Photoreceptor discs form through peripherin-dependent suppression of ciliary ectosome release

被引:95
作者
Salinas, Raquel Y. [1 ,2 ]
Pearring, Jillian N. [1 ]
Ding, Jin-Dong [1 ]
Spencer, William J. [1 ,2 ]
Hao, Ying [1 ]
Arshavsky, Vadim Y. [1 ,2 ]
机构
[1] Duke Univ, Dept Ophthalmol, Durham, NC 27710 USA
[2] Duke Univ, Dept Pharmacol, Durham, NC 27710 USA
基金
美国国家卫生研究院;
关键词
RDS MUTANT MICE; DEGENERATION SLOW RDS; ROD OUTER SEGMENTS; RETINAL DEGENERATION; MEMBRANE CURVATURE; XENOPUS-LAEVIS; IN-VIVO; PROTEIN; MORPHOGENESIS; CELLS;
D O I
10.1083/jcb.201608081
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
The primary cilium is a highly conserved organelle housing specialized molecules responsible for receiving and processing extracellular signals. A recently discovered property shared across many cilia is the ability to release small vesicles called ectosomes, which are used for exchanging protein and genetic material among cells. In this study, we report a novel role for ciliary ectosomes in building the elaborate photoreceptor outer segment filled with hundreds of tightly packed "disc" membranes. We demonstrate that the photoreceptor cilium has an innate ability to release massive amounts of ectosomes. However, this process is suppressed by the disc-specific protein peripherin, which enables retained ectosomes to be morphed into discs. This new function of peripherin is performed independently from its well-established role in maintaining the high curvature of disc edges, and each function is fulfilled by a separate part of peripherin's molecule. Our findings explain how the outer segment structure evolved from the primary cilium to provide photoreceptor cells with vast membrane surfaces for efficient light capture.
引用
收藏
页码:1489 / 1499
页数:11
相关论文
共 54 条
[1]   Photoreceptor Signaling: Supporting Vision across a Wide Range of Light Intensities [J].
Arshavsky, Vadim Y. ;
Burns, Marie E. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2012, 287 (03) :1620-1626
[2]  
Boesze-Battaglia K, 2002, INT REV CYTOL, V217, P183
[3]   Rod disc renewal occurs by evagination of the ciliary plasma membrane that makes cadherin-based contacts with the inner segment [J].
Burgoyne, Thomas ;
Meschede, Ingrid P. ;
Burden, Jemima J. ;
Bailly, Maryse ;
Seabra, Miguel C. ;
Futter, Clare E. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2015, 112 (52) :15922-15927
[4]   Uni-directional ciliary membrane protein trafficking by a cytoplasmic retrograde IFT motor and ciliary ectosome shedding [J].
Cao, Muqing ;
Ning, Jue ;
Hernandez-Lara, Carmen I. ;
Belzile, Olivier ;
Wang, Qian ;
Dutcher, Susan K. ;
Liu, Yanjie ;
Snell, William J. .
ELIFE, 2015, 4
[5]   SARA-regulated vesicular targeting underlies formation of the Light-Sensing organelle in mammalian rods [J].
Chuang, Jen-Zen ;
Zhao, Yu ;
Sung, Ching-Hwa .
CELL, 2007, 130 (03) :535-547
[6]   Ectosomes [J].
Cocucci, Emanulele ;
Meldolesi, Jacopo .
CURRENT BIOLOGY, 2011, 21 (23) :R940-R941
[7]  
COHEN AI, 1983, INVEST OPHTH VIS SCI, V24, P832
[8]   PHOTORECEPTOR PERIPHERIN IS THE NORMAL PRODUCT OF THE GENE RESPONSIBLE FOR RETINAL DEGENERATION IN THE RDS MOUSE [J].
CONNELL, G ;
BASCOM, R ;
MOLDAY, L ;
REID, D ;
MCINNES, RR ;
MOLDAY, RS .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1991, 88 (03) :723-726
[9]   Discs of mammalian rod photoreceptors form through the membrane evagination mechanism [J].
Ding, Jin-Dong ;
Salinas, Raquel Y. ;
Arshavsky, Vadim Y. .
JOURNAL OF CELL BIOLOGY, 2015, 211 (03) :495-502
[10]   Untangling ciliary access and enrichment of two rhodopsin-like receptors using quantitative fluorescence microscopy reveals cell-specific sorting pathways [J].
Geneva, Ivayla I. ;
Tan, Han Yen ;
Calvert, Peter D. .
MOLECULAR BIOLOGY OF THE CELL, 2017, 28 (04) :554-566