Migrasomal autophagosomes relieve endoplasmic reticulum stress in glioblastoma cells

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Abstract

Background

Glioblastoma (GBM) is more difficult to treat than other intractable adult tumors. The main reason that GBM is so difficult to treat is that it is highly infiltrative. Migrasomes are newly discovered membrane structures observed in migrating cells. Thus, they can be generated from GBM cells that have the ability to migrate along the brain parenchyma. However, the function of migrasomes has not yet been elucidated in GBM cells.

Results

Here, we describe the composition and function of migrasomes generated along with GBM cell migration. Proteomic analysis revealed that LC3B-positive autophagosomes were abundant in the migrasomes of GBM cells. An increased number of migrasomes was observed following treatment with chloroquine (CQ) or inhibition of the expression of STX17 and SNAP29, which are involved in autophagosome/lysosome fusion. Furthermore, depletion of ITGA5 or TSPAN4 did not relieve endoplasmic reticulum (ER) stress in cells, resulting in cell death.

Conclusions

Taken together, our study suggests that increasing the number of autophagosomes, through inhibition of autophagosome/lysosome fusion, generates migrasomes that have the capacity to alleviate cellular stress.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12915-024-01829-w.

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Most cited references 66

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Enrichr: a comprehensive gene set enrichment analysis web server 2016 update

Maxim Kuleshov, Matthew Jones, Andrew D. Rouillard … (2016)

Enrichment analysis is a popular method for analyzing gene sets generated by genome-wide experiments. Here we present a significant update to one of the tools in this domain called Enrichr. Enrichr currently contains a large collection of diverse gene set libraries available for analysis and download. In total, Enrichr currently contains 180 184 annotated gene sets from 102 gene set libraries. New features have been added to Enrichr including the ability to submit fuzzy sets, upload BED files, improved application programming interface and visualization of the results as clustergrams. Overall, Enrichr is a comprehensive resource for curated gene sets and a search engine that accumulates biological knowledge for further biological discoveries. Enrichr is freely available at: http://amp.pharm.mssm.edu/Enrichr.

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Radiotherapy plus Concomitant and Adjuvant Temozolomide for Glioblastoma

Roger Stupp, Warren P Mason, Martin van den Bent … (2005)

Glioblastoma, the most common primary brain tumor in adults, is usually rapidly fatal. The current standard of care for newly diagnosed glioblastoma is surgical resection to the extent feasible, followed by adjuvant radiotherapy. In this trial we compared radiotherapy alone with radiotherapy plus temozolomide, given concomitantly with and after radiotherapy, in terms of efficacy and safety. Patients with newly diagnosed, histologically confirmed glioblastoma were randomly assigned to receive radiotherapy alone (fractionated focal irradiation in daily fractions of 2 Gy given 5 days per week for 6 weeks, for a total of 60 Gy) or radiotherapy plus continuous daily temozolomide (75 mg per square meter of body-surface area per day, 7 days per week from the first to the last day of radiotherapy), followed by six cycles of adjuvant temozolomide (150 to 200 mg per square meter for 5 days during each 28-day cycle). The primary end point was overall survival. A total of 573 patients from 85 centers underwent randomization. The median age was 56 years, and 84 percent of patients had undergone debulking surgery. At a median follow-up of 28 months, the median survival was 14.6 months with radiotherapy plus temozolomide and 12.1 months with radiotherapy alone. The unadjusted hazard ratio for death in the radiotherapy-plus-temozolomide group was 0.63 (95 percent confidence interval, 0.52 to 0.75; P<0.001 by the log-rank test). The two-year survival rate was 26.5 percent with radiotherapy plus temozolomide and 10.4 percent with radiotherapy alone. Concomitant treatment with radiotherapy plus temozolomide resulted in grade 3 or 4 hematologic toxic effects in 7 percent of patients. The addition of temozolomide to radiotherapy for newly diagnosed glioblastoma resulted in a clinically meaningful and statistically significant survival benefit with minimal additional toxicity. Copyright 2005 Massachusetts Medical Society.

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The PRIDE database and related tools and resources in 2019: improving support for quantification data

Yasset Perez-Riverol, Attila Csordas, Jingwen Bai … (2018)

Abstract The PRoteomics IDEntifications (PRIDE) database (https://www.ebi.ac.uk/pride/) is the world’s largest data repository of mass spectrometry-based proteomics data, and is one of the founding members of the global ProteomeXchange (PX) consortium. In this manuscript, we summarize the developments in PRIDE resources and related tools since the previous update manuscript was published in Nucleic Acids Research in 2016. In the last 3 years, public data sharing through PRIDE (as part of PX) has definitely become the norm in the field. In parallel, data re-use of public proteomics data has increased enormously, with multiple applications. We first describe the new architecture of PRIDE Archive, the archival component of PRIDE. PRIDE Archive and the related data submission framework have been further developed to support the increase in submitted data volumes and additional data types. A new scalable and fault tolerant storage backend, Application Programming Interface and web interface have been implemented, as a part of an ongoing process. Additionally, we emphasize the improved support for quantitative proteomics data through the mzTab format. At last, we outline key statistics on the current data contents and volume of downloads, and how PRIDE data are starting to be disseminated to added-value resources including Ensembl, UniProt and Expression Atlas.

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Author and article information

Contributors

Hyunggee Kim:

ORCID: http://orcid.org/0000-0002-5164-1663

hg-kim@korea.ac.kr

Journal

Journal ID (nlm-ta): BMC Biol

Journal ID (iso-abbrev): BMC Biol

Title: BMC Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1741-7007

Publication date (Electronic): 30 January 2024

Publication date PMC-release: 30 January 2024

Publication date Collection: 2024

Volume: 22

Electronic Location Identifier: 23

Affiliations

[1 ]Department of Biotechnology, Korea University, ( https://ror.org/047dqcg40) Seoul, Republic of Korea

[2 ]Institute of Animal Molecular Biotechnology, Korea University, ( https://ror.org/047dqcg40) Seoul, Republic of Korea

[3 ]Convergence Medicine Research Center, Asan Institute for Life Sciences, Asan Medical Center, ( https://ror.org/03s5q0090) Seoul, Republic of Korea

[4 ]Department of Life Sciences, Korea University, ( https://ror.org/047dqcg40) Seoul, Republic of Korea

[5 ]GRID grid.267370.7, ISNI 0000 0004 0533 4667, Department of Convergence Medicine, Asan Medical Center, , University of Ulsan College of Medicine, ; Seoul, Republic of Korea

[6 ]Division of Life Sciences, College of Life Sciences and Biotechnology, Korea University, ( https://ror.org/047dqcg40) Seoul, Republic of Korea

Author information

Hyunggee Kim http://orcid.org/0000-0002-5164-1663

Article

Publisher ID: 1829

DOI: 10.1186/s12915-024-01829-w

PMC ID: 10826056

PubMed ID: 38287397

SO-VID: 9d1cc7a1-81f6-4e3a-808e-7dd555b90808

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 18 July 2022

Date accepted : 16 January 2024

Funding

Funded by: National Research Foundation of Korea

Award ID: 2015R1A5A1009024

Award ID: 2019M3E5D3073106

Award ID: 2015R1A5A1009024

Award Recipient : Young-Gyu Ko Kyunggon Kim Sung Wook Chi Hyunggee Kim

Funded by: FundRef http://dx.doi.org/10.13039/100014718, Innovative Research Group Project of the National Natural Science Foundation of China;

Award ID: RS-2023-00218838

Award Recipient : Hyunggee Kim

Funded by: FundRef http://dx.doi.org/10.13039/501100004093, Kwanjeong Educational Foundation;

Award ID: KEF1378

Award Recipient : Yoonji Kim

Custom metadata

ScienceOpen disciplines: Life sciences

Keywords: autophagosome,er stress,migrasome,retraction fiber,cell death,itga5,tspan4

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: autophagosome, er stress, migrasome, retraction fiber, cell death, itga5, tspan4

Migrasomal autophagosomes relieve endoplasmic reticulum stress in glioblastoma cells

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Most cited references 66

Enrichr: a comprehensive gene set enrichment analysis web server 2016 update

Radiotherapy plus Concomitant and Adjuvant Temozolomide for Glioblastoma

The PRIDE database and related tools and resources in 2019: improving support for quantification data

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