Summary.
Glucagon is known to be a central modulator of neural activity and a peripheral thermogenic effect. The purpose of this study was to better understand the role of glucagon in the control of heat production, shivering and particularly as a mediator of nonshivering thermogenesis (NST) in ducklings. In order to study the mechanism of NST, an intracerebroventricular (i.c.v.) injection of glucagon (10−7 M) in to thermoneutral (TN), chronically glucagon treated (GT) and cold acclimatized (CA) ducklings exposed to acute cold (4°C) or a thermoneutrality (25°C), was performed. At 25°C ambient temperature (Ta), the metabolic rate (MR) remained unchanged after glucagon injection. At 4°C Ta i.c.v. glucagon injection, no significant change in MR was observed in GT and CA ducklings during 160 min of cold exposure, whereas there was 63% decrease in MR in (TN) ducklings (5.02 ± 0.1 2 vs 7.91 ± 0.1 4 W/kg−1 p < 0.05). Shivering activity was completely suppressed in TN and GT ducklings after glucagon administration. The NST was estimated to be 3.26 W/kg. This findings suggest that glucagon administered into the brain has no thermogenic effect but could be involved in the central control of somatic motricity, and here we demonstrated for the first time, of our knowledge, that central glucagon have a role in the development of nonshivering thermogenesis during prolonged cold via an inhibition of shivering in birds.
References
H Abdelmelek T Fechtali Y Filali-Zegzouti JL Rouanet JM Cottet-Emard JM Pequignot H Barre (2001) ArticleTitleResponsiveness of plasma catecholamines to intracerebroventricular injection of glucagon in Muscovy ducklings J Neural Transm 108 793–801 Occurrence Handle11515745 Occurrence Handle1:CAS:528:DC%2BD3MXnslKrt7w%3D Occurrence Handle10.1007/s007020170029
H Barré JL Rouanet (1983) ArticleTitleCalorigenic effect of glucagon and catecholamines in king penguin chicks Am J Physiol 244 R758–R763 Occurrence Handle6859289
H Barré F Cohen-Adad C Duchamp JL Rouanet (1986) ArticleTitleMultilocular adipocytes from muscovy ducklings differentiated in response to cold acclimation J Physiol (Lond) 375 27–38
H Barré F Cohen-Adad JL Rouanet (1987) ArticleTitleTwo daily glucagon injections induce nonshivering thermogenesis in Muscovy ducklings Am J Physiol 252 E616–E620 Occurrence Handle3578510
A Collin S Cassy J Buyse E Decuypere M Damon (2005) ArticleTitlePotential involvement of mammalian and avian uncoupling proteins in the thermogenic effect of thyroid hormones Domest Anim Endocrinol 29 78–87 Occurrence Handle15927767 Occurrence Handle1:CAS:528:DC%2BD2MXltVegsrs%3D Occurrence Handle10.1016/j.domaniend.2005.02.007
F Depocas JS Hart (1975) ArticleTitleUse of the pauling oxygen analyser for measurement of oxygen consumption of animals in open-circuit systems and in a short-lag, closed-circuit apparatus J Appl Physiol 10 388–392
C Duchamp J Chatonnet A Dittmar H Barré (1993) ArticleTitleIncreased role of skeletal muscle in the calorigenic response to glucagon of cold-acclimated ducklings Am J Physiol 265 R1084–R1091 Occurrence Handle8238609 Occurrence Handle1:CAS:528:DyaK2cXltVGgug%3D%3D
C Duchamp F Marmonier F Denjean J Lachuer T Eldershaw JL Rouanet D Roussel H Barré (1999) ArticleTitleRegulatory, cellular and molecular aspects of avian muscle nonshivering thermogenesis Ornis Fennica 76 151–165
TP Eldershaw C Duchamp J Ye MG Clark EQ Colquhoun (1997) ArticleTitlePotential for non-shivering thermogenesis in perfused chicken (Gallus domesticus) muscle Comp Biochem Physiol 117 545–554 Occurrence Handle1:STN:280:DyaK2szmt1yqsQ%3D%3D Occurrence Handle10.1016/S0300-9629(96)00401-X
W Fan A Voss-Andreae WH Cao SF Morrison (2005) ArticleTitleRegulation of thermogenesis by the central melanocortin system Peptides 26 1800–1813 Occurrence Handle15979759 Occurrence Handle1:CAS:528:DC%2BD2MXhtVarsL3O Occurrence Handle10.1016/j.peptides.2004.11.033
Y Filali-Zegzouti H Abdelmelek JL Rouanet JM Cottet-Emard JM Pequignot H Barre (2000) ArticleTitleInvolvement of the catecholaminergic system in glucagon-induced thermogenesis in Muscovy ducklings (Cairina moschata) Pflügers Arch Eur J Physiol 441 275–280 Occurrence Handle1:CAS:528:DC%2BD3cXos1KhtLY%3D Occurrence Handle10.1007/s004240000409
Y Filali-Zegzouti H Abdelmelek JL Rouanet JM Cottet-Emard JM Pequignot H Barre (2005) ArticleTitleRole of catecholamines in glucagon-induced thermogenesis J Neural Transm 112 481–489 Occurrence Handle15480854 Occurrence Handle1:CAS:528:DC%2BD2MXisV2hsL8%3D Occurrence Handle10.1007/s00702-004-0199-7
HM Goodman (2003) Basic medical endocrinology Acad Press Amsterdam 98–100
SM Gustavson CA Chu M Nishizawa B Farmer D Neal Y Yang S Vaughan EP Donahue P Flakoll AD Cherrington (2003) ArticleTitleGlucagon’s actions are modified by the combination of epinephrine and gluconeogenic precursor infusion Am J Physiol Endocrinol Metab 285 E534–E544 Occurrence Handle12736160 Occurrence Handle1:CAS:528:DC%2BD3sXnsVGmt7k%3D
I Halvorson J Thornhill (1993) ArticleTitlePosterior hypothalamic stimulation of anesthetized normothermic and hypothermic rats evokes shivering thermogenesis Brain Res 610 208–215 Occurrence Handle8319083 Occurrence Handle1:STN:280:DyaK3szgs1Cltw%3D%3D Occurrence Handle10.1016/0006-8993(93)91402-E
R Hampl L Starka L Jansky (2005) ArticleTitleSteroids and thermogenesis Physiol Res 24 97–102
E Hohtola (1982) ArticleTitleThermal and electromyographic correlates of shivering thermogenesis in the Pigeons Comp Biochem Physiol 73 159–166 Occurrence Handle1:STN:280:DyaL3s%2Flt1Smsg%3D%3D Occurrence Handle10.1016/0300-9629(82)90049-4
E Hohtola S Saarela R Harjula R Hissa (1989) ArticleTitleCardiovascular and thermoregulatory responses to intrahypothalamically injected neurotransmitters in the pigeon J Therm Biol 14 41–45 Occurrence Handle1:CAS:528:DyaL1MXpt1CjtQ%3D%3D Occurrence Handle10.1016/0306-4565(89)90028-4
L Janský (1995) ArticleTitleHumoral thermogenesis and its role in maintaining energy balance Physiol Rev 75 237–259 Occurrence Handle7724662
P Janský L Janský (2002) ArticleTitleSites and cellular mechanisms of human adrenergic thermogenesis J Thermal Biol 27 269–277 Occurrence Handle10.1016/S0306-4565(01)00089-4
Y Jiang AM Cypes ED Muse CR Wu CG Unson RB Merrifield TP Sakmar (2001) ArticleTitleSakmar Glucagon receptor activates extracellular signal-regulated protein kinase ½ via cAMP-dependent proteine kinase Proc Natl Acad Sci USA 98 10102–10107 Occurrence Handle11517300 Occurrence Handle1:CAS:528:DC%2BD3MXmvFWit78%3D Occurrence Handle10.1073/pnas.131200398
K Kanosue YH Zhang M Yanase-Fujiwara T Hosono (1994) ArticleTitleHypothalamic network for thermoregulatory shivering Am J Physiol 267 R275–R282 Occurrence Handle8048633 Occurrence Handle1:STN:280:DyaK2czisVKhsA%3D%3D
JC Keller (1980) Role of glucagon in the regulation of metabolism in growing chicken LE Mount (Eds) Energy metabolism Butterworth London 417–419
M Krimphove K Opitz (1975) ArticleTitleUntersuchung der calorigenen wirkung von Glucagon Arch Int Pharmacodyn Ther 216 328–350 Occurrence Handle241304 Occurrence Handle1:CAS:528:DyaE2MXlsVagsrs%3D
A Lanni M Moreno A Lombardi F Goglia (2003) ArticleTitleThyroid hormone and uncoupling proteins FEBS Lett 543 5–10 Occurrence Handle12753895 Occurrence Handle1:CAS:528:DC%2BD3sXjs1CrsL0%3D Occurrence Handle10.1016/S0014-5793(03)00320-X
G Lusk (1942) ArticleTitleAnimal calorimandry, analysis of the oxidation of mixture of carbohydrate and fat. A correction J Biol Chem 59 41–42
K Marjoniemi E Hohtola (2000) ArticleTitleDoes cold acclimation induce nonshivering thermogenesis in juvenile birds? Experiments with Pekin ducklings and Japanese quail chicks J Comp Physiol (B) 170 537–543 Occurrence Handle1:STN:280:DC%2BD3M7gsVGruw%3D%3D
F Marmonier C Duchamp F Cohen-Adad TP Eldershaw H Barre (1997) ArticleTitleHormonal control of thermogenesis in perfused muscle of Muscovy ducklings Am J Physiol 273 1638–1648
R Martin E Simon C Simon-Oppermann (1981) ArticleTitleBrain stem sites mediating specific and non-specific temperature effects on thermoregulation in the Pekin duck J Physiol (Lond) 314 161–173 Occurrence Handle1:STN:280:DyaL38%2FnslKktw%3D%3D
A Montaron E Moyes H Barré (1994) ArticleTitleRadioautographic demonstration and localisation of glucagon receptors in duck brain Brain Res 663 121–130 Occurrence Handle7850460 Occurrence Handle1:CAS:528:DyaK2cXmvFOntrk%3D Occurrence Handle10.1016/0006-8993(94)90469-3
A Montaron JL Rouanet H Barré (1995) ArticleTitleInhibition of shivering thermogenesis by the centrally applied glucagon in muscovy ducklings Brain Res 702 49–54 Occurrence Handle8846095 Occurrence Handle1:CAS:528:DyaK2MXpvVykurs%3D Occurrence Handle10.1016/0006-8993(95)00961-9
GJ Murphy VJ Hruby D Trivedi MJO Wakelmam MD Houslay (1987) ArticleTitleThe rapid desensitization of glucagon-stimulated adenylate cyclase is a cyclic AMP-independent process that can be mimicked by hormones which stimulate inositol phospholipid metabolism Biochem J 243 39–46 Occurrence Handle3038085 Occurrence Handle1:CAS:528:DyaL2sXitVyisr8%3D
TP Oscar (1995) ArticleTitleGlucagon binding to receptors on the surface of chicken adipocytes J Anim Sci 73 728–737 Occurrence Handle7608005 Occurrence Handle1:CAS:528:DyaK2MXktFGgtLg%3D
J Ostnes C Bech (1992) ArticleTitleThermosensitivity of different parts of the spinal cord of the pigeon (Colombia livia) J Exp Biol 162 185–196
E Padrell JT Herberg B Monsatirsky G Floyd RT Premont R Iyengar (1987) ArticleTitleThe hepatic glucagon receptor: a comparative study of the regulatory and structural properties Endocrinology 120 2316–2325 Occurrence Handle3032585 Occurrence Handle1:CAS:528:DyaL2sXktlelsbs%3D Occurrence Handle10.1210/endo-120-6-2316
H Shimizu M Egawa H Yoshimatsu GA Bray (1993) ArticleTitleGlucagon injected in the lateral hypothalamus stimulates sympathetic activity and suppresses monoamine metabolism Brain Res 630 95–100 Occurrence Handle8118708 Occurrence Handle1:CAS:528:DyaK2cXmvF2muw%3D%3D Occurrence Handle10.1016/0006-8993(93)90647-6
A Uehara H Yoshiaki A Kuroshima (1986) ArticleTitleEffect of cold acclimation on glucagon receptors of rat white adipocytes Jpn J Physiol 36 891–903 Occurrence Handle3031347 Occurrence Handle1:CAS:528:DyaL2sXmtFGlsw%3D%3D
CG Unson EM Gurzenda RB Merrifield (1989) ArticleTitleBiological activities of des-Hisl (Glu9) glucagon amide, a glucagon antagonist Peptides 10 1171–1177 Occurrence Handle2560175 Occurrence Handle1:CAS:528:DyaK3cXhtFanu78%3D Occurrence Handle10.1016/0196-9781(89)90010-7
MJO Wakelam GJ Murphy VJ Hruby MD Hous1ay (1986) ArticleTitleActivation of two signal-transduction systems in hepatocytes by glucagons Nature 323 68–71 Occurrence Handle3018586 Occurrence Handle1:CAS:528:DyaL28Xls1Gms7g%3D Occurrence Handle10.1038/323068a0
K Yoshida M Konishi K Nagashima CB Saper K Kanosue (2005) ArticleTitleFos activation in hypothalamic neurons during cold or warm exposure: projections to periaqueductal gray matter Neuroscience 133 1039–1046 Occurrence Handle15927405 Occurrence Handle1:CAS:528:DC%2BD2MXlt1Khs7w%3D Occurrence Handle10.1016/j.neuroscience.2005.03.044
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Squalli, A., Slimani, M., Filali, Y. et al. Role of glucagon in the control of heat production in ducklings. J Neural Transm 113, 1417–1424 (2006). https://doi.org/10.1007/s00702-005-0418-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00702-005-0418-x