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An RNA-zipcode-independent mechanism that localizes Dia1 mRNA to the perinuclear ER through interactions between Dia1 nascent peptide and Rho–GTP
Abstract
Signal-peptide-mediated ER localization of mRNAs encoding for membrane and secreted proteins, and RNA-zipcode-mediated intracellular targeting of mRNAs encoding for cytosolic proteins are two well-known mechanisms for mRNA localization. Here, we report a previously unidentified mechanism by which mRNA encoding for Dia1, a cytosolic protein without the signal peptide, is localized to the perinuclear ER in an RNA-zipcode-independent manner in fibroblasts. Dia1 mRNA localization is also independent of the actin and microtubule cytoskeleton but requires translation and the association of Dia1 nascent peptide with the ribosome–mRNA complex. Sequence mapping suggests that interactions of the GTPase binding domain of Dia1 peptide with active Rho are important for Dia1 mRNA localization. This mechanism can override the β-actin RNA zipcode and redirect β-actin mRNA to the perinuclear region, providing a new way to manipulate intracellular mRNA localization.
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“Notably, although Gapdh is a cytosolic protein-encoded gene, several studies have documented the presence of Gapdh mRNA in association with the ER [57–61].”
From The Mitochondria-Associated ER Membranes Are Novel Subcellular Locations Enriched for Inflammatory-Responsive MicroRNAs (2020) · cites this paper as [59]
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Research works printed but not linked: 100
- Alberts, 2001, Identification of a carboxyl-terminal diaphanous-related formin homology protein autoregulatory domain, J. Biol. Chem., 276, 2824, 10.1074/jbc.M006205200 · DOI
- Arai, 2002, STARS, a striated muscle activator of Rho signaling and serum response factor-dependent transcription, J. Biol. Chem., 277, 24453, 10.1074/jbc.M202216200 · DOI
- Arthur, 2002, Regulation of Rho family GTPases by cell-cell and cell-matrix adhesion, Biol. Res., 35, 239, 10.4067/S0716-97602002000200016 · DOI
- Bassell, 2004, Binding proteins for mRNA localization and local translation, and their dysfunction in genetic neurological disease, Curr. Opin. Neurobiol., 14, 574, 10.1016/j.conb.2004.08.010 · DOI
- Blobel, 1975, Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma, J. Cell Biol., 67, 835, 10.1083/jcb.67.3.835 · DOI
- Blobel, 1975, Transfer to proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components, J. Cell Biol., 67, 852, 10.1083/jcb.67.3.852 · DOI
- Buchsbaum, 2007, Rho activation at a glance, J. Cell Sci., 120, 1149, 10.1242/jcs.03428 · DOI
- Casella, 1981, Cytochalasin D inhibits actin polymerization and induces depolymerization of actin filaments formed during platelet shape change, Nature, 293, 302, 10.1038/293302a0 · DOI · Paper page
- Chabanon, 2004, Zipcodes and postage stamps: mRNA localisation signals and their trans-acting binding proteins, Brief. Funct. Genomic. Proteomic., 3, 240, 10.1093/bfgp/3.3.240 · DOI
- Chardin, 1989, The mammalian G protein rhoC is ADP-ribosylated by Clostridium botulinum exoenzyme C3 and affects actin microfilaments in Vero cells, EMBO J., 8, 1087, 10.1002/j.1460-2075.1989.tb03477.x · DOI
- Chartrand, 1999, Structural elements required for the localization of ASH1 mRNA and of a green fluorescent protein reporter particle in vivo, Curr. Biol., 9, 333, 10.1016/S0960-9822(99)80144-4 · DOI
- Chartrand, 2002, Asymmetric sorting of ash1p in yeast results from inhibition of translation by localization elements in the mRNA, Mol. Cell, 10, 1319, 10.1016/S1097-2765(02)00694-9 · DOI
- Cheng, 2006, Human mRNA export machinery recruited to the 5′ end of mRNA, Cell, 127, 1389, 10.1016/j.cell.2006.10.044 · DOI
- Chesarone, 2009, Actin nucleation and elongation factors: mechanisms and interplay, Curr. Opin. Cell Biol., 21, 28, 10.1016/j.ceb.2008.12.001 · DOI
- Cohen, 2005, The role of membranes and membrane trafficking in RNA localization, Biol. Cell, 97, 5, 10.1042/BC20040056 · DOI
- Condeelis, 2005, How and why does beta-actin mRNA target?, Biol. Cell, 97, 97, 10.1042/BC20040063 · DOI
- Corral-Debrinski, 2007, mRNA specific subcellular localization represents a crucial step for fine-tuning of gene expression in mammalian cells, Biochim. Biophys. Acta, 1773, 473, 10.1016/j.bbamcr.2006.06.008 · DOI
- Cussac, 1996, Rho proteins are localized with different membrane compartments involved in vesicular trafficking in anterior pituitary cells, Mol. Cell. Endocrinol., 119, 195, 10.1016/0303-7207(96)03814-2 · DOI
- Czaplinski, 2006, Pathways for mRNA localization in the cytoplasm, Trends Biochem. Sci., 31, 687, 10.1016/j.tibs.2006.10.007 · DOI
- Du, 2007, Why cells move messages: the biological functions of mRNA localization, Semin. Cell Dev. Biol., 18, 171, 10.1016/j.semcdb.2007.01.010 · DOI
- Eisenmann, 2005, Rho GTPase-formin pairs in cytoskeletal remodelling, Novartis Found. Symp., 269, 206, 10.1002/047001766X.ch16 · DOI
- Eisenmann, 2007, T cell responses in mammalian diaphanous-related formin mDia1 knock-out mice, J. Biol. Chem., 282, 25152, 10.1074/jbc.M703243200 · DOI
- Eom, 2003, Localization of a beta-actin messenger ribonucleoprotein complex with zipcode-binding protein modulates the density of dendritic filopodia and filopodial synapses, J. Neurosci., 23, 10433, 10.1523/JNEUROSCI.23-32-10433.2003 · DOI
- Faix, 2006, Staying in shape with formins, Dev. Cell, 10, 693, 10.1016/j.devcel.2006.05.001 · DOI
- Fukata, 2003, Roles of Rho-family GTPases in cell polarisation and directional migration, Curr. Opin. Cell Biol., 15, 590, 10.1016/S0955-0674(03)00097-8 · DOI
- Gadea, 2007, Loss of p53 promotes RhoA-ROCK-dependent cell migration and invasion in 3D matrices, J. Cell Biol., 178, 23, 10.1083/jcb.200701120 · DOI
- Geneste, 2002, LIM kinase and Diaphanous cooperate to regulate serum response factor and actin dynamics, J. Cell Biol., 157, 831, 10.1083/jcb.200203126 · DOI
- Godchaux, 1967, Effects of cycloheximide on polyribosome function in reticulocytes, J. Mol. Biol., 27, 57, 10.1016/0022-2836(67)90351-8 · DOI
- Gonzalez, 1999, ASH1 mRNA localization in yeast involves multiple secondary structural elements and Ash1 protein translation, Curr. Biol., 9, 337, 10.1016/S0960-9822(99)80145-6 · DOI
- Goode, 2007, Mechanism and function of formins in the control of actin assembly, Annu. Rev. Biochem., 76, 593, 10.1146/annurev.biochem.75.103004.142647 · DOI
- Goulimari, 2005, Galpha12/13 is essential for directed cell migration and localized Rho-Dia1 function, J. Biol. Chem., 280, 42242, 10.1074/jbc.M508690200 · DOI
- Graham, 2002, Fractionation of Golgi, endoplasmic reticulum, and plasma membrane from cultured cells in a preformed continuous iodixanol gradient, ScientificWorldJournal, 2, 1435, 10.1100/tsw.2002.286 · DOI
- Griffin, 1998, Specific covalent labeling of recombinant protein molecules inside live cells, Science, 281, 269, 10.1126/science.281.5374.269 · DOI
- Griffin, 2000, Fluorescent labeling of recombinant proteins in living cells with FlAsH, Methods Enzymol., 327, 565, 10.1016/S0076-6879(00)27302-3 · DOI
- Gu, 2002, A predominantly nuclear protein affecting cytoplasmic localization of beta-actin mRNA in fibroblasts and neurons, J. Cell Biol., 156, 41, 10.1083/jcb.200105133 · DOI
- Hall, 2005, Rho GTPases and the control of cell behaviour, Biochem. Soc. Trans., 33, 891, 10.1042/BST0330891 · DOI
- Hesketh, 2004, 3′-Untranslated regions are important in mRNA localization and translation: lessons from selenium and metallothionein, Biochem. Soc. Trans., 32, 990, 10.1042/BST0320990 · DOI
- Higgs, 2005, Formin proteins: a domain-based approach, Trends Biochem. Sci., 30, 342, 10.1016/j.tibs.2005.04.014 · DOI
- Holt, 2009, Subcellular mRNA localization in animal cells and why it matters, Science, 326, 1212, 10.1126/science.1176488 · DOI
- Huttelmaier, 2005, Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1, Nature, 438, 512, 10.1038/nature04115 · DOI
- Jaffe, 2005, Rho GTPases: biochemistry and biology, Annu. Rev. Cell Dev. Biol., 21, 247, 10.1146/annurev.cellbio.21.020604.150721 · DOI · Paper page
- Joklik, 1965, Studies on the genesis of polyribosomes. I. Origin and significance of the subribosomal particles, J. Mol. Biol., 13, 496, 10.1016/S0022-2836(65)80112-7 · DOI
- Kiebler, 2006, Neuronal RNA granules: movers and makers, Neuron, 51, 685, 10.1016/j.neuron.2006.08.021 · DOI
- King, 2005, Putting RNAs in the right place at the right time: RNA localization in the frog oocyte, Biol. Cell, 97, 19, 10.1042/BC20040067 · DOI
- Kislauskis, 1993, Isoform-specific 3′-untranslated sequences sort alpha-cardiac and beta-cytoplasmic actin messenger RNAs to different cytoplasmic compartments, J. Cell Biol., 123, 165, 10.1083/jcb.123.1.165 · DOI
- Kislauskis, 1994, Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype, J. Cell Biol., 127, 441, 10.1083/jcb.127.2.441 · DOI
- Kislauskis, 1997, beta-Actin messenger RNA localization and protein synthesis augment cell motility, J. Cell Biol., 136, 1263, 10.1083/jcb.136.6.1263 · DOI · Paper page
- Kraut-Cohen, 2010, Addressing mRNAs to the ER: cis sequences act up!, Trends Biochem. Sci., 35, 459, 10.1016/j.tibs.2010.02.006 · DOI
- Latham, 2001, A Rho-dependent signaling pathway operating through myosin localizes beta-actin mRNA in fibroblasts, Curr. Biol., 11, 1010, 10.1016/S0960-9822(01)00291-3 · DOI
- Lawrence, 1986, Intracellular localization of messenger RNAs for cytoskeletal proteins, Cell, 45, 407, 10.1016/0092-8674(86)90326-0 · DOI
- Lecuyer, 2009, Global implications of mRNA localization pathways in cellular organization, Curr. Opin. Cell Biol., 21, 409, 10.1016/j.ceb.2009.01.027 · DOI
- Lerner, 2003, Partitioning and translation of mRNAs encoding soluble proteins on membrane-bound ribosomes, RNA, 9, 1123, 10.1261/rna.5610403 · DOI
- Li, 2003, The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition, Curr. Biol., 13, 1335, 10.1016/S0960-9822(03)00540-2 · DOI
- Liao, 2010, Mis-localization of Arp2 mRNA impairs persistence of directional cell migration, Exp. Cell Res.
- Liu, 2006, A quantitative evaluation of peroxidase inhibitors for tyramide signal amplification mediated cytochemistry and histochemistry, Histochem. Cell Biol., 126, 283, 10.1007/s00418-006-0161-x · DOI
- Liu, 2006, A PDZ-binding motif as a critical determinant of Rho guanine exchange factor function and cell phenotype, Mol. Biol. Cell, 17, 1880, 10.1091/mbc.e06-01-0002 · DOI
- Lodish, 1971, Alpha and beta globin messenger ribonucleic acid. Different amounts and rates of initiation of translation, J. Biol. Chem., 246, 7131, 10.1016/S0021-9258(19)45864-X · DOI
- Lopez de Heredia, 2004, mRNA localization and the cytoskeleton, Curr. Opin. Cell Biol., 16, 80, 10.1016/j.ceb.2003.11.002 · DOI
- Machesky, 1997, Mammalian actin-related protein 2/3 complex localizes to regions of lamellipodial protrusion and is composed of evolutionarily conserved proteins, Biochem. J., 328, 105, 10.1042/bj3280105 · DOI
- Malliri, 2003, Role of Rho-family proteins in cell adhesion and cancer, Curr. Opin. Cell Biol., 15, 583, 10.1016/S0955-0674(03)00098-X · DOI
- Martin, 2005, Mammalian cell-based optimization of the biarsenical-binding tetracysteine motif for improved fluorescence and affinity, Nat. Biotechnol., 23, 1308, 10.1038/nbt1136 · DOI
- Martin, 2009, mRNA localization: gene expression in the spatial dimension, Cell, 136, 719, 10.1016/j.cell.2009.01.044 · DOI · Paper page
- Meignin, 2010, Transmitting the message: intracellular mRNA localization, Curr. Opin. Cell Biol., 22, 112, 10.1016/j.ceb.2009.11.011 · DOI
- Mili, 2009, RNA localization and polarity: from A(PC) to Z(BP), Trends Cell. Biol., 19, 156, 10.1016/j.tcb.2009.02.001 · DOI
- Mingle, 2005, Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts, J. Cell Sci., 118, 2425, 10.1242/jcs.02371 · DOI
- Mingle, 2009, LPA-induced mutually exclusive subcellular localization of active RhoA and Arp2 mRNA revealed by sequential FRET and FISH, Histochem. Cell Biol., 132, 47, 10.1007/s00418-009-0589-x · DOI
- Moore, 2005, From birth to death: the complex lives of eukaryotic mRNAs, Science, 309, 1514, 10.1126/science.1111443 · DOI
- Mullins, 1998, The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments, Proc. Natl. Acad. Sci. USA, 95, 6181, 10.1073/pnas.95.11.6181 · DOI
- Nicchitta, 2005, Pathways for compartmentalizing protein synthesis in eukaryotic cells: the template-partitioning model, Biochem. Cell Biol., 83, 687, 10.1139/o05-147 · DOI
- Oleynikov, 1998, RNA localization: different zipcodes, same postman?, Trends Cell. Biol., 8, 381, 10.1016/S0962-8924(98)01348-8 · DOI
- Oleynikov, 2003, Real-time visualization of ZBP1 association with beta-actin mRNA during transcription and localization, Curr. Biol., 13, 199, 10.1016/S0960-9822(03)00044-7 · DOI
- Otomo, 2005, Structural basis of Rho GTPase-mediated activation of the formin mDia1, Mol. Cell, 18, 273, 10.1016/j.molcel.2005.04.002 · DOI
- Pan, 2007, ZBP2 facilitates binding of ZBP1 to beta-actin mRNA during transcription, Mol. Cell. Biol., 27, 8340, 10.1128/MCB.00972-07 · DOI
- Paquin, 2007, Local activation of yeast ASH1 mRNA translation through phosphorylation of Khd1p by the casein kinase Yck1p, Mol. Cell, 26, 795, 10.1016/j.molcel.2007.05.016 · DOI
- Peng, 2007, Myeloproliferative defects following targeting of the Drf1 gene encoding the mammalian diaphanous related formin mDia1, Cancer Res., 67, 7565, 10.1158/0008-5472.CAN-07-1467 · DOI
- Picard, 2009, Spatial and temporal activation of the small GTPases RhoA and Rac1 by the netrin-1 receptor UNC5a during neurite outgrowth, Cell. Signal., 21, 1961, 10.1016/j.cellsig.2009.09.004 · DOI
- Pollard, 2007, Regulation of actin filament assembly by Arp2/3 complex and formins, Annu. Rev. Biophys. Biomol. Struct., 36, 451, 10.1146/annurev.biophys.35.040405.101936 · DOI
- Potter, 2000, Regulation of ribosome detachment from the mammalian endoplasmic reticulum membrane, J. Biol. Chem., 275, 33828, 10.1074/jbc.M005294200 · DOI
- Pyhtila, 2008, Signal sequence- and translation-independent mRNA localization to the endoplasmic reticulum, RNA, 14, 445, 10.1261/rna.721108 · DOI
- Raftopoulou, 2004, Cell migration: Rho GTPases lead the way, Dev. Biol., 265, 23, 10.1016/j.ydbio.2003.06.003 · DOI
- Ridley, 2006, Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking, Trends Cell. Biol., 16, 522, 10.1016/j.tcb.2006.08.006 · DOI
- Rodriguez, 2006, Visualization of mRNA translation in living cells, J. Cell. Biol., 175, 67, 10.1083/jcb.200512137 · DOI
- Rose, 2005, Structural and mechanistic insights into the interaction between Rho and mammalian Dia, Nature, 435, 513, 10.1038/nature03604 · DOI
- Rubin, 1988, Functional modification of a 21-kilodalton G protein when ADP-ribosylated by exoenzyme C3 of Clostridium botulinum, Mol. Cell. Biol., 8, 418, 10.1128/MCB.8.1.418 · DOI
- Schirenbeck, 2005, The Diaphanous-related formin dDia2 is required for the formation and maintenance of filopodia, Nat. Cell Biol., 7, 619, 10.1038/ncb1266 · DOI
- Schmid, 2006, Coordination of endoplasmic reticulum and mRNA localization to the yeast bud, Curr. Biol., 16, 1538, 10.1016/j.cub.2006.06.025 · DOI
- Seth, 2006, Autoinhibition regulates cellular localization and actin assembly activity of the diaphanous-related formins FRLalpha and mDia1, J. Cell Biol., 174, 701, 10.1083/jcb.200605006 · DOI
- Shestakova, 2001, The physiological significance of beta-actin mRNA localization in determining cell polarity and directional motility, Proc. Natl. Acad. Sci. USA, 98, 7045, 10.1073/pnas.121146098 · DOI
- St Johnston, 2005, Moving messages: the intracellular localization of mRNAs, Nat. Rev. Mol. Cell Biol., 6, 363, 10.1038/nrm1643 · DOI
- Stephens, 2007, In vitro and tissue culture methods for analysis of translation initiation on the endoplasmic reticulum, Methods Enzymol., 431, 47, 10.1016/S0076-6879(07)31004-5 · DOI
- Sternlicht, 1979, Colchicine inhibition of microtubule assembly via copolymer formation, J. Biol. Chem., 254, 10540, 10.1016/S0021-9258(19)86741-8 · DOI
- Su, 2009, p190RhoGAP negatively regulates Rho activity at the cleavage furrow of mitotic cells, Exp. Cell Res., 315, 1347, 10.1016/j.yexcr.2009.02.014 · DOI
- Tominaga, 2000, Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling, Mol. Cell, 5, 13, 10.1016/S1097-2765(00)80399-8 · DOI
- Walter, 1981, Translocation of proteins across the endoplasmic reticulum. II. Signal recognition protein (SRP) mediates the selective binding to microsomal membranes of in-vitro-assembled polysomes synthesizing secretory protein, J. Cell Biol., 91, 551, 10.1083/jcb.91.2.551 · DOI
- Washida, 2009, Identification of cis-localization elements that target glutelin RNAs to a specific subdomain of the cortical endoplasmic reticulum in rice endosperm cells, Plant Cell Physiol., 50, 1710, 10.1093/pcp/pcp103 · DOI
- Watanabe, 1997, p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin, EMBO J., 16, 3044, 10.1093/emboj/16.11.3044 · DOI · Paper page
- Wen, 2004, EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration, Nat. Cell Biol., 6, 820, 10.1038/ncb1160 · DOI
- Westendorf, 1999, Identification and characterization of a protein containing formin homology (FH1/FH2) domains, Gene, 232, 173, 10.1016/S0378-1119(99)00127-4 · DOI
- Yarmolinsky, 1959, Inhibition By Puromycin Of Amino Acid Incorporation Into Protein, Proc. Natl. Acad. Sci. USA, 45, 1721, 10.1073/pnas.45.12.1721 · DOI
- Yoshizaki, 2003, Activity of Rho-family GTPases during cell division as visualized with FRET-based probes, J. Cell Biol., 162, 223, 10.1083/jcb.200212049 · DOI
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Wang, W.-X., Prajapati, P., Nelson, P. T., & Springer, J. E. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-01937-y · Cited by 49
Metadata
- Authors
- Liao, G., Ma, X., & Liu, G.
- Affiliations
- Center for Cell Biology and Cancer Research, Albany Medical College, Albany, NY 12208, USA
- Venue
- Journal of Cell Science
- Publisher
- The Company of Biologists
- Published
- 2011-02-15
- Volume
- 124
- Issue
- 4
- Pages
- 589-599
- ISSN
- 1477-9137
- 0021-9533
- Cited by
- 25
- References
- 0
- Language
- en
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