Aipl1 is required for cone photoreceptor function and survival through the stability of Pde6c and Gc3 in zebrafish

被引:15
作者
Iribarne, Maria [1 ]
Nishiwaki, Yuko [1 ]
Nakamura, Shohei [1 ]
Araragi, Masato [1 ]
Oguri, Eri [1 ]
Masai, Ichiro [1 ]
机构
[1] Okinawa Inst Sci & Technol Grad Univ, 1919-1 Tancha, Okinawa 9040495, Japan
关键词
LEBER CONGENITAL AMAUROSIS; CELL-DEATH; NECROTIC CONE; MOUSE MODEL; ROD; PROTEIN; GENE; DEGENERATION; MUTATIONS; BLINDNESS;
D O I
10.1038/srep45962
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Genetic mutations in aryl hydrocarbon receptor interacting protein-like 1 (AIPL1) cause photoreceptor degeneration associated with Leber congenital amaurosis 4 (LCA4) in human patients. Here we report retinal phenotypes of a zebrafish aipl1 mutant, gold rush (gosh). In zebrafish, there are two aipl1 genes, aipl1a and aipl1b, which are expressed mainly in rods and cones, respectively. The gosh mutant gene encodes cone-specific aipl1, aipl1b. Cone photoreceptors undergo progressive degeneration in the gosh mutant, indicating that aipl1b is required for cone survival. Furthermore, the cone-specific subunit of cGMP phosphodiesterase 6 (Pde6c) is markedly decreased in the gosh mutant, and the gosh mutation genetically interacts with zebrafish pde6c mutation eclipse (els). These data suggest that Aipl1 is required for Pde6c stability and function. In addition to Pde6c, we found that zebrafish cone-specific guanylate cyclase, zGc3, is also decreased in the gosh and els mutants. Furthermore, zGc3 knockdown embryos showed a marked reduction in Pde6c. These observations illustrate the interdependence of cGMP metabolism regulators between Aipl1, Pde6c, and Gc3 in photoreceptors.
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页数:13
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共 41 条
[11]   Human Retinal Disease from AIPL1 Gene Mutations: Foveal Cone Loss with Minimal Macular Photoreceptors and Rod Function Remaining [J].
Jacobson, Samuel G. ;
Cideciyan, Artur V. ;
Aleman, Tomas S. ;
Sumaroka, Alexander ;
Roman, Alejandro J. ;
Swider, Malgorzata ;
Schwartz, Sharon B. ;
Banin, Eyal ;
Stone, Edwin M. .
INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE, 2011, 52 (01) :70-79
[12]   Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system [J].
Jao, Li-En ;
Wente, Susan R. ;
Chen, Wenbiao .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2013, 110 (34) :13904-13909
[13]   Nonsense-mediated mRNA decay: novel mechanistic insights and biological impact [J].
Karousis, Evangelos D. ;
Nasif, Sofia ;
Muhlemann, Oliver .
WILEY INTERDISCIPLINARY REVIEWS-RNA, 2016, 7 (05) :661-682
[14]   The Leber congenital amaurosis protein, AIPL1, is needed for the viability and functioning of cone photoreceptor cells [J].
Kirschman, Lindsay T. ;
Kolandaivelu, Saravanan ;
Frederick, Jeanne M. ;
Dang, Loan ;
Goldberg, Andrew F. X. ;
Baehr, Wolfgang ;
Ramamurthy, Visvanathan .
HUMAN MOLECULAR GENETICS, 2010, 19 (06) :1076-1087
[15]   AIPL1, A protein linked to blindness, is essential for the stability of enzymes mediating cGMP metabolism in cone photoreceptor cells [J].
Kolandaivelu, Saravanan ;
Singh, Ratnesh K. ;
Ramamurthy, Visvanathan .
HUMAN MOLECULAR GENETICS, 2014, 23 (04) :1002-1012
[16]   AIPL1, a Protein Associated with Childhood Blindness, Interacts with α-Subunit of Rod Phosphodiesterase (PDE6) and Is Essential for Its Proper Assembly [J].
Kolandaivelu, Saravanan ;
Huang, Jing ;
Hurley, James B. ;
Ramamurthy, Visvanathan .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2009, 284 (45) :30853-30861
[17]   Wild-Type Cone Photoreceptors Persist Despite Neighboring Mutant Cone Degeneration [J].
Lewis, Alaron ;
Williams, Philip ;
Lawrence, Owen ;
Wong, Rachel O. L. ;
Brockerhoff, Susan E. .
JOURNAL OF NEUROSCIENCE, 2010, 30 (01) :382-389
[18]   AIPL1, the protein that is defective in Leber congenital amaurosis, is essential for the biosynthesis of retinal rod cGMP phosphodiesterase [J].
Liu, XQ ;
Bulgakov, OV ;
Wen, XH ;
Woodruff, ML ;
Pawlyk, B ;
Yang, J ;
Fain, GL ;
Sandberg, MA ;
Makino, CL ;
Li, TS .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2004, 101 (38) :13903-13908
[19]   N-cadherin mediates retinal lamination, maintenance of forebrain compartments and patterning of retinal neurites [J].
Masai, I ;
Lele, Z ;
Yamaguchi, M ;
Komori, A ;
Nakata, A ;
Nishiwaki, Y ;
Wada, H ;
Tanaka, H ;
Nojima, Y ;
Hammerschmidt, M ;
Wilson, SW ;
Okamoto, H .
DEVELOPMENT, 2003, 130 (11) :2479-2494
[20]   Nrl is required for rod photoreceptor development [J].
Mears, AJ ;
Kondo, M ;
Swain, PK ;
Takada, Y ;
Bush, RA ;
Saunders, TL ;
Sieving, PA ;
Swaroop, A .
NATURE GENETICS, 2001, 29 (04) :447-452