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Positive natural selection of TRIB2, a novel gene that influences visceral fat accumulation, in East Asia

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Abstract

Accumulation of visceral fat increases cardiovascular mortality in industrialized societies. However, during the evolution of the modern human, visceral fat may have acted as energy storage facility to survive in times of famine. Therefore, past natural selection might contribute to shaping the variation of visceral fat accumulation in present populations. Here, we report that the gene encoding tribbles homolog 2 (TRIB2) influenced visceral fat accumulation and was operated by recent positive natural selection in East Asians. Our candidate gene association analysis on 11 metabolic traits of 5,810 East Asians revealed that rs1057001, a T/A transversion polymorphism in 3′untranslated region (UTR) of TRIB2, was strongly associated with visceral fat area (VFA) and waist circumference adjusted for body mass index (P = 2.7 × 10−6 and P = 9.0 × 10−6, respectively). rs1057001 was in absolute linkage disequilibrium with a conserved insertion-deletion polymorphism in the 3′UTR and was associated with allelic imbalance of TRIB2 transcript levels in adipose tissues. rs1057001 showed high degree of interpopulation variation of the allele frequency; the low-VFA-associated A allele was found with high frequencies in East Asians. Haplotypes containing the rs1057001 A allele exhibited a signature of a selective sweep, which may have occurred 16,546–27,827 years ago in East Asians. Given the predominance of the thrifty gene hypothesis, it is surprising that the apparently non-thrifty allele was selectively favored in the evolution of modern humans. Environmental/physiological factors other than famine would be needed to explain the non-neutral evolution of TRIB2 in East Asians.

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Acknowledgments

We would like to thank our colleagues at the Division of Human Genetics, Jichi Medical University. We are also grateful the staff of the Jichi Medical University Hospital Health Checkup Center for their cooperation in the collection of samples from Japanese individuals. We would like to thank Editage for providing editorial assistance. This study was supported in part by a KAKENHI Grant-in-Aid for young researchers (A) [23687036 to K.N.], a Grant-in Aid for Basic Science (C) [22591001 to S.I.] from the Ministry of Education, Culture, Sports, Science and Technology of Japan, a grant from the Kao Research Council for the Study of Healthcare Science (KN), and JKA through its promotion funds from KEIRIN RACE.

Conflict of interest

Y.Y., M.K., and T.O. are employees of the Kao Corporation. K.O. is an employee of the Panasonic Corporation. S.F. is an employee of the Panasonic Healthcare Co., Ltd.

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Authors and Affiliations

  1. Division of Human Genetics, Center for Molecular Medicine, Jichi Medical University, 3311-1 Yakushiji, Shimotsuke, Tochigi, 329-0498, Japan

    Kazuhiro Nakayama, Ayumi Ogawa, Yoshiko Yanagisawa & Sadahiko Iwamoto

  2. Jichi Medical University Hospital, Jichi Medical University, Shimotsuke, Tochigi, 329-0498, Japan

    Hiroshi Miyashita

  3. Center for Genomic Medicine, Kyoto University Graduate School of Medicine, Sakyo-ku, Kyoto, 606-8507, Japan

    Yasuharu Tabara

  4. Department of Geriatric Medicine, Ehime University Graduate School of Medicine, Toon, Ehime, 791-0295, Japan

    Michiya Igase, Katsuhiko Kohara & Tetsuro Miki

  5. High Technology Research Center, Kagawa Nutrition University, Sakado, Saitama, 350-0288, Japan

    Yasuo Kagawa

  6. Health Care Food Research, Human Health Care Research, Research and Development, Kao Corporation, Sumida-ku, Tokyo, 131-8501, Japan

    Yoshiko Yanagisawa & Mitsuhiro Katashima

  7. Processing Development Research, Research and Development, Kao Corporation, Sumida-ku, Tokyo, 131-8501, Japan

    Tomohiro Onda

  8. Appliances Company Corporate Engineering Division, Panasonic Corporation, Kusatsu, Shiga, 525-8555, Japan

    Koichi Okada

  9. Corporate Research and Development Center, Panasonic Healthcare Co., Ltd, Kodama, Osaka, 571-8686, Japan

    Shogo Fukushima

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  1. Kazuhiro Nakayama
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  2. Ayumi Ogawa
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  14. Sadahiko Iwamoto
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Corresponding authors

Correspondence to Kazuhiro Nakayama or Sadahiko Iwamoto.

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Nakayama, K., Ogawa, A., Miyashita, H. et al. Positive natural selection of TRIB2, a novel gene that influences visceral fat accumulation, in East Asia. Hum Genet 132, 201–217 (2013). https://doi.org/10.1007/s00439-012-1240-9

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  • DOI: https://doi.org/10.1007/s00439-012-1240-9

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