Public Health Sciences Division/Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Graduate Program in Molecular and Cellular Biology, University of Washington, Seattle, WA, USA.
Nat Cell Biol. 2022 Apr;24(4):538-553. doi: 10.1038/s41556-022-00881-4. Epub 2022 Apr 11.
Skeletal muscle has long been recognized as an inhospitable site for disseminated tumour cells (DTCs). Yet its antimetastatic nature has eluded a thorough mechanistic examination. Here, we show that DTCs traffic to and persist within skeletal muscle in mice and in humans, which raises the question of how this tissue suppresses colonization. Results from mouse and organotypic culture models along with metabolomic profiling suggested that skeletal muscle imposes a sustained oxidative stress on DTCs that impairs their proliferation. Functional studies demonstrated that disrupting reduction-oxidation homeostasis via chemogenetic induction of reactive oxygen species slowed proliferation in a more fertile organ: the lung. Conversely, enhancement of the antioxidant potential of tumour cells through ectopic expression of catalase in the tumour or host mitochondria allowed robust colonization of skeletal muscle. These findings reveal a profound metabolic bottleneck imposed on DTCs and sustained by skeletal muscle. A thorough understanding of this biology could reveal previously undocumented DTC vulnerabilities that can be exploited to prevent metastasis in other more susceptible tissues.
骨骼肌一直被认为是转移性肿瘤细胞(DTCs)不易扩散的部位。然而,其抗转移的性质尚未得到彻底的机制研究。在这里,我们表明 DTCs 在小鼠和人类中迁移到并存在于骨骼肌中,这就提出了一个问题,即这种组织如何抑制定植。来自小鼠和器官型培养模型以及代谢组学分析的结果表明,骨骼肌对 DTCs 施加持续的氧化应激,从而损害其增殖。功能研究表明,通过化学遗传学诱导活性氧来破坏氧化还原稳态会在更肥沃的器官(肺)中减缓增殖。相反,通过在肿瘤或宿主线粒体中外源表达过氧化氢酶来增强肿瘤细胞的抗氧化能力,可以使骨骼肌大量定植。这些发现揭示了骨骼肌对 DTCs 施加的深刻代谢瓶颈,并使其得以维持。对这种生物学的深入了解可能会揭示以前未记录的 DTC 脆弱性,从而可以利用这些脆弱性来防止其他更易受影响的组织中的转移。