IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-30261-3.html
   My bibliography  Save this article

A multiplex platform for small RNA sequencing elucidates multifaceted tRNA stress response and translational regulation

Author

Listed:
  • Christopher P. Watkins

    (Department of Biochemistry and Molecular Biology)

  • Wen Zhang

    (University of Chicago)

  • Adam C. Wylder

    (University of Chicago)

  • Christopher D. Katanski

    (Department of Biochemistry and Molecular Biology)

  • Tao Pan

    (Department of Biochemistry and Molecular Biology)

Abstract

Small RNAs include tRNA, snRNA, micro-RNA, tRNA fragments and others that constitute > 90% of RNA copy numbers in a human cell and perform many essential functions. Popular small RNA-seq strategies limit the insights into coordinated small RNA response to cellular stress. Small RNA-seq also lacks multiplexing capabilities. Here, we report a multiplex small RNA-seq library preparation method (MSR-seq) to investigate cellular small RNA and mRNA response to heat shock, hydrogen peroxide, and arsenite stress. Comparing stress-induced changes of total cellular RNA and polysome-associated RNA, we identify a coordinated tRNA response that involves polysome-specific tRNA abundance and synergistic N3-methylcytosine (m3C) tRNA modification. Combining tRNA and mRNA response to stress we reveal a mechanism of stress-induced down-regulation in translational elongation. We also find that native tRNA molecules lacking several modifications are biased reservoirs for the biogenesis of tRNA fragments. Our results demonstrate the importance of simultaneous investigation of small RNAs and their modifications in response to varying biological conditions.

Suggested Citation

  • Christopher P. Watkins & Wen Zhang & Adam C. Wylder & Christopher D. Katanski & Tao Pan, 2022. "A multiplex platform for small RNA sequencing elucidates multifaceted tRNA stress response and translational regulation," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30261-3
    DOI: 10.1038/s41467-022-30261-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-30261-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-30261-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Dan Dominissini & Sigrid Nachtergaele & Sharon Moshitch-Moshkovitz & Eyal Peer & Nitzan Kol & Moshe Shay Ben-Haim & Qing Dai & Ayelet Di Segni & Mali Salmon-Divon & Wesley C. Clark & Guanqun Zheng & T, 2016. "The dynamic N1-methyladenosine methylome in eukaryotic messenger RNA," Nature, Nature, vol. 530(7591), pages 441-446, February.
    2. Xiao Wang & Zhike Lu & Adrian Gomez & Gary C. Hon & Yanan Yue & Dali Han & Ye Fu & Marc Parisien & Qing Dai & Guifang Jia & Bing Ren & Tao Pan & Chuan He, 2014. "N6-methyladenosine-dependent regulation of messenger RNA stability," Nature, Nature, vol. 505(7481), pages 117-120, January.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. You Wu & Wenna Shao & Mengxiao Yan & Yuqin Wang & Pengfei Xu & Guoqiang Huang & Xiaofei Li & Brian D. Gregory & Jun Yang & Hongxia Wang & Xiang Yu, 2024. "Transfer learning enables identification of multiple types of RNA modifications using nanopore direct RNA sequencing," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Moshe Shay Ben-Haim & Yishay Pinto & Sharon Moshitch-Moshkovitz & Vera Hershkovitz & Nitzan Kol & Tammy Diamant-Levi & Michal Schnaider Beeri & Ninette Amariglio & Haim Y. Cohen & Gideon Rechavi, 2021. "Dynamic regulation of N6,2′-O-dimethyladenosine (m6Am) in obesity," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    3. Shujie Chen, & Lu Zhang & Mengjie Li & Ying Zhang & Meng Sun & Lingfang Wang & Jiebo Lin & Yun Cui & Qian Chen & Chenqi Jin & Xiang Li & Boya Wang & Hao Chen & Tianhua Zhou & Liangjing Wang & Chih-Hun, 2022. "Fusobacterium nucleatum reduces METTL3-mediated m6A modification and contributes to colorectal cancer metastasis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Zhiyuan Luo & Jiacheng Zhang & Jingyi Fei & Shengdong Ke, 2022. "Deep learning modeling m6A deposition reveals the importance of downstream cis-element sequences," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Xiao Han & Lijuan Liu & Saihua Huang & Wenfeng Xiao & Yajing Gao & Weitao Zhou & Caiyan Zhang & Hongmei Zheng & Lan Yang & Xueru Xie & Qiuyan Liang & Zikun Tu & Hongmiao Yu & Jinrong Fu & Libo Wang & , 2023. "RNA m6A methylation modulates airway inflammation in allergic asthma via PTX3-dependent macrophage homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Sakshi Jain & Lukasz Koziej & Panagiotis Poulis & Igor Kaczmarczyk & Monika Gaik & Michal Rawski & Namit Ranjan & Sebastian Glatt & Marina V. Rodnina, 2023. "Modulation of translational decoding by m6A modification of mRNA," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. Yanying Wang & Jing Wang & Xiaoyu Li & Xushen Xiong & Jianyi Wang & Ziheng Zhou & Xiaoxiao Zhu & Yang Gu & Dan Dominissini & Lei He & Yong Tian & Chengqi Yi & Zusen Fan, 2021. "N1-methyladenosine methylation in tRNA drives liver tumourigenesis by regulating cholesterol metabolism," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    8. Xiaojie Ma & Jie Cao & Ziyu Zhou & Yunkun Lu & Qin Li & Yan Jin & Guo Chen & Weiyun Wang & Wenyan Ge & Xi Chen & Zhensheng Hu & Xiao Shu & Qian Deng & Jiaqi Pu & Chengzhen Liang & Junfen Fu & Jianzhao, 2022. "N6-methyladenosine modification-mediated mRNA metabolism is essential for human pancreatic lineage specification and islet organogenesis," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    9. Valter Bergant & Daniel Schnepf & Niklas Andrade Krätzig & Philipp Hubel & Christian Urban & Thomas Engleitner & Ronald Dijkman & Bernhard Ryffel & Katja Steiger & Percy A. Knolle & Georg Kochs & Rola, 2023. "mRNA 3’UTR lengthening by alternative polyadenylation attenuates inflammatory responses and correlates with virulence of Influenza A virus," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Christopher J. Gilbert & Charles P. Rabolli & Volha A. Golubeva & Kristina M. Sattler & Meifang Wang & Arsh Ketabforoush & W. David Arnold & Christoph Lepper & Federica Accornero, 2024. "YTHDF2 governs muscle size through a targeted modulation of proteostasis," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Belinda Baquero-Pérez & Ivaylo D. Yonchev & Anna Delgado-Tejedor & Rebeca Medina & Mireia Puig-Torrents & Ian Sudbery & Oguzhan Begik & Stuart A. Wilson & Eva Maria Novoa & Juana Díez, 2024. "N6-methyladenosine modification is not a general trait of viral RNA genomes," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    12. Fabian Poetz & Joshua Corbo & Yevgen Levdansky & Alexander Spiegelhalter & Doris Lindner & Vera Magg & Svetlana Lebedeva & Jörg Schweiggert & Johanna Schott & Eugene Valkov & Georg Stoecklin, 2021. "RNF219 attenuates global mRNA decay through inhibition of CCR4-NOT complex-mediated deadenylation," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    13. Hyun Jung Hwang & Tae Lim Park & Hyeong-In Kim & Yeonkyoung Park & Geunhee Kim & Chiyeol Song & Won-Ki Cho & Yoon Ki Kim, 2023. "YTHDF2 facilitates aggresome formation via UPF1 in an m6A-independent manner," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    14. Zhangli Su & Ida Monshaugen & Briana Wilson & Fengbin Wang & Arne Klungland & Rune Ougland & Anindya Dutta, 2022. "TRMT6/61A-dependent base methylation of tRNA-derived fragments regulates gene-silencing activity and the unfolded protein response in bladder cancer," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    15. Sepideh Tavakoli & Mohammad Nabizadeh & Amr Makhamreh & Howard Gamper & Caroline A. McCormick & Neda K. Rezapour & Ya-Ming Hou & Meni Wanunu & Sara H. Rouhanifard, 2023. "Semi-quantitative detection of pseudouridine modifications and type I/II hypermodifications in human mRNAs using direct long-read sequencing," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    16. Xin Yang & Robinson Triboulet & Qi Liu & Erdem Sendinc & Richard I. Gregory, 2022. "Exon junction complex shapes the m6A epitranscriptome," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    17. Zhiyuan Luo & Qilian Ma & Shan Sun & Ningning Li & Hongfeng Wang & Zheng Ying & Shengdong Ke, 2023. "Exon-intron boundary inhibits m6A deposition, enabling m6A distribution hallmark, longer mRNA half-life and flexible protein coding," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    18. Huaxia Shi & Ying Xu & Na Tian & Ming Yang & Fu-Sen Liang, 2022. "Inducible and reversible RNA N6-methyladenosine editing," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    19. Bin Li & Wen Xi & Ying Bai & Xue Liu & Yuan Zhang & Lu Li & Liang Bian & Chenchen Liu & Ying Tang & Ling Shen & Li Yang & Xiaochun Gu & Jian Xie & Zhongqiu Zhou & Yu Wang & Xiaoyu Yu & Jianhong Wang &, 2023. "FTO-dependent m6A modification of Plpp3 in circSCMH1-regulated vascular repair and functional recovery following stroke," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    20. Hyun Jung Hwang & Hongseok Ha & Ban Seok Lee & Bong Heon Kim & Hyun Kyu Song & Yoon Ki Kim, 2022. "LC3B is an RNA-binding protein to trigger rapid mRNA degradation during autophagy," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30261-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.