Localization of a subset of yeast mRNAs depends on inheritance of endoplasmic reticulum

Traffic

Volumn 13, Issue 12, 2012, Pages 1642-1652

  Fundakowski, Julia ^a   Hermesh, Orit ^a   Jansen, Ralf Peter ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Budding yeast; Cortical ER; Endoplasmic reticulum; mRNA localization

Indexed keywords

ASH1 PROTEIN; FUNGAL PROTEIN; MESSENGER RNA; RIBONUCLEOPROTEIN; SHE1 PROTEIN; SHE2 PROTEIN; SHE3 PROTEIN; UNCLASSIFIED DRUG; EXOCYST; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; CELL BUDDING; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; INHERITANCE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; SEGREGATION ANALYSIS; YEAST; AMINO TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; FUNGAL CELL WALL; PROMOTER REGION; PROTEIN EXPRESSION; RNA TRANSPORT; START CODON; YEAST CELL;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; CELL DIVISION; ENDOPLASMIC RETICULUM; G2 PHASE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; REPRESSOR PROTEINS; RIBONUCLEOPROTEINS; RNA TRANSPORT; RNA, MESSENGER; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84873273578     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12011     Document Type: Article

References (66)

1. Du T-G, Schmid M, Jansen R-P. Why cells move messages: the biological functions of mRNA localization. Semin Cell Dev Biol 2007;18:171-177.
2. Holt CE, Bullock SL. Subcellular mRNA localization in animal cells and why it matters. Science 2009;326:1212-1216.
3. Martin KC, Ephrussi A. mRNA localization: gene expression in the spatial dimension. Cell 2009;136:719-730.
4. Besse F, Ephrussi A. Translational control of localized mRNAs: restricting protein synthesis in space and time. Nat Rev Mol Cell Biol 2008;9:971-980.
5. Paquin N, Chartrand P. Local regulation of mRNA translation: new insights from the bud. Trends Cell Biol 2008;18:105-111.
6. Chartrand P, Singer RH, Long RM. RNP localization and transport in yeast. Annu Rev Cell Dev Biol 2001;17:297-310.
7. Long RM, Singer RH, Meng X, Gonzalez I, Nasmyth K, Jansen RP. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 1997;277:383-387.
8. Aronov S, Gelin-Licht R, Zipor G, Haim L, Safran E, Gerst JE. 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.
9. Oeffinger M, Wei KE, Rogers R, DeGrasse JA, Chait BT, Aitchison JD, Rout MP. Comprehensive analysis of diverse ribonucleoprotein complexes. Nat Methods 2007;4:951-956.
10. Shepard KA, Gerber AP, Jambhekar A, Takizawa PA, Brown PO, Herschlag D, DeRisi JL, Vale RD. 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.
11. Böhl F, Kruse C, Frank A, Ferring D, Jansen RP. She2p, a novel RNAbinding protein tethers ASH1 mRNA to the Myo4p myosin motor via She3p. EMBO J 2000;19:5514-5524.
12. Niessing D, Hüttelmaier S, Zenklusen D, Singer RH, Burley SK. She2p is a novel RNA binding protein with a basic helical hairpin motif. Cell 2004;119:491-502.
13. Shen Z, St-Denis A, Chartrand P. Cotranscriptional recruitment of She2p by RNA pol II elongation factor Spt4-Spt5/DSIF promotes mRNA localization to the yeast bud. Genes Dev 2010; 24:1914-1926.
14. Du T-G, Jellbauer S, Müller 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.
15. 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.
16. Heuck A, Fetka I, Brewer DN, Hüls 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.
17. Hodges AR, Krementsova EB, Trybus KM. She3p binds to the rod of yeast myosin V and prevents it from dimerizing, forming a singleheaded motor complex. J Biol Chem 2008;283:6906-6914.
18. Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM. Localization of ASH1 mRNA particles in living yeast. Mol Cell 1998;2:437-445.
19. Gu W, Deng Y, Zenklusen D, Singer RH. A new yeast PUF family protein, Puf6p, represses ASH1 mRNA translation and is required for its localization. Genes Dev 2004;18:1452-1465.
20. Irie K, Tadauchi T, Takizawa PA, Vale RD, Matsumoto K, Herskowitz I. The Khd1 protein, which has three KH RNA-binding motifs, is required for proper localization of ASH1 mRNA in yeast. EMBO J 2002;21:1158-1167.
21. Long RM, Gu W, Meng X, Gonsalvez G, Singer RH, Chartrand P. An exclusively nuclear RNA-binding protein affects asymmetric localization of ASH1 mRNA and Ash1p in yeast. J Cell Biol 2001;153:307-318.
22. Paquin N, Ménade M, Poirier G, Donato D, Drouet E, Chartrand P. Local activation of yeast ASH1 mRNA translation through phosphorylation of Khd1p by the casein kinase Yck1p. Mol Cell 2007;26:795-809.
23. 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.
24. Du Y, Ferro-Novick S, Novick P. Dynamics and inheritance of the endoplasmic reticulum. J Cell Sci 2004;117(Pt 14):2871-2878.
25. West M, Zurek N, Hoenger A, Voeltz GK. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J Cell Biol 2011;193:333-346.
26. Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 2006;124:573-586.
27. Hu J, Shibata Y, Voss C, Shemesh T, Li Z, Coughlin M, Kozlov MM, Rapoport TA, Prinz WA. Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 2008;319:1247-1250.
28. Du Y, Walker L, Novick P, Ferro-Novick S. Ptc1p regulates cortical ER inheritance via Slt2p. EMBO J 2006;25:4413-4422.
29. Wiederkehr A, Du Y, Pypaert M, Ferro-Novick S, Novick P. Sec3p is needed for the spatial regulation of secretion and for the inheritance of the cortical endoplasmic reticulum. Mol Biol Cell 2003;14:4770-4782.
30. Pishvaee B, Costaguta G, Yeung BG, Ryazantsev S, Greener T, Greene LE, Eisenberg E, McCaffery JM, Payne GS. A yeast DNA J protein required for uncoating of clathrin-coated vesicles in vivo. Nat Cell Biol 2000;2:958-963.
31. 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.
32. 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.
33. Lange S, Katayama Y, Schmid M, Burkacky O, Bräuchle C, Lamb DC, Jansen R-P. Simultaneous transport of different localized mRNA species revealed by live-cell imaging. Traffic 2008;9:1256-1267.
34. Slobodin B, Gerst JE. A novel mRNA affinity purification technique for the identification of interacting proteins and transcripts in ribonucleoprotein complexes. RNA (New York, NY) 2010; 16:2277-2290.
35. Haim L, Zipor G, Aronov S, Gerst JE. A genomic integration method to visualize localization of endogenous mRNAs in living yeast. Nat Methods 2007;4:409-412.
36. Verna J, Lodder A, Lee K, Vagts A, Ballester R. A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 1997;94:13804-13809.
37. Léon S, Erpapazoglou Z, Haguenauer-Tsapis R. Ear1p and Ssh4p are new adaptors of the ubiquitin ligase Rsp5p for cargo ubiquitylation and sorting at multivesicular bodies. Mol Biol Cell 2008;19:2379-2388.
38. Terashima H, Fukuchi S, Nakai K, Arisawa M, Hamada K, Yabuki N, Kitada K. Sequence-based approach for identification of cell wall proteins in Saccharomyces cerevisiae. Curr Genet 2002;40:311-316.
39. Ercan E, Momburg F, Engel U, Temmerman K, Nickel W, Seedorf M. A conserved, lipid-mediated sorting mechanism of yeast Ist2 and mammalian STIM proteins to the peripheral ER. Traffic 2009;10:1802-1818.
40. Takizawa PA, DeRisi JL, Wilhelm JE, Vale RD. Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science 2000;290:341-344.
41. Bobola N, Jansen RP, Shin TH, Nasmyth K. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells. Cell 1996;84:699-709.
42. Loewen CJR, Young BP, Tavassoli S, Levine TP. Inheritance of cortical ER in yeast is required for normal septin organization. J Cell Biol 2007;179:467-483.
43. He B, GuoW. The exocyst complex in polarized exocytosis. Curr Opin Cell Biol 2009;21:537-542.
44. Reinke CA, Kozik P, Glick BS. Golgi inheritance in small buds of Saccharomyces cerevisiae is linked to endoplasmic reticulum inheritance. Proc Natl Acad Sci U S A 2004;101:18018-18023.
45. Li X, Du Y, Siegel S, Ferro-Novick S, Novick P. Activation of the mitogen-activated protein kinase, Slt2p, at bud tips blocks a late stage of endoplasmic reticulum inheritance in Saccharomyces cerevisiae. Mol Biol Cell 2010;21:1772-1782.
46. Hu J, Shibata Y, Zhu P-P, Voss C, Rismanchi N, Prinz WA, Rapoport TA, Blackstone C. A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell 2009;138:549-561.
47. Shan S-o, Walter P. Co-translational protein targeting by the signal recognition particle. FEBS Lett 2005;579:921-926.
48. Lerner RS, Nicchitta CV. mRNA translation is compartmentalized to the endoplasmic reticulum following physiological inhibition of capdependent translation. RNA 2006;12:775-789.
49. Pyhtila B, Zheng T, Lager PJ, Keene JD, Reedy MC, Nicchitta CV. Signal sequence- and translation-independent mRNA localization to the endoplasmic reticulum. RNA 2008;14:445-453.
50. Kraut-Cohen J, Gerst JE. Addressing mRNAs to the ER: cis sequences act up. Trends Biochem Sci 2010; 35:459-469.
51. Cui XA, Zhang H, Palazzo AF. p180 Promotes the Ribosome- Independent Localization of a Subset of mRNA to the Endoplasmic Reticulum. PLoS Biol 2012;10:e1001336.
52. Frey S, Pool M, Seedorf M. Scp160p, an RNA-binding, polysomeassociated protein, localizes to the endoplasmic reticulum of Saccharomyces cerevisiae in a microtubule-dependent manner. J Biol Chem 2001;276:15905-15912.
53. Lang BD, Am L, Black-Brewster HD, Fridovich-Keil JL. The brefeldin A resistance protein Bfr1p is a component of polyribosome-associated mRNP complexes in yeast. Nucleic Acids Res 2001;29:2567-2574.
54. Shibata Y, Shemesh T, Prinz WA, Palazzo AF, Kozlov MM, Rapoport TA. Mechanisms determining the morphology of the peripheral ER. Cell 2010;143:774-788.
55. Müller M, Heym RG, Mayer A, Kramer K, Schmid M, Cramer P, Urlaub H, Jansen R-P, Niessing D. A cytoplasmic complex mediates specific mRNA recognition and localization in yeast. PLoS Biol 2011;9:e1000611.
56. Gonzalez I, Buonomo SB, Nasmyth K, von Ahsen U. ASH1 mRNA localization in yeast involves multiple secondary structural elements and Ash1 protein translation. Curr Biol 1999;9:337-340.
57. Calero M, Whittaker GR, Collins RN. Yop1p, the yeast homolog of the polyposis locus protein 1, interacts with Yip1p and negatively regulates cell growth. J Biol Chem 2001;276:12100-12112.
58. Deshler JO, Highett MI, Schnapp BJ. Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum. Science 1997;276:1128-1131.
59. Wilhelm JE, BuszczakM, Sayles S. Efficient protein trafficking requires trailer hitch, a component of a ribonucleoprotein complex localized to the ER in Drosophila. Dev Cell 2005;9:675-685.
60. Crofts AJ, Washida H, Okita TW, Ogawa M, Kumamaru T, Satoh H. Targeting of proteins to endoplasmic reticulum-derived compartments in plants. The importance of RNA localization. Plant Physiol 2004;136:3414-3419.
61. Wach A, Brachat A, Pöhlmann R, Philippsen P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast (Chichester, England) 1994;10:1793-1808.
62. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, Moreno-Borchart A, Doenges G, Schwob E, Schiebel E, Knop M. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 2004;21:947-962.
63. Gietz RD, Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 1988;74:527-534.
64. Heckman KL, Pease LR. Gene splicing and mutagenesis by PCR-driven overlap extension. Nat Protoc 2007;2:924-932.
65. Li MZ, Elledge SJ. Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. Nat Methods 2007;4:251-256.
66. Cross FR, Tinkelenberg AH. A potential positive feedback loop controlling CLN1 and CLN2 gene expression at the start of the yeast cell cycle. Cell 1991;65:875-883. 1652