The Deoxyhypusine Synthase Mutant dys1-1 Reveals the Association of eIF5A and Asc1 with Cell Wall Integrity

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Galvão, Fabio Carrilho ^a   Rossi, Danuza ^a   Silveira, Wagner da Silva ^a   Valentini, Sandro Roberto ^a   Zanelli, Cleslei Fernando ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYHYPUSINE SYNTHASE; DEOXYHYPUSINE SYNTHASE 1; DEOXYHYPUSINE SYNTHASE 1 1; FUNGAL PROTEIN; HYPUSINE; INITIATION FACTOR 5A; PROTEIN ASC1; PROTEIN KINASE C; SORBITOL; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; ASC1 GENE; BINDING AFFINITY; CELL GROWTH; CELL WALL; CELL WALL INTEGRITY; CONTROLLED STUDY; CYTOLYSIS; DEOXYHYPUSINE SYNTHASE 1 GENE; EUKARYOTIC TRANSLATION INITIATION FACTOR 5A GENE; GENE; GENE FUNCTION; GENE INTERACTION; GENE OVEREXPRESSION; GENETIC IDENTIFICATION; MUTANT; NONHUMAN; OSMOSIS; POLYSOME; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN KINASE C GENE; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RIBOSOME; RNA TRANSLATION; SENSITIVITY ANALYSIS; TRANSLATION REGULATION; WILD TYPE; YEAST;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL WALL; EPISTASIS, GENETIC; GENE EXPRESSION REGULATION, FUNGAL; GTP-BINDING PROTEINS; LYSINE; MUTATION, MISSENSE; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PEPTIDE INITIATION FACTORS; POLYRIBOSOMES; PROTEIN BINDING; PROTEIN KINASE C; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84875686470     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060140     Document Type: Article

References (53)

1. Acker MG, Kolitz SE, Mitchell SF, Nanda JS, Lorsch JR, (2007) Reconstitution of yeast translation initiation. Methods Enzymol 430: 111-145.
2. Kang HA, Hershey JW, (1994) Effect of initiation factor eIF-5A depletion on protein synthesis and proliferation of Saccharomyces cerevisiae. J Biol Chem 269: 3934-3940.
3. Zuk D, Jacobson A, (1998) A single amino acid substitution in yeast eIF-5A results in mRNA stabilization. Embo Journal 17: 2914-2925.
4. Park MH, Lee YB, Joe YA, (1997) Hypusine is essential for eukaryotic cell proliferation. Biological Signals 6: 115-123.
5. Valentini SR, Casolari JM, Oliveira CC, Silver PA, McBride AE, (2002) Genetic interactions of yeast eukaryotic translation initiation factor 5A (eIF5A) reveal connections to poly(A)-binding protein and protein kinase C signaling. Genetics 160: 393-405.
6. Gregio AP, Cano VP, Avaca JS, Valentini SR, Zanelli CF, (2009) eIF5A has a function in the elongation step of translation in yeast. Biochem Biophys Res Commun 380: 785-790.
7. Peltz SW, Donahue JL, Jacobson A, (1992) A mutation in the tRNA nucleotidyltransferase gene promotes stabilization of mRNAs in Saccharomyces cerevisiae. Mol Cell Biol 12: 5778-5784.
8. Ruhl M, Himmelspach M, Bahr GM, Hammerschmid F, Jaksche H, et al. (1993) Eukaryotic initiation factor 5A is a cellular target of the human immunodeficiency virus type 1 Rev activation domain mediating trans-activation. J Cell Biol 123: 1309-1320.
9. Bevec D, Jaksche H, Oft M, Wohl T, Himmelspach M, et al. (1996) Inhibition of HIV-1 replication in lymphocytes by mutants of the Rev cofactor eIF-5A. Science 271: 1858-1860.
10. Rosorius O, Reichart B, Kratzer F, Heger P, Dabauvalle MC, et al. (1999) Nuclear pore localization and nucleocytoplasmic transport of eIF-5A: evidence for direct interaction with the export receptor CRM1. J Cell Sci 112 (Pt 14): 2369-2380.
11. Henderson BR, Percipalle P, (1997) Interactions between HIV Rev and nuclear import and export factors: the Rev nuclear localisation signal mediates specific binding to human importin-beta. J Mol Biol 274: 693-707.
12. Shi XP, Yin KC, Waxman L, (1997) Effects of inhibitors of RNA and protein synthesis on the subcellular distribution of the eukaryotic translation initiation factor, eIF-5A, and the HIV-1 Rev protein. Biol Signals 6: 143-149.
13. Lipowsky G, Bischoff FR, Schwarzmaier P, Kraft R, Kostka S, et al. (2000) Exportin 4: a mediator of a novel nuclear export pathway in higher eukaryotes. Embo J 19: 4362-4371.
14. Jao DL, Yu Chen K, (2002) Subcellular localization of the hypusine-containing eukaryotic initiation factor 5A by immunofluorescent staining and green fluorescent protein tagging. J Cell Biochem 86: 590-600.
15. Henderson A, Hershey JW, (2011) Eukaryotic translation initiation factor (eIF) 5A stimulates protein synthesis in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America 108: 6415-6419.
16. Jao DLE, Chen KY, (2006) Tandem affinity purification revealed the hypusine-dependent binding of eukaryotic initiation factor 5A to the translating 80S ribosomal complex. Journal of Cellular Biochemistry 97: 583-598.
17. Zanelli CF, Maragno AL, Gregio AP, Komili S, Pandolfi JR, et al. (2006) eIF5A binds to translational machinery components and affects translation in yeast. Biochem Biophys Res Commun 348: 1358-1366.
18. Dias CA, Gregio AP, Rossi D, Galvão FC, Watanabe TF, et al. (2011) eIF5A interacts functionally with eEF2. Amino Acids.
19. Saini P, Eyler DE, Green R, Dever TE, (2009) Hypusine-containing protein eIF5A promotes translation elongation. Nature 459: 118-121.
20. Kim KK, Hung LW, Yokota H, Kim R, Kim SH, (1998) Crystal structures of eukaryotic translation initiation factor 5A from Methanococcus jannaschii at 1.8 A resolution. Proc Natl Acad Sci U S A 95: 10419-10424.
21. Peat TS, Newman J, Waldo GS, Berendzen J, Terwilliger TC, (1998) Structure of translation initiation factor 5A from Pyrobaculum aerophilum at 1.75 A resolution. Structure 6: 1207-1214.
22. Tong Y, Park I, Hong BS, Nedyalkova L, Tempel W, et al. (2009) Crystal structure of human eIF5A1: insight into functional similarity of human eIF5A1 and eIF5A2. Proteins 75: 1040-1045.
23. Yao M, Ohsawa A, Kikukawa S, Tanaka I, Kimura M, (2003) Crystal structure of hyperthermophilic archaeal initiation factor 5A: A homologue of eukaryotic initiation factor 5A (eIF-5A). Journal of Biochemistry 133: 75-81.
24. Park MH, (2006) The Post-Translational Synthesis of a Polyamine-Derived Amino Acid, Hypusine, in the Eukaryotic Translation Initiation Factor 5A (eIF5A). J Biochem (Tokyo) 139: 161-169.
25. Thompson GM, Cano VSP, Valentini SR, (2003) Mapping eIF5A binding sites for Dys1 and Lia1: in vivo evidence for regulation of eIF5A hypusination. Febs Letters 555: 464-468.
26. Dias CA, Cano VS, Rangel SM, Apponi LH, Frigieri MC, et al. (2008) Structural modeling and mutational analysis of yeast eukaryotic translation initiation factor 5A reveal new critical residues and reinforce its involvement in protein synthesis. Febs J 275: 1874-1888.
27. Levin DE, (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189: 1145-1175.
28. Krause SA, Gray JV, (2002) The protein kinase C pathway is required for viability in quiescence in Saccharomyces cerevisiae. Curr Biol 12: 588-593.
29. Melamed D, Bar-Ziv L, Truzman Y, Arava Y, (2010) Asc1 supports cell-wall integrity near bud sites by a Pkc1 independent mechanism. PLoS One 5: e11389.
30. Gerbasi VR, Weaver CM, Hill S, Friedman DB, Link AJ, (2004) Yeast Asc1p and mammalian RACK1 are functionally orthologous core 40S ribosomal proteins that repress gene expression. Mol Cell Biol 24: 8276-8287.
31. Zeller CE, Parnell SC, Dohlman HG, (2007) The RACK1 ortholog Asc1 functions as a G-protein beta subunit coupled to glucose responsiveness in yeast. J Biol Chem 282: 25168-25176.
32. Chantrel Y, Gaisne M, Lions C, Verdière J, (1998) The transcriptional regulator Hap1p (Cyp1p) is essential for anaerobic or heme-deficient growth of Saccharomyces cerevisiae: Genetic and molecular characterization of an extragenic suppressor that encodes a WD repeat protein. Genetics 148: 559-569.
33. Kiss-László Z, Henry Y, Bachellerie JP, Caizergues-Ferrer M, Kiss T, (1996) Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell 85: 1077-1088.
34. Coyle SM, Gilbert WV, Doudna JA, (2009) Direct link between RACK1 function and localization at the ribosome in vivo. Mol Cell Biol 29: 1626-1634.
35. Kuroha K, Akamatsu M, Dimitrova L, Ito T, Kato Y, et al. (2010) Receptor for activated C kinase 1 stimulates nascent polypeptide-dependent translation arrest. EMBO Rep 11: 956-961.
36. Kouba T, Rutkai E, Karásková M, Valášek L, (2012) The eIF3c/NIP1 PCI domain interacts with RNA and RACK1/ASC1 and promotes assembly of translation preinitiation complexes. Nucleic Acids Res 40: 2683-2699.
37. Park MH, Nishimura K, Zanelli CF, Valentini SR, (2010) Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids 38: 491-500.
38. Dever TE, Green R (2012) The elongation, termination, and recycling phases of translation in eukaryotes. Cold Spring Harb Perspect Biol 4.
39. Jao DL, Chen KY, (2006) Tandem affinity purification revealed the hypusine-dependent binding of eukaryotic initiation factor 5A to the translating 80S ribosomal complex. J Cell Biochem 97: 583-598.
40. Zanelli CF, Valentini SR, (2005) Pkc1 acts through Zds1 and Gic1 to suppress growth and cell polarity defects of a yeast eIF5A mutant. Genetics 171: 1571-1581.
41. Rachfall N, Schmitt K, Bandau S, Smolinski N, Ehrenreich A, et al. (2013) RACK1/Asc1p, a Ribosomal Node in Cellular Signaling. Mol Cell Proteomics 12: 87-105.
42. Bearson SM, Bearson BL, Brunelle BW, Sharma VK, Lee IS, (2011) A mutation in the poxA gene of Salmonella enterica serovar Typhimurium alters protein production, elevates susceptibility to environmental challenges, and decreases swine colonization. Foodborne Pathog Dis 8: 725-732.
43. Kaniga K, Compton MS, Curtiss R, Sundaram P, (1998) Molecular and functional characterization of Salmonella enterica serovar typhimurium poxA gene: effect on attenuation of virulence and protection. Infect Immun 66: 5599-5606.
44. Navarre WW, Zou SB, Roy H, Xie JL, Savchenko A, et al. (2010) PoxA, yjeK, and elongation factor P coordinately modulate virulence and drug resistance in Salmonella enterica. Mol Cell 39: 209-221.
45. Peng WT, Banta LM, Charles TC, Nester EW, (2001) The chvH locus of Agrobacterium encodes a homologue of an elongation factor involved in protein synthesis. J Bacteriol 183: 36-45.
46. Zou SB, Roy H, Ibba M, Navarre WW, (2011) Elongation factor P mediates a novel post-transcriptional regulatory pathway critical for bacterial virulence. Virulence 2: 147-151.
47. Zou SB, Hersch SJ, Roy H, Wiggers JB, Leung AS, et al. (2012) Loss of elongation factor P disrupts bacterial outer membrane integrity. J Bacteriol 194: 413-425.
48. Ude S, Lassak J, Starosta AL, Kraxenberger T, Wilson DN, et al. (2013) Translation elongation factor EF-P alleviates ribosome stalling at polyproline stretches. Science 339: 82-85.
49. Doerfel LK, Wohlgemuth I, Kothe C, Peske F, Urlaub H, et al. (2013) EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 339: 85-88.
50. Yu L, Peña Castillo L, Mnaimneh S, Hughes TR, Brown GW, (2006) A survey of essential gene function in the yeast cell division cycle. Mol Biol Cell 17: 4736-4747.
51. Guthrie C, Fink GRE (1991) Guide to Yeast Genetics. Academic Press, New York, NY.
52. Kang HA, Schwelberger HG, Hershey JW, (1993) Translation initiation factor eIF-5A, the hypusine-containing protein, is phosphorylated on serine in Saccharomyces cerevisiae. J Biol Chem 268: 14750-14756.
53. Lorsh J (2007). Methods in enzymology. In: Bumjun Lee, Tsuyoshi Udagawa, Chingakham Ranjit Singh, and Katsura Asano. Yeast Phenotypic Assays on Translational Control. 105-137.