HSP90 and the R2TP co-chaperone complex: Building multi-protein machineries essential for cell growth and gene expression

RNA Biology

Volumn 9, Issue 2, 2012, Pages 148-154

  Boulon, Séverine ^a   Bertrand, Edouard ^b   Pradet Balade, Bérengère ^b  

^a Centre National de la Recherche Scientifique   (France)

^b INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

Author keywords

Complex assembly; HSP90; NMD; PIKK; Protein synthesis; R2TP; RNA polymerase; snoRNP

Indexed keywords

ADAPTOR PROTEIN; CHAPERONE; HEAT SHOCK PROTEIN 90; MAMMALIAN TARGET OF RAPAMYCIN; R2TP PROTEIN; RIBONUCLEOPROTEIN; RNA POLYMERASE; SMALL NUCLEOLAR RIBONUCLEOPROTEIN; TELOMERASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BACTERIUM; CELL GROWTH; CELL PROLIFERATION; COMPLEX FORMATION; EUKARYOTE; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; HUMAN; MOLECULAR RECOGNITION; MOLECULAR STABILITY; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; REVIEW; TRANSLATION REGULATION; TUMOR GROWTH;

EUKARYOTA;

EID: 84858210854     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.9.2.18494     Document Type: Review

References (66)

1. Taipale M, Jarosz DF, Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 2010; 11:515-28; PMID: 20531426; http://dx.doi.org/10.1038/nrm2918
2. Trepel J, Mollapour M, Giaccone G, Neckers L. Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 2010; 10:537-49; PMID:20651736; http://dx.doi.org/10.1038/nrc2887
3. Pratt WB, Morishima Y, Peng HM, Osawa Y. Proposal for a role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergo oxidative and toxic damage. Exp Biol Med (Maywood) 2010; 235:278-89; PMID:20404045; http://dx.doi.org/10.1258/ebm.2009.009250
4. Zhao R, Houry WA. Hsp90: a chaperone for protein folding and gene regulation. Biochem Cell Biol 2005; 83:703-10; PMID:16333321; http://dx.doi.org/10.1139/o05-158
5. Zhao R, Davey M, Hsu YC, Kaplanek P, Tong A, Parsons AB, et al. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 2005; 120:715-27; PMID:15766533; http://dx.doi.org/10.1016/j.cell.2004.12.024
6. Millson SH, Vaughan CK, Zhai C, Ali MM, Panaretou B, Piper PW, et al. Chaperone ligand-discrimination by the TPR-domain protein Tah1. Biochem J 2008; 413: 261-8; PMID:18412542; http://dx.doi.org/10.1042/BJ20080105
7. Eckert K, Saliou JM, Monlezun L, Vigouroux A, Atmane N, Caillat C, et al. The Pih1-Tah1 cochaperone complex inhibits Hsp90 molecular chaperone ATPase activity. J Biol Chem 2010; 285:31304-12; PMID:20663878; http://dx.doi.org/10. 1074/jbc.M110.138263
8. Zhao R, Kakihara Y, Gribun A, Huen J, Yang G, Khanna M, et al. Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. J Cell Biol 2008; 180:563-78; PMID:18268103; http://dx.doi.org/10.1083/jcb.200709061
9. Hanson PI, Whiteheart SW. AAA+ proteins: have engine, will work. Nat Rev Mol Cell Biol 2005; 6:519-29; PMID:16072036; http://dx.doi.org/10.1038/nrm1684
10. Jha S, Dutta A. RVB1/RVB2: running rings around molecular biology. Mol Cell 2009; 34:521-33; PMID: 19524533; http://dx.doi.org/10.1016/j.molcel.2009. 05.016
11. Jónsson ZO, Dhar SK, Narlikar GJ, Auty R, Wagle N, Pellman D, et al. Rvb1p and Rvb2p are essential components of a chromatin remodeling complex that regulates transcription of over 5% of yeast genes. J Biol Chem 2001; 276:16279-88; PMID:11278922; http:// dx.doi.org/10.1074/jbc.M011523200
12. Mizuguchi G, Shen X, Landry J, Wu WH, Sen S, Wu C. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 2004; 303:343-8; PMID:14645854; http://dx.doi.org/10.1126/science.1090701
13. Jha S, Shibata E, Dutta A. Human Rvb1/Tip49 is required for the histone acetyltransferase activity of Tip60/NuA4 and for the downregulation of phosphorylation on H2AX after DNA damage. Mol Cell Biol 2008; 28:2690-700; PMID:18285460; http://dx.doi.org/10.1128/MCB.01983-07
14. Izumi N, Yamashita A, Iwamatsu A, Kurata R, Nakamura H, Saari B, et al. AAA+ proteins RUVBL1 and RUVBL2 coordinate PIKK activity and function in nonsense-mediated mRNA decay. Sci Signal 2010; 3:ra27; PMID:20371770; http://dx.doi.org/10.1126/scisignal.2000468
15. Venteicher AS, Meng Z, Mason PJ, Veenstra TD, Artandi SE. Identification of ATPases pontin and reptin as telomerase components essential for holoenzyme assembly. Cell 2008; 132:945-57; PMID:18358808; http://dx.doi.org/10.1016/j. cell.2008.01.019
16. Te J, Jia L, Rogers J, Miller A, Hartson SD. Novel subunits of the mammalian Hsp90 signal transduction chaperone. J Proteome Res 2007; 6:1963-73; PMID: 17348703; http://dx.doi.org/10.1021/pr060595i
17. Boulon S, Marmier-Gourrier N, Pradet-Balade B, Wurth L, Verheggen C, Jady BE, et al. The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J Cell Biol 2008; 180: 579-95; PMID:18268104; http://dx.doi.org/10.1083/jcb.200708110
18. Boulon S, Pradet-Balade B, Verheggen C, Molle D, Boireau S, Georgieva M, et al. HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II. Mol Cell 2010; 39:912-24; PMID:20864038; http://dx.doi.org/10.1016/j.molcel.2010.08.023
19. Cloutier P, Coulombe B. New insights into the biogenesis of nuclear RNA polymerases?Biochem Cell Biol 2010; 88:211-21; PMID:20453924; http://dx.doi.org/10.1139/O09-173
20. Sardiu ME, Cai Y, Jin J, Swanson SK, Conaway RC, Conaway JW, et al. Probabilistic assembly of human protein interaction networks from label-free quantitative proteomics. Proc Natl Acad Sci USA 2008; 105: 1454-9; PMID:18218781; http://dx.doi.org/10.1073/pnas.0706983105
21. Kiss T, Fayet E, Jady BE, Richard P, Weber M. Biogenesis and intranuclear trafficking of human box C/D and H/ACA RNPs. Cold Spring Harb Symp Quant Biol 2006; 71:407-17; PMID:17381323; http://dx.doi.org/10.1101/sqb.2006.71.025
22. Boulon S, Verheggen C, Jady BE, Girard C, Pescia C, Paul C, et al. PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell 2004; 16:777-87; PMID:15574332; http://dx.doi.org/10.1016/j.molcel.2004.11.013
23. Watkins NJ, Lemm I, Ingelfinger D, Schneider C, Hossbach M, Urlaub H, et al. Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol Cell 2004; 16:789-98; PMID:15574333; http://dx.doi.org/10.1016/j.molcel.2004.11.012
24. Pradet-Balade B, Girard C, Boulon S, Paul C, Azzag K, Bordonne R, et al. CRM1 controls the composition of nucleoplasmic pre-snoRNA complexes to licence them for nucleolar transport. EMBO J 2011; 30:2205-18; PMID:21522132; http://dx.doi.org/10.1038/emboj.2011.128
25. King TH, Decatur WA, Bertrand E, Maxwell ES, Fournier MJ. 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; 21:7731-46; PMID: 11604509; http://dx.doi.org/10.1128/MCB.21.22.7731-7746. 2001
26. Gonzales FA, Zanchin NI, Luz JS, Oliveira CC. Characterization of Saccharomyces cerevisiae Nop17p, a novel Nop58p-interacting protein that is involved in Pre-rRNA processing. J Mol Biol 2005; 346:437-55; PMID:15670595; http://dx.doi.org/10.1016/j.jmb.2004.11.071
27. Rodor J, Jobet E, Bizarro J, Vignols F, Carles C, Suzuki T, et al. AtNUFIP, an essential protein for plant development, reveals the impact of snoRNA gene organisation on the assembly of snoRNPs and rRNA methylation in Arabidopsis thaliana. Plant J 2011; 65:807-19; PMID:21261762; http://dx.doi.org/10.1111/j.1365-313X.2010.04468.x
28. Klein DJ, Schmeing TM, Moore PB, Steitz TA. The kink-turn: a new RNA secondary structure motif. EMBO J 2001; 20:4214-21; PMID:11483524; http://dx.doi.org/10.1093/emboj/20.15.4214
29. Watkins NJ, Segault V, Charpentier B, Nottrott S, Fabrizio P, Bachi A, et al. A common core RNP structure shared between the small nucleoar box C/D RNPs and the spliceosomal U4 snRNP. Cell 2000; 103:457-66; PMID:11081632; http://dx.doi.org/10.1016/S0092-8674(00)00137-9
30. Rozhdestvensky TS, Tang TH, Tchirkova IV, Brosius J, Bachellerie JP, Huttenhofer A. Binding of L7Ae protein to the K-turn of archaeal snoRNAs: a shared RNA binding motif for C/D and H/ACA box snoRNAs in Archaea. Nucleic Acids Res 2003; 31: 869-77; PMID:12560482; http://dx.doi.org/10.1093/nar/gkg175
31. Allmang C, Carbon P, Krol A. The SBP2 and 15.5 kD/Snu13p proteins share the same RNA binding domain: identification of SBP2 amino acids important to SECIS RNA binding. RNA 2002; 8: 1308-18; PMID:12403468; http://dx.doi.org/10. 1017/S1355838202020034
32. Jeronimo C, Forget D, Bouchard A, Li Q, Chua G, Poitras C, et al. Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme. Mol Cell 2007; 27:262-74; PMID:17643375; http://dx.doi.org/10.1016/j.molcel.2007.06.027
33. Kolodziej PA, Young RA. Mutations in the three largest subunits of yeast RNA polymerase II that affect enzyme assembly. Mol Cell Biol 1991; 11:4669-78; PMID: 1715023
34. Ishihama A. Subunit of assembly of Escherichia coli RNA polymerase. Adv Biophys 1981; 14:1-35; PMID: 7015808
35. Kimura M, Ishihama A. Subunit assembly in vivo of Escherichia coli RNA polymerase: role of the aminoterminal assembly domain of alpha subunit. Genes Cells 1996; 1:517-28; PMID:9078382; http://dx.doi.org/10.1046/j.1365-2443.1996. d01-258.x
36. Ziemienowicz A, Skowyra D, Zeilstra-Ryalls J, Fayet O, Georgopoulos C, Zylicz M. Both the Escherichia coli chaperone systems, GroEL/GroES and DnaK/DnaJ/GrpE, can reactivate heat-treated RNA polymerase. Different mechanisms for the same activity. J Biol Chem 1993; 268:25425-31; PMID:7902351
37. Forget D, Lacombe AA, Cloutier P, Al-Khoury R, Bouchard A, Lavallee-Adam M, et al. 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; 9:2827-39; PMID:20855544; http://dx.doi.org/10.1074/mcp.M110.003616
38. Kimura M, Ishiguro A, Ishihama A. RNA polymerase II subunits 2, 3, and 11 form a core subassembly with DNA binding activity. J Biol Chem 1997; 272:25851-5; PMID:9325316; http://dx.doi.org/10.1074/jbc.272.41.25851
39. Minakhin L, Bhagat S, Brunning A, Campbell EA, Darst SA, Ebright RH, et al. Bacterial RNA polymerase subunit omega and eukaryotic RNA polymerase subunit RPB6 are sequence, structural, and functional homologs and promote RNA polymerase assembly. Proc Natl Acad Sci USA 2001; 98:892-7; PMID: 11158566; http://dx.doi.org/10.1073/pnas.98.3.892
40. Gandhi SJ, Zenklusen D, Lionnet T, Singer RH. Transcription of functionally related constitutive genes is not coordinated. Nat Struct Mol Biol 2011; 18:27-34; PMID:21131977; http://dx.doi.org/10.1038/nsmb.1934
41. Czeko E, Seizl M, Augsberger C, Mielke T, Cramer P. Iwr1 directs RNA polymerase II nuclear import. Mol Cell 2011; 42:261-6; PMID:21504834; http://dx.doi.org/10.1016/j.molcel.2011.02.033
42. Bertrand E, Bordonne R. Assembly and traffic of small nuclear RNPs. Prog Mol Subcell Biol 2004; 35:79-97; PMID:15113080; http://dx.doi.org/10.1007/978-3- 540-74266-1-4
43. Fischer U, Englbrecht C, Chari A. Biogenesis of spliceosomal small nuclear ribonucleoproteins. Wiley Interdiscip Rev RNA 2011; 2:718-31; PMID: 21823231; http://dx.doi.org/10.1002/wrna.87
44. Henras AK, Soudet J, Gerus M, Lebaron S, Caizergues-Ferrer M, Mougin A, et al. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci 2008; 65:2334-59; PMID:18408888; http://dx.doi.org/10.1007/s00018- 008-8027-0
45. Kressler D, Hurt E, Bassler J. Driving ribosome assembly. Biochim Biophys Acta 2010; 1803:673-83; PMID:19879902; http://dx.doi.org/10.1016/j.bbamcr.2009. 10.009
46. Gorski SA, Snyder SK, John S, Grummt I, Misteli T. Modulation of RNA polymerase assembly dynamics in transcriptional regulation. Mol Cell 2008; 30:486-97; PMID:18498750; http://dx.doi.org/10.1016/j.molcel.2008.04.021
47. Dundr M, Hoffmann-Rohrer U, Hu Q, Grummt I, Rothblum LI, Phair RD, et al. A kinetic framework for a mammalian RNA polymerase in vivo. Science 2002; 298:1623-6; PMID:12446911; http://dx.doi.org/10.1126/science.1076164
48. Schneider DA, Nomura M. RNA polymerase I remains intact without subunit exchange through multiple rounds of transcription in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2004; 101:15112-7; PMID: 15477604; http://dx.doi.org/10. 1073/pnas.0406746101
49. Hardeland U, Hurt E. Coordinated nuclear import of RNA polymerase III subunits. Traffic 2006; 7:465-73; PMID:16536744; http://dx.doi.org/10.1111/j. 1600-0854.2006.00399.x
50. Takai H, Wang RC, Takai KK, Yang H, de Lange T. Tel2 regulates the stability of PI3K-related protein kinases. Cell 2007; 131:1248-59; PMID:18160036; http://dx.doi.org/10.1016/j.cell.2007.10.052
51. Takai H, Xie Y, de Lange T, Pavletich NP. Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexes. Genes Dev 2010; 24:2019-30; PMID:20801936; http://dx.doi.org/10.1101/gad.1956410
52. Kaizuka T, Hara T, Oshiro N, Kikkawa U, Yonezawa K, Takehana K, et al. Tti1 and Tel2 are critical factors in mammalian target of rapamycin complex assembly. J Biol Chem 2010; 285:20109-16; PMID:20427287; http://dx.doi.org/10. 1074/jbc.M110.121699
53. Horejsí Z, Takai H, Adelman CA, Collis SJ, Flynn H, Maslen S, et al. CK2 phospho-dependent binding of R2TP complex to TEL2 is essential for mTOR and SMG1 stability. Mol Cell 2010; 39:839-50; PMID: 20864032; http://dx.doi.org/10.1016/j.molcel.2010.08.037
54. Mahalingam D, Swords R, Carew JS, Nawrocki ST, Bhalla K, Giles FJ. Targeting HSP90 for cancer therapy. Br J Cancer 2009; 100:1523-9; PMID: 19401686; http://dx.doi.org/10.1038/sj.bjc.6605066
55. Lauscher JC, Loddenkemper C, Kosel L, Grone J, Buhr HJ, Huber O. Increased pontin expression in human colorectal cancer tissue. Hum Pathol 2007; 38:978-85; PMID:17442372; http://dx.doi.org/10.1016/j.humpath.2007.01.005
56. Haurie V, Menard L, Nicou A, Touriol C, Metzler P, Fernandez J, et al. Adenosine triphosphatase pontin is overexpressed in hepatocellular carcinoma and coregulated with reptin through a new posttranslational mechanism. Hepatology 2009; 50:1871-83; PMID: 19877184; http://dx.doi.org/10.1002/hep.23215
57. Huber O, Menard L, Haurie V, Nicou A, Taras D, Rosenbaum J. Pontin and reptin, two related ATPases with multiple roles in cancer. Cancer Res 2008; 68: 6873-6; PMID:18757398; http://dx.doi.org/10.1158/0008-5472.CAN-08-0547
58. Rousseau B, Menard L, Haurie V, Taras D, Blanc JF, Moreau-Gaudry F, et al. Overexpression and role of the ATPase and putative DNA helicase RuvB-like 2 in human hepatocellular carcinoma. Hepatology 2007; 46:1108-18; PMID:17657734; http://dx.doi.org/10.1002/hep.21770
59. Ménard L, Taras D, Grigoletto A, Haurie V, Nicou A, Dugot-Senant N, et al. In vivo silencing of Reptin blocks the progression of human hepatocellular carcinoma in xenografts and is associated with replicative senescence. J Hepatol 2010; 52:681-9; PMID: 20346530; http://dx.doi.org/10.1016/ j.jhep.2009.12.029
60. Grigoletto A, Lestienne P, Rosenbaum J. The multifaceted proteins Reptin and Pontin as major players in cancer. Biochim Biophys Acta 2011. In Press. PMID:21111787
61. Zoncu R, Efeyan A, Sabatini DM. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 2011; 12:21-35; PMID:21157483; http://dx.doi.org/10.1038/nrm3025
62. Johnson SM, Gulhati P, Rampy BA, Han Y, Rychahou PG, Doan HQ, Weiss HL, Evers BM. Novel expression patterns of PI3K/Akt/mTOR signaling pathway components in colorectal cancer. J Am Coll Surg 2010; 210:767-776; PMID:20421047; http://dx.doi.org/10.1016/j.jamcollsurg.2009.12.008
63. Whittaker S, Marais R, Zhu AX. The role of signaling pathways in the development and treatment of hepatocellular carcinoma. Oncogene 2010; 29:4989-5005; PMID:20639898; http://dx.doi.org/10.1038/onc.2010.236
64. Zhou L, Huang Y, Li J, Wang Z. The mTOR pathway is associated with the poor prognosis of human hepatocellular carcinoma. Med Oncol 2010; 27:255-61; PMID:19301157; http://dx.doi.org/10.1007/s12032-009-9201-4
65. Toshikuni N, Nouso K, Higashi T, Nakatsukasa H, Onishi T, Kaneyoshi T, et al. Expression of telomerase-associated protein 1 and telomerase reverse transcriptase in hepatocellular carcinoma. Br J Cancer 2000; 82: 833-7; PMID:10732755; http://dx.doi.org/10.1054/bjoc.1999.1008
66. Wei R, Younes M. Immunohistochemical detection of telomerase reverse transcriptase in colorectal adenocarcinoma and benign colonic mucosa. Hum Pathol 2002; 33:693-6; PMID:12196919; http://dx.doi.org/10.1053/hupa.2002.124719