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In vivo transomic analyses of glucose-responsive metabolism in skeletal muscle reveal core differences between the healthy and obese states

View ORCID ProfileToshiya Kokaji, Miki Eto, View ORCID ProfileAtsushi Hatano, View ORCID ProfileKatsuyuki Yugi, View ORCID ProfileKeigo Morita, Satoshi Ohno, View ORCID ProfileMasashi Fujii, View ORCID ProfileKen-ichi Hironaka, Yuki Ito, Riku Egami, View ORCID ProfileSaori Uematsu, Akira Terakawa, Yifei Pan, Hideki Maehara, Dongzi Li, Yunfan Bai, View ORCID ProfileTakaho Tsuchiya, View ORCID ProfileHaruka Ozaki, Hiroshi Inoue, Hiroyuki Kubota, Yutaka Suzuki, Akiyoshi Hirayama, Tomoyoshi Soga, View ORCID ProfileShinya Kuroda
doi: https://doi.org/10.1101/2022.03.27.486003
Toshiya Kokaji
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
2Data Science Center, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara, Japan
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Miki Eto
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
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Atsushi Hatano
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
3Laboratory for Integrated Cellular Systems, RIKEN Center for Integrative Medical Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan
4Department of Omics and Systems Biology, Niigata University Graduate School of Medical and Dental Sciences, 757 Ichibancho, Asahimachi-dori, Chuo Ward, Niigata City 951-8510, Japan
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Katsuyuki Yugi
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
3Laboratory for Integrated Cellular Systems, RIKEN Center for Integrative Medical Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan
5Institute for Advanced Biosciences, Keio University, Fujisawa, 252-8520, Japan
6PRESTO, Japan Science and Technology Agency, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan
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Keigo Morita
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
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Satoshi Ohno
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
7Molecular Genetics Research Laboratory, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
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Masashi Fujii
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
7Molecular Genetics Research Laboratory, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
8Department of Mathematical and Life Sciences, Graduate School of Integrated Sciences for Life, Hiroshima University 1-3-1 Kagamiyama, Higashi-hiroshima city, Hiroshima, 739-8526, Japan
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Ken-ichi Hironaka
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
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Yuki Ito
9Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan
10Division of Integrated Omics, Research Center for Transomics Medicine, Medical Institute of Bioregulation, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan
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Riku Egami
9Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan
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Saori Uematsu
9Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan
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Akira Terakawa
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
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Yifei Pan
9Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan
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Hideki Maehara
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
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Dongzi Li
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
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Yunfan Bai
9Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan
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Takaho Tsuchiya
11Bioinformatics Laboratory, Faculty of Medicine, University of Tsukuba, Ibaraki, 305-8575, Japan
12Center for Artificial Intelligence Research, University of Tsukuba, Ibaraki, 305-8577, Japan
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Haruka Ozaki
11Bioinformatics Laboratory, Faculty of Medicine, University of Tsukuba, Ibaraki, 305-8575, Japan
12Center for Artificial Intelligence Research, University of Tsukuba, Ibaraki, 305-8577, Japan
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Hiroshi Inoue
13Metabolism and Nutrition Research Unit, Institute for Frontier Science Initiative, Kanazawa University, 13-1 Takaramachi, Kanazawa, Ishikawa, 920-8641, Japan
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Hiroyuki Kubota
10Division of Integrated Omics, Research Center for Transomics Medicine, Medical Institute of Bioregulation, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan
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Yutaka Suzuki
9Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan
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Akiyoshi Hirayama
14Institute for Advanced Biosciences, Keio University, 246-2 Mizukami, Kakuganji, Tsuruoka, Yamagata 997-0052, Japan
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Tomoyoshi Soga
14Institute for Advanced Biosciences, Keio University, 246-2 Mizukami, Kakuganji, Tsuruoka, Yamagata 997-0052, Japan
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Shinya Kuroda
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
9Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan
15Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency, Bunkyo-ku, Tokyo 113-0033, Japan
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  • For correspondence: skuroda@bs.s.u-tokyo.ac.jp
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Abstract

Metabolic regulation in skeletal muscle is essential for blood glucose homeostasis. Obesity causes insulin resistance in skeletal muscle, leading to hyperglycemia and type 2 diabetes. In this study, we performed multiomic analysis of the skeletal muscle of wild-type (WT) and genetically obese (ob/ob) mice, and constructed regulatory transomic networks for metabolism after oral glucose administration. Our network revealed that metabolic regulation by glucose-responsive metabolites had a major effect on WT mice, especially carbohydrate metabolic pathways. By contrast, in ob/ob mice, much of the metabolic regulation by glucose-responsive metabolites was lost and metabolic regulation by glucose-responsive genes was largely increased, especially in carbohydrate and lipid metabolic pathways. We present some characteristic metabolic regulatory pathways found in central carbon, branched amino acids, and ketone body metabolism. Our transomic analysis will provide insights into how skeletal muscle responds to changes in blood glucose and how it fails to respond in obesity.

Competing Interest Statement

The authors have declared no competing interest.

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Posted March 28, 2022.
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In vivo transomic analyses of glucose-responsive metabolism in skeletal muscle reveal core differences between the healthy and obese states
Toshiya Kokaji, Miki Eto, Atsushi Hatano, Katsuyuki Yugi, Keigo Morita, Satoshi Ohno, Masashi Fujii, Ken-ichi Hironaka, Yuki Ito, Riku Egami, Saori Uematsu, Akira Terakawa, Yifei Pan, Hideki Maehara, Dongzi Li, Yunfan Bai, Takaho Tsuchiya, Haruka Ozaki, Hiroshi Inoue, Hiroyuki Kubota, Yutaka Suzuki, Akiyoshi Hirayama, Tomoyoshi Soga, Shinya Kuroda
bioRxiv 2022.03.27.486003; doi: https://doi.org/10.1101/2022.03.27.486003
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In vivo transomic analyses of glucose-responsive metabolism in skeletal muscle reveal core differences between the healthy and obese states
Toshiya Kokaji, Miki Eto, Atsushi Hatano, Katsuyuki Yugi, Keigo Morita, Satoshi Ohno, Masashi Fujii, Ken-ichi Hironaka, Yuki Ito, Riku Egami, Saori Uematsu, Akira Terakawa, Yifei Pan, Hideki Maehara, Dongzi Li, Yunfan Bai, Takaho Tsuchiya, Haruka Ozaki, Hiroshi Inoue, Hiroyuki Kubota, Yutaka Suzuki, Akiyoshi Hirayama, Tomoyoshi Soga, Shinya Kuroda
bioRxiv 2022.03.27.486003; doi: https://doi.org/10.1101/2022.03.27.486003

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