Combination inhibition of PI 3 K and mTORC 1 yields durable remissions in mice bearing orthotopic patient-derived xenografts of HER 2-positive breast cancer brain metastases

nature medicine To develop therapeutic strategies for HER2-positive BCBM, we established a panel of orthotopic PDXs (Fig. 1a). Fresh BCBMs from two patients, Dana-Farber Brain Metastasis (DF-BM)354 and DF-BM355, were grafted directly into the brains of SCID mice with a median survival of roughly 2–3 months (Supplementary Fig. 1). The PDXs resembled the parental BCBMs histologically, as well in their estrogen receptor (ER), progesterone receptor (PR) and HER2 expression (Fig. 1b). We also verified the expression of epithelial marker cytokeratin 7 (CK7) and the absence of glial markers (GFAP and OLIG2) (Fig. 1b). We subsequently established PDXs by using BCBMs from three other patients with HER2-positive BCBM. None of the five PDXs expressed detectable levels of the tumor suppressor protein PTEN (Fig. 1b and Supplementary Table 1). Of 27 clinical specimens of HER2-positive BCBMs, 67% showed no PTEN staining (Fig. 1c), which further confirms that the loss of PTEN is widespread in BCBMs1,2. To assess the response of HER2-positive BCBMs to targeted therapy, we treated DF-BM355 PDXs with a HER2 kinase inhibitor lapatinib. DF-BM355 PDXs showed no response to lapatinib, which is consistent with the resistance of the donor’s tumor to HER2-directed therapy (Supplementary Fig. 2a,b). Because DF-BM355 lacks PTEN—a key regulator of the PI3K pathway—we tested the combination of lapatinib with BKM120, a pan-PI3K inhibitor that penetrates the blood–brain barrier (BBB)3–5. Again, no response was observed (Supplementary Fig. 2a,b). To understand the lack of response to combined inhibition with HER2 and PI3K, we assessed tumor PI3K-pathway signaling in response to lapatinib and/or BKM120. Although, as compared to the control, these treatments reduced the phosphorlyation of AKT and S6RP—the downstream effectors of PI3K and mTOR, respectively— we observed little change in p-4EBP1, an mTORC1 effector that mediates translation (Supplementary Fig. 2c,d). Even combined HER2 and PI3K inhibition therefore did not completely suppress mTORC1 activity in the DF-BM355 model. Notably, persistent mTOR activity in breast cancers can mediate resistance to PI3K inhibition, and this can be overcome by inhibition with mTORC1 (ref. 6). However, the brain microenvironment is unique, and brain metastases are notoriously refractory to systemic therapies that are effective against extracranial metastases. In keeping with this, it is not known whether mTOR inhibition might overcome PI3K-inhibitor resistance in BCBMs. To explore this, we combined either lapatinib or BKM120 with RAD001, an mTORC1 inhibitor that penetrates the BBB7,8. Whereas DF-BM355 PDXs showed limited response to the combination of lapatinib and RAD001 (Supplementary Fig. 2e), the administration of BKM120 and RAD001 together resulted in marked tumor regression, as measured by bioluminescence (Fig. 2a). Owing to the unprecedented nature of this response, we removed two mice from the control group bearing large tumors, and introduced BKM120 and RAD001. The large tumors also regressed over time (Fig. 2a). Magnetic resonance imaging (MRI) before and after treatment confirmed these results (Fig. 2b). The remaining mice in the control group quickly reached the study endpoint (developing systemic Combination inhibition of PI3K and mTORC1 yields durable remissions in mice bearing orthotopic patient-derived xenografts of HER2-positive breast cancer brain metastases