<p>Resistance to cyclin-dependent kinase 4/6 (CDK4/CDK6) inhibitors leads to treatment failure and disease progression in women with hormone receptor<sup>+</sup>HER2<sup>−</sup> (HR<sup>+</sup>HER2<sup>−</sup>) breast cancer (BC). We delineated a hypoxia-sensitive, CCL2-dependent pathway recruiting interleukin-17A (IL-17A)-secreting γδ T cells to mouse HR<sup>+</sup>HER2<sup>−</sup> BCs following CDK4/CDK6 inhibition, resulting in repolarization of tumor-associated macrophages (TAMs) toward an immunosuppressive CX3CR1<sup>+</sup> phenotype associated with resistance. Increased IL-17A signaling and intratumoral γδ T cell abundance positively correlated with advanced grade and/or reduced survival in two cohorts of individuals with HR<sup>+</sup>HER2<sup>−</sup> BC. Circulating γδ T cells and plasma CCL2 levels negatively correlated with progression in an independent series of individuals with HR<sup>+</sup>HER2<sup>−</sup> BC receiving CDK4/CDK6 inhibitors. Intratumoral γδ T cells were increased in post- versus pretreatment biopsies from individuals with HR<sup>+</sup>HER2<sup>−</sup> BC relapsing on CDK4/CDK6 inhibitors. CX3CR1<sup>+</sup> TAMs had negative prognostic impact in women with HR<sup>+</sup>HER2<sup>−</sup> BC receiving neoadjuvant PD-1 blockage and radiotherapy. Thus, γδ T cells and CX3XR1<sup>+</sup> TAMs may favor resistance to CDK4/CDK6 inhibitors in individuals with HR<sup>+</sup>HER2<sup>−</sup> BC.</p>

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IL-17A-secreting γδ T cells promote resistance to CDK4/CDK6 inhibitors in HR+HER2 breast cancer via CX3CR1+ macrophages

  • Giulia Petroni,
  • Claudia Galassi,
  • Kenneth H. Gouin III,
  • Hsiang-Han Chen,
  • Aitziber Buqué,
  • Norma Bloy,
  • Takahiro Yamazaki,
  • Ai Sato,
  • Manuel Beltrán-Visiedo,
  • Ginevra Campia,
  • Carlos Jiménez-Cortegana,
  • Aagam Shah,
  • Alexander Kirchmair,
  • Chiara Massa,
  • Claudia Wickenhauser,
  • Carlos Eduardo de Andrea,
  • Belén Navarro-Rubio,
  • Irantzu Serrano-Mendioroz,
  • Esther Navarro Manzano,
  • Alexandra M. Satty,
  • Brady Rippon,
  • Francesca Finotello,
  • Zlatko Trajanoski,
  • Xi Kathy Zhou,
  • Joseph M. Scandura,
  • Elena García-Martínez,
  • Francisco Ayala de la Peña,
  • María Esperanza Rodríguez-Ruiz,
  • Barbara Seliger,
  • Víctor Sánchez-Margalet,
  • Luis de la Cruz-Merino,
  • Reva K. Basho,
  • Stephen L. Shiao,
  • Heather L. McArthur,
  • Silvia C. Formenti,
  • Simon R. V. Knott,
  • Lorenzo Galluzzi

摘要

Resistance to cyclin-dependent kinase 4/6 (CDK4/CDK6) inhibitors leads to treatment failure and disease progression in women with hormone receptor+HER2 (HR+HER2) breast cancer (BC). We delineated a hypoxia-sensitive, CCL2-dependent pathway recruiting interleukin-17A (IL-17A)-secreting γδ T cells to mouse HR+HER2 BCs following CDK4/CDK6 inhibition, resulting in repolarization of tumor-associated macrophages (TAMs) toward an immunosuppressive CX3CR1+ phenotype associated with resistance. Increased IL-17A signaling and intratumoral γδ T cell abundance positively correlated with advanced grade and/or reduced survival in two cohorts of individuals with HR+HER2 BC. Circulating γδ T cells and plasma CCL2 levels negatively correlated with progression in an independent series of individuals with HR+HER2 BC receiving CDK4/CDK6 inhibitors. Intratumoral γδ T cells were increased in post- versus pretreatment biopsies from individuals with HR+HER2 BC relapsing on CDK4/CDK6 inhibitors. CX3CR1+ TAMs had negative prognostic impact in women with HR+HER2 BC receiving neoadjuvant PD-1 blockage and radiotherapy. Thus, γδ T cells and CX3XR1+ TAMs may favor resistance to CDK4/CDK6 inhibitors in individuals with HR+HER2 BC.