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Control and Regulatory Mechanisms Associated with Thermogenesis in Flying Insects and Birds

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Most insects and birds are able to fly. The chitin made exoskeleton of insects poses them several constraints, and this is one the reasons they are in general small sized animals. On the other hand, because birds possess an endoskeleton made of bones they may grow much larger when compared to insects. The two taxa are quite different with regards to their general “design” platform, in particular with respect to their respiratory and circulatory systems. However, because they fly, they may share in common several traits, namely those associated with the control and regulatory mechanisms governing thermogenesis. High core temperatures are essential for animal flight irrespective of the taxa they belong to. Birds and insects have thus evolved mechanisms which allowed them to control and regulate high rates of heat fluxes. This article discusses possible convergent thermogenic control and regulatory mechanisms associated with flight in insects and birds.

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References

  • S. A. Adamo C. E. Linn R. R. Hoy (1995) ArticleTitleThe role of neurohormonal octopamine during “fight or flight” behaviour in the field cricket Gryllus bimaculatus J. Exp. Biol. 198 1691–1700 Occurrence Handle7636443

    PubMed  Google Scholar 

  • S. H. Adams (2000) ArticleTitleUncoupling protein homologs: emerging views of physiological function J. Nutr. 130 711–714 Occurrence Handle10736318

    PubMed  Google Scholar 

  • R. R.S. Ahima D. Prabakaran C. Mantzoros D. Qu B. Lowell E. Maratos-Flier J. Flier (1996) ArticleTitleRole of leptin in the neuroeadocrine response to fasting Nature 382 250–252 Occurrence Handle10.1038/382250a0 Occurrence Handle8717038

    Article  PubMed  Google Scholar 

  • G. Argyopoulos M. Harper (2002) ArticleTitleInvited review: uncoupling proteins and thermoregulation J. Appl. Physiol. 92 2187–2198 Occurrence Handle11960973

    PubMed  Google Scholar 

  • A. Aulie O. Toien (1988) ArticleTitleThreshold for shivering in aerobic and anaerobic muscles in bantam cocks and incubating hens J. Comp. Physiol. B 158 431–435 Occurrence Handle10.1007/BF00691140 Occurrence Handle3220987

    Article  PubMed  Google Scholar 

  • A. B. Barron D. J. Schulz G. E. Robinson (2002) ArticleTitleOctopamine modulates responsiveness to foraging – stimulated stimuli in honey bees (Apis mellifera) J. Comp. Physiol. A 188 603–610 Occurrence Handle10.1007/s00359-002-0335-5

    Article  Google Scholar 

  • L Bartalena F. Bogazzi S. Brogioni L. Grasso E. Martino (1998) ArticleTitleRole of cytokines in the pathogenesis of the euthyroid sik syndrome Eur. J. Endocrinol. 138 603–614 Occurrence Handle10.1530/eje.0.1380603 Occurrence Handle9678522

    Article  PubMed  Google Scholar 

  • G. A. Bartholomew (1981) A matter of size: an examination of endothermy in insects and terrestrial vertebrates B. Heinrich (Eds) Insect Thermoregulation Wiley-Interscience Publication New York

    Google Scholar 

  • G. A. Bartholomew B. Heinrich (1978) ArticleTitleEndothermy in African dung beetles during flight, ball making, and ball rolling J. Exp. Biol. 73 65–83

    Google Scholar 

  • L. P. Belzunces R. Vandame X. Gu (1996) ArticleTitleModulation of honeybee thermoregulation by adrenergic compounds Neuroreport 7 IssueID10 1601–1604 Occurrence Handle8904764

    PubMed  Google Scholar 

  • M. N. Berry R. B. Gregory A. R. Grivell D. C. Henly J. W. Phillips P. G. Wallace (1989) The thermodynamic regulation of cellular metabolism and heat production W. Wieser E. Gnaiger (Eds) Energy Transformations in Cells and Organisms Georg Thieme Verlag NewYork 18–27

    Google Scholar 

  • A. C. Bianco J. E. Silva (1987a) ArticleTitleIntracelular conversion of thyroxine to triiodothyronine is required for the optimal thermogenic function of brown adipose tissue J. Clin. Invest. 79 295–300

    Google Scholar 

  • A. C. Bianco J. E. Silva (1987b) ArticleTitleOptimal response of key enzymes and uncoupling protein to cold in BAT depends on local T3 generation Am. J. Physiol. 253 E255–263

    Google Scholar 

  • J. E. P. W. Bicudo A. C. Bianco C. R. Vianna (2002) ArticleTitleAdaptative thermogenesis in hummingbirds J. Exp. Biol. 205 2267–2273 Occurrence Handle12110660

    PubMed  Google Scholar 

  • C. Blau G. Wegener (1994) ArticleTitleMetabolic integration in locust flight: the effect of octopamine on the glycolytic activator fructose 2,6-bisphosphate in flight muscle in vivo J. Comp. Physiol. B 164 11–15 Occurrence Handle10.1007/BF00714565

    Article  Google Scholar 

  • C. Blau G. Wegener D. J. Candy (1994) ArticleTitleThe effect of octopamine on the glycolytic activator fructose 2,6-bisphosphate in perfursed locust flight muscle Insect. Biochem. Mol. Biol. 24 677–683 Occurrence Handle10.1016/0965-1748(94)90055-8

    Article  Google Scholar 

  • W. Blenau A. Baumann (2001) ArticleTitleMolecular and pharmacological properties of insect biogenic amines receptors: lessons from Drosophila melanogaster and Apis mellifera Arch. Insect Biochem. Physiol. 48 13–38 Occurrence Handle10.1002/arch.1055 Occurrence Handle11519073

    Article  PubMed  Google Scholar 

  • G. Bloch D. E Wheeter G. E. Robinson (2002) Endocrine influences on the organization of insect societies D. W. Pfaff (Eds) Hormones, Brain and Behavior Academic Press San Diego, CA

    Google Scholar 

  • B. A. Block (1994) ArticleTitleThermogenesis in muscle Annu. Rev. Physiol. 56 535–577 Occurrence Handle10.1146/annurev.ph.56.030194.002535 Occurrence Handle8010751

    Article  PubMed  Google Scholar 

  • F. Bouillaud E. Couplan C. Pecqueur D. Ricquier (2001) ArticleTitleHomologues of the uncoupling protein from brown adipose tissue 1UCP1: UCP2. UCP3, BMCP1 and UCP4 Biochim. Biophys. Acta 1504 107–119 Occurrence Handle11239488

    PubMed  Google Scholar 

  • M. Bounias (1986) ArticleTitleNoradrenaline, propranolol and adrenochrome interactions with the dynamic of haemolymph lipids in worker honeybees Hom. Metab. Res. 18 804–810

    Google Scholar 

  • M. D. Brand (2000) ArticleTitleUncoupling to survive? The role of mitochondrial inefficiency in ageing Exp. Gerontol. 35 811–820 Occurrence Handle10.1016/S0531-5565(00)00135-2 Occurrence Handle11053672

    Article  PubMed  Google Scholar 

  • B. Cannon J. Nedergaard (2004) ArticleTitleBrown adipose tissue: function and physiological significance Physiol. Rev. 84 277–359 Occurrence Handle10.1152/physrev.00015.2003 Occurrence Handle14715917

    Article  PubMed  Google Scholar 

  • T. M. Casey C. P. Ellington (1989) Energetics of insect flight W. Weiser E. Gnaiger (Eds) Energy Transformation in Cells and Animals Stuttgart Thieme Stuttgart 200–210

    Google Scholar 

  • R. F. Chapman (1998) The Insects – Structure and Function EditionNumber4th Cambridge Univesity Press Cambridge

    Google Scholar 

  • M. G. Clark D. P. Bloxham P. C. Holland H. A. Laedy (1973) ArticleTitleEstimation of the fructose diphosphatase — phosphofructokinase substrate cycle in the flight muscle of Bombus affinisi Biochem. J. 134 589–597

    Google Scholar 

  • A. Collin R. D. Malheiros V. M. Moraes P. As ParticleVan V. M. Darras M. Taouis E. Decuypere J. Buyse (2003) ArticleTitleEffects of dietary macronutrient content on energy metabolism and uncoupling protein mRNA expression in broiler chickens Br. J. Nutr. 90 IssueID2 261–269 Occurrence Handle10.1079/BJN2003910 Occurrence Handle12908886

    Article  PubMed  Google Scholar 

  • M. J. Considine D. O. Daley J. Whelan (2001) ArticleTitleThe expression of alternative oxidase and uncoupling protein during fruit ripening in mango Plant Physiol. 126 1619–1629 Occurrence Handle10.1104/pp.126.4.1619 Occurrence Handle11500560

    Article  PubMed  Google Scholar 

  • J. Davenport (1992) Animal Life at Low Temperature Chapman and Hall London

    Google Scholar 

  • W. R. Dawson Hudson (1973) Birds G. C. Whittow (Eds) Comparative Physiology of Thermoregulation Academic Press New York

    Google Scholar 

  • A. M. Diehl J. B. Hoek (1999) ArticleTitleMitochondrial uncoupling: role of uncoupling protein anion carriers and relationship to thermo-genesis and weight control “the benefits of losing control J. Bioenerg. Biomembr. 31 493–506 Occurrence Handle10.1023/A:1005452624640 Occurrence Handle10653477

    Article  PubMed  Google Scholar 

  • C. Duch H. J. Pfluger (1999) ArticleTitleDUM neurons in locust flight: a model system for amine-mediated peripheral adjustments to a central motor program J. Comp. Physiol. A 184 489–499 Occurrence Handle10.1007/s003590050349

    Article  Google Scholar 

  • R. Dudley (1998) ArticleTitleAtmospheric oxygen, giant Paleozoic insects and the evolution of aerial locomotor performance J. Exp. Biol. 201 1043–1050 Occurrence Handle9510518

    PubMed  Google Scholar 

  • E. Dumonteil H. Barre G. Meissner (1995) ArticleTitleExpression of sarcoplasmatic reticulum Ca2+ transport proteins in cold-acclimating ducklings Am. J. Physiol. 269 955–960

    Google Scholar 

  • C. Durst S. Eichmuller R. Menzel (1994) ArticleTitleDevelopment and experience lead to increased volume of subcompartments of the honeybee mushroom body Behav. Neural. Biol. 62 259–263 Occurrence Handle7857249

    PubMed  Google Scholar 

  • M. M Elekonich D. J. Schulz G. Bloch G. E. Robinson (2001) ArticleTitleJuvenile hormone leveis in honey bee (Apis mellifera L.) foragers: foraging experience and diurnal variation J. Insect Physiol. 47 1119–1125 Occurrence Handle10.1016/S0022-1910(01)00090-7 Occurrence Handle12770189

    Article  PubMed  Google Scholar 

  • C. P. Ellington (1985) ArticleTitlePower and efficiency of insect flight muscle J. Exp. Biol. 115 293–304 Occurrence Handle4031771

    PubMed  Google Scholar 

  • H. Esch F. Goller B. Heinrich (1991) ArticleTitleHow do bees shiver? Naturwissenschaften 78 325–328 Occurrence Handle10.1007/BF01221422

    Article  Google Scholar 

  • P. D. Evans (1980) ArticleTitleBiogenic amines in the insect nervous system Adv. Insect Physiol. 15 417–473

    Google Scholar 

  • P. D. Evans (1985) Octopamine G. A. Kerkut L. I. Gilbert (Eds) Comprehensive Insect Physiology, Biochemistry, and Pharmacology NumberInSeries 11 Pharmacology, Pergamon Press Oxford 4990–530

    Google Scholar 

  • P. D. Evans (1993) Molecular studies on insect octopamine receptors Y. Pichon (Eds) Comparative Molecular Neurobiology Birkhauser Basel 286–296

    Google Scholar 

  • C. M. Evock-Clover S. M. Poch M. P. Richards C. M. Ashwell J. P. McMurtry (2002) ArticleTitleExpression of an uncoupling protein gene homolog in chickens Comp. Biochem. Physiol. A Mol. Integr. Physiol. 133 IssueID2 345–358 Occurrence Handle10.1016/S1095-6433(02)00113-7 Occurrence Handle12208305

    Article  PubMed  Google Scholar 

  • S. E. Fahrbach (1997) ArticleTitleRegulation of age polyethism in bees and wasps by juvenile hormone Adv. Study Behav. 26 285–316

    Google Scholar 

  • S. E. Fahrbach T. Giray S. M. Farris G. E. Robinson (1997) ArticleTitleExpansion of the neuropil of the mushroom bodies in male honeybees is coincident with initiation of flight Neurosci. Lett. 236 IssueID3 135–138 Occurrence Handle10.1016/S0304-3940(97)00772-6 Occurrence Handle9406755

    Article  PubMed  Google Scholar 

  • S. E. Fahrbach T. Giray G. E. Robinson (1995) ArticleTitleVolume changes in the mushroom bodies of adult honey bee queens Neurobiol. Learn. Mem. 63 181–191 Occurrence Handle10.1006/nlme.1995.1019 Occurrence Handle7663892

    Article  PubMed  Google Scholar 

  • C. Fleury M. Neverova S. Collins S. Raimbault O. Champigny C. Levi-Mcyrucis F. Bouillaud M. F. Seldin R. S. Surwit D. Ricquier. C. H. Warden (1997) ArticleTitleUncoupung protein−2: a novel gene linked to obesity and hyperinsulinemia Nat. Genet. 15 269–272 Occurrence Handle10.1038/ng0397-269 Occurrence Handle9054939

    Article  PubMed  Google Scholar 

  • Françoso-Júnior, O. A. (1999) Estudo comparativo do metabolismo aeróbico de Melipona bicolor Lepeletier (Hymenoptera: Apidae: Meliponinae). PhD Dissertation, Bioscience Institute, University of São Paulo

  • Y. C. Fridell A. Sanches-Blanco B. A. Silvia S. L. Helfand (2004) ArticleTitleFunctional characterization of a Drosophila mitochondrial uncoupling protein J. Bioenerg. Biomembr. 36 IssueID3 219–228 Occurrence Handle10.1023/B:JOBB.0000031973.20153.c6 Occurrence Handle15337852

    Article  PubMed  Google Scholar 

  • J. Galitzky D. Langin P. Verwaerde J. L. Montastruc M. Lafontan M. Berlan (1997) ArticleTitleLipolytic effects of conventional beta 3-adrenoceptor agonists and of CGP 12,177 in rat and human fat cells: preliminary pharmacological evidence for a putative beta 4-adrenoceptor Br. J. Pharmacol. 122 1244–1250 Occurrence Handle10.1038/sj.bjp.0701523 Occurrence Handle9401793

    Article  PubMed  Google Scholar 

  • T. Giray G. E. Rohinson (1996) ArticleTitleCommon endocrine and genetic mechanisms of behavioral development in male and worker honey bees and the evolution of division of labor Proc. Natl. Acad. Sci. USA 93 11718–11722 Occurrence Handle10.1073/pnas.93.21.11718 Occurrence Handle8876203

    Article  PubMed  Google Scholar 

  • D. W. Gong Y. He M. Karas M. Reitman (1997) ArticleTitleUncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, beta3-adrenergic agonists and leptin J. Biol. Chem. 272 24129–24132 Occurrence Handle10.1074/jbc.272.39.24129 Occurrence Handle9305858

    Article  PubMed  Google Scholar 

  • M. W. Goosey D. J. Candy (1982) ArticleTitleThe release and removal of octopamine by tissues of the locust Schistocerca Americana gregaria Insect Biochem. 12 681–685 Occurrence Handle10.1016/0020-1790(82)90057-9

    Article  Google Scholar 

  • J. G. Granneman M. Burnazi Z. Zhu L. A. Schwamb (2003) ArticleTitleWhite adipose tissue contributes to UCP1-independent thermogenesis Am. J. Physiol. Endocrinol. Metab. 285 IssueID6 E1230–E1236 Occurrence Handle12954594

    PubMed  Google Scholar 

  • L. Grohmann W. Blenau J. Erber P. R. Ebert T. Strunker A. Baumann (2003) ArticleTitleMolecular and functional characterization of an octopamine receptor from honeybee (Apis mellifera) brain J. Neurochem. 86 IssueID3 725–735 Occurrence Handle10.1046/j.1471-4159.2003.01876.x Occurrence Handle12859685

    Article  PubMed  Google Scholar 

  • D. Grujic V. S. Susulic M. E. Harper J. Himms-Hagen B. A. Cunningham B. E. Corkey B. B. Lowell (1997) ArticleTitleBeta3-adrenergic receptors on white and brown adipocytes mediate beta3-selective agonist-induced effects on energy expenditure, insulin secretion, and food intake: a study using transgenic and gene knockout mice J. Biol. Chem. 272 17686–17693 Occurrence Handle10.1074/jbc.272.28.17686 Occurrence Handle9211919

    Article  PubMed  Google Scholar 

  • A. C. Guyton J. E. Hall (1996) Textbook of Medical Physiology Saunders Philadelphia

    Google Scholar 

  • P. Hanak P. Jezek (2001) ArticleTitleMitochondrial uncoupling proteins and phylogenesis – UCP4 as the ancestral uncoupling protein FEBS Lett. 495 137–141 Occurrence Handle10.1016/S0014-5793(01)02338-9 Occurrence Handle11334880

    Article  PubMed  Google Scholar 

  • J. Harrison (1986) ArticleTitleCaste-specific changes in honeybee flight capacity Physiol. Zoo./ 59 175–187

    Google Scholar 

  • J. F. Harrison J. H. Fewell (2002) ArticleTitleEnvironmental and genetic influences on flight metabolic rate in the honeybee Apis mellifera Comp. Biochem. Physiol. 133A 323–333

    Google Scholar 

  • K. Hartfelder (2000) ArticleTitleInsect juvenile hormone: from ``status quo” to high society Braz. J.Med. Biol. Res. 33 157–177 Occurrence Handle10.1590/S0100-879X2000000200003 Occurrence Handle10657056

    Article  PubMed  Google Scholar 

  • J. E. Heath R. K. Josephson (1970) ArticleTitleBody temperature and singing in the katydid, , Neoconocephalus robustus (Orthoptera, Tetragoniidae) Biol. Bull. 138 272–285

    Google Scholar 

  • B. Heinrich (1970) ArticleTitleThoracic temperature stabilization by blood circulation in a free-flying moth Science 168 580–582

    Google Scholar 

  • B. Heinrich (1972) ArticleTitleEnergetics of temperature regulation and foraging in a bumblebee, Bambus terricola Kirby J. Comp. Physiol. 77 49–64 Occurrence Handle10.1007/BF00696519

    Article  Google Scholar 

  • B. Heinrich (1974) ArticleTitleThermoregulation in endothermic insects Science 185 747–756 Occurrence Handle4602075

    PubMed  Google Scholar 

  • B. Heinrich (1975) ArticleTitleThermoregulation in bumblebees. II. Energetics of warm-up and free flight J. Comp. Physiol. 96 155–166

    Google Scholar 

  • B. Heinrich (1976) ArticleTitleMechanisms of heat exchange between thorax and abdomen in bumblebees J. Exp. Biol. 64 561–585 Occurrence Handle945321

    PubMed  Google Scholar 

  • B. Heinrich (1979) ArticleTitleKeeping a cool head: honeybee thermoregulation Science 205 269–271

    Google Scholar 

  • B. Heinrich (1993) Hot-blooded Insects: Strategies and Mechanisms of Thermoregulation Springer-Verlag Berlin

    Google Scholar 

  • R. C. Herold (1965) ArticleTitleDevelopment and ultrastructural changes of sarcosomes during honey bee flight muscle development Dev. Biol. 12 269–286 Occurrence Handle10.1016/0012-1606(65)90031-X Occurrence Handle5884146

    Article  PubMed  Google Scholar 

  • R. C. Herold H. Borei (1963) ArticleTitleCytochrome changes during honey bee flight muscle development Dev. Biol. 8 67–79 Occurrence Handle10.1016/0012-1606(63)90026-5

    Article  Google Scholar 

  • J. Hinuns-Hagen (1990) ArticleTitleBrown adipose tissue thennogenesis: inter-disciplinary studies FASEB J. 4 2890–2898 Occurrence Handle2199286

    PubMed  Google Scholar 

  • C. Hioki T. Yoshida A. Kogure Y. Takakura T. Umekawa K. Yoshioka A. Shimatsu T. Yoshikawa (2004) ArticleTitleEffects of growth hormone (GH) on mRNA levels of uncoupling proteins 1,2, and 3 in brown and white adipose tissues and skeletal muscle in obese mice Horm. Metab. Res. 36 IssueID9 607–613 Occurrence Handle10.1055/s-2004-825905 Occurrence Handle15486811

    Article  PubMed  Google Scholar 

  • P. Hochachka G. N. Somero (1984) Biochemical Adaptation Princeton University Press Preinceton

    Google Scholar 

  • P. Hochachka G. N. Somero (2002) Biochemical Adaptation – Mechanisms and Processes in Physiological Evolution Oxford University Press Oxford

    Google Scholar 

  • H. Hoppeler S. L. Lindstedt (1985) ArticleTitleMalleability of skeletal muscle in overcoming limitations: structural elements J. Exp. Biol. 115 355–364 Occurrence Handle4031775

    PubMed  Google Scholar 

  • G. Horseman R. Hartman M. Virant-Doberlet W. Loher F. Huber (1994) ArticleTitleNervous control of juvenile hormone biosysnthesis in Locusta migratoria Proc. Nat. Acad. Sci. USA 91 2960–2964 Occurrence Handle8159687

    PubMed  Google Scholar 

  • A. J. Hulbert (2000) ArticleTitleThyroid hormones and their effects: a new perspective Biol. Rev. 75 519–631 Occurrence Handle10.1017/S146479310000556X Occurrence Handle11117200

    Article  PubMed  Google Scholar 

  • Z. -Y. Huang G. E. Robinson D. W. Borst (1994) ArticleTitlePhysiological correlates of division of labor among similarly aged honey bees J. Comp. Physiol. A 174 731–739 Occurrence Handle10.1007/BF00192722 Occurrence Handle8014920

    Article  PubMed  Google Scholar 

  • O. Jassim Z. Y. Huang G. E. Robinson (2000) ArticleTitleJuvenile hormone profiles of worker honey bees,, Apis mellifera, during normal and accelerated behavioural development J. Insect Physiol. 46 243–249 Occurrence Handle10.1016/S0022-1910(99)00176-6 Occurrence Handle12770228

    Article  PubMed  Google Scholar 

  • W. Jarmuszkiewicz C. M. Sluse-Goffart L. Hryniewiecka F. E. Sluse (1999) ArticleTitleIdentification and characterization of a protozoan uncoupling protein in Acanthamoeba castellanii J. Biol. Chem. 274 IssueID33 23198–23202 Occurrence Handle10.1074/jbc.274.33.23198 Occurrence Handle10438491

    Article  PubMed  Google Scholar 

  • W. Jarmuszkiewicz N. Antos A. Swida M. Czarna F. E. Sluse (2004) ArticleTitleThe effect of growth at low temperature on the activity and expression of the uncoupling protein in Acanthamoeba castellanii mitochondria FEBS Lett. 569 IssueID1–3 178–184 Occurrence Handle10.1016/j.febslet.2004.05.046 Occurrence Handle15225630

    Article  PubMed  Google Scholar 

  • P. Jezek (2002) ArticleTitlePossible physiological roles of mitochondrial uncoupling proteins—UCP Int. J. Biochem. Cell. Biol. 34 1190–1206 Occurrence Handle10.1016/S1357-2725(02)00061-4 Occurrence Handle12127570

    Article  PubMed  Google Scholar 

  • R. K. Josephson (1981) Temperature and the mechanical performance of insect muscle B. Heinrich (Eds) Insect Thermoregulation Wiley-Interscience Publication New York

    Google Scholar 

  • A. Kaatz S. Eichmulkr U. S. Kreiss (1994) ArticleTitleStimulatory effect of octopamine on Juvenile hormone biosynthesis in honey bees (Apis mellifera): physiological and immunocytochemical evidence J. Insect Physiol. 40 865–872 Occurrence Handle10.1016/0022-1910(94)90020-5

    Article  Google Scholar 

  • Y. Kagawa S. H. Chá K. Hasegawa T. Hamamoto H. Endo (1999) ArticleTitleRegulation of energy metabolism in human cells in aging and diabetes Biochem. Biophys. Res. Commun. 266 662–676 Occurrence Handle10.1006/bbrc.1999.1884 Occurrence Handle10603304

    Article  PubMed  Google Scholar 

  • K. Kajimoto N. Yamazaki M. Kataoka H. Terada Y. Shinohara (2004) ArticleTitleIdentification of possible protein machinery involved in the thermogenic function of brown adipose tissue J. Med. Invest. 51 IssueID1–2 20–28 Occurrence Handle10.2152/jmi.51.20 Occurrence Handle15000252

    Article  PubMed  Google Scholar 

  • A. E. Kammer (1981) Physiological mechanisms of thermoregulation B. Heinrich (Eds) Insect Thermoregulation Wiley-Interscience Publication New York

    Google Scholar 

  • A. J. Kaumann (1997) ArticleTitleFour beta-adrenoceptor subtypes in the mammalian heart Trends Pharmacol. Sci. 18 70–76 Occurrence Handle10.1016/S0165-6147(96)01033-4 Occurrence Handle9133774

    Article  PubMed  Google Scholar 

  • J. G. Kingsolver M. A. R. Koehl (1985) ArticleTitleAerodynamics, thermoregulation and the evolution of insect wings: differential scaling and evolutionary change Evolution 39 488–504

    Google Scholar 

  • J. G. Kingsolver M. A. R. Koehl (1994) ArticleTitleSelective factors in the evolution of insect wings A. Rev. Ent. 39 425–451 Occurrence Handle10.1146/annurev.en.39.010194.002233

    Article  Google Scholar 

  • M. Laloi M. Klein J. W. Ricsraeicr B. MuDer-Rober C. Fleury F. Bouillaud D. Ricquier (1997) ArticleTitleA plant cold-induced uncoupling protein Nature 389 135–136 Occurrence Handle10.1038/38156 Occurrence Handle9296489

    Article  PubMed  Google Scholar 

  • M. Liebig C. Praun ParticleVon G. Heldmaier M. Klingenspor (2004) ArticleTitleAbsence of UCP3 in brown adipose tissue does not impair nonshivering thermogenesis Physiol. Biochem. Zool. 77 IssueID1 116–126 Occurrence Handle10.1086/381464 Occurrence Handle15057722

    Article  PubMed  Google Scholar 

  • O. Lindberg J. DePierre E. Rylander B. A. Afzelius (1967) ArticleTitleStudies of the mitochondrial energy-transfer system of brown adipose tissue J. Cell. Biol. 34 293–310 Occurrence Handle10.1083/jcb.34.1.293 Occurrence Handle6033537

    Article  PubMed  Google Scholar 

  • W. Mao X. X. Yu A. Zhong W. Li J. Brush S. W. Sherwood S. H. Adams G. Pan (1999) ArticleTitleUCP4, a novel brain-specific mitochondrial protein that reduces membrane potential in mammalian cells FEBS Lett. 443 326–330 Occurrence Handle10.1016/S0014-5793(98)01713-X Occurrence Handle10025957

    Article  PubMed  Google Scholar 

  • K. Maruyama K. Moriwaki (1958) ArticleTitleRespiratory enzyme systems and muscular function in honeybee thoracic muscle Enzymologia 19 211–219 Occurrence Handle13562038

    PubMed  Google Scholar 

  • A. Matthias K. E. B. Ohlson J. M. Fredriksson A. Jacobsson J. Nedergaard B. Cannon (2000) ArticleTitleThermogenic responses in brown-fat cells are fully UCP1-dependent: UCP2 or UCP3 do not substitute for UCP1 in adrenergically or fatty-acid induced thermogenesis J. Biol. Chem. 275 25073–25081 Occurrence Handle10.1074/jbc.M000547200 Occurrence Handle10825155

    Article  PubMed  Google Scholar 

  • M. L. May (1976) ArticleTitleThermoregulation and adaptation to temperature in dragonflies (Odonata: Anisoptera) Ecol. Monogr. 46 1–32

    Google Scholar 

  • T. Mentel C. Duch H. Stypa G. Wegener U. Muller H. J. Pfluger (2003) ArticleTitleCentral modulatory neurons control fuel selection in flight muscle of migratory locust J. Neurosci. 23 IssueID4 1109–1113 Occurrence Handle12598597

    PubMed  Google Scholar 

  • A. R. Mercer P. G. Mobbs A. P. Davenport P. D. Evans (1983) ArticleTitleBiogenic amines in the brain of the honeybee Apis mellifera Cell Tissue Res. 234 655–677 Occurrence Handle10.1007/BF00218658 Occurrence Handle6420063

    Article  PubMed  Google Scholar 

  • G. Mory D. Ricquier P. Pesquies P. Hemon (1981) ArticleTitleEffects of hypothyroidism on the brown adipose tissue of adult rats; comparison with the effects of adaptation to cold J. Endocrinol. 91 515–524 Occurrence Handle7328374

    PubMed  Google Scholar 

  • E. A. Newsholme B. Crabtree S. J. Higgins S. D. Thornton C. Start (1972) ArticleTitleThe activities of fructose diphosphatase in flight muscles from the bumblebee and the role of this enzyme in heat generation Biochem. J. 128 89–97 Occurrence Handle4343671

    PubMed  Google Scholar 

  • H. F. Nijhout (1994) Insect Hormones Princeton University Press Princeton

    Google Scholar 

  • F. Nijkamp P. Engels A. Henricks A. J. Oosterhout ParticleVan (1992) ArticleTitleMechanisms of beta-adrenergic receptor regulation in lungs and its implications for physiological responses Physiol. Rev. 72 323–367 Occurrence Handle1313586

    PubMed  Google Scholar 

  • D. O. Norris (1997) Vertebrate Endocrinology EditionNumber3rd Academic Press New York

    Google Scholar 

  • V. J. A. Novak (1966) Insect Hormones Methuen and Co. Ltd London

    Google Scholar 

  • J. H. Oppenheimer H. L. Schwartz J. T. Lane M. P. Thompson (1991) ArticleTitleFunctional relationship thyroid hormone-induced lipogenesis, lipolysis, and thermogenesis in the rat J. Clin. Invest. 87 125–132 Occurrence Handle1985090

    PubMed  Google Scholar 

  • I. Orchard B. G. Loughton (1981) ArticleTitleIs octopamine a transmitter mediating hormone release in insects? J. Neurobiol. 12 IssueID2 143–153 Occurrence Handle10.1002/neu.480120204 Occurrence Handle6260893

    Article  PubMed  Google Scholar 

  • I. Orchard J. M. Ramirez A. B. Lange (1993) ArticleTitleA multifunctional role for octopamine in locust flight Annu. Rev. Entomol. 38 227–249 Occurrence Handle10.1146/annurev.en.38.010193.001303

    Article  Google Scholar 

  • F. Preitner P. Muzzin J. P. Revelli J. Seydoux J. Galitzky M. Berlan M. Lafontan J. P. Giacobino (1998) ArticleTitleMetabolic response to various beta-adrenoceptor agonists in beta 3−adrenoceptor knockout mice: evidence for a new beta – adrenergic receptor in brown adipose tissue Br. J. Pharmacol. 124 1684–1688 Occurrence Handle10.1038/sj.bjp.0702007 Occurrence Handle9756384

    Article  PubMed  Google Scholar 

  • S. B Prusiner B. Cannon T. M. Ching O. Lindberg (1968) ArticleTitleOxidative metabolism in cells isolated from brown adipose tissue – Catecholamine-regulated respiratory control Eur. J. Biochem. 7 51–57 Occurrence Handle10.1111/j.1432-1033.1968.tb19572.x Occurrence Handle5707712

    Article  PubMed  Google Scholar 

  • S. Raimbault S. Dridi F. Denjean J. Lachuer E. Couplan F. Bouillaud A. Bordas C. Duchamp M. Taouis D. Ricquier (2001) ArticleTitleAn uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds Biochem. J. 353 441–444 Occurrence Handle10.1042/0264-6021:3530441 Occurrence Handle11171038

    Article  PubMed  Google Scholar 

  • D. Randall W. Burggren K. French (1997) Animal Physiology EditionNumber4th W. H. Freeman and Company, New York

    Google Scholar 

  • M. A. Rankin (1989) Hormonal control of flight G. J. Goldsworthy C. H. Wheeler (Eds) Insect Flight CRC Press Boca Raton 139–163

    Google Scholar 

  • L. L. Restifo K. White (1990) ArticleTitleMolecular and genetic approaches to neurotransmitter and neuromodulator systems in Drosophila Adv. Insect Physiol. 22 115–119

    Google Scholar 

  • G. Riccioni V. Mennla M. S. Lambo R. Della Vecchia C. Ílio ParticleDi A. Lorenzo ParticleDe N. D’Orazio (2004) ArticleTitleLeptin and hypothalamus-hypophysis-thyroid axis Clin. Ter. 155 IssueID1 29–31 Occurrence Handle15147079

    PubMed  Google Scholar 

  • D. Ricquier F. Bouillaud (2000) ArticleTitleThe uncoupling protein homologues: UCP1. UCP2, UCP3. StUCP and AtUCP Biochem. J. 345 161–179 Occurrence Handle10.1042/0264-6021:3450161 Occurrence Handle10620491

    Article  PubMed  Google Scholar 

  • G. E. Robinson (1987) Hormonal regulation of age polyethism in the honeybee, Apis mellifera R. Menzel A. Mercer (Eds) Neurobiology and Behavior of Honeybees Springer-Verlag Berlin 266–279

    Google Scholar 

  • G. E. Robinson J. R. E. Page C. Strambi A. Strambi (1989) ArticleTitleHormonal and genetic control of behavioral integration in honey bee colonies Science 246 109–112

    Google Scholar 

  • G. E. Robinson C. Strambi M. F. Feldlaufer (1991) ArticleTitleComparision of juvenile hormone and ecdysteroid hemolymph titers in adult worker and queen honey bees (Apis mellifera) J. Insect Physiol. 37 929–935 Occurrence Handle10.1016/0022-1910(91)90008-N

    Article  Google Scholar 

  • G. E. Robinson (2002) ArticleTitleGenomics and integrative analyses of division of labor in honeybee colonies Am. Nat. 160 S160–S172 Occurrence Handle10.1086/342901

    Article  Google Scholar 

  • T. Roeder (1995) ArticleTitlePharmacology of the octopamine receptor from locust central nervous tissue (OAR3) Br. J. Pharmacol. 114 210–216 Occurrence Handle7712020

    PubMed  Google Scholar 

  • T. Roeder (1999) ArticleTitleOctopamine in invertebrates Prog. Neurobiol. 59 533–561 Occurrence Handle10.1016/S0301-0082(99)00016-7 Occurrence Handle10515667

    Article  PubMed  Google Scholar 

  • A. K. Salm K. D. McCarthy (1992) ArticleTitleThe evidence for astrocytes as a target for central noradrenergic activity: expression of adrenergic receptors Brain. Res. Bull. 29 265–275 Occurrence Handle10.1016/0361-9230(92)90056-4 Occurrence Handle1393601

    Article  PubMed  Google Scholar 

  • D. Sanchis C. Fleury N. Choraϊki M. Goubern Q. Huang M. Nevcrova F. Gregoire J. Easlick S. Raimbault C. Levi-Meyrueis B. Miroux S. Collins M. Seldin D. Richard C Warden F. Bouillaud D. Ricquier (1998) ArticleTitleBMCP1, a novel mitochondrial carrier with high expression in the central nervous system of humans and rodents, and respiration uncoupling activity in recombinant yeast J. Biol. Chem. 273 34611–34615 Occurrence Handle10.1074/jbc.273.51.34611 Occurrence Handle9852133

    Article  PubMed  Google Scholar 

  • R. Scheiner S. Pluckhahn B. Oney W. Blenau J. Erber (2002) ArticleTitleBehavioural pharmacology of octopamine,, tyramine and dopamine in honey bees Behav. Brain Res. 136 545–553 Occurrence Handle10.1016/S0166-4328(02)00205-X Occurrence Handle12429417

    Article  PubMed  Google Scholar 

  • P. Schrauwen M. Hesselink (2002) ArticleTitleUCP2 and UCP3 in muscle controlling body metabolism J. Exp. Biol. 205 2275–2285 Occurrence Handle12110661

    PubMed  Google Scholar 

  • D. J. Schulz G. E. Robinson (1999) ArticleTitleBiogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies J. Comp. Physiol. A 184 481–488 Occurrence Handle10.1007/s003590050348 Occurrence Handle10377981

    Article  PubMed  Google Scholar 

  • D. J. Schulz Z. Y. Hnang G. E. Robinson (1998) ArticleTitleEffects of colony food shortage on behavioral development in honey bees Behav. Ecol. Sociobiol. 42 295–303 Occurrence Handle10.1007/s002650050442

    Article  Google Scholar 

  • D. J. Schulz G. E. Robinson (2001) ArticleTitleOctopamine influences division of labor in honey bee colonies J. Comp. Physiol. A 187 53–61 Occurrence Handle10.1007/s003590000177 Occurrence Handle11318378

    Article  PubMed  Google Scholar 

  • D. J. Schulz M. M. Elekonich G. E. Robinson (2002a) ArticleTitleBiogenic amines in the antenna lobes and the initiation and maintenance of foraging behavior in honey bees J. Neurobiol. 54 406–416 Occurrence Handle10.1002/neu.10138

    Article  Google Scholar 

  • D. J. Schulz J. P. Sullivan G. E. Robinson (2002b) ArticleTitleJuvenile hormone and octopamine in the regulation of division of labor in honeybee colonies Horm. Behav. 42 IssueID2 222–231 Occurrence Handle10.1006/hbeh.2002.1806

    Article  Google Scholar 

  • J. Seydoux J. P. Giacobuio L. Giranuer. (1982) ArticleTitleImpaired metabolic response to nerve stimulation in brown adipose tissue of hypothyroid rats Mol. Cell. Endocrinol. 25 213–226 Occurrence Handle10.1016/0303-7207(82)90054-5 Occurrence Handle6276252

    Article  PubMed  Google Scholar 

  • J. E. Silva (1995) ArticleTitleThyroid hormone control of thermogenesis and energy balance Thyroid 5 481–492 Occurrence Handle8808101

    PubMed  Google Scholar 

  • J. E. Silva (2003) ArticleTitleThe thermogenic effect of thyroid hormone and its clinical implications Ann. Intern. Med. 139 205–213 Occurrence Handle12899588

    PubMed  Google Scholar 

  • R. Spiess U. Rose (2004) ArticleTitleJuvenile hormone-dependent motor activation in the adult locust Locusta migratoria J. Comp. Physiol. A 190 IssueID11 883–894

    Google Scholar 

  • J. F. Staples E. L. Koen T. M. Laverty (2004) ArticleTitle``Futile cycle” enzymes in the flight muscles of North American bumblebees J. Exp. Biol. 207 IssueIDPt 5 749–754 Occurrence Handle10.1242/jeb.00825 Occurrence Handle14747407

    Article  PubMed  Google Scholar 

  • G. Stepien M. Renaud I. Savre R. Durand (1988) ArticleTitleJuvenile hormone increases mitochondrial activities in Drosophila cells Insect Biochem. 18 313–321 Occurrence Handle10.1016/0020-1790(88)90096-0

    Article  Google Scholar 

  • R. K. Suarez C. D. Moyes (1992) ArticleTitleMitochondrial respiration in locust flight muscles J. Exp. Biol. 263 351–355

    Google Scholar 

  • J. P. Sullivan O. Jassim S. E. Fahrbach G. E. Robinson (2000) ArticleTitleJuvenile hormone paces behavioral development in the adult worker honeybee Horm. Behav. 37 1–14 Occurrence Handle10.1006/hbeh.1999.1552 Occurrence Handle10712853

    Article  PubMed  Google Scholar 

  • J. P. Sullivan S. E. Fahrbach J. F. Harrison E. A. Capaldi J. H. Fewell G. E. Robinson (2003) ArticleTitleJuvenile hormone and division of labor in honey bee colonies: effects of allatectomy on flight behavior and metabolism J. Exp. Biol. 206 2287–2296 Occurrence Handle10.1242/jeb.00432 Occurrence Handle12771177

    Article  PubMed  Google Scholar 

  • V. S. Susulic R. C. Frederich J. Lawitts E. Tozzo B. B. Kahn M. E. Harper J. Himms-Hagen J. S. Flier B. B. Lowell (1995) ArticleTitleTargeted disruption of the beta3-drenergic receptor gene J. Biol. Chem. 270 29483–29492 Occurrence Handle10.1074/jbc.270.49.29483 Occurrence Handle7493988

    Article  PubMed  Google Scholar 

  • C. S. Thompson K. J. Yagi Z. F. Chen S. S. Tobe (1990) ArticleTitleThe effects of octopamine on juvenile hormone biosynthesis,, electrophysiology, and cAMP content of the Corpora allata of the cockroach Diploptera punctata J. Comp. Physiol. B. 160 IssueID3 41–49 Occurrence Handle10.1007/BF00302589 Occurrence Handle2355116

    Article  PubMed  Google Scholar 

  • S. S. Tobe B. Stay (1985) ArticleTitleStructure and regulation of the Corpus allatum Adv. Insect Physiol. 18 305–432

    Google Scholar 

  • M. Toyomizu M. Ueda S. Sato Y. Seki K Sato Y. Akiba (2002) ArticleTitleCold-induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle FEBS Lett. 529 IssueID2–3 313–318 Occurrence Handle10.1016/S0014-5793(02)03395-1 Occurrence Handle12372620

    Article  PubMed  Google Scholar 

  • S. O. Tozetto A. Rachinsky W. Engels (1997) ArticleTitleJuvenile hormone promotes flight activity in drones (Apis mellifera carnica) Apidologie 28 77–84

    Google Scholar 

  • C. R. Vianna T. Hagen C. Y. Zhang E. Bachman O. Boss B. Gereben A. S. Moriscot B. B. Lowell J. E. P. W. Bicudo A. C. Bianco (2001) ArticleTitleCloning and functional characterization of an uncoupling protein homolog in hummingbirds Physiol. Genomics. 5 IssueID3 137–145 Occurrence Handle11285367

    PubMed  Google Scholar 

  • A. J. Vidal-Puig D. Grujic C. Y. Zhang T. Hagen O. Boss Y Ido A. Szczepanik J. Wade V. Mootha R. Cortright D. M. Muoio B. B. Lowell (2000) ArticleTitleEnergy metabolism in uncoupling protein 3 gene knockout mice J. Biol. Chem. 275 16258–16266 Occurrence Handle10.1074/jbc.M910179199 Occurrence Handle10748196

    Article  PubMed  Google Scholar 

  • R. T. Weirich H. L. Schwartz J. H. Oppenheimer (1987) ArticleTitleAn analysis of the interrelationship of nuclear and plasma triiodothyronine in the sea lamprey, lake trout, and rat: evolutionary considerations Endocrinology 120 664–677 Occurrence Handle3803297

    PubMed  Google Scholar 

  • G. Wegener R. Michel E. A. Newsholme (1986) ArticleTitleFructose 2,,6-bisphosphate as a signal for changing from sugar to lipid oxidation during flight in locusts FEBS Lett. 201 129–132 Occurrence Handle10.1016/0014-5793(86)80584-1

    Article  Google Scholar 

  • D. M. Wilson (1962) ArticleTitleBifunctional muscles in the thorax of grasshoppers J. Exp. Biol. 39 669–677

    Google Scholar 

  • G. S. Withers S. E. Fahrbach G. E. Robinson (1993) ArticleTitleSelective neuroanatomical plasticity and division of labour in the honeybee Nature 364 238–240 Occurrence Handle10.1038/364238a0 Occurrence Handle8321320

    Article  PubMed  Google Scholar 

  • G. S. Withers S. E. Fahrbach G. E. Robinson (1995) ArticleTitleEffects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees J. Neurobiol. 26 130–144 Occurrence Handle10.1002/neu.480260111 Occurrence Handle7714522

    Article  PubMed  Google Scholar 

  • T. R. F. Wright (1987) ArticleTitleThe genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster Adv. Genet. 24 127–222 Occurrence Handle3124532

    PubMed  Google Scholar 

  • G. R. Wyatt K. G. Davey (1996) ArticleTitleCellular and molecular actions of juvenile hormone. II. Roles of juvenile hormone in adult insects Adv. Insect Physiol. 26 2–155

    Google Scholar 

  • X. Q. Xiao K. L. Grove B. E. Grayson M. S. Smith (2004) ArticleTitleInhibition of uncoupling protein expression during lactation: role of leptin Endocrinology 145 IssueID2 830–838 Occurrence Handle10.1210/en.2003-0836 Occurrence Handle14605003

    Article  PubMed  Google Scholar 

  • A. J. Zera Z. Zhao (2004) ArticleTitleEffect of a juvenile hormone analogue on lipid metabolism in a wing-polymorphic cricket: implications for the endocrine-biochemical bases of life-history trade-offs Physiol. Biochem. Zool. 77 IssueID2 255–266 Occurrence Handle10.1086/383500 Occurrence Handle15095245

    Article  PubMed  Google Scholar 

  • J. Zhao L. Unelius T. Bengtsson B. Cannon J. Nedergaard (1994) ArticleTitleCoexisting beta–adrenoceptor subtypes: significance for thermogenic process in brown fat cells Am. J. Physiol. Cell. Physiol. 267 C969–C979

    Google Scholar 

  • Z. Zhao A. J. Zera (2002) ArticleTitleDifferential lipid biosynthesis underlies a tradeoff between reproduction and flight capability in a wing-polymorphic cricket Proc. Natl. Acad. Sci. USA 99 IssueID26 16829–16834 Occurrence Handle10.1073/pnas.262533999 Occurrence Handle12486227

    Article  PubMed  Google Scholar 

  • Z. Zhao A. J. Zera (2004) ArticleTitleThe hemolymph JH titer exhibits a large-amplitude, morph-dependent, diurnal cycle in the wing-polymorphic cricket, Gryllus firmus J. Insect. Physiol. 50 IssueID1 93–102 Occurrence Handle10.1016/j.jinsphys.2003.10.003 Occurrence Handle15037097

    Article  PubMed  Google Scholar 

  • A. Zorzano D. Bach S. Pich M. Palacin (2004) ArticleTitleRole of novel mitochondrial proteins in energy balance Rev. Med. Univ. Navarra 48 IssueID2 30–35 Occurrence Handle15382611

    PubMed  Google Scholar 

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Loli, D., Bicudo, J.E.P.W. Control and Regulatory Mechanisms Associated with Thermogenesis in Flying Insects and Birds. Biosci Rep 25, 149–180 (2005). https://doi.org/10.1007/s10540-005-2883-8

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