IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35095-7.html
   My bibliography  Save this article

Integrated proteomic and transcriptomic landscape of macrophages in mouse tissues

Author

Listed:
  • Jingbo Qie

    (Fudan University)

  • Yang Liu

    (Fudan University)

  • Yunzhi Wang

    (Fudan University)

  • Fan Zhang

    (Fudan University)

  • Zhaoyu Qin

    (Fudan University)

  • Sha Tian

    (Fudan University)

  • Mingwei Liu

    (National Center for Protein Sciences)

  • Kai Li

    (National Center for Protein Sciences)

  • Wenhao Shi

    (National Center for Protein Sciences)

  • Lei Song

    (National Center for Protein Sciences)

  • Mingjun Sun

    (Fudan University)

  • Yexin Tong

    (Fudan University)

  • Ping Hu

    (Xin Hua Hospital Affiliated to Shanghai Jiao Tong University, School of Medicine)

  • Tao Gong

    (University of Science and Technology of China)

  • Xiaqiong Wang

    (University of Science and Technology of China)

  • Yi Huang

    (University of Science and Technology of China)

  • Bolong Lin

    (University of Science and Technology of China)

  • Xuesen Zheng

    (University of Science and Technology of China)

  • Rongbin Zhou

    (University of Science and Technology of China)

  • Jie Lv

    (Tongji University)

  • Changsheng Du

    (Tongji University)

  • Yi Wang

    (National Center for Protein Sciences
    Baylor College of Medicine)

  • Jun Qin

    (Fudan University
    National Center for Protein Sciences
    Baylor College of Medicine)

  • Wenjun Yang

    (Xin Hua Hospital Affiliated to Shanghai Jiao Tong University, School of Medicine)

  • Fuchu He

    (Fudan University
    National Center for Protein Sciences
    Chinese Academy of Medical Sciences)

  • Chen Ding

    (Fudan University
    National Center for Protein Sciences)

Abstract

Macrophages are involved in tissue homeostasis and are critical for innate immune responses, yet distinct macrophage populations in different tissues exhibit diverse gene expression patterns and biological processes. While tissue-specific macrophage epigenomic and transcriptomic profiles have been reported, proteomes of different macrophage populations remain poorly characterized. Here we use mass spectrometry and bulk RNA sequencing to assess the proteomic and transcriptomic patterns, respectively, of 10 primary macrophage populations from seven mouse tissues, bone marrow-derived macrophages and the cell line RAW264.7. The results show distinct proteomic landscape and protein copy numbers between tissue-resident and recruited macrophages. Construction of a hierarchical regulatory network finds cell-type-specific transcription factors of macrophages serving as hubs for denoting tissue and functional identity of individual macrophage subsets. Finally, Il18 is validated to be essential in distinguishing molecular signatures and cellular function features between tissue-resident and recruited macrophages in the lung and liver. In summary, these deposited datasets and our open proteome server ( http://macrophage.mouseprotein.cn ) integrating all information will provide a valuable resource for future functional and mechanistic studies of mouse macrophages.

Suggested Citation

  • Jingbo Qie & Yang Liu & Yunzhi Wang & Fan Zhang & Zhaoyu Qin & Sha Tian & Mingwei Liu & Kai Li & Wenhao Shi & Lei Song & Mingjun Sun & Yexin Tong & Ping Hu & Tao Gong & Xiaqiong Wang & Yi Huang & Bolo, 2022. "Integrated proteomic and transcriptomic landscape of macrophages in mouse tissues," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35095-7
    DOI: 10.1038/s41467-022-35095-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35095-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-35095-7?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. S. Heinz & C. E. Romanoski & C. Benner & K. A. Allison & M. U. Kaikkonen & L. D. Orozco & C. K. Glass, 2013. "Effect of natural genetic variation on enhancer selection and function," Nature, Nature, vol. 503(7477), pages 487-492, November.
    2. Quan Zhou & Mingwei Liu & Xia Xia & Tongqing Gong & Jinwen Feng & Wanlin Liu & Yang Liu & Bei Zhen & Yi Wang & Chen Ding & Jun Qin, 2017. "A mouse tissue transcription factor atlas," Nature Communications, Nature, vol. 8(1), pages 1-15, April.
    3. Björn Schwanhäusser & Dorothea Busse & Na Li & Gunnar Dittmar & Johannes Schuchhardt & Jana Wolf & Wei Chen & Matthias Selbach, 2011. "Global quantification of mammalian gene expression control," Nature, Nature, vol. 473(7347), pages 337-342, May.
    4. Anat Shemer & Jonathan Grozovski & Tuan Leng Tay & Jenhan Tao & Alon Volaski & Patrick Süß & Alberto Ardura-Fabregat & Mor Gross-Vered & Jung-Seok Kim & Eyal David & Louise Chappell-Maor & Lars Thiele, 2018. "Engrafted parenchymal brain macrophages differ from microglia in transcriptome, chromatin landscape and response to challenge," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    5. Rocío Rojo & Anna Raper & Derya D. Ozdemir & Lucas Lefevre & Kathleen Grabert & Evi Wollscheid-Lengeling & Barry Bradford & Melanie Caruso & Iveta Gazova & Alejandra Sánchez & Zofia M. Lisowski & Joan, 2019. "Deletion of a Csf1r enhancer selectively impacts CSF1R expression and development of tissue macrophage populations," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    6. Sophia Doll & Martina Dreßen & Philipp E. Geyer & Daniel N. Itzhak & Christian Braun & Stefanie A. Doppler & Florian Meier & Marcus-Andre Deutsch & Harald Lahm & Rüdiger Lange & Markus Krane & Matthia, 2017. "Region and cell-type resolved quantitative proteomic map of the human heart," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    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. Wenhao Shi & Yushen Wang & Chen Xu & Yan Li & Sai Ge & Bin Bai & Kecheng Zhang & Yunzhi Wang & Nairen Zheng & Juan Wang & Shiqi Wang & Gang Ji & Jipeng Li & Yongzhan Nie & Wenquan Liang & Xiaosong Wu , 2023. "Multilevel proteomic analyses reveal molecular diversity between diffuse-type and intestinal-type gastric cancer," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    2. Claude Gérard & Laurane De Mot & Sabine Cordi & Jonathan van Eyll & Frédéric P Lemaigre, 2021. "Temporal dynamics of a CSF1R signaling gene regulatory network involved in epilepsy," PLOS Computational Biology, Public Library of Science, vol. 17(4), pages 1-20, April.
    3. Ji Min Lee & Henrik M. Hammarén & Mikhail M. Savitski & Sung Hee Baek, 2023. "Control of protein stability by post-translational modifications," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Mohammad Soltani & Cesar A Vargas-Garcia & Duarte Antunes & Abhyudai Singh, 2016. "Intercellular Variability in Protein Levels from Stochastic Expression and Noisy Cell Cycle Processes," PLOS Computational Biology, Public Library of Science, vol. 12(8), pages 1-23, August.
    5. 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.
    6. Yuping Chen & Jo-Hsi Huang & Connie Phong & James E. Ferrell, 2024. "Viscosity-dependent control of protein synthesis and degradation," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    7. Gábor Csárdi & Alexander Franks & David S Choi & Edoardo M Airoldi & D Allan Drummond, 2015. "Accounting for Experimental Noise Reveals That mRNA Levels, Amplified by Post-Transcriptional Processes, Largely Determine Steady-State Protein Levels in Yeast," PLOS Genetics, Public Library of Science, vol. 11(5), pages 1-32, May.
    8. Yan Li & Chen Xu & Bing Wang & Fujiang Xu & Fahan Ma & Yuanyuan Qu & Dongxian Jiang & Kai Li & Jinwen Feng & Sha Tian & Xiaohui Wu & Yunzhi Wang & Yang Liu & Zhaoyu Qin & Yalan Liu & Jing Qin & Qi Son, 2022. "Proteomic characterization of gastric cancer response to chemotherapy and targeted therapy reveals potential therapeutic strategies," Nature Communications, Nature, vol. 13(1), pages 1-26, December.
    9. Zichen Ma & Shannon W. Davis & Yen‐Yi Ho, 2023. "Flexible copula model for integrating correlated multi‐omics data from single‐cell experiments," Biometrics, The International Biometric Society, vol. 79(2), pages 1559-1572, June.
    10. Pasqualina Colella & Ruhi Sayana & Maria Valentina Suarez-Nieto & Jolanda Sarno & Kwamina Nyame & Jian Xiong & Luisa Natalia Pimentel Vera & Jessica Arozqueta Basurto & Marco Corbo & Anay Limaye & Kar, 2024. "CNS-wide repopulation by hematopoietic-derived microglia-like cells corrects progranulin deficiency in mice," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
    11. Kaslik, Eva & Rădulescu, Ileana Rodica, 2022. "Stability and bifurcations in fractional-order gene regulatory networks," Applied Mathematics and Computation, Elsevier, vol. 421(C).
    12. Suran Kim & Sungjin Min & Yi Sun Choi & Sung-Hyun Jo & Jae Hun Jung & Kyusun Han & Jin Kim & Soohwan An & Yong Woo Ji & Yun-Gon Kim & Seung-Woo Cho, 2022. "Tissue extracellular matrix hydrogels as alternatives to Matrigel for culturing gastrointestinal organoids," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    13. Lingling Li & Dongxian Jiang & Qiao Zhang & Hui Liu & Fujiang Xu & Chunmei Guo & Zhaoyu Qin & Haixing Wang & Jinwen Feng & Yang Liu & Weijie Chen & Xue Zhang & Lin Bai & Sha Tian & Subei Tan & Chen Xu, 2023. "Integrative proteogenomic characterization of early esophageal cancer," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    14. Thomas C. J. Tan & Van Kelly & Xiaoyan Zou & David Wright & Tony Ly & Rose Zamoyska, 2022. "Translation factor eIF5a is essential for IFNγ production and cell cycle regulation in primary CD8+ T lymphocytes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    15. Katharina Clemm von Hohenberg & Sandra Müller & Sibylle Schleich & Matthias Meister & Jonathan Bohlen & Thomas G. Hofmann & Aurelio A. Teleman, 2022. "Cyclin B/CDK1 and Cyclin A/CDK2 phosphorylate DENR to promote mitotic protein translation and faithful cell division," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    16. Jonathan J. Swietlik & Stefanie Bärthel & Chiara Falcomatà & Diana Fink & Ankit Sinha & Jingyuan Cheng & Stefan Ebner & Peter Landgraf & Daniela C. Dieterich & Henrik Daub & Dieter Saur & Felix Meissn, 2023. "Cell-selective proteomics segregates pancreatic cancer subtypes by extracellular proteins in tumors and circulation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    17. Ryosuke Ishimura & Afnan H. El-Gowily & Daisuke Noshiro & Satoko Komatsu-Hirota & Yasuko Ono & Mayumi Shindo & Tomohisa Hatta & Manabu Abe & Takefumi Uemura & Hyeon-Cheol Lee-Okada & Tarek M. Mohamed , 2022. "The UFM1 system regulates ER-phagy through the ufmylation of CYB5R3," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    18. Sajib Chakraborty & Hossain Uddin Shekhar, 2017. "Applications of Mass-Spectrometry Based Quantitative Proteomics to Understand Complex Cellular Functions and Cell Fate Decisions," Biomedical Journal of Scientific & Technical Research, Biomedical Research Network+, LLC, vol. 1(1), pages 169-171, June.
    19. Marvin Hering & Alaa Madi & Roger Sandhoff & Sicong Ma & Jingxia Wu & Alessa Mieg & Karsten Richter & Kerstin Mohr & Nora Knabe & Diana Stichling & Gernot Poschet & Felix Bestvater & Larissa Frank & J, 2024. "Sphinganine recruits TLR4 adaptors in macrophages and promotes inflammation in murine models of sepsis and melanoma," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    20. Sébastien Durand & Marion Bruelle & Fleur Bourdelais & Bigitha Bennychen & Juliana Blin-Gonthier & Caroline Isaac & Aurélia Huyghe & Sylvie Martel & Antoine Seyve & Christophe Vanbelle & Annie Adrait , 2023. "RSL24D1 sustains steady-state ribosome biogenesis and pluripotency translational programs in embryonic stem cells," Nature Communications, Nature, vol. 14(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_s41467-022-35095-7. 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.