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Genome-wide association study identifies novel susceptibility loci for KIT D816V positive mastocytosis

Genome-wide association study identifies novel susceptibility loci for KIT D816V positive mastocytosis
Genome-wide association study identifies novel susceptibility loci for KIT D816V positive mastocytosis
Mastocytosis is a rare myeloid neoplasm characterized by uncontrolled expansion of mast cells, driven in >80% of affected individuals by acquisition of the KIT D816V mutation. To explore the hypothesis that inherited variation predisposes to mastocytosis, we performed a two-stage genome-wide association study, analyzing 1,035 individuals with KIT D816V positive disease and 17,960 healthy control individuals from five European populations. After quality control, we tested 592,007 SNPs at stage 1 and 75 SNPs at stage 2 for association by using logistic regression and performed a fixed effects meta-analysis to combine evidence across the two stages. From the meta-analysis, we identified three intergenic SNPs associated with mastocytosis that achieved genome-wide significance without heterogeneity between cohorts: rs4616402 (pmeta = 1.37 × 10−15, OR = 1.52), rs4662380 (pmeta = 2.11 × 10−12, OR = 1.46), and rs13077541 (pmeta = 2.10 × 10−9, OR = 1.33). Expression quantitative trait analyses demonstrated that rs4616402 is associated with the expression of CEBPA (peQTL = 2.3 × 10−14), a gene encoding a transcription factor known to play a critical role in myelopoiesis. The role of the other two SNPs is less clear: rs4662380 is associated with expression of the long non-coding RNA gene TEX41 (peQTL = 2.55 × 10−11), whereas rs13077541 is associated with the expression of TBL1XR1, which encodes transducin (β)-like 1 X-linked receptor 1 (peQTL = 5.70 × 10−8). In individuals with available data and non-advanced disease, rs4616402 was associated with age at presentation (p = 0.009; beta = 4.41; n = 422). Additional focused analysis identified suggestive associations between mastocytosis and genetic variation at TERT, TPSAB1/TPSB2, and IL13. These findings demonstrate that multiple germline variants predispose to KIT D816V positive mastocytosis and provide novel avenues for functional investigation.
CEBPA, D816V, KIT, TBL1XR1, TERT, mastocytosis, myeloid cancer
0002-9297
284-294
Galatà, Gabriella
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García-montero, Andrés C.
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Kristensen, Thomas
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Dawoud, Ahmed A.Z.
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Muñoz-gonzález, Javier I.
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Meggendorfer, Manja
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Guglielmelli, Paola
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Hoade, Yvette
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Alvarez-twose, Ivan
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Gieger, Christian
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Strauch, Konstantin
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Ferrucci, Luigi
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Tanaka, Toshiko
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Bandinelli, Stefania
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Schnurr, Theresia M.
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Haferlach, Torsten
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Broesby-olsen, Sigurd
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Vestergaard, Hanne
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Møller, Michael Boe
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Bindslev-jensen, Carsten
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Vannucchi, Alessandro M.
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Orfao, Alberto
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Radia, Deepti
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Reiter, Andreas
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Chase, Andrew J.
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Cross, Nicholas C.P.
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Tapper, William J.
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Galatà, Gabriella
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García-montero, Andrés C.
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Kristensen, Thomas
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Dawoud, Ahmed A.Z.
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Meggendorfer, Manja
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Guglielmelli, Paola
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Hoade, Yvette
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Alvarez-twose, Ivan
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Gieger, Christian
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Strauch, Konstantin
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Ferrucci, Luigi
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Tanaka, Toshiko
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Bandinelli, Stefania
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Schnurr, Theresia M.
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Haferlach, Torsten
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Broesby-olsen, Sigurd
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Vestergaard, Hanne
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Møller, Michael Boe
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Bindslev-jensen, Carsten
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Vannucchi, Alessandro M.
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Orfao, Alberto
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Radia, Deepti
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Reiter, Andreas
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Chase, Andrew J.
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Cross, Nicholas C.P.
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Tapper, William J.
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Galatà, Gabriella, García-montero, Andrés C., Kristensen, Thomas, Dawoud, Ahmed A.Z., Muñoz-gonzález, Javier I., Meggendorfer, Manja, Guglielmelli, Paola, Hoade, Yvette, Alvarez-twose, Ivan, Gieger, Christian, Strauch, Konstantin, Ferrucci, Luigi, Tanaka, Toshiko, Bandinelli, Stefania, Schnurr, Theresia M., Haferlach, Torsten, Broesby-olsen, Sigurd, Vestergaard, Hanne, Møller, Michael Boe, Bindslev-jensen, Carsten, Vannucchi, Alessandro M., Orfao, Alberto, Radia, Deepti, Reiter, Andreas, Chase, Andrew J., Cross, Nicholas C.P. and Tapper, William J. (2021) Genome-wide association study identifies novel susceptibility loci for KIT D816V positive mastocytosis. The American Journal of Human Genetics, 108 (2), 284-294. (doi:10.1016/j.ajhg.2020.12.007).

Record type: Article

Abstract

Mastocytosis is a rare myeloid neoplasm characterized by uncontrolled expansion of mast cells, driven in >80% of affected individuals by acquisition of the KIT D816V mutation. To explore the hypothesis that inherited variation predisposes to mastocytosis, we performed a two-stage genome-wide association study, analyzing 1,035 individuals with KIT D816V positive disease and 17,960 healthy control individuals from five European populations. After quality control, we tested 592,007 SNPs at stage 1 and 75 SNPs at stage 2 for association by using logistic regression and performed a fixed effects meta-analysis to combine evidence across the two stages. From the meta-analysis, we identified three intergenic SNPs associated with mastocytosis that achieved genome-wide significance without heterogeneity between cohorts: rs4616402 (pmeta = 1.37 × 10−15, OR = 1.52), rs4662380 (pmeta = 2.11 × 10−12, OR = 1.46), and rs13077541 (pmeta = 2.10 × 10−9, OR = 1.33). Expression quantitative trait analyses demonstrated that rs4616402 is associated with the expression of CEBPA (peQTL = 2.3 × 10−14), a gene encoding a transcription factor known to play a critical role in myelopoiesis. The role of the other two SNPs is less clear: rs4662380 is associated with expression of the long non-coding RNA gene TEX41 (peQTL = 2.55 × 10−11), whereas rs13077541 is associated with the expression of TBL1XR1, which encodes transducin (β)-like 1 X-linked receptor 1 (peQTL = 5.70 × 10−8). In individuals with available data and non-advanced disease, rs4616402 was associated with age at presentation (p = 0.009; beta = 4.41; n = 422). Additional focused analysis identified suggestive associations between mastocytosis and genetic variation at TERT, TPSAB1/TPSB2, and IL13. These findings demonstrate that multiple germline variants predispose to KIT D816V positive mastocytosis and provide novel avenues for functional investigation.

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Galata AJHG for PURE - Accepted Manuscript
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Accepted/In Press date: 7 December 2020
e-pub ahead of print date: 8 January 2021
Published date: 4 February 2021
Additional Information: Funding Information: A full list of the investigators who contributed to the generation of the WTCCC data is available from the WTCCC website, funding for which was provided by The Wellcome Trust under award 07611. The KORA study was initiated and financed by the Helmholtz Zentrum M?nchen?German Research Center for Environmental Health, which is funded by the German Federal Ministry of Education and Research (BMBF) and by the State of Bavaria. Furthermore, KORA research was supported within the Munich Center of Health Sciences (MC-Health), Ludwig-Maximilians-Universit?t, as part of LMUinnovativ. The KORA Study Group consists of A. Peters (speaker), J. Heinrich, R. Holle, R. Leidl, C. Meisinger, K. Strauch, and their co-workers, who are responsible for the design and conduct of the KORA studies. We gratefully acknowledge the contribution of all members of field staff conducting the KORA study, and we are grateful to all study participants of KORA for their invaluable contributions to this study. The InCHIANTI
Keywords: CEBPA, D816V, KIT, TBL1XR1, TERT, mastocytosis, myeloid cancer

Identifiers

Local EPrints ID: 446149
URI: http://eprints.soton.ac.uk/id/eprint/446149
ISSN: 0002-9297
PURE UUID: 20cdde24-2aef-4caf-bd9e-23e4c1b58320
ORCID for Ahmed A.Z. Dawoud: ORCID iD orcid.org/0000-0003-0164-7773
ORCID for Andrew J. Chase: ORCID iD orcid.org/0000-0001-6617-9953
ORCID for Nicholas C.P. Cross: ORCID iD orcid.org/0000-0001-5481-2555
ORCID for William J. Tapper: ORCID iD orcid.org/0000-0002-5896-1889

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Date deposited: 22 Jan 2021 17:30
Last modified: 06 Nov 2024 05:01

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Contributors

Author: Gabriella Galatà
Author: Andrés C. García-montero
Author: Thomas Kristensen
Author: Ahmed A.Z. Dawoud ORCID iD
Author: Javier I. Muñoz-gonzález
Author: Manja Meggendorfer
Author: Paola Guglielmelli
Author: Yvette Hoade
Author: Ivan Alvarez-twose
Author: Christian Gieger
Author: Konstantin Strauch
Author: Luigi Ferrucci
Author: Toshiko Tanaka
Author: Stefania Bandinelli
Author: Theresia M. Schnurr
Author: Torsten Haferlach
Author: Sigurd Broesby-olsen
Author: Hanne Vestergaard
Author: Michael Boe Møller
Author: Carsten Bindslev-jensen
Author: Alessandro M. Vannucchi
Author: Alberto Orfao
Author: Deepti Radia
Author: Andreas Reiter
Author: Andrew J. Chase ORCID iD

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