Rod genesis driven by mafba in an nrl knockout zebrafish model with altered photoreceptor composition and progressive retinal degeneration.

Animals Basic-Leucine Zipper Transcription Factors / genetics Eye Proteins / metabolism Mammals / metabolism Retinal Cone Photoreceptor Cells / metabolism Retinal Degeneration / genetics Zebrafish / genetics

Journal

PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074

Informations de publication

Date de publication:
03 2022
Historique:
received: 22 09 2021
accepted: 17 02 2022
revised: 16 03 2022
pubmed: 5 3 2022
medline: 28 4 2022
entrez: 4 3 2022
Statut: epublish

Résumé

Neural retina leucine zipper (NRL) is an essential gene for the fate determination and differentiation of the precursor cells into rod photoreceptors in mammals. Mutations in NRL are associated with the autosomal recessive enhanced S-cone syndrome and autosomal dominant retinitis pigmentosa. However, the exact role of Nrl in regulating the development and maintenance of photoreceptors in the zebrafish (Danio rerio), a popular animal model used for retinal degeneration and regeneration studies, has not been fully determined. In this study, we generated an nrl knockout zebrafish model via the CRISPR-Cas9 technology and observed a surprising phenotype characterized by a reduced number, but not the total loss, of rods and over-growth of green cones. We discovered two waves of rod genesis, nrl-dependent and -independent at the embryonic and post-embryonic stages, respectively, in zebrafish by monitoring the rod development. Through bulk and single-cell RNA sequencing, we characterized the gene expression profiles of the whole retina and each retinal cell type from the wild type and nrl knockout zebrafish. The over-growth of green cones and mis-expression of green-cone-specific genes in rods in nrl mutants suggested that there are rod/green-cone bipotent precursors, whose fate choice between rod versus green-cone is controlled by nrl. Besides, we identified the mafba gene as a novel regulator of the nrl-independent rod development, based on the cell-type-specific expression patterns and the retinal phenotype of nrl/mafba double-knockout zebrafish. Gene collinearity analysis revealed the evolutionary origin of mafba and suggested that the function of mafba in rod development is specific to modern fishes. Furthermore, the altered photoreceptor composition and abnormal gene expression in nrl mutants caused progressive retinal degeneration and subsequent regeneration. Accordingly, this study revealed a novel function of the mafba gene in rod development and established a working model for the developmental and regulatory mechanisms regarding the rod and green-cone photoreceptors in zebrafish.

Identifiants

DOI: 10.1371/journal.pgen.1009841 PMID: 35245286 PMC: PMC8926279
pubmed: 35245286
doi: 10.1371/journal.pgen.1009841
pii: PGENETICS-D-21-01260
pmc: PMC8926279
doi:

Substances chimiques

Basic-Leucine Zipper Transcription Factors 0
Eye Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1009841

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

PLoS Biol. 2019 Jul 3;17(7):e3000365
pubmed: 31269016
PLoS Genet. 2012;8(4):e1002649
pubmed: 22511886
Curr Opin Chem Biol. 2019 Jun;50:37-44
pubmed: 30928773
Annu Rev Vis Sci. 2015 Nov 24;1:211-234
pubmed: 28532380
Proc Natl Acad Sci U S A. 2004 Dec 21;101(51):17819-24
pubmed: 15591106
J Biol Chem. 2011 Oct 7;286(40):34893-902
pubmed: 21849497
Cell Rep. 2020 Jan 21;30(3):658-671.e5
pubmed: 31968244
Dev Neurobiol. 2008 Apr;68(5):605-19
pubmed: 18265406
Hum Mol Genet. 2004 Aug 1;13(15):1563-75
pubmed: 15190009
Nat Genet. 2001 Dec;29(4):447-52
pubmed: 11694879
J Biol Chem. 2004 May 7;279(19):19800-7
pubmed: 15001570
Development. 1996 Dec;122(12):3981-90
pubmed: 9012518
Annu Rev Vis Sci. 2015 Nov 24;1:125-153
pubmed: 28532376
Cell. 2015 May 21;161(5):1202-1214
pubmed: 26000488
PLoS Genet. 2005 Aug;1(2):e11
pubmed: 16110338
Curr Eye Res. 2020 Mar;45(3):385-396
pubmed: 31794277
Epigenetics Chromatin. 2019 Dec 12;12(1):73
pubmed: 31831052
Proc Natl Acad Sci U S A. 2006 Mar 7;103(10):3890-5
pubmed: 16505381
Trends Genet. 2016 Oct;32(10):638-659
pubmed: 27615122
Prog Retin Eye Res. 2013 Sep;36:52-119
pubmed: 23792002
Genes Dev. 2015 Aug 1;29(15):1618-30
pubmed: 26253536
Prog Retin Eye Res. 2018 Jan;62:24-37
pubmed: 28962928
Development. 2020 Jun 19;147(12):
pubmed: 32467236
Invest Ophthalmol Vis Sci. 2016 Oct 01;57(13):5361-5371
pubmed: 27732723
iScience. 2020 Nov 15;23(12):101805
pubmed: 33299975
J Biol Chem. 2000 Sep 22;275(38):29794-9
pubmed: 10887186
Hum Mol Genet. 2006 Sep 1;15(17):2588-602
pubmed: 16868010
J Comp Neurol. 2015 Mar 1;523(4):649-68
pubmed: 25349106
J Neurosci. 2007 Jun 27;27(26):7028-40
pubmed: 17596452
Int J Mol Sci. 2017 Jun 02;18(6):
pubmed: 28574477
Cell. 2015 May 7;161(4):817-32
pubmed: 25957687
Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1679-84
pubmed: 17242361
Proc Natl Acad Sci U S A. 2000 May 9;97(10):5551-6
pubmed: 10805811
Dev Cell. 2016 Jun 20;37(6):520-32
pubmed: 27326930
Brain Res. 2008 Oct 21;1236:16-29
pubmed: 18294621
Cell. 2019 Feb 21;176(5):1222-1237.e22
pubmed: 30712875
Biochim Biophys Acta Mol Basis Dis. 2019 Jun 1;1865(6):1273-1283
pubmed: 30684641
Blood. 2019 Feb 21;133(8):805-815
pubmed: 30482793
Nat Biotechnol. 2018 Jun;36(5):411-420
pubmed: 29608179
Genes (Basel). 2018 Jan 30;9(2):
pubmed: 29385733
Hum Mol Genet. 2014 Aug 15;23(16):4260-71
pubmed: 24691551
Invest Ophthalmol Vis Sci. 2005 Jun;46(6):2156-67
pubmed: 15914637
Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12630-5
pubmed: 14555765
Biochim Biophys Acta Mol Basis Dis. 2019 Oct 1;1865(10):2694-2705
pubmed: 31348989
Hum Mol Genet. 2015 Aug 15;24(16):4648-59
pubmed: 26034134
Front Cell Dev Biol. 2018 Sep 19;6:110
pubmed: 30283779
Clin Ophthalmol. 2020 Mar 05;14:707-719
pubmed: 32184557
PLoS One. 2012;7(3):e32484
pubmed: 22427845
Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):191-5
pubmed: 8552602
Dev Biol. 2017 Nov 1;431(1):26-35
pubmed: 28882401
Dev Dyn. 2008 Oct;237(10):2903-17
pubmed: 18816851
Toxicol Sci. 2014 Jun;139(2):381-95
pubmed: 24675095
Prog Retin Eye Res. 2001 Jan;20(1):49-94
pubmed: 11070368
J Neurosci. 2012 Jan 11;32(2):528-41
pubmed: 22238088
Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):473-8
pubmed: 11773633
Dev Genes Evol. 2005 Jul;215(7):327-39
pubmed: 15759153
Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):266-70
pubmed: 1729696
Brain Res. 2008 Feb 4;1192:134-50
pubmed: 17466954
PLoS Genet. 2019 Jan 29;15(1):e1007939
pubmed: 30695061
Hum Mol Genet. 2001 Aug 1;10(16):1619-26
pubmed: 11487564
Proc Natl Acad Sci U S A. 2020 Feb 4;117(5):2710-2716
pubmed: 31964843
Nat Rev Neurosci. 2020 Jan;21(1):5-20
pubmed: 31780820
Cell Death Differ. 2010 Jul;17(7):1199-210
pubmed: 20139892
Cell. 2015 May 7;161(4):706-8
pubmed: 25957678
Curr Opin Genet Dev. 2016 Oct;40:41-47
pubmed: 27281280
Hum Mol Genet. 2016 Apr 1;25(7):1345-56
pubmed: 26908598
Methods Mol Biol. 2013;935:215-26
pubmed: 23150371

Auteurs

Fei Liu (F)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.
State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, P.R. China.
University of Chinese Academy of Sciences, Beijing, China.
ORCID: 0000-0002-0310-1072

Yayun Qin (Y)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.
Maternal and Child Health Hospital of Hubei Province, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, P.R. China.

Yuwen Huang (Y)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.

Pan Gao (P)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.
ORCID: 0000-0003-3366-2118

Jingzhen Li (J)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.
ORCID: 0000-0003-2974-6677

Shanshan Yu (S)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.
ORCID: 0000-0002-8748-5877

Danna Jia (D)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.
ORCID: 0000-0002-2717-628X

Xiang Chen (X)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.

Yuexia Lv (Y)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.
ORCID: 0000-0003-1588-2547

Jiayi Tu (J)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.

Kui Sun (K)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.
ORCID: 0000-0002-2487-4779

Yunqiao Han (Y)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.
ORCID: 0000-0002-1369-4262

James Reilly (J)

Department of Biological and Biomedical Sciences, Glasgow Caledonian University, Glasgow, United Kingdom.

Xinhua Shu (X)

Department of Biological and Biomedical Sciences, Glasgow Caledonian University, Glasgow, United Kingdom.

Qunwei Lu (Q)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.
ORCID: 0000-0003-4390-052X

Zhaohui Tang (Z)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.

Chengqi Xu (C)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.

Daji Luo (D)

State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, P.R. China.
University of Chinese Academy of Sciences, Beijing, China.
ORCID: 0000-0002-8051-9624

Mugen Liu (M)

Key Laboratory of Molecular Biophysics of Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, P.R. China.
ORCID: 0000-0001-5076-8438

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Rod genesis driven by mafba in an nrl knockout...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Facteurs de transcription à motif basique et à glissière à leucines › Rod genesis driven by mafba in an nrl knockout...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines de l'oeil › Rod genesis driven by mafba in an nrl knockout...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Rod genesis driven by mafba in an nrl knockout...
questionsmedicales.fr › Cellules › Neurones › Neurones afférents › Cellules réceptrices sensorielles › Cellules photoréceptrices › Cellules photoréceptrices de vertébré › Cellules photoréceptrices en cône de la rétine › Rod genesis driven by mafba in an nrl knockout...
questionsmedicales.fr › Maladies de l'oeil › Rétinopathies › Dégénérescence de la rétine › Rod genesis driven by mafba in an nrl knockout...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Poissons › Cypriniformes › Cyprinidae › Danio zébré › Rod genesis driven by mafba in an nrl knockout...