Increased Level of Long Non-Coding RNA MALAT1 is a Common Feature of Amoeboid Invasion

. 2020 May 01 ; 12 (5) : . [epub] 20200501

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32369931

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.

Zobrazit více v PubMed

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

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...