Strong Activation of ID1, ID2, and ID3 Genes Is Coupled with the Formation of Vasculogenic Mimicry Phenotype in Melanoma Cells
Abstract
:1. Introduction
2. Materials and Methods
2.1. Reagents
2.2. Cell Culture
2.3. RNA Isolation and RNA-Seq Procedure
2.4. RNA-Seq Analysis
2.5. Statistical Assessment
3. Results
3.1. Transferring Melanoma Cells from a Plastic Surface to Matrigel Dramatically Changed the Expression of about 2700 Genes
3.2. Upregulated and Downregulated Genes Are Simultaneously Regulated by Many Transcription Factors
3.3. Relationship of Upregulated and Downregulated Genes with rDNA-Contacting Genes and Genes with Hot Spots of DSBs in the Human Genome
3.4. Association of lincRNAs and Active Histone Marks with Upregulation of 976 Genes in Melanoma Cells
3.5. Association of lincRNAs with Downregulated Genes
4. Discussion
4.1. Matrigel Induces an Epigenetic Switch in Melanoma Cells
4.2. Are ID1, ID2, and ID3 Genes Responsible for the Vasculogenic Phenotype of Melanoma Cells?
4.3. Distinct Mechanisms in Regulation of Genes Changing Expression in Melanoma Cells Grown on Matrigel
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
References
- Carè, A.; Del Bufalo, D.; Facchiano, A. Editorial on Special Issue “Advances and Novel Treatment Options in Metastatic Melanoma”. Cancers 2022, 14, 707. [Google Scholar] [CrossRef]
- Maniotis, A.J.; Folberg, R.; Hess, A.; Seftor, E.A.; Gardner, L.M.; Pe’er, J.; Trent, J.M.; Meltzer, P.S.; Hendrix, M.J. Vascular channel formation by human melanoma cells in vivo and in vitro: Vasculogenic mimicry. Am. J. Pathol. 1999, 155, 739–752. [Google Scholar] [CrossRef] [PubMed]
- Cao, Z.; Bao, M.; Miele, L.; Sarkar, F.H.; Wang, Z.; Zhou, Q. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: A systemic review and meta-analysis. Eur. J. Cancer 2013, 49, 3914–3923. [Google Scholar] [CrossRef] [PubMed]
- Hendrix, M.J.; Seftor, E.A.; Seftor, R.E.; Chao, J.T.; Chien, D.S.; Chu, Y.W. Tumor cell vascular mimicry: Novel targeting opportunity in melanoma. Pharmacol. Ther. 2016, 159, 83–92. [Google Scholar] [CrossRef]
- Pathan, S.; Ali, T.; Vincent, S.; Nanjappa, Y.; David, R.M.; Kumar, O.P. A Dermoscopic Inspired System for Localization and Malignancy Classification of Melanocytic Lesions. Appl. Sci. 2022, 12, 4243. [Google Scholar] [CrossRef]
- Liu, H.; Wang, H.; Chen, D.; Gu, C.; Huang, J.; Mi, K. Endoplasmic reticulum stress inhibits 3D Matrigel-induced vasculogenic mimicry of breast cancer cells via TGF-β1/Smad2/3 and β-catenin signaling. FEBS Open Bio 2021, 11, 2607–2618. [Google Scholar] [CrossRef]
- Cavalli, G.; Heard, E. Advances in epigenetics link genetics to the environment and disease. Nature 2019, 571, 489–499. [Google Scholar] [CrossRef]
- Horvath, S. DNA methylation age of human tissues and cell types. Genome Biol. 2013, 14, R115. [Google Scholar] [CrossRef]
- Bird, A. Perceptions of epigenetics. Nature 2007, 447, 396–398. [Google Scholar] [CrossRef]
- Lawrence, M.; Daujat, S.; Schneider, R. Lateral Thinking: How Histone Modifications Regulate Gene Expression. Trends Genet. 2016, 32, 42–56. [Google Scholar] [CrossRef]
- Chen, Y.A.; Aravin, A.A. Non-Coding RNAs in Transcriptional Regulation. Curr. Mol. Biol. Rep. 2015, 1, 10–18. [Google Scholar] [CrossRef] [PubMed]
- Dixon, J.; Selvaraj, S.; Yue, F.; Kim, A.; Li, Y.; Shen, Y.; Hu, M.; Liu, J.S.; Ren, B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485, 376–380. [Google Scholar] [CrossRef] [PubMed]
- Kanwal, R.; Gupta, K.; Gupta, S. Cancer epigenetics: An introduction. Methods Mol. Biol. 2015, 1238, 3–25. [Google Scholar]
- Pathak, A.; Tomar, S.; Pathak, S. Epigenetics and Cancer: A Comprehensive Review. Asian Pac. J. Cancer Biol. 2023, 8, 75–89. [Google Scholar] [CrossRef]
- Vartanian, A.; Stepanova, E.; Grigorieva, I.; Solomko, E.; Belkin, V.; Baryshnikov, A.; Lichinitser, M. Melanoma vasculogenic mimicry capillary-like structure formation depends on integrin and calcium signaling. Microcirculation 2011, 18, 390–399. [Google Scholar] [CrossRef] [PubMed]
- Ikari, R.; Mukaisho, K.I.; Kageyama, S.; Nagasawa, M.; Kubota, S.; Nakayama, T.; Murakami, S.; Taniura, N.; Tanaka, H.; Kushima, R.P.; et al. Differences in the central energy metabolism of cancer cells between conventional 2d and novel 3d culture systems. Int. J. Mol. Sci. 2021, 22, 1805. [Google Scholar] [CrossRef]
- Price, K.J.; Tsykin, A.; Giles, K.M.; Sladic, R.T.; Epis, M.R.; Ganss, R.; Goodall, G.J.; Leedman, P.J. Matrigel basement membrane matrix influences expression of microRNAs in cancer cell lines. Biochem. Biophys. Res. Commun. 2012, 427, 343–348. [Google Scholar] [CrossRef]
- Vartanian, A.A.; Khochenkova, Y.A.; Kosobokova, E.N.; Baryshnikova, M.A.; Kosorukov, V.S. CD437 Reduces Metastatic Potential of Melanoma Cells. Moscow Univ. Chem. Bull. 2021, 76, 208–214. [Google Scholar] [CrossRef]
- Vartanian, A.; Baryshnikova, M.; Burova, O.; Afanasyeva, D.; Misyurin, V.; Belyavsky, A.; Shprakh, Z. Inhibitor of vasculogenic mimicry restores sensitivity of resistant melanoma cells to DNA-damaging agents. Melanoma Res. 2017, 27, 8–16. [Google Scholar] [CrossRef]
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A flexible trimmer for illumina sequence data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef]
- Li, B.; Dewey, C.N. Rsem: Accurate transcript quantification from rna-seq data with or without a reference genome. BMC Bioinform. 2011, 12, 323. [Google Scholar] [CrossRef]
- Dobin, A.; Davis, C.A.; Schlesinger, F.; Drenkow, J.; Zaleski, C.; Jha, S.; Batut, P.; Chaisson, M.; Gingeras, T.R. STAR: Ultrafast universal RNA-Seq aligner. Bioinformatics 2013, 29, 15–21. [Google Scholar] [CrossRef] [PubMed]
- Liao, Y.; Smyth, G.K.; Shi, W. Featurecounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014, 30, 923–930. [Google Scholar] [CrossRef]
- Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef] [PubMed]
- Ramirez, F.; Ryan, D.P.; Gruning, B.; Bhardwaj, V.; Kilpert, F.; Richter, A.S.; Heyne, S.; Dundar, F.; Manke, T. deepTools2: A next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016, 44, W160–W165. [Google Scholar] [CrossRef] [PubMed]
- Wang, M.; Zhao, Y.; Zhang, B. Efficient test and visualization of multi-set intersections. Sci. Rep. 2015, 5, 16923. [Google Scholar] [CrossRef] [PubMed]
- Jögi, A.; Vaapil, M.; Johansson, M.; Påhlman, S. Cancer cell differentiation heterogeneity and aggressive behavior in solid tumors. Ups. J. Med. Sci. 2012, 117, 217–224. [Google Scholar] [CrossRef]
- Amoutzias, G.D.; Robertson, D.L.; Van de Peer, Y.; Oliver, S.G. Choose your partners: Dimerization in eukaryotic transcription factors. Trends Biochem. Sci. 2008, 33, 220–229. [Google Scholar] [CrossRef]
- Peddada, S.; Yasuil, D.H.; LaSalle, J.M. Inhibitors of differentiation (ID1, ID2, ID3 and ID4) genes are neuronal targets of MeCP2 that are elevated in Rett syndrome. Hum. Mol. Genet. 2006, 15, 2003–2014. [Google Scholar] [CrossRef]
- Qian, Y.; Chen, X. ID1, inhibitor of differentiation/DNA binding, is an effector of the p53-dependent DNA damage response pathway. J. Biol. Chem. 2008, 283, 22410–22416. [Google Scholar] [CrossRef]
- Lindström, M.S.; Jurada, D.; Bursac, S.; Orsolic, I.; Bartek, J.; Volarevic, S. Nucleolus as an emerging hub in maintenance of genome stability and cancer pathogenesis. Oncogene 2018, 37, 2351–2366. [Google Scholar] [CrossRef]
- Tchurikov, N.A.; Fedoseeva, D.M.; Klushevskaya, E.S.; Slovohotov, I.Y.; Chechetkin, V.R.; Kravatsky, Y.V.; Kretova, O.V. rDNA Clusters Make Contact with Genes that Are Involved in Differentiation and Cancer and Change Contacts after Heat Shock Treatment. Cells 2019, 8, 1393. [Google Scholar] [CrossRef]
- Ge, H.; Luo, H. Overview of advances in vasculogenic mimicry—A potential target for tumor therapy. Cancer Manag. Res. 2018, 10, 2429–2437. [Google Scholar] [CrossRef] [PubMed]
- Lachmann, A.; Torre, D.; Keenan, A.B.; Jagodnik, K.M.; Lee, H.J.; Wang, L.; Silverstein, M.C.; Ma’ayan, A. Massive mining of publicly available RNA-seq data from human and mouse. Nat. Commun. 2018, 9, 1366. [Google Scholar] [CrossRef]
- Tchurikov, N.A.; Klushevskaya, E.S.; Fedoseeva, D.M.; Alembekov, I.R.; Kravatskaya, G.I.; Chechetkin, V.R.; Kravatsky, Y.V.; Kretova, O.V. Dynamics of Whole-Genome Contacts of Nucleoli in Drosophila Cells Suggests a Role for rDNA Genes in Global Epigenetic Regulation. Cells 2020, 9, 2587. [Google Scholar] [CrossRef] [PubMed]
- Tchurikov, N.A.; Alembekov, I.R.; Klushevskaya, E.S.; Kretova, A.N.; Keremet, A.M.; Sidorova, A.E.; Meilakh, P.B.; Chechetkin, V.R.; Kravatskaya, G.I.; Kravatsky, Y.V. Genes Possessing the Most Frequent DNA DSBs Are Highly Associated with Development and Cancers, and Essentially Overlap with the rDNA-Contacting Genes. Int. J. Mol. Sci. 2022, 23, 7201. [Google Scholar] [CrossRef]
- Tchurikov, N.A.; Fedoseeva, D.M.; Sosin, D.V.; Snezhkina, A.V.; Melnikova, N.V.; Kudryavtseva, A.V.; Kravatsky, Y.V.; Kretova, O.V. Hot spots of DNA double-strand breaks and genomic contacts of human rDNA units are involved in epigenetic regulation. J. Mol. Cell Biol. 2015, 7, 366–382. [Google Scholar] [CrossRef]
- Hörstadius, S. The Neural Crest. Its Properties and Derivatives in the Light of Experimental Research; Oxford University Press: London, UK, 1950. [Google Scholar]
- Le Douarin, N.M.; Dupin, E. The “beginnings” of the neural crest. Dev. Biol. 2018, 444, S3–S13. [Google Scholar] [CrossRef]
- Bronner-Fraser, M.; Fraser, S.E. Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 1988, 335, 161–163. [Google Scholar] [CrossRef]
- Deniz, E.; Erman, B. Long noncoding RNA (lincRNA), a new paradigm in gene expression control. Funct. Integr. Genom. 2017, 17, 135–143. [Google Scholar] [CrossRef]
- Badea, M.A.; Balas, M.; Hermenean, A.; Ciceu, A.; Herman, H.; Ionita, D.; Dinischiotu, A. Influence of Matrigel on Single- and Multiple-Spheroid Cultures in Breast Cancer Research. SLAS Discov. 2019, 24, 563–578. [Google Scholar] [CrossRef]
- Wang, C.; Wang, L.; Ding, Y.; Lu, X.; Zhang, G.; Yang, J.; Zheng, H.; Wang, H.; Jiang, Y.; Xu, L. LncRNA Structural Characteristics in Epigenetic Regulation. Int. J. Mol. Sci. 2017, 18, 2659. [Google Scholar] [CrossRef] [PubMed]
- Jones, S. An overview of the basic helix-loop-helix proteins. Genome Biol. 2004, 5, 226. [Google Scholar] [CrossRef] [PubMed]
- Luscher, B.; Larsson, L.G. The basic region/helix-loop-helix/leucine zipper domain of Myc proto-oncoproteins: Function and regulation. Oncogene 1999, 18, 2955–2966. [Google Scholar] [CrossRef] [PubMed]
- Tchurikov, N.A.; Klushevskaya, E.S.; Alembekov, I.R.; Kretova, A.N.; Chechetkin, V.R.; Kravatskaya, G.I.; Kravatsky, Y.V. Induction of the Erythroid Differentiation of K562 Cells Is Coupled with Changes in the Inter-Chromosomal Contacts of rDNA Clusters. Int. J. Mol. Sci. 2023, 24, 9842. [Google Scholar] [CrossRef]
- Tchurikov, N.A.; Klushevskaya, E.S.; Alembekov, I.R.; Bukreeva, A.S.; Kretova, A.N.; Chechetkin, V.R.; Kravatskaya, G.I.; Kravatsky, Y.V. Fragments of rDNA Genes Scattered over the Human Genome Are Targets of Small RNAs. Int. J. Mol. Sci. 2022, 23, 3014. [Google Scholar] [CrossRef]
- O’Brien, J.; Hayder, H.; Zayed, Y.; Peng, C. Overview of MicroRNA Biogenesis, Mechanisms of Actions, and Circulation. Front. Endocrinol. 2018, 9, 402. [Google Scholar] [CrossRef]
- Tchurikov, N.A.; Kretova, O.V.; Moiseeva, E.D.; Sosin, D.V. Evidence for RNA synthesis in the intergenic region between enhancer and promoter and its inhibition by insulators in Drosophila melanogaster. Nucleic Acids Res. 2009, 37, 111–122. [Google Scholar] [CrossRef]
- Fedoseeva, D.M.; Kretova, O.V.; Gorbacheva, M.A.; Tchurikov, N.A. Individual effects of the copia and gypsy enhancer and insulator on chromatin marks, eRNA synthesis, and binding of insulator proteins in transfected genetic constructs. Gene 2018, 641, 151–160. [Google Scholar] [CrossRef]
- Tchurikov, N.A.; Alembekov, I.R.; Klushevskaya, E.S.; Kretova, A.N.; Lukicheva, V.N.; Chechetkin, V.R.; Kravatskaya, G.I.; Kravatsky, Y.V. Preferential Co-Expression and Colocalization of rDNA-Contacting Genes with LincRNAs Suggest Their Involvement in Shaping Inter-Chromosomal Interactions with Nucleoli. Int. J. Mol. Sci. 2024, 25, 6333. [Google Scholar] [CrossRef]
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Tchurikov, N.A.; Vartanian, A.A.; Klushevskaya, E.S.; Alembekov, I.R.; Kretova, A.N.; Lukicheva, V.N.; Chechetkin, V.R.; Kravatskaya, G.I.; Kosorukov, V.S.; Kravatsky, Y.V. Strong Activation of ID1, ID2, and ID3 Genes Is Coupled with the Formation of Vasculogenic Mimicry Phenotype in Melanoma Cells. Int. J. Mol. Sci. 2024, 25, 9291. https://doi.org/10.3390/ijms25179291
Tchurikov NA, Vartanian AA, Klushevskaya ES, Alembekov IR, Kretova AN, Lukicheva VN, Chechetkin VR, Kravatskaya GI, Kosorukov VS, Kravatsky YV. Strong Activation of ID1, ID2, and ID3 Genes Is Coupled with the Formation of Vasculogenic Mimicry Phenotype in Melanoma Cells. International Journal of Molecular Sciences. 2024; 25(17):9291. https://doi.org/10.3390/ijms25179291
Chicago/Turabian StyleTchurikov, Nickolai A., Amalia A. Vartanian, Elena S. Klushevskaya, Ildar R. Alembekov, Antonina N. Kretova, Viktoriya N. Lukicheva, Vladimir R. Chechetkin, Galina I. Kravatskaya, Vyacheslav S. Kosorukov, and Yuri V. Kravatsky. 2024. "Strong Activation of ID1, ID2, and ID3 Genes Is Coupled with the Formation of Vasculogenic Mimicry Phenotype in Melanoma Cells" International Journal of Molecular Sciences 25, no. 17: 9291. https://doi.org/10.3390/ijms25179291