Mutations in Conserved Residues of the C. elegans microRNA Argonaute ALG-1 Identify Separable Functions in ALG-1 miRISC Loading and Target Repression

PLoS Genetics

Volumn 10, Issue 4, 2014, Pages

  Zinovyeva, Anna Y ^a   Bouasker, Samir ^b   Simard, Martin J ^b   Hammell, Christopher M ^c   Ambros, Victor ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b LAVAL UNIVERSITY   (Canada)

^c Simons Center for Quantitative Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 1 PROTEIN; DICER; MICRORNA; MICRORNA INDUCED SILENCING COMPLEX; UNCLASSIFIED DRUG; AIN-1 PROTEIN, C ELEGANS; ARGONAUTE PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; CARRIER PROTEIN; LIN-28 PROTEIN, C ELEGANS; REPRESSOR PROTEIN;

ALG 1 GENE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GENE; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOSS; GENE MUTATION; GENE REPRESSION; GENETIC ASSOCIATION; GENETIC LOAD; IMMUNOPRECIPITATION; LIN 28 (IF) GENE; NONHUMAN; PHENOTYPE; PROTEIN CLEAVAGE; RNA PROCESSING; ALLELE; AMINO ACID SEQUENCE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; ARGONAUTE PROTEINS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARRIER PROTEINS; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICRORNAS; MOLECULAR SEQUENCE DATA; MUTATION; REPRESSOR PROTEINS; SEQUENCE ALIGNMENT;

EID: 84901343744     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004286     Document Type: Article

References (72)

1. Resnick TD, McCulloch KA, Rougvie AE, (2010) miRNAs give worms the time of their lives: Small RNAs and temporal control in Caenorhabditis elegans. Dev Dyn 239: 1477-1489 doi:10.1002/dvdy.22260.
2. Abbott AL, Alvarez-Saavedra E, Miska EA, Lau NC, Bartel DP, et al. (2005) The let-7 MicroRNA Family Members mir-48, mir-84, and mir-241 Function Together to Regulate Developmental Timing in Caenorhabditis elegans. Developmental Cell 9: 403-414 doi:10.1016/j.devcel.2005.07.009.
3. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, et al. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403: 901-906.
4. Fabian MR, Sonenberg N, (2012) The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol 19: 586-593 doi:10.1038/nsmb.2296.
5. Fabian MR, Sonenberg N, Filipowicz W, (2010) Regulation of mRNA Translation and Stability by microRNAs. Annu Rev Biochem 79: 351-379 doi:10.1146/annurev-biochem-060308-103103.
6. Ding XC, Weiler J, Großhans H, (2009) Regulating the regulators: mechanisms controlling the maturation of microRNAs. Trends in Biotechnology 27: 27-36 doi:10.1016/j.tibtech.2008.09.006.
7. Filipowicz W, Bhattacharyya SN, Sonenberg N, (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nature Publishing Group 2008: 102-114 doi:10.1038/nrg2290.
8. Bouasker S, Simard MJ, (2012) The slicing activity of miRNA-specific Argonautes is essential for the miRNA pathway in C. elegans. Nucleic Acids Research 40: 10452-10462 doi:10.1093/nar/gks748.
9. Grishok A, Pasquinelli AE, Conte D, Li N, Parrish S, et al. (2001) Genes and Mechanisms Related to RNA Interference Regulate Expression of the Small Temporal RNAs that Control C. elegans Developmental Timing. Cell 106: 23-34.
10. Meister G, (2013) Argonaute proteins: functional insights and emerging roles. Nature Publishing Group 14: 447-459 doi:10.1038/nrg3462.
11. Zhang L, Ding L, Cheung TH, Dong M-Q, Chen J, et al. (2007) Systematic Identification of C. elegans miRISC Proteins, miRNAs, and mRNA Targets by Their Interactions with GW182 Proteins AIN-1 and AIN-2. Molecular Cell 28: 598-613 doi:10.1016/j.molcel.2007.09.014.
12. Ding L, Spencer A, Morita K, Han M, (2005) The Developmental Timing Regulator AIN-1 Interacts with miRISCs and May Target the Argonaute Protein ALG-1 to Cytoplasmic P Bodies in C. elegans. Molecular Cell 19: 437-447 doi:10.1016/j.molcel.2005.07.013.
13. Eulalio A, Huntzinger E, Izaurralde E, (2008) GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat Struct Mol Biol 15: 346-353 doi:10.1038/nsmb.1405.
14. REHWINKEL J, (2005) A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 11: 1640-1647 doi:10.1261/rna.2191905.
15. Liu J, Rivas FV, Wohlschlegel J, Yates JR, Parker R, et al. (2005) A role for the P-body component GW182 in microRNA function. Nature Cell Biology 7: 1261-1266 doi:10.1038/ncb1333.
16. Jakymiw A, Lian S, Eystathioy T, Li S, Satoh M, et al. (2005) Disruption of GW bodies impairs mammalian RNA interference. Nature Cell Biology 7: 1267-1274 doi:10.1038/ncb1334.
17. Meister G, Landthaler M, Peters L, Chen PY, Urlaub H, et al. (2005) Identification of Novel Argonaute-Associated Proteins. Current Biology 15: 2149-2155 doi:10.1016/j.cub.2005.10.048.
18. Moss EG, Lee RC, Ambros V, (1997) The Cold Shock Domain Protein LIN-28 Controls Developmental Timing in C. elegans and Is Regulated by the lin-4 RNA. Cell 88: 637-646.
19. Ambros V, Horvitz HR, (1984) Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226: 409-416.
20. Vadla B, Kemper K, Alaimo J, Heine C, Moss EG, (2012) lin-28 controls the succession of cell fate choices via two distinct activities. 8: 11 doi:10.1371/journal.pgen.1002588.
21. Van Wynsberghe PM, Kai ZS, Massirer KB, Burton VH, Yeo GW, et al. (2011) LIN-28 co-transcriptionally binds primary let-7 to regulate miRNA maturation in Caenorhabditis elegans. Nat Struct Mol Biol 18: 302-308 doi:10.1038/nsmb.1986.
22. Lehrbach NJ, Armisen J, Lightfoot HL, Murfitt KJ, Bugaut A, et al. (2009) LIN-28 and the poly(U) polymerase PUP-2 regulate let-7 microRNA processing in Caenorhabditis elegans. Nat Struct Mol Biol 16: 1016-1020 doi:10.1038/nsmb.1675.
23. Hagan JP, Piskounova E, Gregory RI, (2009) Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat Struct Mol Biol 16: 1021-1025 doi:10.1038/nsmb.1676.
24. Heo I, Joo C, Kim Y-K, Ha M, Yoon M-J, et al. (2009) TUT4 in Concert with Lin28 Suppresses MicroRNA Biogenesis through Pre-MicroRNA Uridylation. Cell 138: 696-708 doi:10.1016/j.cell.2009.08.002.
25. Heo I, Joo C, Cho J, Ha M, Han J, et al. (2008) Lin28 Mediates the Terminal Uridylation of let-7 Precursor MicroRNA. Molecular Cell 32: 276-284 doi:10.1016/j.molcel.2008.09.014.
26. Newman MA, Thomson JM, Hammond SM, (2008) Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 14: 1539-1549 doi:10.1261/rna.1155108.
27. Piskounova E, Viswanathan SR, Janas M, LaPierre RJ, Daley GQ, et al. (2008) Determinants of MicroRNA Processing Inhibition by the Developmentally Regulated RNA-binding Protein Lin28. Journal of Biological Chemistry 283: 21310-21314 doi:10.1074/jbc.C800108200.
28. Viswanathan SR, Daley GQ, Gregory RI, (2008) Selective Blockade of MicroRNA Processing by Lin28. Science 320: 97-100 doi:10.1126/science.1154040.
29. Abrahante JE, Daul AL, Li M, Volk ML, Tennessen JM, et al. (2003) The Caenorhabditis elegans hunchback-like Gene lin-57/hbl-1 Controls Developmental Time and Is Regulated by MicroRNAs. Developmental Cell 4: 625-637.
30. Lin S-Y, Johnson SM, Abraham M, Vella MC, Pasquinelli A, et al. (2003) The C elegans hunchback homolog, hbl-1, controls temporal patterning and is a probable microRNA target. Developmental Cell 4: 639-650.
31. Roush SF, Slack FJ, (2009) Transcription of the C. elegans let-7 microRNA is temporally regulated by one of its targets, hbl-1. Dev Biol 334: 523-534 doi:10.1016/j.ydbio.2009.07.012.
32. Morita KK, Han MM, (2006) Multiple mechanisms are involved in regulating the expression of the developmental timing regulator lin-28 in Caenorhabditis elegans. EMBO J 25: 5794-5804 doi:10.1038/sj.emboj.7601451.
33. Moss EG, (2007) Heterochronic Genes and the Nature of Developmental Time. Current Biology 17: R425-R434 Available: http://www.sciencedirect.com/science/article/pii/S0960982207011475.
34. Euling S, Ambros V, (1996) Heterochronic genes control cell cycle progress and developmental competence of C. elegans vulva precursor cells. Cell 84: 667-676 doi:10.1016/S0092-8674(00)81045-4.
35. Pepper ASR, (2004) The C. elegans heterochronic gene lin-46 affects developmental timing at two larval stages and encodes a relative of the scaffolding protein gephyrin. Development 131: 2049-2059 doi:10.1242/dev.01098.
36. Johnston RJ, Hobert O, (2003) A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 426: 845-849 doi:10.1038/nature02255.
37. Sarin S, O'Meara MM, Flowers EB, Antonio C, Poole RJ, et al. (2007) Genetic Screens for Caenorhabditis elegans Mutants Defective in Left/Right Asymmetric Neuronal Fate Specification. Genetics 176: 2109-2130 doi:10.1534/genetics.107.075648.
38. Chang SS, Johnston RJR, Hobert OO, (2003) A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans. Genes & Development 17: 2123-2137 doi:10.1101/gad.1117903.
39. Vasquez-Rifo A, Jannot G, Armisen J, Labouesse M, Bukhari SIA, et al. (2012) Developmental Characterization of the MicroRNA-Specific C. elegans Argonautes alg-1 and alg-2. PLoS ONE 7: e33750 doi:10.1371/journal.pone.0033750.s005.
40. Alvarez-Saavedra E, Horvitz HR, (2010) Many Families of C. elegans MicroRNAs Are Not Essential for Development or Viability. Current Biology 20: 367-373 doi:10.1016/j.cub.2009.12.051.
41. Miska EA, Alvarez-Saavedra E, Abbott AL, Lau NC, Hellman AB, et al. (2007) Most Caenorhabditis elegans microRNAs Are Individually Not Essential for Development or Viability. PLoS Genet 3: e215 doi:10.1371/journal.pgen.0030215.st003.
42. Brenner JL, Jasiewicz KL, Fahley AF, Kemp BJ, Abbott AL, (2010) Loss of Individual MicroRNAs Causes Mutant Phenotypes in Sensitized Genetic Backgrounds in C. elegans. Current Biology 20: 1321-1325 doi:10.1016/j.cub.2010.05.062.
43. Frank F, Sonenberg N, Nagar B, (2010) Structural basis for 5′-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 465: 818-822 doi:10.1038/nature09039.
44. Wang Y, Juranek S, Li H, Sheng G, Wardle GS, et al. (2009) Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 461: 754-761 doi:10.1038/nature08434.
45. Ma J-B, Yuan Y-R, Meister G, Pei Y, Tuschl T, et al. (2005) Structural basis for 5′-end-specific recognition of guide RNA by the A. fulgidus Piwi protein. Nature Cell Biology 434: 666-670 doi:10.1038/nature03514.
46. Parker JS, Roe SM, Barford D, (2005) Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature 434: 663-666 doi:10.1038/nature03462.
47. Wang Y, Juranek S, Li H, Sheng G, Tuschl T, et al. (2008) Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456: 921-926 doi:10.1038/nature07666.
48. Wang Y, Sheng G, Juranek S, Tuschl T, Patel DJ, (2008) Structure of the guide-strand-containing argonaute silencing complex. Nature 456: 209-213 doi:10.1038/nature07315.
49. Ma J-B, Ye K, Patel DJ, (2004) Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429: 318-322 doi:10.1038/nature02519.
50. Schirle NT, MacRae IJ, (2012) The Crystal Structure of Human Argonaute2. Science 336: 1037-1040 doi:10.1126/science.1221551.
51. Nakanishi K, Weinberg DE, Bartel DP, Patel DJ, (2012) Structure of yeast Argonaute with guide RNA. Nature 486: 368-374 doi:10.1038/nature11211.
52. Duchaine TF, Wohlschlegel JA, Kennedy S, Bei Y, Conte D Jr, et al. (2006) Functional Proteomics Reveals the Biochemical Niche of C. elegans DCR-1 in Multiple Small-RNA-Mediated Pathways. Cell 124: 343-354 doi:10.1016/j.cell.2005.11.036.
53. Sawh AN, Duchaine TF, (2013) A Truncated Form of Dicer Tilts the Balance of RNA Interference Pathways. Cell Reports 4: 454-463 doi:10.1016/j.celrep.2013.07.013.
54. Wildwater M, Sander N, de Vreede G, van den Heuvel S, (2011) Cell shape and Wnt signaling redundantly control the division axis of C. elegans epithelial stem cells. Development 138: 4375-4385 doi:10.1242/dev.066431.
55. TOPS BBJ, PLASTERK RHA, KETTING RF, (2006) The Caenorhabditis elegans Argonautes ALG-1 and ALG-2: Almost Identical yet Different. Cold Spring Harbor Symposia on Quantitative Biology 71: 189-194 doi:10.1101/sqb.2006.71.035.
56. Liu J, (2004) Argonaute2 Is the Catalytic Engine of Mammalian RNAi. Science 305: 1437-1441 doi:10.1126/science.1102513.
57. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, et al. (2004) Human Argonaute2 Mediates RNA Cleavage Targeted by miRNAs and siRNAs. Molecular Cell 15: 185-197 doi:10.1016/j.molcel.2004.07.007.
58. PILLAI RS, (2004) Tethering of human Ago proteins to mRNA mimics the miRNA-mediated repression of protein synthesis. RNA 10: 1518-1525 doi:10.1261/rna.7131604.
59. Kumar MS, Lu J, Mercer KL, Golub TR, Jacks T, (2007) Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet 39: 673-677 doi:10.1038/ng2003.
60. Koesters R, Adams V, Betts D, Moos R, Schmid M, et al. (1999) Human eukaryotic initiation factor EIF2C1 gene: cDNA sequence, genomic organization, localization to chromosomal bands 1p34-p35, and expression. Genomics 61: 210-218 doi:10.1006/geno.1999.5951.
61. Dome JS, Coppes MJ, (2002) Recent advances in Wilms tumor genetics. Curr Opin Pediatr 14: 5-11.
62. Kim MS, Oh JE, Kim YR, Park SW, Kang MR, et al. (2010) Somatic mutations and losses of expression of microRNA regulationrelated genes AGO2 and TNRC6A in gastric and colorectal cancers. J Pathol 221: 139-146 doi:10.1002/path.2683.
63. Bahubeshi AA, Tischkowitz MM, Foulkes WDW, (2011) miRNA processing and human cancer: DICER1 cuts the mustard. Sci Transl Med 3: 111ps46-111ps46 doi:10.1126/scitranslmed.3002493.
64. Kumar MS, Pester RE, Chen CY, Lane K, Chin C, et al. (2009) Dicer1 functions as a haploinsufficient tumor suppressor. Genes & Development 23: 2700-2704 doi:10.1101/gad.1848209.
65. Brenner S, (1974) The Genetics of CAENORHABDITIS ELEGANS. Genetics 77: 71-94.
66. Wicks SR, Yeh RT, Gish WR, Waterston RH, Plasterk RH, (2001) Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 28: 160-164 doi:10.1038/88878.
67. Abrahante JE, Miller EA, Rougvie AE, (1998) Identification of heterochronic mutants in Caenorhabditis elegans: temporal misexpression of a collagen:: green fluorescent protein fusion gene. Genetics 149: 1335-1351.
68. Chapin SC, Appleyard DC, Pregibon DC, Doyle PS, (2011) Rapid microRNA Profiling on Encoded Gel Microparticles. Angew Chem Int Ed 50: 2289-2293 doi:10.1002/anie.201006523.
69. LEE RC, (2006) Interacting endogenous and exogenous RNAi pathways in Caenorhabditis elegans. RNA 12: 589-597 doi:10.1261/rna.2231506.
70. LEE RC, (2001) An Extensive Class of Small RNAs in Caenorhabditis elegans. Science 294: 862-864 doi:10.1126/science.1065329.
71. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J, (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biology 2: RESEARCH0002 doi:10.1186/gb-2000-2-1-research0002.
72. Zou Y, Chiu H, Zinovyeva A, Ambros V, Chuang C-F, et al. (2013) Developmental decline in neuronal regeneration by the progressive change of two intrinsic timers. Science 340: 372-376 doi:10.1126/science.1231321.