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Functionally distinct ERAP1 and ERAP2 are a hallmark of HLA-A29-(Birdshot) Uveitis

Functionally distinct ERAP1 and ERAP2 are a hallmark of HLA-A29-(Birdshot) Uveitis
Functionally distinct ERAP1 and ERAP2 are a hallmark of HLA-A29-(Birdshot) Uveitis
Birdshot Uveitis (Birdshot) is a rare eye condition that affects HLA-A29-positive individuals and could be considered a prototypic member of the recently proposed ‘MHC-I (major histocompatibility complex class I)-opathy’ family. Genetic studies have pinpointed the endoplasmic reticulum aminopeptidase (ERAP1) and (ERAP2) genes as shared associations across MHC-I-opathies, which suggests ERAP dysfunction may be a root cause for MHC-I-opathies. We mapped the ERAP1 and ERAP2 haplotypes in 84 Dutch cases and 890 controls. We identified association at variant rs10044354, which mediated a marked increase in ERAP2 expression. We also identified and cloned an independently associated ERAP1 haplotype (tagged by rs2287987) present in more than half of the cases; this ERAP1 haplotype is also the primary risk and protective haplotype for other MHC-I-opathies. We show that the risk ERAP1 haplotype conferred significantly altered expression of ERAP1 isoforms in transcriptomic data (n = 360), resulting in lowered protein expression and distinct enzymatic activity. Both the association for rs10044354 (meta-analysis: odds ratio (OR) [95% CI]=2.07[1.58–2.71], P = 1.24 × 10(−7)) and rs2287987 (OR[95% CI]: =2.01[1.51–2.67], P = 1.41 × 10(−6)) replicated and showed consistent direction of effect in an independent Spanish cohort of 46 cases and 2103 controls. In both cohorts, the combined rs2287987-rs10044354 haplotype associated with Birdshot more strongly than either variant alone [meta-analysis: P=3.9 × 10(−9)]. Finally, we observed that ERAP2 protein expression is dependent on the ERAP1 background across three European populations (n = 3353). In conclusion, a functionally distinct combination of ERAP1 and ERAP2 are a hallmark of Birdshot and provide rationale for strategies designed to correct ERAP function for treatment of Birdshot and MHC-I-opathies more broadly.
0964-6906
4333-4343
Kuiper, Jonas
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van Setten, Jessica
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Devall, Matthew
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Cretu-stancu, mircea
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Hiddingh, Sanne
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Ophoff, Roel
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Missotten, Tom
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van Velthoven, Mirjam
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Den Hollander, Anneke
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Hoyng, Carel B.
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James, Edward
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Reeves, Emma
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Cordero-Coma, Miguel
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Fonollosa, Alejandro
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Adan, Alfredo
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Martin, Javier
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Koeleman, Bobby
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Boer, Joke de
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Pulit, Sara
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Marquez, Ana
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Radstake, Timothy
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Kuiper, Jonas
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van Setten, Jessica
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Devall, Matthew
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Cretu-stancu, mircea
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Hiddingh, Sanne
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Ophoff, Roel
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Missotten, Tom
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van Velthoven, Mirjam
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Den Hollander, Anneke
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Hoyng, Carel B.
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James, Edward
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Reeves, Emma
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Cordero-Coma, Miguel
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Fonollosa, Alejandro
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Adan, Alfredo
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Martin, Javier
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Koeleman, Bobby
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Boer, Joke de
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Pulit, Sara
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Marquez, Ana
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Radstake, Timothy
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Kuiper, Jonas, van Setten, Jessica, Devall, Matthew, Cretu-stancu, mircea, Hiddingh, Sanne, Ophoff, Roel, Missotten, Tom, van Velthoven, Mirjam, Den Hollander, Anneke, Hoyng, Carel B., James, Edward, Reeves, Emma, Cordero-Coma, Miguel, Fonollosa, Alejandro, Adan, Alfredo, Martin, Javier, Koeleman, Bobby, Boer, Joke de, Pulit, Sara, Marquez, Ana and Radstake, Timothy (2018) Functionally distinct ERAP1 and ERAP2 are a hallmark of HLA-A29-(Birdshot) Uveitis. Human Molecular Genetics, 27 (24), 4333-4343. (doi:10.1093/hmg/ddy319).

Record type: Article

Abstract

Birdshot Uveitis (Birdshot) is a rare eye condition that affects HLA-A29-positive individuals and could be considered a prototypic member of the recently proposed ‘MHC-I (major histocompatibility complex class I)-opathy’ family. Genetic studies have pinpointed the endoplasmic reticulum aminopeptidase (ERAP1) and (ERAP2) genes as shared associations across MHC-I-opathies, which suggests ERAP dysfunction may be a root cause for MHC-I-opathies. We mapped the ERAP1 and ERAP2 haplotypes in 84 Dutch cases and 890 controls. We identified association at variant rs10044354, which mediated a marked increase in ERAP2 expression. We also identified and cloned an independently associated ERAP1 haplotype (tagged by rs2287987) present in more than half of the cases; this ERAP1 haplotype is also the primary risk and protective haplotype for other MHC-I-opathies. We show that the risk ERAP1 haplotype conferred significantly altered expression of ERAP1 isoforms in transcriptomic data (n = 360), resulting in lowered protein expression and distinct enzymatic activity. Both the association for rs10044354 (meta-analysis: odds ratio (OR) [95% CI]=2.07[1.58–2.71], P = 1.24 × 10(−7)) and rs2287987 (OR[95% CI]: =2.01[1.51–2.67], P = 1.41 × 10(−6)) replicated and showed consistent direction of effect in an independent Spanish cohort of 46 cases and 2103 controls. In both cohorts, the combined rs2287987-rs10044354 haplotype associated with Birdshot more strongly than either variant alone [meta-analysis: P=3.9 × 10(−9)]. Finally, we observed that ERAP2 protein expression is dependent on the ERAP1 background across three European populations (n = 3353). In conclusion, a functionally distinct combination of ERAP1 and ERAP2 are a hallmark of Birdshot and provide rationale for strategies designed to correct ERAP function for treatment of Birdshot and MHC-I-opathies more broadly.

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Accepted/In Press date: 7 September 2018
e-pub ahead of print date: 12 September 2018
Published date: 15 December 2018

Identifiers

Local EPrints ID: 425954
URI: http://eprints.soton.ac.uk/id/eprint/425954
ISSN: 0964-6906
PURE UUID: 8c72f896-ff68-4134-8709-663ac98ee540
ORCID for Edward James: ORCID iD orcid.org/0000-0001-8638-7928

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Date deposited: 07 Nov 2018 17:30
Last modified: 16 Mar 2024 03:51

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Contributors

Author: Jonas Kuiper
Author: Jessica van Setten
Author: Matthew Devall
Author: mircea Cretu-stancu
Author: Sanne Hiddingh
Author: Roel Ophoff
Author: Tom Missotten
Author: Mirjam van Velthoven
Author: Anneke Den Hollander
Author: Carel B. Hoyng
Author: Edward James ORCID iD
Author: Emma Reeves
Author: Miguel Cordero-Coma
Author: Alejandro Fonollosa
Author: Alfredo Adan
Author: Javier Martin
Author: Bobby Koeleman
Author: Joke de Boer
Author: Sara Pulit
Author: Ana Marquez
Author: Timothy Radstake

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