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PMID: 12684533 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

MAN1 and emerin have overlapping function(s) essential for chromosome segregation and cell division in Caenorhabditis elegans.

Liu J, Lee KK, Segura-Totten M, Neufeld E, Wilson KL, Gruenbaum Y

Abstract

Emerin and MAN1 are LEM domain-containing integral membrane proteins of the vertebrate nuclear envelope. The function of MAN1 is unknown, whereas emerin is known to interact with nuclear lamins, barrier-to-autointegration factor (BAF), nesprin-1 alpha, and a transcription repressor. Mutations in emerin cause X-linked recessive Emery-Dreifuss muscular dystrophy. Emerin and MAN1 homologs are both conserved in Caenorhabditis elegans, but loss of Ce-emerin has no detectable phenotype. We therefore used C. elegans to test the hypothesis that Ce-MAN1 overlaps functionally with Ce-emerin. Supporting this model, Ce-MAN1 interacted directly with Ce-lamin and Ce-BAF in vitro and required Ce-lamin for its nuclear envelope localization. Interestingly, RNA interference-mediated removal of approximately 90% of Ce-MAN1 was lethal to approximately 15% of embryos. However, in the absence of Ce-emerin, approximately 90% reduction of Ce-MAN1 was lethal to all embryos by the 100-cell stage, with a phenotype involving repeated cycles of anaphase chromosome bridging and cytokinesis ["cell untimely torn" (cut) phenotype]. Immunostaining showed that the anaphase-bridged chromatin specifically retained a mitosis-specific phosphohistone H3 epitope and failed to recruit detectable Ce-lamin or Ce-BAF. These findings show that LEM domain proteins are essential for cell division and that Ce-emerin and Ce-MAN1 share at least one and possibly multiple overlapping functions, which may be relevant to Emery-Dreifuss muscular dystrophy.

MeSH Terms
Animals Caenorhabditis elegans/cytology,genetics,metabolism Caenorhabditis elegans Proteins Cell Division/physiology Chromosome Segregation/physiology DNA-Binding Proteins/metabolism Genes, Helminth Humans Membrane Proteins/genetics,metabolism Muscular Dystrophy, Emery-Dreifuss/genetics Mutation Nuclear Proteins/genetics,metabolism Phenotype RNA Interference Thymopoietins/genetics,metabolism
Chemicals
BANF1 protein, human Caenorhabditis elegans Proteins DNA-Binding Proteins LEMD3 protein, human Membrane Proteins Nuclear Proteins Thymopoietins emerin lem-2 protein, C elegans
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Liu Jun
Department of Molecular Biology and Genetics, 439 Biotechnology Building, Cornell University, Ithaca, NY 14853, USA.
Lee Kenneth K
Segura-Totten Miriam
Neufeld Ester
Wilson Katherine L
Gruenbaum Yosef
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Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2003-04-15
Epub
2003-00-08
Pages
4598-603
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC153601
Subset
IM
Grants
NIGMS NIH HHS · R01 GM064535 · United States
NIGMS NIH HHS · R01 GM066953 · United States
NIGMS NIH HHS · GM64535 · United States
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