The basal transcription complex component TAF3 transduces changes in nuclear phosphoinositides into transcriptional output

Yvette Stijf-Bultsma; Lilly Sommer; Maria Tauber; Mai Baalbaki; Panagiota Giardoglou; David R. Jones; Kathy A. Gelato; Jason vanPelt; Zahid Shah; Homa Rahnamoun; Clara Toma; Karen E. Anderson; Philip Hawkins; Shannon M. Lauberth; Anna Pavlina G. Haramis; Daniel Hart; Wolfgang Fischle; Nullin Divecha

doi:10.1016/j.molcel.2015.03.009

The basal transcription complex component TAF3 transduces changes in nuclear phosphoinositides into transcriptional output

Yvette Stijf-Bultsma, Lilly Sommer, Maria Tauber, Mai Baalbaki, Panagiota Giardoglou, David R. Jones, Kathy A. Gelato, Jason vanPelt, Zahid Shah, Homa Rahnamoun, Clara Toma, Karen E. Anderson, Philip Hawkins, Shannon M. Lauberth, Anna Pavlina G. Haramis, Daniel Hart, Wolfgang Fischle, Nullin Divecha^*

^*Corresponding author for this work

Biological, Environmental Sciences and Engineering

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

41 Scopus citations

Abstract

Phosphoinositides (PI) are important signaling molecules in the nucleus that influence gene expression. However, if and how nuclear PI directly affects the transcriptional machinery is not known. We report that the lipid kinase PIP4K2B regulates nuclear PI5P and the expression of myogenic genes during myoblast differentiation. A targeted screen for PI interactors identified the PHD finger of TAF3, a TATA box binding protein-associated factor with important roles in transcription regulation, pluripotency, and differentiation. We show that the PI interaction site is distinct from the known H3K4me3 binding region of TAF3 and that PI binding modulates association of TAF3 with H3K4me3 invitro and with chromatin invivo. Analysis of TAF3 mutants indicates that TAF3 transduces PIP4K2B-mediated alterations in PI into changes in specific gene transcription. Our study reveals TAF3 as a direct target of nuclear PI and further illustrates the importance of basal transcription components as signal transducers.

Original language	English (US)
Pages (from-to)	453-467
Number of pages	15
Journal	Molecular Cell
Volume	58
Issue number	3
DOIs	https://doi.org/10.1016/j.molcel.2015.03.009
State	Published - May 7 2015

Bibliographical note

Funding Information:
We are grateful to the K.W.F. (Netherlands), CRUK (grant no. C5759/A12328), and Southampton University for funding and Prof Timmers (Utrecht University) for reagents and discussion. We would also like to thank colleagues from the Somervaille lab (PICR), the department of biological sciences (U.O.S.) and Y. Yong (PICR) for useful discussions. The work in the lab of W.F. was funded by the Max Planck Society and the Deutsche Forschungsgemeinschaft (grant no. 564967). A.-P.G.H. was funded by the Dutch Cancer Society (KWF) (grant UL 2012-5395). This work was supported in part by the American Cancer Society ACS-IRG #70-002 (S.M.L.). K.A. and P.H. acknowledge support from Biotechnology and Biological Research Council (ISPG BB/J004456/1).

Publisher Copyright:
© 2015 The Authors.

ASJC Scopus subject areas

Molecular Biology
Cell Biology

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10.1016/j.molcel.2015.03.009

Cite this

Stijf-Bultsma, Y., Sommer, L., Tauber, M., Baalbaki, M., Giardoglou, P., Jones, D. R., Gelato, K. A., vanPelt, J., Shah, Z., Rahnamoun, H., Toma, C., Anderson, K. E., Hawkins, P., Lauberth, S. M., Haramis, A. P. G., Hart, D., Fischle, W., & Divecha, N. (2015). The basal transcription complex component TAF3 transduces changes in nuclear phosphoinositides into transcriptional output. Molecular Cell, 58(3), 453-467. https://doi.org/10.1016/j.molcel.2015.03.009

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title = "The basal transcription complex component TAF3 transduces changes in nuclear phosphoinositides into transcriptional output",

abstract = "Phosphoinositides (PI) are important signaling molecules in the nucleus that influence gene expression. However, if and how nuclear PI directly affects the transcriptional machinery is not known. We report that the lipid kinase PIP4K2B regulates nuclear PI5P and the expression of myogenic genes during myoblast differentiation. A targeted screen for PI interactors identified the PHD finger of TAF3, a TATA box binding protein-associated factor with important roles in transcription regulation, pluripotency, and differentiation. We show that the PI interaction site is distinct from the known H3K4me3 binding region of TAF3 and that PI binding modulates association of TAF3 with H3K4me3 invitro and with chromatin invivo. Analysis of TAF3 mutants indicates that TAF3 transduces PIP4K2B-mediated alterations in PI into changes in specific gene transcription. Our study reveals TAF3 as a direct target of nuclear PI and further illustrates the importance of basal transcription components as signal transducers.",

author = "Yvette Stijf-Bultsma and Lilly Sommer and Maria Tauber and Mai Baalbaki and Panagiota Giardoglou and Jones, {David R.} and Gelato, {Kathy A.} and Jason vanPelt and Zahid Shah and Homa Rahnamoun and Clara Toma and Anderson, {Karen E.} and Philip Hawkins and Lauberth, {Shannon M.} and Haramis, {Anna Pavlina G.} and Daniel Hart and Wolfgang Fischle and Nullin Divecha",

note = "Funding Information: We are grateful to the K.W.F. (Netherlands), CRUK (grant no. C5759/A12328), and Southampton University for funding and Prof Timmers (Utrecht University) for reagents and discussion. We would also like to thank colleagues from the Somervaille lab (PICR), the department of biological sciences (U.O.S.) and Y. Yong (PICR) for useful discussions. The work in the lab of W.F. was funded by the Max Planck Society and the Deutsche Forschungsgemeinschaft (grant no. 564967). A.-P.G.H. was funded by the Dutch Cancer Society (KWF) (grant UL 2012-5395). This work was supported in part by the American Cancer Society ACS-IRG #70-002 (S.M.L.). K.A. and P.H. acknowledge support from Biotechnology and Biological Research Council (ISPG BB/J004456/1). Publisher Copyright: {\textcopyright} 2015 The Authors.",

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Stijf-Bultsma, Y, Sommer, L, Tauber, M, Baalbaki, M, Giardoglou, P, Jones, DR, Gelato, KA, vanPelt, J, Shah, Z, Rahnamoun, H, Toma, C, Anderson, KE, Hawkins, P, Lauberth, SM, Haramis, APG, Hart, D, Fischle, W & Divecha, N 2015, 'The basal transcription complex component TAF3 transduces changes in nuclear phosphoinositides into transcriptional output', Molecular Cell, vol. 58, no. 3, pp. 453-467. https://doi.org/10.1016/j.molcel.2015.03.009

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T1 - The basal transcription complex component TAF3 transduces changes in nuclear phosphoinositides into transcriptional output

AU - Stijf-Bultsma, Yvette

AU - Sommer, Lilly

AU - Tauber, Maria

AU - Baalbaki, Mai

AU - Giardoglou, Panagiota

AU - Jones, David R.

AU - Gelato, Kathy A.

AU - vanPelt, Jason

AU - Shah, Zahid

AU - Rahnamoun, Homa

AU - Toma, Clara

AU - Anderson, Karen E.

AU - Hawkins, Philip

AU - Lauberth, Shannon M.

AU - Haramis, Anna Pavlina G.

AU - Hart, Daniel

AU - Fischle, Wolfgang

AU - Divecha, Nullin

N1 - Funding Information: We are grateful to the K.W.F. (Netherlands), CRUK (grant no. C5759/A12328), and Southampton University for funding and Prof Timmers (Utrecht University) for reagents and discussion. We would also like to thank colleagues from the Somervaille lab (PICR), the department of biological sciences (U.O.S.) and Y. Yong (PICR) for useful discussions. The work in the lab of W.F. was funded by the Max Planck Society and the Deutsche Forschungsgemeinschaft (grant no. 564967). A.-P.G.H. was funded by the Dutch Cancer Society (KWF) (grant UL 2012-5395). This work was supported in part by the American Cancer Society ACS-IRG #70-002 (S.M.L.). K.A. and P.H. acknowledge support from Biotechnology and Biological Research Council (ISPG BB/J004456/1). Publisher Copyright: © 2015 The Authors.

PY - 2015/5/7

Y1 - 2015/5/7

N2 - Phosphoinositides (PI) are important signaling molecules in the nucleus that influence gene expression. However, if and how nuclear PI directly affects the transcriptional machinery is not known. We report that the lipid kinase PIP4K2B regulates nuclear PI5P and the expression of myogenic genes during myoblast differentiation. A targeted screen for PI interactors identified the PHD finger of TAF3, a TATA box binding protein-associated factor with important roles in transcription regulation, pluripotency, and differentiation. We show that the PI interaction site is distinct from the known H3K4me3 binding region of TAF3 and that PI binding modulates association of TAF3 with H3K4me3 invitro and with chromatin invivo. Analysis of TAF3 mutants indicates that TAF3 transduces PIP4K2B-mediated alterations in PI into changes in specific gene transcription. Our study reveals TAF3 as a direct target of nuclear PI and further illustrates the importance of basal transcription components as signal transducers.

AB - Phosphoinositides (PI) are important signaling molecules in the nucleus that influence gene expression. However, if and how nuclear PI directly affects the transcriptional machinery is not known. We report that the lipid kinase PIP4K2B regulates nuclear PI5P and the expression of myogenic genes during myoblast differentiation. A targeted screen for PI interactors identified the PHD finger of TAF3, a TATA box binding protein-associated factor with important roles in transcription regulation, pluripotency, and differentiation. We show that the PI interaction site is distinct from the known H3K4me3 binding region of TAF3 and that PI binding modulates association of TAF3 with H3K4me3 invitro and with chromatin invivo. Analysis of TAF3 mutants indicates that TAF3 transduces PIP4K2B-mediated alterations in PI into changes in specific gene transcription. Our study reveals TAF3 as a direct target of nuclear PI and further illustrates the importance of basal transcription components as signal transducers.

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SN - 1097-2765

VL - 58

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EP - 467

JO - Molecular Cell

JF - Molecular Cell

IS - 3

ER -

The basal transcription complex component TAF3 transduces changes in nuclear phosphoinositides into transcriptional output

Abstract

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