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A recurrent mosaic mutation of SMO, encoding the hedgehog signal transducer smoothened, is the major cause of Curry-Jones syndrome

A recurrent mosaic mutation of SMO, encoding the hedgehog signal transducer smoothened, is the major cause of Curry-Jones syndrome
A recurrent mosaic mutation of SMO, encoding the hedgehog signal transducer smoothened, is the major cause of Curry-Jones syndrome
Curry-Jones syndrome (CJS) is a multisystem disorder characterized by patchy skin lesions, polysyndactyly, diverse cerebral malformations, unicoronal craniosynostosis, iris colobomas, microphthalmia, and intestinal malrotation with myofibromas or hamartomas. Cerebellar medulloblastoma has been described in a single affected individual; in another, biopsy of skin lesions showed features of trichoblastoma. The combination of asymmetric clinical features, patchy skin manifestations, and neoplastic association previously led to the suggestion that this could be a mosaic condition, possibly involving hedgehog (Hh) signaling. Here, we show that CJS is caused by recurrent somatic mosaicism for a nonsynonymous variant in SMO (c.1234C>T [p.Leu412Phe]), encoding smoothened (SMO), a G-protein-coupled receptor that transduces Hh signaling. We identified eight mutation-positive individuals (two of whom had not been reported previously) with highly similar phenotypes and demonstrated varying amounts of the mutant allele in different tissues. We present detailed findings from brain MRI in three mutation-positive individuals. Somatic SMO mutations that result in constitutive activation have been described in several tumors, including medulloblastoma, ameloblastoma, and basal cell carcinoma. Strikingly, the most common of these mutations is the identical nonsynonymous variant encoding p.Leu412Phe. Furthermore, this substitution has been shown to activate SMO in the absence of Hh signaling, providing an explanation for tumor development in CJS. This raises therapeutic possibilities for using recently generated Hh-pathway inhibitors. In summary, our work uncovers the major genetic cause of CJS and illustrates strategies for gene discovery in the context of low-level tissue-specific somatic mosaicism.
0002-9297
1256-1265
Twigg, Stephen R.F.
894d2681-a4c2-4571-825b-72577969617b
Hufnagel, Robert B.
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Miller, Kerry A.
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Zhou, Yan
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McGowan, Simon J.
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Taylor, John
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Craft, Jude
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Taylor, Jenny C.
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Santoro, Stephanie L.
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Huang, Taosheng
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Hopkin, Robert J.
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Brady, Angela F.
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Clayton-Smith, Jill
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Clericuzio, Carol L.
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Grange, Dorothy K.
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Groesser, Leopold
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Hafner, Christian
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Horn, Denise
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Temple, I. Karen
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Dobyns, William B.
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Curry, Cynthia J.
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Jones, Marilyn C.
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Wilkie, Andrew O.M.
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Twigg, Stephen R.F.
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Hufnagel, Robert B.
372e28c0-aa21-446b-a19a-4e28fb4924c0
Miller, Kerry A.
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Zhou, Yan
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McGowan, Simon J.
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Taylor, John
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Craft, Jude
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Taylor, Jenny C.
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Santoro, Stephanie L.
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Huang, Taosheng
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Hopkin, Robert J.
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Brady, Angela F.
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Clayton-Smith, Jill
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Clericuzio, Carol L.
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Grange, Dorothy K.
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Groesser, Leopold
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Hafner, Christian
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Horn, Denise
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Temple, I. Karen
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Dobyns, William B.
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Curry, Cynthia J.
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Jones, Marilyn C.
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Wilkie, Andrew O.M.
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Twigg, Stephen R.F., Hufnagel, Robert B., Miller, Kerry A., Zhou, Yan, McGowan, Simon J., Taylor, John, Craft, Jude, Taylor, Jenny C., Santoro, Stephanie L., Huang, Taosheng, Hopkin, Robert J., Brady, Angela F., Clayton-Smith, Jill, Clericuzio, Carol L., Grange, Dorothy K., Groesser, Leopold, Hafner, Christian, Horn, Denise, Temple, I. Karen, Dobyns, William B., Curry, Cynthia J., Jones, Marilyn C. and Wilkie, Andrew O.M. (2016) A recurrent mosaic mutation of SMO, encoding the hedgehog signal transducer smoothened, is the major cause of Curry-Jones syndrome. The American Journal of Human Genetics, 98 (6), 1256-1265. (doi:10.1016/j.ajhg.2016.04.007). (PMID:27236920)

Record type: Article

Abstract

Curry-Jones syndrome (CJS) is a multisystem disorder characterized by patchy skin lesions, polysyndactyly, diverse cerebral malformations, unicoronal craniosynostosis, iris colobomas, microphthalmia, and intestinal malrotation with myofibromas or hamartomas. Cerebellar medulloblastoma has been described in a single affected individual; in another, biopsy of skin lesions showed features of trichoblastoma. The combination of asymmetric clinical features, patchy skin manifestations, and neoplastic association previously led to the suggestion that this could be a mosaic condition, possibly involving hedgehog (Hh) signaling. Here, we show that CJS is caused by recurrent somatic mosaicism for a nonsynonymous variant in SMO (c.1234C>T [p.Leu412Phe]), encoding smoothened (SMO), a G-protein-coupled receptor that transduces Hh signaling. We identified eight mutation-positive individuals (two of whom had not been reported previously) with highly similar phenotypes and demonstrated varying amounts of the mutant allele in different tissues. We present detailed findings from brain MRI in three mutation-positive individuals. Somatic SMO mutations that result in constitutive activation have been described in several tumors, including medulloblastoma, ameloblastoma, and basal cell carcinoma. Strikingly, the most common of these mutations is the identical nonsynonymous variant encoding p.Leu412Phe. Furthermore, this substitution has been shown to activate SMO in the absence of Hh signaling, providing an explanation for tumor development in CJS. This raises therapeutic possibilities for using recently generated Hh-pathway inhibitors. In summary, our work uncovers the major genetic cause of CJS and illustrates strategies for gene discovery in the context of low-level tissue-specific somatic mosaicism.

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Accepted/In Press date: 27 April 2016
e-pub ahead of print date: 26 May 2016
Published date: 2 June 2016
Organisations: Human Development & Health

Identifiers

Local EPrints ID: 393812
URI: http://eprints.soton.ac.uk/id/eprint/393812
ISSN: 0002-9297
PURE UUID: eaad49c0-389b-4e74-b56a-c33f0c680ed7
ORCID for I. Karen Temple: ORCID iD orcid.org/0000-0002-6045-1781

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Date deposited: 06 May 2016 08:49
Last modified: 15 Mar 2024 05:33

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Contributors

Author: Stephen R.F. Twigg
Author: Robert B. Hufnagel
Author: Kerry A. Miller
Author: Yan Zhou
Author: Simon J. McGowan
Author: John Taylor
Author: Jude Craft
Author: Jenny C. Taylor
Author: Stephanie L. Santoro
Author: Taosheng Huang
Author: Robert J. Hopkin
Author: Angela F. Brady
Author: Jill Clayton-Smith
Author: Carol L. Clericuzio
Author: Dorothy K. Grange
Author: Leopold Groesser
Author: Christian Hafner
Author: Denise Horn
Author: I. Karen Temple ORCID iD
Author: William B. Dobyns
Author: Cynthia J. Curry
Author: Marilyn C. Jones
Author: Andrew O.M. Wilkie

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