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Functional Evolution of Leptin of Ochotona curzoniae in Adaptive Thermogenesis Driven by Cold Environmental Stress

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 s...

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Autores principales: Yang, Jie, Bromage, Timothy G., Zhao, Qian, Xu, Bao Hong, Gao, Wei Li, Tian, Hui Fang, Tang, Hui Jun, Liu, Dian Wu, Zhao, Xin Quan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3116822/
https://www.ncbi.nlm.nih.gov/pubmed/21698227
http://dx.doi.org/10.1371/journal.pone.0019833
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author Yang, Jie
Bromage, Timothy G.
Zhao, Qian
Xu, Bao Hong
Gao, Wei Li
Tian, Hui Fang
Tang, Hui Jun
Liu, Dian Wu
Zhao, Xin Quan
author_facet Yang, Jie
Bromage, Timothy G.
Zhao, Qian
Xu, Bao Hong
Gao, Wei Li
Tian, Hui Fang
Tang, Hui Jun
Liu, Dian Wu
Zhao, Xin Quan
author_sort Yang, Jie
collection PubMed
description 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.
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spelling pubmed-31168222011-06-22 Functional Evolution of Leptin of Ochotona curzoniae in Adaptive Thermogenesis Driven by Cold Environmental Stress Yang, Jie Bromage, Timothy G. Zhao, Qian Xu, Bao Hong Gao, Wei Li Tian, Hui Fang Tang, Hui Jun Liu, Dian Wu Zhao, Xin Quan PLoS One Research Article 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. Public Library of Science 2011-06-16 /pmc/articles/PMC3116822/ /pubmed/21698227 http://dx.doi.org/10.1371/journal.pone.0019833 Text en Yang et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Yang, Jie
Bromage, Timothy G.
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
title Functional Evolution of Leptin of Ochotona curzoniae in Adaptive Thermogenesis Driven by Cold Environmental Stress
title_full Functional Evolution of Leptin of Ochotona curzoniae in Adaptive Thermogenesis Driven by Cold Environmental Stress
title_fullStr Functional Evolution of Leptin of Ochotona curzoniae in Adaptive Thermogenesis Driven by Cold Environmental Stress
title_full_unstemmed Functional Evolution of Leptin of Ochotona curzoniae in Adaptive Thermogenesis Driven by Cold Environmental Stress
title_short Functional Evolution of Leptin of Ochotona curzoniae in Adaptive Thermogenesis Driven by Cold Environmental Stress
title_sort functional evolution of leptin of ochotona curzoniae in adaptive thermogenesis driven by cold environmental stress
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3116822/
https://www.ncbi.nlm.nih.gov/pubmed/21698227
http://dx.doi.org/10.1371/journal.pone.0019833
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