The R2TP complex: Discovery and functions

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 1, 2012, Pages 101-107

  Kakihara, Yoshito ^a   Houry, Walid A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Complex assembly; Pih1; R2TP; Rvb1; Rvb2; Tah1

Indexed keywords

ATM PROTEIN; ATR PROTEIN; AXONEMAL DYNEIN; DOXORUBICIN; HEAT SHOCK PROTEIN 90; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MULTIPROTEIN COMPLEX; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN COMPLEX R2TP; PROTEIN INTERACTING WITH HEAT SHOCK PROTEIN 90; PROTEIN KINASE; PROTEIN RVB1; PROTEIN RVB2; RNA POLYMERASE II; SMALL NUCLEOLAR RIBONUCLEOPROTEIN; TETRATRICOPEPTIDE REPEAT CONTAINING PROTEIN ASSOCIATED WITH HEAT SHOCK PROTEIN 90; UNCLASSIFIED DRUG;

APOPTOSIS; BIOGENESIS; CELL DEATH; CELL METABOLISM; CHLAMYDOMONAS; CYTOPLASM; HUMAN; MUTANT; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; NUTRIENT AVAILABILITY; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROCESSING; REVIEW; RIBOSOME SUBUNIT; SPERMATOZOON MOTILITY; STOP CODON; TETRATRICOPEPTIDE REPEAT;

ADENOSINE TRIPHOSPHATASES; ANIMALS; APOPTOSIS; DNA HELICASES; DYNEINS; HUMANS; MOLECULAR CHAPERONES; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RIBONUCLEOPROTEINS, SMALL NUCLEOLAR; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 84855199318     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.08.016     Document Type: Review

References (84)

1. Jha S., Dutta A. RVB1/RVB2: running rings around molecular biology. Mol Cell 2009, 34:521-533.
2. Huen J., Kakihara Y., Ugwu F., Cheung K.L., Ortega J., Houry W.A. Rvb1-Rvb2: essential ATP-dependent helicases for critical complexes. Biochem Cell Biol 2010, 88:29-40.
3. Putnam C.D., Clancy S.B., Tsuruta H., Gonzalez S., Wetmur J.G., Tainer J.A. Structure and mechanism of the RuvB Holliday junction branch migration motor. J Mol Biol 2001, 311:297-310.
4. Yamada K., Kunishima N., Mayanagi K., Ohnishi T., Nishino T., Iwasaki H., Shinagawa H., Morikawa K. Crystal structure of the Holliday junction migration motor protein RuvB from Thermus thermophilus HB8. Proc Natl Acad Sci USA 2001, 98:1442-1447.
5. Qiu X.B., Lin Y.L., Thome K.C., Pian P., Schlegel B.P., Weremowicz S., Parvin J.D., Dutta A. An eukaryotic RuvB-like protein (RUVBL1) essential for growth. J Biol Chem 1998, 273:27786-27793.
6. Kanemaki M., Kurokawa Y., Matsu-ura T., Makino Y., Masani A., Okazaki K., Morishita T., Tamura T.A. TIP49b, a new RuvB-like DNA helicase, is included in a complex together with another RuvB-like DNA helicase, TIP49a. J Biol Chem 1999, 274:22437-22444.
7. Bauer A., Chauvet S., Huber O., Usseglio F., Rothbacher U., Aragnol D., Kemler R., Pradel J. Pontin52 and reptin52 function as antagonistic regulators of beta-catenin signalling activity. EMBO J 2000, 19:6121-6130.
8. Lim C.R., Kimata Y., Ohdate H., Kokubo T., Kikuchi N., Horigome T., Kohno K. The Saccharomyces cerevisiae RuvB-like protein, Tih2p, is required for cell cycle progression and RNA polymerase II-directed transcription. J Biol Chem 2000, 275:22409-22417.
9. Parfait B., Giovangrandi Y., Asheuer M., Laurendeau I., Olivi M., Vodovar N., Vidaud D., Vidaud M., Bieche I. Human TIP49b/RUVBL2 gene: genomic structure, expression pattern, physical link to the human CGB/LHB gene cluster on chromosome 19q13.3. Ann Genet 2000, 43:69-74.
10. Fuchs M., Gerber J., Drapkin R., Sif S., Ikura T., Ogryzko V., Lane W.S., Nakatani Y., Livingston D.M. The p400 complex is an essential E1A transformation target. Cell 2001, 106:297-307.
11. Ikura T., Ogryzko V.V., Grigoriev M., Groisman R., Wang J., Horikoshi M., Scully R., Qin J., Nakatani Y. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 2000, 102:463-473.
12. Shen X., Mizuguchi G., Hamiche A., Wu C. A chromatin remodelling complex involved in transcription and DNA processing. Nature 2000, 406:541-544.
13. Jonsson Z.O., Dhar S.K., Narlikar G.J., Auty R., Wagle N., Pellman D., Pratt R.E., Kingston R., Dutta A. Rvb1p and Rvb2p are essential components of a chromatin remodeling complex that regulates transcription of over 5% of yeast genes. J Biol Chem 2001, 276:16279-16288.
14. Krogan N.J., Keogh M.C., Datta N., Sawa C., Ryan O.W., Ding H., Haw R.A., Pootoolal J., Tong A., Canadien V., Richards D.P., Wu X., Emili A., Hughes T.R., Buratowski S., Greenblatt J.F. A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell 2003, 12:1565-1576.
15. Ohdate H., Lim C.R., Kokubo T., Matsubara K., Kimata Y., Kohno K. Impairment of the DNA binding activity of the TATA-binding protein renders the transcriptional function of Rvb2p/Tih2p, the yeast RuvB-like protein, essential for cell growth. J Biol Chem 2003, 278:14647-14656.
16. Jonsson Z.O., Jha S., Wohlschlegel J.A., Dutta A. Rvb1p/Rvb2p recruit Arp5p and assemble a functional Ino80 chromatin remodeling complex. Mol Cell 2004, 16:465-477.
17. Watkins N.J., Lemm I., Ingelfinger D., Schneider C., Hossbach M., Urlaub H., Luhrmann R. Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol Cell 2004, 16:789-798.
18. Jeronimo C., Forget D., Bouchard A., Li Q., Chua G., Poitras C., Therien C., Bergeron D., Bourassa S., Greenblatt J., Chabot B., Poirier G.G., Hughes T.R., Blanchette M., Price D.H., Coulombe B. Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme. Mol Cell 2007, 27:262-274.
19. McKeegan K.S., Debieux C.M., Boulon S., Bertrand E., Watkins N.J. A dynamic scaffold of pre-snoRNP factors facilitates human box C/D snoRNP assembly. Mol Cell Biol 2007, 27:6782-6793.
20. Boulon S., Marmier-Gourrier N., Pradet-Balade B., Wurth L., Verheggen C., Jady B.E., Rothe B., Pescia C., Robert M.C., Kiss T., Bardoni B., Krol A., Branlant C., Allmang C., Bertrand E., Charpentier B. The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J Cell Biol 2008, 180:579-595.
21. Zhao R., Kakihara Y., Gribun A., Huen J., Yang G., Khanna M., Costanzo M., Brost R.L., Boone C., Hughes T.R., Yip C.M., Houry W.A. Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. J Cell Biol 2008, 180:563-578.
22. Choi J., Heo K., An W. Cooperative action of TIP48 and TIP49 in H2A.Z exchange catalyzed by acetylation of nucleosomal H2A. Nucleic Acids Res 2009, 37:5993-6007.
23. McKeegan K.S., Debieux C.M., Watkins N.J. Evidence that the AAA+proteins TIP48 and TIP49 bridge interactions between 15.5K and the related NOP56 and NOP58 proteins during box C/D snoRNP biogenesis. Mol Cell Biol 2009, 29:4971-4981.
24. Izumi N., Yamashita A., Iwamatsu A., Kurata R., Nakamura H., Saari B., Hirano H., Anderson P., Ohno S. AAA+proteins RUVBL1 and RUVBL2 coordinate PIKK activity and function in nonsense-mediated mRNA decay. Sci Signal 2010, 3. ra27.
25. Si J., Yu X., Zhang Y., DeWille J.W. Myc interacts with Max and Miz1 to repress C/EBPdelta promoter activity and gene expression. Mol Cancer 2010, 9:92.
26. Zhao R., Davey M., Hsu Y.C., Kaplanek P., Tong A., Parsons A.B., Krogan N., Cagney G., Mai D., Greenblatt J., Boone C., Emili A., Houry W.A. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 2005, 120:715-727.
27. Te J., Jia L., Rogers J., Miller A., Hartson S.D. Novel subunits of the mammalian Hsp90 signal transduction chaperone. J Proteome Res 2007, 6:1963-1973.
28. Boulon S., Pradet-Balade B., Verheggen C., Molle D., Boireau S., Georgieva M., Azzag K., Robert M.C., Ahmad Y., Neel H., Lamond A.I., Bertrand E. HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II. Mol Cell 2010, 39:912-924.
29. Cloutier P., Coulombe B. New insights into the biogenesis of nuclear RNA polymerases?. Biochem Cell Biol 2010, 88:211-221.
30. Forget D., Lacombe A.A., Cloutier P., Al-Khoury R., Bouchard A., Lavallee-Adam M., Faubert D., Jeronimo C., Blanchette M., Coulombe B. The protein interaction network of the human transcription machinery reveals a role for the conserved GTPase RPAP4/GPN1 and microtubule assembly in nuclear import and biogenesis of RNA polymerase II. Mol Cell Proteomics 2010, 9:2827-2839.
31. Gonzales F.A., Zanchin N.I., Luz J.S., Oliveira C.C. Characterization of Saccharomyces cerevisiae Nop17p, a novel Nop58p-interacting protein that is involved in Pre-rRNA processing. J Mol Biol 2005, 346:437-455.
32. Granato D.C., Gonzales F.A., Luz J.S., Cassiola F., Machado-Santelli G.M., Oliveira C.C. Nop53p, an essential nucleolar protein that interacts with Nop17p and Nip7p, is required for pre-rRNA processing in Saccharomyces cerevisiae. FEBS J 2005, 272:4450-4463.
33. Goldfeder M.B., Oliveira C.C. Cwc24p, a novel Saccharomyces cerevisiae nuclear ring finger protein, affects pre-snoRNA U3 splicing. J Biol Chem 2008, 283:2644-2653.
34. Takai H., Wang R.C., Takai K.K., Yang H., de Lange T. Tel2 regulates the stability of PI3K-related protein kinases. Cell 2007, 131:1248-1259.
35. Itsuki Y., Saeki M., Nakahara H., Egusa H., Irie Y., Terao Y., Kawabata S., Yatani H., Kamisaki Y. Molecular cloning of novel Monad binding protein containing tetratricopeptide repeat domains. FEBS Lett 2008, 582:2365-2370.
36. Inoue M., Saeki M., Egusa H., Niwa H., Kamisaki Y. PIH1D1, a subunit of R2TP complex, inhibits doxorubicin-induced apoptosis. Biochem Biophys Res Commun 2010, 403:340-344.
37. Smith D.F. Tetratricopeptide repeat cochaperones in steroid receptor complexes. Cell Stress Chaperones 2004, 9:109-121.
38. Matias P.M., Gorynia S., Donner P., Carrondo M.A. Crystal structure of the human AAA+protein RuvBL1. J Biol Chem 2006, 281:38918-38929.
39. Bochtler M., Hartmann C., Song H.K., Bourenkov G.P., Bartunik H.D., Huber R. The structures of HsIU and the ATP-dependent protease HsIU-HsIV. Nature 2000, 403:800-805.
40. Wang J., Song J.J., Seong I.S., Franklin M.C., Kamtekar S., Eom S.H., Chung C.H. Nucleotide-dependent conformational changes in a protease-associated ATPase HsIU. Structure 2001, 9:1107-1116.
41. Gribun A., Cheung K.L., Huen J., Ortega J., Houry W.A. Yeast Rvb1 and Rvb2 are ATP-dependent DNA helicases that form a heterohexameric complex. J Mol Biol 2008, 376:1320-1333.
42. Cheung K.L., Huen J., Houry W.A., Ortega J. Comparison of the multiple oligomeric structures observed for the Rvb1 and Rvb2 proteins. Biochem Cell Biol 2010, 88:77-88.
43. Cheung K.L., Huen J., Kakihara Y., Houry W.A., Ortega J. Alternative oligomeric states of the yeast Rvb1/Rvb2 complex induced by histidine tags. J Mol Biol 2010, 404:478-492.
44. Puri T., Wendler P., Sigala B., Saibil H., Tsaneva I.R. Dodecameric structure and ATPase activity of the human TIP48/TIP49 complex. J Mol Biol 2007, 366:179-192.
45. Torreira E., Jha S., Lopez-Blanco J.R., Arias-Palomo E., Chacon P., Canas C., Ayora S., Dutta A., Llorca O. Architecture of the pontin/reptin complex, essential in the assembly of several macromolecular complexes. Structure 2008, 16:1511-1520.
46. Morrison A.J., Shen X. Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes. Nat Rev Mol Cell Biol 2009, 10:373-384.
47. King T.H., Decatur W.A., Bertrand E., Maxwell E.S., Fournier M.J. A well-connected and conserved nucleoplasmic helicase is required for production of box C/D and H/ACA snoRNAs and localization of snoRNP proteins. Mol Cell Biol 2001, 21:7731-7746.
48. Kressler D., Doere M., Rojo M., Linder P. Synthetic lethality with conditional dbp6 alleles identifies rsa1p, a nucleoplasmic protein involved in the assembly of 60S ribosomal subunits. Mol Cell Biol 1999, 19:8633-8645.
49. Watkins N.J., Newman D.R., Kuhn J.F., Maxwell E.S. In vitro assembly of the mouse U14 snoRNP core complex and identification of a 65-kDa box C/D-binding protein. RNA 1998, 4:582-593.
50. Newman D.R., Kuhn J.F., Shanab G.M., Maxwell E.S. Box C/D snoRNA-associated proteins: two pairs of evolutionarily ancient proteins and possible links to replication and transcription. RNA 2000, 6:861-879.
51. Watkins N.J., Lemm I., Luhrmann R. Involvement of nuclear import and export factors in U8 box C/D snoRNP biogenesis. Mol Cell Biol 2007, 27:7018-7027.
52. Huber J., Cronshagen U., Kadokura M., Marshallsay C., Wada T., Sekine M., Luhrmann R. Snurportin1, an m3G-cap-specific nuclear import receptor with a novel domain structure. EMBO J 1998, 17:4114-4126.
53. Ito T., Chiba T., Ozawa R., Yoshida M., Hattori M., Sakaki Y. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci USA 2001, 98:4569-4574.
54. Bardoni B., Schenck A., Mandel J.L. A novel RNA-binding nuclear protein that interacts with the fragile X mental retardation (FMR1) protein. Hum Mol Genet 1999, 8:2557-2566.
55. Peng W.T., Robinson M.D., Mnaimneh S., Krogan N.J., Cagney G., Morris Q., Davierwala A.P., Grigull J., Yang X., Zhang W., Mitsakakis N., Ryan O.W., Datta N., Jojic V., Pal C., Canadien V., Richards D., Beattie B., Wu L.F., Altschuler S.J., Roweis S., Frey B.J., Emili A., Greenblatt J.F., Hughes T.R. A panoramic view of yeast noncoding RNA processing. Cell 2003, 113:919-933.
56. Watkins N.J., Dickmanns A., Luhrmann R. Conserved stem II of the box C/D motif is essential for nucleolar localization and is required, along with the 15.5K protein, for the hierarchical assembly of the box C/D snoRNP. Mol Cell Biol 2002, 22:8342-8352.
57. Samarsky D.A., Fournier M.J., Singer R.H., Bertrand E. The snoRNA box C/D motif directs nucleolar targeting and also couples snoRNA synthesis and localization. EMBO J 1998, 17:3747-3757.
58. Horejsi Z., Takai H., Adelman C.A., Collis S.J., Flynn H., Maslen S., Skehel J.M., de Lange T., Boulton S.J. CK2 phospho-dependent binding of R2TP complex to TEL2 is essential for mTOR and SMG1 stability. Mol Cell 2010, 39:839-850.
59. Takai H., Xie Y., de Lange T., Pavletich N.P. Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexes. Genes Dev 2010, 24:2019-2030.
60. Lovejoy C.A., Cortez D. Common mechanisms of PIKK regulation. DNA Repair (Amst) 2009, 8:1004-1008.
61. Murr R., Vaissiere T., Sawan C., Shukla V., Herceg Z. Orchestration of chromatin-based processes: mind the TRRAP. Oncogene 2007, 26:5358-5372.
62. Lustig A.J., Petes T.D. Identification of yeast mutants with altered telomere structure. Proc Natl Acad Sci USA 1986, 83:1398-1402.
63. Ahmed S., Alpi A., Hengartner M.O., Gartner A. C. elegans RAD-5/CLK-2 defines a new DNA damage checkpoint protein. Curr Biol 2001, 11:1934-1944.
64. Collis S.J., Barber L.J., Clark A.J., Martin J.S., Ward J.D., Boulton S.J. HCLK2 is essential for the mammalian S-phase checkpoint and impacts on Chk1 stability. Nat Cell Biol 2007, 9:391-401.
65. Shikata M., Ishikawa F., Kanoh J. Tel2 is required for activation of the Mrc1-mediated replication checkpoint. J Biol Chem 2007, 282:5346-5355.
66. Rendtlew Danielsen J.M., Larsen D.H., Schou K.B., Freire R., Falck J., Bartek J., Lukas J. HCLK2 is required for activity of the DNA damage response kinase ATR. J Biol Chem 2009, 284:4140-4147.
67. Hayashi T., Hatanaka M., Nagao K., Nakaseko Y., Kanoh J., Kokubu A., Ebe M., Yanagida M. Rapamycin sensitivity of the Schizosaccharomyces pombe tor2 mutant and organization of two highly phosphorylated TOR complexes by specific and common subunits. Genes Cells 2007, 12:1357-1370.
68. Nguyen V.T., Giannoni F., Dubois M.F., Seo S.J., Vigneron M., Kedinger C., Bensaude O. In vivo degradation of RNA polymerase II largest subunit triggered by alpha-amanitin. Nucleic Acids Res 1996, 24:2924-2929.
69. Rudd M.D., Luse D.S. Amanitin greatly reduces the rate of transcription by RNA polymerase II ternary complexes but fails to inhibit some transcript cleavage modes. J Biol Chem 1996, 271:21549-21558.
70. Fornerod M., Ohno M., Yoshida M., Mattaj I.W. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 1997, 90:1051-1060.
71. Saeki M., Irie Y., Ni L., Yoshida M., Itsuki Y., Kamisaki Y. Monad, a WD40 repeat protein, promotes apoptosis induced by TNF-alpha. Biochem Biophys Res Commun 2006, 342:568-572.
72. Shimada K., Saeki M., Egusa H., Fukuyasu S., Yura Y., Iwai K., Kamisaki Y. RPAP3 enhances cytotoxicity of doxorubicin by impairing NF-kappa B pathway. Biochem Biophys Res Commun 2010, 404:910-914.
73. Yamaoka S., Courtois G., Bessia C., Whiteside S.T., Weil R., Agou F., Kirk H.E., Kay R.J., Israel A. Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation. Cell 1998, 93:1231-1240.
74. Sebban H., Yamaoka S., Courtois G. Posttranslational modifications of NEMO and its partners in NF-kappaB signaling. Trends Cell Biol 2006, 16:569-577.
75. Omran H., Kobayashi D., Olbrich H., Tsukahara T., Loges N.T., Hagiwara H., Zhang Q., Leblond G., O'Toole E., Hara C., Mizuno H., Kawano H., Fliegauf M., Yagi T., Koshida S., Miyawaki A., Zentgraf H., Seithe H., Reinhardt R., Watanabe Y., Kamiya R., Mitchell D.R., Takeda H. Ktu/PF13 is required for cytoplasmic pre-assembly of axonemal dyneins. Nature 2008, 456:611-616.
76. Yamamoto R., Hirono M., Kamiya R. Discrete PIH proteins function in the cytoplasmic preassembly of different subsets of axonemal dyneins. J Cell Biol 2010, 190:65-71.
77. Lindemann C.B., Lesich K.A. Flagellar and ciliary beating: the proven and the possible. J Cell Sci 2010, 123:519-528.
78. Brokaw C.J., Kamiya R. Bending patterns of Chlamydomonas flagella: IV. Mutants with defects in inner and outer dynein arms indicate differences in dynein arm function. Cell Motil Cytoskeleton 1987, 8:68-75.
79. Piperno G., Mead K. Transport of a novel complex in the cytoplasmic matrix of Chlamydomonas flagella. Proc Natl Acad Sci USA 1997, 94:4457-4462.
80. Fowkes M.E., Mitchell D.R. The role of preassembled cytoplasmic complexes in assembly of flagellar dynein subunits. Mol Biol Cell 1998, 9:2337-2347.
81. Rosenbaum J.L., Witman G.B. Intraflagellar transport. Nat Rev Mol Cell Biol 2002, 3:813-825.
82. Scholey J.M. Intraflagellar transport. Annu Rev Cell Dev Biol 2003, 19:423-443.
83. Letunic I., Doerks T., Bork P. SMART 6: recent updates and new developments. Nucleic Acids Res 2009, 37:D229-D232.
84. Marchler-Bauer A., Lu S., Anderson J.B., Chitsaz F., Derbyshire M.K., DeWeese-Scott C., Fong J.H., Geer L.Y., Geer R.C., Gonzales N.R., Gwadz M., Hurwitz D.I., Jackson J.D., Ke Z., Lanczycki C.J., Lu F., Marchler G.H., Mullokandov M., Omelchenko M.V., Robertson C.L., Song J.S., Thanki N., Yamashita R.A., Zhang D., Zhang N., Zheng C., Bryant S.H. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 2011, 39:D225-D229.