Considerations on Temperature, Longevity and Aging

Conti, Bruno

doi:10.1007/s00018-008-7536-1

Cited by 105 publications

(96 citation statements)

References 48 publications

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“…Temperature robustly impacts longevity in both poikilotherms and homeotherms (4,(6)(7)(8)(9)(10)(11). Elucidation of the underlying mechanisms will greatly contribute to the understanding of aging and age-related disease across species.…”

Section: Discussionmentioning

confidence: 99%

“…Longevity-promoting genes include components of the insulin-like signaling pathway, the histone deacetylase Sir2, the GTPase Ras, TRP membrane channels, and transcription factors, among many others (1,2). Environmental manipulations extending life include changes in nutrition (often referred to as caloric or dietary restriction), sexual/reproductive history, and ambient temperature (3)(4)(5).…”

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confidence: 99%

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The 4E-BP growth pathway regulates the effect of ambient temperature on Drosophila metabolism and lifespan

Carvalho

Drago

Hoxha

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Changes in body temperature can profoundly affect survival. The dramatic longevity-enhancing effect of cold has long been known in organisms ranging from invertebrates to mammals, yet the underlying mechanisms have only recently begun to be uncovered. In the nematode Caenorhabditis elegans, this process is regulated by a thermosensitive membrane TRP channel and the DAF-16/FOXO transcription factor, but in more complex organisms the underpinnings of cold-induced longevity remain largely mysterious. We report that, in Drosophila melanogaster, variation in ambient temperature triggers metabolic changes in protein translation, mitochondrial protein synthesis, and posttranslational regulation of the translation repressor, 4E-BP (eukaryotic translation initiation factor 4E-binding protein). We show that 4E-BP determines Drosophila lifespan in the context of temperature changes, revealing a genetic mechanism for cold-induced longevity in this model organism. Our results suggest that the 4E-BP pathway, chiefly thought of as a nutrient sensor, may represent a master metabolic switch responding to diverse environmental factors.S tudies on the biological underpinnings of aging have uncovered numerous genetic and environmental factors regulating animal lifespan. Longevity-promoting genes include components of the insulin-like signaling pathway, the histone deacetylase Sir2, the GTPase Ras, TRP membrane channels, and transcription factors, among many others (1, 2). Environmental manipulations extending life include changes in nutrition (often referred to as caloric or dietary restriction), sexual/reproductive history, and ambient temperature (3-5).Of the factors known to impact aging, temperature is arguably the most promising. Lifespan extension by cold is evolutionarily conserved-documented in poikilotherms, such as worms and flies, and homeotherms, including mammals (4, 6-11)-and more robust than well-studied interventions such as dietary restriction (12, 13). However, the underlying mechanisms remain incompletely understood (10,14,15). In Caenorhabditis elegans, the effect of cold on survival involves the thermosensitive membrane channel TRPA-1 acting upstream of the DAF-16/FOXO transcription factor (14,15). This seminal finding countered the notion that longevity is the passive result of general thermodynamic changes, and favored instead the view that genetic pathways actively control lifespan in response to ambient temperature. However, these results have to date not been extended or replicated in other model organisms. Explanatory theories for the effect of cold on longevity include a reduction in reactive oxygen species generated by mitochondrial uncoupling proteins, suppression of autoimmune response, and changes in neuroendocrine factors (6,16,17), but these views remain largely speculative given the lack of further mechanistic insight into lifespan extension by cold in model organisms.We report that, in Drosophila, changes in temperature trigger a metabolic program impacting protein translation, mitochondrial prot...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

The 4E-BP growth pathway regulates the effect of ambient temperature on Drosophila metabolism and lifespan

Carvalho

Drago

Hoxha

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Body temperature declines in all species in response to caloric restriction (Roth et al 2002;Lane et al 1996;Heilbronn et al 2006), and studies of transgenic mice indicate that a lower temperature offers longevity benefits independent of caloric restriction (Conti 2008). Observations that a lower resting metabolic rate (RMR) is associated with better health and longevity Ruggiero et al 2008) also support the potential benefit of a lower basal temperature as approximately two thirds of RMR or 40-50 % of total energy expenditure is required for thermoregulation (Landsberg 2012) and a 1°C rise in temperature translates into a 10-13 % increase in metabolic rate (Du bois 1921 cited in Landsberg 2012).…”

Section: Introductionmentioning

confidence: 99%

Basal body temperature as a biomarker of healthy aging

Simonsick

Meier

Shaffer

et al. 2016

AGE

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Scattered evidence indicates that a lower basal body temperature may be associated with prolonged health span, yet few studies have directly evaluated this relationship. We examined cross-sectional and longitudinal associations between early morning oral temperature (95.0-98.6°F) and usual gait speed, endurance walk performance, fatigability, and grip strength in 762 non-frail men (52 %) and women aged 65-89 years participating in the Baltimore Longitudinal Study of Aging. Since excessive adiposity (body mass index ≥35 kg/m 2 or waist-to-height ratio ≥0.62) may alter temperature set point, associations were also examined within adiposity strata. Overall, controlling for age, race, sex, height, exercise, and adiposity, lower temperature was associated with faster gait speed, less time to walk 400 m quickly, and lower perceived exertion following 5-min of walking at 0.67 m/s (all p ≤ 0.02). In the nonadipose (N = 662), these associations were more robust (all p ≤ 0.006). Direction of association was reversed in the adipose (N = 100), but none attained significance (all p > 0.22). Over 2.2 years, basal temperature was not associated with functional change in the overall population or non-adipose. Among the adipose, lower baseline temperature was associated with greater decline in endurance walking performance (p = 0.006). In longitudinal analyses predicting future functional performance, low temperature in the non-adipose was associated with faster gait speed (p = 0.021) and less time to walk 400 m quickly (p = 0.003), whereas in the adipose, lower temperature was associated with slower gait speed (p = 0.05) and more time to walk 400 m (p = 0.008). In older adults, lower basal body temperature appears to be associated with healthy aging in the absence of excessive adiposity.

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“…Much of the variation in patterns of mortality in nature may reflect variation in the ability of organisms to respond to naturally occurring stresses (Hughes and Reynolds, 2005;Parsons, 2007;Vleck et al, 2007;Kuningas et al, 2008;Mangel, 2008) and gene-mediating stress responses, either by avoiding or repairing damage, have been shown to have large effects on lifespan (Schumacher et al, 2008). We have no measures of oxidative or other physiological stressors (Conti, 2008), and how they vary with temperature, in C. maculatus. However, using temperature effects on larval survivorship as proxies for the degree of stress experienced by C. maculatus at the temperatures used in this experiment, our treatments range from fairly benign (25 1C) to stressful (the two extremes; , and the sex difference in the inbreeding load is greatest at the intermediate, benign, temperature and smallest at the most stressful temperatures.…”

Section: Discussionmentioning

confidence: 99%

Environmental effects on sex differences in the genetic load for adult lifespan in a seed-feeding beetle

Fox

Stillwell

2009

Heredity

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We have little understanding of how environmental conditions affect the expression of the genetic load for lifespan and adult mortality rates, or how this environmental dependence affect tests of models for the evolution of senescence. We use the seed-feeding beetle, Callosobruchus maculatus, as a model to explore how the inbreeding load (L) affecting adult lifespan varies with rearing conditions (diet and temperature), and how rearing conditions affect tests of the mutation accumulation model of senescence. When reared under benign conditions, there was a large sex difference in inbreeding depression (d) and the inbreeding load (L ¼ 0.51-0.86 lethal equivalents per gamete for females L ¼ B0 for males). This sex difference in L was dependent on temperature, but not on rearing host or heat shock. At both high and low temperatures (relative to intermediate temperature) L increased for males, and L converged for the sexes at low temperature (L ¼ 0.26-0.53 for both sexes). Correlations were small for L between pairs of temperatures, indicating that the genes responsible for the inbreeding load differed between temperatures. In contrast to predictions of the mutation accumulation model of senescence, the agespecific inbreeding load for the adult mortality rate (L u(t) ) did not increase with age in any rearing environment. The genetic load underlying lifespan and adult mortality rates, and large sex differences in the genetic load, is highly dependent on environmental conditions. Estimating the genetic load in benign laboratory environments may be insufficient to predict the genetics underlying lifespan variation in nature where environmental variation is the norm.

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Considerations on Temperature, Longevity and Aging

Abstract: A modest reduction in body temperature prolongs longevity and possibly retards aging in both poikilotherm and homeotherm animals. Some of the possible mechanisms mediating these effects are considered here with respect to major aging models and theories.

Cited by 105 publications

References 48 publications

The 4E-BP growth pathway regulates the effect of ambient temperature on Drosophila metabolism and lifespan

The 4E-BP growth pathway regulates the effect of ambient temperature on Drosophila metabolism and lifespan

Basal body temperature as a biomarker of healthy aging

Environmental effects on sex differences in the genetic load for adult lifespan in a seed-feeding beetle

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