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Trans-acting genetic variants causing multilocus imprinting disturbance (MLID): common mechanisms and consequences

Trans-acting genetic variants causing multilocus imprinting disturbance (MLID): common mechanisms and consequences
Trans-acting genetic variants causing multilocus imprinting disturbance (MLID): common mechanisms and consequences

Background: Imprinting disorders are a group of congenital diseases which are characterized by molecular alterations affecting differentially methylated regions (DMRs). To date, at least twelve imprinting disorders have been defined with overlapping but variable clinical features including growth and metabolic disturbances, cognitive dysfunction, abdominal wall defects and asymmetry. In general, a single specific DMR is affected in an individual with a given imprinting disorder, but there are a growing number of reports on individuals with so-called multilocus imprinting disturbances (MLID), where aberrant imprinting marks (most commonly loss of methylation) occur at multiple DMRs. However, as the literature is fragmented, we reviewed the molecular and clinical data of 55 previously reported or newly identified MLID families with putative pathogenic variants in maternal effect genes (NLRP2, NLRP5, NLRP7, KHDC3L, OOEP, PADI6) and in other candidate genes (ZFP57, ARID4A, ZAR1, UHRF1, ZNF445). Results: In 55 families, a total of 68 different candidate pathogenic variants were identified (7 in NLRP2, 16 in NLRP5, 7 in NLRP7, 17 in PADI6, 15 in ZFP57, and a single variant in each of the genes ARID4A, ZAR1, OOEP, UHRF1, KHDC3L and ZNF445). Clinical diagnoses of affected offspring included Beckwith–Wiedemann syndrome spectrum, Silver–Russell syndrome spectrum, transient neonatal diabetes mellitus, or they were suspected for an imprinting disorder (undiagnosed). Some families had recurrent pregnancy loss. Conclusions: Genomic maternal effect and foetal variants causing MLID allow insights into the mechanisms behind the imprinting cycle of life, and the spatial and temporal function of the different factors involved in oocyte maturation and early development. Further basic research together with identification of new MLID families will enable a better understanding of the link between the different reproductive issues such as recurrent miscarriages and preeclampsia in maternal effect variant carriers/families and aneuploidy and the MLID observed in the offsprings. The current knowledge can already be employed in reproductive and genetic counselling in specific situations.

Beckwith–Wiedemann syndrome spectrum, Differentially methylated regions, Epimutations, Gain of methylation, Growth disturbances, Imprinting disorders, Loss of methylation, Multi locus imprinting disturbance, Silver–Russell syndrome spectrum, Transient neonatal diabetes mellitus, Uniparental disomy
1868-7075
Eggermann, Thomas
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Yapici, Elzem
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Bliek, Jet
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Pereda, Arrate
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Begemann, Matthias
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Russo, Silvia
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Tannorella, Pierpaola
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Calzari, Luciano
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De Nanclares, Guiomar Perez
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Lombardi, Paola
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Temple, I. Karen
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Mackay, Deborah
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Riccio, Andrea
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Kagami, Masayo
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Ogata, Tsutomu
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Lapunzina, Pablo
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Monk, David
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Maher, Eamonn R.
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Tümer, Zeynep
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Eggermann, Thomas
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Yapici, Elzem
a35a3eec-364a-40be-8482-494adc2c265e
Bliek, Jet
71a7b9b1-a591-491d-832a-9b670ef05195
Pereda, Arrate
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Begemann, Matthias
e6e9fa94-7d5c-4a79-86b4-6e17e685f433
Russo, Silvia
c58120ef-376c-49f9-be98-0b72bd45d525
Tannorella, Pierpaola
d39e1aaa-787d-4657-abe7-4d272b947c34
Calzari, Luciano
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De Nanclares, Guiomar Perez
4f5fb1c5-879f-4db8-a9cd-8987d8f3d120
Lombardi, Paola
372aa188-e6c1-4e20-9ebe-934640656bcc
Temple, I. Karen
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Mackay, Deborah
588a653e-9785-4a00-be71-4e547850ee4a
Riccio, Andrea
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Kagami, Masayo
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Ogata, Tsutomu
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Lapunzina, Pablo
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Monk, David
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Maher, Eamonn R.
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Tümer, Zeynep
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Eggermann, Thomas, Yapici, Elzem, Bliek, Jet, Pereda, Arrate, Begemann, Matthias, Russo, Silvia, Tannorella, Pierpaola, Calzari, Luciano, De Nanclares, Guiomar Perez, Lombardi, Paola, Temple, I. Karen, Mackay, Deborah, Riccio, Andrea, Kagami, Masayo, Ogata, Tsutomu, Lapunzina, Pablo, Monk, David, Maher, Eamonn R. and Tümer, Zeynep (2022) Trans-acting genetic variants causing multilocus imprinting disturbance (MLID): common mechanisms and consequences. Clinical Epigenetics, 14, [41 (2022)]. (doi:10.1186/s13148-022-01259-x).

Record type: Article

Abstract

Background: Imprinting disorders are a group of congenital diseases which are characterized by molecular alterations affecting differentially methylated regions (DMRs). To date, at least twelve imprinting disorders have been defined with overlapping but variable clinical features including growth and metabolic disturbances, cognitive dysfunction, abdominal wall defects and asymmetry. In general, a single specific DMR is affected in an individual with a given imprinting disorder, but there are a growing number of reports on individuals with so-called multilocus imprinting disturbances (MLID), where aberrant imprinting marks (most commonly loss of methylation) occur at multiple DMRs. However, as the literature is fragmented, we reviewed the molecular and clinical data of 55 previously reported or newly identified MLID families with putative pathogenic variants in maternal effect genes (NLRP2, NLRP5, NLRP7, KHDC3L, OOEP, PADI6) and in other candidate genes (ZFP57, ARID4A, ZAR1, UHRF1, ZNF445). Results: In 55 families, a total of 68 different candidate pathogenic variants were identified (7 in NLRP2, 16 in NLRP5, 7 in NLRP7, 17 in PADI6, 15 in ZFP57, and a single variant in each of the genes ARID4A, ZAR1, OOEP, UHRF1, KHDC3L and ZNF445). Clinical diagnoses of affected offspring included Beckwith–Wiedemann syndrome spectrum, Silver–Russell syndrome spectrum, transient neonatal diabetes mellitus, or they were suspected for an imprinting disorder (undiagnosed). Some families had recurrent pregnancy loss. Conclusions: Genomic maternal effect and foetal variants causing MLID allow insights into the mechanisms behind the imprinting cycle of life, and the spatial and temporal function of the different factors involved in oocyte maturation and early development. Further basic research together with identification of new MLID families will enable a better understanding of the link between the different reproductive issues such as recurrent miscarriages and preeclampsia in maternal effect variant carriers/families and aneuploidy and the MLID observed in the offsprings. The current knowledge can already be employed in reproductive and genetic counselling in specific situations.

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Accepted/In Press date: 28 February 2022
Published date: 16 March 2022
Additional Information: Funding Open Access funding enabled and organized by Projekt DEAL. This work was funded by a grant from the Istituto de Salud Carlos III [Institute of Health Carlos III] of the Ministry of Economy and Competitiveness [Spain] (to GPdN and AP), co-financed by the European Regional Development Fund (PI20/00950) and the 2019 research unit grant from ESPE (to GdPN). EM is funded by the NIHR Cambridge Biomedical Research Centre, Rosetrees Trust; the University of Cambridge has received salary support (ERM.) from the NHS in the East of England through the Clinical Academic Reserve. The views expressed are those of the authors and not necessarily those of the NHS or Department of Health. PL is funded by the Grant FIS 20/01053, ISCIII. AR is funded by AIRC grant IG 24405.
Keywords: Beckwith–Wiedemann syndrome spectrum, Differentially methylated regions, Epimutations, Gain of methylation, Growth disturbances, Imprinting disorders, Loss of methylation, Multi locus imprinting disturbance, Silver–Russell syndrome spectrum, Transient neonatal diabetes mellitus, Uniparental disomy

Identifiers

Local EPrints ID: 456159
URI: http://eprints.soton.ac.uk/id/eprint/456159
ISSN: 1868-7075
PURE UUID: 3d6531db-16a0-46f7-9be3-85ec62584114
ORCID for I. Karen Temple: ORCID iD orcid.org/0000-0002-6045-1781
ORCID for Deborah Mackay: ORCID iD orcid.org/0000-0003-3088-4401

Catalogue record

Date deposited: 26 Apr 2022 15:07
Last modified: 17 Mar 2024 02:48

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Contributors

Author: Thomas Eggermann
Author: Elzem Yapici
Author: Jet Bliek
Author: Arrate Pereda
Author: Matthias Begemann
Author: Silvia Russo
Author: Pierpaola Tannorella
Author: Luciano Calzari
Author: Guiomar Perez De Nanclares
Author: Paola Lombardi
Author: I. Karen Temple ORCID iD
Author: Deborah Mackay ORCID iD
Author: Andrea Riccio
Author: Masayo Kagami
Author: Tsutomu Ogata
Author: Pablo Lapunzina
Author: David Monk
Author: Eamonn R. Maher
Author: Zeynep Tümer

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