Adaptive evolution in the glucose transporter 4 gene Slc2a4 in old world fruit bats (family: Pteropodidae)

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Shen, Bin ^a   Han, Xiuqun ^a   Zhang, Junpeng ^a   Rossiter, Stephen J ^b   Zhang, Shuyi ^a  

^a EAST CHINA NORMAL UNIVERSITY   (China)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; GLUCOSE TRANSPORTER 4; GLYCINE; ISOLEUCINE; PHENYLALANINE; SERINE; VALINE; GLUCOSE;

AMINO ACID SUBSTITUTION; ANIMAL TISSUE; ARTICLE; BAT; CARBOHYDRATE DIET; CONTROLLED STUDY; GENE; GENE SEQUENCE; GENETIC SELECTION; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLLOSTOMIDAE; PTEROPODIDAE; SLC2A4 GENE; ADAPTATION; ANIMAL; CHEMISTRY; CLASSIFICATION; GENETICS; METABOLISM; NECTAR; PHYLOGENY; PROTEIN TERTIARY STRUCTURE; SKELETAL MUSCLE; TRANSPORT AT THE CELLULAR LEVEL;

HEXAPODA; PHYLLOSTOMIDAE; PTEROPODIDAE;

ADAPTATION, BIOLOGICAL; AMINO ACID SUBSTITUTION; ANIMALS; BIOLOGICAL TRANSPORT; CHIROPTERA; EVOLUTION, MOLECULAR; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; MUSCLE, SKELETAL; PHYLOGENY; PLANT NECTAR; PROTEIN STRUCTURE, TERTIARY; SELECTION, GENETIC;

EID: 84859479197     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033197     Document Type: Article

References (52)

1. Kawahito S, Kitahata H, Oshita S, (2009) Problems associated with glucose toxicity: role of hyperglycemia-induced oxidative stress. World J Gastroenterol 15: 4137-4142.
2. Brunner Y, Schvartz D, Priego-Capote F, Couté Y, Sanchez JC, (2009) Glucotoxicity and pancreatic proteomics. J Proteomics 71: 576-591.
3. Shepherd PR, Kahn BB, (1999) Glucose transporters and insulin action-implications for insulin resistance and diabetes mellitus. N Engl J Med 341: 248-257.
4. Huang S, Czech MP, (2007) The GLUT4 glucose transporter. Cell Metab 5: 237-252.
5. Klip A, (2009) The many ways to regulate glucose transporter 4. Appl Physiol Nutr Metab 34: 481-487.
6. Thong FSL, Dugani CB, Klip A, (2005) Turning signals on and off: GLUT4 traffic in the insulin-signaling highway. Physiology 20: 271-284.
7. Abel ED, Peroni O, Kim JK, Kim YB, Boss O, et al. (2001) Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 409: 729-733.
8. Zisman A, Peroni OD, Abel ED, Michael MD, Mauvais-Jarvis F, et al. (2000) Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat Med 6: 924-928.
9. Altringham JD, McOwat T, Hammond L, (1998) Bats: biology and behaviour. Oxford University Press, USA.
10. Laska M, (1990) Food transit times and carbohydrate use in three phyllostomid bat species. Z Säugetierkunde 55: 49-54.
11. Keegan DJ, (1977) Aspects of the assimilation of sugars by Rousettus aegyptiacus. Comp Biochem Physiol A Physiol 58: 349-352.
12. Caviedes-Vidal E, Karasov WH, Chediack JG, Fasulo V, Cruz-Neto AP, et al. (2008) Paracellular absorption: a bat breaks the mammal paradigm. PLoS ONE 3: e1425.
13. Tracy CR, McWhorter TJ, Korine C, Wojciechowski MS, Pinshow B, et al. (2007) Absorption of sugars in the Egyptian fruit bat (Rousettus aegyptiacus): a paradox explained. J Exp Biol 210: 1726-1734.
14. Caviedes-Vidal E, McWhorter TJ, Lavin SR, Chediack JG, Tracy CR, et al. (2007) The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts. Proc Natl Acad Sci USA 104: 19132-19137.
15. Michelmore AJ, Keegan DJ, Kramer B, (1998) Immunocytochemical identification of endocrine cells in the pancreas of the fruit bat, Rousettus aegyptiacus. Gen Comp Endocrinol 110: 319-325.
16. Protzek AOP, Rafacho A, Viscelli BA, Bosqueiro JR, Cappelli AP, et al. (2010) Insulin and glucose sensitivity, insulin secretion and β-cell distribution in endocrine pancreas of the fruit bat Artibeus lituratus. Comp Biochem Physiol A Mol Integr Physiol 157: 142-148.
17. Suarez RK, Welch KC, Hanna SK, Herrera MLG, (2009) Flight muscle enzymes and metabolic flux rates during hovering flight of the nectar bat, Glossophaga soricina: further evidence of convergence with hummingbirds. Comp Biochem Physiol A Mol Integr Physiol 153: 136-140.
18. Kelm DH, Simon R, Kuhlow D, Voigt CC, Ristow M, (2011) High activity enables life on a high-sugar diet: blood glucose regulation in nectar-feeding bats. Proc R Soc B doi:10.1098/rspb.2011.0465.
19. Amitai O, Holtze S, Barkan S, Amichai E, Korine C, et al. (2010) Fruit bats (Pteropodidae) fuel their metabolism rapidly and directly with exogenous sugars. J Exp Biol 213: 2693-2699.
20. Welch KC, Herrera LG, Suarez RK, (2008) Dietary sugar as a direct fuel for flight in the nectarivorous bat Glossophaga soricina. J Exp Biol 211: 310-316.
21. Voigt CC, Speakman JR, (2007) Nectar-feeding bats fuel their high metabolism directly with exogenous carbohydrates. Funct Ecol 21: 913-921.
22. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
23. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
24. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
25. Posada D, (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
26. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW, (2006) GARD: a genetic algorithm for recombination detection. Bioinformatics 22: 3096-3098.
27. Kosakovsky Pond SL, Frost SDW, Muse SV, (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21: 676-679.
28. Datzmann T, von Helversen O, Mayer F, (2010) Evolution of nectarivory in phyllostomid bats (Phyllostomidae Gray, 1825, Chiroptera: Mammalia). BMC Evol Biol 10: 165.
29. Teeling EC, Springer MS, Madsen O, Bates P, O'Brien SJ, et al. (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307: 580-584.
30. Murphy WJ, Eizirik E, O'Brien SJ, Madsen O, Scally M, et al. (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294: 2348-2351.
31. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
32. Yang Z, (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15: 568-573.
33. Yang Z, Wong WSW, Nielsen R, (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107-1118.
34. Zhang J, Nielsen R, Yang Z, (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22: 2472-2479.
35. Kosakovsky Pond SL, Frost SDW, (2005) A genetic algorithm approach to detecting lineage-specific variation in selection pressure. Mol Biol Evol 22: 478-485.
36. Kosakovsky Pond SL, Murrell B, Fourment M, Frost SDW, Delport W, et al. (2011) A random effects branch-site model for detecting episodic diversifying selection. Mol Biol Evol 28: 3033-3043.
37. Yang Z, Kumar S, Nei M, (1995) A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141: 1641-1650.
38. Maddison WP, Maddison DR, (2009) Mesquite: a modular system for evolutionary analysis. Version 2.74 Available: http://mesquiteproject.org. Accessed 2010 October 3.
39. Liu Y, Xu H, Yuan X, Rossiter SJ, Zhang S, (2012) Multiple adaptive losses of alanine-glyoxylate aminotransferase mitochondrial targeting in fruit eating bats. Mol Biol Evol doi:10.1093/molbev/mss013.
40. Bielawski JP, Yang Z, (2003) Maximum likelihood methods for detecting adaptive evolution after gene duplication. J Struct Funct Genomics 3: 201-212.
41. Anisimova M, Bielawski JP, Yang Z, (2002) Accuracy and power of Bayes prediction of amino acid sites under positive selection. Mol Biol Evol 19: 950-958.
42. Yang Z, Bielawski JP, (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15: 496-503.
43. Betts MJ, Russell RB, (2003) Amino acid properties and consequences of substitutions. In: Barnes MR, Gray IC, editors. Bioinformatics for geneticists West Sussex Wiley.
44. Salas-Burgos A, Iserovich P, Zuniga F, Vera JC, Fischbarg J, (2004) Predicting the three-dimensional structure of the human facilitative glucose transporter Glut1 by a novel evolutionary homology strategy: insights on the molecular mechanism of substrate migration, and binding sites for glucose and inhibitory molecules. Biophys J 87: 2990-2999.
45. Liu Y, Han N, Franchini LF, Xu H, Pisciottano F, et al. (2011) The voltage-gated potassium channel subfamily KQT member 4 (KCNQ4) displays parallel evolution in echolocating bats. Mol Biol Evol (in press).
46. Davies KT, Cotton JA, Kirwan JD, Teeling EC, Rossiter SJ, (2011) Parallel signatures of sequence evolution among hearing genes in echolocating mammals: an emerging model of genetic convergence. Heredity doi:10.1038/hdy.2011.119.
47. Liu Y, Rossiter SJ, Han X, Cotton JA, Zhang S, (2010) Cetaceans on a molecular fast track to ultrasonic hearing. Curr Biol 20: 1834-1839.
48. Li G, Wang J, Rossiter SJ, Jones G, Cotton JA, et al. (2008) The hearing gene Prestin reunites echolocating bats. Proc Natl Acad Sci U S A 105: 13959-13964.
49. Haygood R, Fedrigo O, Hanson B, Yokoyama KD, Wray GA, (2007) Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat Genet 39: 1140-1144.
50. Tarazona-Santos E, Fabbri C, Yeager M, Magalhaes WC, Burdett L, et al. (2010) Diversity in the glucose transporter-4 gene (SLC2A4) in humans reflects the action of natural selection along the Old-World primates evolution. PLoS ONE 5: e9827.
51. Yuan L, Zhao X, Lin B, Rossiter SJ, He L, et al. (2011) Adaptive evolution of Leptin in heterothermic bats. PLoS ONE 6: e27189.
52. Yang J, Wang ZL, Zhao XQ, Wang DP, Qi DL, et al. (2008) Natural selection and adaptive evolution of Leptin in the Ochotona family driven by the cold environmental stress. PLoS ONE 3: e1472.