The Box H/ACA snoRNP Assembly Factor Shq1p is a Chaperone Protein Homologous to Hsp90 Cochaperones that Binds to the Cbf5p Enzyme
Box H/ACA small nucleolar (sno) ribonucleoproteins (RNPs) are responsible for the formation of pseudouridine in a variety of RNAs and are essential for ribosome biogenesis, modification of spliceosomal RNAs, and telomerase stability. A mature snoRNP has been reconstituted in vitro and is composed of...
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| Veröffentlicht in: | Journal of molecular biology 2009-07, Vol.390 (2), p.231-244 |
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| creator | Godin, Katherine S. Walbott, Hélène Leulliot, Nicolas van Tilbeurgh, Herman Varani, Gabriele |
| description | Box H/ACA small nucleolar (sno) ribonucleoproteins (RNPs) are responsible for the formation of pseudouridine in a variety of RNAs and are essential for ribosome biogenesis, modification of spliceosomal RNAs, and telomerase stability. A mature snoRNP has been reconstituted in vitro and is composed of a single RNA and four proteins. However, snoRNP biogenesis in vivo requires multiple factors to coordinate a complex and poorly understood assembly and maturation process. Among the factors required for snoRNP biogenesis in yeast is Shq1p, an essential protein necessary for stable expression of box H/ACA snoRNAs. We have found that Shq1p consists of two independent domains that contain casein kinase 1 phosphorylation sites. We also demonstrate that Shq1p binds the pseudourydilating enzyme Cbf5p through the C-terminal domain, in synergy with the N-terminal domain. The NMR solution structure of the N-terminal domain has striking homology to the ‘Chord and Sgt1’ domain of known Hsp90 cochaperones, yet Shq1p does not interact with the yeast Hsp90 homologue in vitro. Surprisingly, Shq1p has stand-alone chaperone activity in vitro. This activity is harbored by the C-terminal domain, but it is increased by the presence of the N-terminal domain. These results provide the first evidence of a specific biochemical activity for Shq1p and a direct link to the H/ACA snoRNP. |
| doi_str_mv | 10.1016/j.jmb.2009.04.076 |
| format | Article |
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A mature snoRNP has been reconstituted in vitro and is composed of a single RNA and four proteins. However, snoRNP biogenesis in vivo requires multiple factors to coordinate a complex and poorly understood assembly and maturation process. Among the factors required for snoRNP biogenesis in yeast is Shq1p, an essential protein necessary for stable expression of box H/ACA snoRNAs. We have found that Shq1p consists of two independent domains that contain casein kinase 1 phosphorylation sites. We also demonstrate that Shq1p binds the pseudourydilating enzyme Cbf5p through the C-terminal domain, in synergy with the N-terminal domain. The NMR solution structure of the N-terminal domain has striking homology to the ‘Chord and Sgt1’ domain of known Hsp90 cochaperones, yet Shq1p does not interact with the yeast Hsp90 homologue in vitro. Surprisingly, Shq1p has stand-alone chaperone activity in vitro. This activity is harbored by the C-terminal domain, but it is increased by the presence of the N-terminal domain. These results provide the first evidence of a specific biochemical activity for Shq1p and a direct link to the H/ACA snoRNP.</description><identifier>ISSN: 0022-2836</identifier><identifier>EISSN: 1089-8638</identifier><identifier>DOI: 10.1016/j.jmb.2009.04.076</identifier><identifier>PMID: 19426738</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Amino Acid Sequence ; BASIC BIOLOGICAL SCIENCES ; BIOCHEMISTRY ; Biochemistry, Molecular Biology ; Biophysics ; CASEIN ; chaperone ; CS domain ; Environmental Molecular Sciences Laboratory ; ENZYMES ; H/ACA snoRNP biogenesis ; Hydro-Lyases - metabolism ; IN VITRO ; IN VIVO ; Life Sciences ; Magnetic Resonance Spectroscopy ; Microtubule-Associated Proteins - metabolism ; Models, Molecular ; MODIFICATIONS ; Molecular biology ; Molecular Chaperones - metabolism ; Molecular Networks ; Molecular Sequence Data ; Nuclear Proteins - chemistry ; Nuclear Proteins - metabolism ; PHOSPHORYLATION ; PHOSPHOTRANSFERASES ; Protein Binding ; Protein Interaction Domains and Motifs ; Protein Interaction Mapping ; Protein Structure, Tertiary ; PROTEINS ; Ribonucleoproteins, Small Nuclear - metabolism ; RIBOSOMES ; RNA ; Saccharomyces cerevisiae - chemistry ; Saccharomyces cerevisiae - enzymology ; Saccharomyces cerevisiae Proteins - chemistry ; Saccharomyces cerevisiae Proteins - metabolism ; Sequence Alignment ; Shq1 ; STABILITY ; Structural Biology ; YEASTS</subject><ispartof>Journal of molecular biology, 2009-07, Vol.390 (2), p.231-244</ispartof><rights>2009 Elsevier Ltd</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c454t-6f2b63e25b4460171be9df99f44c5fde400ea500ed1823f54d4b07f9f079fe13</citedby><cites>FETCH-LOGICAL-c454t-6f2b63e25b4460171be9df99f44c5fde400ea500ed1823f54d4b07f9f079fe13</cites><orcidid>0000-0002-0438-9493</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.jmb.2009.04.076$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19426738$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02287870$$DView record in HAL$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/966641$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Godin, Katherine S.</creatorcontrib><creatorcontrib>Walbott, Hélène</creatorcontrib><creatorcontrib>Leulliot, Nicolas</creatorcontrib><creatorcontrib>van Tilbeurgh, Herman</creatorcontrib><creatorcontrib>Varani, Gabriele</creatorcontrib><creatorcontrib>Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)</creatorcontrib><title>The Box H/ACA snoRNP Assembly Factor Shq1p is a Chaperone Protein Homologous to Hsp90 Cochaperones that Binds to the Cbf5p Enzyme</title><title>Journal of molecular biology</title><addtitle>J Mol Biol</addtitle><description>Box H/ACA small nucleolar (sno) ribonucleoproteins (RNPs) are responsible for the formation of pseudouridine in a variety of RNAs and are essential for ribosome biogenesis, modification of spliceosomal RNAs, and telomerase stability. A mature snoRNP has been reconstituted in vitro and is composed of a single RNA and four proteins. However, snoRNP biogenesis in vivo requires multiple factors to coordinate a complex and poorly understood assembly and maturation process. Among the factors required for snoRNP biogenesis in yeast is Shq1p, an essential protein necessary for stable expression of box H/ACA snoRNAs. We have found that Shq1p consists of two independent domains that contain casein kinase 1 phosphorylation sites. We also demonstrate that Shq1p binds the pseudourydilating enzyme Cbf5p through the C-terminal domain, in synergy with the N-terminal domain. The NMR solution structure of the N-terminal domain has striking homology to the ‘Chord and Sgt1’ domain of known Hsp90 cochaperones, yet Shq1p does not interact with the yeast Hsp90 homologue in vitro. Surprisingly, Shq1p has stand-alone chaperone activity in vitro. This activity is harbored by the C-terminal domain, but it is increased by the presence of the N-terminal domain. These results provide the first evidence of a specific biochemical activity for Shq1p and a direct link to the H/ACA snoRNP.</description><subject>Amino Acid Sequence</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>BIOCHEMISTRY</subject><subject>Biochemistry, Molecular Biology</subject><subject>Biophysics</subject><subject>CASEIN</subject><subject>chaperone</subject><subject>CS domain</subject><subject>Environmental Molecular Sciences Laboratory</subject><subject>ENZYMES</subject><subject>H/ACA snoRNP biogenesis</subject><subject>Hydro-Lyases - metabolism</subject><subject>IN VITRO</subject><subject>IN VIVO</subject><subject>Life Sciences</subject><subject>Magnetic Resonance Spectroscopy</subject><subject>Microtubule-Associated Proteins - metabolism</subject><subject>Models, Molecular</subject><subject>MODIFICATIONS</subject><subject>Molecular biology</subject><subject>Molecular Chaperones - metabolism</subject><subject>Molecular Networks</subject><subject>Molecular Sequence Data</subject><subject>Nuclear Proteins - chemistry</subject><subject>Nuclear Proteins - metabolism</subject><subject>PHOSPHORYLATION</subject><subject>PHOSPHOTRANSFERASES</subject><subject>Protein Binding</subject><subject>Protein Interaction Domains and Motifs</subject><subject>Protein Interaction Mapping</subject><subject>Protein Structure, Tertiary</subject><subject>PROTEINS</subject><subject>Ribonucleoproteins, Small Nuclear - metabolism</subject><subject>RIBOSOMES</subject><subject>RNA</subject><subject>Saccharomyces cerevisiae - chemistry</subject><subject>Saccharomyces cerevisiae - enzymology</subject><subject>Saccharomyces cerevisiae Proteins - chemistry</subject><subject>Saccharomyces cerevisiae Proteins - metabolism</subject><subject>Sequence Alignment</subject><subject>Shq1</subject><subject>STABILITY</subject><subject>Structural Biology</subject><subject>YEASTS</subject><issn>0022-2836</issn><issn>1089-8638</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUFv1DAQhSMEokvhB3BB5lKJQ7bjxHEScUqjliCtoIK9W4kzJl4lcWpnK5Yb_xyHLHDjMiONvnmjeS8IXlPYUqD8-rA9DM02Asi3wLaQ8ifBhkKWhxmPs6fBBiCKwiiL-UXwwrkDACQxy54HFzRnEU_jbBP83HdIbsx3Ul0XZUHcaL58uieFczg0_Ync1XI2lnztHuhEtCM1Kbt6QmtGJPfWzKhHUpnB9OabOToyG1K5KQdSGvmH89OunsmNHtvfwOwPlo1KJnI7_jgN-DJ4pure4atzvwz2d7f7sgp3nz98LItdKFnC5pCrqOExRknDGAea0gbzVuW5YkwmqkUGgHXiS0uzKFYJa1kDqcoVpLlCGl8Gb1dZ42YtnNQzyk6acUQ5i5xzzhbm3cp0dS8mq4fanoSptaiKnVhm3s8szVJ4XNirlZ2seTiim8WgncS-r0f0VghvL8_iNPUgXUFpjXMW1V9lCmKJURyEj1EsMQpgwsfod96cxY_NgO2_jXNuHni_Augde9Rol49wlNhquzzUGv0f-V9jCKsZ</recordid><startdate>20090710</startdate><enddate>20090710</enddate><creator>Godin, Katherine S.</creator><creator>Walbott, Hélène</creator><creator>Leulliot, Nicolas</creator><creator>van Tilbeurgh, Herman</creator><creator>Varani, Gabriele</creator><general>Elsevier Ltd</general><general>Elsevier</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>OTOTI</scope><orcidid>https://orcid.org/0000-0002-0438-9493</orcidid></search><sort><creationdate>20090710</creationdate><title>The Box H/ACA snoRNP Assembly Factor Shq1p is a Chaperone Protein Homologous to Hsp90 Cochaperones that Binds to the Cbf5p Enzyme</title><author>Godin, Katherine S. ; Walbott, Hélène ; Leulliot, Nicolas ; van Tilbeurgh, Herman ; Varani, Gabriele</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c454t-6f2b63e25b4460171be9df99f44c5fde400ea500ed1823f54d4b07f9f079fe13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Amino Acid Sequence</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>BIOCHEMISTRY</topic><topic>Biochemistry, Molecular Biology</topic><topic>Biophysics</topic><topic>CASEIN</topic><topic>chaperone</topic><topic>CS domain</topic><topic>Environmental Molecular Sciences Laboratory</topic><topic>ENZYMES</topic><topic>H/ACA snoRNP biogenesis</topic><topic>Hydro-Lyases - metabolism</topic><topic>IN VITRO</topic><topic>IN VIVO</topic><topic>Life Sciences</topic><topic>Magnetic Resonance Spectroscopy</topic><topic>Microtubule-Associated Proteins - metabolism</topic><topic>Models, Molecular</topic><topic>MODIFICATIONS</topic><topic>Molecular biology</topic><topic>Molecular Chaperones - metabolism</topic><topic>Molecular Networks</topic><topic>Molecular Sequence Data</topic><topic>Nuclear Proteins - chemistry</topic><topic>Nuclear Proteins - metabolism</topic><topic>PHOSPHORYLATION</topic><topic>PHOSPHOTRANSFERASES</topic><topic>Protein Binding</topic><topic>Protein Interaction Domains and Motifs</topic><topic>Protein Interaction Mapping</topic><topic>Protein Structure, Tertiary</topic><topic>PROTEINS</topic><topic>Ribonucleoproteins, Small Nuclear - metabolism</topic><topic>RIBOSOMES</topic><topic>RNA</topic><topic>Saccharomyces cerevisiae - chemistry</topic><topic>Saccharomyces cerevisiae - enzymology</topic><topic>Saccharomyces cerevisiae Proteins - chemistry</topic><topic>Saccharomyces cerevisiae Proteins - metabolism</topic><topic>Sequence Alignment</topic><topic>Shq1</topic><topic>STABILITY</topic><topic>Structural Biology</topic><topic>YEASTS</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Godin, Katherine S.</creatorcontrib><creatorcontrib>Walbott, Hélène</creatorcontrib><creatorcontrib>Leulliot, Nicolas</creatorcontrib><creatorcontrib>van Tilbeurgh, Herman</creatorcontrib><creatorcontrib>Varani, Gabriele</creatorcontrib><creatorcontrib>Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>OSTI.GOV</collection><jtitle>Journal of molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Godin, Katherine S.</au><au>Walbott, Hélène</au><au>Leulliot, Nicolas</au><au>van Tilbeurgh, Herman</au><au>Varani, Gabriele</au><aucorp>Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Box H/ACA snoRNP Assembly Factor Shq1p is a Chaperone Protein Homologous to Hsp90 Cochaperones that Binds to the Cbf5p Enzyme</atitle><jtitle>Journal of molecular biology</jtitle><addtitle>J Mol Biol</addtitle><date>2009-07-10</date><risdate>2009</risdate><volume>390</volume><issue>2</issue><spage>231</spage><epage>244</epage><pages>231-244</pages><issn>0022-2836</issn><eissn>1089-8638</eissn><abstract>Box H/ACA small nucleolar (sno) ribonucleoproteins (RNPs) are responsible for the formation of pseudouridine in a variety of RNAs and are essential for ribosome biogenesis, modification of spliceosomal RNAs, and telomerase stability. A mature snoRNP has been reconstituted in vitro and is composed of a single RNA and four proteins. However, snoRNP biogenesis in vivo requires multiple factors to coordinate a complex and poorly understood assembly and maturation process. Among the factors required for snoRNP biogenesis in yeast is Shq1p, an essential protein necessary for stable expression of box H/ACA snoRNAs. We have found that Shq1p consists of two independent domains that contain casein kinase 1 phosphorylation sites. We also demonstrate that Shq1p binds the pseudourydilating enzyme Cbf5p through the C-terminal domain, in synergy with the N-terminal domain. The NMR solution structure of the N-terminal domain has striking homology to the ‘Chord and Sgt1’ domain of known Hsp90 cochaperones, yet Shq1p does not interact with the yeast Hsp90 homologue in vitro. Surprisingly, Shq1p has stand-alone chaperone activity in vitro. This activity is harbored by the C-terminal domain, but it is increased by the presence of the N-terminal domain. These results provide the first evidence of a specific biochemical activity for Shq1p and a direct link to the H/ACA snoRNP.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>19426738</pmid><doi>10.1016/j.jmb.2009.04.076</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-0438-9493</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0022-2836 |
| ispartof | Journal of molecular biology, 2009-07, Vol.390 (2), p.231-244 |
| issn | 0022-2836 1089-8638 |
| language | eng |
| recordid | cdi_osti_scitechconnect_966641 |
| source | MEDLINE; ScienceDirect Journals (5 years ago - present) |
| subjects | Amino Acid Sequence BASIC BIOLOGICAL SCIENCES BIOCHEMISTRY Biochemistry, Molecular Biology Biophysics CASEIN chaperone CS domain Environmental Molecular Sciences Laboratory ENZYMES H/ACA snoRNP biogenesis Hydro-Lyases - metabolism IN VITRO IN VIVO Life Sciences Magnetic Resonance Spectroscopy Microtubule-Associated Proteins - metabolism Models, Molecular MODIFICATIONS Molecular biology Molecular Chaperones - metabolism Molecular Networks Molecular Sequence Data Nuclear Proteins - chemistry Nuclear Proteins - metabolism PHOSPHORYLATION PHOSPHOTRANSFERASES Protein Binding Protein Interaction Domains and Motifs Protein Interaction Mapping Protein Structure, Tertiary PROTEINS Ribonucleoproteins, Small Nuclear - metabolism RIBOSOMES RNA Saccharomyces cerevisiae - chemistry Saccharomyces cerevisiae - enzymology Saccharomyces cerevisiae Proteins - chemistry Saccharomyces cerevisiae Proteins - metabolism Sequence Alignment Shq1 STABILITY Structural Biology YEASTS |
| title | The Box H/ACA snoRNP Assembly Factor Shq1p is a Chaperone Protein Homologous to Hsp90 Cochaperones that Binds to the Cbf5p Enzyme |
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