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Photoperiodic regulation of satiety mediating neuropeptides in the brainstem of the seasonal Siberian hamster (Phodopus sungorus)

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Abstract

Central regulation of energy balance in seasonal mammals such as the Siberian hamster is dependent on the precise integration of short-term satiety information arising from the gastrointestinal tract with long-term signals on the status of available energy reserves (e.g. leptin) and prevailing photoperiod. Within the central nervous system, the brainstem nucleus of the solitary tract (NTS) and the parabrachial nucleus (PBN) are major relay nuclei that transmit information from the gastrointestinal tract to higher forebrain centres. We extended studies on the seasonal programming of the hypothalamus to examine the effect of the photoperiod on neuropeptidergic circuitries of this gut–brain axis. In the NTS and PBN we performed gene expression and immunoreactivity (-ir) studies on selected satiety-related neuropeptides and receptors: alpha-melanocyte stimulating hormone, melanocortin-3 receptor, melanocortin-4 receptor (MC4-R), growth hormone secretagogue-receptor, cocaine- and amphetamine-regulated transcript, preproglucagon (PPG), glucagon-like peptide 1 (GLP-1), cholecystokinin (CCK), peptide YY, galanin, neurotensin, and corticotrophin releasing hormone (CRH). Gene expression of PPG and MC4-R, and -ir of CCK and GLP-1, in the NTS were up-regulated after 14 weeks in long-day photoperiod (16 h light:8 h dark) compared to short-days (8 h light:16 h dark), whereas CRH-ir and NT-ir were increased in short-days within the PBN. We suggest that brainstem neuroendocrine mechanisms contribute to the long-term regulation of body mass in the Siberian hamster by a photoperiod-related modulation of satiety signalling.

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Abbreviations

α-MSH:

Alpha-melanocyte stimulating hormone

AgRP:

Agouti-related peptide

CART:

Cocaine- and amphetamine-regulated transcript

CCK:

Cholecystokinin

CNS:

Central nervous system

CRH:

Corticotrophin releasing hormone

GAL:

Galanin

GHS-R:

Growth hormone secretagogue-receptor

GLP:

Glucagon-like peptide

i.c.v.:

Intracerebroventricular

-ir:

Immunoreactivity

LD:

Long day

MCR:

Melanocortin receptor

NPY:

Neuropeptide Y

NT:

Neurotensin

NTS:

Nucleus of the solitary tract

PBN:

Parabrachial nucleus

POMC:

Pro-opiomelanocortin

PPG:

Preproglucagon

PYY:

Peptide YY

SCN:

Suprachiasmatic nucleus

SD:

Short day

References

  • Adam CL, Moar KM, Logie TJ, Ross AW, Barrett P, Morgan PJ, Mercer JG (2000) Photoperiod regulates growth, puberty and hypothalamic neuropeptide and receptor gene expression in female Siberian hamsters. Endocrinology 141:4349–4356

    Article  PubMed  CAS  Google Scholar 

  • Bartness TJ, Morley JE, Levine AS (1986) Photoperiod-peptide interactions in the energy intake of Siberian hamsters. Peptides 7:1079–1085

    Article  PubMed  CAS  Google Scholar 

  • Becskei C, Grabler V, Edwards GL, Riediger T, Lutz TA (2007) Lesion of the lateral parabrachial nucleus attenuates the anorectic effect of peripheral amylin and CCK. Brain Res 1162:76–84

    Article  PubMed  CAS  Google Scholar 

  • Blevins JE, Stanley BG, Reidelberger RD (2000) Brain regions where cholecystokinin suppresses feeding in rats. Brain Res 860:1–10

    Article  PubMed  CAS  Google Scholar 

  • Blevins JE, Schwartz MW, Baskin DG (2004) Evidence that paraventricular nucleus oxytocin neurons link hypothalamic leptin action to caudal brain stem nuclei controlling meal size. Am J Physiol Regul Integr Comp Physiol 287:R87–R96

    PubMed  CAS  Google Scholar 

  • Blevins JE, Chelikani PK, Haver AC, Reidelberger RD (2008) PYY(3–36) induces Fos in the arcuate nucleus and in both catecholaminergic and non-catecholaminergic neurons in the nucleus tractus solitarius of rats. Peptides 29:112–119

    Article  PubMed  CAS  Google Scholar 

  • Block CH, Hoffman GE (1987) Neuropeptide and monoamine components of the parabrachial pontine complex. Peptides 8:267–283

    Article  PubMed  CAS  Google Scholar 

  • Calingasan NY, Ritter S (1992) Presence of galanin in rat vagal sensory neurons: evidence from immunohistochemistry and in situ hybridization. J Auton Nerv Syst 40:229–238

    Article  PubMed  CAS  Google Scholar 

  • Cummings S, Elde R, Ells J, Lindall A (1983) Corticotropin-releasing factor immunoreactivity is widely distributed within the central nervous system of the rat: an immunohistochemical study. J Neurosci 3:1355–1368

    PubMed  CAS  Google Scholar 

  • de Beaurepaire R, Suaudeau C (1988) Anorectic effect of calcitonin, neurotensin and bombesin infused in the area of the rostral part of the nucleus of the tractus solitarius in the rat. Peptides 9:729–733

    Article  PubMed  Google Scholar 

  • de Castro e Silva E, Fregoneze JB, Johnson AK (2006) Corticotropin-releasing hormone in the lateral parabrachial nucleus inhibits sodium appetite in rats. Am J Physiol Regul Integr Comp Physiol 290:R1136–R1141

    PubMed  Google Scholar 

  • Dhillo WS, Bloom SR (2004) Gastrointestinal hormones and regulation of food intake. Horm Metab Res 36:846–851

    Article  PubMed  CAS  Google Scholar 

  • Dun SL, Castellino SJ, Yang J, Chang JK, Dun NJ (2001) Cocaine- and amphetamine-regulated transcript peptide-immunoreactivity in dorsal motor nucleus of the vagus neurons of immature rats. Brain Res Dev Brain Res 131:93–102

    Article  PubMed  CAS  Google Scholar 

  • Dun SL, Ng YK, Brailoiu GC, Ling EA, Dun NJ (2002) Cocaine- and amphetamine-regulated transcript peptide-immunoreactivity in adrenergic C1 neurons projecting to the intermediolateral cell column of the rat. J Chem Neuroanat 23:123–132

    Article  PubMed  CAS  Google Scholar 

  • Elias CF, Kelly JF, Lee CE, Ahima RS, Drucker DJ, Saper CB, Elmquist JK (2000) Chemical characterization of leptin-activated neurons in the rat brain. J Comp Neurol 423:261–281

    Article  PubMed  CAS  Google Scholar 

  • Elmquist JK, Ahima RS, Maratos-Flier E, Flier JS, Saper CB (1997) Leptin activates neurons in ventrobasal hypothalamus and brainstem. Endocrinology 138:839–842

    Article  PubMed  CAS  Google Scholar 

  • Fite KV, Wu PS, Bellemer A (2005) Photostimulation alters c-Fos expression in the dorsal raphe nucleus. Brain Res 1031:245–252

    Article  PubMed  CAS  Google Scholar 

  • Fulwiler CE, Saper CB (1985) Cholecystokinin-immunoreactive innervation of the ventromedial hypothalamus in the rat: possible substrate for autonomic regulation of feeding. Neurosci Lett 53:289–296

    Article  PubMed  CAS  Google Scholar 

  • Gardner JD, Rothwell NJ, Luheshi GN (1998) Leptin affects food intake via CRF-receptor-mediated pathways. Nat Neurosci 1:103

    Article  PubMed  CAS  Google Scholar 

  • Goldstone AP, Mercer JG, Gunn I, Moar KM, Edwards CM, Rossi M, Howard JK, Rasheed S, Turton MD, Small C, Heath MM, O’Shea D, Steere J, Meeran K, Ghatei MA, Hoggard N, Bloom SR (1997) Leptin interacts with glucagon-like peptide-1 neurons to reduce food intake and body weight in rodents. FEBS Lett 415:134–138

    Article  PubMed  CAS  Google Scholar 

  • Grill HJ, Markison S, Ginsberg A, Kaplan JM (2000) Long-term effects on feeding and body weight after stimulation of forebrain or hindbrain CRH receptors with urocortin. Brain Res 867:19–28

    Article  PubMed  CAS  Google Scholar 

  • Herbert H, Saper CB (1990) Cholecystokinin-, galanin-, and corticotropin-releasing factor-like immunoreactive projections from the nucleus of the solitary tract to the parabrachial nucleus in the rat. J Comp Neurol 293:581–598

    Article  PubMed  CAS  Google Scholar 

  • Hermanson O, Larhammar D, Blomqvist A (1998) Preprocholecystokinin mRNA-expressing neurons in the rat parabrachial nucleus: subnuclear localization, efferent projection, and expression of nociceptive-related intracellular signaling substances. J Comp Neurol 400:255–270

    Article  PubMed  CAS  Google Scholar 

  • Hokfelt T, Cortes R, Schalling M, Ceccatelli S, Pelto-Huikko M, Persson H, Villar MJ (1991) Distribution patterns of CCK and CCK mRNA in some neuronal and non-neuronal tissues. Neuropeptides 19:31–43

    Article  PubMed  Google Scholar 

  • Hosoi T, Kawagishi T, Okuma Y, Tanaka J, Nomura Y (2002) Brain stem is a direct target for leptin’s action in the central nervous system. Endocrinology 143:3498–3504

    Article  PubMed  CAS  Google Scholar 

  • Joseph SA, Pilcher WH, nett-Clarke C (1983) Immunocytochemical localization of ACTH perikarya in nucleus tractus solitarius: evidence for a second opiocortin neuronal system. Neurosci Lett 38:221–225

    Article  PubMed  CAS  Google Scholar 

  • Kelly AB, Watts AG (1998) The region of the pontine parabrachial nucleus is a major target of dehydration-sensitive CRH neurons in the rat lateral hypothalamic area. J Comp Neurol 394:48–63

    Article  PubMed  CAS  Google Scholar 

  • Kishi T, Aschkenasi CJ, Lee CE, Mountjoy KG, Saper CB, Elmquist JK (2003) Expression of melanocortin 4 receptor mRNA in the central nervous system of the rat. J Comp Neurol 457:213–235

    Article  PubMed  CAS  Google Scholar 

  • Klingenspor M, Niggemann H, Heldmaier G (2000) Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian hamster, Phodopus sungorus. J Comp Physiol [B] 170:37–43

    CAS  Google Scholar 

  • Larsen PJ, Tang-Christensen M, Holst JJ, Orskov C (1997) Distribution of glucagon-like peptide-1 and other preproglucagon-derived peptides in the rat hypothalamus and brainstem. Neuroscience 77:257–270

    Article  PubMed  CAS  Google Scholar 

  • Mercer JG, Tups A (2003) Neuropeptides and anticipatory changes in behaviour and physiology: seasonal body weight regulation in the Siberian hamster. Eur J Pharmacol 480:43–50

    Article  PubMed  CAS  Google Scholar 

  • Mercer JG, Hoggard N, Williams LM, Lawrence CB, Hannah LT, Trayhurn P (1996) Localization of leptin receptor mRNA and the long form splice variant (Ob-Rb) in mouse hypothalamus and adjacent brain regions by in situ hybridization. FEBS Lett 387:113–116

    Article  PubMed  CAS  Google Scholar 

  • Mercer JG, Moar KM, Hoggard N (1998) Localization of leptin receptor (Ob-R) messenger ribonucleic acid in the rodent hindbrain. Endocrinology 139:29–34

    Article  PubMed  CAS  Google Scholar 

  • Mercer JG, Moar KM, Ross AW, Hoggard N, Morgan PJ (2000) Photoperiod regulates arcuate nucleus POMC, AGRP, and leptin receptor mRNA in Siberian hamster hypothalamus. Am J Physiol Regul Integr Comp Physiol 278:R271–R281

    PubMed  CAS  Google Scholar 

  • Mercer JG, Moar KM, Logie TJ, Findlay PA, Adam CL, Morgan PJ (2001) Seasonally inappropriate body weight induced by food restriction: effect on hypothalamic gene expression in male Siberian hamsters. Endocrinology 142:4173–4181

    Article  PubMed  CAS  Google Scholar 

  • Mercer JG, Ellis C, Moar KM, Logie TJ, Morgan PJ, Adam CL (2003) Early regulation of hypothalamic arcuate nucleus CART gene expression by short photoperiod in the Siberian hamster. Regul Pept 111:129–136

    Article  PubMed  CAS  Google Scholar 

  • Morgan PJ, Mercer JG (1994) Control of seasonality by melatonin. Proc Nutr Soc 53:483–493

    Article  PubMed  CAS  Google Scholar 

  • Morgan PJ, Ross AW, Mercer JG, Barrett P (2003) Photoperiodic programming of body weight through the neuroendocrine hypothalamus. J Endocrinol 177:27–34

    Article  PubMed  CAS  Google Scholar 

  • Murphy KG, Bloom SR (2006) Gut hormones and the regulation of energy homeostasis. Nature 444:854–859

    Article  PubMed  CAS  Google Scholar 

  • Nagase H, Nakajima A, Sekihara H, York DA, Bray GA (2002) Regulation of feeding behavior, gastric emptying, and sympathetic nerve activity to interscapular brown adipose tissue by galanin and enterostatin: the involvement of vagal-central nervous system interactions. J Gastroenterol 37(Suppl 14):118–127

    PubMed  CAS  Google Scholar 

  • Paxinos G, Franklin K (2002) The mouse brain in stereotaxic coordinates. Academic Press, New York

    Google Scholar 

  • Reddy AB, Cronin AS, Ford H, Ebling FJ (1999) Seasonal regulation of food intake and body weight in the male Siberian hamster: studies of hypothalamic orexin (hypocretin), neuropeptide Y (NPY) and pro-opiomelanocortin (POMC). Eur J Neurosci 11:3255–3264

    Article  PubMed  CAS  Google Scholar 

  • Sahu A, Carraway RE, Wang YP (2001) Evidence that neurotensin mediates the central effect of leptin on food intake in rat. Brain Res 888:343–347

    Article  PubMed  CAS  Google Scholar 

  • Saleh TM, Cechetto DF (1996) Peptide changes in the parabrachial nucleus following cervical vagal stimulation. J Comp Neurol 366:390–405

    Article  PubMed  CAS  Google Scholar 

  • Schick RR, Reilly WM, Roddy DR, Yaksh TL, Go VL (1987) Neuronal cholecystokinin-like immunoreactivity is postprandially released from primate hypothalamus. Brain Res 418:20–26

    Article  PubMed  CAS  Google Scholar 

  • Schick RR, Yaksh TL, Roddy DR, Go VL (1989) Release of hypothalamic cholecystokinin in cats: effects of nutrient and volume loading. Am J Physiol 256:R248–R254

    PubMed  CAS  Google Scholar 

  • Simmons DM, Arriza JL, Swanson LW (1989) A complete protocol for in situ hybridization of messenger RNAs in brain and other tissues with radiolabeled single-stranded RNA probes. J Histotechnol 12:169–181

    CAS  Google Scholar 

  • Steinlechner S, Heldmaier G (1982) Role of photoperiod and melatonin in seasonal acclimatization of the Djungarian hamster, Phodopus sungorus. Int J Biometeorol 26:329–337

    Article  PubMed  CAS  Google Scholar 

  • Tache Y, Yang H, Kaneko H (1995) Caudal raphe-dorsal vagal complex peptidergic projections: role in gastric vagal control. Peptides 16:431–435

    Article  PubMed  CAS  Google Scholar 

  • Tang-Christensen M, Larsen PJ, Goke R, Fink-Jensen A, Jessop DS, Moller M, Sheikh SP (1996) Central administration of GLP-1-(7–36) amide inhibits food and water intake in rats. Am J Physiol 271:R848–R856

    PubMed  CAS  Google Scholar 

  • Tups A, Ellis C, Moar KM, Logie TJ, Adam CL, Mercer JG, Klingenspor M (2004) Photoperiodic regulation of leptin sensitivity in the Siberian hamster, Phodopus sungorus, is reflected in arcuate nucleus SOCS-3 (suppressor of cytokine signaling) gene expression. Endocrinology 145:1185–1193

    Article  PubMed  CAS  Google Scholar 

  • Tups A, Barrett P, Ross AW, Morgan PJ, Klingenspor M, Mercer JG (2006) The suppressor of cytokine signalling 3, SOCS3, may be one critical modulator of seasonal body weight changes in the Siberian hamster, Phodopus sungorus. J Neuroendocrinol 18:139–145

    Article  PubMed  CAS  Google Scholar 

  • Vrang N, Hansen M, Larsen PJ, Tang-Christensen M (2007) Characterization of brainstem preproglucagon projections to the paraventricular and dorsomedial hypothalamic nuclei. Brain Res 1149:118–126

    Article  PubMed  CAS  Google Scholar 

  • Vrontakis ME, Yamamoto T, Schroedter IC, Nagy JI, Friesen HG (1989) Estrogen induction of galanin synthesis in the rat anterior pituitary gland demonstrated by in situ hybridization and immunohistochemistry. Neurosci Lett 100:59–64

    Article  PubMed  CAS  Google Scholar 

  • Weaver DR, Rivkees SA, Reppert SM (1989) Localization and characterization of melatonin receptors in rodent brain by in vitro autoradiography. J Neurosci 9:2581–2590

    PubMed  CAS  Google Scholar 

  • Williams LM, Hannah LT, Hastings MH, Maywood ES (1995) Melatonin receptors in the rat brain and pituitary. J Pineal Res 19:173–177

    Article  PubMed  CAS  Google Scholar 

  • Zheng H, Patterson LM, Phifer CB, Berthoud HR (2005) Brain stem melanocortinergic modulation of meal size and identification of hypothalamic POMC projections. Am J Physiol Regul Integr Comp Physiol 289:R247–R258

    PubMed  CAS  Google Scholar 

  • Zigman JM, Jones JE, Lee CE, Saper CB, Elmquist JK (2006) Expression of ghrelin receptor mRNA in the rat and the mouse brain. J Comp Neurol 494:528–548

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Sigrid Stöhr for her excellent technical assistance. All described procedures were in accordance with German animal welfare regulations, or were licensed under the UK Home Office Animals (Scientific Procedures) Act, 1986, and had local ethical approval. M. Helwig was recipient of a fellowship funded by the European Commission to attend the ObeSechool European Union Marie Curie Training Site at the Rowett Research Institute. This collaborative study was also funded by the Scottish Government (to J. G. Mercer), EC FP6 funding (‘DIABESITY’ contract no. LSHM-CT-2003-503041 to J. G. Mercer), Deutsche Forschungsgemeinschaft (German Research Foundation KL973/5; to M. Klingenspor) and the National Genome Research Network (NGFN2 01GS0483, NGFNplus 01GS0822; to M. Klingenspor).

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Authors and Affiliations

  1. Molecular Nutritional Medicine, Else Kröner-Fresenius Center, Technische Universität München, Am Forum 5, 85350, Freising-Weihenstephan, Germany

    Michael Helwig & Martin Klingenspor

  2. The Rowett Institute of Nutrition and Health at the University of Aberdeen, Aberdeen, Scotland, UK

    Michael Helwig, Zoë A. Archer & Julian G. Mercer

  3. Department of Animal Physiology, Faculty of Biology, Philipps Universität Marburg, Marburg, Germany

    Gerhard Heldmaier & Alexander Tups

  4. ZIEL, Research Center for Nutrition and Food Science, Technische Universität München, Freising-Weihenstephan, Germany

    Martin Klingenspor

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  1. Michael Helwig
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  2. Zoë A. Archer
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  3. Gerhard Heldmaier
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  5. Julian G. Mercer
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Correspondence to Michael Helwig.

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Helwig, M., Archer, Z.A., Heldmaier, G. et al. Photoperiodic regulation of satiety mediating neuropeptides in the brainstem of the seasonal Siberian hamster (Phodopus sungorus). J Comp Physiol A 195, 631–642 (2009). https://doi.org/10.1007/s00359-009-0438-3

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