Chromatin-bound NLS proteins recruit membrane vesicles and nucleoporins for nuclear envelope assembly via importin-α/β

Quanlong Lu, Zhigang Lu, Qinying Liu, Li Guo, He Ren, Jingyan Fu, Qing Jiang, Paul R. Clarke, Chuanmao Zhang

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

The mechanism for nuclear envelope (NE) assembly is not fully understood. Importin-β and the small GTPase Ran have been implicated in the spatial regulation of NE assembly process. Here we report that chromatin-bound NLS (nuclear localization sequence) proteins provide docking sites for the NE precursor membrane vesicles and nucleoporins via importin-α and -β during NE assembly in Xenopus egg extracts. We show that along with the fast recruitment of the abundant NLS proteins such as nucleoplasmin and histones to the demembranated sperm chromatin in the extracts, importin-α binds the chromatin NLS proteins rapidly. Meanwhile, importin-β binds cytoplasmic NE precursor membrane vesicles and nucleoporins. Through interacting with importin-α on the chromatin NLS proteins, importin-β targets the membrane vesicles and nucleoporins to the chromatin surface. Once encountering Ran-GTP on the chromatin generated by RCC1, importin-β preferentially binds Ran-GTP and releases the membrane vesicles and nucleoporins for NE assembly. NE assembly is disrupted by blocking the interaction between importin-α and NLS proteins with excess soluble NLS proteins or by depletion of importin-β from the extract. Our findings reveal a novel molecular mechanism for NE assembly in Xenopus egg extracts.

Original languageEnglish (US)
Pages (from-to)1562-1575
Number of pages14
JournalCell Research
Volume22
Issue number11
DOIs
StatePublished - Nov 1 2012

Fingerprint

Nuclear Pore Complex Proteins
Karyopherins
Nuclear Envelope
Chromatin
Membrane Proteins
Proteins
Membranes
Xenopus
Guanosine Triphosphate
Ovum
Nucleoplasmins
Monomeric GTP-Binding Proteins
Histones
Spermatozoa

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

Cite this

Chromatin-bound NLS proteins recruit membrane vesicles and nucleoporins for nuclear envelope assembly via importin-α/β. / Lu, Quanlong; Lu, Zhigang; Liu, Qinying; Guo, Li; Ren, He; Fu, Jingyan; Jiang, Qing; Clarke, Paul R.; Zhang, Chuanmao.

In: Cell Research, Vol. 22, No. 11, 01.11.2012, p. 1562-1575.

Research output: Contribution to journalArticle

Lu, Quanlong ; Lu, Zhigang ; Liu, Qinying ; Guo, Li ; Ren, He ; Fu, Jingyan ; Jiang, Qing ; Clarke, Paul R. ; Zhang, Chuanmao. / Chromatin-bound NLS proteins recruit membrane vesicles and nucleoporins for nuclear envelope assembly via importin-α/β. In: Cell Research. 2012 ; Vol. 22, No. 11. pp. 1562-1575.
@article{ddbd2f12c4764f01a6d9523c762bac9a,
title = "Chromatin-bound NLS proteins recruit membrane vesicles and nucleoporins for nuclear envelope assembly via importin-α/β",
abstract = "The mechanism for nuclear envelope (NE) assembly is not fully understood. Importin-β and the small GTPase Ran have been implicated in the spatial regulation of NE assembly process. Here we report that chromatin-bound NLS (nuclear localization sequence) proteins provide docking sites for the NE precursor membrane vesicles and nucleoporins via importin-α and -β during NE assembly in Xenopus egg extracts. We show that along with the fast recruitment of the abundant NLS proteins such as nucleoplasmin and histones to the demembranated sperm chromatin in the extracts, importin-α binds the chromatin NLS proteins rapidly. Meanwhile, importin-β binds cytoplasmic NE precursor membrane vesicles and nucleoporins. Through interacting with importin-α on the chromatin NLS proteins, importin-β targets the membrane vesicles and nucleoporins to the chromatin surface. Once encountering Ran-GTP on the chromatin generated by RCC1, importin-β preferentially binds Ran-GTP and releases the membrane vesicles and nucleoporins for NE assembly. NE assembly is disrupted by blocking the interaction between importin-α and NLS proteins with excess soluble NLS proteins or by depletion of importin-β from the extract. Our findings reveal a novel molecular mechanism for NE assembly in Xenopus egg extracts.",
author = "Quanlong Lu and Zhigang Lu and Qinying Liu and Li Guo and He Ren and Jingyan Fu and Qing Jiang and Clarke, {Paul R.} and Chuanmao Zhang",
year = "2012",
month = "11",
day = "1",
doi = "10.1038/cr.2012.113",
language = "English (US)",
volume = "22",
pages = "1562--1575",
journal = "Cell Research",
issn = "1001-0602",
publisher = "Nature Publishing Group",
number = "11",

}

TY - JOUR

T1 - Chromatin-bound NLS proteins recruit membrane vesicles and nucleoporins for nuclear envelope assembly via importin-α/β

AU - Lu, Quanlong

AU - Lu, Zhigang

AU - Liu, Qinying

AU - Guo, Li

AU - Ren, He

AU - Fu, Jingyan

AU - Jiang, Qing

AU - Clarke, Paul R.

AU - Zhang, Chuanmao

PY - 2012/11/1

Y1 - 2012/11/1

N2 - The mechanism for nuclear envelope (NE) assembly is not fully understood. Importin-β and the small GTPase Ran have been implicated in the spatial regulation of NE assembly process. Here we report that chromatin-bound NLS (nuclear localization sequence) proteins provide docking sites for the NE precursor membrane vesicles and nucleoporins via importin-α and -β during NE assembly in Xenopus egg extracts. We show that along with the fast recruitment of the abundant NLS proteins such as nucleoplasmin and histones to the demembranated sperm chromatin in the extracts, importin-α binds the chromatin NLS proteins rapidly. Meanwhile, importin-β binds cytoplasmic NE precursor membrane vesicles and nucleoporins. Through interacting with importin-α on the chromatin NLS proteins, importin-β targets the membrane vesicles and nucleoporins to the chromatin surface. Once encountering Ran-GTP on the chromatin generated by RCC1, importin-β preferentially binds Ran-GTP and releases the membrane vesicles and nucleoporins for NE assembly. NE assembly is disrupted by blocking the interaction between importin-α and NLS proteins with excess soluble NLS proteins or by depletion of importin-β from the extract. Our findings reveal a novel molecular mechanism for NE assembly in Xenopus egg extracts.

AB - The mechanism for nuclear envelope (NE) assembly is not fully understood. Importin-β and the small GTPase Ran have been implicated in the spatial regulation of NE assembly process. Here we report that chromatin-bound NLS (nuclear localization sequence) proteins provide docking sites for the NE precursor membrane vesicles and nucleoporins via importin-α and -β during NE assembly in Xenopus egg extracts. We show that along with the fast recruitment of the abundant NLS proteins such as nucleoplasmin and histones to the demembranated sperm chromatin in the extracts, importin-α binds the chromatin NLS proteins rapidly. Meanwhile, importin-β binds cytoplasmic NE precursor membrane vesicles and nucleoporins. Through interacting with importin-α on the chromatin NLS proteins, importin-β targets the membrane vesicles and nucleoporins to the chromatin surface. Once encountering Ran-GTP on the chromatin generated by RCC1, importin-β preferentially binds Ran-GTP and releases the membrane vesicles and nucleoporins for NE assembly. NE assembly is disrupted by blocking the interaction between importin-α and NLS proteins with excess soluble NLS proteins or by depletion of importin-β from the extract. Our findings reveal a novel molecular mechanism for NE assembly in Xenopus egg extracts.

UR - http://www.scopus.com/inward/record.url?scp=84868527724&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84868527724&partnerID=8YFLogxK

U2 - 10.1038/cr.2012.113

DO - 10.1038/cr.2012.113

M3 - Article

VL - 22

SP - 1562

EP - 1575

JO - Cell Research

JF - Cell Research

SN - 1001-0602

IS - 11

ER -