Wang Kaiyuan, Ni Bo, Xie Yongjie, Li Zekun, Yuan Limei, Meng Chenyang, Zhao Tiansuo, Gao Song, Huang Chongbiao, Wang Hongwei, Ma Ying, Zhou Tianxing, Feng Yukuan, Chang Antao, Yang Chao, Yu Jun, Yu Wenwen, Zang Fenglin, Zhang Yanhui, Ji Ru-Rong, Wang Xiuchao, Hao Jihui
Department of Anesthesiology, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, State Key Laboratory of Druggability Evaluation and Systematic Translational Medicine, Tianjin Key Laboratory of Digestive Cancer, Tianjin's Clinical Research Center for Cancer, Tianjin, China.
Pancreas Center, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, State Key Laboratory of Druggability Evaluation and Systematic Translational Medicine, Tianjin Key Laboratory of Digestive Cancer, Tianjin's Clinical Research Center for Cancer, Tianjin, China.
Cell Res. 2025 May;35(5):362-380. doi: 10.1038/s41422-025-01098-4. Epub 2025 Mar 24.
The emerging field of cancer neuroscience has demonstrated great progress in revealing the crucial role of the nervous system in cancer initiation and progression. Pancreatic ductal adenocarcinoma (PDAC) is characterized by perineural invasion and modulated by autonomic (sympathetic and parasympathetic) and sensory innervations. Here, we further demonstrated that within the tumor microenvironment of PDAC, nociceptor neurons interacted with cancer-associated fibroblasts (CAFs) through calcitonin gene-related peptide (CGRP) and nerve growth factor (NGF). This interaction led to the inhibition of interleukin-15 expression in CAFs, suppressing the infiltration and cytotoxic function of natural killer (NK) cells and thereby promoting PDAC progression and cancer pain. In PDAC patients, nociceptive innervation of tumor tissue is negatively correlated with the infiltration of NK cells while positively correlated with pain intensity. This association serves as an independent prognostic factor for both overall survival and relapse-free survival for PDAC patients. Our findings highlight the crucial regulation of NK cells by nociceptor neurons through interaction with CAFs in the development of PDAC. We also propose that targeting nociceptor neurons or CGRP signaling may offer a promising therapy for PDAC and cancer pain.
癌症神经科学这一新兴领域在揭示神经系统在癌症发生和发展中的关键作用方面已取得巨大进展。胰腺导管腺癌(PDAC)的特征是神经周围浸润,并受自主神经(交感神经和副交感神经)和感觉神经支配的调节。在此,我们进一步证明,在PDAC的肿瘤微环境中,伤害感受神经元通过降钙素基因相关肽(CGRP)和神经生长因子(NGF)与癌症相关成纤维细胞(CAF)相互作用。这种相互作用导致CAF中白细胞介素-15表达受到抑制,抑制自然杀伤(NK)细胞的浸润和细胞毒性功能,从而促进PDAC进展和癌痛。在PDAC患者中,肿瘤组织的伤害性神经支配与NK细胞浸润呈负相关,而与疼痛强度呈正相关。这种关联是PDAC患者总生存期和无复发生存期的独立预后因素。我们的研究结果突出了在PDAC发展过程中,伤害感受神经元通过与CAF相互作用对NK细胞的关键调节作用。我们还提出,靶向伤害感受神经元或CGRP信号通路可能为PDAC和癌痛提供一种有前景的治疗方法。