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Genomic profiling of mitochondrion-rich breast carcinoma: chromosomal changes may be relevant for mitochondria accumulation and tumour biology

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Abstract

Oncocytic carcinomas are composed of mitochondrion-rich cells. Though recognised by the WHO classification as a histological special type of breast cancer, their status as a discrete pathological entity remains a matter of contention. Given that oncocytic tumours of other anatomical sites display distinct clinico-pathological and molecular features, we sought to define the molecular genetic features of mitochondrion-rich breast tumours and to compare them with a series of histological grade- and oestrogen receptor status-matched invasive ductal carcinomas of no special type. Seventeen mitochondrion-rich breast carcinomas, including nine bona fide oncocytic carcinomas, were profiled with antibodies against oestrogen, progesterone and androgen receptors, HER2, Ki67, GCDFP-15, chromogranin, epithelial membrane antigen, cytokeratin 7, cytokeratin 14, CD68 and mitochondria antigen. These tumours were microdissected and DNA extracted from samples with >70% of tumour cells. Fourteen cases yielded DNA of sufficient quality/quantity and were subjected to high-resolution microarray comparative genomic hybridisation analysis. The genomic profiles were compared to those of 28 grade- and oestrogen receptor status-matched invasive ductal carcinomas of no special type. Oncocytic and other mitochondrion-rich tumours did not differ significantly between themselves. As a group, mitochondrion-rich carcinomas were immunophenotypically heterogenous. Recurrent copy number changes were similar to those described in unselected breast cancers. However, unsupervised and supervised analysis identified a subset of mitochondrion-rich cancers, which often displayed gains of 11q13.1-q13.2 and 19p13. Changes in the latter two chromosomal regions have been shown to be associated with oncocytic tumours of the kidney and thyroid, respectively, and host several nuclear genes with specific mitochondrial function. Our results indicate that in a way akin to oncocytic tumours of other anatomical sites, at least a subset of mitochondrion-rich breast carcinomas may be underpinned by a distinct pattern of chromosomal changes potentially relevant for mitochondria accumulation and constitute a discrete molecular entity.

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Acknowledgments

This study was funded by the Breakthrough Breast Cancer Research Centre and by the University of Bologna School of Medicine-Dipartimento di Ematologia e Scienze Oncologiche “L. e A. Seràgnoli”; the study was also supported in part by a research AIRC regional grant (code 1145) to GT and by Italian Government research grants to GT (Ricerca Fondamentale Orientata, number 20074zw8la) and GG (FIRB-’Futuro in Ricerca’ J31J10000040001); DdB was the recipient of a fellowship from the Centro Interdipartimentale di Ricerca sul Cancro “G. Prodi” (CIRC), University of Bologna.

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The authors have no conflicts of interest to declare.

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Authors and Affiliations

  1. The Breakthrough Breast Cancer Research Centre, ICR, 237 Fulham Road, London, SW3 6JB, UK

    Felipe C. Geyer, Dario de Biase, Maryou B. K. Lambros, Maria A. Lopez-Garcia, Rachael Natrajan, Alan Mackay, Alan Ashworth & Jorge S. Reis-Filho

  2. Sezione Anatomia Patologica “M. Malpighi”, Ospedale Bellaria, University of Bologna School of Medicine, Via Altura 3, 40139, Bologna, Italy

    Dario de Biase, Moira Ragazzi, Vincenzo Eusebi & Giovanni Tallini

  3. Hospital Universitario Virgen del Rocio, Seville, Spain

    Maria A. Lopez-Garcia

  4. Unità di Genetica Medica, Dip. Scienze Ginecologiche, Ostetriche e Pediatriche, Policlinico Universitario S. Orsola-Malpighi, University of Bologna School of Medicine, Bologna, Italy

    Ivana Kurelac & Giuseppe Gasparre

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  1. Felipe C. Geyer
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  2. Dario de Biase
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  11. Vincenzo Eusebi
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  12. Jorge S. Reis-Filho
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Correspondence to Jorge S. Reis-Filho or Giovanni Tallini.

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Felipe C. Geyer and Dario de Biase contributed equally to this work. Jorge S. Reis-Filho and Giovanni Tallini contributed equally to this work.

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Geyer, F.C., de Biase, D., Lambros, M.B.K. et al. Genomic profiling of mitochondrion-rich breast carcinoma: chromosomal changes may be relevant for mitochondria accumulation and tumour biology. Breast Cancer Res Treat 132, 15–28 (2012). https://doi.org/10.1007/s10549-011-1504-4

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