Global metabolic reprogramming of colorectal cancer occurs at adenoma stage and is induced by MYC
Cancer cells alter their metabolism for the production of precursors of macromolecules. However, the control mechanisms underlying this reprogramming are poorly understood. Here we show that metabolic reprogramming of colorectal cancer is caused chiefly by aberrant MYC expression. Multiomics-based a...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 114; no. 37; pp. E7697 - E7706 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
12.09.2017
|
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Cancer cells alter their metabolism for the production of precursors of macromolecules. However, the control mechanisms underlying this reprogramming are poorly understood. Here we show that metabolic reprogramming of colorectal cancer is caused chiefly by aberrant MYC expression. Multiomics-based analyses of paired normal and tumor tissues from 275 patients with colorectal cancer revealed that metabolic alterations occur at the adenoma stage of carcinogenesis, in a manner not associated with specific gene mutations involved in colorectal carcinogenesis. MYC expression induced at least 215 metabolic reactions by changing the expression levels of 121 metabolic genes and 39 transporter genes. Further, MYC negatively regulated the expression of genes involved in mitochondrial biogenesis and maintenance but positively regulated genes involved in DNA and histone methylation. Knockdown of MYC in colorectal cancer cells reset the altered metabolism and suppressed cell growth. Moreover, inhibition of MYC target pyrimidine synthesis genes such as CAD, UMPS, and CTPS blocked cell growth, and thus are potential targets for colorectal cancer therapy. |
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| AbstractList | Cancer cells alter their metabolism for the production of precursors of macromolecules. However, the control mechanisms underlying this reprogramming are poorly understood. Here we show that metabolic reprogramming of colorectal cancer is caused chiefly by aberrant MYC expression. Multiomics-based analyses of paired normal and tumor tissues from 275 patients with colorectal cancer revealed that metabolic alterations occur at the adenoma stage of carcinogenesis, in a manner not associated with specific gene mutations involved in colorectal carcinogenesis. MYC expression induced at least 215 metabolic reactions by changing the expression levels of 121 metabolic genes and 39 transporter genes. Further, MYC negatively regulated the expression of genes involved in mitochondrial biogenesis and maintenance but positively regulated genes involved in DNA and histone methylation. Knockdown of MYC in colorectal cancer cells reset the altered metabolism and suppressed cell growth. Moreover, inhibition of MYC target pyrimidine synthesis genes such as CAD, UMPS, and CTPS blocked cell growth, and thus are potential targets for colorectal cancer therapy.Cancer cells alter their metabolism for the production of precursors of macromolecules. However, the control mechanisms underlying this reprogramming are poorly understood. Here we show that metabolic reprogramming of colorectal cancer is caused chiefly by aberrant MYC expression. Multiomics-based analyses of paired normal and tumor tissues from 275 patients with colorectal cancer revealed that metabolic alterations occur at the adenoma stage of carcinogenesis, in a manner not associated with specific gene mutations involved in colorectal carcinogenesis. MYC expression induced at least 215 metabolic reactions by changing the expression levels of 121 metabolic genes and 39 transporter genes. Further, MYC negatively regulated the expression of genes involved in mitochondrial biogenesis and maintenance but positively regulated genes involved in DNA and histone methylation. Knockdown of MYC in colorectal cancer cells reset the altered metabolism and suppressed cell growth. Moreover, inhibition of MYC target pyrimidine synthesis genes such as CAD, UMPS, and CTPS blocked cell growth, and thus are potential targets for colorectal cancer therapy. Cancer cells alter their metabolism for the production of precursors of macromolecules. However, the control mechanisms underlying this reprogramming are poorly understood. Here we show that metabolic reprogramming of colorectal cancer is caused chiefly by aberrant MYC expression. Multiomics-based analyses of paired normal and tumor tissues from 275 patients with colorectal cancer revealed that metabolic alterations occur at the adenoma stage of carcinogenesis, in a manner not associated with specific gene mutations involved in colorectal carcinogenesis. MYC expression induced at least 215 metabolic reactions by changing the expression levels of 121 metabolic genes and 39 transporter genes. Further, MYC negatively regulated the expression of genes involved in mitochondrial biogenesis and maintenance but positively regulated genes involved in DNA and histone methylation. Knockdown of MYC in colorectal cancer cells reset the altered metabolism and suppressed cell growth. Moreover, inhibition of MYC target pyrimidine synthesis genes such as CAD, UMPS, and CTPS blocked cell growth, and thus are potential targets for colorectal cancer therapy. Metabolic reprogramming is one of the hallmarks of cancer. However, the underlying mechanisms that regulate cancer metabolism are poorly understood. Here we performed multiomics-based analysis of paired normal–tumor tissues from patients with colorectal cancer, which revealed that the protooncogene protein MYC regulated global metabolic reprogramming of colorectal cancer by modulating 215 metabolic reactions. Importantly, this metabolic reprogramming occurred in a manner not associated with specific gene mutations in colorectal carcinogenesis. For many years, small-molecule or biologic inhibitors of MYC have been required. Here we demonstrate that knockdown of MYC downstream pyrimidine synthesis genes contributes to the suppression of colorectal cancer cell proliferation similar to MYC, and thus pyrimidine synthesis pathways could be potential targets for colorectal cancer therapy. Cancer cells alter their metabolism for the production of precursors of macromolecules. However, the control mechanisms underlying this reprogramming are poorly understood. Here we show that metabolic reprogramming of colorectal cancer is caused chiefly by aberrant MYC expression. Multiomics-based analyses of paired normal and tumor tissues from 275 patients with colorectal cancer revealed that metabolic alterations occur at the adenoma stage of carcinogenesis, in a manner not associated with specific gene mutations involved in colorectal carcinogenesis. MYC expression induced at least 215 metabolic reactions by changing the expression levels of 121 metabolic genes and 39 transporter genes. Further, MYC negatively regulated the expression of genes involved in mitochondrial biogenesis and maintenance but positively regulated genes involved in DNA and histone methylation. Knockdown of MYC in colorectal cancer cells reset the altered metabolism and suppressed cell growth. Moreover, inhibition of MYC target pyrimidine synthesis genes such as CAD , UMPS , and CTPS blocked cell growth, and thus are potential targets for colorectal cancer therapy. Cancer cells alter their metabolism for the production of precursors of macromolecules. However, the control mechanisms underlying this reprogramming are poorly understood. Here we show that metabolic reprogramming of colorectal cancer is caused chiefly by aberrant expression. Multiomics-based analyses of paired normal and tumor tissues from 275 patients with colorectal cancer revealed that metabolic alterations occur at the adenoma stage of carcinogenesis, in a manner not associated with specific gene mutations involved in colorectal carcinogenesis. expression induced at least 215 metabolic reactions by changing the expression levels of 121 metabolic genes and 39 transporter genes. Further, negatively regulated the expression of genes involved in mitochondrial biogenesis and maintenance but positively regulated genes involved in DNA and histone methylation. Knockdown of in colorectal cancer cells reset the altered metabolism and suppressed cell growth. Moreover, inhibition of MYC target pyrimidine synthesis genes such as , , and blocked cell growth, and thus are potential targets for colorectal cancer therapy. |
| Author | Soga, Tomoyoshi Igarashi, Kaori Aizawa, Yumi Fujishita, Teruaki Kushida, Yoshio Sato, Saya Saitoh, Kaori Ishikawa, Takamasa Taketo, Makoto Mark Hirayama, Akiyoshi Fukuda, Shinji Yachida, Shinichi Oshima, Minoru Sugimoto, Masahiro Enomoto, Ayame Suzuki, Yasuyuki Haba, Reiji Akamoto, Shintaro Nakagawa, Toshitaka Kajino-Sakamoto, Rie Satoh, Kiyotoshi Tomita, Masaru Aoki, Masahiro Kojima, Yasushi Kato, Keiko Tabata, Sho Okano, Keiichi |
| Author_xml | – sequence: 1 givenname: Kiyotoshi surname: Satoh fullname: Satoh, Kiyotoshi organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 2 givenname: Shinichi surname: Yachida fullname: Yachida, Shinichi organization: National Cancer Center Research Institute, Chuo-ku, Tokyo 104-0045, Japan – sequence: 3 givenname: Masahiro surname: Sugimoto fullname: Sugimoto, Masahiro organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 4 givenname: Minoru surname: Oshima fullname: Oshima, Minoru organization: Gastroenterological Surgery, Faculty of Medicine, Kagawa University, Kagawa 761-0793, Japan – sequence: 5 givenname: Toshitaka surname: Nakagawa fullname: Nakagawa, Toshitaka organization: Life Science Center, Kagawa University, Kagawa 761-0793, Japan – sequence: 6 givenname: Shintaro surname: Akamoto fullname: Akamoto, Shintaro organization: Gastroenterological Surgery, Faculty of Medicine, Kagawa University, Kagawa 761-0793, Japan – sequence: 7 givenname: Sho surname: Tabata fullname: Tabata, Sho organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 8 givenname: Kaori surname: Saitoh fullname: Saitoh, Kaori organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 9 givenname: Keiko surname: Kato fullname: Kato, Keiko organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 10 givenname: Saya surname: Sato fullname: Sato, Saya organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 11 givenname: Kaori surname: Igarashi fullname: Igarashi, Kaori organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 12 givenname: Yumi surname: Aizawa fullname: Aizawa, Yumi organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 13 givenname: Rie surname: Kajino-Sakamoto fullname: Kajino-Sakamoto, Rie organization: Division of Molecular Pathology, Aichi Cancer Center Research Institute, Chikusa-Ku, Nagoya, Aichi 464-8681, Japan – sequence: 14 givenname: Yasushi surname: Kojima fullname: Kojima, Yasushi organization: Division of Molecular Pathology, Aichi Cancer Center Research Institute, Chikusa-Ku, Nagoya, Aichi 464-8681, Japan – sequence: 15 givenname: Teruaki surname: Fujishita fullname: Fujishita, Teruaki organization: Division of Molecular Pathology, Aichi Cancer Center Research Institute, Chikusa-Ku, Nagoya, Aichi 464-8681, Japan – sequence: 16 givenname: Ayame surname: Enomoto fullname: Enomoto, Ayame organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 17 givenname: Akiyoshi surname: Hirayama fullname: Hirayama, Akiyoshi organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 18 givenname: Takamasa surname: Ishikawa fullname: Ishikawa, Takamasa organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 19 givenname: Makoto Mark surname: Taketo fullname: Taketo, Makoto Mark organization: Department of Pharmacology, Graduate School of Medicine, Kyoto University, Sakyo-ku, Kyoto 606-8501, Japan – sequence: 20 givenname: Yoshio surname: Kushida fullname: Kushida, Yoshio organization: Gastroenterological Surgery, Faculty of Medicine, Kagawa University, Kagawa 761-0793, Japan – sequence: 21 givenname: Reiji surname: Haba fullname: Haba, Reiji organization: Gastroenterological Surgery, Faculty of Medicine, Kagawa University, Kagawa 761-0793, Japan – sequence: 22 givenname: Keiichi surname: Okano fullname: Okano, Keiichi organization: Gastroenterological Surgery, Faculty of Medicine, Kagawa University, Kagawa 761-0793, Japan – sequence: 23 givenname: Masaru surname: Tomita fullname: Tomita, Masaru organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 24 givenname: Yasuyuki surname: Suzuki fullname: Suzuki, Yasuyuki organization: Gastroenterological Surgery, Faculty of Medicine, Kagawa University, Kagawa 761-0793, Japan – sequence: 25 givenname: Shinji surname: Fukuda fullname: Fukuda, Shinji organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan – sequence: 26 givenname: Masahiro surname: Aoki fullname: Aoki, Masahiro organization: Division of Molecular Pathology, Aichi Cancer Center Research Institute, Chikusa-Ku, Nagoya, Aichi 464-8681, Japan – sequence: 27 givenname: Tomoyoshi surname: Soga fullname: Soga, Tomoyoshi organization: Institute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka 997-0052, Japan |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28847964$$D View this record in MEDLINE/PubMed |
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| Copyright | Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles Copyright National Academy of Sciences Sep 12, 2017 |
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| DocumentTitleAlternate | MYC shifts global metabolism in colon adenoma |
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| Keywords | metabolism colorectal cancer omics metabolomics MYC |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author contributions: K. Satoh, S.Y., S.F., and T.S. designed research; K. Satoh, S.Y., M.O., T.N., S.A., S.T., K. Saitoh, K.K., S.S., K.I., Y.A., R.K.-S., Y. Kojima, T.F., A.H., T.I., Y. Kushida, R.H., K.O., M.T., M.A., and T.S. performed research; M.M.T. and Y.S. contributed new reagents/analytic tools; K. Satoh, S.Y., M.S., A.E., and T.S. analyzed data; and K. Satoh, S.Y., M.S., M.A., and T.S. wrote the paper. Edited by Tak W. Mak, The Campbell Family Institute for Breast Cancer Research at Princess Margaret Cancer Centre, University Health Network, Toronto, Canada, and approved August 9, 2017 (received for review June 9, 2017) |
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| Snippet | Cancer cells alter their metabolism for the production of precursors of macromolecules. However, the control mechanisms underlying this reprogramming are... Metabolic reprogramming is one of the hallmarks of cancer. However, the underlying mechanisms that regulate cancer metabolism are poorly understood. Here we... |
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| SubjectTerms | Aberration Adenoma Biological Sciences Cancer Cancer therapies Carcinogenesis Carcinogens Colorectal cancer Colorectal carcinoma Deoxyribonucleic acid DNA DNA methylation Evolution Gene expression Genes Macromolecules Metabolism Mitochondria Mutation Myc protein PNAS Plus Studies Tumors |
| Title | Global metabolic reprogramming of colorectal cancer occurs at adenoma stage and is induced by MYC |
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