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Distinct expression and function of breast cancer metastasis suppressor 1 in mutant P53 glioblastoma

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Abstract

Purpose

Glioblastoma (GBM) is the most malignant subtype of astrocytic tumors with the worst prognosis in all its progressive forms. Breast cancer metastasis suppressor 1 (BRMS1) is a metastasis suppressor gene that controls malignancy in multiple tumors. As yet, however, its clinical and functional significance in mutant P53 GBM remains inconclusive. Here, we attempted to study the importance of BRMS1 in mutant P53 GBM.

Methods

BRMS1 expression was evaluated in 74 human astrocytoma tissues by qRT-PCR, Western blotting and immunohistochemistry. BRMS1 expression in the astrocytoma tissues was correlated with clinicopathological parameters, the P53 mutation status and BRMS1 downstream targets, and compared with TCGA and NCI-60 datasets. siRNA-mediated knockdown of BRMS1 was performed in selected GBM cell lines to evaluate the functional role of BRMS1.

Results

Our study revealed an enhanced expression of BRMS1 in GBM which was associated with a poor patient survival, and this observation was corroborated by the TCGA dataset. We also found a positive correlation between BRMS1 expression and a mutant P53 status in GBM which was associated with a poor prognosis. In vitro BRMS1 silencing reduced the growth of mutant P53 GBM cells and repressed their colonization and migration/invasion by modulating EGFR-AKT/NF-κB signaling. Transcriptional profiling revealed a positive and negative correlation of uPA and ING4 expression with BRMS1 expression, respectively.

Conclusion

Our data indicate upregulation of BRMS1 in high grade astrocytomas which correlates positively with mutant P53 and a poor patient survival. Silencing of BRMS1 in mutant P53 GBM cell lines resulted in a reduced cellular growth and migration/invasion by suppressing the EGFR-AKT/NF-kB signaling pathway. BRMS1 may serve as a predictive biomarker and therapeutic target in mutant P53 GBM.

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Data availability

All data generated or analyzed during this study are included in the manuscript or its supplementary files, and if more is needed, it shall be made available by the authors upon reasonable request.

Abbreviations

GBM:

Glioblastoma

 BRMS1 :

Breast cancer metastasis suppressor 1

wt/mut P53:

wild/mutant P53

MSG:

Metastasis suppressor gene

UPA :

Urokinase plasminogen activator

ING4 :

Inhibitor of growth family-4

EGFR :

Epidermal growth factor receptor

siRNA:

Small interfering RNA

NT-siRNA:

Non-targeting-small interfering RNA

qPCR:

Quantitative polymerase chain reaction

IHC:

Immunohistochemistry

TCGA:

The Cancer Genome Atlas

CPTAC:

Clinical Proteomic Tumor Analysis Consortium

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Acknowledgements

The authors thank Dr. Chandra Sekhar from the Krishna Institute of Medical Sciences, India, for helping in the clinicopathological assessments. We also acknowledge all members of the PPB laboratory, especially Dr. Anwita Mudiraj and Dr. Ravindra Pramod Deshpande for their valuable contributions to the manuscript.

Funding

We acknowledge the financial assistance to the Lab from the Ministry of Science and Technology, Department of Science and Technology, Govt. of India, DST- SERB Core grant, file No. SR/CSRI/196/2016, and CRG/2020/005021, Department of Biotechnology, Govt. of India, BT/PR18168/MED/29/1064/2016, BT/PR17686/MED/30/1664/2016, and financial support to the University of Hyderabad-IoE by the Ministry of Education, Govt. of India F11/9/2019-U3 (A), and DST-FIST, and UGC-SAP for the department. D.B. acknowledges the Department of Biotechnology (DBT) India for the student fellowship (Award no: DBT/2013/UOH/79).

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  1. Neuroscience Laboratory, Department of Biotechnology and Bioinformatics, School of Life Sciences, University of Hyderabad, Room No: F-23/F-71, Hyderabad, Telangana State, 500 046, India

    Deepak Babu, Ramulu Chintal & Prakash Babu Phanithi

  2. Department of Neurosurgery, Krishna Institute of Medical Sciences, 500 003, Secunderabad, Telangana State, India

    Manas Panigrahi

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DB and PPB designed the study. DB and CR performed the experiments. DB and MP collected the tumor samples and the related clinical information. DB, CR, MP and PPB analyzed the data. DB drafted the manuscript. DB and PPB finalized the manuscript. All authors read and approved the final manuscript.

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Correspondence to Prakash Babu Phanithi.

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All procedures performed in this study involving human participants were approved by the Institutional Ethics Committee (IEC), University of Hyderabad, Hyderabad (TS), India, with IEC reference number UH/IEC/2016/180. Written informed consent was obtained from all participants included in the study.

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Babu, D., Chintal, R., Panigrahi, M. et al. Distinct expression and function of breast cancer metastasis suppressor 1 in mutant P53 glioblastoma. Cell Oncol. 45, 1451–1465 (2022). https://doi.org/10.1007/s13402-022-00729-x

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