Choi Jayoung, Park Gayoung, Lee Steve Seung-Young, Dominici Erin, Becker Lev, Macleod Kay F, Kron Stephen J, Hwang Seungmin
Department of Pathology, The University of Chicago, Chicago, IL 60637, USA.
Ludwig Center for Metastasis Research, Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL 60637, USA.
bioRxiv. 2024 Jul 16:2024.07.12.603292. doi: 10.1101/2024.07.12.603292.
Autophagy is known to suppress tumor initiation by removing genotoxic stresses in normal cells. Conversely, autophagy is also known to support tumor progression by alleviating metabolic stresses in neoplastic cells. Centered on this pro-tumor role of autophagy, there have been many clinical trials to treat cancers through systemic blocking of autophagy. Such systemic inhibition affects both tumor cells and non-tumor cells, and the consequence of blocked autophagy in non-tumor cells in the context of tumor microenvironment is relatively understudied. Here, we examined the effect of autophagy-deficient myeloid cells on the progression of autophagy-competent tumors. We found that blocking autophagy only in myeloid cells modulated tumor progression markedly but such effects were context dependent. In a tumor implantation model, the growth of implanted tumor cells was substantially reduced in mice with autophagy-deficient myeloid cells; T cells infiltrated deeper into the tumors and were responsible for the reduced growth of the implanted tumor cells. In an oncogene-driven tumor induction model, however, tumors grew faster and metastasized more in mice with autophagy-deficient myeloid cells. These data demonstrate that the autophagy status of myeloid cells plays a critical role in tumor progression, promoting or suppressing tumor growth depending on the context of tumor-myeloid cell interactions. This study indicates that systemic use of autophagy inhibitors in cancer therapy may have differential effects on rates of tumor progression in patients due to effects on myeloid cells and that this warrants more targeted use of selective autophagy inhibitors in a cancer therapy in a clinical setting.
自噬通过清除正常细胞中的基因毒性应激来抑制肿瘤起始。相反,自噬也通过减轻肿瘤细胞中的代谢应激来促进肿瘤进展。围绕自噬的这种促肿瘤作用,已经有许多通过全身阻断自噬来治疗癌症的临床试验。这种全身抑制作用会影响肿瘤细胞和非肿瘤细胞,而在肿瘤微环境背景下,非肿瘤细胞中自噬被阻断的后果相对研究较少。在此,我们研究了自噬缺陷型髓系细胞对具有自噬能力的肿瘤进展的影响。我们发现仅在髓系细胞中阻断自噬会显著调节肿瘤进展,但这种作用取决于具体情况。在肿瘤植入模型中,自噬缺陷型髓系细胞的小鼠体内植入的肿瘤细胞生长显著减少;T细胞更深地浸润到肿瘤中,并导致植入的肿瘤细胞生长减少。然而,在癌基因驱动的肿瘤诱导模型中,自噬缺陷型髓系细胞的小鼠肿瘤生长更快且转移更多。这些数据表明髓系细胞的自噬状态在肿瘤进展中起关键作用,根据肿瘤与髓系细胞相互作用的情况促进或抑制肿瘤生长。这项研究表明,在癌症治疗中全身使用自噬抑制剂可能因对髓系细胞的影响而对患者的肿瘤进展速度产生不同影响,这就需要在临床环境中更有针对性地使用选择性自噬抑制剂进行癌症治疗。