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PMID:26744419

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Citation

Barrales, RR, Forn, M, Georgescu, PR, Sarkadi, Z and Braun, S (2016) Control of heterochromatin localization and silencing by the nuclear membrane protein Lem2. Genes Dev. 30:133-48

Abstract

Transcriptionally silent chromatin localizes to the nuclear periphery, which provides a special microenvironment for gene repression. A variety of nuclear membrane proteins interact with repressed chromatin, yet the functional role of these interactions remains poorly understood. Here, we show that, in Schizosaccharomyces pombe, the nuclear membrane protein Lem2 associates with chromatin and mediates silencing and heterochromatin localization. Unexpectedly, we found that these functions can be separated and assigned to different structural domains within Lem2, excluding a simple tethering mechanism. Chromatin association and tethering of centromeres to the periphery are mediated by the N-terminal LEM (LAP2-Emerin-MAN1) domain of Lem2, whereas telomere anchoring and heterochromatin silencing require exclusively its conserved C-terminal MSC (MAN1-Src1 C-terminal) domain. Particularly, silencing by Lem2 is epistatic with the Snf2/HDAC (histone deacetylase) repressor complex SHREC at telomeres, while its necessity can be bypassed by deleting Epe1, a JmjC protein with anti-silencing activity. Furthermore, we found that loss of Lem2 reduces heterochromatin association of SHREC, which is accompanied by increased binding of Epe1. This reveals a critical function of Lem2 in coordinating these antagonistic factors at heterochromatin. The distinct silencing and localization functions mediated by Lem2 suggest that these conserved LEM-containing proteins go beyond simple tethering to play active roles in perinuclear silencing.

Links

PubMed Online version:10.1101/gad.271288.115

Keywords


Significance

Annotations

Gene product Qualifier GO Term Evidence Code with/from Aspect Extension Notes Status

SCHPO:TAZ1

is_active_in

GO:0034399: nuclear periphery

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

SCHPO:LEM2

enables

GO:0003682: chromatin binding

ECO:0000314: direct assay evidence used in manual assertion

F

Seeded From UniProt

complete

SCHPO:LEM2

is_active_in

GO:0005635: nuclear envelope

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

SCHPO:LEM2

is_active_in

GO:0005721: pericentric heterochromatin

ECO:0000314: direct assay evidence used in manual assertion

C

  • coincident_with:(SO:0001796)

Seeded From UniProt

complete

SCHPO:LEM2

enables

GO:0140449: centromere-nuclear envelope anchor activity

ECO:0000314: direct assay evidence used in manual assertion

F

Seeded From UniProt

complete

SCHPO:LEM2

enables

GO:0062239: heterochromatin-nuclear membrane anchor activity

ECO:0000314: direct assay evidence used in manual assertion

F

Seeded From UniProt

complete

SCHPO:LEM2

involved_in

GO:0140462: pericentric heterochromatin organization

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

SCHPO:LEM2

involved_in

GO:0140464: silent mating-type cassette heterochromatin organization

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

SCHPO:LEM2

involved_in

GO:0140698: attachment of telomeric heterochromatin to nuclear envelope

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

SCHPO:LEM2

involved_in

GO:0072766: centromere clustering at the mitotic interphase nuclear envelope

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

SCHPO:TAZ1

part_of

GO:0034399: nuclear periphery

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

SCHPO:LEM2

involved_in

GO:0072766: centromere clustering at the mitotic nuclear envelope

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

SCHPO:LEM2

involved_in

GO:0099114: chromatin silencing at subtelomere

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

SCHPO:LEM2

involved_in

GO:1990141: chromatin silencing at centromere outer repeat region

ECO:0000315: mutant phenotype evidence used in manual assertion

P

occurs_at:(SO:0001799)

Seeded From UniProt

complete

SCHPO:LEM2

GO:0140462: pericentric heterochromatin organization

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Figure 1C Quantitative analysis by RT-qPCR revealed that lem2Δ cells display a twofold increase in reporter gene expression

needs relation

complete
CACAO 11261

SCHPO:LEM2

NOT

GO:0010629: negative regulation of gene expression

ECO:0000315:

P

Lem2 is deleted and there is more transcription

complete
CACAO 11794

SCHPO:LEM2

enables

GO:0003682: chromatin binding

ECO:0000314: direct assay evidence used in manual assertion

F

occurs_at:(SO:0001796)

Seeded From UniProt

complete

SCHPO:LEM2

part_of

GO:0005635: nuclear envelope

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

SCHPO:LEM2

involved_in

GO:0030466: chromatin silencing at silent mating-type cassette

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

SCHPO:LEM2

part_of

GO:0031618: nuclear pericentric heterochromatin

ECO:0000314: direct assay evidence used in manual assertion

C

coincident_with:(SO:0001796)

Seeded From UniProt

complete

SCHPO:LEM2

involved_in

GO:0034398: telomere tethering at nuclear periphery

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

Notes

See also

References

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