Immunotherapy-related cognitive impairment after CAR T cell therapy in mice

IF 45.5 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY
Cell Pub Date : 2025-05-12 DOI:10.1016/j.cell.2025.03.041
Anna C. Geraghty, Lehi Acosta-Alvarez, Maria C. Rotiroti, Selena Dutton, Michael R. O’Dea, Wonju Kim, Vrunda Trivedi, Rebecca Mancusi, Kiarash Shamardani, Karen Malacon, Pamelyn J. Woo, Naiara Martinez-Velez, Theresa Pham, Noemi N. Reche-Ley, Gabriel Otubu, Enrique H. Castenada, Kamsi Nwangwu, Haojun Xu, Sara B. Mulinyawe, Daniel B. Zamler, Michelle Monje
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引用次数: 0

Abstract

Immunotherapies have revolutionized cancer care for many tumor types, but their potential long-term cognitive impacts are incompletely understood. Here, we demonstrated in mouse models that chimeric antigen receptor (CAR) T cell therapy for both central nervous system (CNS) and non-CNS cancers impaired cognitive function and induced a persistent CNS immune response characterized by white matter microglial reactivity, microglial chemokine expression, and elevated cerebrospinal fluid (CSF) cytokines and chemokines. Consequently, oligodendroglial homeostasis and hippocampal neurogenesis were disrupted. Single-nucleus sequencing studies of human frontal lobe from patients with or without previous CAR T cell therapy for brainstem tumors confirmed reactive states of microglia and oligodendrocytes following treatment. In mice, transient microglial depletion or CCR3 chemokine receptor blockade rescued oligodendroglial deficits and cognitive performance in a behavioral test of attention and short-term memory function following CAR T cell therapy. Taken together, these findings illustrate targetable neural-immune mechanisms underlying immunotherapy-related cognitive impairment.

Abstract Image

CAR - T细胞治疗后小鼠免疫治疗相关的认知障碍
免疫疗法已经彻底改变了许多肿瘤类型的癌症治疗,但其潜在的长期认知影响尚不完全清楚。在这里,我们在小鼠模型中证明了嵌合抗原受体(CAR) T细胞治疗中枢神经系统(CNS)和非中枢神经系统癌症会损害认知功能,并诱导持续的中枢神经系统免疫反应,其特征是白质小胶质反应性、小胶质趋化因子表达以及脑脊液(CSF)细胞因子和趋化因子升高。因此,少突胶质内平衡和海马神经发生被破坏。接受或未接受CAR - T细胞治疗的脑干肿瘤患者的人类额叶单核测序研究证实了治疗后小胶质细胞和少突胶质细胞的反应状态。在一项CAR - T细胞治疗后的小鼠注意力和短期记忆功能行为测试中,短暂性小胶质细胞耗散或CCR3趋化因子受体阻断可挽救少突胶质细胞缺陷和认知表现。综上所述,这些发现阐明了免疫治疗相关认知障碍的可靶向神经免疫机制。
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来源期刊
Cell
Cell 生物-生化与分子生物学
CiteScore
110.00
自引率
0.80%
发文量
396
审稿时长
2 months
期刊介绍: Cells is an international, peer-reviewed, open access journal that focuses on cell biology, molecular biology, and biophysics. It is affiliated with several societies, including the Spanish Society for Biochemistry and Molecular Biology (SEBBM), Nordic Autophagy Society (NAS), Spanish Society of Hematology and Hemotherapy (SEHH), and Society for Regenerative Medicine (Russian Federation) (RPO). The journal publishes research findings of significant importance in various areas of experimental biology, such as cell biology, molecular biology, neuroscience, immunology, virology, microbiology, cancer, human genetics, systems biology, signaling, and disease mechanisms and therapeutics. The primary criterion for considering papers is whether the results contribute to significant conceptual advances or raise thought-provoking questions and hypotheses related to interesting and important biological inquiries. In addition to primary research articles presented in four formats, Cells also features review and opinion articles in its "leading edge" section, discussing recent research advancements and topics of interest to its wide readership.
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