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Genomic studies have identified a clonal relationship between ILC and concurrent lobular carcinoma <jats:italic>in situ<\/jats:italic> (LCIS) lesions, suggesting that LCIS may be a precursor lesion. It has been shown that an LCIS diagnosis confers a 15\u201320% risk of progression to ILC over a lifetime. Currently no molecular test or markers can identify LCIS lesions likely to progress to ILC. Since microRNA (miRNA) expression changes have been detected in a number of other cancer types, we explored whether their dysregulation might be detected during progression from LCIS to ILC. Using the Illumina miRNA profiling platform, designed for simultaneous analysis of 470 mature miRNAs, we analysed the profiles of archived normal breast epithelium, LCIS lesions found alone, LCIS lesions concurrent with ILC, and the concurrent ILCs as a model of linear histological progression towards ILC. We identified two sets of differentially expressed miRNAs, the first set highly expressed in normal epithelium, including hsa\u2010miR\u2010224, \u2010139, \u201010b, \u2010450, 140, and \u2010365, and the second set up\u2010regulated during lobular neoplasia progression, including hsa\u2010miR\u2010375, \u2010203, \u2010425\u20105p, \u2010183, \u2010565, and \u2010182. Using quantitative RT\u2010PCR, we validated a trend of increasing expression for hsa\u2010miR\u2010375, hsa\u2010miR\u2010182, and hsa\u2010miR\u2010183 correlating with ILC progression. As we detected increased expression of hsa\u2010miR\u2010375 in LCIS lesions synchronous with ILC, we sought to determine whether hsa\u2010miR\u2010375 might induce phenotypes reminiscent of lobular neoplasia by expressing it in the MCF\u201010A 3D culture model of mammary acinar morphogenesis. Increased expression of hsa\u2010miR\u2010375 resulted in loss of cellular organization and acquisition of a hyperplastic phenotype. These data suggest that dysregulated miRNA expression contributes to lobular neoplastic progression. Copyright \u00a9 2011 Pathological Society of Great Britain and Ireland. 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