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Janus-faced EPHB4-associated disorders: novel pathogenic variants and unreported intrafamilial overlapping phenotypes

Janus-faced EPHB4-associated disorders: novel pathogenic variants and unreported intrafamilial overlapping phenotypes
Janus-faced EPHB4-associated disorders: novel pathogenic variants and unreported intrafamilial overlapping phenotypes
Purpose

Several clinical phenotypes including fetal hydrops, central conducting lymphatic anomaly or capillary malformations with arteriovenous malformations 2 (CM-AVM2) have been associated with EPHB4 (Ephrin type B receptor 4) variants, demanding new approaches for deciphering pathogenesis of novel variants of uncertain significance (VUS) identified in EPHB4, and for the identification of differentiated disease mechanisms at the molecular level.

Methods

Ten index cases with various phenotypes, either fetal hydrops, CM-AVM2, or peripheral lower limb lymphedema, whose distinct clinical phenotypes are described in detail in this study, presented with a variant in EPHB4. In vitro functional studies were performed to confirm pathogenicity.

Results

Pathogenicity was demonstrated for six of the seven novel EPHB4 VUS investigated. A heterogeneity of molecular disease mechanisms was identified, from loss of protein production or aberrant subcellular localization to total reduction of the phosphorylation capability of the receptor. There was some phenotype–genotype correlation; however, previously unreported intrafamilial overlapping phenotypes such as lymphatic-related fetal hydrops (LRFH) and CM-AVM2 in the same family were observed.

Conclusion

This study highlights the usefulness of protein expression and subcellular localization studies to predict EPHB4 variant pathogenesis. Our accurate clinical phenotyping expands our interpretation of the Janus-faced spectrum of EPHB4-related disorders, introducing the discovery of cases with overlapping phenotypes.

1098-3600
1315-1324
Martin-almedina, Silvia
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Ogmen, Kazim
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Sackey, Ege
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Grigoriadis, Dionysios
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Karapouliou, Christina
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Nadarajah, Noeline
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Ebbing, Cathrine
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Lord, Jenny
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Mellis, Rhiannon
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Kortuem, Fanny
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Dinulos, Mary Beth
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Polun, Cassandra
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Bale, Sherri
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Atton, Giles
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Robinson, Alexandra
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Reigstad, Hallvard
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Houge, Gunnar
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Von Der Wense, Axel
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Becker, Wolf-henning
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Jeffery, Steve
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Mortimer, Peter S.
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Gordon, Kristiana
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Josephs, Katherine S.
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Robart, Sarah
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Kilby, Mark D.
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Vallee, Stephanie
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Gorski, Jerome L.
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Hempel, Maja
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Berland, Siren
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Mansour, Sahar
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Ostergaard, Pia
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Martin-almedina, Silvia
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Ogmen, Kazim
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Sackey, Ege
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Grigoriadis, Dionysios
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Karapouliou, Christina
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Nadarajah, Noeline
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Ebbing, Cathrine
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Lord, Jenny
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Mellis, Rhiannon
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Kortuem, Fanny
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Dinulos, Mary Beth
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Polun, Cassandra
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Bale, Sherri
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Atton, Giles
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Robinson, Alexandra
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Reigstad, Hallvard
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Houge, Gunnar
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Von Der Wense, Axel
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Becker, Wolf-henning
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Jeffery, Steve
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Mortimer, Peter S.
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Gordon, Kristiana
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Josephs, Katherine S.
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Robart, Sarah
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Kilby, Mark D.
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Vallee, Stephanie
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Gorski, Jerome L.
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Hempel, Maja
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Berland, Siren
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Mansour, Sahar
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Ostergaard, Pia
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Martin-almedina, Silvia, Ogmen, Kazim, Sackey, Ege, Grigoriadis, Dionysios, Karapouliou, Christina, Nadarajah, Noeline, Ebbing, Cathrine, Lord, Jenny, Mellis, Rhiannon, Kortuem, Fanny, Dinulos, Mary Beth, Polun, Cassandra, Bale, Sherri, Atton, Giles, Robinson, Alexandra, Reigstad, Hallvard, Houge, Gunnar, Von Der Wense, Axel, Becker, Wolf-henning, Jeffery, Steve, Mortimer, Peter S., Gordon, Kristiana, Josephs, Katherine S., Robart, Sarah, Kilby, Mark D., Vallee, Stephanie, Gorski, Jerome L., Hempel, Maja, Berland, Siren, Mansour, Sahar and Ostergaard, Pia (2021) Janus-faced EPHB4-associated disorders: novel pathogenic variants and unreported intrafamilial overlapping phenotypes. Genetics in Medicine, 23 (7), 1315-1324. (doi:10.1038/s41436-021-01136-7).

Record type: Article

Abstract

Purpose

Several clinical phenotypes including fetal hydrops, central conducting lymphatic anomaly or capillary malformations with arteriovenous malformations 2 (CM-AVM2) have been associated with EPHB4 (Ephrin type B receptor 4) variants, demanding new approaches for deciphering pathogenesis of novel variants of uncertain significance (VUS) identified in EPHB4, and for the identification of differentiated disease mechanisms at the molecular level.

Methods

Ten index cases with various phenotypes, either fetal hydrops, CM-AVM2, or peripheral lower limb lymphedema, whose distinct clinical phenotypes are described in detail in this study, presented with a variant in EPHB4. In vitro functional studies were performed to confirm pathogenicity.

Results

Pathogenicity was demonstrated for six of the seven novel EPHB4 VUS investigated. A heterogeneity of molecular disease mechanisms was identified, from loss of protein production or aberrant subcellular localization to total reduction of the phosphorylation capability of the receptor. There was some phenotype–genotype correlation; however, previously unreported intrafamilial overlapping phenotypes such as lymphatic-related fetal hydrops (LRFH) and CM-AVM2 in the same family were observed.

Conclusion

This study highlights the usefulness of protein expression and subcellular localization studies to predict EPHB4 variant pathogenesis. Our accurate clinical phenotyping expands our interpretation of the Janus-faced spectrum of EPHB4-related disorders, introducing the discovery of cases with overlapping phenotypes.

Text
Martin Almedina et al_GIM_2020_accepted version - Accepted Manuscript
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More information

Accepted/In Press date: 18 February 2021
e-pub ahead of print date: 16 April 2021
Published date: July 2021

Identifiers

Local EPrints ID: 449282
URI: http://eprints.soton.ac.uk/id/eprint/449282
ISSN: 1098-3600
PURE UUID: 0714d661-cfb2-4430-8631-f010af8e3671
ORCID for Jenny Lord: ORCID iD orcid.org/0000-0002-0539-9343

Catalogue record

Date deposited: 21 May 2021 16:31
Last modified: 17 Mar 2024 06:34

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Contributors

Author: Silvia Martin-almedina
Author: Kazim Ogmen
Author: Ege Sackey
Author: Dionysios Grigoriadis
Author: Christina Karapouliou
Author: Noeline Nadarajah
Author: Cathrine Ebbing
Author: Jenny Lord ORCID iD
Author: Rhiannon Mellis
Author: Fanny Kortuem
Author: Mary Beth Dinulos
Author: Cassandra Polun
Author: Sherri Bale
Author: Giles Atton
Author: Alexandra Robinson
Author: Hallvard Reigstad
Author: Gunnar Houge
Author: Axel Von Der Wense
Author: Wolf-henning Becker
Author: Steve Jeffery
Author: Peter S. Mortimer
Author: Kristiana Gordon
Author: Katherine S. Josephs
Author: Sarah Robart
Author: Mark D. Kilby
Author: Stephanie Vallee
Author: Jerome L. Gorski
Author: Maja Hempel
Author: Siren Berland
Author: Sahar Mansour
Author: Pia Ostergaard

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