Skip to main content
Top
Published in: Cancer Cell International 1/2022

Open Access 01-12-2022 | Glioblastoma | Primary Research

Molecular mechanism by which CDCP1 promotes proneural-mesenchymal transformation in primary glioblastoma

Authors: Zhiying Lin, Zhu Zhang, Haojie Zheng, Haiyan Xu, Yajuan Wang, Chao Chen, Junlu Liu, Guozhong Yi, Zhiyong Li, Xiaoyan Wang, Guanglong Huang

Published in: Cancer Cell International | Issue 1/2022

Login to get access

Abstract

Background

Compared with the proneural (PN) subtype of glioblastoma (GBM), the mesenchymal (MES) subtype is more invasive and immune evasive and is closely related to poor prognosis. Here, we used transcriptome data and experimental evidence to indicate that CUB domain-containing protein 1 (CDCP1) is a novel regulator that facilitates the transformation of PN-GBM to MES-GBM.

Methods

The mRNA expression data of CDCP1 in glioma were collected from the TCGA, CGGA and GEO databases, and in vitro experiments verified CDCP1 expression in glioma tissue samples. Independent prognostic analysis revealed the correlation of the CDCP1 expression level and patient survival. Bioinformatics analysis and experiments verified the biological function of CDCP1. Multivariate proportional hazards models and a PPI network were used to select key genes. A prognostic risk model for predicting the survival of glioma patients was constructed based on the selected genes.

Results

The results showed that the expression of CDCP1 increased with increasing tumor grade and that the overexpression of CDCP1 correlated with a poor prognosis. CDCP1 was highly expressed in MES-GBM but weakly expressed in PN-GBM. The risk model (considering CDCP1 combined with CD44 and ITGAM expression) could represent a tool for predicting survival and prognosis in glioma patients.

Conclusions

Our study indicates that CDCP1 plays an important role in facilitating the transformation of PN-GBM to MES-GBM.
Appendix
Available only for authorised users
Literature
1.
go back to reference Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131(6):803–20.PubMedCrossRef Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131(6):803–20.PubMedCrossRef
2.
go back to reference Thakkar JP, Dolecek TA, Horbinski C, Ostrom QT, Lightner DD, Barnholtz-Sloan JS, Villano JL. Epidemiologic and molecular prognostic review of glioblastoma. Cancer Epidemiol Biomarkers Prev. 2014;23(10):1985–96.PubMedPubMedCentralCrossRef Thakkar JP, Dolecek TA, Horbinski C, Ostrom QT, Lightner DD, Barnholtz-Sloan JS, Villano JL. Epidemiologic and molecular prognostic review of glioblastoma. Cancer Epidemiol Biomarkers Prev. 2014;23(10):1985–96.PubMedPubMedCentralCrossRef
3.
go back to reference Wang L, Babikir H, Muller S, Yagnik G, Shamardani K, Catalan F, Kohanbash G, Alvarado B, Di Lullo E, Kriegstein A, et al. The phenotypes of proliferating glioblastoma cells reside on a single axis of variation. Cancer Discov. 2019;9(12):1708–19.PubMedPubMedCentralCrossRef Wang L, Babikir H, Muller S, Yagnik G, Shamardani K, Catalan F, Kohanbash G, Alvarado B, Di Lullo E, Kriegstein A, et al. The phenotypes of proliferating glioblastoma cells reside on a single axis of variation. Cancer Discov. 2019;9(12):1708–19.PubMedPubMedCentralCrossRef
4.
go back to reference Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17(1):98–110.PubMedPubMedCentralCrossRef Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17(1):98–110.PubMedPubMedCentralCrossRef
5.
go back to reference Bhat KPL, Balasubramaniyan V, Vaillant B, Ezhilarasan R, Hummelink K, Hollingsworth F, Wani K, Heathcock L, James JD, Goodman LD, et al. Mesenchymal differentiation mediated by NF-kappaB promotes radiation resistance in glioblastoma. Cancer Cell. 2013;24(3):331–46.PubMedCrossRef Bhat KPL, Balasubramaniyan V, Vaillant B, Ezhilarasan R, Hummelink K, Hollingsworth F, Wani K, Heathcock L, James JD, Goodman LD, et al. Mesenchymal differentiation mediated by NF-kappaB promotes radiation resistance in glioblastoma. Cancer Cell. 2013;24(3):331–46.PubMedCrossRef
6.
go back to reference Prins RM, Soto H, Konkankit V, Odesa SK, Eskin A, Yong WH, Nelson SF, Liau LM. Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy. Clin Cancer Res. 2011;17(6):1603–15.PubMedCrossRef Prins RM, Soto H, Konkankit V, Odesa SK, Eskin A, Yong WH, Nelson SF, Liau LM. Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy. Clin Cancer Res. 2011;17(6):1603–15.PubMedCrossRef
7.
go back to reference Kaffes I, Szulzewsky F, Chen Z, Herting CJ, Gabanic B, Velazquez Vega JE, Shelton J, Switchenko JM, Ross JL, McSwain LF, et al. Human mesenchymal glioblastomas are characterized by an increased immune cell presence compared to proneural and classical tumors. Oncoimmunology. 2019;8(11):e1655360.PubMedPubMedCentralCrossRef Kaffes I, Szulzewsky F, Chen Z, Herting CJ, Gabanic B, Velazquez Vega JE, Shelton J, Switchenko JM, Ross JL, McSwain LF, et al. Human mesenchymal glioblastomas are characterized by an increased immune cell presence compared to proneural and classical tumors. Oncoimmunology. 2019;8(11):e1655360.PubMedPubMedCentralCrossRef
8.
go back to reference Rutledge WC, Kong J, Gao J, Gutman DA, Cooper LA, Appin C, Park Y, Scarpace L, Mikkelsen T, Cohen ML, et al. Tumor-infiltrating lymphocytes in glioblastoma are associated with specific genomic alterations and related to transcriptional class. Clin Cancer Res. 2013;19(18):4951–60.PubMedCrossRef Rutledge WC, Kong J, Gao J, Gutman DA, Cooper LA, Appin C, Park Y, Scarpace L, Mikkelsen T, Cohen ML, et al. Tumor-infiltrating lymphocytes in glioblastoma are associated with specific genomic alterations and related to transcriptional class. Clin Cancer Res. 2013;19(18):4951–60.PubMedCrossRef
9.
go back to reference Martinez-Lage M, Lynch TM, Bi Y, Cocito C, Way GP, Pal S, Haller J, Yan RE, Ziober A, Nguyen A, et al. Immune landscapes associated with different glioblastoma molecular subtypes. Acta Neuropathol Commun. 2019;7(1):203.PubMedPubMedCentralCrossRef Martinez-Lage M, Lynch TM, Bi Y, Cocito C, Way GP, Pal S, Haller J, Yan RE, Ziober A, Nguyen A, et al. Immune landscapes associated with different glioblastoma molecular subtypes. Acta Neuropathol Commun. 2019;7(1):203.PubMedPubMedCentralCrossRef
10.
go back to reference Bailey M, Tokheim C, Porta-Pardo E, Sengupta S, Bertrand D, Weerasinghe A, Colaprico A, Wendl M, Kim J, Reardon B, et al. Comprehensive characterization of cancer driver genes and mutations. Cell. 2018;173(2):371-385.e318.PubMedPubMedCentralCrossRef Bailey M, Tokheim C, Porta-Pardo E, Sengupta S, Bertrand D, Weerasinghe A, Colaprico A, Wendl M, Kim J, Reardon B, et al. Comprehensive characterization of cancer driver genes and mutations. Cell. 2018;173(2):371-385.e318.PubMedPubMedCentralCrossRef
11.
go back to reference Weinstein JN, Collisson EA, Mills GB, Shaw KR, Ozenberger BA, Ellrott K, Shmulevich I, Sander C, Stuart JM, Cancer Genome Atlas Research N. The cancer genome atlas pan-cancer analysis project. Nat Genet. 2013;45(10):1113–20.PubMedPubMedCentralCrossRef Weinstein JN, Collisson EA, Mills GB, Shaw KR, Ozenberger BA, Ellrott K, Shmulevich I, Sander C, Stuart JM, Cancer Genome Atlas Research N. The cancer genome atlas pan-cancer analysis project. Nat Genet. 2013;45(10):1113–20.PubMedPubMedCentralCrossRef
12.
go back to reference Feng X, Zhang L, Ke S, Liu T, Hao L, Zhao P, Tu W, Cang S. High expression of GPNMB indicates an unfavorable prognosis in glioma: Combination of data from the GEO and CGGA databases and validation in tissue microarray. Oncol Lett. 2020;20(3):2356–68.PubMedPubMedCentralCrossRef Feng X, Zhang L, Ke S, Liu T, Hao L, Zhao P, Tu W, Cang S. High expression of GPNMB indicates an unfavorable prognosis in glioma: Combination of data from the GEO and CGGA databases and validation in tissue microarray. Oncol Lett. 2020;20(3):2356–68.PubMedPubMedCentralCrossRef
13.
go back to reference Liu W, Xu Z, Zhou J, Xing S, Li Z, Gao X, Feng S, Xiao Y. High levels of HIST1H2BK in low-grade glioma predicts poor prognosis: a study using CGGA and TCGA data. Front Oncol. 2020;10:627.PubMedPubMedCentralCrossRef Liu W, Xu Z, Zhou J, Xing S, Li Z, Gao X, Feng S, Xiao Y. High levels of HIST1H2BK in low-grade glioma predicts poor prognosis: a study using CGGA and TCGA data. Front Oncol. 2020;10:627.PubMedPubMedCentralCrossRef
14.
go back to reference Sokratous G, Polyzoidis S, Ashkan K. Immune infiltration of tumor microenvironment following immunotherapy for glioblastoma multiforme. Hum Vaccin Immunother. 2017;13(11):2575–82.PubMedPubMedCentralCrossRef Sokratous G, Polyzoidis S, Ashkan K. Immune infiltration of tumor microenvironment following immunotherapy for glioblastoma multiforme. Hum Vaccin Immunother. 2017;13(11):2575–82.PubMedPubMedCentralCrossRef
15.
go back to reference Ruan S, Xie R, Qin L, Yu M, Xiao W, Hu C, Yu W, Qian Z, Ouyang L, He Q, et al. Aggregable nanoparticles-enabled chemotherapy and autophagy inhibition combined with Anti-PD-L1 antibody for improved glioma treatment. Nano Lett. 2019;19(11):8318–32.PubMedCrossRef Ruan S, Xie R, Qin L, Yu M, Xiao W, Hu C, Yu W, Qian Z, Ouyang L, He Q, et al. Aggregable nanoparticles-enabled chemotherapy and autophagy inhibition combined with Anti-PD-L1 antibody for improved glioma treatment. Nano Lett. 2019;19(11):8318–32.PubMedCrossRef
16.
go back to reference Chen RQ, Liu F, Qiu XY, Chen XQ. The Prognostic and Therapeutic Value of PD-L1 in Glioma. Front Pharmacol. 2018;9:1503.PubMedCrossRef Chen RQ, Liu F, Qiu XY, Chen XQ. The Prognostic and Therapeutic Value of PD-L1 in Glioma. Front Pharmacol. 2018;9:1503.PubMedCrossRef
17.
go back to reference Palma L, Di Lorenzo N, Guidetti B. Lymphocytic infiltrates in primary glioblastomas and recidivous gliomas. Incidence, fate, and relevance to prognosis in 228 operated cases. J Neurosurg. 1978;49(6):854–61.PubMedCrossRef Palma L, Di Lorenzo N, Guidetti B. Lymphocytic infiltrates in primary glioblastomas and recidivous gliomas. Incidence, fate, and relevance to prognosis in 228 operated cases. J Neurosurg. 1978;49(6):854–61.PubMedCrossRef
18.
go back to reference Scherl-Mostageer M, Sommergruber W, Abseher R, Hauptmann R, Ambros P, Schweifer N. Identification of a novel gene, CDCP1, overexpressed in human colorectal cancer. Oncogene. 2001;20(32):4402–8.PubMedCrossRef Scherl-Mostageer M, Sommergruber W, Abseher R, Hauptmann R, Ambros P, Schweifer N. Identification of a novel gene, CDCP1, overexpressed in human colorectal cancer. Oncogene. 2001;20(32):4402–8.PubMedCrossRef
19.
go back to reference Lin CY, Chen HJ, Huang CC, Lai LC, Lu TP, Tseng GC, Kuo TT, Kuok QY, Hsu JL, Sung SY, et al. ADAM9 promotes lung cancer metastases to brain by a plasminogen activator-based pathway. Cancer Res. 2014;74(18):5229–43.PubMedCrossRef Lin CY, Chen HJ, Huang CC, Lai LC, Lu TP, Tseng GC, Kuo TT, Kuok QY, Hsu JL, Sung SY, et al. ADAM9 promotes lung cancer metastases to brain by a plasminogen activator-based pathway. Cancer Res. 2014;74(18):5229–43.PubMedCrossRef
20.
go back to reference Uekita T, Jia L, Narisawa-Saito M, Yokota J, Kiyono T, Sakai R. CUB domain-containing protein 1 is a novel regulator of anoikis resistance in lung adenocarcinoma. Mol Cell Biol. 2007;27(21):7649–60.PubMedPubMedCentralCrossRef Uekita T, Jia L, Narisawa-Saito M, Yokota J, Kiyono T, Sakai R. CUB domain-containing protein 1 is a novel regulator of anoikis resistance in lung adenocarcinoma. Mol Cell Biol. 2007;27(21):7649–60.PubMedPubMedCentralCrossRef
21.
go back to reference Casar B, Rimann I, Kato H, Shattil SJ, Quigley JP, Deryugina EI. In vivo cleaved CDCP1 promotes early tumor dissemination via complexing with activated beta1 integrin and induction of FAK/PI3K/Akt motility signaling. Oncogene. 2014;33(2):255–68.PubMedCrossRef Casar B, Rimann I, Kato H, Shattil SJ, Quigley JP, Deryugina EI. In vivo cleaved CDCP1 promotes early tumor dissemination via complexing with activated beta1 integrin and induction of FAK/PI3K/Akt motility signaling. Oncogene. 2014;33(2):255–68.PubMedCrossRef
22.
go back to reference Casar B, He Y, Iconomou M, Hooper JD, Quigley JP, Deryugina EI. Blocking of CDCP1 cleavage in vivo prevents Akt-dependent survival and inhibits metastatic colonization through PARP1-mediated apoptosis of cancer cells. Oncogene. 2012;31(35):3924–38.PubMedCrossRef Casar B, He Y, Iconomou M, Hooper JD, Quigley JP, Deryugina EI. Blocking of CDCP1 cleavage in vivo prevents Akt-dependent survival and inhibits metastatic colonization through PARP1-mediated apoptosis of cancer cells. Oncogene. 2012;31(35):3924–38.PubMedCrossRef
23.
go back to reference Alajati A, Guccini I, Pinton S, Garcia-Escudero R, Bernasocchi T, Sarti M, Montani E, Rinaldi A, Montemurro F, Catapano C, et al. Interaction of CDCP1 with HER2 enhances HER2-driven tumorigenesis and promotes trastuzumab resistance in breast cancer. Cell Rep. 2015;11(4):564–76.PubMedCrossRef Alajati A, Guccini I, Pinton S, Garcia-Escudero R, Bernasocchi T, Sarti M, Montani E, Rinaldi A, Montemurro F, Catapano C, et al. Interaction of CDCP1 with HER2 enhances HER2-driven tumorigenesis and promotes trastuzumab resistance in breast cancer. Cell Rep. 2015;11(4):564–76.PubMedCrossRef
24.
go back to reference Wright HJ, Hou J, Xu B, Cortez M, Potma EO, Tromberg BJ, Razorenova OV. CDCP1 drives triple-negative breast cancer metastasis through reduction of lipid-droplet abundance and stimulation of fatty acid oxidation. Proc Natl Acad Sci U S A. 2017;114(32):E6556–65.PubMedPubMedCentral Wright HJ, Hou J, Xu B, Cortez M, Potma EO, Tromberg BJ, Razorenova OV. CDCP1 drives triple-negative breast cancer metastasis through reduction of lipid-droplet abundance and stimulation of fatty acid oxidation. Proc Natl Acad Sci U S A. 2017;114(32):E6556–65.PubMedPubMedCentral
25.
go back to reference He Y, Wu AC, Harrington BS, Davies CM, Wallace SJ, Adams MN, Palmer JS, Roche DK, Hollier BG, Westbrook TF, et al. Elevated CDCP1 predicts poor patient outcome and mediates ovarian clear cell carcinoma by promoting tumor spheroid formation, cell migration and chemoresistance. Oncogene. 2016;35(4):468–78.PubMedCrossRef He Y, Wu AC, Harrington BS, Davies CM, Wallace SJ, Adams MN, Palmer JS, Roche DK, Hollier BG, Westbrook TF, et al. Elevated CDCP1 predicts poor patient outcome and mediates ovarian clear cell carcinoma by promoting tumor spheroid formation, cell migration and chemoresistance. Oncogene. 2016;35(4):468–78.PubMedCrossRef
26.
go back to reference Harrington BS, He Y, Davies CM, Wallace SJ, Adams MN, Beaven EA, Roche DK, Kennedy C, Chetty NP, Crandon AJ, et al. Cell line and patient-derived xenograft models reveal elevated CDCP1 as a target in high-grade serous ovarian cancer. Br J Cancer. 2016;114(4):417–26.PubMedPubMedCentralCrossRef Harrington BS, He Y, Davies CM, Wallace SJ, Adams MN, Beaven EA, Roche DK, Kennedy C, Chetty NP, Crandon AJ, et al. Cell line and patient-derived xenograft models reveal elevated CDCP1 as a target in high-grade serous ovarian cancer. Br J Cancer. 2016;114(4):417–26.PubMedPubMedCentralCrossRef
27.
go back to reference Dong Y, He Y, de Boer L, Stack MS, Lumley JW, Clements JA, Hooper JD. The cell surface glycoprotein CUB domain-containing protein 1 (CDCP1) contributes to epidermal growth factor receptor-mediated cell migration. J Biol Chem. 2012;287(13):9792–803.PubMedPubMedCentralCrossRef Dong Y, He Y, de Boer L, Stack MS, Lumley JW, Clements JA, Hooper JD. The cell surface glycoprotein CUB domain-containing protein 1 (CDCP1) contributes to epidermal growth factor receptor-mediated cell migration. J Biol Chem. 2012;287(13):9792–803.PubMedPubMedCentralCrossRef
28.
go back to reference Benes CH, Wu N, Elia AE, Dharia T, Cantley LC, Soltoff SP. The C2 domain of PKCdelta is a phosphotyrosine binding domain. Cell. 2005;121(2):271–80.PubMedCrossRef Benes CH, Wu N, Elia AE, Dharia T, Cantley LC, Soltoff SP. The C2 domain of PKCdelta is a phosphotyrosine binding domain. Cell. 2005;121(2):271–80.PubMedCrossRef
29.
go back to reference Wortmann A, He Y, Christensen ME, Linn M, Lumley JW, Pollock PM, Waterhouse NJ, Hooper JD. Cellular settings mediating Src Substrate switching between focal adhesion kinase tyrosine 861 and CUB-domain-containing protein 1 (CDCP1) tyrosine 734. J Biol Chem. 2011;286(49):42303–15.PubMedPubMedCentralCrossRef Wortmann A, He Y, Christensen ME, Linn M, Lumley JW, Pollock PM, Waterhouse NJ, Hooper JD. Cellular settings mediating Src Substrate switching between focal adhesion kinase tyrosine 861 and CUB-domain-containing protein 1 (CDCP1) tyrosine 734. J Biol Chem. 2011;286(49):42303–15.PubMedPubMedCentralCrossRef
30.
go back to reference Varghese RT, Liang Y, Guan T, Franck CT, Kelly DF, Sheng Z. Survival kinase genes present prognostic significance in glioblastoma. Oncotarget. 2016;7(15):20140–51.PubMedPubMedCentralCrossRef Varghese RT, Liang Y, Guan T, Franck CT, Kelly DF, Sheng Z. Survival kinase genes present prognostic significance in glioblastoma. Oncotarget. 2016;7(15):20140–51.PubMedPubMedCentralCrossRef
31.
go back to reference Geng F, Lu GF, Luo YJ, Dominguez S, Kong DY, Shen LH, Luo XM, Yang X, Hu M, Lai WS, et al. The emerging role of the MiR-1272-ADAM9-CDCP1 signaling pathway in the progression of glioma. Aging (Albany NY). 2020;13(1):894–909.CrossRef Geng F, Lu GF, Luo YJ, Dominguez S, Kong DY, Shen LH, Luo XM, Yang X, Hu M, Lai WS, et al. The emerging role of the MiR-1272-ADAM9-CDCP1 signaling pathway in the progression of glioma. Aging (Albany NY). 2020;13(1):894–909.CrossRef
33.
go back to reference Tang Z, Li C, Kang B, Gao G, Li C, Zhang Z. GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res. 2017;45(W1):W98–102.PubMedPubMedCentralCrossRef Tang Z, Li C, Kang B, Gao G, Li C, Zhang Z. GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res. 2017;45(W1):W98–102.PubMedPubMedCentralCrossRef
34.
go back to reference Liu YQ, Chai RC, Wang YZ, Wang Z, Liu X, Wu F, Jiang T. Amino acid metabolism-related gene expression-based risk signature can better predict overall survival for glioma. Cancer Sci. 2019;110(1):321–33.PubMedCrossRef Liu YQ, Chai RC, Wang YZ, Wang Z, Liu X, Wu F, Jiang T. Amino acid metabolism-related gene expression-based risk signature can better predict overall survival for glioma. Cancer Sci. 2019;110(1):321–33.PubMedCrossRef
37.
go back to reference Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47(D1):D607–13.PubMedCrossRef Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47(D1):D607–13.PubMedCrossRef
38.
go back to reference Wang L, Li Z, Song X, Liu L, Su G, Cui Y. Bioinformatic analysis of genes and MicroRNAs associated with atrioventricular septal defect in down syndrome patients. Int Heart J. 2016;57(4):490–5.PubMedCrossRef Wang L, Li Z, Song X, Liu L, Su G, Cui Y. Bioinformatic analysis of genes and MicroRNAs associated with atrioventricular septal defect in down syndrome patients. Int Heart J. 2016;57(4):490–5.PubMedCrossRef
39.
go back to reference Kohl M, Wiese S, Warscheid B. Cytoscape: software for visualization and analysis of biological networks. Methods Mol Biol. 2011;696:291–303.PubMedCrossRef Kohl M, Wiese S, Warscheid B. Cytoscape: software for visualization and analysis of biological networks. Methods Mol Biol. 2011;696:291–303.PubMedCrossRef
40.
41.
go back to reference Tang Y, Li M, Wang J, Pan Y, Wu FX. CytoNCA: a cytoscape plugin for centrality analysis and evaluation of protein interaction networks. Biosystems. 2015;127:67–72.PubMedCrossRef Tang Y, Li M, Wang J, Pan Y, Wu FX. CytoNCA: a cytoscape plugin for centrality analysis and evaluation of protein interaction networks. Biosystems. 2015;127:67–72.PubMedCrossRef
42.
go back to reference Luo X, Guo L, Dai XJ, Wang Q, Zhu W, Miao X, Gong H. Abnormal intrinsic functional hubs in alcohol dependence: evidence from a voxelwise degree centrality analysis. Neuropsychiatr Dis Treat. 2017;13:2011–20.PubMedPubMedCentralCrossRef Luo X, Guo L, Dai XJ, Wang Q, Zhu W, Miao X, Gong H. Abnormal intrinsic functional hubs in alcohol dependence: evidence from a voxelwise degree centrality analysis. Neuropsychiatr Dis Treat. 2017;13:2011–20.PubMedPubMedCentralCrossRef
43.
44.
go back to reference Peyvandi AA, Okhovatian F, Rezaei Tavirani M, ZamanianAzodi M, Rezaei Tavirani M. Protein interaction mapping related to becker muscular dystrophy. Iran J Child Neurol. 2019;13(2):125–34.PubMedPubMedCentral Peyvandi AA, Okhovatian F, Rezaei Tavirani M, ZamanianAzodi M, Rezaei Tavirani M. Protein interaction mapping related to becker muscular dystrophy. Iran J Child Neurol. 2019;13(2):125–34.PubMedPubMedCentral
45.
go back to reference Lv J, Zhu YX, Liu YQ, Xue X. Distinctive pathways characterize A. actinomycetemcomitans and P. gingivalis. Mol Biol Rep. 2015;42(2):441–9.PubMedCrossRef Lv J, Zhu YX, Liu YQ, Xue X. Distinctive pathways characterize A. actinomycetemcomitans and P. gingivalis. Mol Biol Rep. 2015;42(2):441–9.PubMedCrossRef
46.
go back to reference Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, Hoang CD, Diehn M, Alizadeh AA. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015;12(5):453–7.PubMedPubMedCentralCrossRef Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, Hoang CD, Diehn M, Alizadeh AA. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015;12(5):453–7.PubMedPubMedCentralCrossRef
47.
go back to reference Yi GZ, Huang G, Guo M, Zhang X, Wang H, Deng S, Li Y, Xiang W, Chen Z, Pan J, et al. Acquired temozolomide resistance in MGMT-deficient glioblastoma cells is associated with regulation of DNA repair by DHC2. Brain. 2019;142(8):2352–66.PubMedPubMedCentralCrossRef Yi GZ, Huang G, Guo M, Zhang X, Wang H, Deng S, Li Y, Xiang W, Chen Z, Pan J, et al. Acquired temozolomide resistance in MGMT-deficient glioblastoma cells is associated with regulation of DNA repair by DHC2. Brain. 2019;142(8):2352–66.PubMedPubMedCentralCrossRef
48.
go back to reference Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002;2(6):442–54.PubMedCrossRef Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002;2(6):442–54.PubMedCrossRef
49.
go back to reference Yoshida T, Matsuda Y, Naito Z, Ishiwata T. CD44 in human glioma correlates with histopathological grade and cell migration. Pathol Int. 2012;62(7):463–70.PubMedCrossRef Yoshida T, Matsuda Y, Naito Z, Ishiwata T. CD44 in human glioma correlates with histopathological grade and cell migration. Pathol Int. 2012;62(7):463–70.PubMedCrossRef
50.
go back to reference Shan Q, Li S, Cao Q, Yue C, Niu M, Chen X, Shi L, Li H, Gao S, Liang J, et al. Inhibition of chromosomal region maintenance 1 suppresses the migration and invasion of glioma cells via inactivation of the STAT3/MMP2 signaling pathway. Korean J Physiol Pharmacol. 2020;24(3):193–201.PubMedPubMedCentralCrossRef Shan Q, Li S, Cao Q, Yue C, Niu M, Chen X, Shi L, Li H, Gao S, Liang J, et al. Inhibition of chromosomal region maintenance 1 suppresses the migration and invasion of glioma cells via inactivation of the STAT3/MMP2 signaling pathway. Korean J Physiol Pharmacol. 2020;24(3):193–201.PubMedPubMedCentralCrossRef
51.
go back to reference Michaud-Levesque J, Bousquet-Gagnon N, Beliveau R. Quercetin abrogates IL-6/STAT3 signaling and inhibits glioblastoma cell line growth and migration. Exp Cell Res. 2012;318(8):925–35.PubMedCrossRef Michaud-Levesque J, Bousquet-Gagnon N, Beliveau R. Quercetin abrogates IL-6/STAT3 signaling and inhibits glioblastoma cell line growth and migration. Exp Cell Res. 2012;318(8):925–35.PubMedCrossRef
52.
go back to reference Wang F, Zhang P, Yang L, Yu X, Ye X, Yang J, Qian C, Zhang X, Cui YH, Bian XW. Activation of toll-like receptor 2 promotes invasion by upregulating MMPs in glioma stem cells. Am J Transl Res. 2015;7(3):607–15.PubMedPubMedCentral Wang F, Zhang P, Yang L, Yu X, Ye X, Yang J, Qian C, Zhang X, Cui YH, Bian XW. Activation of toll-like receptor 2 promotes invasion by upregulating MMPs in glioma stem cells. Am J Transl Res. 2015;7(3):607–15.PubMedPubMedCentral
53.
go back to reference Chen D, Li D, Xu X-B, Qiu S, Luo S, Qiu E, Rong Z, Zhang J, Zheng D. Galangin inhibits epithelial-mesenchymal transition and angiogenesis by downregulating CD44 in glioma. J Cancer. 2019;10(19):4499–508.PubMedPubMedCentralCrossRef Chen D, Li D, Xu X-B, Qiu S, Luo S, Qiu E, Rong Z, Zhang J, Zheng D. Galangin inhibits epithelial-mesenchymal transition and angiogenesis by downregulating CD44 in glioma. J Cancer. 2019;10(19):4499–508.PubMedPubMedCentralCrossRef
54.
go back to reference Anido J, Saez-Borderias A, Gonzalez-Junca A, Rodon L, Folch G, Carmona MA, Prieto-Sanchez RM, Barba I, Martinez-Saez E, Prudkin L, et al. TGF-beta receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell. 2010;18(6):655–68.PubMedCrossRef Anido J, Saez-Borderias A, Gonzalez-Junca A, Rodon L, Folch G, Carmona MA, Prieto-Sanchez RM, Barba I, Martinez-Saez E, Prudkin L, et al. TGF-beta receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell. 2010;18(6):655–68.PubMedCrossRef
55.
go back to reference Merzak A, Koocheckpour S, Pilkington GJCR. CD44 mediates human glioma cell adhesion and invasion in vitro. Cancer Res. 1994;54(15):3988–92.PubMed Merzak A, Koocheckpour S, Pilkington GJCR. CD44 mediates human glioma cell adhesion and invasion in vitro. Cancer Res. 1994;54(15):3988–92.PubMed
56.
go back to reference Parney IF, Waldron JS, Parsa AT. Flow cytometry and in vitro analysis of human glioma-associated macrophages. Laboratory investigation. J Neurosurg. 2009;110(3):572–82.PubMedPubMedCentralCrossRef Parney IF, Waldron JS, Parsa AT. Flow cytometry and in vitro analysis of human glioma-associated macrophages. Laboratory investigation. J Neurosurg. 2009;110(3):572–82.PubMedPubMedCentralCrossRef
57.
go back to reference Harrington B, Davies CM, Wallace SJ, He Y, Hooper JD: Targeting the Cell Surface Protein Cdcp1 in a Model of Advanced Ovarian Cancer. In: International Journal of Gynecological Cancer. 2014; 2014. Harrington B, Davies CM, Wallace SJ, He Y, Hooper JD: Targeting the Cell Surface Protein Cdcp1 in a Model of Advanced Ovarian Cancer. In: International Journal of Gynecological Cancer. 2014; 2014.
58.
go back to reference Wright HJ, Arulmoli J, Motazedi M, Nelson LJ, Heinemann FS, Flanagan LA, Razorenova OV. CDCP1 cleavage is necessary for homodimerization-induced migration of triple-negative breast cancer. Oncogene. 2016;35(36):4762–72.PubMedPubMedCentralCrossRef Wright HJ, Arulmoli J, Motazedi M, Nelson LJ, Heinemann FS, Flanagan LA, Razorenova OV. CDCP1 cleavage is necessary for homodimerization-induced migration of triple-negative breast cancer. Oncogene. 2016;35(36):4762–72.PubMedPubMedCentralCrossRef
59.
go back to reference Huang L, Chen Y, Lai S, Guan H, Hu X, Liu J, Zhang H, Zhang Z, Zhou J. CUB domain-containing protein-1 promotes proliferation, migration and invasion in cervical cancer cells. Cancer Manag Res. 2020;12:3759–69.PubMedPubMedCentralCrossRef Huang L, Chen Y, Lai S, Guan H, Hu X, Liu J, Zhang H, Zhang Z, Zhou J. CUB domain-containing protein-1 promotes proliferation, migration and invasion in cervical cancer cells. Cancer Manag Res. 2020;12:3759–69.PubMedPubMedCentralCrossRef
Metadata
Title
Molecular mechanism by which CDCP1 promotes proneural-mesenchymal transformation in primary glioblastoma
Authors
Zhiying Lin
Zhu Zhang
Haojie Zheng
Haiyan Xu
Yajuan Wang
Chao Chen
Junlu Liu
Guozhong Yi
Zhiyong Li
Xiaoyan Wang
Guanglong Huang
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2022
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-021-02373-1

Other articles of this Issue 1/2022

Cancer Cell International 1/2022 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine