Daugherty-Lopès Amélie, Pérez-Guijarro Eva, Gopalan Vishaka, Rappaport Jessica, Chen Quanyi, Huang April, Lam Khiem C, Chin Sung, Ebersole Jessica, Wu Emily, Needle Gabriel A, Church Isabella, Kyriakopoulos George, Xie Shaojun, Zhao Yongmei, Gruen Charli, Sassano Antonella, Araya Romina E, Thorkelsson Andres, Smith Cari, Lee Maxwell P, Hannenhalli Sridhar, Day Chi-Ping, Merlino Glenn, Goldszmid Romina S
Inflammatory Cell Dynamics Section, Laboratory of Integrative Cancer Immunology, Center for Cancer Research, National Cancer Institute, NIH, Bethesda, MD 20892, USA.
Laboratory of Cancer Biology and Genetics, Center for Cancer Research, National Cancer Institute, NIH, Bethesda, MD 20892, USA.
bioRxiv. 2024 Oct 9:2024.08.26.609785. doi: 10.1101/2024.08.26.609785.
Despite the promising results of immune checkpoint blockade (ICB) therapy, outcomes for patients with brain metastasis (BrM) remain poor. Identifying resistance mechanisms has been hindered by limited access to patient samples and relevant preclinical models. Here, we developed two mouse melanoma BrM models that recapitulate the disparate responses to ICB seen in patients. We demonstrate that these models capture the cellular and molecular complexity of human disease and reveal key factors shaping the tumor microenvironment and influencing ICB response. BR1-responsive tumor cells express inflammatory programs that polarize microglia into reactive states, eliciting robust T cell recruitment. In contrast, BR3-resistant melanoma cells are enriched in neurological programs and exploit tolerance mechanisms to maintain microglia homeostasis and limit T cell infiltration. In humans, BR1 and BR3 expression signatures correlate positively or negatively with T cell infiltration and BrM patient outcomes, respectively. Our study provides clinically relevant models and uncovers mechanistic insights into BrM ICB responses, offering potential biomarkers and therapeutic targets to improve therapy efficacy.
尽管免疫检查点阻断(ICB)疗法取得了令人鼓舞的结果,但脑转移(BrM)患者的预后仍然很差。获取患者样本和相关临床前模型的机会有限,阻碍了对耐药机制的识别。在此,我们开发了两种小鼠黑色素瘤脑转移模型,它们概括了患者对ICB的不同反应。我们证明,这些模型捕捉到了人类疾病的细胞和分子复杂性,并揭示了塑造肿瘤微环境和影响ICB反应的关键因素。对BR1有反应的肿瘤细胞表达炎症程序,使小胶质细胞极化为反应性状态,引发强大的T细胞募集。相比之下,对BR3耐药的黑色素瘤细胞在神经程序方面富集,并利用耐受机制维持小胶质细胞稳态并限制T细胞浸润。在人类中,BR1和BR3表达特征分别与T细胞浸润和BrM患者的预后呈正相关或负相关。我们的研究提供了临床相关模型,并揭示了对BrM ICB反应的机制性见解,为提高治疗效果提供了潜在的生物标志物和治疗靶点。