Increased Level of Long Non-Coding RNA MALAT1 is a Common Feature of Amoeboid Invasion
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
32369931
PubMed Central
PMC7281393
DOI
10.3390/cancers12051136
PII: cancers12051136
Knihovny.cz E-zdroje
- Klíčová slova
- MALAT1, amoeboid invasion, cancer, invasion plasticity, lncRNA, melanoma, mesenchymal invasion,
- Publikační typ
- časopisecké články MeSH
The ability of cancer cells to adopt various migration modes (the plasticity of cancer cell invasiveness) is a substantive obstacle in the treatment of metastasis, yet still an incompletely understood process. We performed a comparison of publicly available transcriptomic datasets from various cell types undergoing a switch between the mesenchymal and amoeboid migration modes. Strikingly, lncRNA MALAT1 (metastasis-associated lung adenocarcinoma transcript 1) was one of three genes that were found upregulated in all amoeboid cells analyzed. Accordingly, downregulation of MALAT1 in predominantly amoeboid cell lines A375m2 and A2058 resulted in decrease of active RhoA (Ras homolog family member A) and was accompanied by the amoeboid-mesenchymal transition in A375m2 cells. Moreover, MALAT1 downregulation in amoeboid cells led to increased cell proliferation. Our work is the first to address the role of MALAT1 in MAT/AMT (mesenchymal to amoeboid transition/amoeboid to mesenchymal transition) and suggests that increased MALAT1 expression is a common feature of amoeboid cells.
Department of Cell Biology Charles University Viničná 7 12843 Prague Czech Republic
Medical Faculty Martin Luther University Halle Wittenberg Kurt Mothes Str 3a 06120 Halle Germany
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Cancer Research UK Worldwide Cancer Statistics. [(accessed on 20 August 2019)]; Available online: https://www.cancerresearchuk.org/health-professional/cancer-statistics/worldwide-cancer#heading-Zero.
Sleeman J., Steeg P.S. Cancer metastasis as a therapeutic target. Eur. J. Cancer. 2010;46:1177–1180. doi: 10.1016/j.ejca.2010.02.039. PubMed DOI PMC
Paňková K., Rösel D., Novotný M., Brábek J. The molecular mechanisms of transition between mesenchymal and amoeboid invasiveness in tumor cells. Cell. Mol. Life Sci. 2010;67:63–71. doi: 10.1007/s00018-009-0132-1. PubMed DOI PMC
Kosla J., Paňková D., Plachý J., Tolde O., Bicanová K., Dvořák M., Rösel D., Brábek J. Metastasis of aggressive amoeboid sarcoma cells is dependent on Rho/ROCK/MLC signaling. Cell Commun. Signal. 2013;11:51. doi: 10.1186/1478-811X-11-51. PubMed DOI PMC
Pandya P., Orgaz J.L., Sanz-Moreno V. Modes of invasion during tumour dissemination. Mol. Oncol. 2017;11:5–27. doi: 10.1002/1878-0261.12019. PubMed DOI PMC
Lawson C.D., Ridley A.J. Rho GTPase signaling complexes in cell migration and invasion. J. Cell Biol. 2018;217:447–457. doi: 10.1083/jcb.201612069. PubMed DOI PMC
Brábek J., Mierke C.T., Rösel D., Veselý P., Fabry B. The role of the tissue microenvironment in the regulation of cancer cell motility and invasion. Cell Commun. Signal. 2010;8:22. doi: 10.1186/1478-811X-8-22. PubMed DOI PMC
Gandalovičová A., Rosel D., Fernandes M., Veselý P., Heneberg P., Čermák V., Petruželka L., Kumar S., Sanz-Moreno V., Brábek J. Migrastatics—Anti-metastatic and Anti-invasion Drugs: Promises and Challenges. Trends Cancer. 2017;3:391–406. doi: 10.1016/j.trecan.2017.04.008. PubMed DOI PMC
Te Boekhorst V., Friedl P. Plasticity of Cancer Cell Invasion—Mechanisms and Implications for Therapy. Adv. Cancer Res. 2016;132:209–264. PubMed
Wilusz J.E., Freier S.M., Spector D.L. 3´ End Processing of a Long Nuclear-Retained Noncoding RNA Yields a tRNA-like Cytoplasmic RNA. Cell. 2008;135:919–932. doi: 10.1016/j.cell.2008.10.012. PubMed DOI PMC
Hutchinson J.N., Ensminger A.W., Clemson C.M., Lynch C.R., Lawrence J.B., Chess A. A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains. BMC Genom. 2007;8:39. doi: 10.1186/1471-2164-8-39. PubMed DOI PMC
Ji P., Diederichs S., Wang W., Böing S., Metzger R., Schneider P.M., Tidow N., Brandt B., Buerger H., Bulk E., et al. MALAT-1, a novel noncoding RNA, and thymosin β4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene. 2003;22:8031–8041. doi: 10.1038/sj.onc.1206928. PubMed DOI
Miyagawa R., Tano K., Mizuno R., Nakamura Y., Ijiri K., Rakwal R., Shibato J., Masuo Y., Mayeda A., Hirose T., et al. Identification of cis- and trans-acting factors involved in the localization of MALAT-1 noncoding RNA to nuclear speckles. RNA. 2012;18:738–751. doi: 10.1261/rna.028639.111. PubMed DOI PMC
Sun Y., Ma L. New Insights into Long Non-Coding RNA MALAT1 in Cancer and Metastasis. Cancers. 2019;11:216. doi: 10.3390/cancers11020216. PubMed DOI PMC
Eißmann M., Gutschner T., Hämmerle M., Günther S., Caudron-Herger M., Groß M., Schirmacher P., Rippe K., Braun T., Zörnig M., et al. Loss of the abundant nuclear non-coding RNA MALAT1 is compatible with life and development. RNA Biol. 2012;9:1076–1087. doi: 10.4161/rna.21089. PubMed DOI PMC
Zhang B., Arun G., Mao Y.S., Lazar Z., Hung G., Bhattacharjee G., Xiao X., Booth C.J., Wu J., Zhang C., et al. The lncRNA Malat1 Is Dispensable for Mouse Development but Its Transcription Plays a cis-Regulatory Role in the Adult. Cell Rep. 2012;2:111–123. doi: 10.1016/j.celrep.2012.06.003. PubMed DOI PMC
Arun G., Diermeier S., Akerman M., Chang K.-C., Wilkinson J.E., Hearn S., Kim Y., MacLeod A.R., Krainer A.R., Norton L., et al. Differentiation of mammary tumors and reduction in metastasis upon Malat1 LncRNA loss. Genes Dev. 2016;30:34–51. doi: 10.1101/gad.270959.115. PubMed DOI PMC
Lin R., Maeda S., Liu C., Karin M., Edgington T.S. A large noncoding RNA is a marker for murine hepatocellular carcinomas and a spectrum of human carcinomas. Oncogene. 2007;26:851–858. doi: 10.1038/sj.onc.1209846. PubMed DOI
Ying L., Chen Q., Wang Y., Zhou Z., Huang Y., Qiu F. Upregulated MALAT-1 contributes to bladder cancer cell migration by inducing epithelial-to-mesenchymal transition. Mol. Biosyst. 2012;8:2289–2294. doi: 10.1039/c2mb25070e. PubMed DOI
Guo F., Li Y., Liu Y., Wang J., Li Y., Li G. Inhibition of metastasis-associated lung adenocarcinoma transcript 1 in CaSki human cervical cancer cells suppresses cell proliferation and invasion. Acta Biochim. Biophys. Sin. Shanghai. 2010;42:224–229. doi: 10.1093/abbs/gmq008. PubMed DOI
Michalik K.M., You X., Manavski Y., Doddaballapur A., Zörnig M., Braun T., John D., Ponomareva Y., Chen W., Uchida S., et al. Long Noncoding RNA MALAT1 Regulates Endothelial Cell Function and Vessel Growth. Circ. Res. 2014;114:1389–1397. doi: 10.1161/CIRCRESAHA.114.303265. PubMed DOI
Han Y., Wu Z., Wu T., Huang Y., Cheng Z., Li X., Sun T., Xie X., Zhou Y., Du Z. Tumor-suppressive function of long noncoding RNA MALAT1 in glioma cells by downregulation of MMP2 and inactivation of ERK/MAPK signaling. Cell Death Dis. 2016;7:e2123. doi: 10.1038/cddis.2015.407. PubMed DOI PMC
Kwok Z.H., Roche V., Chew X.H., Fadieieva A., Tay Y. A non-canonical tumor suppressive role for the long non-coding RNA MALAT1 in colon and breast cancers. Int. J. Cancer. 2018;143:668–678. doi: 10.1002/ijc.31386. PubMed DOI
Gutschner T., Hämmerle M., Eissmann M., Hsu J., Kim Y., Hung G., Revenko A., Arun G., Stentrup M., Gross M., et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res. 2013;73:1180–1189. doi: 10.1158/0008-5472.CAN-12-2850. PubMed DOI PMC
Schmidt L.H., Spieker T., Koschmieder S., Humberg J., Jungen D., Bulk E., Hascher A., Wittmer D., Marra A., Hillejan L., et al. The Long Noncoding MALAT-1 RNA Indicates a Poor Prognosis in Non-small Cell Lung Cancer and Induces Migration and Tumor Growth. J. Thorac. Oncol. 2011;6:1984–1992. doi: 10.1097/JTO.0b013e3182307eac. PubMed DOI
Huang J., Ma L., Song W., Lu B., Huang Y., Dong H., Ma X., Zhu Z., Zhou R. MALAT1 promotes the proliferation and invasion of thyroid cancer cells via regulating the expression of IQGAP1. Biomed. Pharmacother. 2016;83:1–7. doi: 10.1016/j.biopha.2016.05.039. PubMed DOI
Kim J., Piao H.L., Kim B.J., Yao F., Han Z., Wang Y., Xiao Z., Siverly A.N., Lawhon S.E., Ton B.N., et al. Long noncoding RNA MALAT1 suppresses breast cancer metastasis. Nat. Genet. 2018;50:1705–1715. doi: 10.1038/s41588-018-0252-3. PubMed DOI PMC
Sanz-Moreno V., Gaggioli C., Yeo M., Albrengues J., Wallberg F., Viros A., Hooper S., Mitter R., Féral C.C., Cook M., et al. ROCK and JAK1 signaling cooperate to control actomyosin contractility in tumor cells and stroma. Cancer Cell. 2011;20:229–245. doi: 10.1016/j.ccr.2011.06.018. PubMed DOI
Čermák V., Gandalovičová A., Merta L., Fučíková J., Špíšek R., Rösel D., Brábek J. RNA-seq of macrophages of amoeboid or mesenchymal migratory phenotype due to specific structure of environment. Sci. Data. 2018;5:1–8. doi: 10.1038/sdata.2018.198. PubMed DOI PMC
West J.A., Davis C.P., Sunwoo H., Simon M.D., Sadreyev R.I., Wang P.I., Tolstorukov M.Y., Kingston R.E. The Long Noncoding RNAs NEAT1 and MALAT1 Bind Active Chromatin Sites. Mol. Cell. 2014;55:791–802. doi: 10.1016/j.molcel.2014.07.012. PubMed DOI PMC
Evensen N.A., Li Y., Kuscu C., Liu J., Cathcart J., Banach A., Zhang Q., Li E., Joshi S., Yang J., et al. Hypoxia promotes colon cancer dissemination through up-regulation of cell migration-inducing protein (CEMIP) Oncotarget. 2015;6:20723–20739. doi: 10.18632/oncotarget.3978. PubMed DOI PMC
Tolde O., Gandalovičová A., Křížová A., Veselý P., Chmelík R., Rosel D., Brábek J. Quantitative phase imaging unravels new insight into dynamics of mesenchymal and amoeboid cancer cell invasion. Sci. Rep. 2018;8:12020. doi: 10.1038/s41598-018-30408-7. PubMed DOI PMC
Čermák V., Gandalovičová A., Merta L., Harant K., Rösel D., Brábek J. High-throughput transcriptomic and proteomic profiling of mesenchymal-amoeboid transition in 3D collagen. Scientific Data. 2020 accepted. PubMed PMC
Gutschner T., Baas M., Diederichs S. Noncoding RNA gene silencing through genomic integration of RNA destabilizing elements using zinc finger nucleases. Genome Res. 2011;21:1944–1954. doi: 10.1101/gr.122358.111. PubMed DOI PMC
Benbow U., Schoenermark M.P., Mitchell T.I., Rutter J.L., Shimokawa K.I., Nagase H., Brinckerhoff C.E. A novel host/tumor cell interaction activates matrix metalloproteinase I and mediates invasion through type I collagen. J. Biol. Chem. 1999;274:25371–25378. doi: 10.1074/jbc.274.36.25371. PubMed DOI
Petrie R.J., Yamada K.M. Multiple mechanisms of 3D migration: The origins of plasticity. Curr. Opin. Cell Biol. 2016;42:7–12. doi: 10.1016/j.ceb.2016.03.025. PubMed DOI PMC
Sahai E., Marshall C.J. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 2003;5:711–719. doi: 10.1038/ncb1019. PubMed DOI
Sanz-Moreno V., Gadea G., Ahn J., Paterson H., Marra P., Pinner S., Sahai E., Marshall C.J. Rac activation and inactivation control plasticity of tumor cell movement. Cell. 2008;135:510–523. doi: 10.1016/j.cell.2008.09.043. PubMed DOI
Cai X., Liu Y., Yang W., Xia Y., Yang C., Yang S., Liu X. Long noncoding RNA MALAT1 as a potential therapeutic target in osteosarcoma. J. Orthop. Res. 2016;34:932–941. doi: 10.1002/jor.23105. PubMed DOI
Wang Y., Zhang Y., Yang T., Zhao W., Wang N., Li P., Zeng X., Zhang W. Long non-coding RNA MALAT1 for promoting metastasis and proliferation by acting as a ceRNA of miR-144-3p in osteosarcoma cells. Oncotarget. 2017;8:59417–59434. doi: 10.18632/oncotarget.19727. PubMed DOI PMC
Kölling M., Genschel C., Kaucsar T., Hübner A., Rong S., Schmitt R., Sörensen-Zender I., Haddad G., Kistler A., Seeger H., et al. Hypoxia-induced long non-coding RNA Malat1 is dispensable for renal ischemia/reperfusion-injury. Sci. Rep. 2018;8:3438. doi: 10.1038/s41598-018-21720-3. PubMed DOI PMC
Lehmann S., te Boekhorst V., Odenthal J., Bianchi R., van Helvert S., Ikenberg K., Ilina O., Stoma S., Xandry J., Jiang L., et al. Hypoxia Induces a HIF-1-Dependent Transition from Collective-to-Amoeboid Dissemination in Epithelial Cancer Cells. Curr. Biol. 2017;27:392–400. doi: 10.1016/j.cub.2016.11.057. PubMed DOI
Li J., Wei L., Han Z., Chen Z., Zhang Q. Silencing of Long Non-Coding RNA MALAT1 Prevents Inflammatory Injury after Lung Transplant Ischemia-Reperfusion by Downregulation of IL8 through Recruiting p300. Mol. Ther. Nucleic Acids. 2019;18:285–297. PubMed PMC
Zhou H.-J., Wang L.-Q., Wang D.-B., Yu J.-B., Zhu Y., Xu Q.-S., Zheng X.-J., Zhan R.-Y. Long noncoding RNA MALAT1 contributes to inflammatory response of microglia following spinal cord injury via the modulation of a miR-199b/IKKβ/NF-κB signaling pathway. Am. J. Physiol. Physiol. 2018;315:C52–C61. doi: 10.1152/ajpcell.00278.2017. PubMed DOI
Georgouli M., Herraiz C., Crosas-Molist E., Fanshawe B., Maiques O., Perdrix A., Pandya P., Rodriguez-Hernandez I., Ilieva K.M., Cantelli G., et al. Regional Activation of Myosin II in Cancer Cells Drives Tumor Progression via a Secretory Cross-Talk with the Immune Microenvironment. Cell. 2019;176:757–774. doi: 10.1016/j.cell.2018.12.038. PubMed DOI PMC
Wolf K., Te Lindert M., Krause M., Alexander S., Te Riet J., Willis A.L., Hoffman R.M., Figdor C.G., Weiss S.J., Friedl P. Physical limits of cell migration: Control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J. Cell Biol. 2013;201:1069–1084. doi: 10.1083/jcb.201210152. PubMed DOI PMC
Chen M., Xia Z., Chen C., Hu W., Yuan Y. LncRNA MALAT1 promotes epithelial-to-mesenchymal transition of esophageal cancer through Ezh2-Notch1 signaling pathway. Anticancer Drugs. 2018;29:767–773. doi: 10.1097/CAD.0000000000000645. PubMed DOI
Gutschner T., Hämmerle M., Diederichs S. MALAT1—A paradigm for long noncoding RNA function in cancer. J. Mol. Med. 2013;91:791–801. doi: 10.1007/s00109-013-1028-y. PubMed DOI
Arun G., Spector D.L. MALAT1 long non-coding RNA and breast cancer. RNA Biol. 2019;16:860–863. doi: 10.1080/15476286.2019.1592072. PubMed DOI PMC
Ritchie M.E., Phipson B., Wu D., Hu Y., Law C.W., Shi W., Smyth G.K. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43:e47. doi: 10.1093/nar/gkv007. PubMed DOI PMC
Law C.W., Chen Y., Shi W., Smyth G.K. voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 2014;15:R29. doi: 10.1186/gb-2014-15-2-r29. PubMed DOI PMC
Oliveros J.C. Venny 2.1. An Interactive Tool for Comparing Lists with Venn’s Diagrams. [(accessed on 1 March 2020)]; Available online: https://bioinfogp.cnb.csic.es/tools/venny/
Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., et al. The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments. Clin. Chem. 2009;55:611–622. doi: 10.1373/clinchem.2008.112797. PubMed DOI
Hellemans J., Mortier G., De Paepe A., Speleman F., Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007;8:R19. doi: 10.1186/gb-2007-8-2-r19. PubMed DOI PMC