Vimentin promotes glioma progression and maintains glioma cell resistance to oxidative phosphorylation inhibition.
Drug resistance
Glioma
Immune infiltration
Oxidative phosphorylation
Vimentin
Journal
Cellular oncology (Dordrecht)
ISSN: 2211-3436
Titre abrégé: Cell Oncol (Dordr)
Pays: Netherlands
ID NLM: 101552938
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
accepted:
12
07
2023
medline:
6
12
2023
pubmed:
30
8
2023
entrez:
30
8
2023
Statut:
ppublish
Résumé
Glioma has been demonstrated as one of the most malignant intracranial tumors and currently there is no effective treatment. Based on our previous RNA-sequencing data for oxidative phosphorylation (OXPHOS)-inhibition resistant and OXPHOS-inhibition sensitive cancer cells, we found that vimentin (VIM) is highly expressed in the OXPHOS-inhibition resistant cancer cells, especially in glioma cancer cells. Further study of VIM in the literature indicates that it plays important roles in cancer progression, immunotherapy suppression, cancer stemness and drug resistance. However, its role in glioma remains elusive. This study aims to decipher the role of VIM in glioma, especially its role in OXPHOS-inhibition sensitivity, which may provide a promising therapeutic target for glioma treatment. The expression of VIM in glioma and the normal tissue has been obtained from The Cancer Genome Atlas (TCGA) database, and further validated in Human Protein Atlas (HPA) and Chinese Glioma Genome Atlas (CGGA). And the single-cell sequencing data was obtained from TISCH2. The immune infiltration was calculated via Tumor Immune Estimation Resource (TIMER), Estimation of Stromal and Immune Cells in Malignant Tumors using Expression Data (ESTIMATE) and ssGSEA, and the Immunophenoscore (IPS) was calculated via R package. The differentiated expressed genes were analyzed including GO/KEGG and Gene Set Enrichment Analysis (GSEA) between the VIM-high and -low groups. The methylation of VIM was checked at the EWAS and Methsurv. The correlation between VIM expression and cancer stemness was obtained from SangerBox. We also employed DepMap data and verified the role of VIM by knocking down it in VIM-high glioma cell and over-expressing it in VIM-low glioma cells to check the cell viability. Vim is highly expressed in the glioma patients compared to normal samples and its high expression negatively correlates with patients' survival. The DNA methylation in VIM promoters in glioma patients is lower than that in the normal samples. High VIM expression positively correlates with the immune infiltration and tumor progression. Furthermore, Vim is expressed high in the OXPHOS-inhibition glioma cancer cells and low in the OXPHOS-inhibition sensitive ones and its expression maintains the OXPHOS-inhibition resistance. In conclusion, we comprehensively deciphered the role of VIM in the progression of glioma and its clinical outcomes. Thus provide new insights into targeting VIM in glioma cancer immunotherapy in combination with the current treatment.
Identifiants
pubmed: 37646965
doi: 10.1007/s13402-023-00844-3
pii: 10.1007/s13402-023-00844-3
doi:
Substances chimiques
Vimentin
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1791-1806Subventions
Organisme : National Natural Science Foundation of China
ID : 82073274
Organisme : Science and Technology Commission of Shanghai Municipality
ID : 20S11900700, Y.S
Organisme : Discipline Climbing Scheme
ID : 2019YXK030
Organisme : Neuroscience Innovation and Development Research Project
ID : YXJL-2022-00351-0183
Informations de copyright
© 2023. Springer Nature Switzerland AG.
Références
V. Venkataramani, Y. Yang, M.C. Schubert et al., Glioblastoma hijacks neuronal mechanisms for brain invasion. Cell 185(16), 2899-2917 e2831 (2022)
doi: 10.1016/j.cell.2022.06.054
pubmed: 35914528
P. Wesseling, D. Capper, WHO 2016 classification of gliomas. Neuropathol. Appl. Neurobiol. 44(2), 139–150 (2018)
doi: 10.1111/nan.12432
pubmed: 28815663
S. Huang, Y. Liu, Y. Zhang et al., Baicalein inhibits SARS-CoV-2/VSV replication with interfering mitochondrial oxidative phosphorylation in a mPTP dependent manner. Signal Transduct. Target. Ther. 5(1), 266 (2020)
doi: 10.1038/s41392-020-00353-x
pubmed: 33188163
pmcid: 7662024
Y. Liu, C. Chen, X. Wang, et al., An epigenetic role of mitochondria in cancer. Cells 11(16), 2518 (2022)
Y.E. Liu, Y.F. Shi, Mitochondria as a target in cancer treatment. Medcomm 1(2), 129–139 (2020)
doi: 10.1002/mco2.16
pubmed: 34766113
pmcid: 8491233
Y. Liu, Y. Sun, Y. Guo et al., An overview: the diversified role of mitochondria in cancer metabolism. Int. J. Biol. Sci. 19(3), 897–915 (2023)
doi: 10.7150/ijbs.81609
pubmed: 36778129
pmcid: 9910000
C. Wu, Y. Liu, W. Liu et al., NNMT-DNMT1 axis is essential for maintaining cancer cell sensitivity to oxidative phosphorylation inhibition. Adv. Sci. (Weinh) 10(1), e2202642 (2022)
doi: 10.1002/advs.202202642
pubmed: 36382559
R.A. Battaglia, S. Delic, H. Herrmann, N.T. Snider, Vimentin on the move: new developments in cell migration. F1000Res 7, (2018)
N.A. Kuburich, P. den Hollander, J.T. Pietz, S.A. Mani, Vimentin and cytokeratin: Good alone, bad together. Semin. Cancer Biol. 86(Pt 3), 816–826 (2022)
doi: 10.1016/j.semcancer.2021.12.006
pubmed: 34953942
H.J. Sim, M.S. Song, S.Y. Lee, Kv3 channels contribute to cancer cell migration via vimentin regulation. Biochem. Biophys. Res. Commun. 551, 140–147 (2021)
doi: 10.1016/j.bbrc.2021.03.019
pubmed: 33740620
S. Usman, A. Jamal, A. Bushaala, et al., Transcriptome analysis reveals vimentin-induced disruption of ell-cell associations augments breast cancer cell migration. Cells 11(24), 4035 (2022)
C. Wei, C. Yang, S. Wang et al., Crosstalk between cancer cells and tumor associated macrophages is required for mesenchymal circulating tumor cell-mediated colorectal cancer metastasis. Mol. Cancer 18(1), 64 (2019)
doi: 10.1186/s12943-019-0976-4
pubmed: 30927925
pmcid: 6441214
N. Zhang, X. Hua, H. Tu et al., Isorhapontigenin (ISO) inhibits EMT through FOXO3A/METTL14/VIMENTIN pathway in bladder cancer cells. Cancer Lett. 520, 400–408 (2021)
doi: 10.1016/j.canlet.2021.07.041
pubmed: 34332039
pmcid: 9161647
D.L. Lazarova, M. Bordonaro, Vimentin, colon cancer progression and resistance to butyrate and other HDACis. J. Cell. Mol. Med. 20(6), 989–993 (2016)
doi: 10.1111/jcmm.12850
pubmed: 27072512
pmcid: 4882977
Y. Huo, Z. Zheng, Y. Chen et al., Downregulation of vimentin expression increased drug resistance in ovarian cancer cells. Oncotarget 7(29), 45876–45888 (2016)
doi: 10.18632/oncotarget.9970
pubmed: 27322682
pmcid: 5216767
M. Hashemi, H.Z. Arani, S. Orouei et al., EMT mechanism in breast cancer metastasis and drug resistance: Revisiting molecular interactions and biological functions. Biomed. Pharmacother. 155, 113774 (2022)
doi: 10.1016/j.biopha.2022.113774
pubmed: 36271556
Y. Han, Y. Wang, X. Dong, et al., TISCH2: expanded datasets and new tools for single-cell transcriptome analyses of the tumor microenvironment. Nucleic Acids Res. 51(D1), D1425–D1431 (2023)
M.E. Ritchie, B. Phipson, D. Wu et al., limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43(7), e47 (2015)
doi: 10.1093/nar/gkv007
pubmed: 25605792
pmcid: 4402510
G. Yu, L.G. Wang, Y. Han, Q.Y. He, clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16(5), 284–287 (2012)
doi: 10.1089/omi.2011.0118
pubmed: 22455463
pmcid: 3339379
K. Yoshihara, M. Shahmoradgoli, E. Martinez et al., Inferring tumour purity and stromal and immune cell admixture from expression data. Nat. Commun. 4, 2612 (2013)
doi: 10.1038/ncomms3612
pubmed: 24113773
D. Zeng, Z. Ye, R. Shen et al., IOBR: Multi-Omics immuno-oncology biological research to decode tumor microenvironment and signatures. Front. Immunol. 12, 687975 (2021)
doi: 10.3389/fimmu.2021.687975
pubmed: 34276676
pmcid: 8283787
P. Charoentong, F. Finotello, M. Angelova et al., Pan-cancer immunogenomic analyses reveal genotype-immunophenotype relationships and predictors of response to checkpoint blockade. Cell Rep. 18(1), 248–262 (2017)
doi: 10.1016/j.celrep.2016.12.019
pubmed: 28052254
V. Thorsson, D.L. Gibbs, S.D. Brown et al., The immune landscape of cancer. Immunity 48(4), 812-830 e814 (2018)
doi: 10.1016/j.immuni.2018.03.023
pubmed: 29628290
pmcid: 5982584
Z. Xiong, F. Yang, M. Li et al., EWAS Open Platform: integrated data, knowledge and toolkit for epigenome-wide association study. Nucleic Acids Res. 50(D1), D1004–D1009 (2022)
doi: 10.1093/nar/gkab972
pubmed: 34718752
Y. Liu, Y. Wang, Y. Yang et al., Emerging phagocytosis checkpoints in cancer immunotherapy. Signal Transduct. Target. Ther. 8(1), 104 (2023)
doi: 10.1038/s41392-023-01365-z
pubmed: 36882399
pmcid: 9990587
Y.e. Liu, S. Lu, Y. Sun, et al., Deciphering the role of QPCTL in glioma progression and cancer immunotherapy. Front. Immunol. 14, 1166377 (2023)
Y. Shi, S.K. Lim, Q. Liang et al., Gboxin is an oxidative phosphorylation inhibitor that targets glioblastoma. Nature 567(7748), 341–346 (2019)
doi: 10.1038/s41586-019-0993-x
pubmed: 30842654
pmcid: 6655586
M.E. Kidd, D.K. Shumaker, K.M. Ridge, The role of vimentin intermediate filaments in the progression of lung cancer. Am. J. Respir. Cell. Mol. Biol. 50(1), 1–6 (2014)
doi: 10.1165/rcmb.2013-0314TR
pubmed: 23980547
pmcid: 3930939
H.R. Jang, S.B. Shin, C.H. Kim et al., PLK1/vimentin signaling facilitates immune escape by recruiting Smad2/3 to PD-L1 promoter in metastatic lung adenocarcinoma. Cell. Death Differ. 28(9), 2745–2764 (2021)
doi: 10.1038/s41418-021-00781-4
pubmed: 33963314
pmcid: 8408167
J.M. Peng, C.F. Chiu, J.H. Cheng et al., Evasion of NK cell immune surveillance via the vimentin-mediated cytoskeleton remodeling. Front. Immunol. 13, 883178 (2022)
doi: 10.3389/fimmu.2022.883178
pubmed: 36032170
pmcid: 9402923
H. Liu, G. Ye, X. Liu et al., Vimentin inhibits type I interferon production by disrupting the TBK1-IKKepsilon-IRF3 axis. Cell Rep. 41(2), 111469 (2022)
doi: 10.1016/j.celrep.2022.111469
pubmed: 36223739
S. Kim, W. Cho, I. Kim et al., Oxidized LDL induces vimentin secretion by macrophages and contributes to atherosclerotic inflammation. J. Mol. Med. (Berl) 98(7), 973–983 (2020)
doi: 10.1007/s00109-020-01923-w
pubmed: 32451671
M.B. Yu, J. Guerra, A. Firek, W.H.R. Langridge, Extracellular vimentin modulates human dendritic cell activation. Mol. Immunol. 104, 37–46 (2018)
doi: 10.1016/j.molimm.2018.09.017
pubmed: 30399492
pmcid: 6497527
S. Pattabiraman, G.K. Azad, T. Amen et al., Vimentin protects differentiating stem cells from stress. Sci. Rep. 10(1), 19525 (2020)
doi: 10.1038/s41598-020-76076-4
pubmed: 33177544
pmcid: 7658978