Lamin B Receptor Recognizes Specific Modifications of Histone H4 in Heterochromatin Formation

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2012 Oct 27

PMID 23100253

Citations 54

Authors

Yasuhiro Hirano

Kohji Hizume

Hiroshi Kimura

Kunio Takeyasu

Tokuko Haraguchi

Yasushi Hiraoka

Affiliations

Soon will be listed here.

Abstract

Inner nuclear membrane proteins provide a structural framework for chromatin, modulating transcription beneath the nuclear envelope. Lamin B receptor (LBR) is a classical inner nuclear membrane protein that associates with heterochromatin, and its mutations are known to cause Pelger-Huët anomaly in humans. However, the mechanisms by which LBR organizes heterochromatin remain to be elucidated. Here, we show that LBR represses transcription by binding to chromatin regions that are marked by specific histone modifications. The tudor domain (residues 1-62) of LBR primarily recognizes histone H4 lysine 20 dimethylation and is essential for chromatin compaction, whereas the whole nucleoplasmic region (residues 1-211) is required for transcriptional repression. We propose a model in which the nucleoplasmic domain of LBR tethers epigenetically marked chromatin to the nuclear envelope and transcriptional repressors are loaded onto the chromatin through their interaction with LBR.

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References

Polioudaki H, Kourmouli N, Drosou V, Bakou A, Theodoropoulos P, Singh P . Histones H3/H4 form a tight complex with the inner nuclear membrane protein LBR and heterochromatin protein 1. EMBO Rep. 2001; 2(10):920-5. PMC: 1084077. DOI: 10.1093/embo-reports/kve199. View

Takano M, Takeuchi M, Ito H, Furukawa K, Sugimoto K, Omata S . The binding of lamin B receptor to chromatin is regulated by phosphorylation in the RS region. Eur J Biochem. 2002; 269(3):943-53. DOI: 10.1046/j.0014-2956.2001.02730.x. View

HAYES J, Clark D, Wolffe A . Histone contributions to the structure of DNA in the nucleosome. Proc Natl Acad Sci U S A. 1991; 88(15):6829-33. PMC: 52182. DOI: 10.1073/pnas.88.15.6829. View

Guarda A, Bolognese F, Bonapace I, Badaracco G . Interaction between the inner nuclear membrane lamin B receptor and the heterochromatic methyl binding protein, MeCP2. Exp Cell Res. 2009; 315(11):1895-903. DOI: 10.1016/j.yexcr.2009.01.019. View

Martins S, Eide T, Steen R, Jahnsen T, Skalhegg B S, Collas P . HA95 is a protein of the chromatin and nuclear matrix regulating nuclear envelope dynamics. J Cell Sci. 2000; 113 Pt 21:3703-13. DOI: 10.1242/jcs.113.21.3703. View

Greeson N, Sengupta R, Arida A, Jenuwein T, Sanders S . Di-methyl H4 lysine 20 targets the checkpoint protein Crb2 to sites of DNA damage. J Biol Chem. 2008; 283(48):33168-74. PMC: 2662251. DOI: 10.1074/jbc.M806857200. View

Hoffmann K, Sperling K, Olins A, Olins D . The granulocyte nucleus and lamin B receptor: avoiding the ovoid. Chromosoma. 2007; 116(3):227-35. DOI: 10.1007/s00412-007-0094-8. View

Wysocka J, Swigut T, Milne T, Dou Y, Zhang X, Burlingame A . WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell. 2005; 121(6):859-72. DOI: 10.1016/j.cell.2005.03.036. View

Tsuchiya M, Ogawa H, Suzuki T, Sugiyama N, Haraguchi T, Hiraoka Y . Exportin 4 interacts with Sox9 through the HMG Box and inhibits the DNA binding of Sox9. PLoS One. 2011; 6(10):e25694. PMC: 3185033. DOI: 10.1371/journal.pone.0025694. View

10.

Bock I, Kudithipudi S, Tamas R, Kungulovski G, Dhayalan A, Jeltsch A . Application of Celluspots peptide arrays for the analysis of the binding specificity of epigenetic reading domains to modified histone tails. BMC Biochem. 2011; 12:48. PMC: 3176149. DOI: 10.1186/1471-2091-12-48. View

11.

Ye Q, Callebaut I, Pezhman A, Courvalin J, Worman H . Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR. J Biol Chem. 1997; 272(23):14983-9. DOI: 10.1074/jbc.272.23.14983. View

12.

Hirano Y, Ishii K, Kumeta M, Furukawa K, Takeyasu K, Horigome T . Proteomic and targeted analytical identification of BXDC1 and EBNA1BP2 as dynamic scaffold proteins in the nucleolus. Genes Cells. 2009; 14(2):155-66. DOI: 10.1111/j.1365-2443.2008.01262.x. View

13.

Courvalin J . Inner nuclear membrane protein LBR preferentially interacts with DNA secondary structures and nucleosomal linker. Biochemistry. 2000; 39(21):6483-8. DOI: 10.1021/bi992908b. View

14.

Towbin B, Meister P, Gasser S . The nuclear envelope--a scaffold for silencing?. Curr Opin Genet Dev. 2009; 19(2):180-6. DOI: 10.1016/j.gde.2009.01.006. View

15.

Hizume K, Yoshimura S, Takeyasu K . Linker histone H1 per se can induce three-dimensional folding of chromatin fiber. Biochemistry. 2005; 44(39):12978-89. DOI: 10.1021/bi050623v. View

16.

Hoffmann K, Dreger C, Olins A, Olins D, Shultz L, Lucke B . Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger-Huët anomaly). Nat Genet. 2002; 31(4):410-4. DOI: 10.1038/ng925. View

17.

Zwerger M, Herrmann H, Gaines P, Olins A, Olins D . Granulocytic nuclear differentiation of lamin B receptor-deficient mouse EPRO cells. Exp Hematol. 2008; 36(8):977-87. PMC: 2547467. DOI: 10.1016/j.exphem.2008.03.003. View

18.

Hirano Y, Takahashi H, Kumeta M, Hizume K, Hirai Y, Otsuka S . Nuclear architecture and chromatin dynamics revealed by atomic force microscopy in combination with biochemistry and cell biology. Pflugers Arch. 2008; 456(1):139-53. DOI: 10.1007/s00424-007-0431-z. View

19.

Sprague B, Pego R, Stavreva D, McNally J . Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys J. 2004; 86(6):3473-95. PMC: 1304253. DOI: 10.1529/biophysj.103.026765. View

20.

Ohniwa R, Morikawa K, Takeshita S, Kim J, Ohta T, Wada C . Transcription-coupled nucleoid architecture in bacteria. Genes Cells. 2007; 12(10):1141-52. DOI: 10.1111/j.1365-2443.2007.01125.x. View