Being cool: how body temperature influences ageing and longevity

Biogerontology

Volumn 16, Issue 4, 2015, Pages 383-397

  Keil, Gerald ^a   Cummings, Elizabeth ^a   de Magalhães, João Pedro ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Life extension; Metabolism; Neuroendocrine system; Rate of living theory; Thermodynamics

Indexed keywords

GROWTH HORMONE; GROWTH HORMONE RECEPTOR; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN C; THYROTROPIN; UNCOUPLING PROTEIN 2;

AGING; BODY FAT; BODY TEMPERATURE; BROWN ADIPOSE TISSUE; CALORIC RESTRICTION; DNA DAMAGE; ENERGY METABOLISM; ENVIRONMENTAL TEMPERATURE; HEAT STRESS; HETEROCEPHALUS; HIBERNATION; HUMAN; INVERTEBRATE; LIFE EXTENSION; LIFE HISTORY TRAIT; LIFESPAN; LONGEVITY; METABOLIC RATE; NEUROENDOCRINE SYSTEM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SPECIES DIFFERENCE; SURVIVAL RATE; THERMODYNAMICS; VERTEBRATE; AGE; ANIMAL; BIOLOGICAL MODEL; MOLE RAT; PHYSIOLOGY; THERMOREGULATION;

AGE FACTORS; AGING; ANIMALS; BODY TEMPERATURE REGULATION; CALORIC RESTRICTION; HUMANS; LONGEVITY; MODELS, BIOLOGICAL; MOLE RATS; SPECIES SPECIFICITY; THERMODYNAMICS;

EID: 84933677356     PISSN: 13895729     EISSN: 15736768     Source Type: Journal    
DOI: 10.1007/s10522-015-9571-2     Document Type: Review

References (112)

1. Andrews MT (2007) Advances in molecular biology of hibernation in mammals. BioEssays 29:431–440. doi:10.1002/bies.20560
2. Angilletta MJ Jr, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509. doi:10.1093/icb/44.6.498
3. Bartke A (2011) Growth hormone, insulin and aging: the benefits of endocrine defects. Exp Gerontol 46:108–111. doi:10.1016/j.exger.2010.08.020
4. Bartke A, Westbrook R (2012) Metabolic characteristics of long-lived mice. Front Genet 3:288. doi:10.3389/fgene.2012.00288
5. Bartke A, Coschigano K, Kopchick J, Chandrashekar V, Mattison J, Kinney B, Hauck S (2001) Genes that prolong life: relationships of growth hormone and growth to aging and life span. J Gerontol Ser A Biol Sci Med Sci 56:B340–B349
6. Beverton RJH (1987) Longevity in fish: some ecological and evolutionary considerations. In: Woodhead AD, Beverton RJH (eds) Evolution in animals. Plenum Press, New York, pp 161–185
7. Bozhkov A, Nikitchenko YV (2014) Thermogenesis and longevity in mammals. Thyroxin model of accelerated aging. Exp Gerontol 60:173–182
8. Bridge MW, Weller AS, Rayson M, Jones DA (2003) Ambient temperature and the pituitary hormone responses to exercise in humans. Exp Physiol 88:627–635
9. Brown-Borg HM, Borg KE, Meliska CJ, Bartke A (1996) Dwarf mice and the ageing process. Nature 384:33. doi:10.1038/384033a0
10. Buffenstein R (2008) Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species. J Comp Physiol B 178:439–445. doi:10.1007/s00360-007-0237-5
11. Buffenstein R, Yahav S (1991) Is the naked mole-rat Heterocephalus glaber a poikilothermic or poorly thermoregulating endothermic mammal? J Therm Biol 16:227–232
12. Buffenstein R, Urison NT, Woodley R, van der Westhuizen LA, Jarvis J (1996) Temperature changes during pregnancy in the subterranean naked mole-rat (Heterocephalus glaber): the role of altered body composition and basking behaviour. Mammalia 60:619–628
13. Bulog B, van der Meijden A (1992) Proteus anguinus. http://amphibiaweb.org/
14. Carrillo AE, Flouris AD (2011) Caloric restriction and longevity: effects of reduced body temperature. Ageing Res Rev 10:153–162
15. Colman RJ et al (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325:201–204. doi:10.1126/science.1173635
16. Conti B (2008) Considerations on temperature, longevity and aging. Cell Mol Life Sci 65:1626–1630
17. Conti B et al (2006) Transgenic mice with a reduced core body temperature have an increased life span. Science 314:825–828. doi:10.1126/science.1132191
18. Davidson C (1993) Californian nevada amphibian population task force. http://www.canvamphibs.com/Species/aurora.html
19. de Magalhaes JP (2013) How ageing processes influence cancer. Nat Rev Cancer 13:357–365. doi:10.1038/nrc3497
20. de Magalhaes JP, Church GM (2006) Cells discover fire: employing reactive oxygen species in development and consequences for aging. Exp Gerontol 41:1–10. doi:10.1016/j.exger.2005.09.002
21. de Magalhaes JP, Costa J, Church GM (2007) An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. J Gerontol Ser A Biol Sci Med Sci 62:149–160
22. de Magalhaes JP, Wuttke D, Wood SH, Plank M, Vora C (2012) Genome-environment interactions that modulate aging: powerful targets for drug discovery. Pharmacol Rev 64:88–101. doi:10.1124/pr.110.004499
23. Demetrius LA (2013) Boltzmann, Darwin and directionality theory. Phys Rep 530:1–85. doi:10.1016/j.physrep.2013.04.001
24. Demetrius LA, Gundlach VM (2014) Directionality theory and the entropic principle of natural selection. Entropy Switz 16:5428–5522. doi:10.3390/E16105428
25. Duffy PH, Feuers RJ, Leakey JA, Nakamura K, Turturro A, Hart RW (1989) Effect of chronic caloric restriction on physiological variables related to energy metabolism in the male Fischer 344 rat. Mech Ageing Dev 48:117–133
26. Etnier DA, Starnes WC (1993) The fishes of Tennessee. University of Tennessee Press, Knoxville
27. Farmer KJ, Sohal RS (1987) Effects of ambient temperature on free radical generation, antioxidant defenses and life span in the adult housefly, Musca domestica. Exp Gerontol 22:59–65
28. Finch CE (1990) Longevity, senescence, and the genome. The University of Chicago Press, Chicago and London
29. Florez-Duquet M, Horwitz BA, McDonald RB (1998) Cellular proliferation and UCP content in brown adipose tissue of cold-exposed aging Fischer 344 rats. Am J Physiol Regul Integr Comp Physiol 274:R196–R203
30. Gabillard JC, Weil C, Rescan PY, Navarro I, Gutierrez J, Le Bail PI (2005) Does the GH/IGF system mediate the effect of water temperature on fish growth? A review. Cybium 29:107–117
31. Gao G-Z, Perkins LE, Zalucki MP, Lu Z-Z, Ma J-H (2013) Effect of temperature on the biology of Acyrthosiphon gossypii Mordvilko (Homoptera: Aphididae) on cotton. J Pest Sci 86:167–172. doi:10.1007/s10340-012-0470-x
32. Gatti S (2002) The role of sponges in high-Antarctic carbon and silicon cycling: a modelling approach. Alfred-Wegener-Institut für Polar-und Meeresforschung, Bremerhaven
33. George JC (2009) Growth, morphology and energetics of bowhead whales (Balaena mysticetus). University of Alaska Fairbanks, Fairbanks
34. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251. doi:10.1126/science.1061967
35. Gillooly JF, Charnov EL, West GB, Savage VM, Brown JH (2002) Effects of size and temperature on developmental time. Nature 417:70–73. doi:10.1038/417070a
36. Gorbunova V, Seluanov A, Zhang Z, Gladyshev VN, Vijg J (2014) Comparative genetics of longevity and cancer: insights from long-lived rodents. Nat Rev Genet 15:531–540. doi:10.1038/nrg3728
37. Gosden R (1996) Cheating time. W. H. Freeman & Company, New York
38. Greenberg JA, Boozer CN (2000) Metabolic mass, metabolic rate, caloric restriction, and aging in male Fischer 344 rats. Mech Ageing Dev 113:37–48
39. Gunay F, Alten B, Ozsoy ED (2010) Estimating reaction norms for predictive population parameters, age specific mortality, and mean longevity in temperature-dependent cohorts of Culex quinquefasciatus Say (Diptera: Culicidae). J Vector Ecol 35:354–362. doi:10.1111/j.1948-7134.2010.00094.x
40. Hauck SJ, Hunter WS, Danilovich N, Kopchick JJ, Bartke A (2001) Reduced levels of thyroid hormones, insulin, and glucose, and lower body core temperature in the growth hormone receptor/binding protein knockout mouse. Exp Biol Med (Maywood) 226:552–558
41. Hayflick L (2007) Biological aging is no longer an unsolved problem. Ann N Y Acad Sci 1100:1–13. doi:10.1196/annals.1395.001
42. Heilbronn LK et al (2006) Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: a randomized controlled trial. JAMA 295:1539–1548
43. Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York
44. Holzenberger M et al (2003) IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421:182–187. doi:10.1038/nature01298
45. Hsu CY, Chiu YC (2009) Ambient temperature influences aging in an annual fish (Nothobranchius rachovii). Aging Cell 8:726–737. doi:10.1111/j.1474-9726.2009.00525.x
46. Hunter W, Croson W, Bartke A, Gentry M, Meliska C (1999) Low body temperature in long-lived Ames dwarf mice at rest and during stress. Physiol Behav 67:433–437
47. Howard JL (1997) Ambystoma macrodactylum In: Fire effects information system. http://www.fs.fed.us/database/feis/
48. Keane M et al (2014) The naked mole rat genome resource: facilitating analyses of cancer and longevity-related adaptations. Bioinformatics. doi:10.1093/bioinformatics/btu579
49. Keane M et al (2015) Insights into the evolution of longevity from the bowhead whale genome. Cell reports 10:112–122. doi:10.1016/j.celrep.2014.12.008
50. Kelly MA, Zieba AP, Buttemer WA, Hulbert AJ (2013) Effect of temperature on the rate of ageing: an experimental study of the blowfly Calliphora stygia. PLoS One 8:e73781. doi:10.1371/journal.pone.0073781
51. Kim K, Lin YR, Park Y (2010) Enhancement of stress resistances and downregulation of Imd pathway by lower developmental temperature in Drosophila melanogaster. Exp Gerontol 45:984–987. doi:10.1016/j.exger.2010.08.033
52. Koizumi A et al (1996) A tumor preventive effect of dietary restriction is antagonized by a high housing temperature through deprivation of torpor. Mech Ageing Dev 92:67–82
53. Kontani Y et al (2005) UCP1 deficiency increases susceptibility to diet-induced obesity with age. Aging Cell 4:147–155
54. Lane MA et al (1996) Calorie restriction lowers body temperature in rhesus monkeys, consistent with a postulated anti-aging mechanism in rodents. Proc Natl Acad Sci 93:4159–4164
55. Lapointe J, Hekimi S (2010) When a theory of aging ages badly. Cell Mol Life Sci 67:1–8. doi:10.1007/s00018-009-0138-8
56. Larkin S et al (1997) Regulation of the third member of the uncoupling protein family, UCP3, by cold and thyroid hormone. Biochem Biophys Res Commun 240:222–227
57. Lee S-J, Kenyon C (2009) Regulation of the longevity response to temperature by thermosensory neurons in Caenorhabditis elegans. Curr Biol 19:715–722
58. Leiser SF, Begun A, Kaeberlein M (2011) HIF-1 modulates longevity and healthspan in a temperature-dependent manner. Aging Cell 10:318–326. doi:10.1111/j.1474-9726.2011.00672.x
59. Liao CY, Rikke BA, Johnson TE, Gelfond JA, Diaz V, Nelson JF (2011) Fat maintenance is a predictor of the murine lifespan response to dietary restriction. Aging Cell 10:629–639
60. Lin L, Lee JH, Bongmba OY, Ma X, Zhu X, Sheikh-Hamad D, Sun Y (2014) The suppression of ghrelin signaling mitigates age-associated thermogenic impairment. Aging Albany N Y 6:1019–1032
61. Lindahl T, Nyberg B (1972) Rate of depurination of native deoxyribonucleic acid. Biochemistry 11:3610–3618
62. Liu YH, Tsai JH (2000) Effects of temperature on biology and life table parameters of the Asian citrus psyllid, Diaphorina citri Kuwayama (Homoptera: Psyllidae). Ann Appl Biol 137:201–206. doi:10.1111/j.1744-7348.2000.tb00060.x
63. Liu RK, Walford RL (1966) Increased growth and life-span with lowered ambient temperature in the annual fish Cynolebias adloffi. Nature 212:1277–1278
64. Liu RK, Walford RL (1972) The effect of lowered body temperature on lifespan and immune and non-immune processes. Gerontologia 18:363–388
65. Liu RK, Walford RL (1975) Mid-life temperature-transfer effects on life-span of annual fish. J Gerontol 30:129–131
66. Loeb J, Northrop JH (1916) Is there a temperature coefficient for the duration of life? Proc Natl Acad Sci USA 2:456–457. doi:10.1073/Pnas.2.8.456
67. MacArthur J, Baillie W (1929) Metabolic activity and duration of life. I. Influence of temperature on longevity in Daphnia magna. J Exp Zool 53:221–242
68. Mair W, Goymer P, Pletcher SD, Partridge L (2003) Demography of dietary restriction and death in Drosophila. Science 301:1731–1733
69. Masoro EJ (2005) Overview of caloric restriction and ageing. Mech Ageing Dev 126:913–922
70. Matadha D, Hamilton GC, Lashomb JH (2004) Effect of temperature on development, fecundity, and life table parameters of Encarsia citrina Craw (Hymenoptera: Aphelinidae), a parasitoid of Euonymus scale, Unaspis euonymi (Comstock), and Quadraspidiotus perniciosus (Comstock) (Homoptera: Diaspididae). Environ Entomol 33:1185–1191
71. Mattison JA et al (2012) Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 489:318–321. doi:10.1038/nature11432
72. McCarter RJ, Palmer J (1992) Energy metabolism and aging: a lifelong study of Fischer 344 rats. Am J Physiol 263:E448–E452
73. McDougall SJ, Mills NJ (1997) The influence of hosts, temperature and food sources on the longevity of Trichogramma platneri. Entomol Exp Appl 83:195–203
74. McKinney ML, McNamara KJ (1991) Heterochrony: the evolution of ontogeny. Plenum, New York
75. McNab BK (1980) On estimating thermal conductance in endotherms. Physiol Zool 53:145–156
76. Miquel J, Lundgren PR, Bensch KG, Atlan H (1976) Effects of temperature on the life span, vitality and fine structure of Drosophila melanogaster. Mech Ageing Dev 5:347–370
77. Mobbs CV et al (2001) Neuroendocrine and pharmacological manipulations to assess how caloric restriction increases life span. J Gerontol Ser A 56:34–44
78. Munch SB, Salinas S (2009) Latitudinal variation in lifespan within species is explained by the metabolic theory of ecology. Proc Natl Acad Sci USA 106:13860–13864. doi:10.1073/pnas.0900300106
79. Pakyari H, Fathipour Y, Enkegaard A (2011) Effect of temperature on life table parameters of predatory thrips Scolothrips longicornis (Thysanoptera: Thripidae) fed on twospotted spider mites (Acari: Tetranychidae). J Econ Entomol 104:799–805. doi:10.1603/ec10144
80. Pandey AK, Tripathi CPM (2008) Effect of temperature on the development, fecundity, progeny sex ratio and life-table of Campoletis chlorideae, an endolarval parasitoid of the pod borer, Helicoverpa armigera. Biocontrol 53:461–471. doi:10.1007/s10526-007-9083-3
81. Patnaik B, Mahapatro N, Jena B (1994) Ageing in fishes. Gerontology 40:113–132
82. Pauly D (1980) On the interrelationships between natural mortality, growth parameters, and mean environmental temperature in 175 fish stocks. ICES J Mar Sci 39:175–192
83. Pfannenberg C et al (2010) Impact of age on the relationships of brown adipose tissue with sex and adiposity in humans. Diabetes 59:1789–1793. doi:10.2337/db10-0004
84. Portner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A 132:739–761
85. Ragland SS, Sohal RS (1975) Ambient temperature, physical activity and aging in the housefly, Musca domestica. Exp Gerontol 10:279–289
86. Rikke BA, Johnson TE (2004) Lower body temperature as a potential mechanism of life extension in homeotherms. Exp Gerontol 39:927–930
87. Rikke BA, Johnson TE (2007) Physiological genetics of dietary restriction: uncoupling the body temperature and body weight responses. Am J Physiol Regul Integr Comp Physiol 293:R1522–R1527. doi:10.1152/ajpregu.00215.2007
88. Roth GS et al (2002) Biomarkers of caloric restriction may predict longevity in humans. Science 297:811–811
89. Sanchez-Alavez M, Alboni S, Conti B (2011) Sex-and age-specific differences in core body temperature of C57Bl/6 mice. Age 33:89–99
90. Sarup P, Sørensen P, Loeschcke V (2014) The long-term effects of a life-prolonging heat treatment on the Drosophila melanogaster transcriptome suggest that heat shock proteins extend lifespan. Exp Gerontol 50:34–39
91. Soare A, Cangemi R, Omodei D, Holloszy JO, Fontana L (2011) Long-term calorie restriction, but not endurance exercise, lowers core body temperature in humans. Aging (Albany NY) 3:374
92. Speakman JR (2005) Body size, energy metabolism and lifespan. J Exp Biol 208:1717–1730. doi:10.1242/jeb.01556
93. Speakman JR et al (2004) Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3:87–95
94. Spindler SR (2010) Caloric restriction: from soup to nuts. Ageing Res Rev 9:324–353. doi:10.1016/j.arr.2009.10.003
95. Sramkova D et al (2007) The UCP1 gene polymorphism A-3826G in relation to DM2 and body composition in Czech population. Exp Clin Endocrinol Diabetes 115:303–307
96. Tacutu R et al (2013) Human ageing genomic resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Res 41:D1027–D1033. doi:10.1093/nar/gks1155
97. Trudgill DL, Honek A, Li D, Van Straalen NM (2005) Thermal time-concepts and utility. Ann Appl Biol 146:1–14. doi:10.1111/j.1744-7348.2005.04088.x
98. Turbill C, Bieber C, Ruf T (2011) Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc R Soc B 278:3355–3363
99. Valenzano DR, Terzibasi E, Cattaneo A, Domenici L, Cellerino A (2006) Temperature affects longevity and age-related locomotor and cognitive decay in the short-lived fish Nothobranchius furzeri. Aging Cell 5:275–278. doi:10.1111/j.1474-9726.2006.00212.x
100. Van Voorhies WA, Ward S (1999) Genetic and environmental conditions that increase longevity in Caenorhabditis elegans decrease metabolic rate. Proc Natl Acad Sci USA 96:11399–11403
101. Waalen J, Buxbaum JN (2011) Is older colder or colder older? The association of age with body temperature in 18,630 individuals. J Gerontol Ser A Biol Sci Med Sci 66:487–492. doi:10.1093/gerona/glr001
102. Walford RL (1983) Maximum lifespan. WW Norton/Avon, New York
103. Walford RL, Liu RK (1965) Husbandry, life span, and growth rate of the annual fish, Cynolebias adloffi E. Ahl. Exp Gerontol 1:161–168
104. Walford RL, Spindler SR (1997) The response to calorie restriction in mammals shows features also common to hibernation: a cross-adaptation hypothesis. J Gerontol Ser A Biol Sci Med Sci 52:B179–B183
105. Wang JJ, Tsai JH (2001) Development, survival and reproduction of black citrus aphid, Toxoptera aurantii (Hemiptera: Aphididae), as a function of temperature. Bull Entomol Res 91:477–487. doi:10.1079/ber2001120
106. Wang X, Chang Q, Wang Y, Su F, Zhang S (2014) Late-onset temperature reduction can retard the aging process in aged fish via a combined action of an anti-oxidant system and the insulin/insulin-like growth factor 1 signaling pathway. Rejuvenation Res 17:507–517. doi:10.1089/rej.2014.1581
107. Warn P, Brampton M, Sharp A, Morrissey G, Steel N, Denning D, Priest T (2003) Infrared body temperature measurement of mice as an early predictor of death in experimental fungal infections. Lab Anim 37:126–131
108. White CR, Seymour RS (2003) Mammalian basal metabolic rate is proportional to body mass 2/3. Proc Natl Acad Sci USA 100:4046–4049. doi:10.1073/pnas.0436428100
109. Wilkinson GS, South JM (2002) Life history, ecology and longevity in bats. Aging Cell 1:124–131
110. Xiao R, Zhang B, Dong Y, Gong J, Xu T, Liu J, Xu X (2013) A genetic program promotes C. elegans longevity at cold temperatures via a thermosensitive TRP channel. Cell 152:806–817
111. Zhang L, Lu X (2012) Amphibians live longer at higher altitudes but not at higher latitudes. Biol J Linn Soc 106:623–632
112. Zhou Z-S, Guo J-Y, Chen H-S, Wan F-H (2010) Effects of temperature on survival, development, longevity, and fecundity of Ophraella communa (Coleoptera: Chrysomelidae), a potential biological control agent against Ambrosia artemisiifolia (Asterales: Asteraceae). Environ Entomol 39:1021–1027. doi:10.1603/en09176