Networking and Specificity-Changing DNA Methyltransferases in Helicobacter pylori
Epigenetic DNA base methylation plays important roles in gene expression regulation. We here describe a gene expression regulation network consisting of many DNA methyltransferases each frequently changing its target sequence-specificity. Our object Helicobacter pylori, a bacterium responsible for m...
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Format: | Article |
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Frontiers Media S.A.
2020-07-01
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Series: | Frontiers in Microbiology |
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Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.01628/full |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Hirokazu Yano Hirokazu Yano Md. Zobaidul Alam Emiko Rimbara Tomoko F. Shibata Masaki Fukuyo Yoshikazu Furuta Yoshikazu Furuta Tomoaki Nishiyama Shuji Shigenobu Mitsuyasu Hasebe Mitsuyasu Hasebe Atsushi Toyoda Yutaka Suzuki Sumio Sugano Sumio Sugano Keigo Shibayama Ichizo Kobayashi Ichizo Kobayashi Ichizo Kobayashi Ichizo Kobayashi Ichizo Kobayashi |
spellingShingle |
Hirokazu Yano Hirokazu Yano Md. Zobaidul Alam Emiko Rimbara Tomoko F. Shibata Masaki Fukuyo Yoshikazu Furuta Yoshikazu Furuta Tomoaki Nishiyama Shuji Shigenobu Mitsuyasu Hasebe Mitsuyasu Hasebe Atsushi Toyoda Yutaka Suzuki Sumio Sugano Sumio Sugano Keigo Shibayama Ichizo Kobayashi Ichizo Kobayashi Ichizo Kobayashi Ichizo Kobayashi Ichizo Kobayashi Networking and Specificity-Changing DNA Methyltransferases in Helicobacter pylori Frontiers in Microbiology epigenetics methylome DNA methylation gastric cancer epigenome DNA methyltransferase |
author_facet |
Hirokazu Yano Hirokazu Yano Md. Zobaidul Alam Emiko Rimbara Tomoko F. Shibata Masaki Fukuyo Yoshikazu Furuta Yoshikazu Furuta Tomoaki Nishiyama Shuji Shigenobu Mitsuyasu Hasebe Mitsuyasu Hasebe Atsushi Toyoda Yutaka Suzuki Sumio Sugano Sumio Sugano Keigo Shibayama Ichizo Kobayashi Ichizo Kobayashi Ichizo Kobayashi Ichizo Kobayashi Ichizo Kobayashi |
author_sort |
Hirokazu Yano |
title |
Networking and Specificity-Changing DNA Methyltransferases in Helicobacter pylori |
title_short |
Networking and Specificity-Changing DNA Methyltransferases in Helicobacter pylori |
title_full |
Networking and Specificity-Changing DNA Methyltransferases in Helicobacter pylori |
title_fullStr |
Networking and Specificity-Changing DNA Methyltransferases in Helicobacter pylori |
title_full_unstemmed |
Networking and Specificity-Changing DNA Methyltransferases in Helicobacter pylori |
title_sort |
networking and specificity-changing dna methyltransferases in helicobacter pylori |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2020-07-01 |
description |
Epigenetic DNA base methylation plays important roles in gene expression regulation. We here describe a gene expression regulation network consisting of many DNA methyltransferases each frequently changing its target sequence-specificity. Our object Helicobacter pylori, a bacterium responsible for most incidence of stomach cancer, carries a large and variable repertoire of sequence-specific DNA methyltransferases. By creating a dozen of single-gene knockout strains for the methyltransferases, we revealed that they form a network controlling methylome, transcriptome and adaptive phenotype sets. The methyltransferases interact with each other in a hierarchical way, sometimes regulated positively by one methyltransferase but negatively with another. Motility, oxidative stress tolerance and DNA damage repair are likewise regulated by multiple methyltransferases. Their regulation sometimes involves translation start and stop codons suggesting coupling of methylation, transcription and translation. The methyltransferases frequently change their sequence-specificity through gene conversion of their target recognition domain and switch their target sets to remodel the network. The emerging picture of a metamorphosing gene regulation network, or firework, consisting of epigenetic systems ever-changing their specificity in search for adaptation, provides a new paradigm in understanding global gene regulation and adaptive evolution. |
topic |
epigenetics methylome DNA methylation gastric cancer epigenome DNA methyltransferase |
url |
https://www.frontiersin.org/article/10.3389/fmicb.2020.01628/full |
work_keys_str_mv |
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doaj-82ee3c4f720e4b97b8f25fe635f882072020-11-25T03:28:24ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-07-011110.3389/fmicb.2020.01628546911Networking and Specificity-Changing DNA Methyltransferases in Helicobacter pyloriHirokazu Yano0Hirokazu Yano1Md. Zobaidul Alam2Emiko Rimbara3Tomoko F. Shibata4Masaki Fukuyo5Yoshikazu Furuta6Yoshikazu Furuta7Tomoaki Nishiyama8Shuji Shigenobu9Mitsuyasu Hasebe10Mitsuyasu Hasebe11Atsushi Toyoda12Yutaka Suzuki13Sumio Sugano14Sumio Sugano15Keigo Shibayama16Ichizo Kobayashi17Ichizo Kobayashi18Ichizo Kobayashi19Ichizo Kobayashi20Ichizo Kobayashi21Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Tokyo, JapanInstitute of Medical Science, The University of Tokyo, Tokyo, JapanDepartment of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Tokyo, JapanDepartment of Bacteriology II, National Institute of Infectious Diseases (NIID), Musashimurayama, JapanNational Institute for Basic Biology (NIBB), Okazaki, JapanSchool of Medicine, Chiba University, Chiba, JapanDepartment of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Tokyo, JapanInstitute of Medical Science, The University of Tokyo, Tokyo, JapanAdvanced Science Research Center, Kanazawa University, Kanazawa, JapanNational Institute for Basic Biology (NIBB), Okazaki, JapanNational Institute for Basic Biology (NIBB), Okazaki, JapanDepartment of Basic Biology, School of Life Sciences, SOKENDAI (The Graduate University for Advanced Studies), Okazaki, JapanAdvanced Genomics Center, National Institute of Genetics, Mishima, JapanDepartment of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Tokyo, JapanDepartment of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Tokyo, JapanInstitute of Medical Science, The University of Tokyo, Tokyo, JapanDepartment of Bacteriology II, National Institute of Infectious Diseases (NIID), Musashimurayama, JapanDepartment of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Tokyo, JapanInstitute of Medical Science, The University of Tokyo, Tokyo, JapanDepartment of Infectious Diseases, School of Medicine, Kyorin University, Mitaka, Japan0Institut de Biologie Intégrative de la Cellule (I2BC), Université Paris-Saclay, Gif-sur-Yvette, France1Research Center for Micro-Nano Technology, Hosei University, Koganei, JapanEpigenetic DNA base methylation plays important roles in gene expression regulation. We here describe a gene expression regulation network consisting of many DNA methyltransferases each frequently changing its target sequence-specificity. Our object Helicobacter pylori, a bacterium responsible for most incidence of stomach cancer, carries a large and variable repertoire of sequence-specific DNA methyltransferases. By creating a dozen of single-gene knockout strains for the methyltransferases, we revealed that they form a network controlling methylome, transcriptome and adaptive phenotype sets. The methyltransferases interact with each other in a hierarchical way, sometimes regulated positively by one methyltransferase but negatively with another. Motility, oxidative stress tolerance and DNA damage repair are likewise regulated by multiple methyltransferases. Their regulation sometimes involves translation start and stop codons suggesting coupling of methylation, transcription and translation. The methyltransferases frequently change their sequence-specificity through gene conversion of their target recognition domain and switch their target sets to remodel the network. The emerging picture of a metamorphosing gene regulation network, or firework, consisting of epigenetic systems ever-changing their specificity in search for adaptation, provides a new paradigm in understanding global gene regulation and adaptive evolution.https://www.frontiersin.org/article/10.3389/fmicb.2020.01628/fullepigeneticsmethylomeDNA methylationgastric cancerepigenomeDNA methyltransferase |