Dual Targeting of CDK4/6 and BCL2 Pathways Augments Tumor Response in Estrogen Receptor-Positive Breast Cancer

Clin Cancer Res. 2020 Aug 1;26(15):4120-4134. doi: 10.1158/1078-0432.CCR-19-1872. Epub 2020 Apr 3.

Abstract

Purpose: Although cyclin-dependent kinase 4 and 6 (CDK4/6) inhibitors significantly extend tumor response in patients with metastatic estrogen receptor-positive (ER+) breast cancer, relapse is almost inevitable. This may, in part, reflect the failure of CDK4/6 inhibitors to induce apoptotic cell death. We therefore evaluated combination therapy with ABT-199 (venetoclax), a potent and selective BCL2 inhibitor.

Experimental design: BCL2 family member expression was assessed following treatment with endocrine therapy and the CDK4/6 inhibitor palbociclib. Functional assays were used to determine the impact of adding ABT-199 to fulvestrant and palbociclib in ER+ breast cancer cell lines, patient-derived organoid (PDO), and patient-derived xenograft (PDX) models. A syngeneic ER+ mouse mammary tumor model was used to study the effect of combination therapy on the immune system.

Results: Triple therapy was well tolerated and produced a superior and more durable tumor response compared with single or doublet therapy. This was associated with marked apoptosis, including of senescent cells, indicative of senolysis. Unexpectedly, ABT-199 resulted in Rb dephosphorylation and reduced G1-S cyclins, most notably at high doses, thereby intensifying the fulvestrant/palbociclib-induced cell-cycle arrest. Interestingly, a CRISPR/Cas9 screen suggested that ABT-199 could mitigate loss of Rb (and potentially other mechanisms of acquired resistance) to palbociclib. ABT-199 did not abrogate the favorable immunomodulatory effects of palbociclib in a syngeneic ER+ mammary tumor model and extended tumor response when combined with anti-PD1 therapy.

Conclusions: This study illustrates the potential for targeting BCL2 in combination with CDK4/6 inhibitors and supports investigation of combination therapy in ER+ breast cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • Apoptosis / drug effects
  • Breast / pathology
  • Breast / surgery
  • Breast Neoplasms / pathology
  • Breast Neoplasms / therapy*
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology
  • Bridged Bicyclo Compounds, Heterocyclic / therapeutic use
  • Cell Line, Tumor
  • Chemotherapy, Adjuvant / methods
  • Cyclin-Dependent Kinase 4 / antagonists & inhibitors
  • Cyclin-Dependent Kinase 6 / antagonists & inhibitors
  • Disease Models, Animal
  • Drug Resistance, Neoplasm / drug effects
  • Female
  • Fulvestrant / pharmacology
  • Fulvestrant / therapeutic use
  • Humans
  • Mastectomy
  • Mice
  • Middle Aged
  • Neoadjuvant Therapy / methods*
  • Organoids
  • Piperazines / pharmacology
  • Piperazines / therapeutic use
  • Primary Cell Culture
  • Protein Kinase Inhibitors / pharmacology
  • Protein Kinase Inhibitors / therapeutic use*
  • Proto-Oncogene Proteins c-bcl-2 / antagonists & inhibitors*
  • Pyridines / pharmacology
  • Pyridines / therapeutic use
  • Receptors, Estrogen / analysis
  • Receptors, Estrogen / metabolism
  • Sulfonamides / pharmacology
  • Sulfonamides / therapeutic use
  • Xenograft Model Antitumor Assays

Substances

  • BCL2 protein, human
  • Bridged Bicyclo Compounds, Heterocyclic
  • Piperazines
  • Protein Kinase Inhibitors
  • Proto-Oncogene Proteins c-bcl-2
  • Pyridines
  • Receptors, Estrogen
  • Sulfonamides
  • Fulvestrant
  • CDK4 protein, human
  • CDK6 protein, human
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase 6
  • palbociclib
  • venetoclax