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PTPN11 Knockdown Prevents Changes in the Expression of Genes Controlling Cell Cycle, Chemotherapy Resistance, and Oncogene-Induced Senescence in Human Thyroid Cells Overexpressing BRAF V600E Oncogenic Protein

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Abstract

The MAPK (RAS/BRAF/MEK/ERK) signaling pathway is a kinase cascade involved in the regulation of cell proliferation, differentiation, and survival in response to external stimuli. The V600E mutation in the BRAF gene has been detected in various tumors, resulting in a 500-fold increase in BRAF kinase activity. However, monotherapy with selective BRAF V600E inhibitors often leads to reactivation of MAPK signaling cascade and emergence of drug resistance. Therefore, new targets are being developed for the inhibition of components of the aberrantly activated cascade. It was recently discovered that resistance to BRAF V600E inhibitors may be associated with the activity of the tyrosine phosphatase SHP-2 encoded by the PTPN11 gene. In this paper, we analyzed transcriptional effects of PTPN11 gene knockdown and selective suppression of BRAF V600E in a model of thyroid follicular epithelium. We found that the siRNA-mediated knockdown of PTPN11 after vemurafenib treatment prevented an increase in the expression CCNA1 and NOTCH4 genes involved in the formation of drug resistance of tumors. On the other hand, downregulation of PTPN11 expression blocked the transcriptional activation of genes (p21, pl5, pl6, RBI, and IGFBP7) involved in cell cycle regulation and oncogene-induced senescence in response to BRAF V600E expression. Therefore, it can be assumed that SHP-2 participates not only in emergence of drug resistance in cancer cells, but also in oncogene-induced cell senescence.

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Abbreviations

EGFR:

epidermal growth factor receptor

OIS:

oncogene-induced senescence

RT-qPCR:

reverse transcription/quantitative PCR.

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Funding

This study was supported by the Russian Foundation for Basic Research (project no. 18-315-00171 mol_a) and the Russian Science Foundation (grant no. 16-15-10423; construction of the BRAF V600E-expressing lentiviral vector and data presented in Fig. 1).

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Authors and Affiliations

  1. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991, Moscow, Russia

    L. V. Putlyaeva, D. E. Demin, A. N. Uvarova, M. M. Prokofjeva & A. M. Schwartz

  2. Center of Life Sciences, Skolkovo Institute of Science and Technology, 121205, Moscow, Russia

    L. V. Putlyaeva

  3. Moscow Institute of Physics and Technology, 141701, Dolgoprudnyi, Moscow Region, Russia

    D. E. Demin & A. M. Schwartz

  4. Faculty of Biology, Lomonosov Moscow State University, 119234, Moscow, Russia

    A. N. Uvarova

  5. Koltzov Institute of Developmental Biology, Russian Academy of Sciences, 119334, Moscow, Russia

    L. S. Zinevich

  6. Institute of Fundamental Medicine and Biology, Kazan Federal University, 420008, Kazan, Russia

    G. R. Gazizova & E. I. Shagimardanova

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  1. L. V. Putlyaeva
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  2. D. E. Demin
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  3. A. N. Uvarova
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  4. L. S. Zinevich
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  5. M. M. Prokofjeva
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  6. G. R. Gazizova
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  7. E. I. Shagimardanova
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  8. A. M. Schwartz
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Corresponding author

Correspondence to A. M. Schwartz.

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The authors declare no conflict of interest.

Compliance with ethical standards

The article does not contain description of experiments with the participation of humans or animals performed by any of the authors.

Russian Text © The Author(s), 2020, published in Biokhimiya, 2020, Vol. 85, No. 1, pp. 126–138.

Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM19-271, December 2, 2019.

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Putlyaeva, L.V., Demin, D.E., Uvarova, A.N. et al. PTPN11 Knockdown Prevents Changes in the Expression of Genes Controlling Cell Cycle, Chemotherapy Resistance, and Oncogene-Induced Senescence in Human Thyroid Cells Overexpressing BRAF V600E Oncogenic Protein. Biochemistry Moscow 85, 108–118 (2020). https://doi.org/10.1134/S0006297920010101

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  • DOI: https://doi.org/10.1134/S0006297920010101

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