Putative SF2 helicases of the early-branching eukaryote Giardia lamblia are involved in antigenic variation and parasite differentiation into cysts

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• 作者：Pablo R Gargantini (1)
  Marianela C Serradell (1)
  Alessandro Torri (1)
  Hugo D Lujan (1)
  
• 关键词：RNA/DNA helicases ; Giardia lamblia ; Encystation ; Antigenic variation ; Cell differentiation ; Gene expression ; RNAi ; Dicer
• 刊名：BMC Microbiology
• 出版年：2012
• 出版时间：December 2012
• 年：2012
• 卷：12
• 期：1
• 全文大小：1136KB
• 参考文献：1. Abdelhaleem M: Helicases: an overview. / Methods Mol Biol 2010, 587:1鈥?2. CrossRef
  2. Linder P, Jankowsky E: From unwinding to clamping - the DEAD box RNA helicase family. / Nat Rev Mol Cell Biol 2011, 12:505鈥?16. CrossRef
  3. Singleton MR, Dillingham MS, Wigley DB: Structure and mechanism of helicases and nucleic acid translocases. / Annu Rev Biochem 2007, 76:23鈥?0. CrossRef
  4. Kainov DE, Tuma R, Mancini EJ: Hexameric molecular motors: P4 packaging ATPase unravels the mechanism. / Cell Mol Life Sci 2006, 63:1095鈥?105. CrossRef
  5. Rocak S, Linder P: DEAD-box proteins: the driving forces behind RNA metabolism. / Nat Rev Mol Cell Biol 2004, 5:232鈥?41. CrossRef
  6. Iost I, Dreyfus M: DEAD-box RNA helicases in Escherichia coli. / Nucleic Acids Res 2006, 34:4189鈥?197. CrossRef
  7. Gorbalenya AE, Koonin EV: Helicases: amino acid sequence comparisons and structure-function relationships. / Current Opinion in Structural Biology 1993, 3:419鈥?29. CrossRef
  8. Fairman-Williams ME, Guenther UP, Jankowsky E: SF1 and SF2 helicases: family matters. / Curr Opin Struct Biol 2010, 20:313鈥?24. CrossRef
  9. Wang Y, Guthrie C: PRP16, a DEAH-box RNA helicase, is recruited to the spliceosome primarily via its nonconserved N-terminal domain. / RNA 1998, 4:1216鈥?229. CrossRef
  10. Hall MC, Matson SW: Helicase motifs: the engine that powers DNA unwinding. / Mol Microbiol 1999, 34:867鈥?77. CrossRef
  11. Bernstein E, Caudy AA, Hammond SM, Hannon GJ: Role for a bidentate ribonuclease in the initiation step of RNA interference. / Nature 2001, 409:363鈥?66. CrossRef
  12. Jankowsky E, Fairman ME: RNA helicases鈥搊ne fold for many functions. / Curr Opin Struct Biol 2007, 17:316鈥?24. CrossRef
  13. Edlind TD, Chakraborty PR: Unusual ribosomal RNA of the intestinal parasite Giardia lamblia. / Nucleic Acids Res 1987, 15:7889鈥?901. CrossRef
  14. Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA: Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. / Science 1989, 243:75鈥?7. CrossRef
  15. Van Keulen H, Gutell RR, Gates MA, Campbell SR, Erlandsen SL, Jarroll EL, Kulda J, Meyer EA: Unique phylogenetic position of Diplomonadida based on the complete small subunit ribosomal RNA sequence of Giardia ardeae, G. muris, G. duodenalis and Hexamita sp. / FASEB J 1993, 7:223鈥?31.
  16. Hashimoto T, Nakamura Y, Nakamura F, Shirakura T, Adachi J, Goto N, Okamoto K, Hasegawa M: Protein phylogeny gives a robust estimation for early divergences of eukaryotes: phylogenetic place of a mitochondria-lacking protozoan. / Giardia lamblia. Mol Biol Evol 1994, 11:65鈥?1.
  17. Feng JM, Sun J, Xin DD, Wen JF: Comparative analysis of the 5S rRNA and its associated proteins reveals unique primitive rather than parasitic features in Giardia lamblia. / PLoS One 2012, 7:e36878. CrossRef
  18. Adam RD: Biology of Giardia lamblia. / Clin Microbiol Rev 2001, 14:447鈥?75. CrossRef
  19. Lujan HD, Mowatt MR, Nash TE: Mechanisms of Giardia lamblia differentiation into cysts. / Microbiol Mol Biol Rev 1997, 61:294鈥?04.
  20. Nash TE: Surface antigenic variation in Giardia lamblia. / Mol Microbiol 2002, 45:585鈥?90. CrossRef
  21. Davids BJ, Reiner DS, Birkeland SR, Preheim SP, Cipriano MJ, McArthur AG, Gillin FD: A new family of giardial cysteine-rich non-VSP protein genes and a novel cyst protein. / PLoS One 2006, 1:e44. CrossRef
  22. Prucca CG, Slavin I, Quiroga R, Elias EV, Rivero FD, Saura A, Carranza PG, Lujan HD: Antigenic variation in Giardia lamblia is regulated by RNA interference. / Nature 2008, 456:750鈥?54. CrossRef
  23. Rivero FD, Saura A, Prucca CG, Carranza PG, Torri A, Lujan HD: Disruption of antigenic variation is crucial for effective parasite vaccine. / Nat Med 2010, 16:551鈥?57. 551p following 557 CrossRef
  24. Prucca CG, Lujan HD: Antigenic variation in Giardia lamblia. / Cell Microbiol 2009, 11:1706鈥?715. CrossRef
  25. Li W, Saraiya AA, Wang CC: Gene regulation in Giardia lambia involves a putative microRNA derived from a small nucleolar RNA. / PLoS Negl Trop Dis 2011, 5:e1338. CrossRef
  26. Macrae IJ, Zhou K, Li F, Repic A, Brooks AN, Cande WZ, Adams PD, Doudna JA: Structural basis for double-stranded RNA processing by Dicer. / Science 2006, 311:195鈥?98. CrossRef
  27. Tanner NK, Linder P: DExD/H box RNA helicases: from generic motors to specific dissociation functions. / Mol Cell 2001, 8:251鈥?62. CrossRef
  28. Aurrecoechea C, Brestelli J, Brunk BP, Carlton JM, Dommer J, Fischer S, Gajria B, Gao X, Gingle A, Grant G, / et al.: GiardiaDB and TrichDB: integrated genomic resources for the eukaryotic protist pathogens Giardia lamblia and Trichomonas vaginalis. / Nucleic Acids Res 2009, 37:D526鈥?30. CrossRef
  29. Chen YH, Su LH, Huang YC, Wang YT, Kao YY, Sun CH: UPF1, a conserved nonsense-mediated mRNA decay factor, regulates cyst wall protein transcripts in Giardia lamblia. / PLoS One 2008, 3:e3609. CrossRef
  30. Umate P, Tuteja N, Tuteja R: Genome-wide comprehensive analysis of human helicases. / Commun Integr Biol 2011, 4:118鈥?37.
  31. Umate P, Tuteja R, Tuteja N: Genome-wide analysis of helicase gene family from rice and Arabidopsis: a comparison with yeast and human. / Plant Mol Biol 2010, 73:449鈥?65. CrossRef
  32. de la Cruz J, Kressler D, Linder P: Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. / Trends Biochem Sci 1999, 24:192鈥?98. CrossRef
  33. Marchat LA, Orozco E, Guillen N, Weber C, Lopez-Camarillo C: Putative DEAD and DExH-box RNA helicases families in Entamoeba histolytica. / Gene 2008, 424:1鈥?0. CrossRef
  34. Tuteja R, Pradhan A: Unraveling the 'DEAD-box' helicases of Plasmodium falciparum. / Gene 2006, 376:1鈥?2. CrossRef
  35. Gargantini PR, Lujan HD, Pereira CA: In silico analysis of trypanosomatids' helicases. / FEMS Microbiol Lett 2012, 335:123鈥?29. CrossRef
  36. Cordin O, Tanner NK, Doere M, Linder P, Banroques J: The newly discovered Q motif of DEAD-box RNA helicases regulates RNA-binding and helicase activity. / EMBO J 2004, 23:2478鈥?487. CrossRef
  37. Schneider TD, Stephens RM: Sequence logos: a new way to display consensus sequences. / Nucleic Acids Res 1990, 18:6097鈥?100. CrossRef
  38. Crooks GE, Hon G, Chandonia JM, Brenner SE: WebLogo: a sequence logo generator. / Genome Res 2004, 14:1188鈥?190. CrossRef
  39. Umate P, Tuteja R, Tuteja N: Architectures of the unique domains associated with the DEAD-box helicase motif. / Cell Cycle 2010, 9:4228鈥?235. CrossRef
  40. Banroques J, Cordin O, Doere M, Linder P, Tanner NK: Analyses of the functional regions of DEAD-Box RNA "helicases" with deletion and chimera constructs tested in vivo and in vitro. / J Mol Biol 2011, 413:451鈥?72. CrossRef
  41. Abramczyk D, Tchorzewski M, Grankowski N: Non-AUG translation initiation of mRNA encoding acidic ribosomal P2A protein in Candida albicans. / Yeast 2003, 20:1045鈥?052. CrossRef
  42. Takahashi K, Maruyama M, Tokuzawa Y, Murakami M, Oda Y, Yoshikane N, Makabe KW, Ichisaka T, Yamanaka S: Evolutionarily conserved non-AUG translation initiation in NAT1/p97/DAP5 (EIF4G2). / Genomics 2005, 85:360鈥?71. CrossRef
  43. Linder P, Owttrim GW: Plant RNA helicases: linking aberrant and silencing RNA. / Trends Plant Sci 2009, 14:344鈥?52. CrossRef
  44. Schultz J, Milpetz F, Bork P, Ponting CP: SMART, a simple modular architecture research tool: identification of signaling domains. / Proc Natl Acad Sci U S A 1998, 95:5857鈥?864. CrossRef
  45. Jermy AJ, Willer M, Davis E, Wilkinson BM, Stirling CJ: The Brl domain in Sec63p is required for assembly of functional endoplasmic reticulum translocons. / J Biol Chem 2006, 281:7899鈥?906. CrossRef
  46. Ponting CP: Proteins of the endoplasmic-reticulum-associated degradation pathway: domain detection and function prediction. / Biochem J 2000,351(Pt 2):527鈥?35. CrossRef
  47. Doherty AJ, Serpell LC, Ponting CP: The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA. / Nucleic Acids Res 1996, 24:2488鈥?497. CrossRef
  48. Staub E, Fiziev P, Rosenthal A, Hinzmann B: Insights into the evolution of the nucleolus by an analysis of its protein domain repertoire. / Bioessays 2004, 26:567鈥?81. CrossRef
  49. Larocque JR, Jasin M: Mechanisms of recombination between diverged sequences in wild-type and BLM-deficient mouse and human cells. / Mol Cell Biol 2010, 30:1887鈥?897. CrossRef
  50. Ngo HP, Lydall D: Survival and growth of yeast without telomere capping by Cdc13 in the absence of Sgs1, Exo1, and Rad9. / PLoS Genet 2010, 6:e1001072. CrossRef
  51. Ma E, MacRae IJ, Kirsch JF, Doudna JA: Autoinhibition of human dicer by its internal helicase domain. / J Mol Biol 2008, 380:237鈥?43. CrossRef
  52. Robb GB, Rana TM: RNA helicase A interacts with RISC in human cells and functions in RISC loading. / Mol Cell 2007, 26:523鈥?37. CrossRef
  53. Zhou R, Hotta I, Denli AM, Hong P, Perrimon N, Hannon GJ: Comparative analysis of argonaute-dependent small RNA pathways in Drosophila. / Mol Cell 2008, 32:592鈥?99. CrossRef
  54. Tomari Y, Du T, Haley B, Schwarz DS, Bennett R, Cook HA, Koppetsch BS, Theurkauf WE, Zamore PD: RISC assembly defects in the Drosophila RNAi mutant armitage. / Cell 2004, 116:831鈥?41. CrossRef
  55. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K: Modulation of microRNA processing by p53. / Nature 2009, 460:529鈥?33. CrossRef
  56. Jonassen I, Collins JF, Higgins DG: Finding flexible patterns in unaligned protein sequences. / Protein Sci 1995, 4:1587鈥?595. CrossRef
  57. Faghiri Z, Widmer G: A comparison of the Giardia lamblia trophozoite and cyst transcriptome using microarrays. / BMC Microbiol 2011, 11:91. CrossRef
  58. Lujan HD, Mowatt MR, Byrd LG, Nash TE: Cholesterol starvation induces differentiation of the intestinal parasite Giardia lamblia. / Proc Natl Acad Sci U S A 1996, 93:7628鈥?633. CrossRef
  59. Birkeland SR, Preheim SP, Davids BJ, Cipriano MJ, Palm D, Reiner DS, Svard SG, Gillin FD, McArthur AG: Transcriptome analyses of the Giardia lamblia life cycle. / Mol Biochem Parasitol 2010, 174:62鈥?5. CrossRef
  60. Morey JS, Ryan JC, Van Dolah FM: Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. / Biol Proced Online 2006, 8:175鈥?93. CrossRef
  61. Etienne W, Meyer MH, Peppers J, Meyer RA Jr: Comparison of mRNA gene expression by RT-PCR and DNA microarray. / Biotechniques 2004, 36:618鈥?20. 622, 624鈥?16
  62. Morf L, Spycher C, Rehrauer H, Fournier CA, Morrison HG, Hehl AB: The transcriptional response to encystation stimuli in Giardia lamblia is restricted to a small set of genes. / Eukaryot Cell 2010, 9:1566鈥?576. CrossRef
  63. Chu CY, Rana TM: Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. / PLoS Biol 2006, 4:e210. CrossRef
  64. Fukuda T, Yamagata K, Fujiyama S, Matsumoto T, Koshida I, Yoshimura K, Mihara M, Naitou M, Endoh H, Nakamura T, / et al.: DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. / Nat Cell Biol 2007, 9:604鈥?11. CrossRef
  65. Naqvi AR, Islam MN, Choudhury NR, Haq QM: The fascinating world of RNA interference. / Int J Biol Sci 2009, 5:97鈥?17. CrossRef
  66. Ambrus AM, Frolov MV: The diverse roles of RNA helicases in RNAi. / Cell Cycle 2009, 8:3500鈥?505. CrossRef
  67. Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, / et al.: Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. / Science 2007, 317:1921鈥?926. CrossRef
  68. Linder P: Dead-box proteins: a family affair鈥揳ctive and passive players in RNP-remodeling. / Nucleic Acids Res 2006, 34:4168鈥?180. CrossRef
  69. Carranza PG, Lujan HD: New insights regarding the biology of Giardia lamblia. / Microbes Infect 2010, 12:71鈥?0. CrossRef
  70. Lujan HD, Mowatt MR, Conrad JT, Bowers B, Nash TE: Identification of a novel Giardia lamblia cyst wall protein with leucine-rich repeats. Implications for secretory granule formation and protein assembly into the cyst wall. / J Biol Chem 1995, 270:29307鈥?9313. CrossRef
  71. Sun CH, Palm D, McArthur AG, Svard SG, Gillin FD: A novel Myb-related protein involved in transcriptional activation of encystation genes in Giardia lamblia. / Mol Microbiol 2002, 46:971鈥?84. CrossRef
  72. Wang CH, Su LH, Sun CH: A novel ARID/Bright-like protein involved in transcriptional activation of cyst wall protein 1 gene in Giardia lamblia. / J Biol Chem 2007, 282:8905鈥?914. CrossRef
  73. Sun CH, Su LH, Gillin FD: Novel plant-GARP-like transcription factors in Giardia lamblia. / Mol Biochem Parasitol 2006, 146:45鈥?7. CrossRef
  74. Pan YJ, Cho CC, Kao YY, Sun CH: A novel WRKY-like protein involved in transcriptional activation of cyst wall protein genes in Giardia lamblia. / J Biol Chem 2009, 284:17975鈥?7988. CrossRef
  75. Sonda S, Morf L, Bottova I, Baetschmann H, Rehrauer H, Caflisch A, Hakimi MA, Hehl AB: Epigenetic mechanisms regulate stage differentiation in the minimized protozoan Giardia lamblia. / Mol Microbiol 2010, 76:48鈥?7. CrossRef
  76. Klappacher GW, Lunyak VV, Sykes DB, Sawka-Verhelle D, Sage J, Brard G, Ngo SD, Gangadharan D, Jacks T, Kamps MP, / et al.: An induced Ets repressor complex regulates growth arrest during terminal macrophage differentiation. / Cell 2002, 109:169鈥?80. CrossRef
  77. Wilson BJ, Bates GJ, Nicol SM, Gregory DJ, Perkins ND, Fuller-Pace FV: The p68 and p72 DEAD box RNA helicases interact with HDAC1 and repress transcription in a promoter-specific manner. / BMC Mol Biol 2004, 5:11. CrossRef
  78. Mooney SM, Grande JP, Salisbury JL, Janknecht R: Sumoylation of p68 and p72 RNA helicases affects protein stability and transactivation potential. / Biochemistry 2010, 49:1鈥?0. CrossRef
  79. Welker NC, Maity TS, Ye X, Aruscavage PJ, Krauchuk AA, Liu Q, Bass BL: Dicer's helicase domain discriminates dsRNA termini to promote an altered reaction mode. / Mol Cell 2011, 41:589鈥?99. CrossRef
  80. Zhang YQ, Chen DL, Tian HF, Zhang BH, Wen JF: Genome-wide computational identification of microRNAs and their targets in the deep-branching eukaryote Giardia lamblia. / Comput Biol Chem 2009, 33:391鈥?96. CrossRef
  81. Puntervoll P, Linding R, Gemund C, Chabanis-Davidson S, Mattingsdal M, Cameron S, Martin DM, Ausiello G, Brannetti B, Costantini A, / et al.: ELM server: A new resource for investigating short functional sites in modular eukaryotic proteins. / Nucleic Acids Res 2003, 31:3625鈥?630. CrossRef
  82. Sigrist CJ, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, Bairoch A, Hulo N: PROSITE, a protein domain database for functional characterization and annotation. / Nucleic Acids Res 2010, 38:D161鈥?66. CrossRef
  83. Gouy M, Guindon S, Gascuel O: SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. / Mol Biol Evol 2010, 27:221鈥?24. CrossRef
  84. Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. / Nucleic Acids Res 2004, 32:1792鈥?797. CrossRef
  85. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, / et al.: Clustal W and Clustal X version 2.0. / Bioinformatics 2007, 23:2947鈥?948. CrossRef
  86. Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. / Syst Biol 2003, 52:696鈥?04. CrossRef
  87. Diamond LS, Clark CG, Cunnick CC: YI-S, a casein-free medium for axenic cultivation of Entamoeba histolytica, related Entamoeba, Giardia intestinalis and Trichomonas vaginalis. / J Eukaryot Microbiol 1995, 42:277鈥?78. CrossRef
  88. Boucher SE, Gillin FD: Excystation of in vitro-derived Giardia lamblia cysts. / Infect Immun 1990, 58:3516鈥?522.
  89. Pfaffl MW, Horgan GW, Dempfle L: Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. / Nucleic Acids Res 2002, 30:e36. CrossRef
  
• 作者单位：Pablo R Gargantini (1)
  Marianela C Serradell (1)
  Alessandro Torri (1)
  Hugo D Lujan (1)
  
  1. Laboratory of Biochemistry and Molecular Biology, School of Medicine, Catholic University of C贸rdoba, C贸rdoba, X5004ASK, Argentina
  
• ISSN：1471-2180

文摘

Background Regulation of surface antigenic variation in Giardia lamblia is controlled post-transcriptionally by an RNA-interference (RNAi) pathway that includes a Dicer-like bidentate RNase III (gDicer). This enzyme, however, lacks the RNA helicase domain present in Dicer enzymes from higher eukaryotes. The participation of several RNA helicases in practically all organisms in which RNAi was studied suggests that RNA helicases are potentially involved in antigenic variation, as well as during Giardia differentiation into cysts. Results An extensive in silico analysis of the Giardia genome identified 32 putative Super Family 2 RNA helicases that contain almost all the conserved RNA helicase motifs. Phylogenetic studies and sequence analysis separated them into 22 DEAD-box, 6 DEAH-box and 4 Ski2p-box RNA helicases, some of which are homologs of well-characterized helicases from higher organisms. No Giardia putative helicase was found to have significant homology to the RNA helicase domain of Dicer enzymes. Additionally a series of up- and down-regulated putative RNA helicases were found during encystation and antigenic variation by qPCR experiments. Finally, we were able to recognize 14 additional putative helicases from three different families (RecQ family, Swi2/Snf2 and Rad3 family) that could be considered DNA helicases. Conclusions This is the first comprehensive analysis of the Super Family 2 helicases from the human intestinal parasite G. lamblia. The relative and variable expression of particular RNA helicases during both antigenic variation and encystation agrees with the proposed participation of these enzymes during both adaptive processes. The putatives RNA and DNA helicases identified in this early-branching eukaryote provide initial information regarding the biological role of these enzymes in cell adaptation and differentiation.