Human-specific SNP in obesity genes, adrenergic receptor beta2 (ADRB2), beta3 (ADRB3), and PPAR γ2 (PPARG), during primate evolution

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Takenaka, Akiko ^a   Nakamura, Shin ^b   Mitsunaga, Fusako ^b   Inoue Murayama, Miho ^c   Udono, Toshifumi ^b   Suryobroto, Bambang ^d  

^a NAGOYA BUNRI UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c WILDLIFE RESEARCH CENTER OF KYOTO UNIVERSITY   (Japan)

^d BOGOR AGRICULTURAL UNIVERSITY   (Indonesia)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; BETA 2 ADRENERGIC RECEPTOR; BETA 3 ADRENERGIC RECEPTOR; GLUTAMIC ACID; GLUTAMINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROLINE;

ABDOMINAL OBESITY; ADIPOCYTE; ADRENERGIC RECEPTOR BETA 2 GENE; ADRENERGIC RECEPTOR BETA 3 GENE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENERGY BALANCE; ENERGY EXPENDITURE; ETHNIC GROUP; EVOLUTIONARY ADAPTATION; GENE; GENE FREQUENCY; GENETIC ASSOCIATION; GORILLA; HUMAN; HYLOBATES AGILIS; LIPID STORAGE; LIPOLYSIS; MACACA; MOLECULAR EVOLUTION; MUTATIONAL ANALYSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORANG UTAN; PAN TROGLODYTES; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA GENE; PRIMATE; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; THERMOGENESIS;

ANIMALS; BIOLOGICAL EVOLUTION; HUMANS; OBESITY; POLYMORPHISM, SINGLE NUCLEOTIDE; PPAR GAMMA; PRIMATES; RECEPTORS, ADRENERGIC, BETA-2; RECEPTORS, ADRENERGIC, BETA-3;

MACACA; PRIMATES;

EID: 84866627441     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043461     Document Type: Article

References (95)

1. Girardier L, Seydoux J, (1981) Is there a sympathetic regulation of the efficiency of energy utilization? Diabetologia 20: 362-365.
2. Tappy L, (1996) Thermic effect of food and sympathetic nervous system activity in humans. Reprod Nutr Dev 36: 391-397.
3. Walston J, Silver K, Bogardus C, Knowler WC, Celi FS, et al. (1995) Time of onset of non-insulin- dependent diabetes mellitus and genetic variation in the β3-adrenergic receptor gene. N Engl J Med 333: 343-347.
4. Widén E, Lehto M, Kanninen T, Walston J, Shuldiner AR, et al. (1995) Association of a polymorphism in the β3-adrenergic receptor gene with features of the insulin resistance syndrome in Finns. N Engl J Med 333: 348-351.
5. Kim-Motoyama H, Yasuda K, Yamaguchi T, Yamada N, Katakura T, et al. (1997) A mutation of the beta-3-adrenergic receptor is associated with visceral obesity but decreased serum triglyceride. Diabetologia 40: 469-472.
6. Clément K, Vaisse C, Manning BSJ, Basdevant A, Guy-Grand B, et al. (1995) Genetic variation in the β3-adrenergic receptor and an increased capacity to gain weight in patients with morbid obesity. N Engl J Med 333: 352-354.
7. Yoshida T, Sakane N, Umekawa T, Sakai M, Takahashi T, et al. (1995) Mutation of β3-adrenergic-receptor gene and response to treatment of obesity. Lancet 346: 1433-1434.
8. Piétri-Rouxel F, St John Manning B, Gros J, Strosberg AD, (1997) The biochemical effect of the naturally occurring Trp64→Arg mutation on human β3-adrenoceptor activity. Eur J Biochem 247: 1174-1179.
9. Umekawa T, Yoshida T, Sakane N, Kogure A, Kondo M, et al. (1999) Trp64Arg mutation of β3-adrenoceptor gene deteriorates lipolysis induced by β3-adrenoceptor agonist in human omental adipocytes. Diabetes 48: 117-120.
10. Kadowaki H, Yasuda K, Iwamoto K, Otabe S, Shimokawa K, et al. (1995) A mutation in the β3-adrenergic receptor gene is associated with obesity and hyperinsulinemia in Japanese subjects. Biochem Biophys Res Commun 215: 555-560.
11. Biery AJ, Ebbesson SOE, Shuldiner AR, Boyer BB, (1997) The β3-adrenergic- receptor TRP64ARG polymorphism and obesity in Alaskan Eskimos. Int J Obesity 21: 1176-1179.
12. Sakane N, Yoshida T, Umekawa T, Kondo M, Sakai Y, et al. (1997) β3-adrenergic-receptor polymorphism: a genetic maker for visceral fat obesity and the insulin resistance syndrome. Diabetologia 40: 200-204.
13. Sun L, Yoko I, Shun I, (2000) Investigation and comparison of the beta3-adrenergic receptor gene Trp64Arg mutation in the Chinese and Japanese. Zhonghua Yi Xue Za Zhi 80: 107-110.
14. Silver K, Walston J, Wang Y, Dowse G, Zimmet P, et al. (1996) Molecular scanning for mutations in the β3-adrenergic receptor gene in Nauruans with obesity and noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab 81: 4155-4158.
15. Silver K, Mitchell BD, Walston J, Sorkin JD, Stern MP, et al. (1997) Trp64Arg β3-adrenergic receptor and obesity in Mexican Americans. Hum Genet 101: 306-311.
16. Büettner R, Schäffler A, Arndt H, Rogler G, Nusser J, et al. (1998) The Trp64Arg polymorphism of the β3-adrenergic receptor gene is not associated with obesity or type 2 diabetes mellitus in a large population-based Caucasian cohort. J Clin Endocrinol Metab 83: 2892-2897.
17. Corella D, Guillén M, Portolés O, Sorlí JV, Alonso V, et al. (2001) Gender specific associations of the Trp64Arg mutation in theβ3-adregergic receptor gene with obesity-related phenotypes in a Mediterranean population: interaction with a common lipoprotein lipase gene variation. J Int Med 250: 348-360.
18. Barbe P, Millet L, Galitzky J, Lafontan M, Berlan M, (1996) In situ assessment of the role of the β1-, β2- and β3-adrenoceptors in the control of lipolysis and nutritive blood flow in human subcutaneous adipose tissue. Br J Pharmacol 117: 907-913.
19. Green SA, Turki J, Hall IP, Liggett SB, (1995) Implication of genetic valiability of human β2-adrenergic receptor structure. Pulm Phamacol 8: 1-10.
20. Large V, Hellström L, Reynisdottir S, Lönnqvist F, Eriksson P, et al. (1997) Human beta-2 adrenoceptor gene polymorphisms are highly frequent in obesity and associate with altered adipocyte beta-2 adrenoceptor function. J Clin Invest 100: 3005-3013.
21. González Sánchez JL, Proenza AM, Martínez Larrad MT, Ramis JM, Fernández Pérez C, et al. (2003) The glutamine 27 glutamic acid polymorphism of the β2-adrenoceptor gene is associated with abdominal obesity and greater risk of impaired glucose tolerance in men but not in women: a population-based study in Spain. Clin Endocrinol 59: 476-481.
22. Masuo K, Katsuya T, Kawaguchi H, Fu Y, Rakugi H, et al. (2006) β2-adrenoceptor polymorphisms relate to obesity through blunted leptin-mediated sympathetic activation. Am J Hypertens 19: 1084-1091.
23. Hellström L, Large V, Reynisdottir S, Wahrenberg H, Arner P, (1999) The different effects of a Gln27Glu β2-adrenoceptor gene polymorphism on obesity in males and in females. J Int Med 245: 253-259.
24. Ishiyama-Shigemoto S, Yamada K, Yuan X, Ichikawa F, Nonaka K, (1999) Association of polymorphisms in the β2-adrenergic receptor gene with obesity, hypertriglyceridaemia, and diabetes mellitus. Diabetologia 42: 98-101.
25. Macho-Azcarate T, Marti A, Calabuig J, Martinez JA, (2003) Basal far oxidation and after a peak oxygen consumption test in obese women with a β2 adrenoceptor gene polymorphism. J Nutr Biochem 14: 275-279.
26. Ellsworth DL, Coady SA, Chen W, Srinivasan SR, Elkasabany A, et al. (2002) Influence of the β2-adrenergic receptor Arg16Gly polymorphism on longitudinal changes in obesity from childhood through young adulthood in a biracial cohort: the Bogalusa Heart Study. Int J Obesity 26: 928-937.
27. Cagliani R, Fumagalli M, Pozzoli U, Riva S, Comi GP, et al. (2009) Diverse evolutionary histories for β-adrenoreceptor genes in humans. Am J Hum Genet 85: 64-75.
28. Wilson RH, Moran CN, Cole JJ, Pitsiladis YP, Bailey MES, (2010) Evolutionary history of the ADRB2 gene in humans. Am J Hum Genet 86: 490-500.
29. Walston J, Lowe A, Silver K, Yang Y, Bodkin NL, et al. (1997) The β3-adrenergic receptor in the obesity and diabetes prone rhesus monkey is very similar to human and contains arginine at codon 64. Gene 188: 207-213.
30. Kadowaki T, (2000) Insights into insulin resistance and type2 diabetes from knockout mouse models. J Clin Invest 106: 459-465.
31. Kubota N, Terauchi Y, Miki H, Tamemoto H, Yamauchi T, et al. (1999) PPARγ mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell 4: 597-609.
32. Yen CJ, Beamer BA, Negri C, Silver K, Brown KA, et al. (1997) Molecular scanning of the human peroxisome proliferator activated receptor γ (hPPARγ) gene in diabetic Caucasians: Identification of a Pro12Ala PPAR γ2 missense mutation. Biochem Biophys Res Commun 241: 270-274.
33. Deeb SS, Fajas L, Nemoto M, Pihlajamäki J, Mykkänen L, et al. (1998) A Pro12Ala substitution in PPARγ2 associated with decreased receptor activity, lower body mass index and improved insulin sensitivity. Nat Genet 20: 284-287.
34. Hara K, Okada T, Tobe K, Yasuda K, Mori Y, et al. (2000) The Pro12Ala polymorphism in PPARγ2 may confer resistance to type 2 diabetes. Biochem Biophys Res Commun 271: 212-216.
35. Neel JV, (1962) Diabetes mellitus: A "thrifty" genotype rendered detrimental by "progress"? Am J Hum Genet 14: 353-362.
36. Nakagawa N, (1997) Determinants of the dramatic seasonal changes in the intake of energy and protein by Japanese monkeys in a cool temperature forest. Am J Primatol 41: 267-288.
37. Symington MM, (1990) Fission-fusion social organization in Ateles and Pan. Int J Primatol 11: 47-61.
38. Tutin CEG, Ham RM, White LJT, Harrison MJS, (1997) The primate community of the Lopé Reserve, Gabon: diets, responses to fruit scarcity, and effects on biomass. Am J Primatol 42: 1-24.
39. Nakagawa N, (2000) Foraging energetics in patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus): Implications for reproductive seasonality. Am J Primatol 52: 169-185.
40. Hashimoto C, Suzuki S, Takenoshita Y, Yamagiwa J, Basabbose AK, et al. (2003) How fruit abundance affects the chimpanzee party size: a comparison between four study sites. Primates 44: 77-81.
41. Takemoto H, (2004) Seasonal change in terrestriality of chimpanzees in relation to microclimate in the tropical forest. Am J Phys Anthropol 124: 81-92.
42. Yamagiwa J, Basabose AK, (2006) Diet and seasonal changes in sympatric gorillas and chimpanzees at Kahuzi-Biega National Park. Primates 47: 74-90.
43. Thompson ME, Knott CD, (2008) Urinary C-peptide of insulin as a non-invasive marker of energy balance in wild orangutans. Horm Behav 53: 526-535.
44. Uehara S, Nishida T, (1987) Body weights of wild chimpanzees (Pan troglodytes schweinfurthii) of the Mahale Mountains National Park, Tanzania. Am J Phys Anthropol 72: 315-321.
45. Muroyama Y, Kanamori H, Kitahara E, (2006) Seasonal variation and sex differences in the nutritional status in two local populations of wild Japanese macaques. Primates 47: 355-364.
46. Harrison MJS, (1985) Time budget of the green monkey, Cercopithecus sabaeus: some optimal strategies. Int J Primatol 6: 351-376.
47. Agetsuma N, Nakagawa N, (1998) Effects of habitat differences on feeding behaviors of Japanese monkeys: comparison between Yakushima and Kinkazan. Primates 39: 275-289.
48. Kimura K, Sasaki N, Asano A, Mizukami J, Kayahashi S, et al. (2000) Mutated human beta-3-adrenergic receptor (Trp64Arg) lowers the response to beta3-adrenergic agonists in transfected 3T3-L1 predipocytes. Horm Metab Res 32: 91-96.
49. Macho-Azcarate T, Marti A, González A, Martinez JA, Ibañez J, (2002) Gln27Glu polymorphism in the beta2 adrenergic receptor gene and lipid metabolism during exercise in obese women. Int J Obesity 26: 1434-1441.
50. Haile-Selassie Y, Suwa G, White TD, (2004) Late Miocene teeth from middle Awash, Ethiopia, and early hominid dental evolution. Science 303: 1503-1505.
51. White TD, Suwa G, Asfaw B, (1994) Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 371: 306-312.
52. White TD, Asfaw B, Beyene Y, Haile-Selassie Y, Lovejoy CO, et al. (2009) Ardipithecus ramidus and the paleobiology of early hominids. Science 326: 75-86.
53. Leakey MD, Hay RL, (1979) Pliocene footprints in the Laetolil Beds at Laetoli, northern Tanzania. Nature 278: 317-323.
54. McHenry HM, Berger LR, (1998) Body proportions in Australopithecus afarensis and A. africanus and the origin of the genus Homo. J Human Evol 35: 1-22.
55. Semaw S, Renne P, Harris JWK, Feibel CS, Bernor RL, et al. (1997) 2.5-million-year-old stone tools from Gona, Ethiopia. Nature 385: 333-336.
56. Kimbel WH, Johanson DC, Rak Y, (1997) Systematic assessment of a maxilla of Homo from Hadar, Ethiopia. Am J Phys Anthropol 103: 235-262.
57. McHenry HM, (1994) Tempo and mode in human evolution. Proc Natl Acad Sci USA 91: 6780-6786.
58. Leakey MD (1976) A summary and discussion of the archaeological evidence from bed I and bed II, Olduvai Gorge, Tanzania. In: G. L. Isaac & E. McCown (eds.), Human origins: Louis Leakey and the East African evidence (pp. 431-59). Menlo Park: Staples Press.
59. Bunn HT, (1981) Archaeological evidence for meat-eating by Plio-Pleistocene hominids from Koobi Fora and Olduvai Gorge. Nature 291: 574-577.
60. Wood B, Collard M, (1999) The human genus. Science 284: 65-71.
61. Susman RL, Stern JT, (1982) Functional morphology of Homo habilis. Science 217: 931-934.
62. Harcourt-Smith WEH, Aiello LC, (2004) Fossila, feet and the evolution of human bipedal locomotion. J Anat 204: 403-416.
63. Ruff CB, Walker AC (1993) Body size and body shape. In: Walker AC, Leakey RE, editors. The nariokotome Homo erectus skeleton. Cambridge, MA: Harvard Press pp.234-265.
64. Antón SC, (2003) Natural history of Homo erectus. Yrbk Phys Anthropol 46: 126-169.
65. Aiello L, Wells JCK, (2002) Energetics and the evolution of the genus Homo. Ann Rev Anthropol 31: 323-338.
66. Lepre CJ, Roche H, Kent DV, Harmand S, Quinn RL, et al. (2011) An earlier origin for the Acheulian. Nature 477: 82-85.
67. Swisher CC III, Curtis GH, Jacob T, Getty AG, Suprijo A, et al. (1994) Age of the earliest known hominids in Java, Indonesia. Science 263: 1118-1121.
68. Gabunia L, Antón SC, Lordkipanidze D, Vekua A, Justus A, et al. (2001) Dmanisi and dispersal. Evol Anthropol 10: 158-170.
69. Cann RL, Stoneking M, Wilson AC, (1987) Mitochondrial DNA and human evolution. Nature 325: 31-36.
70. Tishkoff SA, Dietzsch E, Speed W, Pakstis AJ, Kidd JR, et al. (1996) Global patterns of linkage disequilibrium at the CD4 locus and modern human origins. Science 271: 1380-1387.
71. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, et al. (2008) Worldwide human relationships inferred from genome-wide patterns of variation. Science 319: 1100-1104.
72. Folk GE Jr, Semken HA Jr, (1991) The evolution of sweat glands. Int J Biometeorol 35: 180-186.
73. Hiley PG, (1976) The thermoregulatory responses of the galago (Galago crassicaudatus), the baboon (Papio cynocephalus) and the chimpanzee (Pan satyrus) to heat stress. J Physiol 254: 657-671.
74. Robertshaw D (1975) Catecholamines and the control of sweat glands. In Handbook of Physiology, pp.591-603. Bethesda, Md.: American Physiological Society.
75. Schwartz GG, Rosenblum LA, (1981) Allometry of primate hair density and the evolution of human hairlessness. Am J Phys Anthropol 55: 9-12.
76. Wheeler PE, (1992) The influence of the loss of functional body hair on the water budgets of early hominids. J Hum Evol 23: 379-388.
77. Shackleton NJ, Backman J, Zimmerman H, Kent DV, Hall MA, et al. (1984) Oxygen isotope calibration of the onset of ice-rafting and history of glaciation in the North Atlantic region. Nature 307: 620-623.
78. Trauth MH, Maslin MA, Deino AL, Strecker MR, Bergner AGN, et al. (2007) High- and low-latitude forcing of Plio-Pleistocene east African climate and human evolution. J Hum Evol 53: 475-486.
79. Levin NE, Quade J, Simpson SW, Semaw S, Rogers M, (2004) Isotopic evidence for Plio-Pleistocene environmental change at Gona, Ethiopia. Earth Planet Sci Lett 219: 93-110.
80. Wynn JG, (2004) Influence of Plio-Pleistocene aridification on human evolution: Evidence from paleosols of theTurkana Basin, Kenya. Am J Phys Anthropol 123: 106-118.
81. deMenocal PB, (2004) African climate change and faunal evolution during the Pliocene-Pleistocene. Earth Planet Sci Lett 220: 3-24.
82. Dansgaard W (2004) Frozen annals: Greenland ice cap research. Narayana Press.
83. Grootes PM, Stuiver M, White JWC, Johnsen S, Jouzel J, (1993) Comparison of oxygen isotope records from the GISP2 and GRIP Greenland ice cores. Nature 366: 552-554.
84. Jouzel J, Lorius C, Petit JR, Genthon C, Barkov NI, et al. (1987) Vostok ice core: a continuous isotope temperature record over the last climate cycle (160,000 years). Nature 329: 403-408.
85. Thompson LG, Mosley-Thompson E, Davis ME, Henderson KA, Brecher HH, et al. (2002) Kilimanjaro ice core records: Evidence of Holocene climate change in tropical Africa. Science 298: 589-593.
86. Heaton JM, (1972) The distribution of brown adipose tissue in the human. J Anat 112: 35-39.
87. Wrangham R (2009) How cooking made us human. New York, Basic Press.
88. McHenry HM, Coffing K, (2000) Australopithecs to Homo: Transformations in body and mind. Annu Rev Anthropol 29: 125-146.
89. Hong KW, Weiss A, Morimura N, Udono T, Hayasaka I, et al. (2011) Polymorphism of the tryptophan hydroxylase 2 (TPH2) gene is associated with chimpanzee neuroticism. PLoS ONE 6 (7):: e22144.
90. Takenaka A, Udono T, Miwa N, Varavudhi P, Takenaka O, (1993) High frequency of triplicated α-globin genes in tropical primates, crab-eating macaques (Macaca fascicularis), chimpanzees (Pan troglodytes), and orangutans (Pongo pygmaeus). Primates 34: 55-60.
91. Hirai H, Mootnick AR, Takenaka O, Suryobroto B, Mouri T, et al. (2003) Genetic mechanism and property of a whole-arm translocation (WAT) between chromosomes 8 and 9 of agile gibbons (Hylobates agilis). Chromosome Res 11: 37-50.
92. Hayama S, Suzuki K, Yanai T, Masegi T, Kuroda S, et al. (1993) Constations Clonicopathologiques sur les Gorilles Orphelins du Congo, Rapport Annuel 1992-1993 par les quipes Japanaises et Congolaises: République du et Centre des Etudes Africaines, Université de Kyoto Japan.
93. Hayama S, (1994) The clinical pathological studies and comparable anatomical studies of African great apes in Republic of the Congo. Africa Research 44: 97-107 (in Japanese).
94. NCBI website. Available: http://www.ncbi.nlm.nih.gov/projects/SNP/snp_ref.cgi?rs=1042713. Accessed 2012 Jan 30.
95. NCBI website. Available: http://www.ncbi.nlm.nih.gov/projects/SNP/snp_ref.cgi?rs=1042714. Accessed 2012 Jan 30.