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Here, we developed a somatic CRISPR\/Cas9 mutagenesis screen to study 215 recurrent \u201clong-tail\u201d breast cancer genes, which revealed epigenetic regulation as a major tumor-suppressive mechanism. We report that components of the BAP1 and COMPASS-like complexes, including KMT2C\/D, KDM6A, BAP1, and ASXL1\/2 (\u201cEpiDrivers\u201d), cooperate with PIK3CAH1047R to transform mouse and human breast epithelial cells. Mechanistically, we find that activation of PIK3CAH1047R and concomitant EpiDriver loss triggered an alveolar-like lineage conversion of basal mammary epithelial cells and accelerated formation of luminal-like tumors, suggesting a basal origin for luminal tumors. EpiDriver mutations are found in \u223c39% of human breast cancers, and \u223c50% of ductal carcinoma in situ express casein, suggesting that lineage infidelity and alveogenic mimicry may significantly contribute to early steps of breast cancer etiology.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Significance:<\/jats:title>\n                    <jats:p>Infrequently mutated genes comprise most of the mutational burden in breast tumors but are poorly understood. In vivo CRISPR screening identified functional tumor suppressors that converged on epigenetic regulation. Loss of epigenetic regulators accelerated tumorigenesis and revealed lineage infidelity and aberrant expression of alveogenesis genes as potential early events in tumorigenesis.<\/jats:p>\n                    <jats:p>This article is highlighted in the In This Issue feature, p. 2711<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1158\/2159-8290.cd-21-0865","type":"journal-article","created":{"date-parts":[[2022,9,15]],"date-time":"2022-09-15T15:41:01Z","timestamp":1663256461000},"page":"2930-2953","update-policy":"https:\/\/doi.org\/10.1158\/crossmark_policy","source":"Crossref","is-referenced-by-count":61,"title":["Loss of Epigenetic Regulation Disrupts Lineage Integrity, Induces Aberrant Alveogenesis, and Promotes Breast Cancer"],"prefix":"10.1158","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3616-3616","authenticated-orcid":false,"given":"Ellen","family":"Langille","sequence":"first","affiliation":[{"name":"1Centre for Molecular and Systems Biology, Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada."},{"name":"2Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5771-7537","authenticated-orcid":false,"given":"Khalid N.","family":"Al-Zahrani","sequence":"additional","affiliation":[{"name":"1Centre for Molecular and Systems Biology, Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5801-0354","authenticated-orcid":false,"given":"Zhibo","family":"Ma","sequence":"additional","affiliation":[{"name":"3Gene Expression Laboratory, Salk Institute for Biological Studies, La Jolla, California."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4451-0921","authenticated-orcid":false,"given":"Minggao","family":"Liang","sequence":"additional","affiliation":[{"name":"4Hospital for Sick Children, Toronto, Ontario, Canada."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5322-5524","authenticated-orcid":false,"given":"Liis","family":"Uuskula-Reimand","sequence":"additional","affiliation":[{"name":"4Hospital for Sick Children, Toronto, Ontario, Canada."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2494-0964","authenticated-orcid":false,"given":"Roderic","family":"Espin","sequence":"additional","affiliation":[{"name":"5Program Against Cancer Therapeutic Resistance (ProCURE), Catalan Institute of Oncology (ICO), Oncobell, Bellvitge Institute for Biomedical Research (IDIBELL), L'Hospitalet del Llobregat, Barcelona, 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