The multidomain protein Brpf1 binds histones and is required for hox gene expression and segmental identity

Kathrin Laue, Sylvain Daujat, Justin Gage Crump, Nikki Plaster, Henry H. Roehl, F. van Bebber, E. Busch-Nentwich, R. Dahm, H. G. Frohnhöfer, H. Geiger, D. Gilmour, S. Holley, J. Hooge, D. Jülich, H. Knaut, F. Maderspacher, H. M. Maischein, C. Neumann, Teresa Nicolson, C. Nüsslein-VolhardH. H. Roehl, U. Schönberger, C. Seiler, C. Söllner, M. Sonawane, A. Wehner, P. Erker, H. Habeck, U. Hagner, C. Hennen, E. Kaps, A. Kirchner, T. Koblitzek, U. Langheinrich, C. Loeschke, C. Metzger, R. Nordin, J. Odenthal, M. Pezzuti, K. Schlombs, J. deSatana-Stamm, T. Trowe, G. Vacun, B. Walderich, A. Walker, C. Weiler, Charles B. Kimmel, Robert Schneider, Matthias Hammerschmidt

Research output: Contribution to journalArticle

78 Citations (Scopus)

Abstract

The Trithorax group (TrxG) is composed of diverse, evolutionary conserved proteins that form chromatin-associated complexes accounting for epigenetic transcriptional memory. However, the molecular mechanisms by which particular loci are marked for reactivation after mitosis are only partially understood. Here, based on genetic analyses in zebrafish, we identify the multidomain protein Brpf1 as a novel TrxG member with a central role during development. brpf1 mutants display anterior transformations of pharyngeal arches due to progressive loss of anterior Hox gene expression. Brpf1 functions in association with the histone acetyltransferase Moz (Myst3), an interaction mediated by the N-terminal domain of Brpf1, and promotes histone acetylation in vivo. Brpf1 recruits Moz to distinct sites of active chromatin and remains at chromosomes during mitosis, mediated by direct histone binding of its bromodomain, which has a preference for acetylated histones, and its PWWP domain, which binds histones independently of their acetylation status. This is the first demonstration of histone binding for PWWP domains. Mutant analyses further show that the PWWP domain is absolutely essential for Brpf1 function in vivo. We conclude that Brpf1, coordinated by its particular set of domains, acts by multiple mechanisms to mediate Moz-dependent histone acetylation and to mark Hox genes for maintained expression throughout vertebrate development.

Original languageEnglish (US)
Pages (from-to)1935-1946
Number of pages12
JournalDevelopment
Volume135
Issue number11
DOIs
StatePublished - Jun 2008
Externally publishedYes

Fingerprint

Homeobox Genes
Histones
Gene Expression
Acetylation
Proteins
Mitosis
Chromatin
Branchial Region
Histone Acetyltransferases
Zebrafish
Epigenomics
Vertebrates
Catalytic Domain
Chromosomes

Keywords

  • Anterior-posterior patterning
  • Bromodomain
  • Brpf1
  • Cranial neural crest
  • Craniofacial development
  • Homeotic transformation
  • Hox gene expression
  • Moz
  • Pharyngeal arch
  • PWWP domain
  • Zebrafish

ASJC Scopus subject areas

  • Anatomy
  • Cell Biology

Cite this

Laue, K., Daujat, S., Crump, J. G., Plaster, N., Roehl, H. H., van Bebber, F., ... Hammerschmidt, M. (2008). The multidomain protein Brpf1 binds histones and is required for hox gene expression and segmental identity. Development, 135(11), 1935-1946. https://doi.org/10.1242/dev.017160

The multidomain protein Brpf1 binds histones and is required for hox gene expression and segmental identity. / Laue, Kathrin; Daujat, Sylvain; Crump, Justin Gage; Plaster, Nikki; Roehl, Henry H.; van Bebber, F.; Busch-Nentwich, E.; Dahm, R.; Frohnhöfer, H. G.; Geiger, H.; Gilmour, D.; Holley, S.; Hooge, J.; Jülich, D.; Knaut, H.; Maderspacher, F.; Maischein, H. M.; Neumann, C.; Nicolson, Teresa; Nüsslein-Volhard, C.; Roehl, H. H.; Schönberger, U.; Seiler, C.; Söllner, C.; Sonawane, M.; Wehner, A.; Erker, P.; Habeck, H.; Hagner, U.; Hennen, C.; Kaps, E.; Kirchner, A.; Koblitzek, T.; Langheinrich, U.; Loeschke, C.; Metzger, C.; Nordin, R.; Odenthal, J.; Pezzuti, M.; Schlombs, K.; deSatana-Stamm, J.; Trowe, T.; Vacun, G.; Walderich, B.; Walker, A.; Weiler, C.; Kimmel, Charles B.; Schneider, Robert; Hammerschmidt, Matthias.

In: Development, Vol. 135, No. 11, 06.2008, p. 1935-1946.

Research output: Contribution to journalArticle

Laue, K, Daujat, S, Crump, JG, Plaster, N, Roehl, HH, van Bebber, F, Busch-Nentwich, E, Dahm, R, Frohnhöfer, HG, Geiger, H, Gilmour, D, Holley, S, Hooge, J, Jülich, D, Knaut, H, Maderspacher, F, Maischein, HM, Neumann, C, Nicolson, T, Nüsslein-Volhard, C, Roehl, HH, Schönberger, U, Seiler, C, Söllner, C, Sonawane, M, Wehner, A, Erker, P, Habeck, H, Hagner, U, Hennen, C, Kaps, E, Kirchner, A, Koblitzek, T, Langheinrich, U, Loeschke, C, Metzger, C, Nordin, R, Odenthal, J, Pezzuti, M, Schlombs, K, deSatana-Stamm, J, Trowe, T, Vacun, G, Walderich, B, Walker, A, Weiler, C, Kimmel, CB, Schneider, R & Hammerschmidt, M 2008, 'The multidomain protein Brpf1 binds histones and is required for hox gene expression and segmental identity', Development, vol. 135, no. 11, pp. 1935-1946. https://doi.org/10.1242/dev.017160
Laue, Kathrin ; Daujat, Sylvain ; Crump, Justin Gage ; Plaster, Nikki ; Roehl, Henry H. ; van Bebber, F. ; Busch-Nentwich, E. ; Dahm, R. ; Frohnhöfer, H. G. ; Geiger, H. ; Gilmour, D. ; Holley, S. ; Hooge, J. ; Jülich, D. ; Knaut, H. ; Maderspacher, F. ; Maischein, H. M. ; Neumann, C. ; Nicolson, Teresa ; Nüsslein-Volhard, C. ; Roehl, H. H. ; Schönberger, U. ; Seiler, C. ; Söllner, C. ; Sonawane, M. ; Wehner, A. ; Erker, P. ; Habeck, H. ; Hagner, U. ; Hennen, C. ; Kaps, E. ; Kirchner, A. ; Koblitzek, T. ; Langheinrich, U. ; Loeschke, C. ; Metzger, C. ; Nordin, R. ; Odenthal, J. ; Pezzuti, M. ; Schlombs, K. ; deSatana-Stamm, J. ; Trowe, T. ; Vacun, G. ; Walderich, B. ; Walker, A. ; Weiler, C. ; Kimmel, Charles B. ; Schneider, Robert ; Hammerschmidt, Matthias. / The multidomain protein Brpf1 binds histones and is required for hox gene expression and segmental identity. In: Development. 2008 ; Vol. 135, No. 11. pp. 1935-1946.
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AU - Daujat, Sylvain

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AU - Roehl, Henry H.

AU - van Bebber, F.

AU - Busch-Nentwich, E.

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AU - Geiger, H.

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AU - Holley, S.

AU - Hooge, J.

AU - Jülich, D.

AU - Knaut, H.

AU - Maderspacher, F.

AU - Maischein, H. M.

AU - Neumann, C.

AU - Nicolson, Teresa

AU - Nüsslein-Volhard, C.

AU - Roehl, H. H.

AU - Schönberger, U.

AU - Seiler, C.

AU - Söllner, C.

AU - Sonawane, M.

AU - Wehner, A.

AU - Erker, P.

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AU - Hagner, U.

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AU - Koblitzek, T.

AU - Langheinrich, U.

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AU - Nordin, R.

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AU - Pezzuti, M.

AU - Schlombs, K.

AU - deSatana-Stamm, J.

AU - Trowe, T.

AU - Vacun, G.

AU - Walderich, B.

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KW - Bromodomain

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KW - Cranial neural crest

KW - Craniofacial development

KW - Homeotic transformation

KW - Hox gene expression

KW - Moz

KW - Pharyngeal arch

KW - PWWP domain

KW - Zebrafish

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