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A proximity-dependent biotinylation map of a human cell

Author

Listed:
  • Christopher D. Go

    (Mount Sinai Hospital, Sinai Health System
    University of Toronto)

  • James D. R. Knight

    (Mount Sinai Hospital, Sinai Health System)

  • Archita Rajasekharan

    (McGill University)

  • Bhavisha Rathod

    (Mount Sinai Hospital, Sinai Health System)

  • Geoffrey G. Hesketh

    (Mount Sinai Hospital, Sinai Health System)

  • Kento T. Abe

    (Mount Sinai Hospital, Sinai Health System
    University of Toronto)

  • Ji-Young Youn

    (Mount Sinai Hospital, Sinai Health System
    University of Toronto
    Hospital for Sick Children)

  • Payman Samavarchi-Tehrani

    (Mount Sinai Hospital, Sinai Health System)

  • Hui Zhang

    (University of Toronto)

  • Lucie Y. Zhu

    (University of Toronto)

  • Evelyn Popiel

    (University of Toronto)

  • Jean-Philippe Lambert

    (Mount Sinai Hospital, Sinai Health System
    Cancer Research Centre, Big Data Research Centre, Université Laval
    CHU de Québec-Université Laval Research Center (CHUL))

  • Étienne Coyaud

    (University Health Network
    PRISM INSERM U1192, Université de Lille)

  • Sally W. T. Cheung

    (Mount Sinai Hospital, Sinai Health System)

  • Dushyandi Rajendran

    (Mount Sinai Hospital, Sinai Health System)

  • Cassandra J. Wong

    (Mount Sinai Hospital, Sinai Health System)

  • Hana Antonicka

    (McGill University)

  • Laurence Pelletier

    (Mount Sinai Hospital, Sinai Health System
    University of Toronto)

  • Alexander F. Palazzo

    (University of Toronto)

  • Eric A. Shoubridge

    (McGill University)

  • Brian Raught

    (University Health Network
    University of Toronto)

  • Anne-Claude Gingras

    (Mount Sinai Hospital, Sinai Health System
    University of Toronto)

Abstract

Compartmentalization is a defining characteristic of eukaryotic cells, and partitions distinct biochemical processes into discrete subcellular locations. Microscopy1 and biochemical fractionation coupled with mass spectrometry2–4 have defined the proteomes of a variety of different organelles, but many intracellular compartments have remained refractory to such approaches. Proximity-dependent biotinylation techniques such as BioID provide an alternative approach to define the composition of cellular compartments in living cells5–7. Here we present a BioID-based map of a human cell on the basis of 192 subcellular markers, and define the intracellular locations of 4,145 unique proteins in HEK293 cells. Our localization predictions exceed the specificity of previous approaches, and enabled the discovery of proteins at the interface between the mitochondrial outer membrane and the endoplasmic reticulum that are crucial for mitochondrial homeostasis. On the basis of this dataset, we created humancellmap.org as a community resource that provides online tools for localization analysis of user BioID data, and demonstrate how this resource can be used to understand BioID results better.

Suggested Citation

  • Christopher D. Go & James D. R. Knight & Archita Rajasekharan & Bhavisha Rathod & Geoffrey G. Hesketh & Kento T. Abe & Ji-Young Youn & Payman Samavarchi-Tehrani & Hui Zhang & Lucie Y. Zhu & Evelyn Pop, 2021. "A proximity-dependent biotinylation map of a human cell," Nature, Nature, vol. 595(7865), pages 120-124, July.
  • Handle: RePEc:nat:nature:v:595:y:2021:i:7865:d:10.1038_s41586-021-03592-2
    DOI: 10.1038/s41586-021-03592-2
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    Cited by:

    1. Kohdai Yamada & Ryouhei Shioya & Kohei Nishino & Hirotake Furihata & Atsushi Hijikata & Mika K. Kaneko & Yukinari Kato & Tsuyoshi Shirai & Hidetaka Kosako & Tatsuya Sawasaki, 2023. "Proximity extracellular protein-protein interaction analysis of EGFR using AirID-conjugated fragment of antigen binding," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Donghua Hu & Min Tan & Dongliang Lu & Brian Kleiboeker & Xuejing Liu & Hongsuk Park & Alexxai V. Kravitz & Kooresh I. Shoghi & Yu-Hua Tseng & Babak Razani & Akihiro Ikeda & Irfan J. Lodhi, 2023. "TMEM135 links peroxisomes to the regulation of brown fat mitochondrial fission and energy homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Jasjot Singh & Hadeer Elhabashy & Pathma Muthukottiappan & Markus Stepath & Martin Eisenacher & Oliver Kohlbacher & Volkmar Gieselmann & Dominic Winter, 2022. "Cross-linking of the endolysosomal system reveals potential flotillin structures and cargo," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Joanne Watson & Harriet R. Ferguson & Rosie M. Brady & Jennifer Ferguson & Paul Fullwood & Hanyi Mo & Katherine H. Bexley & David Knight & Gareth Howell & Jean-Marc Schwartz & Michael P. Smith & Chiar, 2022. "Spatially resolved phosphoproteomics reveals fibroblast growth factor receptor recycling-driven regulation of autophagy and survival," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    5. Ying Zhu & Kerem Can Akkaya & Julia Ruta & Nanako Yokoyama & Cong Wang & Max Ruwolt & Diogo Borges Lima & Martin Lehmann & Fan Liu, 2024. "Cross-link assisted spatial proteomics to map sub-organelle proteomes and membrane protein topologies," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    6. Matvei Khoroshkin & Andrey Buyan & Martin Dodel & Albertas Navickas & Johnny Yu & Fathima Trejo & Anthony Doty & Rithvik Baratam & Shaopu Zhou & Sean B. Lee & Tanvi Joshi & Kristle Garcia & Benedict C, 2024. "Systematic identification of post-transcriptional regulatory modules," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    7. Rahul Kumar & Maleeha Khan & Vincent Francis & Adriana Aguila & Gopinath Kulasekaran & Emily Banks & Peter S. McPherson, 2024. "DENND6A links Arl8b to a Rab34/RILP/dynein complex, regulating lysosomal positioning and autophagy," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    8. Maik Müller & Fabienne Gräbnitz & Niculò Barandun & Yang Shen & Fabian Wendt & Sebastian N. Steiner & Yannik Severin & Stefan U. Vetterli & Milon Mondal & James R. Prudent & Raphael Hofmann & Marc Oos, 2021. "Light-mediated discovery of surfaceome nanoscale organization and intercellular receptor interaction networks," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    9. Wenbin Xu & Han Yao & Zhen Wu & Xiaojun Yan & Zishan Jiao & Yajing Liu & Meng Zhang & Donglai Wang, 2024. "Oncoprotein SET-associated transcription factor ZBTB11 triggers lung cancer metastasis," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    10. Sinan Xiong & Jianbiao Zhou & Tze King Tan & Tae-Hoon Chung & Tuan Zea Tan & Sabrina Hui-Min Toh & Nicole Xin Ning Tang & Yunlu Jia & Yi Xiang See & Melissa Jane Fullwood & Takaomi Sanda & Wee-Joo Chn, 2024. "Super enhancer acquisition drives expression of oncogenic PPP1R15B that regulates protein homeostasis in multiple myeloma," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    11. Lili Zhao & Yuxin An & Nan Zhao & Hang Gao & Weijie Zhang & Zhou Gong & Xiaolong Liu & Baofeng Zhao & Zhen Liang & Chun Tang & Lihua Zhang & Yukui Zhang & Qun Zhao, 2024. "Spatially resolved profiling of protein conformation and interactions by biocompatible chemical cross-linking in living cells," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    12. Julian Petersen & Lukas Englmaier & Artem V. Artemov & Irina Poverennaya & Ruba Mahmoud & Thibault Bouderlique & Marketa Tesarova & Ruslan Deviatiiarov & Anett Szilvásy-Szabó & Evgeny E. Akkuratov & D, 2023. "A previously uncharacterized Factor Associated with Metabolism and Energy (FAME/C14orf105/CCDC198/1700011H14Rik) is related to evolutionary adaptation, energy balance, and kidney physiology," Nature Communications, Nature, vol. 14(1), pages 1-22, December.

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