Tissue distribution of cold-induced thermogenesis in conscious warm- or cold-acclimated rats reevaluated from changes in tissue blood flow: The dominant role of brown adipose tissue in the replacement of shivering by nonshivering thermogenesis
Abstract
Radioactive microspheres (12–16 μm) were used to measure cardiac output (CO), its fractional distribution, and hence tissue blood flow in conscious, warm-acclimated (WA) or cold-acclimated (CA) white rats exposed to temperatures of 25, 21, 6, −6, and −19 °C, the objective being to assess the tissue distribution of cold-induced thermogenesis. Total oxygen consumption was also measured. CA rats at 25 °C (CA 25) had elevated arteriovenous shunting and other signs of heat stress. CA 21 proved more suitable controls for the CA group. The cold-induced changes in blood flow to total skeletal muscle not involved in respiratory movements (M) and to the major masses of brown adipose tissue (BAT) were quantitatively very different in the two acclimation groups: in WA 25 and CA 21 flows to M were 31 (0.24 CO) and 27 (0.17 CO) mL/min, respectively, while flows to BAT were 2.1 and 9.7 mL/min; in WA−19 and CA−19 flows to M were 62 (0.32 CO) and 35 (0.16 CO) mL/min, respectively, while flows to BAT were 25 and 56 mL/min. In contrast, the effects of cold exposure on flows to other tissues and organs were remarkably alike in the two acclimation groups: e.g., flows to heart, ribcage, and diaphragm increased about three times between 25 and −19 °C, flow to the skin fell about 50%, and flows to the hepatosplanchnic region and kidneys were little or not at all affected by cold exposure. Estimates of the contributions of different tissues and organs to cold-induced thermogenesis were made on the basis of the relative changes in blood flow. It is concluded that BAT is by far the dominant anatomical site of the increased heat production of cold-exposed CA rats, and that nonshivering thermogenesis in BAT supplements considerably the shivering thermogenesis of cold-exposed WA rats.
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Humans have much greater body mass (~200X), only moderately greater BAT mass (~10X), and much lower basal metabolic rate (~0.15X) than rats.
“Humans are quite different from rats, with much greater body mass (~200X), only moderately greater BAT mass (~10X), and much lower basal metabolic rate (~0.15X) 13,37,36.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [36]
In a cold-acclimatized rat weighing 350-400 g, oxygen consumption by 3 g of BAT is approximately twice the basal metabolic rate.
“In a cold-acclimatized rat weighting 350–400 g, oxygen consumption by 3 g of BAT is approximately twice the basal metabolic rate 36.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [36]
Cites
Guyton, A. C. (1965) · The American Journal of the Medical Sciences · doi:10.1097/00000441-196501000-00051 · Cited by 635 · see citing works
Depocas, F., & Hart, J. S. (1957) · Journal of Applied Physiology · doi:10.1152/jappl.1957.10.3.388 · Cited by 561 · see citing works
Use of radioactive microspheres to assess distribution of cardiac output in rabbits
Jm, N., Wyler, F., & Am, R. (1968) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1968.215.2.486 · Cited by 287 · see citing works
Hales, J. R. S. (1973) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00586547 · Cited by 149 · see citing works
Measurement of the distribution of cardiac output in unanesthetized rats
Sasaki, Y., & Wagner, H. N. (1971) · Journal of Applied Physiology · doi:10.1152/jappl.1971.30.6.879 · Cited by 149 · see citing works
NORMAL ARTERIOVENOUS ANASTOMOSES
Sherman, J. L. (1963) · Medicine · doi:10.1097/00005792-196307000-00001 · Cited by 142 · see citing works
Trayhurn, P. (1979) · FEBS Letters · doi:10.1016/0014-5793(79)81075-3 · Cited by 132 · see citing works
Circulation in skeletal muscle
(1969) · American Heart Journal · doi:10.1016/0002-8703(69)90426-8 · Cited by 98 · see citing works
The redistribution of cardiac output in the dog during heat stress
Hales, J. R. S., & Dampney, R. A. L. (1975) · Journal of Thermal Biology · doi:10.1016/0306-4565(75)90008-x · Cited by 86 · see citing works
Energy Metabolism of the White Rat After Acclimation to Warm and Cold Environments
Depocas, F., Hart, J. S., & Héroux, O. (1957) · Journal of Applied Physiology · doi:10.1152/jappl.1957.10.3.393 · Cited by 81 · see citing works
Janský, L., & Hart, J. S. (1963) · Canadian Journal of Biochemistry and Physiology · doi:10.1139/y63-108 · Cited by 71 · see citing works
Foster, D. O., & Frydman, M. L. (1978) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y78-014 · Cited by 69 · see citing works
Self-citationBody glucose as fuel for thermogenesis in the white rat exposed to cold
Depocas, F., & Masironi, R. (1960) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1960.199.6.1051 · Cited by 61 · see citing works
Arteriovenous anastomotic blood flow in the mesenteric organs
Delaney, J. (1969) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1969.216.6.1556 · Cited by 50 · see citing works
Trayhurn, P. (1980) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/0005-2760(80)90179-4 · Cited by 36 · see citing works
Arteriovenous shunting in extremities
LOPEZ-MAJANO, V., Rhodes, B. A., & Wagner, H. N. (1969) · Journal of Applied Physiology · doi:10.1152/jappl.1969.27.6.782 · Cited by 35 · see citing works
Effect of exercise and cold on cardiac output in warm- and cold-acclimated rats.
Popović, Kent, K. M., Mojovic, N., et al. (1969) · PubMed · Cited by 33 · see citing works
Krog, H., Monson, M., & Irving, L. (1955) · Journal of Applied Physiology · doi:10.1152/jappl.1955.7.4.349 · Cited by 32 · see citing works
Depocas, F., & Behrens, W. A. (1978) · Proceedings of the Fourth International Symposium on Polarization Phenomena in Nuclear Reactions · doi:10.1007/978-3-0348-5559-4_15 · Cited by 29 · see citing works
CHEMICAL THERMOGENESIS IN THE FUNCTIONALLY EVISCERATED COLD-ACCLIMATED RAT
Depocas, F. (1958) · Canadian Journal of Biochemistry and Physiology · doi:10.1139/y58-075 · Cited by 25 · see citing works
Foster, D. O. (1974) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y74-139 · Cited by 25 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Brown Adipose Tissue: Function and Physiological Significance
CANNON, B., & NEDERGAARD, J. (2004) · Physiological Reviews · doi:10.1152/physrev.00015.2003 · Cited by 6,433 · see citing works
Towards a molecular understanding of adaptive thermogenesis
Lowell, B. B., & Spiegelman, B. M. (2000) · Nature · doi:10.1038/35007527 · Cited by 1,630 · see citing works
Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese
Enerbäck, S., Jacobsson, A., Simpson, E. M., Guerra, C., Yamashita, H., Harper, M.-E., & Kozak, L. P. (1997) · Nature · doi:10.1038/387090a0 · Cited by 1,379 · see citing works
Development of obesity in transgenic mice after genetic ablation of brown adipose tissue
Lowell, B. B., S-Susulic, V., Hamann, A., Lawitts, J. A., Himms-Hagen, J., Boyer, B. B., Kozak, L. P., & Flier, J. S. (1993) · Nature · doi:10.1038/366740a0 · Cited by 1,075 · see citing works
Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1
Baar, K., Wende, A. R., Jones, T. E., Marison, M., Nolte, L. A., Chen, M., Kelly, D. P., & Holloszy, J. O. (2002) · The FASEB Journal · doi:10.1096/fj.02-0367com · Cited by 1,020 · see citing works
Nonshivering thermogenesis and its adequate measurement in metabolic studies
Cannon, B., & Nedergaard, J. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.050989 · Cited by 677 · see citing works
Guerra, C., Koza, R. A., Yamashita, H., Walsh, K., & Kozak, L. P. (1998) · Journal of Clinical Investigation · doi:10.1172/jci3155 · Cited by 635 · see citing works
Thermogenic Activation Induces FGF21 Expression and Release in Brown Adipose Tissue
Hondares, E., Iglesias, R., Giralt, A., Gonzalez, F. J., Giralt, M., Mampel, T., & Villarroya, F. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.215889 · Cited by 623 · see citing works
Cellular bioenergetics as a target for obesity therapy
Tseng, Y.-H., Cypess, A. M., & Kahn, C. R. (2010) · Nature Reviews Drug Discovery · doi:10.1038/nrd3138 · Cited by 591 · see citing works
Thermal biology of the laboratory rat
Gordon, C. J. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90025-y · Cited by 521 · see citing works
Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold
Golozoubova, V., Hohtola, E., Matthias, A., Jacobsson, A., Cannon, B., & Nedergaard, J. (2001) · The FASEB Journal · doi:10.1096/fj.00-0536fje · Cited by 503 · see citing works
Brown fat as a therapy for obesity and diabetes
Cypess, A. M., & Kahn, C. R. (2010) · Current Opinion in Endocrinology, Diabetes & Obesity · doi:10.1097/med.0b013e328337a81f · Cited by 376 · see citing works
Jacobsson, A., Stadler, U., Glotzer, M. A., & Kozak, L. P. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36228-2 · Cited by 300 · see citing works
Hypoxia and Adipocyte Physiology: Implications for Adipose Tissue Dysfunction in Obesity
Trayhurn, P. (2014) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071812-161156 · Cited by 194 · see citing works
Mercer, S. W., & Trayhurn, P. (1987) · The Journal of Nutrition · doi:10.1093/jn/117.12.2147 · Cited by 146 · see citing works
Bukowiecki, L. J., Folléa, N., Lupien, J., & Paradis, A. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)42972-9 · Cited by 122 · see citing works
The development of obesity in animals: The role of dietary factors
Rothwell, N. J., & Stock, M. J. (1984) · Clinics in Endocrinology and Metabolism · doi:10.1016/s0300-595x(84)80032-8 · Cited by 65 · see citing works
Yamashita, H., Sato, Y., Kizaki, T., Oh-ishi, S., Nagasawa, J. I., & Ohno, H. (1994) · Pfl�gers Archiv European Journal of Physiology · doi:10.1007/bf00724518 · Cited by 46 · see citing works
A role for brown adipose tissue in the genesis of obesity? Studies on experimental animals
Trayhurn, P., Goodbody, A. E., & Tames, W. P. T. (1982) · Proceedings of the Nutrition Society · doi:10.1079/pns19820022 · Cited by 22 · see citing works
Calonne, J., Arsenijevic, D., Scerri, I., Miles-Chan, J. L., Montani, J.-P., & Dulloo, A. G. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00092.2019 · Cited by 15 · see citing works
- Authors
- Foster, D. O., & Frydman, M. L.
- Venue
- Canadian Journal of Physiology and Pharmacology
- Publisher
- Canadian Science Publishing
- Published
- 1979-03-01
- Volume
- 57
- Issue
- 3
- Pages
- 257-270
- ISSN
- 0008-4212 (ISSN-L)
- 1205-7541
- OpenAlex
- W2168270522
- Cited by
- 518
- References
- 21
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 5 · 2023: 9 · 2022: 14 · 2021: 8 · 2020: 7 · 2019: 6 · 2018: 13 · 2017: 10 · 2016: 11 · 2015: 9 · 2014: 9 · 2013: 18 · 2012: 8
- FWCI
- 18.76
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Canadian Journal of Physiology and Pharmacology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Directorate for Biological Sciences
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Physiology › Thermoregulation and physiological responses
- Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
- Keywords
- cold-induced thermogenesis, brown adipose tissue, non-shivering thermogenesis, shivering thermogenesis, tissue blood flow, cold acclimation, warm acclimation, cardiac output, skeletal muscle blood flow, oxygen consumption, thermogenesis, radioactive microspheres
- MeSH terms
- Acclimatization, Animals, Body Temperature Regulation, Adipose Tissue, Brown, Cardiac Output, Cold Temperature, Oxygen, Oxygen Consumption, Regional Blood Flow, Shivering, Strontium Radioisotopes, Rats
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