A bioinformatic survey of RNA-binding proteins in Plasmodium

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Reddy, BP Niranjan ^a   Shrestha, Sony ^a   Hart, Kevin J ^a   Liang, Xiaoying ^a   Kemirembe, Karen ^a   Cui, Liwang ^a   Lindner, Scott E ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Malaria; MRNA processing; Plasmodium; Post transcriptional regulation (PTR); Pre mRNA splicing; Ribosome biogenesis; RNA binding proteins (RBPs); Stress granules

Indexed keywords

DEAD H BOX RNA HELICASE; MESSENGER RNA; RNA BINDING PROTEIN; RNA HELICASE; TRANSCRIPTOME; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; PROTOZOAL PROTEIN;

ALBA GENE; ARTICLE; ASEXUAL STAGE; BIOINFORMATICS; COMPLEX FORMATION; CONTROLLED STUDY; GAMETOCYTE; GENE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC CONSERVATION; GENOME; INTRAERYTHROCYTIC DEVELOPMENT CYCLE; KH GENE; LIFE CYCLE; LIFE CYCLE STAGE; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; NONBIOLOGICAL MODEL; NONHUMAN; OOKINETE STAGE; PARASITE GENOME; PLASMODIUM FALCIPARUM; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PUF GENE; RNA RECOGNITION MOTIF; RNA SEQUENCE; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION; THREE DIMENSIONAL MODEL; TRANSCRIPTION REGULATION; BIOLOGY; GENETICS; PLASMODIUM;

COMPUTATIONAL BIOLOGY; PLASMODIUM; PROTOZOAN PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84959086317     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-2092-1     Document Type: Article

References (121)

1. Tun KM, Imwong M, Lwin KM, Win AA, Hlaing TM, Hlaing T, et al. Spread of artemisinin-resistant Plasmodium falciparum in Myanmar: a cross-sectional survey of the K13 molecular marker. Lancet Infect Dis. 2015;15:415-21.
2. Cui L, Wang Z, Miao J, Miao M, Chandra R, Jiang H, et al. Mechanisms of in vitro resistance to dihydroartemisinin in Plasmodium falciparum. Mol Microbiol. 2012;86:111-28.
3. Fidock DA, Rosenthal PJ, Croft SL, Brun R, Nwaka S. Antimalarial drug discovery: efficacy models for compound screening. Nat Rev Drug Discov. 2004;3:509-20.
4. Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, Roos DS, et al. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science. 2003;299:705-8.
5. De Silva EK, Gehrke AR, Olszewski K, León I, Chahal JS, Bulyk ML, et al. Specific DNA-binding by apicomplexan AP2 transcription factors. Proc Natl Acad Sci U S A. 2008;105:8393-8.
6. Coulson RMR, Hall N, Ouzounis C a. Comparative genomics of transcriptional control in the human malaria parasite Plasmodium falciparum. Genome Res. 2004;14:1548-54.
7. Cui L, Fan Q, Li J. The malaria parasite Plasmodium falciparum encodes members of the Puf RNA-binding protein family with conserved RNA binding activity. Nucleic Acids Res. 2002;30:4607-17.
8. Painter HJ, Campbell TL, Llinás M. The Apicomplexan AP2 family: Integral factors regulating Plasmodium development. Mol Biochem Parasitol. 2011;1-7.
9. Hall N, Karras M, Raine JD, Carlton JM, Kooij TWA, Berriman M, et al. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science. 2005;307:82-6.
10. Shock JL, Fischer KF, DeRisi JL. Whole-genome analysis of mRNA decay in Plasmodium falciparum reveals a global lengthening of mRNA half-life during the intra-erythrocytic development cycle. Genome Biol. 2007;8:R134.
11. Cui L, Lindner S, Miao J. Translational regulation during stage transitions in malaria parasites. Ann N Y Acad Sci. 2014;1-9.
12. Gomes-Santos CSS, Braks J, Prudêncio M, Carret C, Gomes AR, Pain A, et al. Transition of Plasmodium sporozoites into liver stage-like forms is regulated by the RNA binding protein Pumilio. PLoS Pathog. 2011;7, e1002046.
13. Mair GR, Lasonder E, Garver LS, Franke-Fayard BMD, Carret CK, Wiegant JCAG, et al. Universal features of post-transcriptional gene regulation are critical for Plasmodium zygote development. PLoS Pathog. 2010;6, e1000767.
14. Gerstberger S, Hafner M, Tuschl T. A census of human RNA-binding proteins. Nat Rev Genet. 2014;15:829-45.
15. Tsvetanova NG, Klass DM, Salzman J, Brown PO. Proteome-wide search reveals unexpected RNA-binding proteins in saccharomyces cerevisiae. PLoS One. 2010;5:1-12.
16. Malhotra S, Sowdhamini R. Sequence search and analysis of gene products containing RNA recognition motifs in the human genome. BMC Genomics. 2014;15:1159.
17. Tarique M, Ahmad M, Ansari A, Tuteja R. Plasmodium falciparum DOZI, an RNA helicase interacts with eIF4E. Gene. 2013;522:46-59.
18. Miao J, Fan Q, Parker D, Li X, Li J, Cui L. Puf mediates translation repression of transmission-blocking vaccine candidates in malaria parasites. PLoS Pathog. 2013;9, e1003268.
19. Lindner SE, Mikolajczak SA, Vaughan AM, Moon W, Joyce BR, Sullivan WJ, et al. Perturbations of Plasmodium Puf2 expression and RNA-seq of Puf2-deficient sporozoites reveal a critical role in maintaining RNA homeostasis and parasite transmissibility. Cell Microbiol. 2013;15:1266-83.
20. Chêne A, Vembar SS, Rivière L, Lopez-Rubio JJ, Claes A, Siegel TN, et al. PfAlbas constitute a new eukaryotic DNA/RNA-binding protein family in malaria parasites. Nucleic Acids Res. 2012;40:3066-77.
21. De Gaudenzi J, Frasch AC, Clayton C. RNA-binding domain proteins in Kinetoplastids: a comparative analysis. Eukaryot Cell. 2005;4:2106-14.
22. Wongsombat C, Aroonsri A, Kamchonwongpaisan S, Morgan HP, Walkinshaw MD, Yuthavong Y, et al. Molecular characterization of Plasmodium falciparum Bruno/CELF RNA binding proteins. Mol Biochem Parasitol. 2014;198:1-10.
23. Cordin O, Banroques J, Tanner NK, Linder P. The DEAD-box protein family of RNA helicases. Gene. 2006;367:17-37.
24. Linder P, Fuller-Pace FV. Looking back on the birth of DEAD-box RNA helicases. Biochim Biophys Acta - Gene Regul Mech. 1829;2013:750-5.
25. Tuteja R, Pradhan A. Unraveling the "DEAD-box" helicases of Plasmodium falciparum. Gene. 2006;376:1-12.
26. Abdelhaleem M, Maltais L, Wain H. The human DDX and DHX gene families of putative RNA helicases. Genomics. 2003;81:618-22.
27. Tanner NK, Linder P, Servet M. Gene C-: DExD / H Box RNA helicases: from generic motors to specific dissociation functions. Mol Cell. 2001;8:251-62.
28. De la Cruz J, Kressler D, Linder P. Unwinding RNA in saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem Sci. 1999;192-198.
29. Banroques J, Tanner NK. Bioinformatics and biochemical methods to study the structural and functional elements of DEAD-box RNA helicases. Methods Mol Biol. 2015;1259:165-81.
30. Rocak S, Linder P. DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol. 2004;5:232-41.
31. Tuteja R. Helicases - feasible antimalarial drug target for Plasmodium falciparum. FEBS J. 2007;274:4699-704.
32. Mehta J, Tuteja R. A novel dual Dbp5/DDX19 homologue from Plasmodium falciparum requires Q motif for activity. Mol Biochem Parasitol. 2011;176:58-63.
33. Prakash K, Tuteja R. A novel DEAD box helicase Has1p from Plasmodium falciparum: N-terminal is essential for activity. Parasitol Int. 2010;59:271-7.
34. Mair GR, Braks JAM, Garver LS, Wiegant JCAG, Hall N, Dirks RW, et al. Regulation of sexual development of Plasmodium by translational repression. Science. 2006;313:667-9.
35. Guerreiro A, Deligianni E, Santos JM, Silva PAGC, Louis C, Pain A, et al. Genome-wide RIP-Chip analysis of translational repressor-bound mRNAs in the Plasmodium gametocyte. Genome Biol. 2014;15:493.
36. Slomi H, Choi M, Slomi MC, Nussbaum RL, Dreyfuss G. Essential role for KH domains in RNA binding: Impaired RNA binding by a mutation in the KH domain of FMR1 that causes fragile X syndrome. Cell. 1994;77:33-9.
37. Valverde R, Edwards L, Regan L. Structure and function of KH domains. FEBS J. 2008;275:2712-26.
38. Siomi H, Matunis MJ, Michael WM, Dreyfuss G. The pre-mRNA binding K protein contains a novel evolutionarily conserved motif. Nucleic Acids Res. 1993;21:1193-8.
39. Grishin NV. KH domain: one motif, two folds. Nucleic Acids Res. 2001;29:638-43.
40. Dennerlein S, Rozanska A, Wydro M, Chrzanowska-Lightowlers ZMA, Lightowlers RN. Human ERAL1 is a mitochondrial RNA chaperone involved in the assembly of the 28S small mitochondrial ribosomal subunit. Biochem J. 2010;430:551-8.
41. Komaki-Yasuda K, Okuwaki M, Nagata K, Ichiro KS, Kano S. Identification of a novel and unique transcription factor in the intraerythrocytic stage of Plasmodium falciparum. PLoS One. 2013;8, e74701.
42. Galgano A, Forrer M, Jaskiewicz L, Kanitz A, Zavolan M, Gerber AP. Comparative analysis of mRNA targets for human PUF-family proteins suggests extensive interaction with the miRNA regulatory system. PLoS One. 2008;3, e3164.
43. Wickens M, Bernstein DS, Kimble J, Parker R. A PUF family portrait: 3'UTR regulation as a way of life. Trends Genet. 2002;18:150-7.
44. Miao J, Li J, Fan Q, Li X, Li X, Cui L. The Puf-family RNA-binding protein PfPuf2 regulates sexual development and sex differentiation in the malaria parasite Plasmodium falciparum. J Cell Sci. 2010;123(Pt 7):1039-49.
45. Müller K, Matuschewski K, Silvie O. The Puf-family RNA-binding protein Puf2 controls sporozoite conversion to liver stages in the malaria parasite. PLoS One. 2011;6, e19860.
46. Fan Q, Li J, Kariuki M, Cui L. Characterization of PfPuf2, member of the Puf family RNA-binding proteins from the malaria parasite Plasmodium falciparum. DNA Cell Biol. 2004;23:753-60.
47. Wardleworth BN, Russell RJM, Bell SD, Taylor GL, White MF. Structure of Alba: an archaeal chromatin protein modulated by acetylation. EMBO J. 2002;21:4654-62.
48. Goyal M, Alam A, Iqbal MS, Dey S, Bindu S, Pal C, et al. Identification and molecular characterization of an Alba-family protein from human malaria parasite Plasmodium falciparum. Nucleic Acids Res. 2012;40:1174-90.
49. Schimanski B, Heller M, Acosta-serrano A, Mani J, Gu A, Güttinger A, et al. Alba-domain proteins of trypanosoma brucei are cytoplasmic RNA-binding proteins that interact with the translation machinery. PLoS One. 2011;6, e22463.
50. Dupé A, Dumas C, Papadopoulou B. An Alba-domain protein contributes to the stage-regulated stability of amastin transcripts in Leishmania. Mol Microbiol. 2013;91:548-61.
51. Gissot M, Walker R, Delhaye S, Alayi TD, Huot L, Hot D, et al. Toxoplasma gondii Alba proteins are involved in translational control of gene expression. J Mol Biol. 2013;425:1287-301.
52. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, et al. Antisense transcription in the mammalian transcriptome. Science. 2005;309:1564-6.
53. Krishna SS, Majumdar I, Grishin NV. Structural classification of zinc fingers: survey and summary. Nucleic Acids Res. 2003;31:532-50.
54. Lunde BM, Moore C, Varani G. RNA-binding proteins: modular design for efficient function. Nat Rev Mol Cell Biol. 2007;8:479-90.
55. Pérez-Arellano I, Gallego J, Cervera J. The PUA domain - a structural and functional overview. FEBS J. 2007;274:4972-84.
56. Hartmann AM, Nayler O, Schwaiger FW, Obermeier A, Stamm S. The interaction and colocalization of Sam68 with the splicing-associated factor YT521-B in nuclear dots is regulated by the Src family kinase p59(fyn). Mol Biol Cell. 1999;10:3909-26.
57. Corsi A, Robbins A, Agarwal R, Megee P, Cohen-fix O, Stoilov P, et al. YTH: a new domain in nuclear proteins. Trends Biochem Sci. 2002;27:495-7.
58. Siomi H, Dreyfuss G. RNA-binding proteins as regulators of gene expression. Curr Opin Genet Dev. 1997;345-353.
59. Bycroft M, Hubbard TJ, Proctor M, Freund SM, Murzin AG. The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell. 1997;88:235-42.
60. Blencowe BJ, Ouzounis CA. The PWI motif: a new protein domain in splicing factors. Trends Biochem Sci. 1999;24:179-80.
61. Szymczyna BR, Bowman J, McCracken S, Pineda-Lucena A, Lu Y, Cox B, et al. Structure and function of the PWI motif: a novel nucleic acid-binding domain that facilitates pre-MRNA processing. Genes Dev. 2003;17:461-75.
62. Aravind L, Koonin EV. G-patch: a new conserved domain in eukaryotic RNA-processing proteins and type D retroviral polyproteins. Trends Biochem Sci. 1999;24:342-4.
63. Dreyfuss G, Kim VN, Kataoka N. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol. 2002;3:195-205.
64. Sorber K, Dimon MT, Derisi JL. RNA-Seq analysis of splicing in Plasmodium falciparum uncovers new splice junctions, alternative splicing and splicing of antisense transcripts. Nucleic Acids Res. 2011;39:3820-35.
65. Tuteja R. Genome wide identification of Plasmodium falciparum helicases: a comparison with human host. Cell Cycle. 2014;9:104-20.
66. Chakrabarti K, Pearson M, Grate L, Sterne-Weiler T, Deans J, Donohue JP, et al. Structural RNAs of known and unknown function identified in malaria parasites by comparative genomics and RNA analysis. RNA. 2007;13:1923-39.
67. Shankar J, Pradhan A, Tuteja R. Isolation and characterization of Plasmodium falciparum UAP56 homolog: evidence for the coupling of RNA binding and splicing activity by site-directed mutations. Arch Biochem Biophys. 2008;478:143-53.
68. Upadhyay R, Bawankar P, Malhotra D, Patankar S. A screen for conserved sequences with biased base composition identifies noncoding RNAs in the A-T rich genome of Plasmodium falciparum. Mol Biochem Parasitol. 2005;144:149-58.
69. Tuteja R. Helicases involved in splicing from malaria parasite Plasmodium falciparum. Parasitol Int. 2011;335-340.
70. Singh PK, Kanodia S, Dandin CJ, Vijayraghavan U, Malhotra P. Plasmodium falciparum Prp16 homologue and its role in splicing. Biochim Biophys Acta - Gene Regul Mech. 1819;2012:1186-99.
71. Otto TD, Wilinski D, Assefa S, Keane TM, Sarry LR, Böhme U, et al. New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol Microbiol. 2010;76:12-24.
72. Iriko H, Jin L, Kaneko O, Takeo S, Han E-T, Tachibana M, et al. A small-scale systematic analysis of alternative splicing in Plasmodium falciparum. Parasitol Int. 2009;58:196-9.
73. Dixit A, Singh PK, Sharma GP, Malhotra P, Sharma P. PfSRPK1, a novel splicing-related kinase from Plasmodium falciparum. J Biol Chem. 2010;285:38315-23.
74. Eshar S, Allemand E, Sebag A, Glaser F, Muchardt C, Mandel-Gutfreund Y, et al. A novel Plasmodium falciparum SR protein is an alternative splicing factor required for the parasites' proliferation in human erythrocytes. Nucleic Acids Res. 2012;40:9903-16.
75. Dasgupta T, Ladd AN. The importance of CELF control: molecular and biological roles of the CUG-BP, Elav-like family of RNA-binding proteins. Wiley Interdisciplinary Reviews: RNA 2012:104-121.
76. Ladd AN, Charlet N, Cooper TA. The CELF family of RNA binding proteins is implicated in cell-specific and developmentally regulated alternative splicing. Mol Cell Biol. 2001;21:1285-96.
77. Beisang D, Bohjanen PR, Louis IAV. CELF1, a multifunctional regulator of posttranscriptional networks. INTECH Open Access Publisher; 2012:181-206.
78. Chen M, Manley JL. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol. 2009;10:741-54.
79. Han A, Stoilov P, Linares AJ, Zhou Y, Fu XD, Black DL. De Novo prediction of PTBP1 binding and splicing targets reveals unexpected features of its RNA recognition and function. PLoS Comput Biol. 2014;10, e1003442.
80. Barabino SML, Hübner W, Jenny A, Minvielle-Sebastia L, Keller W. The 30-kd subunit of mammalian cleavage and polyadenylation specificity factor and its yeast homolog are rna-binding zinc finger proteins. Genes Dev. 1997;11:1703-16.
81. Gatfield D, Izaurralde E. REF1/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export. J Cell Biol. 2002;159:579-88.
82. Lau C-K, Diem MD, Dreyfuss G, Van Duyne GD. Structure of the Y14-magoh core of the exon junction complex. Curr Biol. 2003;13:933-41.
83. Li L, Monckton EA, Godbout R. A role for DEAD box 1 at DNA double-strand breaks. Mol Cell Biol. 2008;28:6413-25.
84. Edgcomb SP, Carmel AB, Naji S, Ambrus-Aikelin G, Reyes JR, Saphire ACS, et al. DDX1 is an RNA-dependent ATPase involved in HIV-1 Rev function and virus replication. J Mol Biol. 2012;415:61-74.
85. Guo XE, Chen CF, Wang DDH, Modrek AS, Phan VH, Lee WH, et al. Uncoupling the roles of the SUV3 helicase in maintenance of mitochondrial genome stability and RNA degradation. J Biol Chem. 2011;286:38783-94.
86. Minczuk M, Dmochowska A, Palczewska M, Stepien PP. Overexpressed yeast mitochondrial putative RNA helicase Mss116 partially restores proper mtRNA metabolism in strains lacking the Suv3 mtRNA helicase. Yeast. 2002;19:1285-93.
87. Buchan JR, Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol Cell. 2009;36:932-41.
88. Kedersha N, Anderson P. Mammalian stress granules and processing bodies. Methods Enzymol. 2007;431:61-81.
89. Marnef A, Sommerville J, Ladomery MR. RAP55: insights into an evolutionarily conserved protein family. Int J Biochem Cell Biol. 2009;41:977-81.
90. Sheth U, Parker R. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science (80-). 2003;300:805-8.
91. Coller JM, Tucker M, Sheth U, Valencia-Sanchez MA, Parker R. The DEAD box helicase, Dhh1p, functions in mRNA decapping and interacts with both the decapping and deadenylase complexes. RNA. 2001;7:1717-27.
92. Collart MA, Panasenko OO. The Ccr4--not complex. Gene. 2012;492:42-53.
93. Tucker M, Valencia-Sanchez MA, Staples RR, Chen J, Denis CL, Parker R. The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell. 2001;104:377-86.
94. Mulder KW, Inagaki A, Cameroni E, Mousson F, Winkler GS, De Virgilio C, et al. Modulation of Ubc4p/Ubc5p-mediated stress responses by the RING-finger-dependent ubiquitin-protein ligase Not4p in Saccharomyces cerevisiae. Genetics. 2007;176:181-92.
95. Balu B, Maher SP, Pance A, Chauhan C, Naumov AV, Andrews RM, et al. CCR4-associated factor 1 coordinates the expression of Plasmodium falciparum egress and invasion proteins. Eukaryot Cell. 2011;10:1257-63.
96. Halbach F, Reichelt P, Rode M, Conti E. The yeast ski complex: crystal structure and rna channeling to the exosome complex. Cell. 2013;154:814-26.
97. Bozdech Z, Llinás M, Pulliam BL, Wong ED, Zhu J, DeRisi JL. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 2003;1:085.
98. Llinás M, Bozdech Z, Wong ED, Adai AT, DeRisi JL. Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains. Nucleic Acids Res. 2006;34:1166-73.
99. Natalang O, Bischoff E, Deplaine G, Proux C, Dillies M-A, Sismeiro O, et al. Dynamic RNA profiling in Plasmodium falciparum synchronized blood stages exposed to lethal doses of artesunate. BMC Genomics. 2008;9:388.
100. Caro F, Ahyong V, Betegon M, DeRisi JL. Genome-wide regulatory dynamics of translation in the Plasmodium falciparum asexual blood stages. Elife. 2014;3:1-24.
101. Bischoff E, Vaquero C. In silico and biological survey of transcription-associated proteins implicated in the transcriptional machinery during the erythrocytic development of Plasmodium falciparum. BMC Genomics. 2010;11:34.
102. LaCount DJ, Vignali M, Chettier R, Phansalkar A, Bell R, Hesselberth JR, et al. A protein interaction network of the malaria parasite Plasmodium falciparum. Nature. 2005;438:103-7.
103. Suthram S, Sittler T, Ideker T. The Plasmodium protein network diverges from those of other eukaryotes. Nature. 2005;438:108-12.
104. Wuchty S, Adams JH, Ferdig MT. A comprehensive Plasmodium falciparum protein interaction map reveals a distinct architecture of a core interactome. Proteomics. 2009;9:1841-9.
105. Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 2009;37:D539-43.
106. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011;39:W29-37.
107. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 2004;5:113.
108. Schultz J, Copley RR, Doerks T, Ponting CP, Bork P. SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res. 2000;28:231-4.
109. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, et al. CDD: NCBI's conserved domain database. Nucleic Acids Res. 2014;43(Database issue):D222-6.
110. Letunic I, Doerks T, Bork P. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 2015;43(Database issue):D257-60.
111. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: a better web interface. Nucleic Acids Res. 2008;36:W5-9.
112. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725-9.
113. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406-25.
114. Roy A, Kucukural A, Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc. 2010;5:725-38.
115. Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 2014;42:W252-8.
116. Bordoli L, Schwede T. Automated protein structure modeling with SWISS-MODEL workspace and the protein model portal. Methods Mol Biol. 2012;857:107-36.
117. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;3389-3402.
118. Zhang Y, Skolnick J. TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 2005;33:2302-9.
119. López-Barragán MJ, Lemieux J, Quiñones M, Williamson KC, Molina-Cruz A, Cui K, et al. Directional gene expression and antisense transcripts in sexual and asexual stages of Plasmodium falciparum. BMC Genomics. 2011;12:587.
120. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques. 2003;34:374-8.
121. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, et al. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 2011;39:D561-8.