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Laminin Subunit Alpha-4 and Osteopontin Are Glioblastoma-Selective Secreted Proteins That Are Increased in the Cerebrospinal Fluid of Glioblastoma Patients

  • Tomohiro Kohata
    Tomohiro Kohata
    Department of Pharmaceutical Microbiology, Graduate School of Pharmaceutical Sciences, Kumamoto University, Kumamoto, Japan
  • Shingo Ito
    Shingo Ito
    Department of Pharmaceutical Microbiology, Graduate School of Pharmaceutical Sciences, Kumamoto University, Kumamoto, Japan
    Department of Pharmaceutical Microbiology, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan
    AMED-CREST, Tokyo, Japan
    More by Shingo Ito
  • Takeshi Masuda
    Takeshi Masuda
    Department of Pharmaceutical Microbiology, Graduate School of Pharmaceutical Sciences, Kumamoto University, Kumamoto, Japan
    Department of Pharmaceutical Microbiology, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan
    AMED-CREST, Tokyo, Japan
  • Takuya Furuta
    Takuya Furuta
    Department of Pathology, Kurume University School of Medicine, Kurume, Japan
    Department of Neurosurgery, Kanazawa University, Kanazawa, Japan
  • Mitsutoshi Nakada
    Mitsutoshi Nakada
    Department of Neurosurgery, Kanazawa University, Kanazawa, Japan
  • , and 
  • Sumio Ohtsuki*
    Sumio Ohtsuki
    Department of Pharmaceutical Microbiology, Graduate School of Pharmaceutical Sciences, Kumamoto University, Kumamoto, Japan
    Department of Pharmaceutical Microbiology, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan
    AMED-CREST, Tokyo, Japan
    *Tel.: +81-96-371-4323. Fax: +81-96-371-4329. Email: [email protected]
Cite this: J. Proteome Res. 2020, 19, 8, 3542–3553
Publication Date (Web):July 6, 2020
https://doi.org/10.1021/acs.jproteome.0c00415
Copyright © 2020 American Chemical Society

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    Abstract

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    Glioblastoma (GBM) is the most common and aggressive brain tumor in adults. The purpose of the present study was to identify GBM cell-selective secreted proteins by analyzing conditioned media (CM) from GBM, breast, and colon cancer cell lines using sequential window acquisition of all theoretical spectra-mass spectrometry (SWATH-MS) and targeted proteomics. We identified 2371 proteins in the CM from GBM and the other cancer cell lines. Among the proteins identified, 15 showed significantly higher expression in the CM from GBM cell lines than in those from other cancer cell lines. These GBM-selective secreted proteins were further quantified in the cerebrospinal fluid (CSF) from patients with GBM. Laminin subunit alpha-4 (LAMA4) and osteopontin (OPN) had increased expression levels in the CSF from GBM patients compared to those from non-brain tumor patients. In addition, the areas under the curves in a receiver operating characteristic analysis of LAMA4 and OPN were greater than 0.9, allowing for discrimination of GBM patients from non-brain tumor patients. The CSF levels of LAMA4 and OPN were also significantly correlated with the GBM tumor volume. These results suggest that LAMA4 and OPN are secreted from GBM cells into the CSF and appear to be candidates as diagnostic markers and therapeutic targets for GBM.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.jproteome.0c00415.

    • Morphology of breast cancer and colon cancer cell lines under serum starvation conditions; expression levels of nonsignificant GBM-selective secreted proteins in the CM of GBM and non-GBM cell lines; standard curves of peptides measured by targeted proteomics and LAMA4 measured by Simple Western; gel-like image of Simple Western detecting LAMA4 in the CSF samples; levels of GSN secreted in the CM of GBM and non-GBM cell lines; cellular component analysis of GBM-selective secreted proteins; proteins selectively identified in the CM of two breast cancer cell lines and colon cancer cell line; signature tryptic peptides for quantification by targeted proteomics (PDF)

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    Cited By

    This article is cited by 7 publications.

    1. Lawrence L. Leung, Timothy Myles, John Morser. Thrombin Cleavage of Osteopontin and the Host Anti-Tumor Immune Response. Cancers 2023, 15 (13) , 3480. https://doi.org/10.3390/cancers15133480
    2. Ryotaro Yagi, Takeshi Masuda, Shingo Ito, Sumio Ohtsuki. Effect of antibiotic-administration period on hepatic bile acid profile and expression of pharmacokinetic-related proteins in mouse liver, kidney, and brain capillaries. Drug Metabolism and Pharmacokinetics 2023, 50 , 100494. https://doi.org/10.1016/j.dmpk.2023.100494
    3. Sanaa A. El-Benhawy, Ola A. Sakr, Enayat I. Fahmy, Raed A. Ali, Mohamed S. Hussein, Esraa M. Nassar, Sherif M. Salem, Nehal Abu-Samra, Sherif Elzawawy. Assessment of Serum Hypoxia Biomarkers Pre- and Post-radiotherapy in Patients with Brain Tumors. Journal of Molecular Neuroscience 2022, 72 (11) , 2303-2312. https://doi.org/10.1007/s12031-022-02065-z
    4. Syed M. Faisal, Andrea Comba, Maria L. Varela, Anna E. Argento, Emily Brumley, Clifford Abel, Maria G. Castro, Pedro R. Lowenstein. The complex interactions between the cellular and non-cellular components of the brain tumor microenvironmental landscape and their therapeutic implications. Frontiers in Oncology 2022, 12 https://doi.org/10.3389/fonc.2022.1005069
    5. Yoshinobu Kariya, Yukiko Kariya. Osteopontin in Cancer: Mechanisms and Therapeutic Targets. International Journal of Translational Medicine 2022, 2 (3) , 419-447. https://doi.org/10.3390/ijtm2030033
    6. Hinako Nagano, Shingo Ito, Takeshi Masuda, Sumio Ohtsuki. Effect of Insulin Receptor-Knockdown on the Expression Levels of Blood–Brain Barrier Functional Proteins in Human Brain Microvascular Endothelial Cells. Pharmaceutical Research 2022, 39 (7) , 1561-1574. https://doi.org/10.1007/s11095-021-03131-8
    7. Takeshi Masuda, Shingo Ito, Sumio Ohtsuki. Advances in sample preparation for membrane proteome quantification. Drug Discovery Today: Technologies 2021, 39 , 23-29. https://doi.org/10.1016/j.ddtec.2021.06.005

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