Translating animal model research: Does it matter that our rodents are cold?

Physiology

Volumn 29, Issue 6, 2014, Pages 413-420

  Maloney, Shane K ^a,b   Fuller, Andrea ^b   Mitchell, Duncan ^a,b   Gordon, Christopher ^c   Michael Overton, J ^d  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^d FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ANIMAL HOUSING; ANIMAL MODEL; CARDIOVASCULAR FUNCTION; COLD; COLD SHOCK RESPONSE; ENERGY METABOLISM; GENOTYPE; HUMAN; LONGEVITY; MICROCLIMATE; MOUSE; PHENOTYPE; PROCEDURES; RAT; SPECIES DIFFERENCE; THERMOREGULATION; TRANSLATIONAL RESEARCH;

ANIMALS; BODY TEMPERATURE REGULATION; CARDIOVASCULAR PHYSIOLOGICAL PHENOMENA; COLD TEMPERATURE; COLD-SHOCK RESPONSE; ENERGY METABOLISM; ENVIRONMENT, CONTROLLED; GENOTYPE; HOUSING, ANIMAL; HUMANS; LONGEVITY; MICE; MODELS, ANIMAL; PHENOTYPE; RATS; SPECIES SPECIFICITY; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84908450050     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00029.2014     Document Type: Review

References (67)

1. Banavar JR, Moses ME, Brown JH, Damuth J, Rinaldo A, Sibly RM, Maritan A. A general basis for quarter-power scaling in animals. Proc Natl Acad Sci USA 107: 15816-15820, 2010.
2. Bartholomew GA. Body temperature and energy metabolism. In: Animal Physiology: Principles and Adaptations, edited by Gordon MS. New York: MacMillan, 1977, p. 364-449.
3. Bartke A, Westbrook R. Metabolic characteristics of longlived mice. Front Genetics 288: 1-6, 2012.
4. Baumans V. Use of animals in experimental research: an ethical dilemma? Gene Ther 11: S64-S66, 2004.
5. Boon MR, van den Berg SAA, Wang Y, van den Bossche J, Karkampouna S, Bauwens M, De Saint-Hubert M, van der Horst G, Vukicevic S, de Winther MPJ, Havekes LM, Jukema JW, Tamsma JT, van der Pluijm G, van Dijk KW, Rensen PCN. BMP7 activates brown adipose tissue and reduces diet-induced obesity only at subthermoneutrality. PLos One 8: e74083, 2013.
6. Bradley A, Anastassiadis K, Ayadi A, Battey J, Bell C, Birling MC, Bottomley J, Brown S, Bürger A, Bult C, Bushell W, Collins F, Desaintes C, Doe B, Economides A, Eppig J, Finnell R, Fletcher C, Fray M, Frendewey D, Friedel R, Grosveld F, Hansen J, Hérault Y, Hicks G, Hörlein A, Houghton R, Hrabé de Angelis M, Huylebroeck D, Iyer V, Jong P, Kadin J, Kaloff C, Kennedy K, Koutsourakis M, Kent Lloyd KC, Marschall S, Mason J, McKerlie C, McLeod M, Melchner H, Moore M, Mujica A, Nagy A, Nefedov M, Nutter L, Pavlovic G, Peterson J, Pollock J, Ramirez-Solis R, Rancourt D, Raspa M, Remacle J, Ringwald M, Rosen B, Rosenthal N, Rossant J, Ruiz Noppinger P, Ryder E, Schick J, Schnütgen F, Schofield P, Seisenberger C, Selloum M, Simpson E, Skarnes W, Smedley D, Stanford W, Francis Stewart A, Stone K, Swan K, Tadepally H, Teboul L, Tocchini-Valentini G, Valenzuela D, West A, Yamamura Ki Yoshinaga Y, Wurst W. The mammalian gene function resource: the international knockout mouse consortium. Mamm Genome 23: 580-586, 2012.
7. Brown-Borg HM, Bartke A. GH and IGF1: roles in energy metabolism of long-living GH mutant mice. J Gerontol A Biol Sci Med Sci 67: 652-660, 2012.
8. Brown-Borg HM, Borg KE, Meliska CJ, Bartke A. Dwarf mice and the aging process. Nature 384: 33, 1996.
9. Buchanan JB, Peloso E, Satinoff E. A warmer ambient temperature increases the passage of interleukin-1_into the brains of old rats. Am J Physiol Regul Integr Comp Physiol 295: R361-R368, 2008.
10. Calder WA. Scaling of physiological processes in homeothermic animals. Annu Rev Physiol 43: 301-322, 1981.
11. Calder WA. Size, Function, and Life History. Mineola, NY: Dover, 1996, p. 449.
12. Cannon B, Nedergaard J. Nonshivering thermogenesis and its adequate measurement in metabolic studies. J Exp Biol 214: 242-253, 2011.
13. Castillo M, Hall JA, Correa-Medina M, Ueta C, Won Kang H, Cohen DE, Bianco AC. Disruption of thyroid hormone activation in type 2 deiodinase knockout mice causes obesity with glucose intolerance and liver steatosis only at thermoneutrality. Diabetes 60: 1082-1089, 2011.
14. Conti B, Sanchez-Alavez M, Winsky-Sommerer R, Morale MC, Lucero J, Brownell S, Fabre V, Huitron-Resendiz S, Henriksen S, Zorrilla EP, de Lecea L, Bartfai T. Transgenic mice with a reduced core body temperature have an increased life span. Science 314: 825-828, 2006.
15. David JM, Chatziioannou AF, Taschereau R, Wang H, Stout DB. The hidden cost of housing practices: using noninvasive imaging to quantify the metabolic demands of chronic cold stress of laboratory mice. Comparative Med 63: 386-391, 2013.
16. Enerback S, Jacobsson A, Simpson EM, Guerra C, Yamashita H, Harper ME, Kozak LP. Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387: 90-94, 1997.
17. Feldmann HM, Golozoubova V, Cannon B, Nedergaard J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab 9: 203-209, 2009.
18. Gaskill BN, Rohr SA, Pajor EA, Lucas JR, Garner JP. Some like it hot: mouse temperature preferences in laboratory housing. Appl Anim Behav Sci 116: 279-285, 2009.
19. Gordon CJ. Effect of cage bedding on temperature regulation and metabolism of group-housed female mice. Comparative Med 54: 63-68, 2004.
20. Gordon CJ. Thermal biology of the laboratory rat. Physiol Behav 47: 963-991, 1990.
21. Gordon CJ. Thermal physiology of laboratory mice: defining thermoneutrality. J Therm Biol 37: 654-685, 2012.
22. Healy S. Air-conditioning and the ‘homogenization’ of people and built environments. Build Res Inf 36: 312-322, 2008.
23. Hill RW, Muhich TE, Humphries MM. City-scale expansion of human thermoregulatory costs. PLos One 8: e76238, 2013.
24. Hoffman JF. The red cell membrane and the transport of sodium and potassium. Am J Med 41: 666-680, 1966.
25. IUPS Thermal Commission. Glossary of terms for thermal physiology: third edition (reprinted from the Japanese Journal of Physiology). J Therm Biol 28: 75-106, 2003.
26. Jessen C. Temperature Regulation in Humans and Other Mammals. Berlin: Springer-Verlag, 2001, p. 193.
27. Johnson F, Mavrogianni A, Ucci M, Vidal-Puig A, Wardle J. Could increased time spent in a thermal comfort zone contribute to population increases in obesity? Obes Rev 12: 543-551, 2011.
28. Jun JC, Shin MK, Yao Q, Devera R, Fonti-Bevans S, Polotsky VY. Thermoneutrality modifies the impact of hypoxia on lipid metabolism. Am J Physiol Endocrinol Metab 304: E424-E435, 2013.
29. Kaiyala KJ, Morton GJ, Thaler JP, Meek TH, Tylee T, Ogimoto K, Wisse BE. Acutely decreased thermoregulatory energy expenditure or decreased activity energy expenditure both acutely reduce food intake in mice. PLos One 7: e41473, 2012.
30. Karp CL. Unstressing intemperate models: how cold stress undermines mouse modeling. J Exp Med 209: 1069-1074, 2012.
31. Kingma B, Frijns A, Lichtenbelt WM. The thermoneutral zone: implications for metabolic studies. Front Biosci E4: 1975-1985, 2012.
32. Klaus S, Münzberg H, Trüloff C, Heldmaier G. Physiology of transgenic mice with brown fat ablation: obesity is due to lowered body temperature. Am J Physiol Regul Integr Comp Physiol 274: R287-R293, 1998.
33. Kleiber M. The Fire of Life: An Introduction to Animal Energetics. New York: Wiley, 1961.
34. Koizumi A, Tsukada M, Wada Y, Masuda H, Weindruch R. Mitotic activity in mice is suppressed by energy restriction-induced torpor. J Nutr 122: 1446-1453, 1992.
35. Koizumi A, Wada Y, Tuskada M, Kayo T, Naruse M, Horiuchi K, Mogi T, Yoshioka M, Sasaki M, Miyamaura Y, Abe T, Ohtomo K, Walford RL. A tumor preventive effect of dietary restriction is antagonized by a high housing temperature through deprivation of torpor. Mech Ageing Dev 92: 67-82, 1996.
36. Kokolus KM, Capitano ML, Lee CT, Eng JWL, Waight JD, Hylander BL, Sexton S, Hong CC, Gordon CJ, Abrams SI, Repasky EA. Baseline tumor growth and immune control in laboratory mice are significantly influenced by subthermoneutral housing temperature. Proc Natl Acad Sci USA 110: 20176-20181, 2013.
37. Kokolus KM, Spangler HM, Povinelli BJ, Farren MR, Lee KP, Repasky EA. Stressful presentations: mild chronic cold stress in mice influences baseline properties of dendritic cells. Front Immunol. In Press.
38. Krebs HA. The August Krogh principle: “For many problems there is an animal on which it can be most conveniently studied”. J Exp Zool 194: 221-226, 1975.
39. Lee YH, Jung YS, Choi D. Recent advance in brown adipose physiology and its therapeutic potential. Exp Mol Med 46: e78, 2014.
40. Leon LR. The use of gene knockout mice in thermoregulation studies. J Therm Biol 30: 273-288, 2005.
41. Liu X, Rossmeisl M, McClaine J, Kozak LP. Paradoxical resistance to diet-induced obesity in UCP1-deficient mice. J Clin Invest 111: 399-407, 2003.
42. Lo Martire V, Silvani A, Bastianini S, Berteotti C, Zoccoli G. Effects of ambient temperature on sleep and cardiovascular regulation in mice: the role of hypocretin/orexin neurons. PLos One 7: e47032, 2012.
43. Lodhi IJ, Semenkovich CF. Why we should put clothes on mice. Cell Metab 9: 111-112, 2009.
44. Maloney S, Forbes C. What effect will a few degrees of climate change have on human heat balance? Implications for human activity. Int J Biometeorol 55: 147-160, 2011.
45. Meyer CW, Willershäuser M, Jastroch M, Rourke BC, Fromme T, Oelkrug R, Heldmaier G, Klingenspor M. Adaptive thermogenesis and thermal conductance in wild-type and UCP1-KO mice. Am J Physiol Regul Integr Comp Physiol 299: R1396-R1406, 2010.
46. Moragues V, Pinkerton H. Variation in morbidity and mortality of murine typhus infection in mice with changes in the environmental temperature. J Exp Med 79: 41-43, 1944.
47. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 293: E444-E452, 2007.
48. Nedergaard J, Golozoubova V, Matthias A, Asadi A, Jacobsson A, Cannon B. UCP1: the only protein able to mediate adaptive non-shivering thermogenesis and metabolic inefficiency. Biochim Biophys Acta 1504: 82-106, 2001.
49. NRC. Guide for the Care and Use of Laboratory Animals. Washington, DC: National Research Council of the National Academy of Science, 2011.
50. Okon EE. The effect of environmental temperature on the production of ultrasounds by isolated non-handled albino mouse pups. J Zool Lond 162: 71-83, 1970.
51. Overton JM. Phenotyping small animals as models for the human metabolic syndrome: thermoneutrality matters. Int J Obes 34: S53-S58, 2010.
52. Overton JM, Williams TD. Behavioral and physiologic responses to caloric restriction in mice. Physiol Behav 81: 749-754, 2004.
53. Owens B. Cell physiology: the changing colour of fat. Nature 508: S52-S53, 2014.
54. Peloso ED, Florez-Duquet M, Buchanan JB, Satinoff E. LPS fever in old rats depends on the ambient temperature. Physiol Behav 78: 651-654, 2003.
55. Prange HD, Anderson JF, Rahn H. Scaling of skeletal mass to body mass in birds and mammals. Am Nat 113: 103-122, 1979.
56. Rothwell NJ, Stock MJ. A role for brown adipose tissue in diet-induced thermogenesis. Nature 281: 31-35, 1979.
57. Rudaya AY, Steiner AA, Robbins JR, Dragic AS, Romanovsky AA. Thermoregulatory responses to lipopolysaccharide in the mouse: dependence on the dose and ambient temperature. Am J Physiol Regul Integr Comp Physiol 289: R1244-R1252, 2005.
58. Sabir IN, Killeen MJ, Grace AA, Huang CLH. Ventricular arrhythmogenesis: Insights from murine models. Progr Biophys Mol Biol 98: 208-218, 2008.
59. Schmidt-Nielsen K. Scaling. Why is Animal Size so Important? Cambridge, UK: Cambridge Univ. Press, 1984, p. 245.
60. Speakman JR, Keijer J. Not so hot: optimal housing temperatures for mice to mimic the thermal environment of humans. Mol Metab 2: 5-9, 2013.
61. Swoap SJ, Li C, Wess J, Parsons AD, Williams TD, Overton JM. Vagal tone dominates autonomic control of mouse heart rate at thermoneutrality. Am J Physiol Heart Circ Physiol 294: H1581-H1588, 2008.
62. Swoap SJ, Overton JM, Garber G. Effect of ambient temperature on cardiovascular parameters in rats and mice: a comparative approach. Am J Physiol Regul Integr Comp Physiol 287: R391-R396, 2004.
63. Wanner SP, Yoshida K, Kulchitsky VA, Ivanov AI, Kanosue K, Romanovsky AA. Lipopolysaccharide-induced neuronal activation in the paraventricular and dorsomedial hypothalamus depends on ambient temperature. PLos One 8: e75733, 2013.
64. White CR, Seymour RS. Allometric scaling of mammalian metabolism. J Exp Biol 208: 1611-1619, 2005.
65. White CR, Seymour RS. Mammalian basal metabolic rate is proportional to body mass2/3. Proc Natl Acad Sci USA 100: 4046-4049, 2003.
66. Williams TD, Chambers JB, Henderson RP, Rashotte ME, Overton JM. Cardiovascular responses to caloric restriction and thermoneutrality in C57BL/6J mice. Am J Physiol Regul Integr Comp Physiol 282: R1459-R1467, 2002.
67. Yamauchi C, Fujita S, Obara T, Ueda T. Effects of room temperature on reproduction, body and organ weights, food and water intakes, and hematology in mice. Exp Anim 32: 1-11, 1983.