The functional interactome landscape of the human histone deacetylase family

Abstract

Histone deacetylases (HDACs) are a diverse family of essential transcriptional regulatory enzymes, that function through the spatial and temporal recruitment of protein complexes. As the composition and regulation of HDAC complexes are only partially characterized, we built the first global protein interaction network for all 11 human HDACs in T cells. Integrating fluorescence microscopy, immunoaffinity purifications, quantitative mass spectrometry, and bioinformatics, we identified over 200 unreported interactions for both well-characterized and lesser-studied HDACs, a subset of which were validated by orthogonal approaches. We establish HDAC11 as a member of the survival of motor neuron complex and pinpoint a functional role in mRNA splicing. We designed a complementary label-free and metabolic-labeling mass spectrometry-based proteomics strategy for profiling interaction stability among different HDAC classes, revealing that HDAC1 interactions within chromatin-remodeling complexes are largely stable, while transcription factors preferentially exist in rapid equilibrium. Overall, this study represents a valuable resource for investigating HDAC functions in health and disease, encompassing emerging themes of HDAC regulation in cell cycle and RNA processing and a deeper functional understanding of HDAC complex stability.

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    Wang M, Weiss M, Simonovic M, Haertinger G, Schrimpf SP, Hengartner MO, von Mering C (2012 ) PaxDb, a Database of Protein Abundance Averages Across All Three Domains of Life. Mol Cell Proteomics: MCP 11: 492–500

    Not in our library10.1074/mcp.o111.014704

91. 91.

    Wang Y, Zhang H, Chen Y, Sun Y, Yang F, Yu W, Liang J, Sun L, Yang X, Shi L, Li R, Li Y, Zhang Y, Li Q, Yi X, Shang Y (2009 ) LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138: 660–672

    Not in our library10.1016/j.cell.2009.05.050

92. 92.

    Wisniewski JR, Zougman A, Mann M (2009 ) Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J Proteome Res 8: 5674–5678

    Not in our library10.1021/pr900748n

93. 93.

    Wu XY, Li H, Park EJ, Chen JD (2001 ) SMRTe inhibits MEF2C transcriptional activation by targeting HDAC4 and 5 to nuclear domains. J Biol Chem 276: 24177–24185

    Not in our library10.1074/jbc.m100412200

94. 94.

    Xiong B, Lu S, Gerton JL (2010 ) Hos1 is a lysine deacetylase for the Smc3 subunit of cohesin. Curr Biol 20: 1660–1665

    Not in our library10.1016/j.cub.2010.08.019

95. 95.

    Xue YT, Wong JM, Moreno GT, Young MK, Cote J, Wang WD (1998 ) NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 2: 851–861

    Not in our library10.1016/s1097-2765(00)80299-3

96. 96.

    Yang XJ, Gregoire S (2005 ) Class II histone deacetylases: from sequence to function, regulation, and clinical implication. Mol Cell Biol 25: 2873–2884

    Not in our library10.1128/mcb.25.8.2873-2884.2005

97. 97.

    Yang XJ, Seto E (2008 ) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Revi Mol Cell Biol 9: 206–218

    Not in our library10.1038/nrm2346

98. 98.

    You A, Tong JK, Grozinger CM, Schreiber SL (2001 ) CoREST is an integral component of the CoREST-human histone deacetylase complex. Proc Nat Acad Sci USA 98: 1454–1458

    Not in our library10.1073/pnas.98.4.1454

99. 99.

    Zhang L, Zhao J, Edenberg HJ (1999 ) A human Raf-responsive zinc-finger protein that binds to divergent sequences. Nucleic Acids Res 27: 2947–2956

    Not in our library10.1093/nar/27.14.2947

100. 100.

     Zhang Y, LeRoy G, Seelig HP, Lane WS, Reinberg D (1998 ) The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95: 279–289

     Not in our library10.1016/s0092-8674(00)81758-4

101. 101.

     Zhang Z, Lotti F, Dittmar K, Younis I, Wan L, Kasim M, Dreyfuss G (2008 ) SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing. Cell 133: 585–600

     Not in our library10.1016/j.cell.2008.03.031

102. 102.

     Zhao W, Kruse JP, Tang Y, Jung SY, Qin J, Gu W (2008 ) Negative regulation of the deacetylase SIRT1 by DBC1. Nature 451: 587–590

     Not in our library10.1038/nature06515

103. 103.

     Zhao X, Ito A, Kane CD, Liao TS, Bolger TA, Lemrow SM, Means AR, Yao TP (2001 ) The modular nature of histone deacetylase HDAC4 confers phosphorylation-dependent intracellular trafficking. J Biol Chem 276: 35042–35048

     Not in our library10.1074/jbc.m105086200

104. 104.

     Zybailov BL, Florens L, Washburn MP (2007 ) Quantitative shotgun proteomics using a protease with broad specificity and normalized spectral abundance factors. Mol Biosyst 3: 354–360

     Not in our library10.1039/b701483j

Cited by papers we hold 5

• Histone Deacetylases (HDACs): Evolution, Specificity, Role in Transcriptional Complexes, and Pharmacological Actionability · 2020
  No notice
• Proteomics and integrative omic approaches for understanding host–pathogen interactions and infectious diseases · 2017
  No notice
• Lysine acetylome profiling uncovers novel histone deacetylase substrate proteins in Arabidopsis · 2017
  No notice
• La FAM fatale: USP9X in development and disease · 2015
  No notice
• Histone Deacetylases in Herpesvirus Replication and Virus-Stimulated Host Defense · 2013
  Not checked

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