanchez N, Ruiz-Pino F, Liu J, Morgan DA, Pinilla L, et al. Estradiol regulates brown adipose tissue thermogenesis via hypothalamic AMPK. Cell Metabolism. 2014;20:41-53.
   PubMed Web of Science ®Google Scholar
• López M, Tena-Sempere M. Estradiol and brown fat. Best Pract Res Clin Endocrinol Metab. 2016;30:527-536. doi:10.1016/j.beem.2016.08.004
   PubMed Web of Science ®Google Scholar
• Clarke SD, Clarke IJ, Rao A, Evans RG, Henry BA. Differential effects of acute and chronic estrogen treatment on thermogenic and metabolic pathways in ovariectomized sheep. Endocrinology. 2013;154:184-192. doi:10.1210/en.2012-1758
   PubMed Web of Science ®Google Scholar
• Tankersley CG, Nicholas WC, Deaver DR, Mikita D, Kenney WL. Estrogen replacement in middle-aged women: thermoregulatory responses to exercise in the heat. J Appl Physiol. 1992;73:1238-1245.
   PubMed Web of Science ®Google Scholar
• Brooks EM, Morgan AL, Pierzga JM, Wladkowski SL, O'Gorman JT, Derr JA, Kenney WL. Chronic hormone replacement therapy alters thermoregulatory and vasomotor function in postmenopausal women. J Appl Physiol. 1997;83:477-484.
   PubMed Web of Science ®Google Scholar
• Brooks-Asplund EM, Cannon JG, Kenney WL. Influence of hormone replacement therapy and aspirin on temperature regulation in postmenopausal women. Am J Physiol Regul Integr Comp Physiol. 2000;279:R839-R848.
   PubMed Web of Science ®Google Scholar
• Roepke TA, Bosch MA, Rick EA, Lee B, Wagner EJ, Seidlova-Wuttke D, Wuttke W, Scanlan TS, Rønnekleiv OK, Kelly MJ. Contribution of a membrane estrogen receptor to the estrogenic regulation of body temperature and energy homeostasis. Endocrinology. 2010;151:4926-4937. doi:10.1210/en.2010-0573
   PubMed Web of Science ®Google Scholar
• Hosono T, Chen X-M, Zhang Y-H, Kanosue K. Effects of estrogen on thermoregulatory responses in freely moving female rats. Ann N Y Acad Sci. 1997;813:207-210. doi:10.1111/j.1749-6632.1997.tb51695.x
   PubMed Web of Science ®Google Scholar
• Marrone BL, Gentry RT, Wade GN. Gonadal hormones and body temperature in rats: effects of estrous cycles, castration and steroid replacement. Physiol Behav. 1976;17:419-425. doi:10.1016/0031-9384(76)90101-3
   PubMed Web of Science ®Google Scholar
• Wilkinson CW, Carlisle HJ, Reynolds RW. Estrogenic effects on behavioral thermoregulation and body temperature of rats. Physiol Behav. 1980;24:337-340. doi:10.1016/0031-9384(80)90096-7
   PubMed Web of Science ®Google Scholar
• Hosono T, Chen X-M, Miyatsuji A, Yoda T, Yoshida K, Yanase-Fujiwara M, Kanosue K. Effects of estrogen on thermoregulatory tail vasomotion and heat-escape behavior in freely moving female rats. Am J Physiol Regul Integr Comp Physiol. 2001;280:R1341-R1347.
   PubMed Web of Science ®Google Scholar
• Laudenslager ML, Wilkinson CW, Carlisle HJ, Hammel HT. Energy balance in ovariectomized rats with and without estrogen replacement. Am J Physiol Regul Integr Comp Physiol. 1980;238:R400-R405.
   Google Scholar
• Berendsen HHG, Weekers AHJ, Kloosterboer HJ. Effect of tibolone and raloxifene on the tail temperature of oestrogen-deficient rats. Eur J Pharmacol. 2001;419:47-54. doi:10.1016/S0014-2999(01)00966-9
   PubMed Web of Science ®Google Scholar
• Cosmi S, Pawlyk AC, Alfinito PD, Roman J, Zhou T, Deecher DC. Simultaneous telemetric monitoring of tail-skin and core body temperature in a rat model of thermoregulatory dysfunction. J Neurosci Methods. 2009;178:270-275. doi:10.1016/j.jneumeth.2008.12.013
   PubMed Web of Science ®Google Scholar
• Girbig D, Keller K, Prelle K, Patchev V, Vonk R, Igl B-W. A dynamic model of circadian rhythms in rodent tail skin temperature for comparison of drug effects. J Circadian Rhythms. 2012;10:1-11. doi:10.1186/1740-3391-10-1 PMID:22221596
   PubMedGoogle Scholar
• Nakamura K, Morrison SF. A thermosensory pathway mediating heat-defense responses. Proc Natl Acad Sci U S A. 2010;107:8848-8853. doi:10.1073/pnas.0913358107
   PubMed Web of Science ®Google Scholar
• Cholanian M, Krajewski-Hall SJ, McMullen NT, Rance NE. Chronic oestradiol reduces the dendritic spine density of KNDy (kisspeptin/neurokinin B/dynorphin) neurones in the arcuate nucleus of ovariectomised Tac2-enhanced green fluorescent protein transgenic mice. J Neuroendocrinol. 2015;27:253-263. doi:10.1111/jne.12263
   PubMed Web of Science ®Google Scholar
• Han SY, McLennan T, Czieselsky K, Herbison AE. Selective optogenetic activation of arcuate kisspeptin neurons generates pulsatile luteinizing hormone secretion. Proc Natl Acad Sci U S A. 2015;112:13109-13114. doi:10.1073/pnas.1512243112
   PubMed Web of Science ®Google Scholar
• Qiu J, Nestor CC, Zhang C, Padilla SL, Palmiter RD, Kelly MJ, Ronnekleiv OK. High-frequency stimulation-induced peptide release synchronizes arcuate kisspeptin neurons and excites GnRH neurons. eLife. 2016;5:e16246. doi:10.7554/eLife.16246 PMID:27549338
   PubMed Web of Science ®Google Scholar
• Casper RF, Yen SSC, Wilkes MM. Menopausal flushes: a neuroendocrine link with pulsatile luteinizing hormone secretion. Science. 1979;205:823-825. doi:10.1126/science.462193
   PubMed Web of Science ®Google Scholar
• Ruka KA, Burger LL, Moenter SM. Regulation of Arcuate Neurons Coexpressing Kisspeptin, Neurokinin B, and Dynorphin by Modulators of Neurokinin 3 and κ-Opioid Receptors in Adult Male Mice. Endocrinology. 2013;154:2761-2771. doi:10.1210/en.2013-1268
   PubMed Web of Science ®Google Scholar
• Molnar GW. Body temperatures during menopausal hot flashes. J Appl Physiol. 1975;38:499-503.
   PubMed Web of Science ®Google Scholar
• Krull AA, Larsen SA, Clifton DK, Neal-Perry G, Steiner RA. A comprehensive method to quantify adaptations by male and female mice with hot flashes induced by the neurokinin B receptor agonist, senktide. Endocrinology. 2017;158:3259-3268. doi:10.1210/en.2017-00142 PMID:28531316
   PubMed Web of Science ®Google Scholar
• Molnar GW. Menopausal hot flashes: their cycles and relation to air temperature. Obstet Gynecol. 1981;57:52S-55S.
   PubMed Web of Science ®Google Scholar
• Kronenberg F. Hot flashes: phenomenology, quality of life, and search for treatment options. Exp Gerontol. 1994;29:319-336. doi:10.1016/0531-5565(94)90012-4
   PubMed Web of Science ®Google Scholar
• Archer DF, Sturdee DW, Baber R, de Villiers TJ, Pines A, Freedman RR, Gompel A, Hickey M, Hunter MS, Lobo RA, et al. Menopausal hot flushes and night sweats: where are we now? Climacteric. 2011;14:515-528. doi:10.3109/13697137.2011.608596
   PubMed Web of Science ®Google Scholar
• Freedman RR, Krell W. Reduced thermoregulatory null zone in postmenopausal women with hot flashes. Am J Obstet Gynecol. 1999;181:66-70. doi:10.1016/S0002-9378(99)70437-0
   PubMed Web of Science ®Google Scholar
• Freedman RR, Blacker CM. Estrogen raises the sweating threshold in postmenopausal women with hot flashes. Fertil Steril. 2002;77:487-490. doi:10.1016/S0015-0282(01)03009-6
   PubMed Web of Science ®Google Scholar