Abstract
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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Hafner M S, Nadler S A. Phylogenetic trees support the coevolution of parasites and their hosts. Nature, 1988, 332: 258–259
Fryxell K J. The coevolution of gene family trees. Trends Genet, 1996, 12: 364–369
Pellegrini M, Marcotte E M, Thompson M J, et al. Assigning protein functions by comparative genome analysis: Protein phylogenetic profiles. Proc Natl Acad Sci USA, 1999, 96: 4285–4288
Swanson W J, Yang Z, Wolfner M F, et al. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc Natl Acad Sci USA, 2001, 98: 2509–2514
Panhuis T M, Clark N L, Swanson W J. Rapid evolution of reproductive proteins in abalone and Drosophila. Philos Trans R Soc Lond B Biol Sci, 2006, 361: 261–268
Marcotte E M, Pellegrini M, Thompson M J, et al. A combined algorithm for genome-wide prediction of protein function. Nature, 1999, 402: 83–86
Fraser H B, Hirsh A E, Wall D P, et al. Coevolution of gene expression among interacting proteins. Proc Natl Acad Sci USA, 2004, 101: 9033–9038
Goh C S, Bogan A A, Joachimiak M, et al. Co-evolution of proteins with their interaction partners. J Mol Biol, 2000, 299: 283–293
McPartland J M, Norris R W, Kilpatrick C W. Coevolution between cannabinoid receptors and endocannabinoid ligands. Gene, 2007, 397: 126–135
Golozoubova V, Hohtola E, Matthias A, et al. Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold. Faseb J, 2001, 15: 2048–2050
Yang J, Wang Z L, Zhao X Q, et al. Natural selection and adaptive evolution of leptin in the ochotona family driven by the cold environmental stress. PLoS ONE, 2008, 3: e1472
Takada I, Kato S. PPARs target genes. Nippon Rinsho, 2005, 63: 573–577
Qian H, Hausman G J, Compton M M, et al. Leptin regulation of peroxisome proliferator-activated receptor-gamma, tumor necrosis factor, and uncoupling protein-2 expression in adipose tissues. Biochem Biophys Res Commun, 1998, 246: 660–667
Scarpace P J, Matheny M. Leptin induction of UCP1 gene expression is dependent on sympathetic innervation. Am J Physiol, 1998, 275(2 Pt 1): E259–264
Cannon B, Nedergaard J. Brown adipose tissue: Function and physiological significance. Physiol Rev, 2004, 84: 277–359
Kershaw E E, Flier J S. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab, 2004, 89: 2548–2556
Trayhurn P, Beattie J H. Physiological role of adipose tissue: white adipose tissue as an endocrine and secretory organ. Proc Nutr Soc, 2001, 60: 329–339
Himms-Hagen J. Brown adipose tissue thermogenesis: Interdisciplinary studies. Faseb J, 1990, 4: 2890–2898
Jansky L. Humoral thermogenesis and its role in maintaining energy balance. Physiol Rev, 1995, 75: 237–259
Rothwell N J, Stock M J. Biological distribution and significance of brown adipose tissue. Comp Biochem Physiol A, 1985, 82: 745–751
Cinti S. Adipocyte differentiation and transdifferentiation: Plasticity of the adipose organ. J Endocrinol Invest, 2002, 25: 823–835
Reidy S P, Weber J. Leptin: An essential regulator of lipid metabolism. Comp Biochem Physiol A Mol Integr Physiol, 2000, 125: 285–298
Zhang Y, Proenca R, Maffei M, et al. Positional cloning of the mouse obese gene and its human homologue. Nature, 1994, 372: 425–432
Campfield L A, Smith F J, Guisez Y, et al. Recombinant mouse OB protein: Evidence for a peripheral signal linking adiposity and central neural networks. Science, 1995, 269: 546–549
Chen H, Charlat O, Tartaglia L A, et al. Evidence that the diabetes gene encodes the leptin receptor: Identification of a mutation in the leptin receptor gene in db/db mice. Cell, 1996, 84: 491–495
Lee G H, Proenca R, Montez J M, et al. Abnormal splicing of the leptin receptor in diabetic mice. Nature, 1996, 379: 632–635
Fujii H. PPARs-mediated intracellular signal transduction. Nippon Rinsho, 2005, 63: 565–571
Dreyer C, Krey G, Keller H, et al. Control of the peroxisomal beta-oxidation pathway by a novel family of nuclear hormone receptors. Cell, 1992, 68: 879–887
Kliewer S A, Forman B M, Blumberg B, et al. Differential expression and activation of a family of murine peroxisome proliferator-activated receptors. Proc Natl Acad Sci USA, 1994, 91: 7355–7359
Tontonoz P, Hu E, Devine J, et al. PPAR gamma 2 regulates adipose expression of the phosphoenolpyruvate carboxykinase gene. Mol Cell Biol, 1995, 15: 351–357
Carriere F, Barrowman J A, Verger R, et al. Secretion and contribution to lipolysis of gastric and pancreatic lipases during a test meal in humans. Gastroenterology, 1993, 105: 876–888
Pruitt K D, Tatusova T, Maglott D R. NCBI Reference Sequence (RefSeq): A curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res, 2005, 33(Database issue): D501–D504
Thompson J D, Gibson T J, Plewniak F, et al. The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res, 1997, 25: 4876–4882
Kumar S, Tamura K, Nei M. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform, 2004, 5: 150–163
Springer M S, Burk-Herrick A, Meredith R, et al. The adequacy of morphology for reconstructing the early history of placental mammals. Syst Biol, 2007, 56: 673–684
Murphy W J, Eizirik E, Johnson W E, et al. Molecular phylogenetics and the origins of placental mammals. Nature, 2001, 409: 614–618
Yang Z. PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci, 1997, 13: 555–556
Nielsen R, Yang Z. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics, 1998, 148: 929–936
Huelsenbeck J P, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 2001, 17: 754–755
Yang Z, Wong W S, Nielsen R. Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol, 2005, 22: 1107–1118
Rossiter S J, Ransome R D, Faulkes C G, et al. Mate fidelity and intra-lineage polygyny in greater horseshoe bats. Nature, 2005, 437: 408–411
Yang Z, Nielsen R. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol, 2002, 19: 908–917
MacDougald O A, Lane M D. Transcriptional regulation of gene expression during adipocyte differentiation. Annu Rev Biochem, 1995, 64: 345–373
Berglund A C, Wallner B, Elofsson A, et al. Tertiary windowing to detect positive diversifying selection. J Mol Evol, 2005, 60: 499–504
Benner S A, Caraco M D, Thomson J M, et al. Planetary biology—paleontological, geological, and molecular histories of life. Science, 2002, 296: 864–868
Gaucher E A, Miyamoto M M, Benner S A. Evolutionary, structural and biochemical evidence for a new interaction site of the leptin obesity protein. Genetics, 2003, 163: 1549–1553
Benner S A, Trabesinger N, Schreiber D. Post-genomic science: converting primary structure into physiological function. Adv Enzyme Regul, 1998, 38: 155–180
Hughes D A, Jastroch M, Stoneking M, et al. Molecular evolution of UCP1 and the evolutionary history of mammalian non-shivering thermogenesis. BMC Evol Biol, 2009, 9: 4
Saito S, Saito C T, Shingai R. Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals. Gene, 2008, 408: 37–44
Matsubara M, Maruoka S, Katayose S. Inverse relationship between plasma adiponectin and leptin concentrations in normal-weight and obese women. Eur J Endocrinol, 2002, 147: 173–180
Cancello R, Zingaretti M C, Sarzani R, et al. Leptin and UCP1 genes are reciprocally regulated in brown adipose tissue. Endocrinology, 1998, 139: 4747–4750
Ahima R S, Prabakaran D, Mantzoros C, et al. Role of leptin in the neuroendocrine response to fasting. Nature, 1996, 382: 250–252
Caro J F, Sinha M K, Kolaczynski J W, et al. Leptin: the tale of an obesity gene. Diabetes, 1996, 45: 1455–1462
Zhang F, Basinski M B, Beals J M, et al. Crystal structure of the obese protein leptin-E100. Nature, 1997, 387: 206–209
Hiroike T, Higo J, Jingami H, et al. Homology modeling of human leptin/leptin receptor complex. Biochem Biophys Res Commun, 2000, 275: 154–158
Grasso P, White D W, Tartaglia L A, et al. Inhibitory effects of leptin-related synthetic peptide 116–130 on food intake and body weight gain in female C57BL/6J ob/ob mice may not be mediated by peptide activation of the long isoform of the leptin receptor. Diabetes, 1999, 48: 2204–2209
Winkler F K, D’Arcy A, Hunziker W. Structure of human pancreatic lipase. Nature, 1990, 343: 771–774
Schmitt A, Gutierrez G J, Lenart P, et al. Histone H3 phosphorylation during Xenopus oocyte maturation: Regulation by the MAP kinase/p90Rsk pathway and uncoupling from DNA condensation. FEBS Lett, 2002, 518: 23–28
Shapiro L, Scherer P E. The crystal structure of a complement-1q family protein suggests an evolutionary link to tumor necrosis factor. Curr Biol, 1998, 8: 335–338
Engel J, Prockop D J. The zipper-like folding of collagen triple helices and the effects of mutations that disrupt the zipper. Annu Rev Biophys Biophys Chem, 1991, 20: 137–152
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published with open access at Springerlink.com
Rights and permissions
This article is published under an open access license. Please check the 'Copyright Information' section either on this page or in the PDF for details of this license and what re-use is permitted. If your intended use exceeds what is permitted by the license or if you are unable to locate the licence and re-use information, please contact the Rights and Permissions team.
About this article
Cite this article
Lin, B., Yuan, L. & Chen, J. Selection pressure drives the co-evolution of several lipid metabolism genes in mammals. Chin. Sci. Bull. 57, 877–885 (2012). https://doi.org/10.1007/s11434-011-4862-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11434-011-4862-8