MCPIP1 expression positively correlates with melanoma-specific survival of patients, and its overexpression affects vital intracellular pathways of human melanoma cells.
Akt/mTOR
MCPIP1
cell cycle
melanoma
tumor suppressor
Journal
Molecular carcinogenesis
ISSN: 1098-2744
Titre abrégé: Mol Carcinog
Pays: United States
ID NLM: 8811105
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
received:
06
10
2020
revised:
18
01
2021
accepted:
19
01
2021
pubmed:
6
2
2021
medline:
27
4
2021
entrez:
5
2
2021
Statut:
ppublish
Résumé
The suppressive activity of monocyte chemoattractant protein 1-induced protein 1 (MCPIP1) an inflammation-related ribonuclease, has been described in a few cancer types but has yet to be assessed in the most common subtype of skin cancer: melanoma. Here, we have evaluated the MCPIP1 expression in melanoma tissues by reanalysis of publicly available transcriptome data from 89 melanoma samples, and immunohistochemical staining of 21 primary and 81 metastatic melanomas. Our data implicated decreased MCPIP1 expression in melanoma tumors compared to normal tissues, and positive correlation between high ribonuclease expression and melanoma-specific survival of patients. To investigate the ribonuclease activity in melanoma cells, MCPIP1 was ectopically expressed in the MV3 human melanoma cell line. Following the transcriptome, proteome, and intracellular signaling of MCPIP1-overexpressing MV3 cells was assessed via real-time quantitative polymerase chain reaction, Western blot analysis, and RNAseq. MV3 cells overexpressing MCPIP1 exhibited a broad range of alterations in the transcriptome and proteome, as well as in the phosphorylation status of a number of proteins, strongly indicating MCPIP1-dependent cell cycle arrest and inhibition of Akt/mTOR signaling in these cells. Moreover, we have shown, that MCPIP1 overexpression downregulates miRNA-193a-3p expression in MV3 cells. Furthermore, the majority of the described effects were dependent on the ribonucleolytic activity of the protein. The presented body of data strongly suggests a potential tumor suppressor role and possible future application as a positive prognostic marker of MCPIP1 protein in melanoma.
Substances chimiques
MIRN193 microRNA, human
0
MicroRNAs
0
Transcription Factors
0
Ribonucleases
EC 3.1.-
ZC3H12A protein, human
EC 3.1.-
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
227-241Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Shain AH, Bastian BC. From melanocytes to melanomas. Nat Rev Cancer. 2016;16(6):345-358.
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69(1):7-34.
Griewank KG. Biomarkers in melanoma. Scand J Clin Lab Invest Suppl. 2016;245:S104-S112.
Liang J, Wang J, Azfer A, et al. A novel CCCH-zinc finger protein family regulates proinflammatory activation of macrophages. J Biol Chem. 2008;283(10):6337-6346.
Lu W, Ning H, Gu L, et al. MCPIP1 selectively destabilizes transcripts associated with an antiapoptotic gene expression program in breast cancer cells that can elicit complete tumor regression. Cancer Res. 2016;76(6):1429-1440.
Marona P, Górka J, Mazurek Z, et al. MCPIP1 downregulation in clear cell renal cell carcinoma promotes vascularization and metastatic progression. Cancer Res. 2017;77(18):4905-4920.
Boratyn E, Nowak I, Horwacik I, et al. Monocyte chemoattractant protein-induced protein 1 overexpression modulates transcriptome, including microRNA, in human neuroblastoma cells. J Cell Biochem. 2016;117(3):694-707.
Boratyn E, Nowak I, Durbas M, Horwacik I, Sawicka A, Rokita H. MCPIP1 exogenous overexpression inhibits pathways regulating MYCN oncoprotein stability in neuroblastoma. J Cell Biochem. 2017;118(7):1741-1755.
Boratyn E, Nowak I, Karnas E, et al. MCPIP1 overexpression in human neuroblastoma cell lines causes cell-cycle arrest by G1/S checkpoint block. J Cell Biochem. 2020;121(5-6):3406-3425.
Ren Z, He M, Shen T, et al. MiR-421 promotes the development of osteosarcoma by regulating MCPIP1 expression. Cancer Biol Ther. 2020;21(3):231-240.
Talantov D, Mazumder A, Yu JX, et al. Novel genes associated with malignant melanoma but not benign melanocytic lesions. Clin Cancer Res. 2005;11(20):7234-7242.
Hoek K, Rimm DL, Williams KR, et al. Expression profiling reveals novel pathways in the transformation of melanocytes to melanomas. Cancer Res. 2004;64(15):5270-5282.
Gangemi R, Mirisola V, Barisione G, et al. Mda-9/syntenin is expressed in uveal melanoma and correlates with metastatic progression. PLOS One. 2012;7(1):e29989.
Smith AP, Hoek K, Becker D. Whole-genome expression profiling of the melanoma progression pathway reveals marked molecular differences between nevi/melanoma in situ and advanced-stage melanomas. Cancer Biol Ther. 2005;4(9):1018-1029.
Brozyna AA, Jozwicki W, Jetten AM, Slominski AT. On the relationship between VDR, RORalpha and RORgamma receptors expression and HIF1-alpha levels in human melanomas. Exp Dermatol. 2019;28(9):1036-1043.
Lipert B, Wilamowski M, Gorecki A, Jura J. MCPIP1, alias Regnase-1 binds and cleaves mRNA of C/EBPbeta. PLOS One. 2017;12(3):e0174381.
Bugara B, Konieczny P, Wolnicka-Glubisz A, et al. MCPIP1 contributes to the inflammatory response of UVB-treated keratinocytes. J Dermatol Sci. 2017;87(1):10-18.
Wang J, Wang H, Li Z, et al. c-Myc is required for maintenance of glioma cancer stem cells. PLOS One. 2008;3(11):e3769.
Durbas M, Horwacik I, Boratyn E, Kamycka E, Rokita H. GD2 ganglioside specific antibody treatment downregulates PI3K/Akt/mTOR signaling network in human neuroblastoma cell lines. Int J Oncol. 2015;47(3):1143-1159.
Kasugai Y, Tagawa H, Kameoka Y, Morishima Y, Nakamura S, Seto M. Identification of CCND3 and BYSL as candidate targets for the 6p21 amplification in diffuse large B-cell lymphoma. Clin Cancer Res. 2005;11(23):8265-8272.
Naetar N, Soundarapandian V, Litovchick L, et al. PP2A-mediated regulation of Ras signaling in G2 is essential for stable quiescence and normal G1 length. Mol Cell. 2014;54(6):932-945.
Bednarek K, Kiwerska K, Szaumkessel M, et al. Recurrent CDK1 overexpression in laryngeal squamous cell carcinoma. Tumour Biol. 2016;37(8):11115-11126.
Kaur M, Khan MM, Kar A, Sharma A, Saxena S. CRL4-DDB1-VPRBP ubiquitin ligase mediates the stress triggered proteolysis of Mcm10. Nucleic Acids Res. 2012;40(15):7332-7346.
Dupasquier S, Delmarcelle AS, Marbaix E, Cosyns JP, Courtoy PJ, Pierreux CE. Validation of housekeeping gene and impact on normalized gene expression in clear cell renal cell carcinoma: critical reassessment of YBX3/ZONAB/CSDA expression. BMC Mol Biol. 2014;15:9.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402-408.
Smith PK, Krohn RI, Hermanson GT, et al. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985;150(1):76-85.
Horwacik I, Durbas M, Boratyn E, Wegrzyn P, Rokita H. Targeting GD2 ganglioside and aurora A kinase as a dual strategy leading to cell death in cultures of human neuroblastoma cells. Cancer Lett. 2013;341(2):248-264.
Nowak I, Boratyn E, Durbas M, Horwacik I, Rokita H. Exogenous expression of miRNA-3613-3p causes APAF1 downregulation and affects several proteins involved in apoptosis in BE(2)-C human neuroblastoma cells. Int J Oncol. 2018;53(4):1787-1799.
Nowak I, Boratyn E, Student S, et al. MCPIP1 ribonuclease can bind and cleave AURKA mRNA in MYCN-amplified neuroblastoma cells. RNA Biol. 2021;18(1):144-156.
Mino T, Murakawa Y, Fukao A, et al. Regnase-1 and roquin regulate a common element in inflammatory mRNAs by spatiotemporally distinct mechanisms. Cell. 2015;161(5):1058-1073.
Kraehn GM, Utikal J, Udart M, et al. Extra c-myc oncogene copies in high risk cutaneous malignant melanoma and melanoma metastases. Br J Cancer. 2001;84(1):72-79.
Otto T, Horn S, Brockmann M, et al. Stabilization of N-Myc is a critical function of Aurora A in human neuroblastoma. Cancer Cell. 2009;15(1):67-78.
Yan M, Wang C, He B, et al. Aurora-A kinase: a potent oncogene and target for cancer therapy. Med Res Rev. 2016;36(6):1036-1079.
Nave BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR. Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J. 1999;344(Pt 2):427-431.
Dufner A, Thomas G. Ribosomal S6 kinase signaling and the control of translation. Exp Cell Res. 1999;253(1):100-109.
Polivka J, Jr., Janku F. Molecular targets for cancer therapy in the PI3K/AKT/mTOR pathway. Pharmacol Ther. 2014;142(2):164-175.
Yang Z, Yuan XG, Chen J, Luo SW, Luo ZJ, Lu NH. Reduced expression of PTEN and increased PTEN phosphorylation at residue Ser380 in gastric cancer tissues: a novel mechanism of PTEN inactivation. Clin Res Hepatol Gastroenterol. 2013;37(1):72-79.
Robertson BW, Bonsal L, Chellaiah MA. Regulation of Erk1/2 activation by osteopontin in PC3 human prostate cancer cells. Mol Cancer. 2010;9:260.
Skalniak A, Boratyn E, Tyrkalska SD, et al. Expression of the monocyte chemotactic protein-1-induced protein 1 decreases human neuroblastoma cell survival. Oncol Rep. 2014;31(5):2385-2392.
Bottazzi B, Walter S, Govoni D, Colotta F, Mantovani A. Monocyte chemotactic cytokine gene transfer modulates macrophage infiltration, growth, and susceptibility to IL-2 therapy of a murine melanoma. J Immunol. 1992;148(4):1280-1285.
Lichawska-Cieslar A, Pietrzycka R, Ligeza J, et al. RNA sequencing reveals widespread transcriptome changes in a renal carcinoma cell line. Oncotarget. 2018;9(9):8597-8613.
Lu Y, Baras AS, Halushka MK. miRge 2.0 for comprehensive analysis of microRNA sequencing data. BMC Bioinformatics. 2018;19(1):275.
Vízkeleti L, Ecsedi S, Rákosy Z, et al. The role of CCND1 alterations during the progression of cutaneous malignant melanoma. Tumour Biol. 2012;33(6):2189-2199.
Florenes VA, Faye RS, Maelandsmo GM, Nesland JM, Holm R. Levels of cyclin D1 and D3 in malignant melanoma: deregulated cyclin D3 expression is associated with poor clinical outcome in superficial melanoma. Clin Cancer Res. 2000;6(9):3614-3620.
Ravindran Menon D, Luo Y, Arcaroli JJ, et al. CDK1 interacts with Sox2 and promotes tumor initiation in human melanoma. Cancer Res. 2018;78(23):6561-6574.
Mamane Y, Petroulakis E, Martineau Y, et al. Epigenetic activation of a subset of mRNAs by eIF4E explains its effects on cell proliferation. PLOS One. 2007;2(2):e242.
Avdulov S, Li S, Van Michalek M, et al. Activation of translation complex eIF4F is essential for the genesis and maintenance of the malignant phenotype in human mammary epithelial cells. Cancer Cell. 2004;5(6):553-563.
Müller D, Lasfargues C, El Khawand S, et al. 4E-BP restrains eIF4E phosphorylation. Translation (Austin). 2013;1(2):e25819.