The Role of Peripherin-2/ROM1 Complexes in Photoreceptor Outer Segment Disc Morphogenesis.
Disc
Disc Enclosure
Disc Rim
Outer Segment
PRPH2
Peripherin-2
Photoreceptor
RDS
ROM1
Retina
Journal
Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103
Informations de publication
Date de publication:
2023
2023
Historique:
medline:
17
7
2023
pubmed:
13
7
2023
entrez:
13
7
2023
Statut:
ppublish
Résumé
The light-sensitive outer segment organelle of photoreceptor cells contains a stack of hundreds of flat, disc-shaped membranes called discs. The rims of these discs contain a photoreceptor-specific tetraspanin protein peripherin-2 (also known as rds or PRPH2). Mutations in the PRPH2 gene lead to a wide variety of inherited retinal degenerations in humans. The vast majority of these mutations occur within a large, intradiscal loop of peripherin-2, known as the D2 loop. The D2 loop mediates well-established intermolecular interactions of peripherin-2 molecules among themselves and a homologous protein ROM1. These interactions lead to the formation of large, highly ordered oligomers. In this chapter, we discuss the supramolecular organization of peripherin-2/ROM1 complexes and their contribution to the process of outer segment disc morphogenesis and enclosure.
Identifiants
pubmed: 37440045
doi: 10.1007/978-3-031-27681-1_40
doi:
Substances chimiques
Peripherins
0
Tetraspanins
0
Eye Proteins
0
ROM1 protein, human
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
277-281Subventions
Organisme : NEI NIH HHS
ID : K99 EY033763
Pays : United States
Organisme : NEI NIH HHS
ID : P30 EY005722
Pays : United States
Organisme : NEI NIH HHS
ID : R01 EY012859
Pays : United States
Organisme : NEI NIH HHS
ID : R01 EY030451
Pays : United States
Informations de copyright
© 2023. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Connell GJ, Molday RS. Molecular cloning, primary structure, and orientation of the vertebrate photoreceptor cell protein peripherin in the rod outer segment disk membrane. Biochemistry. 1990;29(19):4691–8.
doi: 10.1021/bi00471a025
pubmed: 2372552
Travis GH, Sutcliffe JG, Bok D. The retinal degeneration slow (rds) gene product is a photoreceptor disc membrane-associated glycoprotein. Neuron. 1991;6(1):61–70.
doi: 10.1016/0896-6273(91)90122-G
pubmed: 1986774
Bascom RA, Manara S, Collins L, Molday RS, Kalnins VI, McInnes RR. Cloning of the cDNA for a novel photoreceptor membrane protein (rom-1) identifies a disk rim protein family implicated in human retinopathies. Neuron. 1992;8(6):1171–84.
doi: 10.1016/0896-6273(92)90137-3
pubmed: 1610568
Moritz OL, Molday RS. Molecular cloning, membrane topology, and localization of bovine rom-1 in rod and cone photoreceptor cells. Invest Ophthalmol Vis Sci. 1996;37(2):352–62.
pubmed: 8603840
Kajiwara K, Hahn LB, Mukai S, Travis GH, Berson EL, Dryja TP. Mutations in the human retinal degeneration slow gene in autosomal dominant retinitis pigmentosa. Nature. 1991;354(6353):480–3.
doi: 10.1038/354480a0
pubmed: 1684223
Peeters M, Khan M, Rooijakkers A, Mulders T, Haer-Wigman L, Boon CJF, et al. PRPH2 mutation update: in silico assessment of 245 reported and 7 novel variants in patients with retinal disease. Hum Mutat. 2021.
Wang X, Wang H, Sun V, Tuan HF, Keser V, Wang K, et al. Comprehensive molecular diagnosis of 179 Leber congenital amaurosis and juvenile retinitis pigmentosa patients by targeted next generation sequencing. J Med Genet. 2013;50(10):674–88.
doi: 10.1136/jmedgenet-2013-101558
pubmed: 23847139
Khan AO, Al Rashaed S, Neuhaus C, Bergmann C, Bolz HJ. Peripherin mutations cause a distinct form of recessive Leber congenital amaurosis and dominant phenotypes in asymptomatic parents heterozygous for the mutation. Br J Ophthalmol. 2016;100(2):209–15.
doi: 10.1136/bjophthalmol-2015-306844
pubmed: 26061163
Kajiwara K, Berson EL, Dryja TP. Digenic retinitis pigmentosa due to mutations at the unlinked peripherin/RDS and ROM1 loci. Science. 1994;264(5165):1604–8.
doi: 10.1126/science.8202715
pubmed: 8202715
Dryja TP, Hahn LB, Kajiwara K, Berson EL. Dominant and digenic mutations in the peripherin/RDS and ROM1 genes in retinitis pigmentosa. Invest Ophthalmol Vis Sci. 1997;38(10):1972–82.
pubmed: 9331261
Bascom RA, Liu L, Heckenlively JR, Stone EM, McInnes RR. Mutation analysis of the ROM1 gene in retinitis pigmentosa. Hum Mol Genet. 1995;4(10):1895–902.
doi: 10.1093/hmg/4.10.1895
pubmed: 8595413
Sakuma H, Inana G, Murakami A, Yajima T, Weleber RG, Murphey WH, et al. A heterozygous putative null mutation in ROM1 without a mutation in peripherin/RDS in a family with retinitis pigmentosa. Genomics. 1995;27(2):384–6.
doi: 10.1006/geno.1995.1066
pubmed: 7558016
Reig C, Martinez-Gimeno M, Carballo M. A heterozygous novel C253Y mutation in the highly conserved cysteine residues of ROM1 gene is the cause of retinitis pigmentosa in a Spanish family? Hum Mutat. 2000;16(3):278.
doi: 10.1002/1098-1004(200009)16:3<278::AID-HUMU29>3.0.CO;2-G
pubmed: 10980553
Goldberg AF, Loewen CJ, Molday RS. Cysteine residues of photoreceptor peripherin/rds: role in subunit assembly and autosomal dominant retinitis pigmentosa. Biochemistry. 1998;37(2):680–5.
doi: 10.1021/bi972036i
pubmed: 9425091
Kedzierski W, Weng J, Travis GH. Analysis of the rds/peripherin.rom1 complex in transgenic photoreceptors that express a chimeric protein. J Biol Chem. 1999;274(41):29181–7.
doi: 10.1074/jbc.274.41.29181
pubmed: 10506174
Ding XQ, Stricker HM, Naash MI. Role of the second intradiscal loop of peripherin/rds in homo and hetero associations. Biochemistry. 2005;44(12):4897–904.
doi: 10.1021/bi048414i
pubmed: 15779916
Goldberg AF, Molday RS. Subunit composition of the peripherin/rds-rom-1 disk rim complex from rod photoreceptors: hydrodynamic evidence for a tetrameric quaternary structure. Biochemistry. 1996;35(19):6144–9.
doi: 10.1021/bi960259n
pubmed: 8634257
Goldberg AF, Moritz OL, Molday RS. Heterologous expression of photoreceptor peripherin/rds and Rom-1 in COS-1 cells: assembly, interactions, and localization of multisubunit complexes. Biochemistry. 1995;34(43):14213–9.
doi: 10.1021/bi00043a028
pubmed: 7578020
Goldberg AF, Molday RS. Defective subunit assembly underlies a digenic form of retinitis pigmentosa linked to mutations in peripherin/rds and rom-1. Proc Natl Acad Sci U S A. 1996;93(24):13726–30.
doi: 10.1073/pnas.93.24.13726
pubmed: 8943002
pmcid: 19405
Loewen CJ, Molday RS. Disulfide-mediated oligomerization of Peripherin/Rds and Rom-1 in photoreceptor disk membranes. Implications for photoreceptor outer segment morphogenesis and degeneration. J Biol Chem. 2000;275(8):5370–8.
doi: 10.1074/jbc.275.8.5370
pubmed: 10681511
Chakraborty D, Ding XQ, Conley SM, Fliesler SJ, Naash MI. Differential requirements for retinal degeneration slow intermolecular disulfide-linked oligomerization in rods versus cones. Hum Mol Genet. 2009;18(5):797–808.
doi: 10.1093/hmg/ddn406
pubmed: 19050038
Zulliger R, Conley SM, Mwoyosvi ML, Al-Ubaidi MR, Naash MI. Oligomerization of Prph2 and Rom1 is essential for photoreceptor outer segment formation. Hum Mol Genet. 2018;27(20):3507–18.
doi: 10.1093/hmg/ddy240
pubmed: 29961824
pmcid: 6168975
Cohen AI. Some cytological and initial biochemical observations on photoreceptors in retinas of rds mice. Invest Ophthalmol Vis Sci. 1983;24(7):832–43.
pubmed: 6862791
Jansen HG, Sanyal S. Development and degeneration of retina in rds mutant mice: electron microscopy. J Comp Neurol. 1984;224(1):71–84.
doi: 10.1002/cne.902240107
pubmed: 6715580
Nir I, Papermaster DS. Immunocytochemical localization of opsin in the inner segment and ciliary plasma membrane of photoreceptors in retinas of rds mutant mice. Invest Ophthalmol Vis Sci. 1986;27(5):836–40.
pubmed: 2939037
Usukura J, Bok D. Changes in the localization and content of opsin during retinal development in the rds mutant mouse: immunocytochemistry and immunoassay. Exp Eye Res. 1987;45(4):501–15.
doi: 10.1016/S0014-4835(87)80061-1
pubmed: 2962880
Salinas RY, Pearring JN, Ding JD, Spencer WJ, Hao Y, Arshavsky VY. Photoreceptor discs form through peripherin-dependent suppression of ciliary ectosome release. J Cell Biol. 2017;216(5):1489–99.
doi: 10.1083/jcb.201608081
pubmed: 28381413
pmcid: 5412563
Wood CR, Huang K, Diener DR, Rosenbaum JL. The cilium secretes bioactive ectosomes. Curr Biol. 2013;23(10):906–11.
doi: 10.1016/j.cub.2013.04.019
pubmed: 23623554
Spencer WJ, Lewis TR, Pearring JN, Arshavsky VY. Photoreceptor discs: built like Ectosomes. Trends Cell Biol. 2020;30(11):904–15.
doi: 10.1016/j.tcb.2020.08.005
pubmed: 32900570
pmcid: 7584774
Arikawa K, Molday LL, Molday RS, Williams DS. Localization of peripherin/rds in the disk membranes of cone and rod photoreceptors: relationship to disk membrane morphogenesis and retinal degeneration. J Cell Biol. 1992;116(3):659–67.
doi: 10.1083/jcb.116.3.659
pubmed: 1730772
Ding JD, Salinas RY, Arshavsky VY. Discs of mammalian rod photoreceptors form through the membrane evagination mechanism. J Cell Biol. 2015;211(3):495–502.
doi: 10.1083/jcb.201508093
pubmed: 26527746
pmcid: 4639867
Kevany BM, Tsybovsky Y, Campuzano ID, Schnier PD, Engel A, Palczewski K. Structural and functional analysis of the native peripherin-ROM1 complex isolated from photoreceptor cells. J Biol Chem. 2013;288(51):36272–84.
doi: 10.1074/jbc.M113.520700
pubmed: 24196967
pmcid: 3868743
Milstein ML, Cavanaugh BL, Roussey NM, Volland S, Williams DS, Goldberg AFX. Multistep peripherin-2/rds self-assembly drives membrane curvature for outer segment disk architecture and photoreceptor viability. Proc Natl Acad Sci U S A. 2020;117(8):4400–10.
doi: 10.1073/pnas.1912513117
pubmed: 32041874
pmcid: 7049111
Milstein ML, Kimler VA, Ghatak C, Ladokhin AS, Goldberg AFX. An inducible amphipathic helix within the intrinsically disordered C terminus can participate in membrane curvature generation by peripherin-2/rds. J Biol Chem. 2017;292(19):7850–65.
doi: 10.1074/jbc.M116.768143
pubmed: 28325841
pmcid: 5427266
Conley SM, Stuck MW, Watson JN, Zulliger R, Burnett JL, Naash MI. Prph2 initiates outer segment morphogenesis but maturation requires Prph2/Rom1 oligomerization. Hum Mol Genet. 2019;28(3):459–75.
pubmed: 30307502
Pöge M, Mahamid J, Imanishi SS, Plitzko JM, Palczewski K, Baumeister W. Determinants shaping the nanoscale architecture of the mouse rod outer segment. bioRxiv. 2021:2021.08.18.456753.
Lewis TR, Makia MS, Castillo CM, Al-Ubaidi MR, Naash MI, Arshavsky VY. Photoreceptor disc enclosure is tightly controlled by peripherin-2 oligomerization. J Neurosci. 2021;41(16):3588–96.
doi: 10.1523/JNEUROSCI.0041-21.2021
pubmed: 33707293
pmcid: 8055076
Lewis TR, Makia MS, Kakakhel M, Al-Ubaidi MR, Arshavsky VY, Naash MI. Photoreceptor disc enclosure occurs in the absence of normal peripherin-2/rds oligomerization. Front Cell Neurosci. 2020;14:92.
doi: 10.3389/fncel.2020.00092
pubmed: 32410962
pmcid: 7198881
Stuck MW, Conley SM, Naash MI. PRPH2/RDS and ROM-1: historical context, current views and future considerations. Prog Retin Eye Res. 2016;52:47–63.
doi: 10.1016/j.preteyeres.2015.12.002
pubmed: 26773759
pmcid: 4842342
Tebbe L, Kakakhel M, Makia MS, Al-Ubaidi MR, Naash MI. The interplay between peripherin 2 complex formation and degenerative retinal diseases. Cell. 2020;9(3).