Pros and cons for the evidence of adaptive non-shivering thermogenesis in marsupials.
Adaptive non-shivering thermogenesis
Brown adipose tissue
Endothermy
Marsupials
Journal
Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology
ISSN: 1432-136X
Titre abrégé: J Comp Physiol B
Pays: Germany
ID NLM: 8413200
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
received:
19
11
2020
accepted:
22
02
2021
revised:
05
02
2021
pubmed:
17
4
2021
medline:
15
12
2021
entrez:
16
4
2021
Statut:
ppublish
Résumé
The thermogenic mechanisms supporting endothermy are still not fully understood in all major mammalian subgroups. In placental mammals, brown adipose tissue currently represents the most accepted source of adaptive non-shivering thermogenesis. Its mitochondrial protein UCP1 (uncoupling protein 1) catalyzes heat production, but the conservation of this mechanism is unclear in non-placental mammals and lost in some placentals. Here, we review the evidence for and against adaptive non-shivering thermogenesis in marsupials, which diverged from placentals about 120-160 million years ago. We critically discuss potential mechanisms that may be involved in the heat-generating process among marsupials.
Identifiants
pubmed: 33860348
doi: 10.1007/s00360-021-01362-0
pii: 10.1007/s00360-021-01362-0
pmc: PMC8572181
doi:
Substances chimiques
Mitochondrial Proteins
0
Uncoupling Protein 1
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1085-1095Informations de copyright
© 2021. The Author(s).
Références
Andreyev AY, Bondareva TO, Dedukhova VI, Mokhova EN, Skulachev VP, Volkov NI (1988) Carboxyatreactylate inhibits the uncoupling effect of free fatty acids. FEBS Lett 226:265–269. https://doi.org/10.1016/0014-5793(88)81436-4
doi: 10.1016/0014-5793(88)81436-4
Andreyev AY, Bondareva TO, Dedukhova VI, Mokhova EN, Skulachev VP, Tsofina LM, Volkov NI, Vygodina TV (1989) The ATP/ADP-antiporter is involved in the uncoupling effect of fatty acids on mitochondria. Eur J Biochem 182:585–592. https://doi.org/10.1111/j.1432-1033.1989.tb14867.x
doi: 10.1111/j.1432-1033.1989.tb14867.x
Aquila H, Link TA, Klingenberg M (1985) The uncoupling protein from brown fat mitochondria is related to the mitochondrial ADP/ATP carrier. analysis of sequence homologies and of folding of the protein in the membrane. EMBO J 4:2369–2376. https://doi.org/10.1002/j.1460-2075.1985.tb03941.x
doi: 10.1002/j.1460-2075.1985.tb03941.x
Bouillaud F, Ricquier D, Thibault J, Weissenbach J (1985) Molecular approach to thermogenesis in brown adipose tissue: CDNA cloning of the mitochondrial uncoupling protein. Proc Natl Acad Sci USA 82:445–448. https://doi.org/10.1073/pnas.82.2.445
doi: 10.1073/pnas.82.2.445
Brander F, Keith JS, Trayhurn P (1993) A 27-mer oligonucleotide probe for the detection and measurement of the mRNA for uncoupling protein in brown adipose tissue of different species. Comp Biochem Physiol B Comp Biochem 104:125–131. https://doi.org/10.1016/0305-0491(93)90348-9
doi: 10.1016/0305-0491(93)90348-9
Brashears JA, DeNardo DF (2013) Revisiting python thermogenesis: Brooding burmese pythons (Python bivittatus) cue on body, not clutch, temperature. J Herpetol 47:440–444. https://doi.org/10.1670/12-050
doi: 10.1670/12-050
Campbell KL, Dicke AA (2018) Sarcolipin makes heat, but is it adaptive thermogenesis? Front Physiol. https://doi.org/10.3389/fphys.2018.00714
doi: 10.3389/fphys.2018.00714
Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359. https://doi.org/10.1152/physrev.00015.2003
doi: 10.1152/physrev.00015.2003
Carey F (1982) A brain heater in the swordfish. Science 216:1327–1329. https://doi.org/10.1126/science.7079766
doi: 10.1126/science.7079766
Carey FG, Teal JM (1966) Heat conservation in tuna fish muscle. Proc Natl Acad Sci USA 56:1464–1469
doi: 10.1073/pnas.56.5.1464
Carey FG, Teal JM (1969) Mako and porbeagle: warm-bodied sharks. Comp Biochem Physiol 28:199–204. https://doi.org/10.1016/0010-406X(69)91335-8
doi: 10.1016/0010-406X(69)91335-8
Casey JP, James MC, Williard AS (2014) Behavioral and metabolic contributions to thermoregulation in freely swimming leatherback turtles at high latitudes. J Exp Biol 217:2331–2337. https://doi.org/10.1242/jeb.100347
doi: 10.1242/jeb.100347
Clements F, Hope P, Daniels C, Chapman I, Wittert G (1998) Thermogenesis in the marsupial Sminthopsis crassicaudata: effect of catecholamines and diet. Aust J Zool 46:381–390. https://doi.org/10.1071/zo98022
doi: 10.1071/zo98022
Cortés PA, Franco M, Moreno-Gómez FN, Barrientos K, Nespolo RF (2014) Thermoregulatory capacities and torpor in the South American marsupial, Dromiciops gliroides. J Therm Biol 45:1–8. https://doi.org/10.1016/j.jtherbio.2014.07.003
doi: 10.1016/j.jtherbio.2014.07.003
Davenport J, Fraher J, Fitzgerald E, McLaughlin P, Doyle T, Harman L, Cuffe T (2009) Fat head: an analysis of head and neck insulation in the leatherback turtle (Dermochelys coriacea). J Exp Biol 212:2753–2759. https://doi.org/10.1242/jeb.026500
doi: 10.1242/jeb.026500
Dawson TJ, Olson JM (1988) Thermogenic capabilities of the opossum Monodelphis domestica when warm and cold-acclimated: Similarities between American and Australian marsupials. Comp Biochem Physiol A Physiol 89:85–91. https://doi.org/10.1016/0300-9629(88)91143-7
doi: 10.1016/0300-9629(88)91143-7
Foster DO, Frydman ML (1978) Nonshivering thermogenesis in the rat. II. Measurements of blood flow with microspheres point to brown adipose tissue as the dominant site of the calorigenesis induced by noradrenaline. Can J Physiol Pharmacol 56:110–122
doi: 10.1139/y78-015
Frair W, Ackman RG, Mrosovsky N (1972) Body temperature of Dermochelys coriacea: warm turtle from cold water. Science 177:791–793. https://doi.org/10.1126/science.177.4051.791
doi: 10.1126/science.177.4051.791
Fritsches KA, Brill RW, Warrant EJ (2005) Warm eyes provide superior vision in swordfishes. Curr Biol 15:55–58. https://doi.org/10.1016/j.cub.2004.12.064
doi: 10.1016/j.cub.2004.12.064
Gaudry MJ, Campbell KL (2017) Evolution of UCP1 transcriptional regulatory elements across the mammalian phylogeny. Front Physiol. https://doi.org/10.3389/fphys.2017.00670
doi: 10.3389/fphys.2017.00670
Gaudry MJ, Jastroch M, Treberg JR, Hofreiter M, Paijmans JLA, Starrett J, Wales N, Signore AV, Springer MS, Campbell KL (2017) Inactivation of thermogenic UCP1 as a historical contingency in multiple placental mammal clades. Sci Adv 15:e1602878
doi: 10.1126/sciadv.1602878
Gaudry MJ, Campbell KL, Jastroch M (2018) Evolution of UCP1. In: Pfeifer A, Klingenspor, M, Herzig S (eds) Brown adipose tissue, Handbook of Experimental Pharmacology, vol 251. Springer International Publishing, New York, pp 127–141. https://doi.org/10.1007/164_2018_116
Geiser F, Drury RL, McAllan BM, Wang DH (2003) Effects of temperature acclimation on maximum heat production, thermal tolerance, and torpor in a marsupial. J Comp Physiol B Biochem Syst Environ Physiol 173:437–442. https://doi.org/10.1007/s00360-003-0352-x
doi: 10.1007/s00360-003-0352-x
Golozoubova V, Hohtola E, Matthias A, Jacobsson A, Cannon B, Nedergaard J (2001) Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold. FASEB J 15:2048–2050. https://doi.org/10.1096/fj.00-0536fje
doi: 10.1096/fj.00-0536fje
Golozoubova V, Cannon B, Nedergaard J (2006) UCP1 is essential for adaptive adrenergic nonshivering thermogenesis. Am J Physiol Endocrinol Metab 291:E350–E357. https://doi.org/10.1152/ajpendo.00387.2005
doi: 10.1152/ajpendo.00387.2005
Greer AE, Lazell JD, Wright RM (1973) Anatomical evidence for a counter-current heat exchanger in the leatherback turtle (Dermochelys coriacea). Nature 244:181–181. https://doi.org/10.1038/244181a0
doi: 10.1038/244181a0
Harlow P, Grigg G (1984) Shivering thermogenesis in a brooding diamond python, Python spilotes spilotes. Copeia 1984:959. https://doi.org/10.2307/1445340
doi: 10.2307/1445340
Hayward JS, Lisson PA (1992) Evolution of brown fat: its absence in marsupials and monotremes. Can J Zool 70:171–179. https://doi.org/10.1139/z92-025
doi: 10.1139/z92-025
Heaton JM (1972) The distribution of brown adipose tissue in the human. J Anat 112:35–39
Heaton GM, Wagenvoord RJ, Kemp A, Nicholls DG (1978) Brown-adipose-tissue mitochondria: photoaffinity labelling of the regulatory site of energy dissipation. Eur J Biochem 82:515–521. https://doi.org/10.1111/j.1432-1033.1978.tb12045.x
doi: 10.1111/j.1432-1033.1978.tb12045.x
Heldmaier G (1971) Zitterfreie wärmebildung und körpergröe bei säugetieren. Z vergl Physiol 73(22):248
Himms-Hagen J, Triandafillou J, Begin-Heick N, Ghorbani M, Kates AL (1995) Apparent lack of beta 3-adrenoceptors and of insulin regulation of glucose transport in brown adipose tissue of guinea pigs. Am J Physiol Regul Integr Comp Physiol 268:R98–R104. https://doi.org/10.1152/ajpregu.1995.268.1.R98
doi: 10.1152/ajpregu.1995.268.1.R98
Hope PJ, Pyle D, Daniels CB, Chapman I, Horowitz M, Morley JE, Trayhurn P, Kumaratilake J, Wittert G (1997) Identification of brown fat and mechanisms for energy balance in the marsupial, Sminthopsis crassicaudata. Am J Physiol Regul Integr Comp Physiol 273:R161–R167. https://doi.org/10.1152/ajpregu.1997.273.1.R161
doi: 10.1152/ajpregu.1997.273.1.R161
Hughes DA, Jastroch M, Stoneking M, Klingenspor M (2009) Molecular evolution of UCP1 and the evolutionary history of mammalian non-shivering thermogenesis. BMC Evol Biol 9:4. https://doi.org/10.1186/1471-2148-9-4
doi: 10.1186/1471-2148-9-4
Jastroch M, Withers KW, Taudien S, Frappell PB, Helwig M, Fromme T, Hirschberg V, Heldmaier G, McAllan BM, Firth BT, Burmester T, Platzer M, Klingenspor M (2008) Marsupial uncoupling protein 1 sheds light on the evolution of mammalian nonshivering thermogenesis. Physiol Genom 32:161–169. https://doi.org/10.1152/physiolgenomics.00183.2007
doi: 10.1152/physiolgenomics.00183.2007
Jastroch M, Withers KW, Stoehr S, Klingenspor M (2009) Mitochondrial proton conductance in skeletal muscle of a cold-exposed marsupial, Antechinus flavipes, is unlikely to be involved in adaptive nonshivering thermogenesis but displays increased sensitivity toward carbon-centered radicals. Physiol Biochem Zool 82:447–454. https://doi.org/10.1086/603631
doi: 10.1086/603631
Jastroch M, Hirschberg V, Klingenspor M (2012) Functional characterization of UCP1 in mammalian HEK293 cells excludes mitochondrial uncoupling artefacts and reveals no contribution to basal proton leak. Biochim Biophys Acta Bioenerg 1817:1660–1670. https://doi.org/10.1016/j.bbabio.2012.05.014
doi: 10.1016/j.bbabio.2012.05.014
Jovanovic O, Pashkovskaya AA, Annibal A, Vazdar M, Burchardt N, Sansone A, Gille L, Fedorova M, Ferreri C, Pohl EE (2015) The molecular mechanism behind reactive aldehyde action on transmembrane translocations of proton and potassium ions. Free Radic Biol Med 89:1067–1076. https://doi.org/10.1016/j.freeradbiomed.2015.10.422
doi: 10.1016/j.freeradbiomed.2015.10.422
Kabat AP, Rose RW, Harris J, West AK (2003a) Molecular identification of uncoupling proteins (UCP2 and UCP3) and absence of UCP1 in the marsupial Tasmanian bettong, Bettongia gaimardi. Comp Biochem Physiol B Biochem Molec Biol 134:71–77. https://doi.org/10.1016/S1096-4959(02)00189-6
doi: 10.1016/S1096-4959(02)00189-6
Kabat AP, Rose RW, West AK (2003b) Non-shivering thermogenesis in a carnivorous marsupial, Sarcophilus harrisii, in the absence of UCP1. J Therm Biol 28:413–420. https://doi.org/10.1016/S0306-4565(03)00026-3
doi: 10.1016/S0306-4565(03)00026-3
Kaethner MM, Good BF (1975) Seasonal thyroid activity in the tammar wallaby, Macropus eugenii (Desmarest). Aust J Zool 23:363–369. https://doi.org/10.1071/zo9750363
doi: 10.1071/zo9750363
Loudon A, Rothwell N, Stock M (1985) Brown fat, thermogenesis and physiological birth in a marsupial. Comp Biochem Physiol 81A:815–819
doi: 10.1016/0300-9629(85)90912-0
Mall S, Broadbridge R, Harrison SL, Gore MG, Lee AG, East JM (2006) The presence of sarcolipin results in increased heat production by Ca
McManus JJ (1969) Temperature regulation in the Opossum, Didelphis marsupialis virginiana. J Mammalogy 50:550–558. https://doi.org/10.2307/1378782
doi: 10.2307/1378782
Morrissette JM (2003) Characterization of ryanodine receptor and Ca2+-ATPase isoforms in the thermogenic heater organ of blue marlin (Makaira nigricans). J Exp Biol 206:805–812. https://doi.org/10.1242/jeb.00158
doi: 10.1242/jeb.00158
Mzilikazi N, Jastroch M, Meyer CW, Klingenspor M (2007) The molecular and biochemical basis of nonshivering thermogenesis in an African endemic mammal, Elephantulus myurus. Am J Physiol Regul Integr Comp Physiol 293:R2120–R2127. https://doi.org/10.1152/ajpregu.00427.2007
doi: 10.1152/ajpregu.00427.2007
Nespolo RF, Bacigalupe LD, Sabat P, Bozinovic F (2002) Interplay among energy metabolism, organ mass and digestive enzyme activity in the mouse-opossum Thylamys elegans: the role of thermal acclimation. J Exp Biol 205:2687–2703
doi: 10.1242/jeb.205.17.2697
Nicol SC (1978) Non-shivering thermogenesis in the potoroo, Potorous tridactylus (Kerr). Comp Biochem Physiol C Comp Pharmacol 59:33–37. https://doi.org/10.1016/0306-4492(78)90008-4
doi: 10.1016/0306-4492(78)90008-4
Nicol SC, Pavlides D, Andersen NA (1997) Nonshivering thermogenesis in marsupials: absence of thermogenic response to β3-adrenergic agonists. Comp Biochem Physiol A Physiol 117:399–405. https://doi.org/10.1016/S0300-9629(96)00357-X
doi: 10.1016/S0300-9629(96)00357-X
Nicol SC, Andersen NA, Arnold W, Ruf T (2009) Rewarming rates of two large hibernators: comparison of a monotreme and a eutherian. J Therm Biol 34:155–159. https://doi.org/10.1016/j.jtherbio.2009.01.003
doi: 10.1016/j.jtherbio.2009.01.003
Oelkrug R, Heldmaier G, Meyer CW (2011) Torpor patterns, arousal rates, and temporal organization of torpor entry in wildtype and UCP1-ablated mice. J Comp Physiol B 181:137–145. https://doi.org/10.1007/s00360-010-0503-9
doi: 10.1007/s00360-010-0503-9
Oelkrug R, Goetze N, Meyer CW, Jastroch M (2014) Antioxidant properties of UCP1 are evolutionarily conserved in mammals and buffer mitochondrial reactive oxygen species. Free Radic Biol Med 77:201–216. https://doi.org/10.1016/j.freeradbiomed.2014.09.004
doi: 10.1016/j.freeradbiomed.2014.09.004
Oelkrug R, Polymeropoulos ET, Jastroch M (2015) Brown adipose tissue: physiological function and evolutionary significance. J Comp Physiol B 185:587–606
doi: 10.1007/s00360-015-0907-7
Opazo JC, Nespolo RF, Bozinovic F (1999) Arousal from torpor in the Chilean mouse-opposum (Thylamys elegans): does non-shivering thermogenesis play a role? Comp Biochem Physiol A Mol Integr Physiol 123:393–397. https://doi.org/10.1016/S1095-6433(99)00081-1
doi: 10.1016/S1095-6433(99)00081-1
Parker N, Vidal-Puig A, Brand MD (2008) Stimulation of mitochondrial proton conductance by hydroxynonenal requires a high membrane potential. Biosci Rep 28:83–88. https://doi.org/10.1042/BSR20080002
doi: 10.1042/BSR20080002
Polymeropoulos ET, Heldmaier G, Frappell PB, Mcallan BM, Withers KW, Klingenspor M et al (2012a) Phylogenetic differences of mammalian basal metabolic rate are not explained by mitochondrial basal proton leak. Proc R Soc B Biol Sci 279:185–193. https://doi.org/10.1098/rspb.2011.0881
doi: 10.1098/rspb.2011.0881
Polymeropoulos ET, Jastroch M, Frappell PB (2012b) Absence of adaptive nonshivering thermogenesis in a marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). J Comp Physiol B 182:393–401. https://doi.org/10.1007/s00360-011-0623-x
doi: 10.1007/s00360-011-0623-x
Renfree MB, Papenfuss AT, Deakin JE, Lindsay J, Heider T, Belov K, Rens W, Waters PD, Pharo EA, Shaw G et al (2011) Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. Genome Biol 12:R81. http://genomebiology.com/2011/12/8/R81
Reynolds W, Hulbert AJ (1982) Cold acclimation in a small dasyurid marsupial: Antechinus stuartii. In: Mosman AM (ed) Carnivorous marsupials. Royal Zoological Society, New South Wales, pp 279–283
Rose RW, Ikonomopoulou MP (2005) Shivering and non-shivering thermogenesis in a marsupial, the eastern barred bandicoot (Perameles gunnii). J Therm Biol 30:85–92. https://doi.org/10.1016/j.jtherbio.2004.07.006
doi: 10.1016/j.jtherbio.2004.07.006
Rose RW, West AK, Ye J, McCormack GH, Colquhoun EQ (1999) Nonshivering thermogenesis in a marsupial (the Tasmanian Bettong Bettongia gaimardi) is not attributable to brown adipose tissue. Physiol Biochem Zool 72:699–704. https://doi.org/10.1086/316709
doi: 10.1086/316709
Rowlatt U, Mrosovsky N, English A (1971) A comparative survey of brown fat in the neck and axilla of mammals at birth. Neonatology 17:53–83. https://doi.org/10.1159/000240303
doi: 10.1159/000240303
Saito S, Saito CT, Shingai R (2008) Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals. Gene 408:37–44. https://doi.org/10.1016/j.gene.2007.10.018
doi: 10.1016/j.gene.2007.10.018
Schaeffer PJ, Villarin JJ, Lindstedt SL (2003) Chronic cold exposure increases skeletal muscle oxidative structure and function in Monodelphis domestica, a marsupial lacking brown adipose tissue. Physiol Biochem Zool 76:877–887. https://doi.org/10.1086/378916
doi: 10.1086/378916
Smith R (1961) Thermogenic activity of the hibernating gland in the cold-acclimated rat. Physiologist 4:113
Storey BC (1995) The role of mantle plumes in continental breakup: case histories from Gondwanaland. Nature 377:301–308. https://doi.org/10.1038/377301a0
doi: 10.1038/377301a0
Talbot DA, Duchamp C, Rey B, Hanuise N, Rouanet JL, Sibille B, Brand MD (2004) Uncoupling protein and ATP/ADP carrier increase mitochondrial proton conductance after cold adaptation of king penguins. J Physiol 558:123–135. https://doi.org/10.1113/jphysiol.2004.063768
doi: 10.1113/jphysiol.2004.063768
Tattersall GJ, Leite CAC, Sanders CE, Cadena V, Andrade DV, Abe AS, Milsom WK (2016) Seasonal reproductive endothermy in tegu lizards. Sci Adv 2:e1500951. https://doi.org/10.1126/sciadv.1500951
doi: 10.1126/sciadv.1500951
Villarin JJ, Schaeffer PJ, Markle RA, Lindstedt SL (2003) Chronic cold exposure increases liver oxidative capacity in the marsupial Monodelphis domestica. Comp Biochem Physiol A Mol Integr Physiol 136:621–630. https://doi.org/10.1016/S1095-6433(03)00210-1
doi: 10.1016/S1095-6433(03)00210-1
Wang H, Willerhäuser M, Li Y, Fromme T, Schnabl K, Bast-Habersbrunner A, Ramisch S, Mocek S, Klingenspor M (2020) Uncoupling protein 1 expression does not protect mice from diet-induced obesity. Am J Physiol Endocrinol Metab. https://doi.org/10.1152/ajpendo.00285.2020
doi: 10.1152/ajpendo.00285.2020
Wegner NC, Snodgrass OE, Dewar H, Hyde JR (2015) Whole-body endothermy in a mesopelagic fish, the opah, Lampris guttatus. Science 348:786–789. https://doi.org/10.1126/science.aaa8902
doi: 10.1126/science.aaa8902
Withers KW, Hulbert AJ (1988) Cold-acclimation in the marsupial Antechinus stuartii—thyroid-function and metabolic-rate. Aust J Zool 36:421–427. https://doi.org/10.1071/zo9880421
doi: 10.1071/zo9880421
Ye JM, Edwards SJ, Rose RW, Rattigan S, Clark MG, Colquhoun EQ (1995) Vasoconstrictors alter oxygen, lactate, and glycerol metabolism in the perfused hindlimb of a rat kangaroo. Am J Physiol Regulatory Integr Comp Physiol 268:R1217–R1223. https://doi.org/10.1152/ajpregu.1995.268.5.R1217
doi: 10.1152/ajpregu.1995.268.5.R1217
Ye JM, Edwards SJ, Rose RW, Steen JT, Clark MG, Colquhoun EQ (1996) Alpha-adrenergic stimulation of thermogenesis in a rat kangaroo (Marsupialia, Bettongia gaimardi). Am J Physiol Regulatory Integr Comp Physiol 271:R586–R592. https://doi.org/10.1152/ajpregu.1996.271.3.R586
doi: 10.1152/ajpregu.1996.271.3.R586