The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: Linking transcriptional elongation to histone methylation

Nevan J. Krogan; Jim Dover; Adam Wood; Jessica Schneider; Jonathan Heidt; Marry Ann Boateng; Kimberly Dean; Owen W. Ryan; Ashkan Golshani; Mark Johnston; Jack F. Greenblatt; Ali Shilatifard

doi:10.1016/S1097-2765(03)00091-1

The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: Linking transcriptional elongation to histone methylation

Nevan J. Krogan, Jim Dover, Adam Wood, Jessica Schneider, Jonathan Heidt, Marry Ann Boateng, Kimberly Dean, Owen W. Ryan, Ashkan Golshani, Mark Johnston, Jack F. Greenblatt, Ali Shilatifard^*

^*Corresponding author for this work

Biochemistry and Molecular Genetics

Research output: Contribution to journal › Article › peer-review

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Abstract

Methylation of histone proteins is one of their many modifications that affect chromatin structure and regulate gene expression. Methylation of histone H3 on lysines 4 and 79, catalyzed by the Set1-containing complex COMPASS and Dot1p, respectively, is required for silencing of expression of genes located near chromosome telomeres in yeast. We report that the Paf1 protein complex, which is associated with the elongating RNA polymerase II, is required for methylation of lysines 4 and 79 of histone H3 and for silencing of expression of a telomere-associated gene. We show that the Paf1 complex is required for recruitment of the COMPASS methyltransferase to RNA polymerase II and that the subunits of these complexes interact physically and genetically. Collectively, our results suggest that the Paf1 complex is required for histone H3 methylation, therefore linking transcriptional elongation to chromatin methylation.

Original language	English (US)
Pages (from-to)	721-729
Number of pages	9
Journal	Molecular cell
Volume	11
Issue number	3
DOIs	https://doi.org/10.1016/S1097-2765(03)00091-1
State	Published - Mar 1 2003

Funding

Methylation of lysine 4 and 79 of histone H3, catalyzed by COMPASS and Dot1p, respectively, requires ubiquitination of histone H2B on lysine 123 (Dover et al., 2002; Sun and Allis, 2002) . Ubiquitination of histone H2B is catalyzed by Rad6 (E2) (Robzyk et al., 2000) and its E3 ligase, Bre1, which seems to guide the recruitment of Rad6 to promoters (Wood et al., 2003) . Our analyses reported in this manuscript indicate that the components of the Paf1 complex are also required for methylation of histone H3 on K4 and K79. The requirement of the Paf1 complex for histone H3 methylation is supported by the following observations. (1) Loss of the components of the Paf1 complex results in defect in histone methylation on K4 and K79 of histone H3. (2) COMPASS interacts with RNA polymerase II and the Paf1 complex, and the interaction of COMPASS with RNA polymerase II requires the presence of the Paf1 complex. (3) The components of COMPASS genetically interact with the components of the Paf1 complex. (4) Dot1p requires the Paf1 complex for its histone methyltransferase function and genetically interacts with the components of the Paf1 complex. (5) Deletion of genes encoding components of the Paf1 complex result in a defect in telomeric-associated gene silencing. (6) Recruitment of COMPASS to the promoters and the early transcribing polymerase requires the Paf1 complex. Together, our data suggest a link between histone methylation and transcription elongation.

ASJC Scopus subject areas

Molecular Biology
Cell Biology

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Krogan, N. J., Dover, J., Wood, A., Schneider, J., Heidt, J., Boateng, M. A., Dean, K., Ryan, O. W., Golshani, A., Johnston, M., Greenblatt, J. F., & Shilatifard, A. (2003). The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: Linking transcriptional elongation to histone methylation. Molecular cell, 11(3), 721-729. https://doi.org/10.1016/S1097-2765(03)00091-1

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title = "The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: Linking transcriptional elongation to histone methylation",

abstract = "Methylation of histone proteins is one of their many modifications that affect chromatin structure and regulate gene expression. Methylation of histone H3 on lysines 4 and 79, catalyzed by the Set1-containing complex COMPASS and Dot1p, respectively, is required for silencing of expression of genes located near chromosome telomeres in yeast. We report that the Paf1 protein complex, which is associated with the elongating RNA polymerase II, is required for methylation of lysines 4 and 79 of histone H3 and for silencing of expression of a telomere-associated gene. We show that the Paf1 complex is required for recruitment of the COMPASS methyltransferase to RNA polymerase II and that the subunits of these complexes interact physically and genetically. Collectively, our results suggest that the Paf1 complex is required for histone H3 methylation, therefore linking transcriptional elongation to chromatin methylation.",

author = "Krogan, {Nevan J.} and Jim Dover and Adam Wood and Jessica Schneider and Jonathan Heidt and Boateng, {Marry Ann} and Kimberly Dean and Ryan, {Owen W.} and Ashkan Golshani and Mark Johnston and Greenblatt, {Jack F.} and Ali Shilatifard",

note = "Funding Information: Methylation of lysine 4 and 79 of histone H3, catalyzed by COMPASS and Dot1p, respectively, requires ubiquitination of histone H2B on lysine 123 (Dover et al., 2002; Sun and Allis, 2002) . Ubiquitination of histone H2B is catalyzed by Rad6 (E2) (Robzyk et al., 2000) and its E3 ligase, Bre1, which seems to guide the recruitment of Rad6 to promoters (Wood et al., 2003) . Our analyses reported in this manuscript indicate that the components of the Paf1 complex are also required for methylation of histone H3 on K4 and K79. The requirement of the Paf1 complex for histone H3 methylation is supported by the following observations. (1) Loss of the components of the Paf1 complex results in defect in histone methylation on K4 and K79 of histone H3. (2) COMPASS interacts with RNA polymerase II and the Paf1 complex, and the interaction of COMPASS with RNA polymerase II requires the presence of the Paf1 complex. (3) The components of COMPASS genetically interact with the components of the Paf1 complex. (4) Dot1p requires the Paf1 complex for its histone methyltransferase function and genetically interacts with the components of the Paf1 complex. (5) Deletion of genes encoding components of the Paf1 complex result in a defect in telomeric-associated gene silencing. (6) Recruitment of COMPASS to the promoters and the early transcribing polymerase requires the Paf1 complex. Together, our data suggest a link between histone methylation and transcription elongation. ",

year = "2003",

month = mar,

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doi = "10.1016/S1097-2765(03)00091-1",

language = "English (US)",

volume = "11",

pages = "721--729",

journal = "Molecular cell",

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Krogan, NJ, Dover, J, Wood, A, Schneider, J, Heidt, J, Boateng, MA, Dean, K, Ryan, OW, Golshani, A, Johnston, M, Greenblatt, JF & Shilatifard, A 2003, 'The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: Linking transcriptional elongation to histone methylation', Molecular cell, vol. 11, no. 3, pp. 721-729. https://doi.org/10.1016/S1097-2765(03)00091-1

TY - JOUR

T1 - The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p

T2 - Linking transcriptional elongation to histone methylation

AU - Krogan, Nevan J.

AU - Dover, Jim

AU - Wood, Adam

AU - Schneider, Jessica

AU - Heidt, Jonathan

AU - Boateng, Marry Ann

AU - Dean, Kimberly

AU - Ryan, Owen W.

AU - Golshani, Ashkan

AU - Johnston, Mark

AU - Greenblatt, Jack F.

AU - Shilatifard, Ali

N1 - Funding Information: Methylation of lysine 4 and 79 of histone H3, catalyzed by COMPASS and Dot1p, respectively, requires ubiquitination of histone H2B on lysine 123 (Dover et al., 2002; Sun and Allis, 2002) . Ubiquitination of histone H2B is catalyzed by Rad6 (E2) (Robzyk et al., 2000) and its E3 ligase, Bre1, which seems to guide the recruitment of Rad6 to promoters (Wood et al., 2003) . Our analyses reported in this manuscript indicate that the components of the Paf1 complex are also required for methylation of histone H3 on K4 and K79. The requirement of the Paf1 complex for histone H3 methylation is supported by the following observations. (1) Loss of the components of the Paf1 complex results in defect in histone methylation on K4 and K79 of histone H3. (2) COMPASS interacts with RNA polymerase II and the Paf1 complex, and the interaction of COMPASS with RNA polymerase II requires the presence of the Paf1 complex. (3) The components of COMPASS genetically interact with the components of the Paf1 complex. (4) Dot1p requires the Paf1 complex for its histone methyltransferase function and genetically interacts with the components of the Paf1 complex. (5) Deletion of genes encoding components of the Paf1 complex result in a defect in telomeric-associated gene silencing. (6) Recruitment of COMPASS to the promoters and the early transcribing polymerase requires the Paf1 complex. Together, our data suggest a link between histone methylation and transcription elongation.

PY - 2003/3/1

Y1 - 2003/3/1

N2 - Methylation of histone proteins is one of their many modifications that affect chromatin structure and regulate gene expression. Methylation of histone H3 on lysines 4 and 79, catalyzed by the Set1-containing complex COMPASS and Dot1p, respectively, is required for silencing of expression of genes located near chromosome telomeres in yeast. We report that the Paf1 protein complex, which is associated with the elongating RNA polymerase II, is required for methylation of lysines 4 and 79 of histone H3 and for silencing of expression of a telomere-associated gene. We show that the Paf1 complex is required for recruitment of the COMPASS methyltransferase to RNA polymerase II and that the subunits of these complexes interact physically and genetically. Collectively, our results suggest that the Paf1 complex is required for histone H3 methylation, therefore linking transcriptional elongation to chromatin methylation.

AB - Methylation of histone proteins is one of their many modifications that affect chromatin structure and regulate gene expression. Methylation of histone H3 on lysines 4 and 79, catalyzed by the Set1-containing complex COMPASS and Dot1p, respectively, is required for silencing of expression of genes located near chromosome telomeres in yeast. We report that the Paf1 protein complex, which is associated with the elongating RNA polymerase II, is required for methylation of lysines 4 and 79 of histone H3 and for silencing of expression of a telomere-associated gene. We show that the Paf1 complex is required for recruitment of the COMPASS methyltransferase to RNA polymerase II and that the subunits of these complexes interact physically and genetically. Collectively, our results suggest that the Paf1 complex is required for histone H3 methylation, therefore linking transcriptional elongation to chromatin methylation.

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UR - http://www.scopus.com/inward/citedby.url?scp=0037524702&partnerID=8YFLogxK

U2 - 10.1016/S1097-2765(03)00091-1

DO - 10.1016/S1097-2765(03)00091-1

M3 - Article

C2 - 12667454

AN - SCOPUS:0037524702

SN - 1097-2765

VL - 11

SP - 721

EP - 729

JO - Molecular cell

JF - Molecular cell

IS - 3

ER -

The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: Linking transcriptional elongation to histone methylation

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