Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals

Saito, Shigeru; Saito, Claire T.; Shingai, Ryuzo

doi:10.1016/j.gene.2007.10.018

Cited by 56 publications

(57 citation statements)

References 30 publications

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“…Many previous studies have shown that positive selection drove the adaptive evolution of leptin in many lineages in Haplorrhini [44][45][46][47] and of UCP1 in Eutheria [48,49]. These results are similar to our findings that positive selection occurred in the superorders of Laurasiatheria and Euarchontoglires and in the suborder of Haplorrhini.…”

Section: Discussionsupporting

confidence: 91%

Selection pressure drives the co-evolution of several lipid metabolism genes in mammals

Lin¹,

Yuan

Chen

2011

Chin. Sci. Bull.

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Adipose tissue is an important endocrine organ and energy supplier. Its physiological effect on the regulation of the energy balance is considered an important factor underlying the evolution of mammals. To test whether the genes controlling lipid metabolism have undergone adaptive molecular change in the evolution of mammals, in this study, we used the orthologous gene sequences of 12 important lipid metabolism proteins (leptin, OB-RL, RXRA, RXRB, RXRG, PPARA, PPARB/D, PPARG, PNLIP, ADIPOQ, LPL and UCP1) from NCBI's databases. We found evidence that 4 of the corresponding genes (leptin, ADIPOQ, PNLIP and PPARA) have undergone positive selection in their evolutionary history and that most adaptive changes occurred during the evolution of the super-clades Laurasiatheria (placentals) and suborders within Euarchontoglires (primates and rodents). Comparisons across sets of genes showed that in a third of cases, bursts of positive selection, more than would be expected by chance, occurred on corresponding branches. We propose that the positive selection drives adaptive changes in some lipid metabolism genes in or within Laurasiatheria and Euarchontoglires clades. Along with evidence from earlier studies, our results show that co-evolution among interacting lipid metabolism proteins has taken place. protein evolution; lipid metabolism; Darwinian selection, positive selection Citation:Lin B F, Yuan L H, Chen J P. Selection pressure drives the co-evolution of several lipid metabolism genes in mammals. Chin Sci Bull, 2012, 57: 877885,

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Section: Discussionsupporting

confidence: 91%

Selection pressure drives the co-evolution of several lipid metabolism genes in mammals

Lin¹,

Yuan

Chen

2011

Chin. Sci. Bull.

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“…It remains controversial as to whether UCP1 and its fatty acid activation evolved part and parcel with BAT and non-shivering thermogenesis (41,42). At the very least, our demonstration that fatty acids can acutely activate UCP1 in mitochondria from thymus shows that fatty acid-activated uncoupling does not strictly imply a thermogenic function.…”

Section: Discussionmentioning

confidence: 71%

Fatty Acids Change the Conformation of Uncoupling Protein 1 (UCP1)

Divakaruni

Humphrey

Brand

2012

Journal of Biological Chemistry

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Background: Fatty acids activate UCP1 to catalyze mitochondrial proton leak. Results: Palmitate changed the kinetics of two processes: mant-GDP binding to UCP1 and enzymatic proteolysis of UCP1. Conclusion:We present the first demonstration that fatty acids induce a conformational change in UCP1. Significance: The finding has profound implications for the mechanism of UCP1, providing crucial insights into cellular metabolic inefficiency.

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“…The exact mechanism of this activation is still not fully resolved . During early mammalian evolution, UCP1 developed rapidly (Saito et al, 2008) from a probably nonthermogenic protoUCP1 that is still found in fish (Jastroch et al, 2005;Jastroch et al, 2007). UCP1 is principally found in all mammals -with the pig family being the only exception (Berg et al, 2006).…”

Section: The Mechanism Of Heat Production In Brown Adipose Tissuementioning

confidence: 99%

Nonshivering thermogenesis and its adequate measurement in metabolic studies

Cannon

Nedergaard

2011

Journal of Experimental Biology

602

610

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SummaryAlterations in nonshivering thermogenesis are presently discussed as being both potentially causative of and able to counteract obesity. However, the necessity for mammals to defend their body temperature means that the ambient temperature profoundly affects the outcome and interpretation of metabolic experiments. An adequate understanding and assessment of nonshivering thermogenesis is therefore paramount for metabolic studies. Classical nonshivering thermogenesis is facultative, i.e. it is only activated when an animal acutely requires extra heat (switched on in minutes), and adaptive, i.e. it takes weeks for an increase in capacity to develop. Nonshivering thermogenesis is fully due to brown adipose tissue activity; adaptation corresponds to the recruitment of this tissue. Diet-induced thermogenesis is probably also facultative and adaptive and due to brown adipose tissue activity. Although all mammals respond to injected/infused norepinephrine (noradrenaline) with an increase in metabolism, in non-adapted mammals this increase mainly represents the response of organs not involved in nonshivering thermogenesis; only the increase after adaptation represents nonshivering thermogenesis. Thermogenesis (metabolism) should be expressed per animal, and not per body mass [not even to any power (0.75 or 0.66)]. A 'cold tolerance test' does not examine nonshivering thermogenesis capacity; rather it tests shivering capacity and endurance. For mice, normal animal house temperatures are markedly below thermoneutrality, and the mice therefore have a metabolic rate and food consumption about 1.5 times higher than their intrinsic requirements. Housing and examining mice at normal house temperatures carries a high risk of identifying false positives for intrinsic metabolic changes; in particular, mutations/treatments that affect the animal's insulation (fur, skin) may lead to such problems. Correspondingly, true alterations in intrinsic metabolic rate remain undetected when metabolism is examined at temperatures below thermoneutrality. Thus, experiments with animals kept and examined at thermoneutrality are likely to yield an improved possibility of identifying agents and genes important for human energy balance.

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Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals

Cited by 56 publications

References 30 publications

Selection pressure drives the co-evolution of several lipid metabolism genes in mammals

Selection pressure drives the co-evolution of several lipid metabolism genes in mammals

Fatty Acids Change the Conformation of Uncoupling Protein 1 (UCP1)

Nonshivering thermogenesis and its adequate measurement in metabolic studies

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