The role of skeletal-muscle-based thermogenic mechanisms in vertebrate endothermy

Biological Reviews

Volumn 90, Issue 4, 2015, Pages 1279-1297

  Rowland, Leslie A ^a   Bal, Naresh C ^a   Periasamy, Muthu ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Brown adipose tissue; Endothermy; Skeletal muscle; SR calcium transport; Thermogenesis

Indexed keywords

ANIMAL; EVOLUTION; GENETICS; PHYSIOLOGY; SKELETAL MUSCLE; THERMOGENESIS; VERTEBRATE;

ANIMALS; BIOLOGICAL EVOLUTION; MUSCLE, SKELETAL; THERMOGENESIS; VERTEBRATES;

EID: 84943386435     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/brv.12157     Document Type: Article

References (228)

1. Alexander, G., Bennett, J. W. & Gemmell, R. T. (1975). Brown adipose tissue in the new-born calf (Bos taurus). Journal of Physiology 244, 223-234.
2. Anunciado-Koza, R. P., Zhang, J., Ukropec, J., Bajpeyi, S., Koza, R. A., Rogers, R. C., Cefalu, W. T., Mynatt, R. L. & Kozak, L. P. (2011). Inactivation of the mitochondrial carrier SLC25A25 (ATP-Mg2+/Pi transporter) reduces physical endurance and metabolic efficiency in mice. Journal of Biological Chemistry 286, 11659-11671.
3. Arruda, A. P., Da-Silva, W. S., Carvalho, D. P. & De Meis, L. (2003). Hyperthyroidism increases the uncoupled ATPase activity and heat production by the sarcoplasmic reticulum Ca2 + -ATPase. Biochemical Journal 375, 753-760.
4. Arruda, A. P., Ketzer, L. A., Nigro, M., Galina, A., Carvalho, D. P. & de Meis, L. (2008). Cold tolerance in hypothyroid rabbits: role of skeletal muscle mitochondria and sarcoplasmic reticulum Ca2+ ATPase isoform 1 heat production. Endocrinology 149, 6262-6271.
5. Arruda, A. P., Nigro, M., Oliveira, G. M. & de Meis, L. (2007). Thermogenic activity of Ca2 + -ATPase from skeletal muscle heavy sarcoplasmic reticulum: the role of ryanodine Ca2+ channel. Biochimica et Biophysica Acta 1768, 1498-1505.
6. Atit, R., Sgaier, S. K., Mohamed, O. A., Taketo, M. M., Dufort, D., Joyner, A. L., Niswander, L. & Conlon, R. A. (2006). Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Developmental Biology 296, 164-176.
7. Aulie, A. (1971). Body temperatures in pigeons and budgerigars during sustained flight. Comparative Biochemistry and Physiology 39, 173-176.
8. Aydin, J., Shabalina, I. G., Place, N., Reiken, S., Zhang, S. J., Bellinger, A. M., Nedergaard, J., Cannon, B., Marks, A. R., Bruton, J. D. & Westerblad, H. (2008). Nonshivering thermogenesis protects against defective calcium handling in muscle. FASEB Journal 22, 3919-3924.
9. Babu, G. J., Bhupathy, P., Carnes, C. A., Billman, G. E. & Periasamy, M. (2007). Differential expression of sarcolipin protein during muscle development and cardiac pathophysiology. Journal of Molecular and Cellular Cardiology 43, 215-222.
10. Bachman, E. S., Dhillon, H., Zhang, C. Y., Cinti, S., Bianco, A. C., Kobilka, B. K. & Lowell, B. B. (2002). betaAR signaling required for diet-induced thermogenesis and obesity resistance. Science 297, 843-845.
11. Bal, N. C., Maurya, S. K., Sopariwala, D. H., Sahoo, S. K., Gupta, S. C., Shaikh, S. A., Pant, M., Rowland, L. A., Bombardier, E., Goonasekera, S. A., Tupling, A. R., Molkentin, J. D. & Periasamy, M. (2012). Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals. Nature Medicine 18, 1575-1579.
12. Barnett, L. B. (1970). Seasonal changes in temperature acclimatization of house sparrow, passer-domesticus. Comparative Biochemistry and Physiology 33, 559-578.
13. Barre, H., Bailly, L. & Rouanet, J. L. (1987). Increased oxidative capacity in skeletal muscles from cold-acclimated ducklings: a comparison with rats. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 88, 519-522.
14. Barre, H., Cohen-Adad, F., Duchamp, C. & Rouanet, J. L. (1989). Muscular nonshivering thermogenesis in birds. Thermal Physiology 871, 667-672.
15. Barre, H., Cohen-Adad, F. & Rouanet, J. L. (1987). Two daily glucagon injections induce nonshivering thermogenesis in Muscovy ducklings. American Journal of Physiology 252, E616-E620.
16. Barre, H., Geloen, A., Chatonnet, J., Dittmar, A. & Rouanet, J. L. (1985). Potentiated muscular thermogenesis in cold-acclimated muscovy duckling. American Journal of Physiology 249, R533-R538.
17. Bennett, A. F. & Ruben, J. A. (1979). Endothermy and activity in vertebrates. Science 206, 649-654.
18. Berg, F., Gustafson, U. & Andersson, L. (2006). The uncoupling protein 1 gene (UCP1) is disrupted in the pig lineage: a genetic explanation for poor thermoregulation in piglets. PLoS Genetics 2, e129.
19. Bicudo, J. E., Bianco, A. C. & Vianna, C. R. (2002). Adaptive thermogenesis in hummingbirds. Journal of Experimental Biology 205, 2267-2273.
20. Bicudo, J. E., Vianna, C. R. & Chaui-Berlinck, J. G. (2001). Thermogenesis in birds. Bioscience Reports 21, 181-188.
21. Billon, N. & Dani, C. (2012). Developmental origins of the adipocyte lineage: new insights from genetics and genomics studies. Stem Cell Reviews 8, 55-66.
22. Block, B. A. (1986). Structure of the brain and eye heater tissue in marlins, sailfish, and spearfishes. Journal of Morphology 190, 169-189.
23. Block, B. A. (1994). Thermogenesis in muscle. Annual Review of Physiology 56, 535-577.
24. Block, B. A. & Franzini-Armstrong, C. (1988). The structure of the membrane systems in a novel muscle cell modified for heat production. Journal of Cell Biology 107, 1099-1112.
25. Block, B. A. & Kim, S. Y. (1992). Localization of junctional Sr proteins in the thermogenic heater cells of billfish. FASEB Journal 6, A429.
26. Block, B. A., Obrien, J. & Meissner, G. (1994). Characterization of the sarcoplasmic-reticulum proteins in the thermogenic muscles of fish. Journal of Cell Biology 127, 1275-1287.
27. Blumberg, M. S., Deaver, K. & Kirby, R. F. (1999). Leptin disinhibits nonshivering thermogenesis in infants after maternal separation. American Journal of Physiology 276, R606-R610.
28. Bombardier, E., Smith, I. C., Gamu, D., Fajardo, V. A., Vigna, C., Sayer, R. A., Gupta, S. C., Bal, N. C., Periasamy, M. & Tupling, A. R. (2013a). Sarcolipin trumps beta-adrenergic receptor signaling as the favored mechanism for muscle-based diet-induced thermogenesis. FASEB Journal 27, 3871-3878.
29. Bombardier, E., Smith, I. C., Vigna, C., Fajardo, V. A. & Tupling, A. R. (2013b). Ablation of sarcolipin decreases the energy requirements for Ca2+ transport by sarco(endo)plasmic reticulum Ca2 + -ATPases in resting skeletal muscle. FEBS Letters 587, 1687-1692.
30. Bourhim, M., Barre, H., Oufara, S., Minaire, Y., Chatonnet, J., Cohen-Adad, F. & Rouanet, J. L. (1990). Increase in cytochrome oxidase capacity of BAT and other tissues in cold-acclimated gerbils. American Journal of Physiology 258, R1291-R1298.
31. Brainerd, E. L. & Owerkowicz, T. (2006). Functional morphology and evolution of aspiration breathing in tetrapods. Respiratory Physiology and Neurobiology 154, 73-88.
32. Butler, P. J. (1991). Exercise in birds. Journal of Experimental Biology 160, 233-262.
33. Butler, P. J. (2000). Energetic costs of surface swimming and diving of birds. Physiological and Biochemical Zoology 73, 699-705.
34. Butler, P. J. & Woakes, A. J. (2001). Seasonal hypothermia in a large migrating bird: saving energy for fat deposition? Journal of Experimental Biology 204, 1361-1367.
35. Cadenas, S., Buckingham, J. A., St-Pierre, J., Dickinson, K., Jones, R. B. & Brand, M. D. (2000). AMP decreases the efficiency of skeletal-muscle mitochondria. Biochemical Journal 351(2), 307-311.
36. Cambon, B., Reyne, Y. & Nougues, J. (1998). In vitro induction of UCP1 mRNA in preadipocytes from rabbit considered as a model of large mammals brown adipose tissue development: importance of PPARgamma agonists for cells isolated in the postnatal period. Molecular and Cellular Endocrinology 146, 49-58.
37. Cannon, B. & Nedergaard, J. (2004). Brown adipose tissue: function and physiological significance. Physiological Reviews 84, 277-359.
38. Carey, F. G. (1982). A brain heater in the swordfish. Science 216, 1327-1329.
39. Carey, F. G. & Teal, J. M. (1966). Heat conservation in tuna fish muscle. Proceedings of the National academy of Sciences of the United States of America 56, 1464-1469.
40. Carrier, D. R. (1987). The evolution of locomotor stamina in tetrapods - circumventing a mechanical constraint. Paleobiology 13, 326-341.
41. Casteilla, L., Champigny, O., Bouillaud, F., Robelin, J. & Ricquier, D. (1989). Sequential changes in the expression of mitochondrial protein mRNA during the development of brown adipose tissue in bovine and ovine species. Sudden occurrence of uncoupling protein mRNA during embryogenesis and its disappearance after birth. Biochemical Journal 257, 665-671.
42. Chaffee, R. R. & Roberts, J. C. (1971). Temperature acclimation in birds and mammals. Annual Review of Physiology 33, 155-202.
43. Clarke, A. (2013). Dinosaur energetics: setting the bounds on feasible physiologies and ecologies. American Naturalist 182, 283-297.
44. Clarke, A. & Portner, H. O. (2010). Temperature, metabolic power and the evolution of endothermy. Biological Reviews of the Cambridge Philosophical Society 85, 703-727.
45. Cohen, P., Levy, J. D., Zhang, Y., Frontini, A., Kolodin, D. P., Svensson, K. J., Lo, J. C., Zeng, X., Ye, L., Khandekar, M. J., Wu, J., Gunawardana, S. C., Banks, A. S., Camporez, J. P., Jurczak, M. J., Kajimura, S., Piston, D. W., Mathis, D., Cinti, S., Shulman, G. I., Seale, P. & Spiegelman, B. M. (2014). Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch. Cell 156, 304-316.
46. Cooke, R. (2011). The role of the myosin ATPase activity in adaptive thermogenesis by skeletal muscle. Biophysical Reviews 3, 33-45.
47. Cousin, B., Cinti, S., Morroni, M., Raimbault, S., Ricquier, D., Penicaud, L. & Casteilla, L. (1992). Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. Journal of Cell Science 103(Pt 4), 931-942.
48. Couture, P. & Hulbert, A. J. (1995). Relationship between body-mass, tissue metabolic-rate, and sodium-pump activity in mammalian liver and kidney. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 268, R641-R650.
49. Davis, T. R. (1967). Contribution of skeletal muscle to nonshivering thermogenesis in the dog. American Journal of Physiology 213, 1423-1426.
50. Dawkins, M. J. & Scopes, J. W. (1965). Non-shivering thermogenesis and brown adipose tissue in the human new-born infant. Nature 206, 201-202.
51. Dickson, K. A. & Graham, J. B. (2004). Evolution and consequences of endothermy in fishes. Physiological and Biochemical Zoology 77, 998-1018.
52. Dizon, A. E., Sharp, G. D. & Inter-American Tropical Tuna Commission, Hubbs-Sea World Research Institute & Southwest Fisheries Center (U.S.) (1978). The Physiological Ecology of Tunas. Academic Press, New York.
53. Duchamp, C. & Barre, H. (1993). Skeletal muscle as the major site of nonshivering thermogenesis in cold-acclimated ducklings. American Journal of Physiology 265, R1076-R1083.
54. Duchamp, C., Barre, H., Delage, D., Rouanet, J. L., Cohen-Adad, F. & Minaire, Y. (1989). Nonshivering thermogenesis and adaptation to fasting in king penguin chicks. American Journal of Physiology 257, R744-R751.
55. Duchamp, C., Barre, H., Rouanet, J. L., Lanni, A., Cohen-Adad, F., Berne, G. & Brebion, P. (1991). Nonshivering thermogenesis in king penguin chicks. I. Role of skeletal muscle. American Journal of Physiology 261, R1438-R1445.
56. Duchamp, C., Chatonnet, J., Dittmar, A. & Barre, H. (1993). Increased role of skeletal muscle in the calorigenic response to glucagon of cold-acclimated ducklings. American Journal of Physiology 265, R1084-R1091.
57. Dumonteil, E., Barre, H. & Meissner, G. (1993). Sarcoplasmic reticulum Ca(2+)-ATPase and ryanodine receptor in cold-acclimated ducklings and thermogenesis. American Journal of Physiology 265, C507-C513.
58. Dumonteil, E., Barre, H. & Meissner, G. (1994). Effects of palmitoyl carnitine and related metabolites on the avian Ca(2+)-ATPase and Ca2+ release channel. Journal of Physiology 479(1), 29-39.
59. Dumonteil, E., Barre, H. & Meissner, G. (1995). Expression of sarcoplasmic reticulum Ca2+ transport proteins in cold-acclimating ducklings. American Journal of Physiology 269, C955-C960.
60. Eldershaw, T. P. D., Duchamp, C., Ye, J. M., Clark, M. G. & Colquhoun, E. Q. (1997). Potential for non-shivering thermogenesis in perfused chicken (Gallus domesticus) muscle. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 117, 545-554.
61. Else, P. L. & Hulbert, A. J. (1981). Comparison of the mammal machine and the reptile machine - energy-production. American Journal of Physiology 240, R3-R9.
62. Else, P. L. & Hulbert, A. J. (1985). An allometric comparison of the mitochondria of mammalian and reptilian tissues: the implications for the evolution of endothermy. Journal of Comparative Physiology B 156, 3-11.
63. Else, P. L. & Hulbert, A. J. (1987). Evolution of mammalian endothermic metabolism: "leaky" membranes as a source of heat. American Journal of Physiology 253, R1-R7.
64. Emmett, B. & Hochachka, P. W. (1981). Scaling of oxidative and glycolytic-enzymes in mammals. Respiration Physiology 45, 261-272.
65. Enerback, S., Jacobsson, A., Simpson, E. M., Guerra, C., Yamashita, H., Harper, M. E. & Kozak, L. P. (1997). Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387, 90-94.
66. Fajardo, V. A., Bombardier, E., Vigna, C., Devji, T., Bloemberg, D., Gamu, D., Gramolini, A. O., Quadrilatero, J. & Tupling, A. R. (2013). Co-expression of SERCA Isoforms, phospholamban and sarcolipin in human skeletal muscle fibers. PLoS ONE 8, e84304.
67. Farmer, S. R. (2008). Brown fat and skeletal muscle: unlikely cousins? Cell 134, 726-727.
68. Fedorenko, A., Lishko, P. V. & Kirichok, Y. (2012). Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria. Cell 151, 400-413.
69. Feldmann, H. M., Golozoubova, V., Cannon, B. & Nedergaard, J. (2009). UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metabolism 9, 203-209.
70. Fernstrom, M., Tonkonogi, M. & Sahlin, K. (2004). Effects of acute and chronic endurance exercise on mitochondrial uncoupling in human skeletal muscle. Journal of Physiology 554, 755-763.
71. Fill, M., Coronado, R., Mickelson, J. R., Vilven, J., Ma, J. J., Jacobson, B. A. & Louis, C. F. (1990). Abnormal ryanodine receptor channels in malignant hyperthermia. Biophysical Journal 57, 471-475.
72. Forner, F., Kumar, C., Luber, C. A., Fromme, T., Klingenspor, M. & Mann, M. (2009). Proteome differences between brown and white fat mitochondria reveal specialized metabolic functions. Cell Metabolism 10, 324-335.
73. Francetic, T. & Li, Q. (2011). Skeletal myogenesis and Myf5 activation. Transcription 2, 109-114.
74. Frontini, A. & Cinti, S. (2010). Distribution and development of brown adipocytes in the murine and human adipose organ. Cell Metabolism 11, 253-256.
75. Gasc, J. P. (2001). Comparative aspects of gait, scaling and mechanics in mammals. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 131, 121-133.
76. Geiser, F. (2008). Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 150, 176-180.
77. Gensch, N., Borchardt, T., Schneider, A., Riethmacher, D. & Braun, T. (2008). Different autonomous myogenic cell populations revealed by ablation of Myf5-expressing cells during mouse embryogenesis. Development 135, 1597-1604.
78. Giralt, M., Martin, I., Iglesias, R., Vinas, O., Villarroya, F. & Mampel, T. (1990). Ontogeny and perinatal modulation of gene expression in rat brown adipose tissue. Unaltered iodothyronine 5′-deiodinase activity is necessary for the response to environmental temperature at birth. European Journal of Biochemistry 193, 297-302.
79. Golozoubova, V., Hohtola, E., Matthias, A., Jacobsson, A., Cannon, B. & Nedergaard, J. (2001). Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold. FASEB Journal 15, 2048-2050.
80. Gorski, P. A., Glaves, J. P., Vangheluwe, P. & Young, H. S. (2013). Sarco(endo)plasmic reticulum calcium ATPase (SERCA) inhibition by sarcolipin is encoded in its luminal tail. Journal of Biological Chemistry 288, 8456-8467.
81. Grigg, G. C., Beard, L. A. & Augee, M. L. (2004). The evolution of endothermy and its diversity in mammals and birds. Physiological and Biochemical Zoology 77, 982-997.
82. Guernsey, D. L. & Morishige, W. K. (1979). Na + pump activity and nuclear T3 receptors in tissues of genetically obese (ob/ob) mice. Metabolism 28, 629-632.
83. Guerra, C., Koza, R. A., Walsh, K., Kurtz, D. M., Wood, P. A. & Kozak, L. P. (1998). Abnormal nonshivering thermogenesis in mice with inherited defects of fatty acid oxidation. Journal of Clinical Investigation 102, 1724-1731.
84. Guppy, M., Hulbert, W. C. & Hochachka, P. W. (1979). Metabolic sources of heat and power in tuna muscles. II. Enzyme and metabolite profiles. Journal of Experimental Biology 82, 303-320.
85. el-Halawani, M. e.-S., Wilson, W. O. & Burger, R. E. (1970). Cold-acclimation and the role of catecholamines in body temperature regulation in male Leghorns. Poultry Science 49, 621-632.
86. Harlow, P. & Grigg, G. (1984). Shivering thermogenesis in a brooding diamond python, Python spilotes spilotes. Copeia 4, 959-965.
87. Harms, M. & Seale, P. (2013). Brown and beige fat: development, function and therapeutic potential. Nature Medicine 19, 1252-1263.
88. Harms, M. J., Ishibashi, J., Wang, W., Lim, H. W., Goyama, S., Sato, T., Kurokawa, M., Won, K. J. & Seale, P. (2014). Prdm16 is required for the maintenance of brown adipocyte identity and function in adult mice. Cell Metabolism 19, 593-604.
89. Hart, J. S. & Roy, O. Z. (1967). Temperature regulation during flight in pigeons. The American Journal of Physiology 213, 1311-1316.
90. Hayes, J. P. (2010). Metabolic rates, genetic constraints, and the evolution of endothermy. Journal of Evolutionary Biology 23, 1868-1877.
91. Heaton, J. M. (1972). The distribution of brown adipose tissue in the human. Journal of Anatomy 112, 35-39.
92. Heim, T. & Hull, D. (1966). The blood flow and oxygen consumption of brown adipose tissue in the new-born rabbit. Journal of Physiology 186, 42-55.
93. Heim, T., Kellermayer, M. & Dani, M. (1968). Thermal conditions and the mobilization of lipids from brown and white adipose tissue in the human neonate. Acta Paediatrica Academiae Scientiarum Hungaricae 9, 109-120.
94. Herpin, P. R., McBride, B. W. & Bayley, H. S. (1987). Effect of cold exposure on energy metabolism in the young pig. Canadian Journal of Physiology and Pharmacology 65, 236-245.
95. Hesse, B., Fischer, M. S. & Schilling, N. (2010). Distribution pattern of muscle fiber types in the perivertebral musculature of two different sized species of mice. Anatomical Record (Hoboken) 293, 446-463.
96. Hillenius, W. J. & Ruben, J. A. (2004). The evolution of endothermy in terrestrial vertebrates: Who? When? Why? Physiological and Biochemical Zoology 77, 1019-1042.
97. Hochachka, P. W. & Mommsen, T. P. (1991). Biochemistry and Molecular biology of Fishes. Elsevier, Amsterdam, New York.
98. Houstek, J., Vizek, K., Pavelka, S., Kopecky, J., Krejcova, E., Hermanska, J. & Cermakova, M. (1993). Type II iodothyronine 5′-deiodinase and uncoupling protein in brown adipose tissue of human newborns. Journal of Clinical Endocrinology and Metabolism 77, 382-387.
99. Hughes, D. A., 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.
100. Hulbert, A. J. & Else, P. L. (1989). Evolution of mammalian endothermic metabolism: mitochondrial activity and cell composition. American Journal of Physiology 256, R63-R69.
101. Hulbert, A. J. & Else, P. L. (1999). Membranes as possible pacemakers of metabolism. Journal of Theoretical Biology 199, 257-274.
102. Hutchinson, J. R. (2004). Biomechanical modeling and sensitivity analysis of bipedal running ability. I. Extant taxa. Journal of Morphology 262, 421-440.
103. Hutchiso, V., Dowling, H. G. & Vinegar, A. (1966). Thermoregulation in a brooding female Indian python Python molurus bivittatus. Science 151, 694-696.
104. Ijiri, D., Miura, M., Kanai, Y. & Hirabayashi, M. (2009). Increased mass of slow-type skeletal muscles and depressed myostatin gene expression in cold-tolerant chicks. Zoological Science 26, 277-283.
105. Inesi, G. & Tadini-Buoninsegni, F. (2013). Ca/H exchange, lumenal Ca release and Ca /ATP coupling ratios in the sarcoplasmic reticulum ATPase. Journal of Cell Communication and Signalling 8, 5-11.
106. Jastroch, M., Withers, K. W., Taudien, S., Frappell, P. B., Helwig, M., Fromme, T., Hirschberg, V., Heldmaier, G., McAllan, B. M., Firth, B. T., Burmester, T., Platzer, M. & Klingenspor, M. (2008). Marsupial uncoupling protein 1 sheds light on the evolution of mammalian nonshivering thermogenesis. Physiological Genomics 32, 161-169.
107. Jenkinson, D. M., Noble, R. C. & Thompson, G. E. (1968). Adipose tissue and heat production in the new-born ox (Bos taurus). Journal of Physiology 195, 639-646.
108. de Jonge, H. W., van der Wiel, C. W., Eizema, K., Weijs, W. A. & Everts, M. E. (2006). Presence of SERCA and calcineurin during fetal development of porcine skeletal muscle. Journal of Histochemistry & Cytochemistry 54, 641-648.
109. Kajimura, S., Seale, P., Kubota, K., Lunsford, E., Frangioni, J. V., Gygi, S. P. & Spiegelman, B. M. (2009). Initiation of myoblast to brown fat switch by a PRDM16-C/EBP-beta transcriptional complex. Nature 460, 1154-1158.
110. Kajimura, S., Seale, P. & Spiegelman, B. M. (2010). Transcriptional control of brown fat development. Cell Metabolism 11, 257-262.
111. Karbowski, J. (2009). Thermodynamic constraints on neural dimensions, firing rates, brain temperature and size. Journal of Computational Neuroscience 27, 415-436.
112. Kawahara, T. & Saito, K. (1976). Genetic parameters of organ and body weights in the Japanese quail. Poultry Science 55, 1247-1252.
113. Kelly, J. M. & McBride, B. W. (1990). The sodium pump and other mechanisms of thermogenesis in selected tissues. Procedings of the Nutrition Society 49, 185-202.
114. Kielan-Jaworowska, Z. & Hurum, J. H. (2006). Limb posture in early mammals: Sprawling or parasagittal. Acta Palaeontologica Polonica 51, 393-406.
115. Kinnunen, S. & Manttari, S. (2012). Specific effects of endurance and sprint training on protein expression of calsequestrin and SERCA in mouse skeletal muscle. Journal of Muscle Research and Cell Motility 33, 123-130.
116. Kjelstrup, S., de Meis, L., Bedeaux, D. & Simon, J. M. (2008). Is the Ca2 + -ATPase from sarcoplasmic reticulum also a heat pump? European Biophysical Journal 38, 59-67.
117. Knight, B. L. & Myant, N. B. (1970). A comparison between the effects of cold exposure in vivo and of noradrenaline in vitro on the metabolism of the brown fat of new-born rabbits. Biochemical Journal 119, 103-111.
118. Kohler, M., Marin-Moratalla, N., Jordana, X. & Aanes, R. (2012). Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487, 358-361.
119. Kosaka, M. & Simon, E. (1968). Central nervous spinal mechanism of cold shivering. Pflügers Archiv 302, 357-373.
120. Kosaka, M., Simon, E. & Thauer, R. (1967a). Shivering in intact and spinal rabbits during spinal cord cooling. Experientia 23, 385-387.
121. Kosaka, M., Takagi, K. & Koyama, Y. (1967b). Reflex inhibition of cold shivering by pressure to the skin and the histological investigation of its afferent spinal pathway. Experientia 23, 453-455.
122. Lamboley, C. R., Murphy, R. M., McKenna, M. J. & Lamb, G. D. (2013). Endogenous and maximal sarcoplasmic reticulum calcium content and calsequestrin expression in type I and type II human skeletal muscle fibres. Journal of Physiology 591, 6053-6068.
123. Lean, M. E. & James, W. P. (1983). Uncoupling protein in human brown adipose tissue mitochondria. Isolation and detection by specific antiserum. FEBS Letters 163, 235-240.
124. Lean, M. E., James, W. P., Jennings, G. & Trayhurn, P. (1986). Brown adipose tissue uncoupling protein content in human infants, children and adults. Clinical Science (London) 71, 291-297.
125. Lee, A. G. (2002). A calcium pump made visible. Current Opinion in Structural Biology 12, 547-554.
126. Lee, A. G. & East, J. M. (2001). What the structure of a calcium pump tells us about its mechanism. Biochemical Journal 356, 665-683.
127. Lefaucheur, L., Ecolan, P., Lossec, G., Gabillard, J. C., Butler-Browne, G. S. & Herpin, P. (2001). Influence of early postnatal cold exposure on myofiber maturation in pig skeletal muscle. Journal of Muscle Research and Cell Motility 22, 439-452.
128. Lepper, C. & Fan, C. M. (2010). Inducible lineage tracing of Pax7-descendant cells reveals embryonic origin of adult satellite cells. Genesis 48, 424-436.
129. Little, A. G. & Seebacher, F. (2013). Thyroid hormone regulates muscle function during cold acclimation in zebrafish (Danio rerio). Journal of Experimental Biology 216, 3514-3521.
130. Lomax, M. A., Sadiq, F., Karamanlidis, G., Karamitri, A., Trayhurn, P. & Hazlerigg, D. G. (2007). Ontogenic loss of brown adipose tissue sensitivity to beta-adrenergic stimulation in the ovine. Endocrinology 148, 461-468.
131. Loncar, D., Afzelius, B. A. & Cannon, B. (1988a). Epididymal white adipose tissue after cold stress in rats. I. Nonmitochondrial changes. Journal of Ultrastructure and Molecular Structure Research 101, 109-122.
132. Loncar, D., Afzelius, B. A. & Cannon, B. (1988b). Epididymal white adipose tissue after cold stress in rats. II. Mitochondrial changes. Journal of Ultrastructure and Molecular Structure Research 101, 199-209.
133. Londraville, R. L., Cramer, T. D., Franck, J. P., Tullis, A. & Block, B. A. (2000). Cloning of a neonatal calcium atpase isoform (SERCA 1B) from extraocular muscle of adult blue marlin (Makaira nigricans). Comparative Biochemistry and Physiology B 127, 223-233.
134. Long, J. Z., Svensson, K. J., Tsai, L., Zeng, X., Roh, H. C., Kong, X., Rao, R. R., Lou, J., Lokurkar, I., Baur, W., Castellot, J. J. Jr., Rosen, E. D. & Spiegelman, B. M. (2014). A smooth muscle-like origin for beige adipocytes. Cell Metabolism 19, 810-820.
135. Lowell, B. B. & Spiegelman, B. M. (2000). Towards a molecular understanding of adaptive thermogenesis. Nature 404, 652-660.
136. Luo, Z. X. (2007). Transformation and diversification in early mammal evolution. Nature 450, 1011-1019.
137. Luo, Z. X. & Crompton, A. W. (1994). Transformation of the quadrate (incus) through the transition from nonmammalian cynodonts to mammals. Journal of Vertebrate Paleontology 14, 341-374.
138. Lytton, J., Westlin, M., Burk, S. E., Shull, G. E. & Maclennan, D. H. (1992). Functional comparisons between isoforms of the sarcoplasmic or endoplasmic-reticulum family of calcium pumps. Journal of Biological Chemistry 267, 14483-14489.
139. MacLennan, D. H. & Phillips, M. S. (1992). Malignant hyperthermia. Science 256, 789-794.
140. Mahmmoud, Y. A. (2008). Capsaicin stimulates uncoupled ATP hydrolysis by the sarcoplasmic reticulum calcium pump. Journal of Biological Chemistry 283, 21418-21426.
141. Mahmmoud, Y. A. & Gaster, M. (2012). Uncoupling of sarcoplasmic reticulum Ca2 + -ATPase by N-arachidonoyl dopamine. Members of the endocannabinoid family as thermogenic drugs. British Journal of Pharmacology 166, 2060-2069.
142. Majesky, M. W. (2007). Developmental basis of vascular smooth muscle diversity. Arteriosclerosis, Thrombosis, and Vascular Biology 27, 1248-1258.
143. Mall, S., Broadbridge, R., Harrison, S. L., Gore, M. G., Lee, A. G. & East, J. M. (2006). The presence of sarcolipin results in increased heat production by Ca(2+)-ATPase. Journal of Biological Chemistry 281, 36597-36602.
144. von Maltzahn, J., Chang, N. C., Bentzinger, C. F. & Rudnicki, M. A. (2012). Wnt signaling in myogenesis. Trends in Cell Biology 22, 602-609.
145. van Marken Lichtenbelt, W. D. & Daanen, H. A. (2003). Cold-induced metabolism. Current Opinion in Clinical Nutrition and Metabolic Care 6, 469-475.
146. Marmonier, F., Duchamp, C., Cohen-Adad, F., Eldershaw, T. P. & Barre, H. (1997). Hormonal control of thermogenesis in perfused muscle of Muscovy ducklings. American Journal of Physiology 273, R1638-R1648.
147. Matthias, A., Ohlson, K. B., Fredriksson, J. M., Jacobsson, A., Nedergaard, J. & Cannon, B. (2000). Thermogenic responses in brown fat cells are fully UCP1-dependent. UCP2 or UCP3 do not substitute for UCP1 in adrenergically or fatty scid-induced thermogenesis. Journal of Biological Chemistry 275, 25073-25081.
148. Mcnab, B. K. (1978). Evolution of endothermy in phylogeny of mammals. American Naturalist 112, 1-21.
149. de Meis, L. (2001). Uncoupled ATPase activity and heat production by the sarcoplasmic reticulum Ca2 + -ATPase. Regulation by ADP. Journal of Biological Chemistry 276, 25078-25087.
150. de Meis, L. (2002). Ca2 + -ATPases (SERCA): energy transduction and heat production in transport ATPases. Journal of Membrane Biology 188, 1-9.
151. de Meis, L., Arruda, A. P. & Carvalho, D. P. (2005). Role of sarco/endoplasmic reticulum Ca(2+)-ATPase in thermogenesis. Bioscience Reports 25, 181-190.
152. Meyer, C. W., Willershauser, M., Jastroch, M., Rourke, B. C., Fromme, T., Oelkrug, R., Heldmaier, G. & Klingenspor, M. (2010). Adaptive thermogenesis and thermal conductance in wild-type and UCP1-KO mice. American Journal of Physiology 299, R1396-R1406.
153. Mezentseva, N. V., Kumaratilake, J. S. & Newman, S. A. (2008). The brown adipocyte differentiation pathway in birds: an evolutionary road not taken. BMC Biology 6, 17.
154. Miller, W. J. (1974). Body temperature of adult pigeons. American Pigeon Journal July, 397.
155. Minaire, Y. & Chatonnet, J. (1968). Influence of the muscular activities of shivering and work on metabolic kinetics of lactate and glucose. Journal of Physiology, Paris 60(Suppl. 2), 500-501.
156. Mitchell, J. R., Jacobsson, A., Kirchgessner, T. G., Schotz, M. C., Cannon, B. & Nedergaard, J. (1992). Regulation of expression of the lipoprotein lipase gene in brown adipose tissue. American Journal of Physiology 263, E500-E506.
157. Morrissette, J. M., Franck, J. P. & Block, B. A. (2003). Characterization of ryanodine receptor and Ca2 + -ATPase isoforms in the thermogenic heater organ of blue marlin (Makaira nigricans). Journal of Experimental Biology 206, 805-812.
158. Muller, M. J. & Seitz, H. J. (1984). Thyroid hormone action on intermediary metabolism. Part I: respiration, thermogenesis and carbohydrate metabolism. Klinische Wochenschrift 62, 11-18.
159. Nespolo, R. F., Bacigalupe, L. D., Figueroa, C. C., Koteja, P. & Opazo, J. C. (2011). Using new tools to solve an old problem: the evolution of endothermy in vertebrates. Trends in Ecology and Evolution 26, 414-423.
160. Newman, S. A. (2011). Thermogenesis, muscle hyperplasia, and the origin of birds. Bioessays 33, 653-656.
161. Newman, S. A., Mezentseva, N. V. & Badyaev, A. V. (2013). Gene loss, thermogenesis, and the origin of birds. Annals of the New York Academy of Sciences 1289, 36-47.
162. Nikki, P. (1969). Biogenic amines, cold-adaptation and halothane shivering in mice. Annales Medicinae Experimentalis et Biologiae Fenniae 47, 129-140.
163. O'Brien, J. & Block, B. A. (1996). Effects of Ca2+ on oxidative phosphorylation in mitochondria from the thermogenic organ of marlin. Journal of Experimental Biology 199, 2679-2687.
164. O'Brien, J., Meissner, G. & Block, B. A. (1993). The fastest contracting muscles of nonmammalian vertebrates express only one isoform of the ryanodine receptor. Biophysical Journal 65, 2418-2427.
165. Oelkrug, R., Goetze, N., Exner, C., Lee, Y., Ganjam, G. K., Kutschke, M., Muller, S., Stohr, S., Tschop, M. H., Crichton, P. G., Heldmaier, G., Jastroch, M. & Meyer, C. W. (2013). Brown fat in a protoendothermic mammal fuels eutherian evolution. Nat Commun 4, 2140.
166. Ohno, H., Shinoda, K., Ohyama, K., Sharp, L. Z. & Kajimura, S. (2013). EHMT1 controls brown adipose cell fate and thermogenesis through the PRDM16 complex. Nature 504, 163-167.
167. Periasamy, M., Bhupathy, P. & Babu, G. J. (2008). Regulation of sarcoplasmic reticulum Ca2+ ATPase pump expression and its relevance to cardiac muscle physiology and pathology. Cardiovascular Research 77, 265-273.
168. Periasamy, M. & Kalyanasundaram, A. (2007). SERCA pump isoforms: their role in calcium transport and disease. Muscle & Nerve 35, 430-442.
169. Pontzer, H., Allen, V. & Hutchinson, J. R. (2009). Biomechanics of running indicates endothermy in bipedal dinosaurs. PLoS ONE 4, e7783.
170. Raimbault, S., Dridi, S., Denjean, F., Lachuer, J., Couplan, E., Bouillaud, F., Bordas, A., Duchamp, C., Taouis, M. & Ricquier, D. (2001). An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds. Biochemical Journal 353, 441-444.
171. Rolfe, D. F. & Brown, G. C. (1997). Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiological Reviews 77, 731-758.
172. Rose, R. W., Kuswanti, N. & Colquhoun, E. Q. (1998). Development of endothermy in a Tasmanian marsupial, Bettongia gaimardi and its response to cold and noradrenaline. Journal of Comparative Physiology B 168, 359-363.
173. Rose, R. W., West, A. K., Ye, J. M., McCormick, G. H. & Colquhoun, E. Q. (1999). Nonshivering thermogenesis in a marsupial (the tasmanian bettong Bettongia gaimardi) is not attributable to brown adipose tissue. Physiological and Biochemical Zoology 72, 699-704.
174. Ruben, J. (1995). The evolution of endothermy in mammals and birds: from physiology to fossils. Annual Review of Physiology 57, 69-95.
175. Runcie, R. M., Dewar, H., Hawn, D. R., Frank, L. R. & Dickson, K. A. (2009). Evidence for cranial endothermy in the opah (Lampris guttatus). Journal of Experimental Biology 212, 461-470.
176. Ruta, M., Botha-Brink, J., Mitchell, S. A. & Benton, M. J. (2013). The radiation of cynodonts and the ground plan of mammalian morphological diversity. Proceedings of the Royal Society B: Biological Sciences 280, 20131865.
177. Sahoo, S. K., Shaikh, S. A., Sopariwala, D. H., Bal, N. C. & Periasamy, M. (2013). Sarcolipin protein interaction with sarco(endo)plasmic reticulum Ca2+ ATPase (SERCA) is distinct from phospholamban protein, and only sarcolipin can promote uncoupling of the SERCA pump. Journal of Biological Chemistry 288, 6881-6889.
178. Saito, S., Saito, C. T. & 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.
179. Sanchez-Gurmaches, J., Hung, C. M., Sparks, C. A., Tang, Y., Li, H. & Guertin, D. A. (2012). PTEN loss in the Myf5 lineage redistributes body fat and reveals subsets of white adipocytes that arise from Myf5 precursors. Cell Metabolism 16, 348-362.
180. Schiaffino, S. & Reggiani, C. (2011). Fiber types in mammalian skeletal muscles. Physiological Reviews 91, 1447-1531.
181. Schubring, C. (1986). Temperature regulation in healthy and resuscitated newborns immediately after birth. Journal of Perinatal Medicine 14, 27-33.
182. Schulz, T. J., Huang, P., Huang, T. L., Xue, R., McDougall, L. E., Townsend, K. L., Cypess, A. M., Mishina, Y., Gussoni, E. & Tseng, Y. H. (2013). Brown-fat paucity due to impaired BMP signalling induces compensatory browning of white fat. Nature 495, 379-383.
183. Schweitzer, M. H. & Marshall, C. L. (2001). A molecular model for the evolution of endothermy in the theropod-bird lineage. Journal of Experimental Zoology 291, 317-338.
184. Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scime, A., Devarakonda, S., Conroe, H. M., Erdjument-Bromage, H., Tempst, P., Rudnicki, M. A., Beier, D. R. & Spiegelman, B. M. (2008). PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961-967.
185. Seow, C. Y. & Ford, L. E. (1991). Shortening velocity and power output of skinned muscle-fibers from mammals having a 25, 000-fold range of body-mass. Journal of General Physiology 97, 541-560.
186. Seymour, R. S. (2013). Maximal aerobic and anaerobic power generation in large crocodiles versus mammals: implications for dinosaur gigantothermy. PLoS ONE 8, e69361.
187. Shabalina, I. G., Hoeks, J., Kramarova, T. V., Schrauwen, P., Cannon, B. & Nedergaard, J. (2010). Cold tolerance of UCP1-ablated mice: a skeletal muscle mitochondria switch toward lipid oxidation with marked UCP3 up-regulation not associated with increased basal, fatty acid- or ROS-induced uncoupling or enhanced GDP effects. Biochimica et Biophysica Acta 1797, 968-980.
188. Shabalina, I. G., Kramarova, T. V., Nedergaard, J. & Cannon, B. (2006). Carboxyatractyloside effects on brown-fat mitochondria imply that the adenine nucleotide translocator isoforms ANT1 and ANT2 may be responsible for basal and fatty-acid-induced uncoupling respectively. Biochemical Journal 399, 405-414.
189. Sidor, C. A. & Hopson, J. A. (1998). Ghost lineages and "mammalness": assessing the temporal pattern of character acquisition in the Synapsida. Paleobiology 24, 254-273.
190. Silva, J. E. (2006). Thermogenic mechanisms and their hormonal regulation. Physiological Reviews 86, 435-464.
191. Silva, J. E. (2011). Physiological importance and control of non-shivering facultative thermogenesis. Frontiers in Bioscience 3, 352-371.
192. Simonides, W. S., Thelen, M. H., van der Linden, C. G., Muller, A. & van Hardeveld, C. (2001). Mechanism of thyroid-hormone regulated expression of the SERCA genes in skeletal muscle: implications for thermogenesis. Bioscience Reports 21, 139-154.
193. Slebodzinski, A. B. (1988). Hyperiodothyroninaemia of neonates, its significance for thermogenesis. Acta Physiologica Polonica 39, 364-379.
194. Slip, D. J. & Shine, R. (1988). Reptilian endothermy - a field-study of thermoregulation by brooding diamond pythons. Journal of Zoology 216, 367-378.
195. Smith, W. S., Broadbridge, R., East, J. M. & Lee, A. G. (2002). Sarcolipin uncouples hydrolysis of ATP from accumulation of Ca2+ by the Ca2 + -ATPase of skeletal-muscle sarcoplasmic reticulum. Biochemical Journal 361, 277-286.
196. Stainsby, W. N. & Lambert, C. R. (1979). Determination of oxygen uptake in skeletal muscle. Exercise and Sports Sciences Review 7, 125-151.
197. Stewart, M. A., Franks-Skiba, K., Chen, S. & Cooke, R. (2010). Myosin ATP turnover rate is a mechanism involved in thermogenesis in resting skeletal muscle fibers. Proceedings of the National Academy of Sciences of the United States of America 107, 430-435.
198. Strang, K. T. & Steudel, K. (1990). Explaining the scaling of transport costs - the role of stride frequency and stride length. Journal of Zoology 221, 343-358.
199. Tanche, M. & Therminarias, A. (1969). Thyroxine and catecholamines during cold exposure in dogs. Federation Procedings 28, 1257-1261.
200. Teulier, L., Rouanet, J. L., Letexier, D., Romestaing, C., Belouze, M., Rey, B., Duchamp, C. & Roussel, D. (2010). Cold-acclimation-induced non-shivering thermogenesis in birds is associated with upregulation of avian UCP but not with innate uncoupling or altered ATP efficiency. Journal of Experimental Biology 213, 2476-2482.
201. Thomas, S. A. & Palmiter, R. D. (1997). Thermoregulatory and metabolic phenotypes of mice lacking noradrenaline and adrenaline. Nature 387, 94-97.
202. Timmons, J. A., Wennmalm, K., Larsson, O., Walden, T. B., Lassmann, T., Petrovic, N., Hamilton, D. L., Gimeno, R. E., Wahlestedt, C., Baar, K., Nedergaard, J. & Cannon, B. (2007). Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages. Proceedings of the National academy of Sciences of the United States of America 104, 4401-4406.
203. Tkachenko, E. (1968). Shivering and non-shivering thermogenesis in skeletal muscles. Fiziologicheskii zhuenal imeni IM Sechenova 54, 1475-1480.
204. Torre-Bueno, J. R. (1976). Temperature regulation and heat dissipation during flight in birds. Journal of Experimental Biology 65, 471-482.
205. Toyomizu, M., Ueda, M., Sato, S., Seki, Y., Sato, K. & Akiba, Y. (2002). Cold-induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle. FEBS Letters 529, 313-318.
206. Toyoshima, C. & Cornelius, F. (2013). New crystal structures of PII-type ATPases: excitement continues. Current Opinion in Structural Biology 23, 507-514.
207. Toyoshima, C., Iwasawa, S., Ogawa, H., Hirata, A., Tsueda, J. & Inesi, G. (2013). Crystal structures of the calcium pump and sarcolipin in the Mg2 + -bound E1 state. Nature 495, 260-264.
208. Trayhurn, P., Thomas, M. E. & Keith, J. S. (1993). Postnatal development of uncoupling protein, uncoupling protein mRNA, and GLUT4 in adipose tissues of goats. American Journal of Physiology 265, R676-R682.
209. Tseng, Y. H., Cypess, A. M. & Kahn, C. R. (2010). Cellular bioenergetics as a target for obesity therapy. Nature Reviews Drug Discovery 9, 465-482.
210. Tullis, A., Block, B. A. & Sidell, B. D. (1991). Activities of key metabolic enzymes in the heater organs of scombroid fishes. Journal of Experimental Biology 161, 383-403.
211. Tupling, A. R., Bombardier, E., Gupta, S. C., Hussain, D., Vigna, C., Bloemberg, D., Quadrilatero, J., Trivieri, M. G., Babu, G. J., Backx, P. H., Periasamy, M., MacLennan, D. H. & Gramolini, A. O. (2011). Enhanced Ca2+ transport and muscle relaxation in skeletal muscle from sarcolipin-null mice. American Journal of Physiology 301, C841-C849.
212. Ukropec, J., Anunciado, R. P., Ravussin, Y., Hulver, M. W. & Kozak, L. P. (2006). UCP1-independent thermogenesis in white adipose tissue of cold-acclimated Ucp1-/- mice. Journal of Biological Chemistry 281, 31894-31908.
213. Vangheluwe, P., Schuermans, M., Zador, E., Waelkens, E., Raeymaekers, L. & Wuytack, F. (2005). Sarcolipin and phospholamban mRNA and protein expression in cardiac and skeletal muscle of different species. Biochemical Journal 389, 151-159.
214. Virtanen, K. A. & Nuutila, P. (2011). Brown adipose tissue in humans. Current Opinion in Lipidology 22, 49-54.
215. Vybiral, S. & Jansky, L. (1974). Non-shivering thermogenesis in the golden hamster. Physiologia Bohemoslovaca 23, 235-243.
216. Walter, I. & Seebacher, F. (2007). Molecular mechanisms underlying the development of endothermy in birds (Gallus gallus): a new role of PGC-1 alpha? American Journal of Physiology 293, R2315-R2322.
217. Walter, I. & Seebacher, F. (2009). Endothermy in birds: underlying molecular mechanisms. Journal of Experimental Biology 212, 2328-2336.
218. Winther, A. M., Bublitz, M., Karlsen, J. L., Moller, J. V., Hansen, J. B., Nissen, P. & Buch-Pedersen, M. J. (2013). The sarcolipin-bound calcium pump stabilizes calcium sites exposed to the cytoplasm. Nature 495, 265-269.
219. Wojciechowicz, K., Gledhill, K., Ambler, C. A., Manning, C. B. & Jahoda, C. A. (2013). Development of the mouse dermal adipose layer occurs independently of subcutaneous adipose tissue and is marked by restricted early expression of FABP4. PLoS ONE 8, e59811.
220. Wu, J., Bostrom, P., Sparks, L. M., Ye, L., Choi, J. H., Giang, A. H., Khandekar, M., Virtanen, K. A., Nuutila, P., Schaart, G., Huang, K., Tu, H., van Marken Lichtenbelt, W. D., Hoeks, J., Enerback, S., Schrauwen, P. & Spiegelman, B. M. (2012). Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366-376.
221. Wu, J., Cohen, P. & Spiegelman, B. M. (2013). Adaptive thermogenesis in adipocytes: is beige the new brown? Genes & Development 27, 234-250.
222. Xue, B., Rim, J. S., Hogan, J. C., Coulter, A. A., Koza, R. A. & Kozak, L. P. (2007). Genetic variability affects the development of brown adipocytes in white fat but not in interscapular brown fat. Journal of Lipid Research 48, 41-51.
223. Ye, J. M., Edwards, S. J., Rose, R. W., Steen, J. T., Clark, M. G. & Colquhoun, E. Q. (1996). Alpha-adrenergic stimulation of thermogenesis in a rat kangaroo (Marsupialia, Bettongia gaimardi). American Journal of Physiology 271, R586-R592.
224. Young, P., Arch, J. R. & Ashwell, M. (1984). Brown adipose tissue in the parametrial fat pad of the mouse. FEBS Letters 167, 10-14.
225. Yu, X. & Inesi, G. (1995). Variable stoichiometric efficiency of Ca2+ and Sr2+ transport by the sarcoplasmic reticulum ATPase. Journal of Biological Chemistry 270, 4361-4367.
226. Yuan, B., Lu, R., Gu, Y., Liao, Y. & Wei, H. (2012). Research progress of sarcolipin-a new regulatory protein of sarcoplasmic reticulum Ca2+ ATPase. Zhong Nan Da Xue Xue Bao Yi Xue Ban 37, 316-319.
227. Zancanaro, C., Carnielli, V. P., Moretti, C., Benati, D. & Gamba, P. (1995). An ultrastructural study of brown adipose tissue in pre-term human new-borns. Tissue and Cell 27, 339-348.
228. Zurlo, F., Larson, K., Bogardus, C. & Ravussin, E. (1990). Skeletal muscle metabolism is a major determinant of resting energy expenditure. Journal of Clinical Investigation 86, 1423-1427.