IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-53683-7.html
   My bibliography  Save this article

Spatial proteomics of single cells and organelles on tissue slides using filter-aided expansion proteomics

Author

Listed:
  • Zhen Dong

    (Westlake University
    Westlake Laboratory of Life Sciences and Biomedicine
    Westlake University)

  • Wenhao Jiang

    (Westlake University
    Westlake Laboratory of Life Sciences and Biomedicine
    Westlake University)

  • Chunlong Wu

    (Westlake University
    Westlake Laboratory of Life Sciences and Biomedicine
    Westlake University)

  • Ting Chen

    (Zhejiang University)

  • Jiayi Chen

    (Westlake University
    Westlake Laboratory of Life Sciences and Biomedicine
    Westlake University)

  • Xuan Ding

    (Westlake University
    Westlake Laboratory of Life Sciences and Biomedicine
    Westlake University)

  • Shu Zheng

    (Zhejiang University)

  • Kiryl D. Piatkevich

    (Westlake Laboratory of Life Sciences and Biomedicine
    Westlake University
    Westlake University)

  • Yi Zhu

    (Westlake University
    Westlake Laboratory of Life Sciences and Biomedicine
    Westlake University)

  • Tiannan Guo

    (Westlake University
    Westlake Laboratory of Life Sciences and Biomedicine
    Westlake University)

Abstract

Hydrogel-based tissue expansion combined with mass spectrometry (MS) offers an emerging spatial proteomics approach. Here, we present a filter-aided expansion proteomics (FAXP) strategy for spatial proteomics analysis of archived formalin-fixed paraffin-embedded (FFPE) specimens. Compared to our previous ProteomEx method, FAXP employed a customized tip device to enhance both the stability and throughput of sample preparation, thus guaranteeing the reproducibility and robustness of the workflow. FAXP achieved a 14.5-fold increase in volumetric resolution. It generated over 8 times higher peptide yield and a 255% rise in protein identifications while reducing sample preparation time by 50%. We also demonstrated the applicability of FAXP using human colorectal FFPE tissue samples. Furthermore, for the first time, we achieved bona fide single-subcellular proteomics under image guidance by integrating FAXP with laser capture microdissection.

Suggested Citation

  • Zhen Dong & Wenhao Jiang & Chunlong Wu & Ting Chen & Jiayi Chen & Xuan Ding & Shu Zheng & Kiryl D. Piatkevich & Yi Zhu & Tiannan Guo, 2024. "Spatial proteomics of single cells and organelles on tissue slides using filter-aided expansion proteomics," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53683-7
    DOI: 10.1038/s41467-024-53683-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-53683-7
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-53683-7?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. Min Ma & Shihan Huo & Ming Zhang & Shuo Qian & Xiaoyu Zhu & Jie Pu & Sailee Rasam & Chao Xue & Shichen Shen & Bo An & Jianmin Wang & Jun Qu, 2022. "In-depth mapping of protein localizations in whole tissue by micro-scaffold assisted spatial proteomics (MASP)," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Zilu Ye & Pierre Sabatier & Javier Martin-Gonzalez & Akihiro Eguchi & Maico Lechner & Ole Østergaard & Jingsheng Xie & Yuan Guo & Lesley Schultz & Rafaela Truffer & Dorte B. Bekker-Jensen & Nicolai Ba, 2024. "One-Tip enables comprehensive proteome coverage in minimal cells and single zygotes," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    3. Lu Li & Cuiji Sun & Yaoting Sun & Zhen Dong & Runxin Wu & Xiaoting Sun & Hanbin Zhang & Wenhao Jiang & Yan Zhou & Xufeng Cen & Shang Cai & Hongguang Xia & Yi Zhu & Tiannan Guo & Kiryl D. Piatkevich, 2022. "Spatially resolved proteomics via tissue expansion," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Ons M’Saad & Joerg Bewersdorf, 2020. "Light microscopy of proteins in their ultrastructural context," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    5. Yunhao Bai & Bokai Zhu & John-Paul Oliveria & Bryan J. Cannon & Dorien Feyaerts & Marc Bosse & Kausalia Vijayaragavan & Noah F. Greenwald & Darci Phillips & Christian M. Schürch & Samuel M. Naik & Edw, 2023. "Expanded vacuum-stable gels for multiplexed high-resolution spatial histopathology," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Vadim Demichev & Lukasz Szyrwiel & Fengchao Yu & Guo Ci Teo & George Rosenberger & Agathe Niewienda & Daniela Ludwig & Jens Decker & Stephanie Kaspar-Schoenefeld & Kathryn S. Lilley & Michael Mülleder, 2022. "dia-PASEF data analysis using FragPipe and DIA-NN for deep proteomics of low sample amounts," Nature Communications, Nature, vol. 13(1), pages 1-8, 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. Yat Ho Chan & Koralege C. Pathmasiri & Dominick Pierre-Jacques & Maddison C. Hibbard & Nannan Tao & Joshua L. Fischer & Ethan Yang & Stephanie M. Cologna & Ruixuan Gao, 2024. "Gel-assisted mass spectrometry imaging enables sub-micrometer spatial lipidomics," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Simon Davis & Connor Scott & Janina Oetjen & Philip D. Charles & Benedikt M. Kessler & Olaf Ansorge & Roman Fischer, 2023. "Deep topographic proteomics of a human brain tumour," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Fengchao Yu & Guo Ci Teo & Andy T. Kong & Klemens Fröhlich & Ginny Xiaohe Li & Vadim Demichev & Alexey I. Nesvizhskii, 2023. "Analysis of DIA proteomics data using MSFragger-DIA and FragPipe computational platform," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Lingli Kong & Jianfang Liu & Meng Zhang & Zhuoyang Lu & Han Xue & Amy Ren & Jiankang Liu & Jinping Li & Wai Li Ling & Gang Ren, 2023. "Facile hermetic TEM grid preparation for molecular imaging of hydrated biological samples at room temperature," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    5. Guilherme Reis-de-Oliveira & Victor Corasolla Carregari & Gabriel Rodrigues dos Reis de Sousa & Daniel Martins-de-Souza, 2024. "OmicScope unravels systems-level insights from quantitative proteomics data," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    6. Yi Yang & Qun Fang, 2024. "Prediction of glycopeptide fragment mass spectra by deep learning," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    7. Alexander A. Morano & Rachel M. Rudlaff & Jeffrey D. Dvorin, 2023. "A PPP-type pseudophosphatase is required for the maintenance of basal complex integrity in Plasmodium falciparum," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Karsten Suhre & Guhan Ram Venkataraman & Harendra Guturu & Anna Halama & Nisha Stephan & Gaurav Thareja & Hina Sarwath & Khatereh Motamedchaboki & Margaret K. R. Donovan & Asim Siddiqui & Serafim Batz, 2024. "Nanoparticle enrichment mass-spectrometry proteomics identifies protein-altering variants for precise pQTL mapping," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    9. Ravish Rashpa & Natacha Klages & Domitille Schvartz & Carla Pasquarello & Mathieu Brochet, 2023. "The Skp1-Cullin1-FBXO1 complex is a pleiotropic regulator required for the formation of gametes and motile forms in Plasmodium berghei," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    10. Vincent Louvel & Romuald Haase & Olivier Mercey & Marine H. Laporte & Thibaut Eloy & Étienne Baudrier & Denis Fortun & Dominique Soldati-Favre & Virginie Hamel & Paul Guichard, 2023. "iU-ExM: nanoscopy of organelles and tissues with iterative ultrastructure expansion microscopy," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Karl K. Krull & Syed Azmal Ali & Jeroen Krijgsveld, 2024. "Enhanced feature matching in single-cell proteomics characterizes IFN-γ response and co-existence of cell states," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    12. Humberto J. Ferreira & Brian J. Stevenson & HuiSong Pak & Fengchao Yu & Jessica Almeida Oliveira & Florian Huber & Marie Taillandier-Coindard & Justine Michaux & Emma Ricart-Altimiras & Anne I. Kraeme, 2024. "Immunopeptidomics-based identification of naturally presented non-canonical circRNA-derived peptides," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    13. Valdemaras Petrosius & Pedro Aragon-Fernandez & Nil Üresin & Gergo Kovacs & Teeradon Phlairaharn & Benjamin Furtwängler & Jeff Op De Beeck & Sarah L. Skovbakke & Steffen Goletz & Simon Francis Thomsen, 2023. "Exploration of cell state heterogeneity using single-cell proteomics through sensitivity-tailored data-independent acquisition," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    14. Claudia Ctortecka & Natalie M. Clark & Brian W. Boyle & Anjali Seth & D. R. Mani & Namrata D. Udeshi & Steven A. Carr, 2024. "Automated single-cell proteomics providing sufficient proteome depth to study complex biology beyond cell type classifications," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    15. Daniel Salas-Lloret & Néstor García-Rodríguez & Emily Soto-Hidalgo & Lourdes González-Vinceiro & Carmen Espejo-Serrano & Lisanne Giebel & María Luisa Mateos-Martín & Arnoud H. Ru & Peter A. Veelen & P, 2024. "BRCA1/BARD1 ubiquitinates PCNA in unperturbed conditions to promote continuous DNA synthesis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    16. Mingdu Luo & Yandong Yin & Zhiwei Zhou & Haosong Zhang & Xi Chen & Hongmiao Wang & Zheng-Jiang Zhu, 2023. "A mass spectrum-oriented computational method for ion mobility-resolved untargeted metabolomics," Nature Communications, Nature, vol. 14(1), pages 1-15, 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:15:y:2024:i:1:d:10.1038_s41467-024-53683-7. 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.