Literature DB >> 31362982

Deletion of the transmembrane protein Prom1b in zebrafish disrupts outer-segment morphogenesis and causes photoreceptor degeneration.

Zhaojing Lu1, Xuebin Hu1,2, James Reilly3, Danna Jia1, Fei Liu1, Shanshan Yu1, Xiliang Liu1, Shanglun Xie1, Zhen Qu1, Yayun Qin1, Yuwen Huang1, Yuexia Lv1, Jingzhen Li1, Pan Gao1, Fulton Wong4, Xinhua Shu3, Zhaohui Tang5, Mugen Liu6.   

Abstract

Mutations in human prominin 1 (PROM1), encoding a transmembrane glycoprotein localized mainly to plasma membrane protrusions, have been reported to cause retinitis pigmentosa, macular degeneration, and cone-rod dystrophy. Although the structural role of PROM1 in outer-segment (OS) morphogenesis has been demonstrated in Prom1-knockout mouse, the mechanisms underlying these complex disease phenotypes remain unclear. Here, we utilized a zebrafish model to further investigate PROM1's role in the retina. The Prom1 orthologs in zebrafish include prom1a and prom1b, and our results showed that prom1b, rather than prom1a, plays an important role in zebrafish photoreceptors. Loss of prom1b disrupted OS morphogenesis, with rods and cones exhibiting differences in impairment: cones degenerated at an early age, whereas rods remained viable but with an abnormal OS, even at 9 months postfertilization. Immunofluorescence experiments with WT zebrafish revealed that Prph2, an ortholog of the human transmembrane protein peripherin 2 and also associated with OS formation, is localized to the edge of OS and is more highly expressed in the cone OS than in the rod OS. Moreover, we found that Prom1b deletion causes mislocalization of Prph2 and disrupts its oligomerization. We conclude that the variation in Prph2 levels between cones and rods was one of the reasons for the different PROM1 mutation-induced phenotypes of these retinal structures. These findings expand our understanding of the phenotypes caused by PROM1 mutations and provide critical insights into its function.
© 2019 Lu et al.

Entities:  

Keywords:  Danio rerio; development; eye disease; morphogenesis; peripherin 2 (PRPH2); photoreceptor; prominin 1 (PROM1); retinal degeneration; zebrafish

Mesh:

Substances:

Year:  2019        PMID: 31362982      PMCID: PMC6755801          DOI: 10.1074/jbc.RA119.008618

Source DB:  PubMed          Journal:  J Biol Chem        ISSN: 0021-9258            Impact factor:   5.157


  50 in total

Review 1.  Focus on molecules: prominin-1 (CD133).

Authors:  József Jászai; Christine A Fargeas; Mareike Florek; Wieland B Huttner; Denis Corbeil
Journal:  Exp Eye Res       Date:  2006-06-02       Impact factor: 3.467

2.  A novel tetraspanin fusion protein, peripherin-2, requires a region upstream of the fusion domain for activity.

Authors:  Monika Damek-Poprawa; Jennifer Krouse; Cheryl Gretzula; Kathleen Boesze-Battaglia
Journal:  J Biol Chem       Date:  2004-12-09       Impact factor: 5.157

3.  A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration.

Authors:  M A Maw; D Corbeil; J Koch; A Hellwig; J C Wilson-Wheeler; R J Bridges; G Kumaramanickavel; S John; D Nancarrow; K Röper; A Weigmann; W B Huttner; M J Denton
Journal:  Hum Mol Genet       Date:  2000-01-01       Impact factor: 6.150

4.  Myosin 3A transgene expression produces abnormal actin filament bundles in transgenic Xenopus laevis rod photoreceptors.

Authors:  Jennifer Lin-Jones; Ed Parker; Mike Wu; Andréa Dosé; Beth Burnside
Journal:  J Cell Sci       Date:  2004-11-02       Impact factor: 5.285

5.  Identification of novel Prominin-1/CD133 splice variants with alternative C-termini and their expression in epididymis and testis.

Authors:  Christine A Fargeas; Angret Joester; Ewa Missol-Kolka; Andrea Hellwig; Wieland B Huttner; Denis Corbeil
Journal:  J Cell Sci       Date:  2004-08-15       Impact factor: 5.285

6.  Outer segment oligomerization of Rds: evidence from mouse models and subcellular fractionation.

Authors:  Dibyendu Chakraborty; Xi-Qin Ding; Steven J Fliesler; Muna I Naash
Journal:  Biochemistry       Date:  2008-01-03       Impact factor: 3.162

7.  Inhibition of the ATP-driven proton pump in RPE lysosomes by the major lipofuscin fluorophore A2-E may contribute to the pathogenesis of age-related macular degeneration.

Authors:  M Bergmann; F Schütt; F G Holz; J Kopitz
Journal:  FASEB J       Date:  2004-01-08       Impact factor: 5.191

Review 8.  The spectrum of retinal dystrophies caused by mutations in the peripherin/RDS gene.

Authors:  Camiel J F Boon; Anneke I den Hollander; Carel B Hoyng; Frans P M Cremers; B Jeroen Klevering; Jan E E Keunen
Journal:  Prog Retin Eye Res       Date:  2008-01-26       Impact factor: 21.198

9.  Severe retinitis pigmentosa mapped to 4p15 and associated with a novel mutation in the PROM1 gene.

Authors:  Qingjiong Zhang; Fareeha Zulfiqar; Xueshan Xiao; S Amer Riazuddin; Zahoor Ahmad; Raphael Caruso; Ian MacDonald; Paul Sieving; Sheikh Riazuddin; J Fielding Hejtmancik
Journal:  Hum Genet       Date:  2007-06-29       Impact factor: 4.132

10.  Expression of the "stem cell marker" CD133 in pancreas and pancreatic ductal adenocarcinomas.

Authors:  Heike Immervoll; Dag Hoem; Per Øystein Sakariassen; Ole Johnny Steffensen; Anders Molven
Journal:  BMC Cancer       Date:  2008-02-08       Impact factor: 4.430

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  11 in total

1.  Photoreceptor disc enclosure is tightly controlled by peripherin-2 oligomerization.

Authors:  Tylor R Lewis; Mustafa S Makia; Carson M Castillo; Muayyad R Al-Ubaidi; Muna I Naash; Vadim Y Arshavsky
Journal:  J Neurosci       Date:  2021-03-11       Impact factor: 6.167

2.  Deciphering the roles of prominins in the visual system.

Authors:  Denis Corbeil; Christine A Fargeas; József Jászai
Journal:  J Biol Chem       Date:  2019-11-08       Impact factor: 5.157

3.  Reply to Corbeil et al.: Deletion of the transmembrane protein Prom1b in zebrafish disrupts outer-segment morphogenesis and causes photoreceptor degeneration.

Authors:  Zhaojing Lu; Xuebin Hu; James Reilly; Danna Jia; Fei Liu; Shanshan Yu; Xiliang Liu; Shanglun Xie; Zhen Qu; Yayun Qin; Yuwen Huang; Yuexia Lv; Jingzhen Li; Pan Gao; Fulton Wong; Xinhua Shu; Zhaohui Tang; Mugen Liu
Journal:  J Biol Chem       Date:  2019-11-08       Impact factor: 5.157

4.  Specialization of the photoreceptor transcriptome by Srrm3-dependent microexons is required for outer segment maintenance and vision.

Authors:  Ludovica Ciampi; Federica Mantica; Laura López-Blanch; Jon Permanyer; Cristina Rodriguez-Marín; Jingjing Zang; Damiano Cianferoni; Senda Jiménez-Delgado; Sophie Bonnal; Samuel Miravet-Verde; Verena Ruprecht; Stephan C F Neuhauss; Sandro Banfi; Sabrina Carrella; Luis Serrano; Sarah A Head; Manuel Irimia
Journal:  Proc Natl Acad Sci U S A       Date:  2022-07-12       Impact factor: 12.779

5.  Prominins control ciliary length throughout the animal kingdom: New lessons from human prominin-1 and zebrafish prominin-3.

Authors:  József Jászai; Kristina Thamm; Jana Karbanová; Peggy Janich; Christine A Fargeas; Wieland B Huttner; Denis Corbeil
Journal:  J Biol Chem       Date:  2020-03-22       Impact factor: 5.157

6.  Whole exome sequencing analysis identifies novel Stargardt disease-related gene mutations in Chinese Stargardt disease and retinitis pigmentosa patients.

Authors:  Tsz Kin Ng; Yingjie Cao; Xiang-Ling Yuan; Shaowan Chen; Yanxuan Xu; Shao-Lang Chen; Yuqian Zheng; Haoyu Chen
Journal:  Eye (Lond)       Date:  2021-04-12       Impact factor: 3.775

Review 7.  Zebrafish Models of Photoreceptor Dysfunction and Degeneration.

Authors:  Nicole C L Noel; Ian M MacDonald; W Ted Allison
Journal:  Biomolecules       Date:  2021-01-09

8.  LIM Homeobox 9 knockdown by morpholino does not affect zebrafish retinal development.

Authors:  Rui Guo; Fei Li; Minxia Lu; Kangkang Ge; Lin Gan; Donglai Sheng
Journal:  Biol Open       Date:  2021-03-08       Impact factor: 2.422

9.  Exocyst-mediated membrane trafficking of the lissencephaly-associated ECM receptor dystroglycan is required for proper brain compartmentalization.

Authors:  Andriy S Yatsenko; Mariya M Kucherenko; Yuanbin Xie; Henning Urlaub; Halyna R Shcherbata
Journal:  Elife       Date:  2021-02-23       Impact factor: 8.140

10.  Electrophysiological and Pupillometric Abnormalities in PROM1 Cone-Rod Dystrophy.

Authors:  Jason C Park; Frederick T Collison; Gerald A Fishman; J Jason McAnany
Journal:  Transl Vis Sci Technol       Date:  2020-08-17       Impact factor: 3.283

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