Infectious Diseases Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, New York, United States of America.
Immunology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, New York, United States of America.
PLoS Pathog. 2019 Mar 21;15(3):e1007627. doi: 10.1371/journal.ppat.1007627. eCollection 2019 Mar.
Cryptococcus neoformans is a leading cause of invasive fungal infections among immunocompromised patients. However, the cellular constituents of the innate immune response that promote clearance versus progression of infection upon respiratory acquisition of C. neoformans remain poorly defined. In this study, we found that during acute C. neoformans infection, CCR2+ Ly6Chi inflammatory monocytes (IM) rapidly infiltrate the lungs and mediate fungal trafficking to lung-draining lymph nodes. Interestingly, this influx of IM is detrimental to the host, since ablating IM or impairing their recruitment to the lungs improves murine survival and reduces fungal proliferation and dissemination. Using a novel conditional gene deletion strategy, we determined that MHC class II expression by IM did not mediate their deleterious impact on the host. Furthermore, although ablation of IM reduced the number of lymphocytes, innate lymphoid cells, and eosinophils in the lungs, the effects of IM were not dependent on these cells. We ascertained that IM in the lungs upregulated transcripts associated with alternatively activated (M2) macrophages in response to C. neoformans, consistent with the model that IM assume a cellular phenotype that is permissive for fungal growth. We also determined that conditional knockout of the prototypical M2 marker arginase 1 in IM and deletion of the M2-associated transcription factor STAT6 were not sufficient to reverse the harmful effects of IM. Overall, our findings indicate that C. neoformans can subvert the fungicidal potential of IM to enable the progression of infection through a mechanism that is not dependent on lymphocyte priming, eosinophil recruitment, or downstream M2 macrophage polarization pathways. These results give us new insight into the plasticity of IM function during fungal infections and the level of control that C. neoformans can exert on host immune responses.
新型隐球菌是免疫功能低下患者侵袭性真菌感染的主要原因。然而,对于呼吸道获得新型隐球菌后促进清除或进展感染的固有免疫反应的细胞成分仍知之甚少。在这项研究中,我们发现,在急性新型隐球菌感染期间,CCR2+Ly6Chi 炎性单核细胞(IM)迅速浸润肺部,并介导真菌向肺引流淋巴结的迁移。有趣的是,IM 的这种涌入对宿主是有害的,因为消除 IM 或阻止其向肺部募集可改善小鼠的存活率并减少真菌的增殖和传播。使用一种新的条件性基因缺失策略,我们确定 IM 中 MHC Ⅱ类的表达不能介导其对宿主的有害影响。此外,尽管消除 IM 减少了肺部淋巴细胞、固有淋巴细胞和嗜酸性粒细胞的数量,但 IM 的作用并不依赖于这些细胞。我们发现,肺部的 IM 上调了与新型隐球菌反应相关的替代激活(M2)巨噬细胞的转录本,这与 IM 假设允许真菌生长的细胞表型的模型一致。我们还确定,IM 中典型的 M2 标志物精氨酸酶 1 的条件性基因敲除和与 M2 相关的转录因子 STAT6 的缺失不足以逆转 IM 的有害影响。总的来说,我们的研究结果表明,新型隐球菌可以颠覆 IM 的杀菌潜能,通过一种不依赖于淋巴细胞启动、嗜酸性粒细胞募集或下游 M2 巨噬细胞极化途径的机制来促进感染的进展。这些结果使我们对真菌感染期间 IM 功能的可塑性以及新型隐球菌对宿主免疫反应的控制程度有了新的认识。