The translation initiation complex eIF3 in trypanosomatids and other pathogenic excavates - identification of conserved and divergent features based on orthologue analysis

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Rezende, Antonio M ^a   Assis, Ludmila A ^a   Nunes, Eduardo C ^b   da Costa Lima, Tamara D ^a   Marchini, Fabricio K ^b   Freire, Eden R ^a   Reis, Christian R S ^a   de Melo Neto, Osvaldo P ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b INSTITUTO CARLOS CHAGAS   (Brazil)

Author keywords

eIF3; Protein synthesis; Protozoa; Translation initiation factor

Indexed keywords

INITIATION FACTOR 1; INITIATION FACTOR 3; INITIATION FACTOR 3A; INITIATION FACTOR 3B; INITIATION FACTOR 3C; INITIATION FACTOR 3D; INITIATION FACTOR 3E; INITIATION FACTOR 3F; INITIATION FACTOR 3G; INITIATION FACTOR 3H; INITIATION FACTOR 3I; INITIATION FACTOR 3J; INITIATION FACTOR 3K; INITIATION FACTOR 3L; INITIATION FACTOR 3M; UNCLASSIFIED DRUG; PROTEIN SUBUNIT;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; GIARDIA INTESTINALIS; LEISHMANIA MAJOR; NONHUMAN; ORTHOLOGY; PROTEIN PROTEIN INTERACTION; PROTEIN SUBUNIT; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TRICHOMONAS VAGINALIS; TRYPANOSOMA BRUCEI; ANIMAL; BIOLOGY; CHEMISTRY; CONSERVED SEQUENCE; GENETIC VARIATION; GENETICS; GENOME; HUMAN; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; TRICHOMONADIDA; TRYPANOSOMA;

EUKARYOTA; EXCAVATA; GIARDIA SP.; LEISHMANIA MAJOR; PROTISTA; PROTOZOA; TRICHOMONAS; TRICHOMONAS VAGINALIS; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE;

AMINO ACID SEQUENCE; ANIMALS; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; EUKARYOTIC INITIATION FACTOR-3; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME, PROTOZOAN; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN SUBUNITS; SEQUENCE ALIGNMENT; TRICHOMONADIDA; TRYPANOSOMA;

EID: 84924291670     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1175     Document Type: Article

References (86)

1. Aitken CE, Lorsch JR: A mechanistic overview of translation initiation in eukaryotes. Nat Struct Mol Biol 2012, 19:568-576. 10.1038/nsmb.2303.
2. Valasek LS: 'Ribozoomin'-translation initiation from the perspective of the ribosome-bound eukaryotic initiation factors (eIFs). Curr Protein Pept Sci 2012, 13:305-330. 10.2174/138920312801619385.
3. Hinnebusch AG: The scanning mechanism of eukaryotic translation initiation. Annu Rev Biochem 2014, 83:779-812. 10.1146/annurev-biochem-060713-035802.
4. Dong Z, Zhang JT: Initiation factor eIF3 and regulation of mRNA translation, cell growth, and cancer. Crit Rev Oncol Hematol 2006, 59:169-180. 10.1016/j.critrevonc.2006.03.005.
5. Hinnebusch AG: eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem Sci 2006, 31:553-562. 10.1016/j.tibs.2006.08.005.
6. Marchione R, Leibovitch SA, Lenormand JL: The translational factor eIF3f: the ambivalent eIF3 subunit. Cell Mol Life Sci 2013, 70:3603-3616. 10.1007/s00018-013-1263-y.
7. Masutani M, Sonenberg N, Yokoyama S, Imataka H: Reconstitution reveals the functional core of mammalian eIF3. EMBO J 2007, 26:3373-3383. 10.1038/sj.emboj.7601765.
8. Zhou M, Sandercock AM, Fraser CS, Ridlova G, Stephens E, Schenauer MR, Yokoi-Fong T, Barsky D, Leary JA, Hershey JW, Doudna JA, Robinson CV: Mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc Natl Acad Sci U S A 2008, 105:18139-18144. 10.1073/pnas.0801313105.
9. Wagner S, Herrmannova A, Malik R, Peclinovska L, Valasek LS: Functional and biochemical characterization of human eIF3 in living cells. Mol Cell Biol 2014,34(16):3041-3052. 10.1128/MCB.00663-14.
10. Siridechadilok B, Fraser CS, Hall RJ, Doudna JA, Nogales E: Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 2005, 310:1513-1515. 10.1126/science.1118977.
11. Hofmann K, Bucher P: The PCI domain: a common theme in three multiprotein complexes. Trends Biochem Sci 1998, 23:204-205. 10.1016/S0968-0004(98)01217-1.
12. Aravind L, Ponting CP: Homologues of 26S proteasome subunits are regulators of transcription and translation. Protein Sci 1998, 7:1250-1254. 10.1002/pro.5560070521.
13. Pick E, Hofmann K, Glickman MH: PCI complexes: Beyond the proteasome, CSN, and eIF3 Troika. Mol Cell 2009, 35:260-264. 10.1016/j.molcel.2009.07.009.
14. Kouba T, Rutkai E, Karaskova M, Valasek L: The eIF3c/NIP1 PCI domain interacts with RNA and RACK1/ASC1 and promotes assembly of translation preinitiation complexes. Nucleic Acids Res 2012, 40:2683-2699. 10.1093/nar/gkr1083.
15. Khoshnevis S, Gunišová S, Vlčková V, Kouba T, Neumann P, Beznosková P, Ficner R, Valášek LS, et al.: Structural integrity of the PCI domain of eIF3a/TIF32 is required for mRNA recruitment to the 43S pre-initiation complexes. Nucleic Acids Res 2014, 42:4123-4139. 10.1093/nar/gkt1369.
16. Sun C, Querol-Audí J, Mortimer SA, Arias-Palomo E, Doudna JA, Nogales E, Cate JH: Two RNA-binding motifs in eIF3 direct HCV IRES-dependent translation. Nucleic Acids Res 2013, 41:7512-7521. 10.1093/nar/gkt510.
17. Asano K, Vornlocher HP, Richter-Cook NJ, Merrick WC, Hinnebusch AG, Hershey JW: Structure of cDNAs encoding human eukaryotic initiation factor 3 subunits. Possible roles in RNA binding and macromolecular assembly. J Biol Chem 1997, 272:27042-27052. 10.1074/jbc.272.43.27042.
18. Sun C, Todorovic A, Querol-Audí J, Bai Y, Villa N, Snyder M, Ashchyan J, Lewis CS, Hartland A, Gradia S, Fraser CS, Doudna JA, Nogales E, Cate JH: Functional reconstitution of human eukaryotic translation initiation factor 3 (eIF3). Proc Natl Acad Sci U S A 2011, 108:20473-20478. 10.1073/pnas.1116821108.
19. Querol-Audi J, Sun C, Vogan JM, Smith MD, Gu Y, Cate JH, Nogales E: Architecture of human translation initiation factor 3. Structure 2013, 21:920-928. 10.1016/j.str.2013.04.002.
20. Hernandez G, Proud CG, Preiss T, Parsyan A: On the diversification of the translation apparatus across eukaryotes. Comp Funct Genomics 2012, 2012:256848.
21. Fernandez-Moya SM, Estevez AM: Posttranscriptional control and the role of RNA-binding proteins in gene regulation in trypanosomatid protozoan parasites. Wiley Interdiscip Rev RNA 2010, 1:34-46.
22. Alsford S, du Bois K, Horn D, Field MC: Epigenetic mechanisms, nuclear architecture and the control of gene expression in trypanosomes. Expert Rev Mol Med 2012, 14:e13.
23. Kramer S: Developmental regulation of gene expression in the absence of transcriptional control: the case of kinetoplastids. Mol Biochem Parasitol 2012, 181:61-72. 10.1016/j.molbiopara.2011.10.002.
24. Clayton CE: Networks of gene expression regulation in Trypanosoma brucei. Mol Biochem Parasitol 2014,195(2):96-106. 10.1016/j.molbiopara.2014.06.005.
25. Jagus R, Bachvaroff TR, Joshi B, Place AR: Diversity of eukaryotic translational Initiation Factor eIF4E in protists. Comp Funct Genomics 2012, 2012:134839.
26. Zinoviev A, Shapira M: Evolutionary conservation and diversification of the translation initiation apparatus in trypanosomatids. Comp Funct Genomics 2012, 2012:813718.
27. Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, Sisk E, Rajandream MA, Adlem E, Aert R, Anupama A, Apostolou Z, Attipoe P, Bason N, Bauser C, Beck A, Beverley SM, Bianchettin G, Borzym K, Bothe G, Bruschi CV, Collins M, Cadag E, Ciarloni L, Clayton C, Coulson RM, Cronin A, Cruz AK, Davies RM, De Gaudenzi J: The genome of the kinetoplastid parasite, Leishmania major. Science 2005, 309:436-442. 10.1126/science.1112680.
28. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, Böhme U, Hannick L, Aslett MA, Shallom J, Marcello L, Hou L, Wickstead B, Alsmark UC, Arrowsmith C, Atkin RJ, Barron AJ, Bringaud F, Brooks K, Carrington M, Cherevach I, Chillingworth TJ, Churcher C, Clark LN, Corton CH, Cronin A: The genome of the African trypanosome Trypanosoma brucei. Science 2005, 309:416-422. 10.1126/science.1112642.
29. El-Sayed NM, Myler PJ, Blandin G, Berriman M, Crabtree J, Aggarwal G, Caler E, Renauld H, Worthey EA, Hertz-Fowler C, Ghedin E, Peacock C, Bartholomeu DC, Haas BJ, Tran AN, Wortman JR, Alsmark UC, Angiuoli S, Anupama A, Badger J, Bringaud F, Cadag E, Carlton JM, Cerqueira GC, Creasy T, Delcher AL, Djikeng A, Embley TM, Hauser C, Ivens AC: Comparative genomics of trypanosomatid parasitic protozoa. Science 2005, 309:404-409. 10.1126/science.1112181.
30. Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, Davids BJ, Dawson SC, Elmendorf HG, Hehl AB, Holder ME, Huse SM, Kim UU, Lasek-Nesselquist E, Manning G, Nigam A, Nixon JE, Palm D, Passamaneck NE, Prabhu A, Reich CI, Reiner DS, Samuelson J, Svard SG, Sogin ML: Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 2007, 317:1921-1926. 10.1126/science.1143837.
31. Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q, Wortman JR, Bidwell SL, Alsmark UC, Besteiro S, Sicheritz-Ponten T, Noel CJ, Dacks JB, Foster PG, Simillion C, Van de Peer Y, Miranda-Saavedra D, Barton GJ, Westrop GD, Müller S, Dessi D, Fiori PL, Ren Q, Paulsen I, Zhang H, Bastida-Corcuera FD, Simoes-Barbosa A, Brown MT, Hayes RD, Mukherjee M: Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 2007, 315:207-212. 10.1126/science.1132894.
32. Plutzer J, Ongerth J, Karanis P: Giardia taxonomy, phylogeny and epidemiology: Facts and open questions. Int J Hyg Environ Health 2010, 213:321-333. 10.1016/j.ijheh.2010.06.005.
33. Saletta F, Suryo RY, Richardson DR: The translational regulator eIF3a: the tricky eIF3 subunit! Biochim Biophys Acta 1806, 2010:275-286.
34. Valasek L, Nielsen KH, Hinnebusch AG: Direct eIF2-eIF3 contact in the multifactor complex is important for translation initiation in vivo. EMBO J 2002, 21:5886-5898. 10.1093/emboj/cdf563.
35. Valasek L, Mathew AA, Shin BS, Nielsen KH, Szamecz B, Hinnebusch AG: The yeast eIF3 subunits TIF32/a, NIP1/c, and eIF5 make critical connections with the 40S ribosome in vivo. Genes Dev 2003, 17:786-799. 10.1101/gad.1065403.
36. Dong Z, Qi J, Peng H, Liu J, Zhang JT: Spectrin domain of eukaryotic Initiation Factor 3a is the docking site for formation of the a:b:i:g subcomplex. J Biol Chem 2013, 288:27951-27959. 10.1074/jbc.M113.483164.
37. ElAntak L, Tzakos AG, Locker N, Lukavsky PJ: Structure of eIF3b RNA recognition motif and its interaction with eIF3j: structural insights into the recruitment of eIF3b to the 40 S ribosomal subunit. J Biol Chem 2007, 282:8165-8174. 10.1074/jbc.M610860200.
38. Smith TF, Gaitatzes C, Saxena K, Neer EJ: The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 1999, 24:181-185. 10.1016/S0968-0004(99)01384-5.
39. Liu Y, Neumann P, Kuhle B, Monecke T, Schell S, Chari A, Ficner R: Translation initiation factor eIF3b contains a nine-bladed beta-propeller and interacts with the 40S ribosomal subunit. Structure 2014, 22:923-930. 10.1016/j.str.2014.03.010.
40. De Gaudenzi J, Frasch AC, Clayton C: RNA-binding domain proteins in Kinetoplastids: a comparative analysis. Eukaryot Cell 2005, 4:2106-2114. 10.1128/EC.4.12.2106-2114.2005.
41. Nielsen KH, Valasek L, Sykes C, Jivotovskaya A, Hinnebusch AG: Interaction of the RNP1 motif in PRT1 with HCR1 promotes 40S binding of eukaryotic initiation factor 3 in yeast. Mol Cell Biol 2006, 26:2984-2998. 10.1128/MCB.26.8.2984-2998.2006.
42. Shalev A, Valásek L, Pise-Masison CA, Radonovich M, Phan L, Clayton J, He H, Brady JN, Hinnebusch AG, Asano K: Saccharomyces cerevisiae protein Pci8p and human protein eIF3e/Int-6 interact with the eIF3 core complex by binding to cognate eIF3b subunits. J Biol Chem 2001, 276:34948-34957. 10.1074/jbc.M102161200.
43. Asano K, Phan L, Anderson J, Hinnebusch AG: Complex formation by all five homologues of mammalian translation initiation factor 3 subunits from yeast Saccharomyces cerevisiae. J Biol Chem 1998, 273:18573-18585. 10.1074/jbc.273.29.18573.
44. Herrmannová A, Daujotyte D, Yang JC, Cuchalová L, Gorrec F, Wagner S, Dányi I, Lukavsky PJ, Valásek LS: Structural analysis of an eIF3 subcomplex reveals conserved interactions required for a stable and proper translation pre-initiation complex assembly. Nucleic Acids Res 2012, 40:2294-2311. 10.1093/nar/gkr765.
45. Asano K, Clayton J, Shalev A, Hinnebusch AG: A multifactor complex of eukaryotic initiation factors, eIF1, eIF2, eIF3, eIF5, and initiator tRNA(Met) is an important translation initiation intermediate in vivo. Genes Dev 2000, 14:2534-2546. 10.1101/gad.831800.
46. Karaskova M, Gunisova S, Herrmannova A, Wagner S, Munzarova V, Valasek L: Functional characterization of the role of the N-terminal domain of the c/Nip1 subunit of eukaryotic initiation factor 3 (eIF3) in AUG recognition. J Biol Chem 2012, 287:28420-28434. 10.1074/jbc.M112.386656.
47. Nygard O, Westermann P: Specific interaction of one subunit of eukaryotic initiation factor eIF-3 with 18S ribosomal RNA within the binary complex, eIF-3 small ribosomal subunit, as shown by cross-linking experiments. Nucleic Acids Res 1982, 10:1327-1334. 10.1093/nar/10.4.1327.
48. von Arnim AG, Chamovitz DA: Protein homeostasis: a degrading role for Int6/eIF3e. Curr Biol 2003, 13:R323-R325. 10.1016/S0960-9822(03)00238-0.
49. Yahalom A, Kim TH, Roy B, Singer R, von Arnim AG, Chamovitz DA: Arabidopsis eIF3e is regulated by the COP9 signalosome and has an impact on development and protein translation. Plant J 2008, 53:300-311.
50. Kim T, Hofmann K, von Arnim AG, Chamovitz DA: PCI complexes: pretty complex interactions in diverse signaling pathways. Trends Plant Sci 2001, 6:379-386. 10.1016/S1360-1385(01)02015-5.
51. Marchetti A, Buttitta F, Miyazaki S, Gallahan D, Smith GH, Callahan R: Int-6, a highly conserved, widely expressed gene, is mutated by mouse mammary tumor virus in mammary preneoplasia. J Virol 1995, 69:1932-1938.
52. Asano K, Kinzy TG, Merrick WC, Hershey JW: Conservation and diversity of eukaryotic translation initiation factor eIF3. J Biol Chem 1997, 272:1101-1109. 10.1074/jbc.272.2.1101.
53. Guo J, Sen GC: Characterization of the interaction between the interferon-induced protein P56 and the Int6 protein encoded by a locus of insertion of the mouse mammary tumor virus. J Virol 2000, 74:1892-1899. 10.1128/JVI.74.4.1892-1899.2000.
54. Browning KS, Gallie DR, Hershey JW, Hinnebusch AG, Maitra U, Merrick WC, Norbury C: Unified nomenclature for the subunits of eukaryotic initiation factor 3. Trends Biochem Sci 2001, 26:284. 10.1016/S0968-0004(01)01825-4.
55. Schwechheimer C: The COP9 signalosome (CSN): an evolutionary conserved proteolysis regulator in eukaryotic development. Biochim Biophys Acta 2004, 1695:45-54. 10.1016/j.bbamcr.2004.09.023.
56. Wei N, Serino G, Deng XW: The COP9 signalosome: more than a protease. Trends Biochem Sci 2008, 33:592-600. 10.1016/j.tibs.2008.09.004.
57. Cuchalova L, Kouba T, Herrmannova A, Danyi I, Chiu WL, Valasek L: The RNA recognition motif of eukaryotic translation initiation factor 3 g (eIF3g) is required for resumption of scanning of posttermination ribosomes for reinitiation on GCN4 and together with eIF3i stimulates linear scanning. Mol Cell Biol 2010, 30:4671-4686. 10.1128/MCB.00430-10.
58. Block KL, Vornlocher HP, Hershey JW: Characterization of cDNAs encoding the p44 and p35 subunits of human translation initiation factor eIF3. J Biol Chem 1998, 273:31901-31908. 10.1074/jbc.273.48.31901.
59. Hanachi P, Hershey JW, Vornlocher HP: Characterization of the p33 subunit of eukaryotic translation initiation factor-3 from Saccharomyces cerevisiae. J Biol Chem 1999, 274:8546-8553. 10.1074/jbc.274.13.8546.
60. Park HS, Browning KS, Hohn T, Ryabova LA: Eucaryotic initiation factor 4B controls eIF3-mediated ribosomal entry of viral reinitiation factor. EMBO J 2004, 23:1381-1391. 10.1038/sj.emboj.7600140.
61. Park HS, Himmelbach A, Browning KS, Hohn T, Ryabova LA: A plant viral "reinitiation" factor interacts with the host translational machinery. Cell 2001, 106:723-733. 10.1016/S0092-8674(01)00487-1.
62. Beznoskova P, Cuchalova L, Wagner S, Shoemaker CJ, Gunisova S, von der HT: Translation Initiation Factors eIF3 and HCR1 control translation termination and stop codon read-through in yeast cells. PLoS Genet 2013, 9:e1003962. 10.1371/journal.pgen.1003962.
63. Burks EA, Bezerra PP, Le H, Gallie DR, Browning KS: Plant initiation factor 3 subunit composition resembles mammalian initiation factor 3 and has a novel subunit. J Biol Chem 2001, 276:2122-2131. 10.1074/jbc.M007236200.
64. Zhou C, Arslan F, Wee S, Krishnan S, Ivanov AR, Oliva A, et al.: PCI proteins eIF3e and eIF3m define distinct translation initiation factor 3 complexes. BMC Biol 2005, 3:14. 10.1186/1741-7007-3-14.
65. Morris-Desbois C, Rety S, Ferro M, Garin J, Jalinot P: The human protein HSPC021 interacts with Int-6 and is associated with eukaryotic translation initiation factor 3. J Biol Chem 2001, 276:45988-45995. 10.1074/jbc.M104966200.
66. Walker G, Dorrell RG, Schlacht A, Dacks JB: Eukaryotic systematics: a user's guide for cell biologists and parasitologists. Parasitology 2011, 138:1638-1663. 10.1017/S0031182010001708.
67. Valasek L, Phan L, Schoenfeld LW, Valaskova V, Hinnebusch AG: Related eIF3 subunits TIF32 and HCR1 interact with an RNA recognition motif in PRT1 required for eIF3 integrity and ribosome binding. EMBO J 2001, 20:891-904. 10.1093/emboj/20.4.891.
68. Chiu WL, Wagner S, Herrmannova A, Burela L, Zhang F, Saini AK, et al.: The C-terminal region of eukaryotic translation initiation factor 3a (eIF3a) promotes mRNA recruitment, scanning, and, together with eIF3j and the eIF3b RNA recognition motif, selection of AUG start codons. Mol Cell Biol 2010, 30:4415-4434. 10.1128/MCB.00280-10.
69. Ankarklev J, Jerlstrom-Hultqvist J, Ringqvist E, Troell K, Svard SG: Behind the smile: cell biology and disease mechanisms of Giardia species. Nat Rev Microbiol 2010, 8:413-422.
70. Villa N, Do A, Hershey JW, Fraser CS: Human eukaryotic Initiation Factor 4G (eIF4G) protein binds to eIF3c, -d, and -e to promote mRNA recruitment to the ribosome. J Biol Chem 2013, 288:32932-32940. 10.1074/jbc.M113.517011.
71. Asano K, Shalev A, Phan L, Nielsen K, Clayton J, Valásek L, Donahue TF, Hinnebusch AG: Multiple roles for the C-terminal domain of eIF5 in translation initiation complex assembly and GTPase activation. EMBO J 2001, 20:2326-2337. 10.1093/emboj/20.9.2326.
72. Damoc E, Fraser CS, Zhou M, Videler H, Mayeur GL, Hershey JW, Doudna JA, Robinson CV, Leary JA: Structural characterization of the human eukaryotic initiation factor 3 protein complex by mass spectrometry. Mol Cell Proteomics 2007, 6:1135-1146. 10.1074/mcp.M600399-MCP200.
73. Khoshnevis S, Hauer F, Milon P, Stark H, Ficner R: Novel insights into the architecture and protein interaction network of yeast eIF3. RNA 2012, 18:2306-2319. 10.1261/rna.032532.112.
74. Phan L, Schoenfeld LW, Valasek L, Nielsen KH, Hinnebusch AG: A subcomplex of three eIF3 subunits binds eIF1 and eIF5 and stimulates ribosome binding of mRNA and tRNA(i)Met. EMBO J 2001, 20:2954-2965. 10.1093/emboj/20.11.2954.
75. Clayton C, Adams M, Almeida R, Baltz T, Barrett M, Bastien P, Belli S, Beverley S, Biteau N, Blackwell J, Blaineau C, Boshart M, Bringaud F, Cross G, Cruz A, Degrave W, Donelson J, El-Sayed N, Fu G, Ersfeld K, Gibson W, Gull K, Ivens A, Kelly J, Vanhamme L, Myler P: Genetic nomenclature for Trypanosoma and Leishmania. Mol Biochem Parasitol 1998, 97:221-224. 10.1016/S0166-6851(98)00115-7.
76. Li L, Stoeckert CJ Jr, Roos DS: OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003, 13:2178-2189. 10.1101/gr.1224503.
77. Enright AJ, Van DS, Ouzounis CA: An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002, 30:1575-1584. 10.1093/nar/30.7.1575.
78. Katoh K, Misawa K, Kuma K, Miyata T: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30:3059-3066. 10.1093/nar/gkf436.
79. Eddy SR: Profile hidden Markov models. Bioinformatics 1998, 14:755-763. 10.1093/bioinformatics/14.9.755.
80. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T: trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009, 25:1972-1973. 10.1093/bioinformatics/btp348.
81. Abascal F, Zardoya R, Posada D: ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105. 10.1093/bioinformatics/bti263.
82. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59:307-321. 10.1093/sysbio/syq010.
83. Dhalia R, Reis CR, Freire ER, Rocha PO, Katz R, Muniz JR, Standart N, de Melo Neto OP: Translation initiation in Leishmania major: characterisation of multiple eIF4F subunit homologues. Mol Biochem Parasitol 2005, 140:23-41. 10.1016/j.molbiopara.2004.12.001.
84. da Costa Lima TD, Moura DM, Reis CR, Vasconcelos JR, Ellis L, Carrington M, Figueiredo RC, de Melo Neto OP: Functional characterization of three leishmania poly(a) binding protein homologues with distinct binding properties to RNA and protein partners. Eukaryot Cell 2010, 9:1484-1494. 10.1128/EC.00148-10.
85. Rappsilber J, Ishihama Y, Mann M: Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem 2003, 75:663-670. 10.1021/ac026117i.
86. Cox J, Mann M: MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008, 26:1367-1372. 10.1038/nbt.1511.