The protective variant rs7173049 at LOXL1 locus impacts on retinoic acid signaling pathway in pseudoexfoliation syndrome.


Journal

Human molecular genetics
ISSN: 1460-2083
Titre abrégé: Hum Mol Genet
Pays: England
ID NLM: 9208958

Informations de publication

Date de publication:
01 08 2019
Historique:
received: 13 12 2018
revised: 29 03 2019
accepted: 01 04 2019
pubmed: 16 4 2019
medline: 1 9 2021
entrez: 16 4 2019
Statut: ppublish

Résumé

LOXL1 (lysyl oxidase-like 1) has been identified as the major effect locus in pseudoexfoliation (PEX) syndrome, a fibrotic disorder of the extracellular matrix and frequent cause of chronic open-angle glaucoma. However, all known PEX-associated common variants show allele effect reversal in populations of different ancestry, casting doubt on their biological significance. Based on extensive LOXL1 deep sequencing, we report here the identification of a common non-coding sequence variant, rs7173049A>G, located downstream of LOXL1, consistently associated with a decrease in PEX risk (odds ratio, OR = 0.63; P = 6.33 × 10-31) in nine different ethnic populations. We provide experimental evidence for a functional enhancer-like regulatory activity of the genomic region surrounding rs7173049 influencing expression levels of ISLR2 (immunoglobulin superfamily containing leucine-rich repeat protein 2) and STRA6 [stimulated by retinoic acid (RA) receptor 6], apparently mediated by allele-specific binding of the transcription factor thyroid hormone receptor beta. We further show that the protective rs7173049-G allele correlates with increased tissue expression levels of ISLR2 and STRA6 and that both genes are significantly downregulated in tissues of PEX patients together with other key components of the STRA6 receptor-driven RA signaling pathway. siRNA-mediated downregulation of RA signaling induces upregulation of LOXL1 and PEX-associated matrix genes in PEX-relevant cell types. These data indicate that dysregulation of STRA6 and impaired retinoid metabolism are involved in the pathophysiology of PEX syndrome and that the variant rs7173049-G, which represents the first common variant at the broad LOXL1 locus without allele effect reversal, mediates a protective effect through upregulation of STRA6 in ocular tissues.

Identifiants

pubmed: 30986821
pii: 5464630
doi: 10.1093/hmg/ddz075
pmc: PMC6644155
doi:

Substances chimiques

Membrane Proteins 0
STRA6 protein, human 0
Tretinoin 5688UTC01R
Amino Acid Oxidoreductases EC 1.4.-
LOXL1 protein, human EC 1.4.3.-

Types de publication

Journal Article Multicenter Study Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2531-2548

Subventions

Organisme : NEI NIH HHS
ID : P30 EY014104
Pays : United States
Organisme : NEI NIH HHS
ID : R01 EY020928
Pays : United States

Informations de copyright

© The Author(s) 2019. Published by Oxford University Press.

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Auteurs

Daniel Berner (D)

Department of Ophthalmology, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Ursula Hoja (U)

Department of Ophthalmology, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Matthias Zenkel (M)

Department of Ophthalmology, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

James Julian Ross (JJ)

Department of Ophthalmology, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Steffen Uebe (S)

Institute of Human Genetics, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Daniela Paoli (D)

Department of Ophthalmology, Monfalcone Hospital, Gorizia, Italy.

Paolo Frezzotti (P)

Ophthalmology Unit, Department of Medicine, Surgery and Neuroscience, University of Siena, Siena, Italy.

Robyn M Rautenbach (RM)

Division of Ophthalmology, Stellenbosch University and Tygerberg Hospital, Cape Town, South Africa.

Ari Ziskind (A)

Division of Ophthalmology, Stellenbosch University and Tygerberg Hospital, Cape Town, South Africa.

Susan E Williams (SE)

Division of Ophthalmology, University of the Witwatersrand, Johannesburg, South Africa.

Trevor R Carmichael (TR)

Division of Ophthalmology, University of the Witwatersrand, Johannesburg, South Africa.

Michele Ramsay (M)

Sydney Brenner Institute for Molecular Bioscience, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.

Fotis Topouzis (F)

Department of Ophthalmology, School of Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece.

Anthi Chatzikyriakidou (A)

Department of Biology and Genetics, School of Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece.

Alexandros Lambropoulos (A)

Department of Biology and Genetics, School of Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece.

Periasamy Sundaresan (P)

Dr. G.Venkataswamy Eye Research Institute, Aravind Medical Research Foundation, Aravind Eye Hospital, Madurai, India.

Humaira Ayub (H)

Department of Environmental Sciences, COMSATS Institute of Information Technology, Abbottabad, Pakistan.

Farah Akhtar (F)

Pakistan Institute of Ophthalmology, Al-Shifa Trust Eye Hospital, Rawalpindi, Pakistan.

Raheel Qamar (R)

Department of Biosciences, COMSATS Institute of Information Technology, Islamabad, Pakistan.

Juan C Zenteno (JC)

Genetics Department, Institute of Ophthalmology 'Conde de Valenciana', Mexico City, Mexico.
Biochemistry Department, Faculty of Medicine, National Autonomous University of Mexico, Mexico City, Mexico.

Marisa Cruz-Aguilar (M)

Genetics Department, Institute of Ophthalmology 'Conde de Valenciana', Mexico City, Mexico.

Yury S Astakhov (YS)

Department of Ophthalmology, Pavlov First Saint Petersburg State Medical University, St Petersburg, Russia.

Michael Dubina (M)

Department of Ophthalmology, Pavlov First Saint Petersburg State Medical University, St Petersburg, Russia.
St Petersburg Academic University, St Petersburg, Russia.

Janey Wiggs (J)

Department of Ophthalmology, Harvard Medical School, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USA.

Mineo Ozaki (M)

Ozaki Eye Hospital, Hyuga, Miyazaki, Japan.
Department of Ophthalmology, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan.

Friedrich E Kruse (FE)

Department of Ophthalmology, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Tin Aung (T)

Singapore Eye Research Institute, Singapore.
Singapore National Eye Center, Singapore.
Department of Ophthalmology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.

André Reis (A)

Institute of Human Genetics, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Chiea Chuen Khor (CC)

Singapore Eye Research Institute, Singapore.
Genome Institute of Singapore, Singapore.
Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.

Francesca Pasutto (F)

Institute of Human Genetics, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Ursula Schlötzer-Schrehardt (U)

Department of Ophthalmology, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

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