Implications of RNG140 (caprin2)-mediated translational regulation in eye lens differentiation

Abstract

Regulation of gene expression at the translational level is key to determining cell fate and function. An RNA-binding protein, RNG140 (caprin2), plays a role in eye lens differentiation and has been reported to function in translational regulation. However, the mechanism and its role in eyes has remained unclear. Here, we show that RNG140 binds to the translation initiation factor eukaryotic initiation factor 3 (eIF3) and suppresses translation through mechanisms involving suppression of eIF3-dependent translation initiation. Comprehensive ribosome profiling revealed that overexpression of RNG140 in cultured Chinese hamster ovary cells reduces translation of long mRNAs, including those associated with cell proliferation. RNG140-mediated translational regulation also operates in the mouse eye, where RNG140 knockout increased the translation of long mRNAs. mRNAs involved in lens differentiation, such as crystallin mRNAs, are short and can escape translational inhibition by RNG140 and be translated in differentiating lenses. Thus, this study provides insights into the mechanistic basis of lens cell transition from proliferation to differentiation via RNG140-mediated translational regulation. Regulation of gene expression at the translational level is key to determining cell fate and function. An RNA-binding protein, RNG140 (caprin2), plays a role in eye lens differentiation and has been reported to function in translational regulation. However, the mechanism and its role in eyes has remained unclear. Here, we show that RNG140 binds to the translation initiation factor eukaryotic initiation factor 3 (eIF3) and suppresses translation through mechanisms involving suppression of eIF3-dependent translation initiation. Comprehensive ribosome profiling revealed that overexpression of RNG140 in cultured Chinese hamster ovary cells reduces translation of long mRNAs, including those associated with cell proliferation. RNG140-mediated translational regulation also operates in the mouse eye, where RNG140 knockout increased the translation of long mRNAs. mRNAs involved in lens differentiation, such as crystallin mRNAs, are short and can escape translational inhibition by RNG140 and be translated in differentiating lenses. Thus, this study provides insights into the mechanistic basis of lens cell transition from proliferation to differentiation via RNG140-mediated translational regulation. Gene expression is an essential process in development, cell differentiation, and other diverse processes in organisms and is regulated in multiple steps. Although transcriptional control has received much attention, post-transcriptional steps such as mRNA splicing, polyadenylation, stabilization, transport, and translation are also important layers of gene expression control (1Mata J. Marguerat S. Bähler J. Post-transcriptional control of gene expression: a genome-wide perspective.Trends Biochem. Sci. 2005; 30 (16054366): 506-51410.1016/j.tibs.2005.07.005Abstract Full Text Full Text PDF PubMed Scopus (222) Google Scholar, 2Keene J.D. RNA regulons: coordination of post-transcriptional events.Nat. Rev. Genet. 2007; 8 (17572691): 533-54310.1038/nrg2111Crossref PubMed Scopus (1008) Google Scholar, 3Hieronymus H. Silver P.A. A systems view of mRNP biology.Genes Dev. 2004; 18 (15574591): 2845-286010.1101/gad.1256904Crossref PubMed Scopus (138) Google Scholar, 4Teixeira F.K. Lehmann R. 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RNA granule protein 140 (RNG140, also known as caprin2) is such an RNA-binding protein that regulates cell differentiation and various functional processes. For example, RNG140 functions in embryonic development through facilitating canonical Wnt/β-catenin signaling (8Ding Y. Xi Y. Chen T. Wang J.Y. Tao D.L. Wu Z.L. Li Y.P. Li C. Zeng R. Li L. Caprin-2 enhances canonical Wnt signaling through regulating LRP5/6 phosphorylation.J. Cell Biol. 2008; 182 (18762581): 865-87210.1083/jcb.200803147Crossref PubMed Scopus (48) Google Scholar). In erythroid cells, RNG140 expression increases during the cells' shift from a proliferative state to a differentiated state (9Aerbajinai W. Lee Y.T. Wojda U. Barr V.A. Miller J.L. Cloning and characterization of a gene expressed during terminal differentiation that encodes a novel inhibitor of growth.J. Biol. Chem. 2004; 279 (14593112): 1916-192110.1074/jbc.M305634200Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar). Indeed, RNG140 expression negatively correlates with cell growth in Chinese hamster ovary (CHO) cells (9Aerbajinai W. Lee Y.T. Wojda U. Barr V.A. Miller J.L. Cloning and characterization of a gene expressed during terminal differentiation that encodes a novel inhibitor of growth.J. Biol. Chem. 2004; 279 (14593112): 1916-192110.1074/jbc.M305634200Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar), confirming its role in inhibiting cell proliferation. In addition to cell differentiation, RNG140 is highly expressed in the brain and is involved in processes such as the formation and maintenance of dendrites and synapses (10Shiina N. Tokunaga M. RNA granule protein 140 (RNG140), a paralog of RNG105 localized to distinct RNA granules in neuronal dendrites in the adult vertebrate brain.J. Biol. Chem. 2010; 285 (20516077): 24260-2426910.1074/jbc.M110.108944Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar) and the osmotic stress response in the hypothalamus (11Konopacka A. Greenwood M. Loh S.Y. Paton J. Murphy D. RNA binding protein Caprin-2 is a pivotal regulator of the central osmotic defense response.ELife. 2015; 4: e0965610.7554/eLife.09656Crossref PubMed Google Scholar). Because RNG140 has two RNA-binding and (10Shiina N. Tokunaga M. RNA granule protein 140 (RNG140), a paralog of RNG105 localized to distinct RNA granules in neuronal dendrites in the adult vertebrate brain.J. Biol. Chem. 2010; 285 (20516077): 24260-2426910.1074/jbc.M110.108944Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar), its function be to the RNA-binding For example, RNG140 has been reported to to mRNA and the mRNA by in response to osmotic stress in the hypothalamus (11Konopacka A. Greenwood M. Loh S.Y. Paton J. Murphy D. RNA binding protein Caprin-2 is a pivotal regulator of the central osmotic defense response.ELife. 2015; 4: e0965610.7554/eLife.09656Crossref PubMed Google Scholar). RNG140 function as a of protein through a Y.T. T. M. S. of proteins in 2005; PubMed Scopus Google with protein and via the and enhances of LRP5/6 to Wnt/β-catenin signaling H. Y. S. Wang J. Y. Li L. insights into the of Caprin-2 in canonical Wnt Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, R. G. protein with cell Wnt signaling regulator protein 2015; PubMed Scopus Google Scholar). other developmental gene expression during the eye lens development is highly In this transcriptional regulation has been such as and the of lens development, and those including the of the proteins such as A. and gene in lens Genet. Full Text Full Text PDF PubMed Scopus Google Scholar, A. R. and mechanisms of vertebrate lens PubMed Scopus Google Scholar). In of the post-transcriptional control during lens development is A. and gene in lens Genet. Full Text Full Text PDF PubMed Scopus Google Scholar, S. RNA-binding proteins in eye development and of RNA granule Rev. PubMed Scopus Google Scholar) the of RNA-binding proteins as in the level of such as the protein mRNA and the crystallin and and T. A. R. Y. in the RNA granule and PubMed Scopus Google Scholar). In the of the eukaryotic translation initiation factor gene translation of crystallin mRNA and brain and eye development A. U. T. initiation factor to during Sci. U. S. A. PubMed Scopus (48) Google Scholar). a post-transcriptional gene RNG140 is such in lens lens differentiation, RNG140 expression is increased by growth factor S. of the RNA binding protein lens and of 2015; PubMed Scopus (31) Google Scholar, U. L. expression in the vertebrate PubMed Scopus Google Scholar). Indeed, RNG140 knockout in lens and of S. of the RNA binding protein lens and of 2015; PubMed Scopus (31) Google Scholar). RNG140 has been to translation in (10Shiina N. Tokunaga M. RNA granule protein 140 (RNG140), a paralog of RNG105 localized to distinct RNA granules in neuronal dendrites in the adult vertebrate brain.J. Biol. Chem. 2010; 285 (20516077): 24260-2426910.1074/jbc.M110.108944Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar). However, is known RNG140 translation and the translational regulation is to the in function of such as lens Here, we show that RNG140 translation in an and ribosome that RNG140 in translation initiation. genome-wide ribosome profiling in cells and RNG140 knockout mouse eyes that RNG140-mediated translational is long mRNAs. Thus, short mRNAs, including crystallin mRNAs, are important lens differentiation, escape RNG140-mediated translational study that RNG140 the translational of gene expression from a proliferative state to a differentiated the of RNG140 translation in this we to of in cells that expressed expressed in cells, and of those cells with that of control with control cells, at that translation by RNG140 expression A and of expression translation of cell as the with cell a lens cell and RNG140 translational of the overexpression of RNG140 in cells by with In the cells from cells by of that of the cells expressed from in cells with two and of the proteins in of in cells with in cells with with cells and that RNG140 we cell that expressed expression of that of RNG140 in mouse eyes However, RNA granules in those that the granule formation and (10Shiina N. Tokunaga M. RNA granule protein 140 (RNG140), a paralog of RNG105 localized to distinct RNA granules in neuronal dendrites in the adult vertebrate brain.J. Biol. Chem. 2010; 285 (20516077): 24260-2426910.1074/jbc.M110.108944Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar). In expression of RNG140 in the eye is to the lens the expression level of RNG140 in the lens is the expression level in the eye and be with the in the cells and in the the cell the and and cells by of the in the and be to the in the and of in the from the cells the cell the with a to be in the In localized to the and be to in the be the the remained in the the with that translation by RNG140 expression and by of the by into in cells in cells, confirming translational suppression by RNG140 expression and the of RNG140 expression the the into the of RNA in at an of and the of RNA in a with a RNA in cells in cells is known to from and the of and the RNA in and increased the in that to and and of and by the of and with and we that the the and and to the Although the in the the two in the of from the increases ribosome from the the two the in cells in cells that from mRNA to mRNA at the in Thus, RNG140 to that are mRNAs. of translational we eukaryotic factor is a of in translational Scopus Google Scholar). through a that increased the of an of and initiation factor with expression the that RNG140 increases to translational suppression by that RNG140 also in we that RNG140 with ribosome proteins translation initiation that are in the we with by that proteins with with and Gene revealed that proteins and proteins in the of the the of RNG140 with and protein and of RNG140 with of cell as in cells at this be that RNG140 the binding to of the RNG140 with A the of with RNG140 of that protein from the by A be to RNG140 through ribosome by A with the that RNG140 a with through to that RNG140 the function of translational we translation by eIF3-dependent and mechanisms In the in of and two and the RNA and ribosome Biochem. Sci. 2008; Full Text Full Text PDF PubMed Scopus Google Scholar). In cells, RNG140 expression translation and translation the that RNG140 eIF3-dependent translation the that RNG140 also translation and other translation Because translation of mRNAs is to be by we mRNAs are by RNG140 in Here, we ribosome profiling S. protein into a translational PubMed Scopus Google Scholar, profiling of translation the Full Text Full Text PDF PubMed Scopus Google Scholar, S. in of translation with ribosome PubMed Scopus Google Scholar) RNG140 overexpression in cells in translation is by of by expression and and as profiling also with increased translation and and as the of RNG140 expression translation we the expression of proteins by in the and and and by the expression of and in cells that RNG140 reduces the translation of RNG140 and its paralog RNG105 the binding to mRNAs. binding is essential the of RNG140 to translation in (10Shiina N. Tokunaga M. RNA granule protein 140 (RNG140), a paralog of RNG105 localized to distinct RNA granules in neuronal dendrites in the adult vertebrate brain.J. Biol. Chem. 2010; 285 (20516077): 24260-2426910.1074/jbc.M110.108944Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar, N. Tokunaga M. A novel RNA-binding protein in neuronal RNA 2005; PubMed Scopus Google Scholar). this RNG140 to mRNAs that multiple binding has been mRNAs in stress where mRNA correlates with to the granules A. T. S. R. stress granule of mRNA in stress Full Text Full Text PDF PubMed Scopus Google Scholar). to the and the of the and of the and and the of of the in the and and and a the of and the of the those of the that RNG140 with and to to the in the and are and and with in the in and a of involved in cell proliferation A. regulates cell proliferation by of PubMed Scopus Google Scholar), M. H. Wu W. Y. T. the of to cell 2015; PubMed Scopus Google Scholar), and Y. L. J. S. R. C. A. cell proliferation and 2015; PubMed Scopus Google W. and the role of in and cell fate PubMed Scopus Google Scholar), such as W. D. C. M. S. Wang of embryonic and in cell Genet. PubMed Scopus Google Scholar), and gene of the function of RNG140 in inhibiting cell proliferation (9Aerbajinai W. Lee Y.T. Wojda U. Barr V.A. Miller J.L. Cloning and characterization of a gene expressed during terminal differentiation that encodes a novel inhibitor of growth.J. Biol. Chem. 2004; 279 (14593112): 1916-192110.1074/jbc.M305634200Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar). we overexpression of RNG140 the proliferation of with expression the of cell growth ribosome profiling the that RNG140-mediated translational of cell mRNAs the cell the RNG140-mediated translational regulation operates in we RNG140 knockout by a a in of the a in the and a in the protein the that binds to mRNA and translation in (10Shiina N. Tokunaga M. RNA granule protein 140 (RNG140), a paralog of RNG105 localized to distinct RNA granules in neuronal dendrites in the adult vertebrate brain.J. Biol. Chem. 2010; 285 (20516077): 24260-2426910.1074/jbc.M110.108944Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar). However, the in the of a of to of in much expression of the the as we RNG140 knockout and into and and in the RNG140 is highly expressed in embryonic and eye lens in and RNG140 developmental in lens S. of the RNA binding protein lens and of 2015; PubMed Scopus (31) Google Scholar), we the expression level of RNG140 in the eye of at that RNG140 in the eye of as that RNG140 protein also in the eye of of eye with the revealed a in lens cell in that the we also other of the lens and and in that RNG140 expression in the eye lens of of RNG140 knockout lens development by of eye with lens with with of lens S. of the RNA binding protein lens and of 2015; PubMed Scopus (31) Google Scholar). the of the with the lens revealed that a of the lens with and with the that RNG140 a in lens cell and the of the lens S. of the RNA binding protein lens and of 2015; PubMed Scopus (31) Google Scholar). we ribosome profiling of mouse eyes at and with that of and For we eyes of lenses. in translation the to that of RNG140 and be to RNG140 However, the to the of RNG140 knockout the RNG140-mediated translational operates in the of RNG140 knockout translation is to be to that of RNG140 overexpression in Indeed, RNG140 increased the translation of the to the in the ribosome profiling in that of the that in the in the ribosome in and and in and and in the translation of mRNAs in the eyes of RNG140 knockout to those of RNG140 overexpression in that the of RNG140 cells and mouse eyes and that in translation with RNG140 RNG140 highly expressed during lens a key that lens differentiation escape RNG140-mediated translational lens differentiation such as and lens protein and P.A. 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L. expression in the vertebrate PubMed Scopus Google Scholar), we that RNG140 the translation of long mRNAs involved in cell the short mRNAs involved in lens differentiation mechanism is to the in the of the lens be by cell and lens differentiation by RNG140 in mouse eyes S. of the RNA binding protein lens and of 2015; PubMed Scopus (31) Google Scholar). A mechanism the long mRNA is that RNG140 binds to long mRNAs and translation through mechanisms such as binding with However, the mechanism by RNG140 long mRNAs the that the of RNG140 increases with mRNAs. mRNAs long in the In to the of mRNAs multiple binding Thus, the of the long mRNA a the of RNG140 in the of the RNG140 binds to an the be in a a mechanism that the the of as is the and translation initiation of and binds to the and translation J. S. A. Y. 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In that RNG140 the and the of short mRNAs escape translational by In the that are translated through an mechanism A. U. T. initiation factor to during Sci. U. S. A. PubMed Scopus (48) Google Scholar). to the in the mouse eye in the study and in translation of by RNG140 knockout that to be by the lens and of translational by the that RNG140 has a the of Thus, mechanism is that RNG140 mRNA through regulating RNG140 the of However, the expression of lens proteins such as and lens by RNG140 knockout S. of the RNA binding protein lens and of 2015; PubMed Scopus (31) Google Scholar), the that RNG140 suppresses the of RNG140 has been reported to RNA granules that are in (10Shiina N. Tokunaga M. RNA granule protein 140 (RNG140), a paralog of RNG105 localized to distinct RNA granules in neuronal dendrites in the adult vertebrate brain.J. Biol. Chem. 2010; 285 (20516077): 24260-2426910.1074/jbc.M110.108944Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar). such granules cell and are to cell those of RNG140 granule formation (10Shiina N. Tokunaga M. RNA granule protein 140 (RNG140), a paralog of RNG105 localized to distinct RNA granules in neuronal dendrites in the adult vertebrate brain.J. Biol. Chem. 2010; 285 (20516077): 24260-2426910.1074/jbc.M110.108944Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar). cell in the study and RNG140 with and in that at RNG140 binds to and the RNG140 to granules and its binding granule formation of RNG140 is during mouse eye RNG140 in lens cells at embryonic the lens from the RNG140 granules and RNG140 is expressed granules in lens cells from to S. of the RNA binding protein lens and of 2015; PubMed Scopus (31) Google Scholar). Thus, RNG140 granules are by at various of lens is known the is regulated by the expression level of RNG140 by other such as of RNG140 granule in the lens In cells in the study the state of lens cells in that RNG140 granule In this study RNG140-mediated translational a mechanistic into post-transcriptional regulation that during lens study also and mRNA is by translational in the coordination of proliferation and that this in this is to lens development is to other of cell fate and function. and by the and of the of and in with the from the of cells cultured in cells cultured in at in a For cells to and with in with the in the of in the and by with the of a with an the expression of RNG140 with and (10Shiina N. Tokunaga M. RNA granule protein 140 (RNG140), a paralog of RNG105 localized to distinct RNA granules in neuronal dendrites in the adult vertebrate brain.J. Biol. Chem. 2010; 285 (20516077): 24260-2426910.1074/jbc.M110.108944Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar). a the expression of RNG140 with a of RNG140 by and a at the of the RNG140 into the of the a control the RNG140 expression from with and the of and the and of in and S. protein into a translational PubMed Scopus Google Scholar). the the the a mRNA the gene with from of the in the and in RNG140 RNA a of the gene and and into the of the as N. and RNA granules through proteins and into Biol. 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Chem. 2010; 285 (20516077): 24260-2426910.1074/jbc.M110.108944Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar) expressed in and by factor and the RNG140 protein in with the protein as an to a in a An from with the and Cell protein Cell Cell and and to the proteins with a with and of as a from a of cell the R. T. N. Comprehensive of RNG105 and response to PubMed Scopus Google Scholar). as N. RNA granule and by factor associated with RNA and factor Biol. Chem. 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