Drosophila male and female germline stem cell niches require the nuclear lamina protein Otefin

被引:17
作者
Barton, Lacy J. [1 ,2 ]
Lovander, Kaylee E. [1 ]
Pinto, Belinda S. [1 ,3 ]
Geyer, Pamela K. [1 ]
机构
[1] Univ Iowa, Dept Biochem, Iowa City, IA 52242 USA
[2] NYU, Sch Med, Dept Cell Biol, Skirball Inst, New York, NY 10016 USA
[3] Univ Florida, Coll Med, Ctr Neurogenet, Dept Mol Genet & Microbiol, Gainesville, FL 32610 USA
关键词
Nuclear lamina; LEM-domain proteins; Spermatogenesis; Oogenesis; Germline stem cells; Drosophila; LEM-DOMAIN PROTEINS; TO-AUTOINTEGRATION FACTOR; SELF-RENEWAL; MEMBRANE PROTEIN; GENE-EXPRESSION; CAENORHABDITIS-ELEGANS; ESSENTIAL ROLES; EMERIN; OVARY; ENVELOPE;
D O I
10.1016/j.ydbio.2016.05.001
中图分类号
Q [生物科学];
学科分类号
090105 [作物生产系统与生态工程];
摘要
The nuclear lamina is an extensive protein network that underlies the inner nuclear envelope. This network includes the (L) under bar AP2-(e) under bar merin-(M) under bar ANI-(d) under bar omain (LEM-D) protein family, proteins that share an association with the chromatin binding protein Barrier-to-autointegration factor (BAF). Loss of individual LEM-D proteins causes progressive, tissue-restricted diseases, known as laminopathies. Mechanisms associated with laminopathies are not yet understood. Here we present our studies of one of the Drosophila nuclear lamina LEM-D proteins, Otefin (Ote), a homologue of emerin. Previous studies have shown that Ote is autonomously required for the survival of female germline stem cells (GSCs). We demonstrate that Ote is also required for survival of somatic cells in the ovarian niche, with loss of Ote causing a decrease in cap cell number and altered signal transduction. We show germ cell-restricted expression of Ote rescues these defects, revealing a non-autonomous function for Ote in niche maintenance and emphasizing that GSCs contribute to the maintenance of their own niches. Further, we investigate the requirement of Ote in the male fertility. We show that ote mutant males become prematurely sterile as they age. Parallel to observations in females, this sterility is associated with GSC loss and changes in somatic cells of the niche, phenotypes that are largely rescued by germ cell-restricted Ote expression. Taken together, our studies demonstrate that Ote is required autonomously for survival of two stem cell populations, as well as non-autonomously for maintenance of two somatic niches. Finally, our data add to growing evidence that LEM-D proteins have critical roles in stem cell survival and tissue homeostasis. (C) 2016 Elsevier Inc. All rights reserved.
引用
收藏
页码:75 / 86
页数:12
相关论文
共 79 条
[1]
Ce-emerin and LEM-2: essential roles in Caenorhabditis elegans development, muscle function, and mitosis [J].
Barkan, Rachel ;
Zahand, Adam J. ;
Sharabi, Kfir ;
Lamm, Ayelet T. ;
Feinstein, Naomi ;
Haithcock, Erin ;
Wilson, Katherine L. ;
Liu, Jun ;
Gruenbaum, Yosef .
MOLECULAR BIOLOGY OF THE CELL, 2012, 23 (04) :543-552
[2]
Networking in the nucleus: a spotlight on LEM-domain proteins [J].
Barton, Lacy J. ;
Soshnev, Alexey A. ;
Geyer, Pamela K. .
CURRENT OPINION IN CELL BIOLOGY, 2015, 34 :1-8
[3]
Unique and Shared Functions of Nuclear Lamina LEM Domain Proteins in Drosophila [J].
Barton, Lacy J. ;
Wilmington, Shameika R. ;
Martin, Melinda J. ;
Skopec, Hannah M. ;
Lovander, Kay Lee E. ;
Pinto, Belinda S. ;
Geyer, Pamela K. .
GENETICS, 2014, 197 (02) :653-U338
[4]
The Drosophila Nuclear Lamina Protein Otefin Is Required for Germline Stem Cell Survival [J].
Barton, Lacy J. ;
Pinto, Belinda S. ;
Wallrath, Lori L. ;
Geyer, Pamela K. .
DEVELOPMENTAL CELL, 2013, 25 (06) :645-654
[5]
The role of the Suppressor of Hairy-wing insulator protein in Drosophila oogenesis [J].
Baxley, Ryan M. ;
Soshnev, Alexey A. ;
Koryakov, Dmitry E. ;
Zhimulev, Igor F. ;
Geyer, Pamela K. .
DEVELOPMENTAL BIOLOGY, 2011, 356 (02) :398-410
[6]
The molecular basis of emerin-emerin and emerin-BAF interactions [J].
Berk, Jason M. ;
Simon, Dan N. ;
Jenkins-Houk, Clifton R. ;
Westerbeck, Jason W. ;
Gronning-Wang, Line M. ;
Carlson, Cathrine R. ;
Wilson, Katherine L. .
JOURNAL OF CELL SCIENCE, 2014, 127 (18) :3956-3969
[7]
The nuclear envelope LEM-domain protein emerin [J].
Berk, Jason M. ;
Tifft, Kathryn E. ;
Wilson, Katherine L. .
NUCLEUS, 2013, 4 (04) :298-314
[8]
Reversible regulation of stem cell niche size associated with dietary control of Notch signalling [J].
Bonfini, Alessandro ;
Wilkin, Marian B. ;
Baron, Martin .
BMC DEVELOPMENTAL BIOLOGY, 2015, 15
[9]
Decline in self-renewal factors contributes to aging of the stem cell niche in the Drosophila testis [J].
Boyle, Monica ;
Wong, Chihunt ;
Rocha, Michael ;
Jones, D. Leanne .
CELL STEM CELL, 2007, 1 (04) :470-478
[10]
The endonuclease Ankle1 requires its LEM and GIY-YIG motifs for DNA cleavage in vivo [J].
Brachner, Andreas ;
Braun, Juliane ;
Ghodgaonkar, Medini ;
Castor, Dennis ;
Zlopasa, Livija ;
Ehrlich, Veronika ;
Jiricny, Josef ;
Gotzmann, Josef ;
Knasmueller, Siegfried ;
Foisner, Roland .
JOURNAL OF CELL SCIENCE, 2012, 125 (04) :1048-1057