Take the (RN)A-train: Localization of mRNA to the endoplasmic reticulum

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 11, 2013, Pages 2519-2525

  Hermesh, Orit ^a   Jansen, Ralf Peter ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Cortical ER; MRNA targeting; P180; Prolamine; Signal recognition particle

Indexed keywords

DOCKING PROTEIN; GLUCOSE REGULATED PROTEIN 94; GLUTENIN; INITIATION FACTOR 4G; MEMBRANE PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MULTIDRUG RESISTANCE PROTEIN 1; MYOSIN V; PROTEIN DISULFIDE ISOMERASE; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; SEED STORAGE PROTEIN; SIGNAL PEPTIDE; SIGNAL RECOGNITION PARTICLE; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; TRANSLOCON;

ACTIN FILAMENT; CELL FRACTIONATION; CODON; COXSACKIE VIRUS B; CROSS LINKING; CYTOPLASM; CYTOSOL; DROSOPHILA; EMBRYO DEVELOPMENT; ENDOPLASMIC RETICULUM; EXOCYTOSIS; GOLGI COMPLEX; INHIBITION KINETICS; NONHUMAN; OOCYTE; PLASMODESMA; PRIORITY JOURNAL; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEIN TARGETING; REVIEW; RIBOSOME; SACCHAROMYCES CEREVISIAE; START CODON; TRANSLATION INITIATION; UNFOLDED PROTEIN RESPONSE; XENOPUS LAEVIS; YEAST CELL;

CORTICAL ER; MRNA TARGETING; P180; PROLAMINE; SIGNAL RECOGNITION PARTICLE;

ANIMALS; ENDOPLASMIC RETICULUM; HUMANS; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RNA, MESSENGER; RNA-BINDING PROTEINS; SIGNAL RECOGNITION PARTICLE;

EID: 84880604441     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.01.013     Document Type: Review

References (94)

1. Blobel G., Walter P., Chang C.N., Goldman B.M., Erickson A.H., Lingappa V.R. Translocation of proteins across membranes: the signal hypothesis and beyond. Symp. Soc. Exp. Biol. 1979, 33:9-36.
2. Siegel V., Walter P. Removal of the Alu structural domain from signal recognition particle leaves its protein translocation activity intact. Nature 1986, 320:81-84.
3. Siegel V., Walter P. Each of the activities of signal recognition particle (SRP) is contained within a distinct domain: analysis of biochemical mutants of SRP. Cell 1988, 52:39-49.
4. Hegde R.S., Keenan R.J. Tail-anchored membrane protein insertion into the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 2011, 12:787-798.
5. Panzner S., Dreier L., Hartmann E., Kostka S., Rapoport T.A. Posttranslational protein transport in yeast reconstituted with a purified complex of Sec proteins and Kar2p. Cell 1995, 81:561-570.
6. Hann B.C., Walter P. The signal recognition particle in S. cerevisiae. Cell 1991, 67:131-144.
7. Mutka S.C., Walter P. Multifaceted physiological response allows yeast to adapt to the loss of the signal recognition particle-dependent protein-targeting pathway. Mol. Biol. Cell 2001, 12:577-588.
8. Pyhtila B., Zheng T., Lager P.J., Keene J.D., Reedy M.C., Nicchitta C.V. Signal sequence- and translation-independent mRNA localization to the endoplasmic reticulum. RNA 2008, 14:445-453.
9. Ren Y.-G., Wagner K.W., Knee D.A., Aza-Blanc P., Nasoff M., Deveraux Q.L. Differential regulation of the TRAIL death receptors DR4 and DR5 by the signal recognition particle. Mol. Biol. Cell 2004, 15:5064-5074.
10. Diehn M., Bhattacharya R., Botstein D., Brown P.O. Genome-scale identification of membrane-associated human mRNAs. PLoS Genet. 2006, 2:e11.
11. Diehn M., Eisen M.B., Botstein D., Brown P.O. Large-scale identification of secreted and membrane-associated gene products using DNA microarrays. Nat. Genet. 2000, 25:58-62.
12. Reid D.W., Nicchitta C.V. Primary role for endoplasmic reticulum-bound ribosomes in cellular translation identified by ribosome profiling. J. Biol. Chem. 2012, 287:5518-5527.
13. Kerekatte V., Keiper B.D., Badorff C., Cai A., Knowlton K.U., Rhoads R.E. Cleavage of Poly(A)-binding protein by coxsackievirus 2A protease in vitro and in vivo: another mechanism for host protein synthesis shutoff?. J. Virol. 1999, 73:709-717.
14. Lamphear B.J., Yan R., Yang F., Waters D., Liebig H.D., Klump H., Kuechler E., Skern T., Rhoads R.E. Mapping the cleavage site in protein synthesis initiation factor eIF-4 gamma of the 2A proteases from human Coxsackievirus and rhinovirus. J. Biol. Chem. 1993, 268:19200-19203.
15. Lerner R.S., Nicchitta C.V. mRNA translation is compartmentalized to the endoplasmic reticulum following physiological inhibition of cap-dependent translation. RNA 2006, 12:775-789.
16. Anderson P., Kedersha N. Stressful initiations. J. Cell Sci. 2002, 115:3227-3234.
17. Unsworth H., Raguz S., Edwards H.J., Higgins C.F., Yague E. mRNA escape from stress granule sequestration is dictated by localization to the endoplasmic reticulum. FASEB J. 2010, 24:3370-3380.
18. Nevo-Dinur K., Nussbaum-Shochat A., Ben-Yehuda S., Amster-Choder O. Translation-independent localization of mRNA in E. coli. Science 2011, 331:1081-1084.
19. Colomina N., Ferrezuelo F., Wang H., Aldea M., Garí E. Whi3, a developmental regulator of budding yeast, binds a large set of mRNAs functionally related to the endoplasmic reticulum. J. Biol. Chem. 2008, 283:28670-28679.
20. Gerber A.P., Herschlag D., Brown P.O. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol. 2004, 2:E79.
21. Hogan D.J., Riordan D.P., Gerber A.P., Herschlag D., Brown P.O. Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol. 2008, 6:e255.
22. Frey S., Pool M., Seedorf M. Scp160p, an RNA-binding, polysome-associated protein, localizes to the endoplasmic reticulum of Saccharomyces cerevisiae in a microtubule-dependent manner. J. Biol. Chem. 2001, 276:15905-15912.
23. Huh W.-K., Falvo J.V., Gerke L.C., Carroll A.S., Howson R.W., Weissman J.S., O'Shea E.K. Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691.
24. Wintersberger U., Kuhne C., Karwan A. Scp160p, a new yeast protein associated with the nuclear membrane and the endoplasmic reticulum, is necessary for maintenance of exact ploidy. Yeast 1995, 11:929-944.
25. Cui X.A., Zhang H., Palazzo A.F. p180 promotes the ribosome-independent localization of a subset of mRNA to the endoplasmic reticulum. PLoS Biol. 2012, 10:e1001336.
26. Savitz A.J., Meyer D.I. Identification of a ribosome receptor in the rough endoplasmic reticulum. Nature 1990, 346:540-544.
27. Görlich D., Prehn S., Hartmann E., Kalies K.U., Rapoport T.A. A mammalian homolog of SEC61p and SECYp is associated with ribosomes and nascent polypeptides during translocation. Cell 1992, 71:489-503.
28. Becker F., Block-Alper L., Nakamura G., Harada J., Wittrup K.D., Meyer D.I. Expression of the 180-kD ribosome receptor induces membrane proliferation and increased secretory activity in yeast. J. Cell Biol. 1999, 146:273-284.
29. Sardet C., Dru P., Prodon F. Maternal determinants and mRNAs in the cortex of ascidian oocytes, zygotes and embryos. Biol. Cell 2005, 97:35-49.
30. Roegiers F., Djediat C., Dumollard R., Rouviere C., Sardet C. Phases of cytoplasmic and cortical reorganizations of the ascidian zygote between fertilization and first division. Development 1999, 126:3101-3117.
31. Speksnijder J.E., Terasaki M., Hage W.J., Jaffe L.F., Sardet C. Polarity and reorganization of the endoplasmic reticulum during fertilization and ooplasmic segregation in the ascidian egg. J. Cell Biol. 1993, 120:1337-1346.
32. Sardet C., Nishida H., Prodon F., Sawada K. Maternal mRNAs of PEM and macho 1, the ascidian muscle determinant, associate and move with a rough endoplasmic reticulum network in the egg cortex. Development 2003, 130:5839-5849.
33. Prodon F., Dru P., Roegiers F., Sardet C. Polarity of the ascidian egg cortex and relocalization of cER and mRNAs in the early embryo. J. Cell Sci. 2005, 118:2393-2404.
34. Sasakura Y., Ogasawara M., Makabe K.W. Two pathways of maternal RNA localization at the posterior-vegetal cytoplasm in early ascidian embryos. Dev. Biol. 2000, 220:365-378.
35. Thomsen G.H., Melton D.A. Processed Vg1 protein is an axial mesoderm inducer in Xenopus. Cell 1993, 74:433-441.
36. Kloc M., Etkin L.D. Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development 1995, 121:287-297.
37. Deshler J.O., Highett M.I., Schnapp B.J. Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum. Science 1997, 276:1128-1131.
38. Kloc M., Etkin L.D. Apparent continuity between the messenger transport organizer and late RNA localization pathways during oogenesis in Xenopus. Mech. Dev. 1998, 73:95-106.
39. Chang P., Torres J., Lewis R.A., Mowry K.L., Houliston E., King M.L. Localization of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. Mol. Biol. Cell 2004, 15:4669-4681.
40. Git A., Allison R., Perdiguero E., Nebreda A.R., Houliston E., Standart N. Vg1RBP phosphorylation by Erk2 MAP kinase correlates with the cortical release of Vg1 mRNA during meiotic maturation of Xenopus oocytes. RNA 2009, 15:1121-1133.
41. Aronov S., Gelin-Licht R., Zipor G., Haim L., Safran E., Gerst J.E. mRNAs encoding polarity and exocytosis factors are cotransported with the cortical endoplasmic reticulum to the incipient bud in Saccharomyces cerevisiae. Mol. Cell. Biol. 2007, 27:3441-3455.
42. Oeffinger M., Wei K.E., Rogers R., DeGrasse J.A., Chait B.T., Aitchison J.D., Rout M.P. Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods 2007, 4:951-956.
43. Shepard K.A., Gerber A.P., Jambhekar A., Takizawa P.A., Brown P.O., Herschlag D., DeRisi J.L., Vale R.D. Widespread cytoplasmic mRNA transport in yeast: identification of 22 bud-localized transcripts using DNA microarray analysis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:11429-11434.
44. Bohl F., Kruse C., Frank A., Ferring D., Jansen R.P. She2p, a novel RNA-binding protein tethers ASH1 mRNA to the Myo4p myosin motor via She3p. EMBO J. 2000, 19:5514-5524.
45. Chartrand P., Singer R.H., Long R.M. RNP localization and transport in yeast. Annu. Rev. Cell Dev. Biol. 2001, 17:297-310.
46. Niessing D., Huttelmaier S., Zenklusen D., Singer R.H., Burley S.K. She2p is a novel RNA binding protein with a basic helical hairpin motif. Cell 2004, 119:491-502.
47. Shen Z., Paquin N., Forget A., Chartrand P. Nuclear shuttling of She2p couples ASH1 mRNA localization to its translational repression by recruiting Loc1p and Puf6p. Mol. Biol. Cell 2009, 20:2265-2275.
48. Du T.G., Jellbauer S., Muller M., Schmid M., Niessing D., Jansen R.P. Nuclear transit of the RNA-binding protein She2 is required for translational control of localized ASH1 mRNA. EMBO Rep. 2008, 9:781-787.
49. Hodges A.R., Krementsova E.B., Trybus K.M. She3p binds to the rod of yeast myosin V and prevents it from dimerizing, forming a single-headed motor complex. J. Biol. Chem. 2008, 283:6906-6914.
50. Heuck A., Fetka I., Brewer D.N., Huls D., Munson M., Jansen R.P., Niessing D. The structure of the Myo4p globular tail and its function in ASH1 mRNA localization. J. Cell Biol. 2010, 189:497-510.
51. Long R.M., Singer R.H., Meng X., Gonzalez I., Nasmyth K., Jansen R.P. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 1997, 277:383-387.
52. Estrada P., Kim J., Coleman J., Walker L., Dunn B., Takizawa P., Novick P., Ferro-Novick S. Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 2003, 163:1255-1266.
53. Gelin-Licht R., Paliwal S., Conlon P., Levchenko A., Gerst J.E. Scp160-dependent mRNA trafficking mediates pheromone gradient sensing and chemotropism in yeast. Cell Rep. 2012, 1:483-494.
54. Preuss D., Mulholland J., Kaiser C.A., Orlean P., Albright C., Rose M.D., Robbins P.W., Botstein D. Structure of the yeast endoplasmic reticulum: localization of ER proteins using immunofluorescence and immunoelectron microscopy. Yeast 1991, 7:891-911.
55. Prinz W.A., Grzyb L., Veenhuis M., Kahana J.A., Silver P.A., Rapoport T.A. Mutants affecting the structure of the cortical endoplasmic reticulum in Saccharomyces cerevisiae. J. Cell Biol. 2000, 150:461-474.
56. Du Y., Ferro-Novick S., Novick P. Dynamics and inheritance of the endoplasmic reticulum. J. Cell Sci. 2004, 117:2871-2878.
57. Fehrenbacher K.L., Davis D., Wu M., Boldogh I., Pon L.A. Endoplasmic reticulum dynamics, inheritance, and cytoskeletal interactions in budding yeast. Mol. Biol. Cell 2002, 13:854-865.
58. West M., Zurek N., Hoenger A., Voeltz G.K. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J. Cell Biol. 2011, 193:333-346.
59. Schmid M., Jaedicke A., Du T.G., Jansen R.P. Coordination of endoplasmic reticulum and mRNA localization to the yeast bud. Curr. Biol. 2006, 16:1538-1543.
60. TerBush D.R., Maurice T., Roth D., Novick P. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 1996, 15:6483-6494.
61. Ogg S.C., Poritz M.A., Walter P. Signal recognition particle receptor is important for cell growth and protein secretion in Saccharomyces cerevisiae. Mol. Biol. Cell 1992, 3:895-911.
62. Fundakowski J., Hermesh O., Jansen R.P. Localization of a subset of yeast mRNAs depends on inheritance of endoplasmic reticulum. Traffic 2012, 13:1642-1652.
63. Pishvaee B., Costaguta G., Yeung B.G., Ryazantsev S., Greener T., Greene L.E., Eisenberg E., McCaffery J.M., Payne G.S. A yeast DNA J protein required for uncoating of clathrin-coated vesicles in vivo. Nat. Cell Biol. 2000, 2:958-963.
64. Du Y., Pypaert M., Novick P., Ferro-Novick S. Aux1p/Swa2p is required for cortical endoplasmic reticulum inheritance in Saccharomyces cerevisiae. Mol. Biol. Cell 2001, 12:2614-2628.
65. De Craene J.O., Coleman J., Estrada de Martin P., Pypaert M., Anderson S., Yates J.R., Ferro-Novick S., Novick P. Rtn1p is involved in structuring the cortical endoplasmic reticulum. Mol. Biol. Cell 2006, 17:3009-3020.
66. Voeltz G.K., Prinz W.A., Shibata Y., Rist J.M., Rapoport T.A. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 2006, 124:573-586.
67. Guo M., Aston C., Burchett S.A., Dyke C., Fields S., Rajarao S.J., Uetz P., Wang Y., Young K., Dohlman H.G. The yeast G protein alpha subunit Gpa1 transmits a signal through an RNA binding effector protein Scp160. Mol. Cell 2003, 12:517-524.
68. Lang B.D., Fridovich-Keil J.L. Scp160p, a multiple KH-domain protein, is a component of mRNP complexes in yeast. Nucleic Acids Res. 2000, 28:1576-1584.
69. Krishnan H.B., Franceschi V.R., Okita T.W. Immunochemical studies on the role of the Golgi complex in protein-body formation in rice seeds. Planta 1986, 169:471-480.
70. Yamagata H., Tanaka K. The site of synthesis and accumulation of rice storage proteins. Plant Cell Physiol. 1986, 27:135-145.
71. Li X., Franceschi V.R., Okita T.W. Segregation of storage protein mRNAs on the rough endoplasmic reticulum membranes of rice endosperm cells. Cell 1993, 72:869-879.
72. Choi S.B., Wang C., Muench D.G., Ozawa K., Franceschi V.R., Wu Y., Okita T.W. Messenger RNA targeting of rice seed storage proteins to specific ER subdomains. Nature 2000, 407:765-767.
73. Hamada S., Ishiyama K., Choi S.B., Wang C., Singh S., Kawai N., Franceschi V.R., Okita T.W. The transport of prolamine RNAs to prolamine protein bodies in living rice endosperm cells. Plant Cell 2003, 15:2253-2264.
74. Crofts A.J., Crofts N., Whitelegge J.P., Okita T.W. Isolation and identification of cytoskeleton-associated prolamine mRNA binding proteins from developing rice seeds. Planta 2010, 231:1261-1276.
75. Washida H., Sugino A., Doroshenk K.A., Satoh-Cruz M., Nagamine A., Katsube-Tanaka T., Ogawa M., Kumamaru T., Satoh H., Okita T.W. RNA targeting to a specific ER sub-domain is required for efficient transport and packaging of alpha-globulins to the protein storage vacuole in developing rice endosperm. Plant J. 2012, 70:471-479.
76. Satoh-Cruz M., Crofts A.J., Takemoto-Kuno Y., Sugino A., Washida H., Crofts N., Okita T.W., Ogawa M., Satoh H., Kumamaru T. Protein disulfide isomerase like 1-1 participates in the maturation of proglutelin within the endoplasmic reticulum in rice endosperm. Plant Cell Physiol. 2010, 51:1581-1593.
77. Takemoto Y., Coughlan S.J., Okita T.W., Satoh H., Ogawa M., Kumamaru T. The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiol. 2002, 128:1212-1222.
78. Wang C., Washida H., Crofts A.J., Hamada S., Katsube-Tanaka T., Kim D., Choi S.B., Modi M., Singh S., Okita T.W. The cytoplasmic-localized, cytoskeletal-associated RNA binding protein OsTudor-SN: evidence for an essential role in storage protein RNA transport and localization. Plant J. 2008, 55:443-454.
79. Neuman-Silberberg F.S., Schupbach T. The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGF alpha-like protein. Cell 1993, 75:165-174.
80. Barlowe C., Orci L., Yeung T., Hosobuchi M., Hamamoto S., Salama N., Rexach M.F., Ravazzola M., Amherdt M., Schekman R. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 1994, 77:895-907.
81. Bonifacino J.S., Glick B.S. The mechanisms of vesicle budding and fusion. Cell 2004, 116:153-166.
82. Herpers B., Rabouille C. mRNA localization and ER-based protein sorting mechanisms dictate the use of transitional endoplasmic reticulum-golgi units involved in gurken transport in Drosophila oocytes. Mol. Biol. Cell 2004, 15:5306-5317.
83. Wodarz A., Nusse R. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 1998, 14:59-88.
84. Simmonds A.J., dosSantos G., Livne-Bar I., Krause H.M. Apical localization of wingless transcripts is required for wingless signaling. Cell 2001, 105:197-207.
85. Hetz C., Glimcher L.H. Fine-tuning of the unfolded protein response: assembling the IRE1alpha interactome. Mol. Cell 2009, 35:551-561.
86. Schroder M., Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 2005, 74:739-789.
87. Cox J.S., Walter P. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 1996, 87:391-404.
88. Kawahara T., Yanagi H., Yura T., Mori K. Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response. Mol. Biol. Cell 1997, 8:1845-1862.
89. Aragon T., van Anken E., Pincus D., Serafimova I.M., Korennykh A.V., Rubio C.A., Walter P. Messenger RNA targeting to endoplasmic reticulum stress signalling sites. Nature 2009, 457:736-740.
90. Yanagitani K., Imagawa Y., Iwawaki T., Hosoda A., Saito M., Kimata Y., Kohno K. Cotranslational targeting of XBP1 protein to the membrane promotes cytoplasmic splicing of its own mRNA. Mol. Cell 2009, 34:191-200.
91. Lucas W.J. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 2006, 344:169-184.
92. Lough T.J., Netzler N.E., Emerson S.J., Sutherland P., Carr F., Beck D.L., Lucas W.J., Forster R.L. Cell-to-cell movement of potexviruses: evidence for a ribonucleoprotein complex involving the coat protein and first triple gene block protein. Mol. Plant Microbe Interact. 2000, 13:962-974.
93. Morozov S.Y., Solovyev A.G. Triple gene block: modular design of a multifunctional machine for plant virus movement. J. Gen. Virol. 2003, 84:1351-1366.
94. Wu C.H., Lee S.C., Wang C.W. Viral protein targeting to the cortical endoplasmic reticulum is required for cell-cell spreading in plants. J. Cell Biol. 2011, 193:521-535.