eIF4F-like complexes formed by cap-binding homolog TbEIF4E5 with TbEIF4G1 or TbEIF4G2 are implicated in post-transcriptional regulation in Trypanosoma brucei

RNA

Volumn 20, Issue 8, 2014, Pages 1272-1286

  Freire, Eden R ^a   Vashisht, Ajay A ^a   Malvezzi, Amaranta M ^a,b   Zuberek, Joanna ^c   Langousis, Gerasimos ^a   Saada, Edwin A ^a   Nascimento, Janaína De F ^b   Stepinski, Janusz ^c   Darzynkiewicz, Edward ^c,d   Hill, Kent ^a   De Melo Neto, Osvaldo P ^b   Wohlschlegel, James A ^a   Sturm, Nancy R ^a   Campbell, David A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c UNIVERSITY OF WARSAW   (Poland)

^d UNIVERSITY OF WARSAW   (Poland)

Author keywords

14 3 3 protein; Kinetoplastid; mRNA cap; Social motility; Translation initiation factor

Indexed keywords

CAP BINDING PROTEIN; GUANYLYLTRANSFERASE; INITIATION FACTOR 4F; METHYLTRANSFERASE; PROTEIN 14 3 3; PROTEIN EIF4E5; PROTEIN EIF4G1; PROTEIN EIF4G2; PROTEIN VARIANT; TRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CELL MOTILITY; CELL MOTION; CONTROLLED STUDY; GENE EXPRESSION; GENE INACTIVATION; IN VITRO STUDY; KINETOPLASTIDA; LIQUID CULTURE; MOLECULAR WEIGHT; NONHUMAN; PLATING MEDIUM; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PURIFICATION; PROTEIN RNA BINDING; SEQUENCE HOMOLOGY; SUSPENSION; TRANSCRIPTION REGULATION; TRYPANOSOMA BRUCEI;

14-3-3 PROTEIN; KINETOPLASTID; MRNA CAP; SOCIAL MOTILITY; TRANSLATION INITIATION FACTOR;

AMINO ACID SEQUENCE; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTOR-4G; GENE KNOCKOUT TECHNIQUES; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RNA CAP-BINDING PROTEINS; RNA CAPS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, PROTOZOAN; SEQUENCE ALIGNMENT; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84904498737     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.045534.114     Document Type: Article

References (99)

1. Adl SM, Simpson AG, Lane CE, Lukes J, Bass D, Bowser SS, Brown MW, Burki F, Dunthorn M, Hampl V, et al. 2012. The revised classification of eukaryotes. J Eukaryot Microbiol 59: 429-493.
2. Aitken CE, Lorsch JR. 2012. A mechanistic overview of translation initiation in eukaryotes. Nat Struct Mol Biol 19: 568-576.
3. Alsford S, Turner DJ, Obado SO, Sanchez-Flores A, Glover L, Berriman M, Hertz-Fowler C, Horn D. 2011. High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res 21: 915-924.
4. Alsford S, duBois K, Horn D, Field MC. 2012. Epigenetic mechanisms, nuclear architecture and the control of gene expression in trypanosomes. Expert Rev Mol Med 14: e13.
5. Ammerman ML, Downey KM, Hashimi H, Fisk JC, Tomasello DL, Faktorova D, Kafkova L, King T, Lukes J, Read LK. 2012. Architecture of the trypanosome RNA editing accessory complex, MRB1. Nucleic Acids Res 40: 5637-5650.
6. Andrei MA, Ingelfinger D, Heintzmann R, Achsel T, Rivera-Pomar R, Luhrmann R. 2005. A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA 11: 717-727. (Pubitemid 40594337)
7. Badjatia N, Ambrosio DL, Lee JH, Gunzl A. 2013. Trypanosome cdc2-related kinase 9 controls spliced leader RNA cap4 methylation and phosphorylation of RNA polymerase II subunit RPB1. Mol Cell Biol 33: 1965-1975.
8. Banerjee H, Palenchar JB, Lukaszewicz M, Bojarska E, Stepinski J, Jemielity J, Guranowski A, Ng S, Wah DA, Darzynkiewicz E, et al. 2009. Identification of the HIT-45 protein from Trypanosoma brucei as an FHIT protein/dinucleoside triphosphatase: substrate specificity studies on the recombinant and endogenous proteins. RNA 15: 1554-1564.
9. Bangs JD, Crain PF, Hashizume T, McCloskey JA, Boothroyd JC. 1992. Mass spectrometry of mRNA cap 4 from trypanosomatids reveals two novel nucleosides. J Biol Chem 267: 9805-9815.
10. Bastin P, Pullen TJ, Sherwin T, Gull K. 1999. Protein transport and flagellum assembly dynamics revealed by analysis of the paralysed trypanosome mutant snl-1. J Cell Sci 112: 3769-3777.
11. Benz C, Engstler M, Hillmer S, Clayton C. 2010. Depletion of 14-3-3 proteins in bloodstream-form Trypanosoma brucei inhibits variant surface glycoprotein recycling. Int J Parasitol 40: 629-634.
12. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, et al. 2005. The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422. (Pubitemid 40994676)
13. Blewett NH, Goldstrohm AC. 2012. A eukaryotic translation initiation factor 4E-binding protein promotes mRNA decapping and is required for PUF repression. Mol Cell Biol 32: 4181-4194.
14. Branche C, Kohl L, Toutirais G, Buisson J, Cosson J, Bastin P. 2006. Conserved and specific functions of axoneme components in trypanosome motility. J Cell Sci 119: 3443-3455. (Pubitemid 44405228)
15. Broadhead R, Dawe HR, Farr H, Griffiths S, Hart SR, Portman N, Shaw MK, Ginger ML, Gaskell SJ, McKean PG, et al. 2006. Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440: 224-227. (Pubitemid 43372101)
16. Cho PF, Poulin F, Cho-Park YA, Cho-Park IB, Chicoine JD, Lasko P, Sonenberg N. 2005. A new paradigm for translational control: inhibition via 5'-3' mRNA tethering by Bicoid and the eIF4E cognate 4EHP. Cell 121: 411-423. (Pubitemid 40692301)
17. Clarkson BK, Gilbert WV, Doudna JA. 2010. Functional overlap between eIF4G isoforms in Saccharomyces cerevisiae. PLoS One 5: e9114.
18. Clayton C, Shapira M. 2007. Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 156: 93-101. (Pubitemid 47600362)
19. Coller J, Parker R. 2004. Eukaryotic mRNA decapping. Ann Rev Biochem 73: 861-890. (Pubitemid 39050388)
20. Contreras V, Richardson MA, Hao E, Keiper BD. 2008. Depletion of the cap-associated isoform of translation factor eIF4G induces germline apoptosis in C. elegans. Cell Death Differ 15: 1232-1242. (Pubitemid 351984753)
21. Culjkovic B, Topisirovic I, Skrabanek L, Ruiz-Gutierrez M, Borden KL. 2005. eIF4E promotes nuclear export of cyclin D1 mRNAs via an element in the 3' UTR. J Cell Biol 169: 245-256. (Pubitemid 40656563)
22. Culjkovic B, Topisirovic I, Skrabanek L, Ruiz-Gutierrez M, Borden KL. 2006. eIF4E is a central node of an RNA regulon that governs cellular proliferation. J Cell Biol 175: 415-426. (Pubitemid 44708066)
23. Culjkovic B, Topisirovic I, Borden KL. 2007. Controlling gene expression through RNA regulons: the role of the eukaryotic translation initiation factor eIF4E. Cell Cycle 6: 65-69. (Pubitemid 46173883)
24. Cunningham I. 1977. New culture medium for maintenance of tsetse tissues and growth of trypanosomatids. J Protozool 24: 325-329. (Pubitemid 8156212)
25. Das A, Morales R, Banday M, Garcia S, Hao L, Cross GA, Estevez AM, Bellofatto V. 2012. The essential polysome-associated RNA-binding protein RBP42 targets mRNAs involved in Trypanosoma brucei energy metabolism. RNA 18: 1968-1983.
26. De Gaudenzi JG, Carmona SJ, Aguero F, Frasch AC. 2013. Genomewide analysis of 3'-untranslated regions supports the existence of post-transcriptional regulons controlling gene expression in trypanosomes. Peer J 1: e118.
27. Dhalia R, Reis CR, Freire ER, Rocha PO, Katz R, Muniz JR, Standart N, de Melo Neto OP. 2005. Translation initiation in Leishmania major: characterisation of multiple eIF4F subunit homologues. Mol Biochem Parasitol 140: 23-41. (Pubitemid 40203412)
28. Dhalia R, Marinsek N, Reis CR, Katz R, Muniz JR, Standart N, Carrington M, de Melo Neto OP. 2006. The two eIF4A helicases in Trypanosoma brucei are functionally distinct. Nucleic Acids Res 34: 2495-2507. (Pubitemid 43985614)
29. Estévez AM. 2008. The RNA-binding protein TbDRBD3 regulates the stability of a specific subset of mRNAs in trypanosomes. Nucleic Acids Res 36: 4573-4586.
30. Fernandez-Moya SM, Estevez AM. 2010. Posttranscriptional control and the role of RNA-binding proteins in gene regulation in trypanosomatid protozoan parasites. Wiley Interdiscip Rev RNA 1: 34-46.
31. Fernandez-Moya SM, Garcia-Perez A, Kramer S, Carrington M, Estevez AM.2012. Alterations in DRBD3 ribonucleoprotein complexes in response to stress in Trypanosoma brucei. PLoS One 7: e48870.
32. Ferraiuolo MA, Basak S, Dostie J, Murray EL, Schoenberg DR, Sonenberg N. 2005. A role for the eIF4E-binding protein 4E-T in P-body formation and mRNA decay. J Cell Biol 170: 913-924. (Pubitemid 41306291)
33. Freire ER, Dhalia R, Moura DM, da Costa Lima TD, Lima RP, Reis CR, Hughes K, Figueiredo RC, Standart N, Carrington M, et al. 2011. The four trypanosomatid eIF4E homologues fall into two separate groups, with distinct features in primary sequence and biological properties. Mol Biochem Parasitol 176: 25-36.
34. Ghosh A, Lima CD. 2010. Enzymology of RNA cap synthesis. Wiley Interdiscip Rev RNA 1: 152-172.
35. Gingras AC, Raught B, Sonenberg N. 1999. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68: 913-963. (Pubitemid 29449212)
36. Gosselin P, Martineau Y, Morales J, Czjzek M, Glippa V, Gauffeny I, Morin E, Le Corguille G, Pyronnet S, Cormier P, et al. 2013. Tracking a refined eIF4E-binding motif reveals Angel1 as a new partner of eIF4E. Nucleic Acids Res 41: 7783-7792.
37. Groppo R, Richter JD. 2009. Translational control from head to tail. Curr Opin Cell Biol 21: 444-451.
38. Günzl A. 2012. RNA polymerases and transcription factors of trypanosomes. In RNA metabolism in trypanosomes (ed. Bindereif A), Vol. 28, pp. 1-27. Springer, Berlin.
39. Hernández G, Altmann M, Sierra JM, Urlaub H, Diez del Corral R, Schwartz P, Rivera-Pomar R. 2005. Functional analysis of seven genes encoding eight translation initiation factor 4E (eIF4E) isoforms in Drosophila. Mech Dev 122: 529-543. (Pubitemid 40445355)
40. Hertz-Fowler C, Peacock CS, Wood V, Aslett M, Kerhornou A, Mooney P, Tivey A, Berriman M, Hall N, Rutherford K, et al. 2004. GeneDB: a resource for prokaryotic and eukaryotic organisms. Nucleic Acids Res 32: D339-D343. (Pubitemid 38081672)
41. Hill KL, Hutchings NR, Russell DG, Donelson JE. 1999. A novel protein targeting domain directs proteins to the anterior cytoplasmic face of the flagellar pocketin African trypanosomes. J Cell Sci 112: 3091-3101. (Pubitemid 29465727)
42. Inoue M, Nakamura Y, Yasuda K, Yasaka N, Hara T, Schnaufer A, Stuart K, Fukuma T. 2005. The 14-3-3 proteins of Trypanosoma brucei function in motility, cytokinesis, and cell cycle. J Biol Chem 280: 14085-14096. (Pubitemid 40517310)
43. Inoue M, Yasuda K, Uemura H, Yasaka N, Inoue H, Sei Y, Horikoshi N, Fukuma T. 2010. Phosphorylation-dependent protein interaction with Trypanosoma brucei 14-3-3 proteins that display atypical target recognition. PLoS One 5: e15566.
44. Jackson RJ, Hellen CU, Pestova TV. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127.
45. Jagus R, Bachvaroff TR, Joshi B, Place AR. 2012. Diversity of eukaryotic translational initiation factor eIF4E in protists. Comp Funct Genomics 2012: 134839.
46. Jankowska-Anyszka M, Lamphear BJ, Aamodt EJ, Harrington T, Darzynkiewicz E, Stolarski R, Rhoads RE. 1998. Multiple isoforms of eukaryotic protein synthesis initiation factor 4E in Caenorhabditis elegans can distinguish between mono- and trimethylated cap structures. J Biol Chem 273: 10538-10542.
47. Joshi B, Cameron A, Jagus R. 2004. Characterization of mammalian eIF4E-family members. Eur J Biochem 271: 2189-2203. (Pubitemid 38747988)
48. Joshi B, Lee K, Maeder DL, Jagus R. 2005. Phylogenetic analysis of eIF4E-family members. BMC Evol Biol 5: 48.
49. Keene JD. 2007. RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 8: 533-543. (Pubitemid 46955210)
50. Keiper BD, Lamphear BJ, Deshpande AM, Jankowska-Anyszka M, Aamodt EJ, Blumenthal T, Rhoads RE. 2000. Functional characterization of five eIF4E isoforms in Caenorhabditis elegans. J Biol Chem 275: 10590-10596. (Pubitemid 30202125)
51. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
52. Kim HS, Li Z, Boothroyd C, Cross GA. 2013. Strategies to construct null and conditional null Trypanosoma brucei mutants using Cre-recombinase and loxP. Mol Biochem Parasitol 191: 16-19.
53. Kramer S. 2012. Developmental regulation of gene expression in the absence of transcriptional control: the case of kinetoplastids. Mol Biochem Parasitol 181: 61-72.
54. Kramer S, Queiroz R, Ellis L, Webb H, Hoheisel JD, Clayton C, Carrington M. 2008. Heat shock causes a decrease in polysomes and the appearance of stress granules in trypanosomes independently of eIF2α phosphorylation at Thr169. J Cell Sci 121: 3002-3014.
55. Kramer S, Marnef A, Standart N, Carrington M. 2012. Inhibition of mRNA maturation in trypanosomes causes the formation of novel foci at the nuclear periphery containing cytoplasmic regulators of mRNA fate. J Cell Sci 125: 2896-2909.
56. Lamb JR, Fu V, Wirtz E, Bangs JD. 2001. Functional analysis of the trypanosomal AAA protein TbVCP with trans-dominant ATP hydrolysis mutants. J Biol Chem 276: 21512-21520.
57. Lasko P, Cho P, Poulin F, Sonenberg N. 2005. Contrasting mechanisms of regulating translation of specific Drosophila germline mRNAs at the level of 5'-cap structure binding. Biochem Soc Trans 33: 1544-1546. (Pubitemid 41779735)
58. Liang X-h, Haritan A, Uliel S, Michaeli S. 2003. trans and cis splicing in trypanosomatids: mechanisms, factors, and regulation. Eukaryot Cell 2: 830-840. (Pubitemid 37298696)
59. Mackintosh C. 2004. Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem J 381: 329-342. (Pubitemid 38976512)
60. Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK. 1997. Cocrystal structure of the messenger RNA 5' cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell 89: 951-961. (Pubitemid 27513521)
61. Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK. 1999. Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol Cell 3: 707-716. (Pubitemid 29323049)
62. Martínez-Calvillo S, Vizuet-de-Rueda JC, Florencio-Martínez LE, Manning-Cela RG, Figueroa-Angulo EE. 2010. Gene expression in trypanosomatid parasites. J Biomed Biotechnol 2010: 525241.
63. Merritt C, Stuart K. 2013. Identification of essential and non-essential protein kinases by a fusion PCR method for efficient production of transgenic Trypanosoma brucei. Mol Biochem Parasitol 190: 44-49.
64. Mony BM, MacGregor P, Ivens A, Rojas F, Cowton A, Young J, Horn D, Matthews K. 2014. Genome-wide dissection of the quorum sensing signalling pathway in Trypanosoma brucei. Nature 505: 681-685.
65. Niedzwiecka A, Marcotrigiano J, Stepinski J, Jankowska-Anyszka M, Wyslouch-Cieszynska A, Dadlez M, Gingras AC, Mak P, Darzynkiewicz E, Sonenberg N, et al. 2002. Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 5' cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins. J Mol Biol 319: 615-635. (Pubitemid 34729439)
66. Oberholzer M, Lopez MA, McLelland BT, Hill KL. 2010. Social motility in african trypanosomes. PLoS Pathogens 6: e1000739.
67. Oberholzer M, Langousis G, Nguyen HT, Saada EA, Shimogawa MM, Jonsson ZO, Nguyen SM, Wohlschlegel JA, Hill KL. 2011. Independent analysis of the flagellum surface and matrix proteomes provides insight into flagellum signaling in mammalian-infectious Trypanosoma brucei. Mol Cell Proteomics 10: M111.010538.
68. Otsuka Y, Kedersha NL, Schoenberg DR. 2009. Identification of a cytoplasmic complex that adds a cap onto 5'-monophosphate RNA. Mol Cell Biol 29: 2155-2167.
69. Ouellette M, Papadopoulou B. 2009. Coordinated gene expression by post-transcriptional regulons in African trypanosomes. J Biol 8: 100.
70. Palmeri A, Gherardini PF, Tsigankov P, Ausiello G, Spath GF, Zilberstein D, Helmer-Citterich M. 2011. PhosTryp: a phosphorylation site predictor specific for parasitic protozoa of the family trypanosomatidae. BMC Genomics 12: 614.
71. Park SH, Nguyen BN, Kirkham JK, Nguyen TN, Gunzl A. 2014. A new strategy of RNA interference that targets heterologous sequences reveals CITFA1 as an essential component of class I transcription factor A in Trypanosoma brucei. Eukaryot Cell 13: 785-795.
72. Parker R, Sheth U. 2007. P bodies and the control of mRNA translation and degradation. Mol Cell 25: 635-646. (Pubitemid 46341926)
73. Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP. 2002. Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2: 43-50.
74. Pestova TV, Hellen CU. 2003. Coupled folding during translation initiation. Cell 115: 650-652. (Pubitemid 38030293)
75. Preußer C, Jaé N, Günzl A, Bindereif A. 2012. Pre-mRNA splicing in Trypanosoma brucei: factors, mechanisms, and regulation. In RNA metabolism in trypanosomes (ed. Bindereif A), pp. 49-78. Springer, Berlin.
76. Prévôt D, Darlix JL, Ohlmann T. 2003. Conducting the initiation of protein synthesis: the role of eIF4G. Biol Cell 95: 141-156. (Pubitemid 36889217)
77. Ptushkina M, Berthelot K, von der Haar T, Geffers L, Warwicker J, McCarthy JE. 2001. A second eIF4E protein in Schizosaccharomyces pombe has distinct eIF4G-binding properties. Nucleic Acids Res 29: 4561-4569. (Pubitemid 33095016)
78. Queiroz R, Benz C, Fellenberg K, Hoheisel JD, Clayton C. 2009. Transcriptome analysis of differentiating trypanosomes reveals the existence of multiple post-transcriptional regulons. BMC Genomics 10: 495.
79. Ralston KS, Hill KL. 2006. Trypanin, a component of the flagellar Dynein regulatory complex, is essential in bloodstream form African trypanosomes. PLoS Pathogens 2: e101.
80. Ralston KS, Lerner AG, Diener DR, Hill KL. 2006. Flagellar motility contributes to cytokinesis in Trypanosoma brucei and is modulated by an evolutionarily conserved dynein regulatory system. Eukaryot Cell 5: 696-711.
81. Raught B, Gingras AC. 1999. eIF4E activity is regulated at multiple levels. Int J Biochem Cell Biol 31: 43-57. (Pubitemid 29094789)
82. Rhoads RE. 2009. eIF4E: new family members, new binding partners, new roles. J Biol Chem 284: 16711-16715.
83. Richter JD, Sonenberg N. 2005. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433: 477-480. (Pubitemid 40204297)
84. Ruan J-p, Shen S, Ullu E, Tschudi C. 2007. Evidence for a capping enzyme with specificity for the trypanosome spliced leader RNA. Mol Biochem Parasitol 156: 246-254. (Pubitemid 47600377)
85. Schimanski B, Nguyen TN, Günzl A. 2005. Highly efficient tandem affinity purification of trypanosome protein complexes based on a novel epitope combination. Eukaryot Cell 4: 1942-1950. (Pubitemid 41636886)
86. Sturm NR, Zamudio JR, Campbell DA. 2012. SL RNA biogenesis in kinetoplastids: a long and winding road. In RNA metabolism in trypanosomes (ed. Bindereif A), pp. 29-47. Springer, Berlin.
87. Takagi Y, Sindkar S, Ekonomidis D, Hall MP, Ho CK. 2007. Trypanosoma brucei encodes a bifunctional capping enzyme essential for cap 4 formation on the spliced leader RNA. J Biol Chem 282: 15995-16005. (Pubitemid 47100359)
88. Topisirovic I, Svitkin YV, Sonenberg N, Shatkin AJ. 2011. Cap and cap-binding proteins in the control of gene expression. Wiley Interdiscip Rev RNA 2: 277-298.
89. Urbaniak MD, Martin DM, Ferguson MA. 2013. Global quantitative SILAC phosphoproteomics reveals differential phosphorylation is widespread between the procyclic and bloodstream form lifecycle stages of Trypanosoma brucei. J Proteome Res 12: 2233-2244.
90. Wickstead B, Ersfeld K, Gull K. 2002. Targeting of a tetracycline- inducible expression system to the transcriptionally silent minichromosomes of Trypanosoma brucei. Mol Biochem Parasitol 125: 211-216. (Pubitemid 35449262)
91. Yoffe Y, Zuberek J, Lewdorowicz M, Zeira Z, Keasar C, Orr-Dahan I, Jankowska-Anyszka M, Stepinski J, Darzynkiewicz E, Shapira M. 2004. Cap-binding activity of an eIF4E homolog from Leishmania. RNA 10: 1764-1775. (Pubitemid 39426376)
92. Yoffe Y, Zuberek J, Lerer A, Lewdorowicz M, Stepinski J, Altmann M, Darzynkiewicz E, Shapira M. 2006. Binding specificities and potential roles of isoforms of eukaryotic initiation factor eIF4E in Leishmania. Eukaryot Cell 5: 1969-1979. (Pubitemid 44956809)
93. Yoffe Y, Léger M, Zinoviev A, Zuberek J, Darzynkiewicz E, Wagner G, Shapira M. 2009. Evolutionary changes in the Leishmania eIF4F complex involve variations in the eIF4E-eIF4G interactions. Nucleic Acids Res 10: 3243-3253.
94. Zamudio JR, Mittra B, Chattopadhyay A, Wohlschlegel JA, Sturm NR, Campbell DA. 2009. Trypanosoma brucei spliced leader RNA maturation by the cap 1 2'-O-ribose methyltransferase and SLA1 H/ACA snoRNA pseudouridine synthase complex. Mol Cell Biol 29: 1202-1211.
95. Zhang X, Cui J, Nilsson D, Gunasekera K, Chanfon A, Song X, Wang H, Xu Y, Ochsenreiter T. 2010. The Trypanosoma brucei MitoCarta and its regulation and splicing pattern during development. Nucleic Acids Res 38: 7378-7387.
96. Zick A, Onn I, Bezalel R, Margalit H, Shlomai J. 2005. Assigning functions to genes: identification of S-phase expressed genes in Leishmania major based on post-transcriptional control elements. Nucleic Acids Res 33: 4235-4242. (Pubitemid 41487282)
97. Zinoviev A, Shapira M. 2012. Evolutionary conservation and diversification of the translation initiation apparatus in trypanosomatids. Comp Funct Genomics 2012: 813718.
98. Zinoviev A, Leger M, Wagner G, Shapira M. 2011. A novel 4E-interacting protein in Leishmania is involved in stage-specific translation pathways. Nucleic Acids Res 39: 8404-8415.
99. Zinoviev A, Manor S, Shapira M. 2012. Nutritional stress affects an atypical cap-binding protein in Leishmania. RNA Biol 9: 1450-1460.