Long non-coding RNA LASSIE regulates shear stress sensing and endothelial barrier function.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
26 05 2020
26 05 2020
Historique:
received:
10
03
2020
accepted:
04
05
2020
entrez:
28
5
2020
pubmed:
28
5
2020
medline:
16
6
2021
Statut:
epublish
Résumé
Blood vessels are constantly exposed to shear stress, a biomechanical force generated by blood flow. Normal shear stress sensing and barrier function are crucial for vascular homeostasis and are controlled by adherens junctions (AJs). Here we show that AJs are stabilized by the shear stress-induced long non-coding RNA LASSIE (linc00520). Silencing of LASSIE in endothelial cells impairs cell survival, cell-cell contacts and cell alignment in the direction of flow. LASSIE associates with junction proteins (e.g. PECAM-1) and the intermediate filament protein nestin, as identified by RNA affinity purification. The AJs component VE-cadherin showed decreased stabilization, due to reduced interaction with nestin and the microtubule cytoskeleton in the absence of LASSIE. This study identifies LASSIE as link between nestin and VE-cadherin, and describes nestin as crucial component in the endothelial response to shear stress. Furthermore, this study indicates that LASSIE regulates barrier function by connecting AJs to the cytoskeleton.
Identifiants
pubmed: 32457386
doi: 10.1038/s42003-020-0987-0
pii: 10.1038/s42003-020-0987-0
pmc: PMC7251106
doi:
Substances chimiques
RNA, Long Noncoding
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
265Références
Dekker, R. J. et al. KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium. Blood 107, 4354–4363 (2006).
pubmed: 16455954
doi: 10.1182/blood-2005-08-3465
Parmar, K. M. et al. Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2. J. Clin. Invest. 116, 49–58 (2006).
pubmed: 16341264
doi: 10.1172/JCI24787
Hamik, A. et al. Kruppel-like factor 4 regulates endothelial inflammation. J. Biol. Chem. 282, 13769–13779 (2007).
pubmed: 17339326
doi: 10.1074/jbc.M700078200
Dewey, C. F. Jr., Bussolari, S. R., Gimbrone, M. A. Jr. & Davies, P. F. The dynamic response of vascular endothelial cells to fluid shear stress. J. Biomech. Eng. 103, 177–185 (1981).
pubmed: 7278196
doi: 10.1115/1.3138276
Kris, A. S., Kamm, R. D. & Sieminski, A. L. VASP involvement in force-mediated adherens junction strengthening. Biochem. Biophys. Res. Commun. 375, 134–138 (2008).
pubmed: 18680720
pmcid: 2561196
doi: 10.1016/j.bbrc.2008.07.132
Liu, Z. et al. Mechanical tugging force regulates the size of cell-cell junctions. Proc. Natl Acad. Sci. USA 107, 9944–9949 (2010).
pubmed: 20463286
doi: 10.1073/pnas.0914547107
Weis, S. M. Vascular permeability in cardiovascular disease and cancer. Curr. Opin. Hematol. 15, 243–249 (2008).
pubmed: 18391792
doi: 10.1097/MOH.0b013e3282f97d86
Mehta, D. & Malik, A. B. Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 86, 279–367 (2006).
pubmed: 16371600
doi: 10.1152/physrev.00012.2005
Gonzalez-Mariscal, L., Tapia, R. & Chamorro, D. Crosstalk of tight junction components with signaling pathways. Biochim. Biophys. Acta 1778, 729–756 (2008).
pubmed: 17950242
doi: 10.1016/j.bbamem.2007.08.018
Bazzoni, G. & Dejana, E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 84, 869–901 (2004).
pubmed: 15269339
doi: 10.1152/physrev.00035.2003
Wallez, Y. & Huber, P. Endothelial adherens and tight junctions in vascular homeostasis, inflammation and angiogenesis. Biochim. Biophys. Acta 1778, 794–809 (2008).
pubmed: 17961505
doi: 10.1016/j.bbamem.2007.09.003
Dejana, E., Tournier-Lasserve, E. & Weinstein, B. M. The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev. Cell 16, 209–221 (2009).
pubmed: 19217423
doi: 10.1016/j.devcel.2009.01.004
Vestweber, D. VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler. Thromb. Vasc. Biol. 28, 223–232 (2008).
pubmed: 18162609
doi: 10.1161/ATVBAHA.107.158014
Biswas, P. et al. Identification of the regions of PECAM-1 involved in beta- and gamma-catenin associations. Biochem. Biophys. Res. Commun. 329, 1225–1233 (2005).
pubmed: 15766557
doi: 10.1016/j.bbrc.2005.02.095
Tzima, E. et al. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437, 426–431 (2005).
doi: 10.1038/nature03952
Conway, D. E. et al. Fluid shear stress on endothelial cells modulates mechanical tension across VE-cadherin and PECAM-1. Curr. Biol. 23, 1024–1030 (2013).
pubmed: 23684974
pmcid: 23684974
doi: 10.1016/j.cub.2013.04.049
Alieva, I. B. Role of microtubule cytoskeleton in regulation of endothelial barrier function. Biochemistry 79, 964–975 (2014).
pubmed: 25385022
Djebali, S. et al. Landscape of transcription in human cells. Nature 489, 101–108 (2012).
pubmed: 3684276
pmcid: 3684276
doi: 10.1038/nature11233
Mercer, T. R., Dinger, M. E. & Mattick, J. S. Long non-coding RNAs: insights into functions. Nat. Rev. Genet. 10, 155–159 (2009).
pubmed: 19188922
doi: 10.1038/nrg2521
Tsai, M. C. et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science 329, 689–693 (2010).
pubmed: 20616235
pmcid: 2967777
doi: 10.1126/science.1192002
Kurian, L. et al. Identification of novel long noncoding RNAs underlying vertebrate cardiovascular development. Circulation 131, 1278–1290 (2015).
pubmed: 25739401
pmcid: 4443804
doi: 10.1161/CIRCULATIONAHA.114.013303
Tichon, A. et al. A conserved abundant cytoplasmic long noncoding RNA modulates repression by Pumilio proteins in human cells. Nat. Commun. 7, 12209 (2016).
pubmed: 27406171
pmcid: 4947167
doi: 10.1038/ncomms12209
Hu, G., Lou, Z. & Gupta, M. The long non-coding RNA GAS5 cooperates with the eukaryotic translation initiation factor 4E to regulate c-Myc translation. PLoS One 9, e107016 (2014).
pubmed: 25197831
pmcid: 4157848
doi: 10.1371/journal.pone.0107016
Kaneko, S. et al. Interactions between JARID2 and noncoding RNAs regulate PRC2 recruitment to chromatin. Mol. Cell 53, 290–300 (2014).
pubmed: 24374312
doi: 10.1016/j.molcel.2013.11.012
Boon, R. A. et al. Long noncoding RNA Meg3 controls endothelial cell aging and function: implications for regenerative angiogenesis. J. Am. Coll. Cardiol. 68, 2589–2591 (2016).
pubmed: 27931619
doi: 10.1016/j.jacc.2016.09.949
Leisegang, M. S. et al. Long noncoding RNA MANTIS facilitates endothelial angiogenic function. Circulation 136, 65–79 (2017).
pubmed: 28351900
pmcid: 5491227
doi: 10.1161/CIRCULATIONAHA.116.026991
Neumann, P. et al. The lncRNA GATA6-AS epigenetically regulates endothelial gene expression via interaction with LOXL2. Nat. Commun. 9, 237 (2018).
pubmed: 29339785
pmcid: 5770451
doi: 10.1038/s41467-017-02431-1
Doddaballapur, A. et al. Laminar shear stress inhibits endothelial cell metabolism via KLF2-mediated repression of PFKFB3. Arterioscler. Thromb. Vasc. Biol. 35, 137–145 (2015).
pubmed: 25359860
doi: 10.1161/ATVBAHA.114.304277
Wang, L. et al. CPAT: Coding-Potential Assessment Tool using an alignment-free logistic regression model. Nucleic Acids Res. 41, e74 (2013).
pubmed: 23335781
pmcid: 3616698
doi: 10.1093/nar/gkt006
Sehnert, A. J. et al. Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat. Genet. 31, 106–110 (2002).
pubmed: 11967535
doi: 10.1038/ng875
Michalik, K. M. et al. Long noncoding RNA MALAT1 regulates endothelial cell function and vessel growth. Circ. Res. 114, 1389–1397 (2014).
pubmed: 24602777
doi: 10.1161/CIRCRESAHA.114.303265
Battich, N., Stoeger, T. & Pelkmans, L. Image-based transcriptomics in thousands of single human cells at single-molecule resolution. Nat. Methods 10, 1127–1133 (2013).
pubmed: 24097269
doi: 10.1038/nmeth.2657
Szulcek, R., Bogaard, H. J. & van Nieuw Amerongen, G. P. Electric cell-substrate impedance sensing for the quantification of endothelial proliferation, barrier function, and motility. J .Vis. Exp. 28, 51300 (2014).
Shay-Salit, A. et al. VEGF receptor 2 and the adherens junction as a mechanical transducer in vascular endothelial cells. Proc. Natl Acad. Sci. USA 99, 9462–9467 (2002).
pubmed: 12080144
doi: 10.1073/pnas.142224299
Chang, L. & Goldman, R. D. Intermediate filaments mediate cytoskeletal crosstalk. Nat. Rev. Mol. Cell Biol. 5, 601–613 (2004).
pubmed: 15366704
doi: 10.1038/nrm1438
Birukova, A. A. et al. Microtubule disassembly induces cytoskeletal remodeling and lung vascular barrier dysfunction: role of Rho-dependent mechanisms. J. Cell Physiol. 201, 55–70 (2004).
pubmed: 15281089
doi: 10.1002/jcp.20055
Man, H. S. J. et al. Angiogenic patterning by STEEL, an endothelial-enriched long noncoding RNA. Proc. Natl Acad. Sci. USA 115, 2401–2406 (2018).
pubmed: 29467285
doi: 10.1073/pnas.1715182115
Lyu, Q. et al. SENCR stabilizes vascular endothelial cell adherens junctions through interaction with CKAP4. Proc. Natl Acad. Sci. USA 116, 546–555 (2019).
pubmed: 30584103
doi: 10.1073/pnas.1810729116
Johnsson, P., Lipovich, L., Grander, D. & Morris, K. V. Evolutionary conservation of long non-coding RNAs; sequence, structure, function. Biochim. Biophys. Acta 1840, 1063–1071 (2014).
pubmed: 24184936
doi: 10.1016/j.bbagen.2013.10.035
Tsuruta, D. & Jones, J. C. The vimentin cytoskeleton regulates focal contact size and adhesion of endothelial cells subjected to shear stress. J. Cell Sci. 116, 4977–4984 (2003).
pubmed: 14625391
doi: 10.1242/jcs.00823
Nieuwenhuizen, R. P. et al. Co-orientation: quantifying simultaneous co-localization and orientational alignment of filaments in light microscopy. PLoS One 10, e0131756 (2015).
pubmed: 26161965
pmcid: 4498647
doi: 10.1371/journal.pone.0131756
Nieminen, M. et al. Vimentin function in lymphocyte adhesion and transcellular migration. Nat. Cell Biol. 8, 156–162 (2006).
pubmed: 16429129
doi: 10.1038/ncb1355
Liu, T. et al. Modulating endothelial barrier function by targeting vimentin phosphorylation. J. Cell Physiol. 229, 1484–1493 (2014).
pubmed: 24648251
doi: 10.1002/jcp.24590
Gan, Z. et al. Vimentin intermediate filaments template microtubule networks to enhance persistence in cell polarity and directed migration. Cell Syst. 3, 252–263.e258 (2016).
pubmed: 27667364
pmcid: 5055390
doi: 10.1016/j.cels.2016.08.007
Spagnuolo, R. et al. Gas1 is induced by VE-cadherin and vascular endothelial growth factor and inhibits endothelial cell apoptosis. Blood 103, 3005–3012 (2004).
pubmed: 15070677
doi: 10.1182/blood-2003-07-2459
Yue, B. et al. A positive feed-forward loop between LncRNA-CYTOR and Wnt/beta-catenin signaling promotes metastasis of colon cancer. Mol. Ther. 26, 1287–1298 (2018).
pubmed: 29606502
pmcid: 5993983
doi: 10.1016/j.ymthe.2018.02.024
Kloc, M. et al. Potential structural role of non-coding and coding RNAs in the organization of the cytoskeleton at the vegetal cortex of Xenopus oocytes. Development 132, 3445–3457 (2005).
pubmed: 16000384
doi: 10.1242/dev.01919
Szulcek, R. et al. Delayed Microvascular Shear Adaptation in Pulmonary Arterial Hypertension. Role of Platelet Endothelial Cell Adhesion Molecule-1 Cleavage. Am. J. Respir. Crit. Care Med. 193, 1410–1420 (2016).
pubmed: 26760925
pmcid: 6915853
doi: 10.1164/rccm.201506-1231OC
Daniel, A. E. et al. Plasminogen activator inhibitor-1 controls vascular integrity by regulating VE-cadherin trafficking. PLoS One 10, e0145684 (2015).
pubmed: 26714278
pmcid: 4694698
doi: 10.1371/journal.pone.0145684
Gagnon, K. T., Li, L., Chu, Y., Janowski, B. A. & Corey, D. R. RNAi factors are present and active in human cell nuclei. Cell Rep. 6, 211–221 (2014).
pubmed: 24388755
pmcid: 3916906
doi: 10.1016/j.celrep.2013.12.013
Wang, S. et al. Endothelial cation channel PIEZO1 controls blood pressure by mediating flow-induced ATP release. J. Clin. Invest. 126, 4527–4536 (2016).
pubmed: 27797339
pmcid: 5127677
doi: 10.1172/JCI87343
Korff, T. & Augustin, H. G. Integration of endothelial cells in multicellular spheroids prevents apoptosis and induces differentiation. J. Cell Biol. 143, 1341–1352 (1998).
pubmed: 9832561
pmcid: 2133072
doi: 10.1083/jcb.143.5.1341
Giaever, I. & Keese, C. R. Micromotion of mammalian cells measured electrically. Proc. Natl Acad. Sci. USA 88, 7896–7900 (1991).
pubmed: 1881923
doi: 10.1073/pnas.88.17.7896
Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008).
pubmed: 19029910
pmcid: 19029910
doi: 10.1038/nbt.1511
Tyanova, S. et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740 (2016).
pubmed: 27348712
pmcid: 27348712
doi: 10.1038/nmeth.3901
Perez-Riverol, Y. et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47, D442–D450 (2019).
pubmed: 30395289
pmcid: 30395289
doi: 10.1093/nar/gky1106
Kwon, H. B. et al. In vivo modulation of endothelial polarization by apelin receptor signalling. Nat. Commun. 7, 11805 (2016).
pubmed: 27248505
pmcid: 4895482
doi: 10.1038/ncomms11805