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Short photoperiod-induced decrease of histamine H3 receptors facilitates activation of hypothalamic neurons in the Siberian Hamster

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Barrett, Perry, van den Top, Marco, Wilson, D., Mercer, Julian G., Song, C. K., Bartness, Timothy J., Morgan, Peter J. and Spanswick, David C.. (2009) Short photoperiod-induced decrease of histamine H3 receptors facilitates activation of hypothalamic neurons in the Siberian Hamster. Endocrinology, Vol.150 (No.8). pp. 3655-3663. ISSN 0013-7227

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Official URL: http://dx.doi.org/10.1210/en.2008-1620

Abstract

Nonhibernating seasonal mammals have adapted to temporal changes in food availability through behavioral and physiological mechanisms to store food and energy during times of predictable plenty and conserve energy during predicted shortage. Little is known, however, of the hypothalamic neuronal events that lead to a change in behavior or physiology. Here we show for the first time that a shift from long summer-like to short inter-like photoperiod, which induces physiological adaptation to winter in the Siberian hamster, including a body weight decrease of up to 30%, increases neuronal activity in the dorsomedial region of the arcuate nucleus (dmpARC) assessed by electro physiological patch-clamping recording. Increased neuronal activity in short days is dependent on a photoperiod-driven down-regulation of H3 receptor expression and can be mimicked in long-day dmpARC neurons by the application of the H3 receptor antagonist, clobenproprit. Short-day activation of dmpARC neurons results in increased c-Fos expression. Tract tracing with the trans-synaptic retrograde tracer, pseudorabies virus, delivered into adipose tissue reveals a multisynaptic neuronal sympathetic outflow from dmpARC to white adipose tissue. These data strongly suggest that increased activity of dmpARC neurons, as a consequence of down-regulation of the histamine H3 receptor, contributes to the physiological adaptation of body weight regulation in seasonal photoperiod.

Item Type:

Journal Article

Subjects:

Q Science > QL Zoology
Q Science > QP Physiology

Divisions:

Faculty of Medicine > Warwick Medical School > Biomedical Sciences > Translational & Experimental Medicine > Metabolic and Vascular Health (- until July 2016)
Faculty of Medicine > Warwick Medical School

Library of Congress Subject Headings (LCSH):

Photoperiodism -- Research, Histamine -- Receptors, Hypothalamus, Body weight -- Regulation, Biological control systems, Hamsters -- Anatomy

Journal or Publication Title:

Endocrinology

Publisher:

The Endocrine Society

ISSN:

0013-7227

Official Date:

August 2009

Dates:

Date	Event
August 2009	Published

Volume:

Vol.150

Number:

No.8

Page Range:

pp. 3655-3663

Identification Number:

10.1210/en.2008-1620

Status:

Peer Reviewed

Publication Status:

Published

Access rights to Published version:

Restricted or Subscription Access

Funder:

Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), Seventh Framework Programme (European Commission) (FP7), Scotland. Rural and Environment Research and Analysis Directorate (RERAD), Great Britain. National Health Service (NHS)

Grant number:

LSHM-CT-2003-503041 (FP7)

References:

1. Schneider JE 2004 Energy balance and reproduction. Physiol Behav 81:289–
317
2. Prendergast BJ, Nelson RJ, Zucker I 2002 Mammalian seasonal rhythms:
behavior and neuroendocrine substrates. In: Pfaff D, Arnold A, Etgen A,
Fahrbach S, Rubin R, eds. Hormones, brain and behaviour. Vol. II. San
Diego: Academic Press; 93–156
3. Morgan PJ, Ross AW, Mercer JG, Barrett P 2006 What can we learn from
seasonal animals about the regulation of energy balance? Prog Brain Res 153:
325–337
4. Sallmen T, Beckman AL, Stanton TL, Eriksson KS, Tarhanen J, Tuomisto L,
Panula P 1999 Major changes in the brain histamine system of the ground
squirrel, Citellus lateralis, during hibernation. J Neurosci 19:1824–1835
5. Barrett P, Ebling FJ, Schuhler S, Wilson D, Ross AW, Warner A, Jethwa P,
Boelen A, Visser TJ, Ozanne DM, Archer ZA, Mercer JG, Morgan PJ 2007
Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal
control of body weight and reproduction. Endocrinology 148:3608–
3617
6. Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K,
Ebihara S 2003 Light-induced hormone conversion of T4 to T3 regulates photoperiodic
response of gonads in birds. Nature 426:178–181
7. Viguie´ C, Battaglia DF, Krasa HB, Thrun LA, Karsch FJ 1999 Thyroid hormones
act primarily within the brain to promote the seasonal inhibition of
luteinizing hormone secretion in the ewe. Endocrinology 140:1111–1117
8. Ross AW, Webster CA, Mercer JG, Moar KM, Ebling FJ, Schuhler S, Barrett
P, Morgan PJ 2004 Photoperiodic regulation of hypothalamic retinoid signaling:
association of retinoid X receptor with body weight. Endocrinology
145:13–20
9. Barrett P, Ross AW, Balik A, Littlewood PA, Mercer JG, Moar KM, Sallmen
T, Kaslin J, Panula P, Schuhler S, Ebling FJ, Ubeaud C, Morgan PJ 2005
Photoperiodic regulation of histamine H3 receptor and VGF messenger ribonucleic
acid in the arcuate nucleus of the Siberian hamster. Endocrinology
146:1930–1939
10. Franklin K, Paxinos G 1997 The mouse brain in sterotactic coordinates. San
Diego: Academic Press
11. Garcia M, Floran B, Arias-Montan˜ o JA, Young JM, Aceves J 1997 Histamine
H3 receptor activation selectively inhibits dopamine D1 receptor-dependent
[3H]GABA release from depolarization-stimulated slices of rat substantia
nigra pars reticulata. Neuroscience 80:241–249
12. Brown RE, Stevens DR, Haas HL 2001 The physiology of brain histamine.
Prog Neurobiol 63:637–672
13. Bamshad M, Aoki VT, Adkison MG, Warren WS, Bartness TJ 1998 Central
nervous system origins of the sympathetic nervous system outflow to white
adipose tissue. Am J Physiol 275:R291–R299
14. Song CK, Bartness TJ 2001CNSsympathetic outflow neurons to white fat that
express MEL receptors may mediate seasonal adiposity. Am J Physiol Regul
Integr Comp Physiol 281:R666–R672
15. Morgan PJ, Webster CA, Mercer JG, Ross AW, Hazlerigg DG, MacLean A,
Barrett P 1996 The ovine pars tuberalis secretes a factor(s) that regulates gene
expression in both lactotropic and nonlactotropic pituitary cells. Endocrinology
137:4018–4126
16. Tups A, Helwig M, Sto¨ hr S, Barrett P, Mercer JG, KlingensporM2006 Photoperiodic
regulation of insulin receptor mRNA and intracellular insulin signaling
in the arcuate nucleus of the Siberian hamster, Phodopus sungorus.AmJ
Physiol Regul Integr Comp Physiol 291:R643–R650
17. Franklin K, Paxinos G 1997 The mouse brain in sterotactic coordinates. San
Diego: Academic Press
18. Spanswick D, Smith MA, Mirshamsi S, Routh VH, Ashford ML 2000 Insulin
activates ATP-sensitive Kchannels in hypothalamic neurons of lean, but not
obese rats. Nat Neurosci 3:757–758
19. Spanswick D, Smith MA, Groppi VE, Logan SD, Ashford ML 1997 Leptin
inhibits hypothalamic neurons by activation of ATP-sensitive potassium channels.
Nature 390:521–525
20. van den Top M, Lee K, Whyment AD, Blanks AM, Spanswick D 2004 Orexigen-
sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus.
Nat Neurosci 7:493–494
21. Nakamura T, Itadani H, Hidaka Y, Ohta M, Tanaka K 2000 Molecular
cloning and characterization of a new human histamine receptor, HH4R.
Biochem Biophys Res Commun 279:615–620
22. Liu C, Wilson SJ, Kuei C, LovenbergTW2001 Comparison of human, mouse,
rat, and guinea pig histamineH4receptors reveals substantial pharmacological
species variation. J Pharmacol Exp Ther 299:121–130
23. Morton GJ, Cummings DE, Baskin DG, Barsh GS, SchwartzMW2006 Central
nervous system control of food intake and body weight. Nature 443:289–
295
24. Enriori PJ, Evans AE, Sinnayah P, Cowley MA 2006 Leptin resistance and
obesity. Obesity (Silver Spring) 14(Suppl 5):254S–258S
25. Gottsch ML, Clifton DK, Steiner RA 2004 Galanin-like peptide as a link in the
integration of metabolism and reproduction. Trends Endocrinol Metab 15:
215–221
26. Revel FG, Ansel L, Klosen P, Saboureau M, Pe´vet P, Mikkelsen JD, Simonneaux
V 2007 Kisspeptin: a key link to seasonal breeding. Rev Endocr Metab
Disord 8:57–65
27. Jamali AK, Tramu G 1997 Daily cycle of fos expression within hypothalamic
POMC neurons of the male rat. Brain Res 771:45–54
28. Jamali KA, TramuG1999 Control of rat hypothalamic pro-opiomelanocortin
neurons by a circadian clock that is entrained by the daily light-off signal.
Neuroscience 93:1051–1061
29. Sallmen T, Lozada AF, Anichtchik OV, Beckman AL, Panula P 2003 Increased
brain histamine H3 receptor expression during hibernation in golden-mantled
ground squirrels. BMC Neurosci 4:24
30. Panula P, Pirvola U, Auvinen S, Airaksinen MS 1989 Histamine-immunoreactive
nerve fibers in the rat brain. Neuroscience 28:585–610
31. Inagaki N, Yamatodani A, Ando-Yamamoto M, Tohyama M, Watanabe T,
Wada H 1988 Organization of histaminergic fibers in the rat brain. J Comp
Neurol 273:283–300
32. Pillot C, Pillot C, Heron A, Cochois V, Tardivel-Lacombe J, Ligneau X,
Schwartz JC, Arrang JM 2002 A detailed mapping of the histamine H(3)
receptor and its gene transcripts in rat brain. Neuroscience 114:173–193
33. Ookuma K, Ookuma K, Sakata T, Fukagawa K, Yoshimatsu H, Kurokawa M,
Machidori H, Fujimoto K 1993 Neuronal histamine in the hypothalamus
suppresses food intake in rats. Brain Res 628:235–242
34. Sakata T, Ookuma K, Fujimoto K, Fukagawa K, Yoshimatsu H1991 Histaminergic
control of energy balance in rats. Brain Res Bull 27:371–375
35. Doi T, Sakata T, Yoshimatsu H, Machidori H, Kurokawa M, Jayasekara LA,
Niki N 1994 Hypothalamic neuronal histamine regulates feeding circadian
rhythm in rats. Brain Res 641:311–318
36. Malmlo¨ f K, Zaragoza F, Golozoubova V, Refsgaard HH, Cremers T, Raun K,
Wulff BS, Johansen PB, Westerink B, Rimvall K 2005 Influence of a selective
histamineH3receptor antagonist on hypothalamic neural activity, food intake
and body weight. Int J Obes (Lond) 29:1402–1412
37. Yoshimoto R, Miyamoto Y, Shimamura K, Ishihara A, Takahashi K, Kotani
H, Chen AS, Chen HY, Macneil DJ, Kanatani A, Tokita S 2006 Therapeutic
potential of histamine H3 receptor agonist for the treatment of obesity and
diabetes mellitus. Proc Natl Acad Sci USA 103:13866–13871
38. Leurs R, Bakker RA, Timmerman H, de Esch IJ 2005 The histamine H3
receptor: from gene cloning toH3receptor drugs. Nat Rev Drug Discov 4:107–
120
39. Nilaweera KN, Archer ZA, Campbell G, Mayer CD, Balik A, Ross AW, Mercer
JG, Ebling FJ, Morgan PJ, Barrett P 2009 Photoperiod regulates genes
encoding melanocortin 3 and serotonin receptors and secretogranins in the
dorsomedial posterior arcuate of the Siberian hamster. J Neuroendocrinol
21:123–131