Functional evolution of leptin of Ochotona curzoniae in adaptive thermogenesis driven by cold environmental stress

Jie Yang, Timothy Bromage, Qian Zhao, Bao Hong Xu, Wei Li Gao, Hui Fang Tian, Hui Jun Tang, Dian Wu Liu, Xin Quan Zhao

Research output: Contribution to journalArticle

Abstract

Background: Environmental stress can accelerate the directional selection and evolutionary rate of specific stress-response proteins to bring about new or altered functions, enhancing an organism's fitness to challenging environments. Plateau pika (Ochotona curzoniae), an endemic and keystone species on Qinghai-Tibetan Plateau, is a high hypoxia and low temperature tolerant mammal with high resting metabolic rate and non-shivering thermogenesis to cope in this harsh plateau environment. Leptin is a key hormone related to how these animals regulate energy homeostasis. Previous molecular evolutionary analysis helped to generate the hypothesis that adaptive evolution of plateau pika leptin may be driven by cold stress. Methodology/Principal Findings: To test the hypothesis, recombinant pika leptin was first purified. The thermogenic characteristics of C57BL/6J mice injected with pika leptin under warm (23±1°C) and cold (5±1°C) acclimation is investigated. Expression levels of genes regulating adaptive thermogenesis in brown adipose tissue and the hypothalamus are compared between pika leptin and human leptin treatment, suggesting that pika leptin has adaptively and functionally evolved. Our results show that pika leptin regulates energy homeostasis via reduced food intake and increased energy expenditure under both warm and cold conditions. Compared with human leptin, pika leptin demonstrates a superior induced capacity for adaptive thermogenesis, which is reflected in a more enhanced β-oxidation, mitochondrial biogenesis and heat production. Moreover, leptin treatment combined with cold stimulation has a significant synergistic effect on adaptive thermogenesis, more so than is observed with a single cold exposure or single leptin treatment. Conclusions/Significance: These findings support the hypothesis that cold stress has driven the functional evolution of plateau pika leptin as an ecological adaptation to the Qinghai-Tibetan Plateau.

Original languageEnglish (US)
Article numbere19833
JournalPLoS One
Volume6
Issue number6
DOIs
StatePublished - 2011

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Lagomorpha
Ochotona
Thermogenesis
heat production
Leptin
leptin
Ochotonidae
plateaus
cold stress
homeostasis
Homeostasis
Basal Metabolism
keystone species
Mammals
Brown Adipose Tissue
brown adipose tissue
resting metabolic rate
China
Acclimatization
energy

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Functional evolution of leptin of Ochotona curzoniae in adaptive thermogenesis driven by cold environmental stress. / Yang, Jie; Bromage, Timothy; Zhao, Qian; Xu, Bao Hong; Gao, Wei Li; Tian, Hui Fang; Tang, Hui Jun; Liu, Dian Wu; Zhao, Xin Quan.

In: PLoS One, Vol. 6, No. 6, e19833, 2011.

Research output: Contribution to journalArticle

Yang, Jie ; Bromage, Timothy ; Zhao, Qian ; Xu, Bao Hong ; Gao, Wei Li ; Tian, Hui Fang ; Tang, Hui Jun ; Liu, Dian Wu ; Zhao, Xin Quan. / Functional evolution of leptin of Ochotona curzoniae in adaptive thermogenesis driven by cold environmental stress. In: PLoS One. 2011 ; Vol. 6, No. 6.
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