The microRNAs in an Ancient Protist Repress the Variant-Specific Surface Protein Expression by Targeting the Entire Coding Sequence

PLoS Pathogens

Volumn 10, Issue 2, 2014, Pages

  Saraiya, Ashesh A ^a   Li, Wei ^a   Wu, Jesse ^b   Chang, Chuan H ^b   Wang, Ching C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MICRORNA; MICRORNA 24; MICRORNA 30; MICRORNA 31; MICRORNA 5; MICRORNA 56; MICRORNA 69; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; DENSITOMETRY; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSFECTION; GIARDIA LAMBLIA; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; TROPHOZOITE; WESTERN BLOTTING;

GENE EXPRESSION REGULATION; GENE LIBRARY; GIARDIA LAMBLIA; MEMBRANE PROTEINS; MICRORNAS; OPEN READING FRAMES; PROTOZOAN PROTEINS; RNA, PROTOZOAN;

EID: 84895769999     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003791     Document Type: Article

References (49)

1. Barwick RS, Levy DA, Craun GF, Beach MJ, Calderon RL, (2000) Surveillance for waterborne-disease outbreaks-United States, 1997-1998. MMWR CDC Surveill Summ 49: 1-21.
2. Savioli L, Smith H, Thompson A, (2006) Giardia and Cryptosporidium join the 'Neglected Diseases Initiative'. Trends Parasitol 22: 203-208.
3. Adam RD, Nigam A, Seshadri V, Martens CA, Farneth GA, et al. (2010) The Giardia lamblia vsp gene repertoire: characteristics, genomic organization, and evolution. BMC Genomics 11: 424.
4. Nash TE, Banks SM, Alling DW, Merritt JW Jr, Conrad JT, (1990) Frequency of variant antigens in Giardia lamblia. Exp Parasitol 71: 415-421.
5. Nash TE, Lujan HT, Mowatt MR, Conrad JT, (2001) Variant-specific surface protein switching in Giardia lamblia. Infect Immun 69: 1922-1923.
6. Deitsch KW, Lukehart SA, Stringer JR, (2009) Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nat Rev Microbiol 7: 493-503.
7. Li W, Saraiya AA, Wang CC, (2013) Experimental Verification of the Identity of Variant-Specific Surface Proteins in Giardia lamblia Trophozoites. MBio 4: e00321-13.
8. Mowatt MR, Aggarwal A, Nash TE, (1991) Carboxy-terminal sequence conservation among variant-specific surface proteins of Giardia lamblia. Mol Biochem Parasitol 49: 215-227.
9. Nash TE, Mowatt MR, (1992) Characterization of a Giardia lamblia variant-specific surface protein (VSP) gene from isolate GS/M and estimation of the VSP gene repertoire size. Mol Biochem Parasitol 51: 219-227.
10. Prucca CG, Slavin I, Quiroga R, Elias EV, Rivero FD, et al. (2008) Antigenic variation in Giardia lamblia is regulated by RNA interference. Nature 456: 750-754.
11. Faghiri Z, Widmer G, (2011) A comparison of the Giardia lamblia trophozoite and cyst transcriptome using microarrays. BMC Microbiol 11: 91.
12. Li W, Saraiya AA, Wang CC, (2011) Gene regulation in Giardia lambia involves a putative microRNA derived from a small nucleolar RNA. PLoS Negl Trop Dis 5: e1338.
13. Li W, Saraiya AA, Wang CC, (2012) The profile of snoRNA-derived microRNAs that regulate expression of variant surface proteins in Giardia lamblia. Cell Microbiol 14: 1455-73.
14. Saraiya AA, Li W, Wang CC, (2011) A microRNA derived from an apparent canonical biogenesis pathway regulates variant surface protein gene expression in Giardia lamblia. RNA 17: 2152-2164.
15. Saraiya AA, Li W, Wang CC, (2013) Transition of a microRNA from repressing to activating translation depending on the extent of base pairing with the target. PLoS One 8: e55672.
16. Saraiya AA, Wang CC, (2008) snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 4: e1000224.
17. Krol J, Loedige I, Filipowicz W, (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11: 597-610.
18. Bazzini AA, Lee MT, Giraldez AJ, (2012) Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 336: 233-237.
19. Djuranovic S, Nahvi A, Green R, (2012) miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336: 237-240.
20. Bartel DP, (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
21. Pasquinelli AE, (2012) MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 13: 271-282.
22. Duursma AM, Kedde M, Schrier M, le Sage C, Agami R, (2008) miR-148 targets human DNMT3b protein coding region. RNA 14: 872-877.
23. Elcheva I, Goswami S, Noubissi FK, Spiegelman VS, (2009) CRD-BP protects the coding region of betaTrCP1 mRNA from miR-183-mediated degradation. Mol Cell 35: 240-246.
24. Mandke P, Wyatt N, Fraser J, Bates B, Berberich SJ, et al. (2012) MicroRNA-34a modulates MDM4 expression via a target site in the open reading frame. PLoS One 7: e42034.
25. Shen WF, Hu YL, Uttarwar L, Passegue E, Largman C, (2008) MicroRNA-126 regulates HOXA9 by binding to the homeobox. Mol Cell Biol 28: 4609-4619.
26. Tay YM, Tam WL, Ang YS, Gaughwin PM, Yang H, et al. (2008) MicroRNA-134 modulates the differentiation of mouse embryonic stem cells, where it causes post-transcriptional attenuation of Nanog and LRH1. Stem Cells 26: 17-29.
27. Yi C, Xie WD, Li F, Lv Q, He J, et al. (2011) MiR-143 enhances adipogenic differentiation of 3T3-L1 cells through targeting the coding region of mouse pleiotrophin. FEBS Lett 585: 3303-3309.
28. Jung HM, Patel RS, Phillips BL, Wang H, Cohen DM, et al. (2013) Tumor suppressor miR-375 regulates MYC expression via repression of CIP2A coding sequence through multiple miRNA-mRNA interactions. Mol Biol Cell 24: 1638-1637, 1638-1648, S1631-1637.
29. Qin W, Shi Y, Zhao B, Yao C, Jin L, et al. (2010) miR-24 regulates apoptosis by targeting the open reading frame (ORF) region of FAF1 in cancer cells. PLoS One 5: e9429.
30. Forman JJ, Legesse-Miller A, Coller HA, (2008) A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc Natl Acad Sci U S A 105: 14879-14884.
31. Gu S, Jin L, Zhang F, Sarnow P, Kay MA, (2009) Biological basis for restriction of microRNA targets to the 3′ untranslated region in mammalian mRNAs. Nat Struct Mol Biol 16: 144-150.
32. Chi SW, Zang JB, Mele A, Darnell RB, (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486.
33. Zisoulis DG, Lovci MT, Wilbert ML, Hutt KR, Liang TY, et al. (2010) Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat Struct Mol Biol 17: 173-179.
34. Fang Z, Rajewsky N, (2011) The impact of miRNA target sites in coding sequences and in 3′UTRs. PLoS One 6: e18067.
35. Adam RD, (2000) The Giardia lamblia genome. Int J Parasitol 30: 475-484.
36. Adam RD, (2001) Biology of Giardia lamblia. Clin Microbiol Rev 14: 447-475.
37. Franzen O, Jerlstrom-Hultqvist J, Einarsson E, Ankarklev J, Ferella M, et al. (2013) Transcriptome profiling of Giardia intestinalis using strand-specific RNA-seq. PLoS Comput Biol 9: e1003000.
38. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
39. Aurrecoechea C, Brestelli J, Brunk BP, Carlton JM, Dommer J, et al. (2009) GiardiaDB and TrichDB: integrated genomic resources for the eukaryotic protist pathogens Giardia lamblia and Trichomonas vaginalis. Nucleic Acids Res 37: D526-530.
40. Macrae IJ, Zhou K, Li F, Repic A, Brooks AN, et al. (2006) Structural basis for double-stranded RNA processing by Dicer. Science 311: 195-198.
41. Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, et al. (1994) Fast folding and comparison of RNA secondary structures. Monatshefte für Chemie/Chemical Monthly 125: 167-188.
42. Hofacker IL, Stadler PF, (2006) Memory efficient folding algorithms for circular RNA secondary structures. Bioinformatics 22: 1172-1176.
43. MacRae IJ, Zhou K, Doudna JA, (2007) Structural determinants of RNA recognition and cleavage by Dicer. Nat Struct Mol Biol 14: 934-940.
44. Park JE, Heo I, Tian Y, Simanshu DK, Chang H, et al. (2011) Dicer recognizes the 5′ end of RNA for efficient and accurate processing. Nature 475: 201-205.
45. Ey PL, Mansouri M, Kulda J, Nohynkova E, Monis PT, et al. (1997) Genetic analysis of Giardia from hoofed farm animals reveals artiodactyl-specific and potentially zoonotic genotypes. J Eukaryot Microbiol 44: 626-635.
46. Jerlstrom-Hultqvist J, Franzen O, Ankarklev J, Xu F, Nohynkova E, et al. (2010) Genome analysis and comparative genomics of a Giardia intestinalis assemblage E isolate. BMC Genomics 11: 543.
47. John B, Enright AJ, Aravin A, Tuschl T, Sander C, et al. (2004) Human MicroRNA targets. PLoS Biol 2: e363.
48. Li L, Wang CC, (2004) Capped mRNA with a single nucleotide leader is optimally translated in a primitive eukaryote, Giardia lamblia. J Biol Chem 279: 14656-14664.
49. Keister DB, (1983) Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 77: 487-488.