HIF-2 Complex Dissociation, Target Inhibition, and Acquired Resistance with PT2385, a First-in-Class HIF-2 Inhibitor in Clear Cell Renal Cell Carcinoma Patients.

The heterodimeric transcription factor HIF-2 is arguably the most important driver of clear cell renal cell carcinoma (ccRCC). While considered undruggable, structural analyses at UT Southwestern Medical Center (UTSW) identified a vulnerability in the a subunit, which heterodimerizes with HIF-1b, ultimately leading to the development of PT2385, a first-in-class inhibitor. PT2385 was safe and active in a first-in-human phase I clinical trial of extensively pretreated ccRCC patients at UTSW and elsewhere. There were no dose-limiting toxicities, and disease control greater than or equal to 4 months was achieved in 42% of patients.

We conducted a prospective companion sub-study involving a subset of patients enrolled in the phase I clinical trial at UTSW (n=10), who were treated at the phase II dose or above, involving multiparametric magnetic resonance imaging, blood draws and serial biopsies for biochemical, whole exome, and RNA-Seq studies.

PT2385 inhibited HIF-2 in non-tumor tissues, as determined by a reduction in erythropoietin levels (a pharmacodynamic marker), in all but one patient, who had the lowest drug concentrations. PT2385 dissociated HIF-2 complexes in ccRCC metastases, and inhibited HIF-2 target gene expression. In contrast, HIF-1 complexes were unaffected. Prolonged PT2385 treatment resulted in the acquisition of resistance, and we identified a gatekeeper mutation (G323E), which interferes with drug binding and precluded HIF-2 complex dissociation. In addition, we identified an acquired TP53 mutation elsewhere suggesting a possible alternate mechanism of resistance.

These findings demonstrate a core dependency on HIF-2 in metastatic ccRCC, and establish PT2385 as a highly specific HIF-2 inhibitor in humans.

Clinical cancer research : an official journal of the American Association for Cancer Research. 2019 Nov 14 [Epub ahead of print]

James Brugarolas, Kevin D Courtney, Yuanqing Ma, Alberto Diaz de Leon, Alana Christie, Zhiqun Xie, Layton Woolford, Nirmish Singla, Allison Joyce, Haley Hill, Ananth J Madhuranthakam, Qing Yuan, Yin Xi, Yue Zhang, Jenny Chang, Oluwatomilade Fatunde, Yull Arriaga, Arthur E Frankel, Sanjeeva Kalva, Song Zhang, Tiffani McKenzie, Oscar Reig, Robert A Figlin, Brian I Rini, Renée M McKay, Payal Kapur, Tao Wang, Ivan Pedrosa

Department of Internal Medicine, University of Texas Southwestern Medical Center ., Division of Hematology / Oncology, The University of Texas Southwestern Medical Center., Internal Medicine - Hematology-Oncology Division, University of Texas Southwestern Medical Center., Radiology, The University of Texas Southwestern Medical Center., Simmons Comprehensive Cancer Center, University of Texas Southwestern Medical Center., Department of Clinical Sciences, The University of Texas Southwestern Medical Center., Department of Urology, University of Texas Southwestern Medical Center., Internal Medicine, The University of Texas Southwestern Medical Center., Department of Radiology, University of Texas Southwestern Medical Center., U of Texas Southwestern Medical Center., Department of Internal Medicine, University of Texas Southwestern Medical Center., Physician, 617 Bishop Lane North., Radiology, University of Texas Southwestern Medical Center., Simmons Cancer Center, UT Southwestern., University of Texas Southwestern Medical Center., Medicine, Cedars-Sinai Medical Center., Hematology/Oncology, Cleveland Clinic Taussig Cancer Institute., Department of Pathology, University of Texas Southwestern Medical Center., Department of Population and Data Sciences, University of Texas Southwestern Medical Center.