Guerini-Rocco Elena, Piscuoglio Salvatore, Ng Charlotte K Y, Geyer Felipe C, De Filippo Maria R, Eberle Carey A, Akram Muzaffar, Fusco Nicola, Ichihara Shu, Sakr Rita A, Yatabe Yasushi, Vincent-Salomon Anne, Rakha Emad A, Ellis Ian O, Wen Y Hannah, Weigelt Britta, Schnitt Stuart J, Reis-Filho Jorge S
Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Department of Pathology, European Institute of Oncology, Milan, Italy.
J Pathol. 2016 Apr;238(5):677-88. doi: 10.1002/path.4691.
Microglandular adenosis (MGA) is a rare proliferative lesion of the breast composed of small glands lacking myoepithelial cells and lined by S100-positive, oestrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative epithelial cells. There is evidence to suggest that MGA may constitute a non-obligate precursor of triple-negative breast cancer (TNBC). We sought to define the genomic landscape of pure MGA and of MGA, atypical MGA (AMGA) and associated TNBCs, and to determine whether synchronous MGA, AMGA, and TNBCs would be clonally related. Two pure MGAs and eight cases of MGA and/or AMGA associated with in situ or invasive TNBC were collected, microdissected, and subjected to massively parallel sequencing targeting all coding regions of 236 genes recurrently mutated in breast cancer or related to DNA repair. Pure MGAs lacked clonal non-synonymous somatic mutations and displayed limited copy number alterations (CNAs); conversely, all MGAs (n = 7) and AMGAs (n = 3) associated with TNBC harboured at least one somatic non-synonymous mutation (range 3-14 and 1-10, respectively). In all cases where TNBCs were analyzed, identical TP53 mutations and similar patterns of gene CNAs were found in the MGA and/or AMGA and in the associated TNBC. In the MGA/AMGA associated with TNBC lacking TP53 mutations, somatic mutations affecting PI3K pathway-related genes (eg PTEN, PIK3CA, and INPP4B) and tyrosine kinase receptor signalling-related genes (eg ERBB3 and FGFR2) were identified. At diagnosis, MGAs associated with TNBC were found to display subclonal populations, and clonal shifts in the progression from MGA to AMGA and/or to TNBC were observed. Our results demonstrate the heterogeneity of MGAs, and that MGAs associated with TNBC, but not necessarily pure MGAs, are genetically advanced, clonal, and neoplastic lesions harbouring recurrent mutations in TP53 and/or other cancer genes, supporting the notion that a subset of MGAs and AMGAs may constitute non-obligate precursors of TNBCs.
微腺性腺病(MGA)是一种罕见的乳腺增殖性病变,由缺乏肌上皮细胞的小腺体组成,内衬S100阳性、雌激素受体(ER)阴性、孕激素受体(PR)阴性和HER2阴性的上皮细胞。有证据表明,MGA可能是三阴性乳腺癌(TNBC)的非必需前体。我们试图确定纯MGA以及MGA、非典型MGA(AMGA)和相关TNBC的基因组图谱,并确定同步发生的MGA、AMGA和TNBC是否存在克隆相关性。收集了两例纯MGA以及八例与原位或浸润性TNBC相关的MGA和/或AMGA,进行显微切割,并对236个在乳腺癌中反复突变或与DNA修复相关的基因的所有编码区进行大规模平行测序。纯MGA缺乏克隆性非同义体细胞突变,且拷贝数改变(CNA)有限;相反,所有与TNBC相关的MGA(n = 7)和AMGA(n = 3)至少含有一个体细胞非同义突变(分别为3 - 14个和1 - 10个)。在所有分析TNBC的病例中,在MGA和/或AMGA以及相关TNBC中发现了相同的TP53突变和相似的基因CNA模式。在与缺乏TP53突变的TNBC相关的MGA/AMGA中,鉴定出影响PI3K途径相关基因(如PTEN、PIK3CA和INPP4B)和酪氨酸激酶受体信号传导相关基因(如ERBB3和FGFR2)的体细胞突变。在诊断时,发现与TNBC相关的MGA显示出亚克隆群体,并且观察到从MGA进展到AMGA和/或TNBC过程中的克隆转变。我们的结果证明了MGA的异质性,并且与TNBC相关的MGA(但不一定是纯MGA)是具有遗传进展、克隆性且在TP53和/或其他癌症基因中存在反复突变的肿瘤性病变,支持了一部分MGA和AMGA可能是TNBC非必需前体的观点。