Proteomic and Genomic Analyses of the Rvb1 and Rvb2 Interaction Network upon Deletion of R2TP Complex Components

The highly conserved yeast R2TP complex, consisting of Rvb1, Rvb2, Pih1, and Tah1, participates in diverse cellular processes ranging from assembly of protein complexes to apoptosis. Rvb1 and Rvb2 are closely related proteins belonging to the AAA+ superfamily and are essential for cell survival. Although Rvbs have been shown to be associated with various protein complexes including the Ino80 and Swr1chromatin remodeling complexes, we performed a systematic quantitative proteomic analysis of their associated proteins and identified two additional complexes that associate with Rvb1 and Rvb2: the chaperonin-containing T-complex and the 19S regulatory particle of the proteasome complex. We also analyzed Rvb1 and Rvb2 purified from yeast strains devoid of PIH1 and TAH1. These analyses revealed that both Rvb1 and Rvb2 still associated with Hsp90 and were highly enriched with RNA polymerase II complex components. Our analyses also revealed that both Rvb1 and Rvb2 were recruited to the Ino80 and Swr1 chromatin remodeling complexes even in the absence of Pih1 and Tah1 proteins. Using further biochemical analysis, we showed that Rvb1 and Rvb2 directly interacted with Hsp90 as well as with the RNA polymerase II complex. RNA-Seq analysis of the deletion strains compared with the wild-type strains revealed an up-regulation of ribosome biogenesis and ribonucleoprotein complex biogenesis genes, down-regulation of response to abiotic stimulus genes, and down-regulation of response to temperature stimulus genes. A Gene Ontology analysis of the 80 proteins whose protein associations were altered in the PIH1 or TAH1 deletion strains found ribonucleoprotein complex proteins to be the most enriched category. This suggests an important function of the R2TP complex in ribonucleoprotein complex biogenesis at both the proteomic and genomic levels. Finally, these results demonstrate that deletion network analyses can provide novel insights into cellular systems. The highly conserved yeast R2TP complex, consisting of Rvb1, Rvb2, Pih1, and Tah1, participates in diverse cellular processes ranging from assembly of protein complexes to apoptosis. Rvb1 and Rvb2 are closely related proteins belonging to the AAA+ superfamily and are essential for cell survival. Although Rvbs have been shown to be associated with various protein complexes including the Ino80 and Swr1chromatin remodeling complexes, we performed a systematic quantitative proteomic analysis of their associated proteins and identified two additional complexes that associate with Rvb1 and Rvb2: the chaperonin-containing T-complex and the 19S regulatory particle of the proteasome complex. We also analyzed Rvb1 and Rvb2 purified from yeast strains devoid of PIH1 and TAH1. These analyses revealed that both Rvb1 and Rvb2 still associated with Hsp90 and were highly enriched with RNA polymerase II complex components. Our analyses also revealed that both Rvb1 and Rvb2 were recruited to the Ino80 and Swr1 chromatin remodeling complexes even in the absence of Pih1 and Tah1 proteins. Using further biochemical analysis, we showed that Rvb1 and Rvb2 directly interacted with Hsp90 as well as with the RNA polymerase II complex. RNA-Seq analysis of the deletion strains compared with the wild-type strains revealed an up-regulation of ribosome biogenesis and ribonucleoprotein complex biogenesis genes, down-regulation of response to abiotic stimulus genes, and down-regulation of response to temperature stimulus genes. A Gene Ontology analysis of the 80 proteins whose protein associations were altered in the PIH1 or TAH1 deletion strains found ribonucleoprotein complex proteins to be the most enriched category. This suggests an important function of the R2TP complex in ribonucleoprotein complex biogenesis at both the proteomic and genomic levels. Finally, these results demonstrate that deletion network analyses can provide novel insights into cellular systems. The Saccharomyces cerevisiae R2TP complex consists of Rvb1, Rvb2, Pih1 (protein interacting with Hsp90) and Tah1 (TPR (tetratricopeptide repeat)-containing protein associated with Hsp90) proteins. Although, the R2TP complex was initially discovered in yeast as an Hsp90-associated complex (1.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: 715-727Abstract Full Text Full Text PDF PubMed Scopus (647) Google Scholar), R2TP subunits are conserved in higher eukaryotes and the R2TP complex was recently identified and purified from human cells (2.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: 1963-1973Crossref PubMed Scopus (50) Google Scholar). The R2TP complex has been implicated in various cellular processes such as assembly of small nucleolar ribonuclearprotein (snoRNP) 1The abbreviations used are:snoRNPsmall nucleolar ribonucleoproteinAAA+adenosine triphosphatase associated with diverse cellular activitiesAP-MSaffinity purification-mass spectrometryCAMchloroacetamideCCTCchaperonin-containing T-complexdBNSAFdistributed bait normalized spectral abundance factordNSAFdistributed normalized spectral abundance factordSdistributed spectral countsDTTdithiothreitolGEOgene expression omnibusFDRfalse discovery rateFPKMfragments per kilobase of exon per protein for interacting with protein polymerase per protein associated with nucleolar complex N. L. C. C. A. C. C. The Hsp90 chaperone the biogenesis of conserved PubMed Scopus Google R. A. J. G. M. M. Boone C. Houry W.A. chaperone Hsp90 to R2TP complex that PubMed Scopus Google Scholar), polymerase complex C. D. M. and are in the assembly of RNA polymerase Full Text Full Text PDF PubMed Scopus Google Scholar), M. M. a of R2TP complex, Res. PubMed Scopus Google Scholar), and protein of R2TP complex to essential for and Full Text Full Text PDF PubMed Scopus Google Scholar). The of R2TP in various complexes to be in of Pih1 and Tah1, as proteins. the assembly of human complex a the complex. the complex and complex are recruited by the R2TP complex P. R. M. D. C. A. D. M. of the protein network for the human and of RNA polymerase PubMed Scopus Google Scholar). Tah1 has been shown to directly with of and the R2TP and complexes to complex assembly C. D. M. and are in the assembly of RNA polymerase Full Text Full Text PDF PubMed Scopus Google Scholar). an function for Pih1 in the Hsp90 chaperone to These the of Hsp90 to the yeast assembly an Pih1 and R. A. J. G. M. M. Boone C. Houry W.A. chaperone Hsp90 to R2TP complex that PubMed Scopus Google and the of by of Hsp90 to an Pih1 and the M. M. C. for of to Hsp90 by Full Text Full Text PDF PubMed Scopus Google Scholar). small nucleolar ribonucleoprotein triphosphatase associated with diverse cellular purification-mass chaperonin-containing T-complex bait normalized spectral abundance normalized spectral abundance spectral expression discovery per kilobase of exon per protein for protein interacting with Hsp90 protein RNA polymerase II per protein associated with Hsp90 yeast Rvb1 and Rvb2 and in are of the AAA+ triphosphatase associated with diverse cellular superfamily both as well as A. J. J. Houry W.A. Rvb1 and Rvb2 are that a PubMed Scopus Google Scholar). Rvb1 and Rvb2 are in both and various and are essential for cell P. A. protein essential for Full Text Full Text PDF PubMed Scopus Google Scholar). This as are in processes ranging from assembly of complexes or the of Pih1 and chromatin remodeling and the of N. Houry W.A. of the AAA+ proteins Rvb1 and Rvb2 in the assembly of various R. PubMed Scopus Google R. N. D. R. 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Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone.Cell. 2005; 120: 715-727Abstract Full Text Full Text PDF PubMed Scopus (647) Google Scholar), that in the absence of Pih1 and Tah1, Rvb1 and Rvb2 are enriched in a of the Ino80 complex. analysis of that the was the up-regulation of from the of Ino80 as well as protein complexes J. C. of the and in cell of Saccharomyces J. PubMed Scopus Google Scholar). Finally, we analyzed the RNA-Seq to the of PIH1 or TAH1 from the or were or These of expression for the of in strains the we compared deletion strains with wild-type strains also with a of expression we performed a analysis of the the the deletion of PIH1 or TAH1 were in the or these were with we compared for of the of in the Saccharomyces C. R. G. J. M. Saccharomyces the of Res. PubMed Scopus Google Scholar). has has TAH1 has and PIH1 has The function in of these are of the and TAH1. 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