Recurrent hotspot mutations in HRAS Q61 and PI3K-AKT pathway genes as drivers of breast adenomyoepitheliomas

Adenomyoepithelioma of the breast is a rare tumor characterized by epithelial-myoepithelial differentiation, of which a subset will progress to invasive or metastatic cancer. We sought to define the genomic landscape of adenomyoepitheliomas. Massively parallel sequencing revealed highly recurrent so...

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Main Authors: Geyer, Felipe C., Li, Anqi, Papanastasiou, Anastasios D., Smith, Alison, Selenica, Pier, Burke, Kathleen A., Edelweiss, Marcia, Wen, Huei-Chi, Piscuoglio, Salvatore, Schultheis, Anne M., Martelotto, Luciano G., Pareja, Fresia, Brandes, Alissa, Lozada, John, Macedo, Gabriel S., de Filippo, Maria R., Jungbluth, Achim A., Foschini, Maria Pia, Wen, Hannah Y., Brogi, Edi, Palazzo, Juan, Rubin, Brian P., Ng, Charlotte K.Y., Norton, Larry, Rakha, Emad A., Varga, Zsuzsanna, Ellis, Ian O., Chandarlapaty, Sarat, Weigelt, Britta, Reis-Filho, Jorge S.
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Published: Nature Publishing Group 2018
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Online Access:https://eprints.nottingham.ac.uk/51065/
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author Geyer, Felipe C.
Li, Anqi
Papanastasiou, Anastasios D.
Smith, Alison
Selenica, Pier
Burke, Kathleen A.
Edelweiss, Marcia
Wen, Huei-Chi
Piscuoglio, Salvatore
Schultheis, Anne M.
Martelotto, Luciano G.
Pareja, Fresia
Brandes, Alissa
Lozada, John
Macedo, Gabriel S.
de Filippo, Maria R.
Jungbluth, Achim A.
Foschini, Maria Pia
Wen, Hannah Y.
Brogi, Edi
Palazzo, Juan
Rubin, Brian P.
Ng, Charlotte K.Y.
Norton, Larry
Rakha, Emad A.
Varga, Zsuzsanna
Ellis, Ian O.
Chandarlapaty, Sarat
Weigelt, Britta
Reis-Filho, Jorge S.
author_facet Geyer, Felipe C.
Li, Anqi
Papanastasiou, Anastasios D.
Smith, Alison
Selenica, Pier
Burke, Kathleen A.
Edelweiss, Marcia
Wen, Huei-Chi
Piscuoglio, Salvatore
Schultheis, Anne M.
Martelotto, Luciano G.
Pareja, Fresia
Brandes, Alissa
Lozada, John
Macedo, Gabriel S.
de Filippo, Maria R.
Jungbluth, Achim A.
Foschini, Maria Pia
Wen, Hannah Y.
Brogi, Edi
Palazzo, Juan
Rubin, Brian P.
Ng, Charlotte K.Y.
Norton, Larry
Rakha, Emad A.
Varga, Zsuzsanna
Ellis, Ian O.
Chandarlapaty, Sarat
Weigelt, Britta
Reis-Filho, Jorge S.
author_sort Geyer, Felipe C.
building Nottingham Research Data Repository
collection Online Access
description Adenomyoepithelioma of the breast is a rare tumor characterized by epithelial-myoepithelial differentiation, of which a subset will progress to invasive or metastatic cancer. We sought to define the genomic landscape of adenomyoepitheliomas. Massively parallel sequencing revealed highly recurrent somatic mutations in HRAS and PI3K-AKT pathway-related genes. Strikingly, HRAS mutations were restricted to estrogen receptor (ER)-negative tumors, all affected codon 61, and all but one co-occurred with PIK3CA or PIK3R1 mutations. To interrogate the functional significance of HRAS Q61 mutations in adenomyoepithelial differentiation, we expressed HRASQ61R alone or in combination with PIK3CAH1047R in non-transformed ER-negative breast epithelial cells. HRASQ61R induced characteristic phenotypes of adenomyoepitheliomas such as the expression of myoepithelial markers and loss of e-cadherin, hyperactivation of AKT signaling, and transformative properties that were arrested by combination therapy with AKT and MEK inhibitors. Our results indicate that breast adenomyoepitheliomas often manifest a unique transformation program featuring HRAS activation.
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spelling nottingham-510652020-05-04T19:35:41Z https://eprints.nottingham.ac.uk/51065/ Recurrent hotspot mutations in HRAS Q61 and PI3K-AKT pathway genes as drivers of breast adenomyoepitheliomas Geyer, Felipe C. Li, Anqi Papanastasiou, Anastasios D. Smith, Alison Selenica, Pier Burke, Kathleen A. Edelweiss, Marcia Wen, Huei-Chi Piscuoglio, Salvatore Schultheis, Anne M. Martelotto, Luciano G. Pareja, Fresia Brandes, Alissa Lozada, John Macedo, Gabriel S. de Filippo, Maria R. Jungbluth, Achim A. Foschini, Maria Pia Wen, Hannah Y. Brogi, Edi Palazzo, Juan Rubin, Brian P. Ng, Charlotte K.Y. Norton, Larry Rakha, Emad A. Varga, Zsuzsanna Ellis, Ian O. Chandarlapaty, Sarat Weigelt, Britta Reis-Filho, Jorge S. Adenomyoepithelioma of the breast is a rare tumor characterized by epithelial-myoepithelial differentiation, of which a subset will progress to invasive or metastatic cancer. We sought to define the genomic landscape of adenomyoepitheliomas. Massively parallel sequencing revealed highly recurrent somatic mutations in HRAS and PI3K-AKT pathway-related genes. Strikingly, HRAS mutations were restricted to estrogen receptor (ER)-negative tumors, all affected codon 61, and all but one co-occurred with PIK3CA or PIK3R1 mutations. To interrogate the functional significance of HRAS Q61 mutations in adenomyoepithelial differentiation, we expressed HRASQ61R alone or in combination with PIK3CAH1047R in non-transformed ER-negative breast epithelial cells. HRASQ61R induced characteristic phenotypes of adenomyoepitheliomas such as the expression of myoepithelial markers and loss of e-cadherin, hyperactivation of AKT signaling, and transformative properties that were arrested by combination therapy with AKT and MEK inhibitors. Our results indicate that breast adenomyoepitheliomas often manifest a unique transformation program featuring HRAS activation. Nature Publishing Group 2018-05-08 Article PeerReviewed Geyer, Felipe C., Li, Anqi, Papanastasiou, Anastasios D., Smith, Alison, Selenica, Pier, Burke, Kathleen A., Edelweiss, Marcia, Wen, Huei-Chi, Piscuoglio, Salvatore, Schultheis, Anne M., Martelotto, Luciano G., Pareja, Fresia, Brandes, Alissa, Lozada, John, Macedo, Gabriel S., de Filippo, Maria R., Jungbluth, Achim A., Foschini, Maria Pia, Wen, Hannah Y., Brogi, Edi, Palazzo, Juan, Rubin, Brian P., Ng, Charlotte K.Y., Norton, Larry, Rakha, Emad A., Varga, Zsuzsanna, Ellis, Ian O., Chandarlapaty, Sarat, Weigelt, Britta and Reis-Filho, Jorge S. (2018) Recurrent hotspot mutations in HRAS Q61 and PI3K-AKT pathway genes as drivers of breast adenomyoepitheliomas. Nature Communications, 9 . 1816/1-1816/16. ISSN 2041-1723 epithelial-myoepithelial carcinoma breast cancer copy number variation single nucleotide variant RNA-sequencing whole-exome sequencing doi:10.1038/s41467-018-04128-5 doi:10.1038/s41467-018-04128-5
spellingShingle epithelial-myoepithelial carcinoma
breast cancer
copy number variation
single nucleotide variant
RNA-sequencing
whole-exome sequencing
Geyer, Felipe C.
Li, Anqi
Papanastasiou, Anastasios D.
Smith, Alison
Selenica, Pier
Burke, Kathleen A.
Edelweiss, Marcia
Wen, Huei-Chi
Piscuoglio, Salvatore
Schultheis, Anne M.
Martelotto, Luciano G.
Pareja, Fresia
Brandes, Alissa
Lozada, John
Macedo, Gabriel S.
de Filippo, Maria R.
Jungbluth, Achim A.
Foschini, Maria Pia
Wen, Hannah Y.
Brogi, Edi
Palazzo, Juan
Rubin, Brian P.
Ng, Charlotte K.Y.
Norton, Larry
Rakha, Emad A.
Varga, Zsuzsanna
Ellis, Ian O.
Chandarlapaty, Sarat
Weigelt, Britta
Reis-Filho, Jorge S.
Recurrent hotspot mutations in HRAS Q61 and PI3K-AKT pathway genes as drivers of breast adenomyoepitheliomas
title Recurrent hotspot mutations in HRAS Q61 and PI3K-AKT pathway genes as drivers of breast adenomyoepitheliomas
title_full Recurrent hotspot mutations in HRAS Q61 and PI3K-AKT pathway genes as drivers of breast adenomyoepitheliomas
title_fullStr Recurrent hotspot mutations in HRAS Q61 and PI3K-AKT pathway genes as drivers of breast adenomyoepitheliomas
title_full_unstemmed Recurrent hotspot mutations in HRAS Q61 and PI3K-AKT pathway genes as drivers of breast adenomyoepitheliomas
title_short Recurrent hotspot mutations in HRAS Q61 and PI3K-AKT pathway genes as drivers of breast adenomyoepitheliomas
title_sort recurrent hotspot mutations in hras q61 and pi3k-akt pathway genes as drivers of breast adenomyoepitheliomas
topic epithelial-myoepithelial carcinoma
breast cancer
copy number variation
single nucleotide variant
RNA-sequencing
whole-exome sequencing
url https://eprints.nottingham.ac.uk/51065/
https://eprints.nottingham.ac.uk/51065/