A Tetrahymena Hsp90 co-chaperone promotes siRNA loading by ATP-dependent and ATP-independent mechanisms

EMBO Journal

Volumn 34, Issue 4, 2015, Pages 559-577

  Woehrer, Sophie L ^a   Aronica, Lucia ^a,b   Suhren, Jan H ^a   Busch, Clara Jana Lui ^a   Noto, Tomoko ^a   Mochizuki, Kazufumi ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

Argonaute protein; Risc assembly; RNAi; SiRNA; Tetrahymena

Indexed keywords

ADENOSINE TRIPHOSPHATE; ARGONAUTE PROTEIN; BINDING PROTEIN; CELL CYCLE PROTEIN 37; COI12P PROTEIN; GIW1P PROTEIN; HEAT SHOCK PROTEIN 90; RECOMBINANT PROTEIN; SMALL INTERFERING RNA; TWI1P PROTEIN; UNCLASSIFIED DRUG; CHAPERONE; MICRORNA;

ANIMAL CELL; ARTICLE; CELL LYSATE; CONJUGATION; EXPRESSED SEQUENCE TAG; FLUORESCENCE IN SITU HYBRIDIZATION; FUNCTIONAL ASSESSMENT; GENE EXPRESSION; HIGH THROUGHPUT SEQUENCING; HUMAN; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REPRODUCTION; TETRAHYMENA THERMOPHILA; TETRATRICOPEPTIDE REPEAT; WESTERN BLOTTING; METABOLISM; TETRAHYMENA;

EUKARYOTA; TETRAHYMENA;

ARGONAUTE PROTEINS; HSP90 HEAT-SHOCK PROTEINS; MICRORNAS; MOLECULAR CHAPERONES; RNA, SMALL INTERFERING; TETRAHYMENA;

EID: 84923105546     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201490062     Document Type: Article

References (61)

1. Albe KR, Butler MH, Wright BE (1990) Cellular concentrations of enzymes and their substrates. J Theor Biol 143: 163-195
2. Aronica L, Bednenko J, Noto T, DeSouza LV, Siu KW, Loidl J, Pearlman RE, Gorovsky MA, Mochizuki K (2008) Study of an RNA helicase implicates small RNA-noncoding RNA interactions in programmed DNA elimination in Tetrahymena. Genes Dev 22: 2228-2241
3. Betancur JG, Tomari Y (2012 ) Dicer is dispensable for asymmetric RISC loading in mammals. RNA 18: 24-30
4. Busch CJ, Vogt A, Mochizuki K (2010) Establishment of a Cre/loxP recombination system for N-terminal epitope tagging of genes in Tetrahymena. BMC Microbiol 10: 191
5. Chalker DL, Meyer E, Mochizuki K (2013) Epigenetics of ciliates. Cold Spring Harbor Perspect Biol 5: a017764
6. Couvillion MT, Lee SR, Hogstad B, Malone CD, Tonkin LA, Sachidanandam R, Hannon GJ, Collins K (2009) Sequence, biogenesis, and function of diverse small RNA classes bound to the Piwi family proteins of Tetrahymena thermophila. Genes Dev 23: 2016-2032
7. Dueck A, Meister G (2014 ) Assembly and function of small RNA - Argonaute protein complexes. Biol Chem 395: 611-629
8. Elkayam E, Kuhn CD, Tocilj A, Haase AD, Greene EM, Hannon GJ, Joshua-Tor L (2012) The structure of human argonaute-2 in complex with miR-20 a. Cell 150: 100-110
9. Fass JN, Joshi NA, Couvillion MT, Bowen J, Gorovsky MA, Hamilton EP, Orias E, Hong K, Coyne RS, Eisen JA, et al (2011) Genome-scale analysis of programmed DNA elimination sites in Tetrahymena thermophila. G3 1: 515-522
10. Gaertig J, Thatcher TH, Gu L, Gorovsky MA (1994) Electroporation-mediated replacement of a positively and negatively selectable beta-tubulin gene in Tetrahymena thermophila. Proc Natl Acad Sci USA 91: 4549-4553
11. Galat A (2008) Functional drift of sequence attributes in the FK506-binding proteins (FKBPs). J Chem Inf Model 48: 1118-1130
12. Gorovsky MA, Yao MC, Keevert JB, Pleger GL (1975 ) Isolation of micro- and macronuclei of Tetrahymena pyriformis. Methods Cell Biol 9: 311-327
13. Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R (2005 ) Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123: 631-640
14. Haslbeck V, Eckl JM, Kaiser CJ, Papsdorf K, Hessling M, Richter K (2013) Chaperone-interacting TPR proteins in Caenorhabditis elegans. J Mol Biol 425: 2922-2939
15. Iki T, Yoshikawa M, Nishikiori M, Jaudal MC, Matsumoto-Yokoyama E, Mitsuhara I, Meshi T, Ishikawa M (2010) In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol Cell 39: 282-291
16. Iki T, Yoshikawa M, Meshi T, Ishikawa M ( 2012) Cyclophilin 40 facilitates HSP90-mediated RISC assembly in plants. EMBO J 31: 267-278
17. Iwasaki S, Kobayashi M, Yoda M, Sakaguchi Y, Katsuma S, Suzuki T, Tomari Y (2010) Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol Cell 39: 292-299
18. Izumi N, Kawaoka S, Yasuhara S, Suzuki Y, Sugano S, Katsuma S, Tomari Y (2013) Hsp90 facilitates accurate loading of precursor piRNAs into PIWI proteins. RNA 19: 896-901
19. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K (2005 ) Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19: 489-501
20. Kawamata T, Seitz H, Tomari Y (2009) Structural determinants of miRNAs for RISC loading and slicer-independent unwinding. Nat Struct Mol Biol 16: 953-960
21. Kawamata T, Tomari Y (2010) Making RISC. Trends Biochem Sci 35: 368-376
22. Lee SR, Collins K (2006 ) Two classes of endogenous small RNAs in Tetrahymena thermophila. Genes Dev 20: 28-33
23. Lee SR, Collins K (2007) Physical and functional coupling of RNA-dependent RNA polymerase and Dicer in the biogenesis of endogenous siRNAs. Nat Struct Mol Biol 14: 604-610
24. Liu Q, Rand TA, Kalidas S, Du F, Kim HE, Smith DP, Wang X (2003) R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301: 1921-1925
25. Liu X, Jiang F, Kalidas S, Smith D, Liu Q (2006) Dicer-2 and R2D2 coordinately bind siRNA to promote assembly of the siRISC complexes. RNA 12: 1514-1520
26. Liu Y, Taverna SD, Muratore TL, Shabanowitz J, Hunt DF, Allis CD (2007) RNAi-dependent H 3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena. Genes Dev 21: 1530-1545
27. MacRae IJ, Ma E, Zhou M, Robinson CV, Doudna JA (2008) In vitro reconstitution of the human RISC-loading complex. Proc Natl Acad Sci USA 105: 512-517
28. Malone CD, Anderson AM, Motl JA, Rexer CH, Chalker DL (2005) Germ line transcripts are processed by a Dicer-like protein that is essential for developmentally programmed genome rearrangements of Tetrahymena thermophila . Mol Cell Biol 25: 9151-9164
29. Maniataki E, Mourelatos Z (2005) A human, ATP-independent, RISC assembly machine fueled by pre-miRNA. Genes Dev 19: 2979-2990
30. Martinez J, Patkaniowska A, Urlaub H, Luhrmann R, Tuschl T ( 2002) Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 110: 563-574
31. Martinez NJ, Chang HM, Borrajo Jde R, Gregory RI (2013) The co-chaperones Fkbp4 /5 control Argonaute2 expression and facilitate RISC assembly. RNA 19: 1583-1593
32. Miao W, Xiong J, Bowen J, Wang W, Liu Y, Braguinets O, Grigull J, Pearlman RE, Orias E, Gorovsky MA (2009) Microarray analyses of gene expression during the Tetrahymena thermophila life cycle. PLoS ONE 4: e4429
33. Miyoshi K, Tsukumo H, Nagami T, Siomi H, Siomi MC (2005) Slicer function of Drosophila Argonautes and its involvement in RISC formation. Genes Dev 19: 2837-2848
34. Miyoshi T, Takeuchi A, Siomi H, Siomi MC (2010) A direct role for Hsp90 in pre-RISC formation in Drosophila. Nat Struct Mol Biol 17: 1024-1026
35. Mochizuki K, Fine NA, Fujisawa T, Gorovsky MA (2002) Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell 110: 689-699
36. Mochizuki K, Gorovsky MA (2004) Conjugation-specific small RNAs in Tetrahymena have predicted properties of scan (scn) RNAs involved in genome rearrangement. Genes Dev 18: 2068-2073
37. Mochizuki K, Gorovsky MA (2005) A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev 19: 77-89
38. Mochizuki K (2008) High efficiency transformation of Tetrahymena using a codon-optimized neomycin resistance gene. Gene 425: 79-83
39. Mochizuki K, Kurth HM (2013) Loading and pre-loading processes generate a distinct siRNA population in Tetrahymena. Biochem Biophys Res Commun 436: 497-502
40. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ (2005) Characterization of Dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci USA 102: 12135-12140
41. Nakanishi K, Weinberg DE, Bartel DP, Patel DJ (2012) Structure of yeast Argonaute with guide RNA. Nature 486: 368-374
42. Noto T, Kurth HM, Kataoka K, Aronica L, DeSouza LV, Siu KW, Pearlman RE, Gorovsky MA, Mochizuki K (2010) The Tetrahymena argonaute-binding protein Giw1p directs a mature argonaute-siRNA complex to the nucleus. Cell 140: 692-703
43. Noto T, Kurth HM, Mochizuki K (2014) Analysis of Piwi-loaded small RNAs in Tetrahymena. Methods Mol Biol 1093: 209-224
44. Olivieri D, Senti KA, Subramanian S, Sachidanandam R, Brennecke J (2012) The cochaperone shutdown defines a group of biogenesis factors essential for all piRNA populations in Drosophila. Mol Cell 47: 954-969
45. Pare JM, LaPointe P, Hobman TC (2013) Hsp 90 cochaperones p23 and FKBP4 physically interact with hAgo2 and activate RNA interference-mediated silencing in mammalian cells. Mol Biol Cell 24: 2303-2310
46. Pearl LH, Prodromou C (2006) Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75: 271-294
47. Pham JW, Pellino JL, Lee YS, Carthew RW, Sontheimer EJ (2004) A Dicer-2-dependent 80 s complex cleaves targeted mRNAs during RNAi in Drosophila. Cell 117: 83-94
48. Preall JB, Czech B, Guzzardo PM, Muerdter F, Hannon GJ (2012) Shutdown is a component of the Drosophila piRNA biogenesis machinery. RNA 18: 1446-1457
49. Rivas FV, Tolia NH, Song JJ, Aragon JP, Liu J, Hannon GJ, Joshua-Tor L (2005) Purified Argonaute2 and an siRNA form recombinant human RISC. Nat Struct Mol Biol 12: 340-349
50. Rohl A, Rohrberg J, Buchner J (2013) The chaperone Hsp90: changing partners for demanding clients. Trends Biochem Sci 38: 253-262
51. Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, Hartl FU, Moarefi I (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp 90 multichaperone machine. Cell 101: 199-210
52. Schoeberl UE, Kurth HM, Noto T, Mochizuki K (2012) Biased transcription and selective degradation of small RNAs shape the pattern of DNA elimination in Tetrahymena. Genes Dev 26: 1729-1742
53. Shang Y, Song X, Bowen J, Corstanje R, Gao Y, Gaertig J, Gorovsky MA (2002) A robust inducible-repressible promoter greatly facilitates gene knockouts, conditional expression, and overexpression of homologous and heterologous genes in Tetrahymena thermophila. Proc Natl Acad Sci USA 99: 3734-3739
54. Taipale M, Jarosz DF, Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11: 515-528
55. Taverna SD, Coyne RS, Allis CD (2002) Methylation of histone h3 at lysine 9 targets programmed DNA elimination in Tetrahymena. Cell 110: 701-711
56. Vogt A, Mochizuki K (2013 ) A domesticated piggybac transposase interacts with heterochromatin and catalyzes reproducible DNA elimination in Tetrahymena. PLoS Genet 9: e1004032
57. Wang Y, Sheng G, Juranek S, Tuschl T, Patel DJ (2008) Structure of the guide-strand-containing argonaute silencing complex. Nature 456: 209-213
58. Williams NE, Nelsen EM (1997) HSP70 and HSP90 homologs are associated with tubulin in hetero-oligomeric complexes, cilia and the cortex of Tetrahymena. J Cell Sci 110: 1665-1672
59. Wuitschick JD, Gershan JA, Lochowicz AJ, Li S, Karrer KM (2002) A novel family of mobile genetic elements is limited to the germline genome in Tetrahymena thermophila. Nucleic Acids Res 30: 2524-2537
60. Xiol J, Cora E, Koglgruber R, Chuma S, Subramanian S, Hosokawa M, Reuter M, Yang Z, Berninger P, Palencia A, et al (2012) A role for Fkbp6 and the chaperone machinery in piRNA amplification and transposon silencing. Mol Cell 47: 970-979
61. Yoda M, Kawamata T, Paroo Z, Ye X, Iwasaki S, Liu Q, Tomari Y (2010) ATP-dependent human RISC assembly pathways. Nat Struct Mol Biol 17: 17-23