Center for Immunology and Inflammation, Feinstein Institutes for Medical Research, 350 Community Drive, Manhasset, NY 11030, United States.
Department of Surgery, Zucker School of Medicine at Hofstra/Northwell, 350 Community Drive, Manhasset, NY 11030, United States.
J Leukoc Biol. 2024 Sep 2;116(3):632-643. doi: 10.1093/jleuko/qiae066.
B-1a cells, a regulatory subset of B lymphocytes, produce natural IgM and interleukin-10. Neutrophil extracellular traps (NETs) play a crucial role in pathogen defense, but their excessive formation during sepsis can cause further inflammation and tissue damage. In sepsis, extracellular cold-inducible RNA-binding protein (eCIRP), a damage-associated molecular pattern, is released to induce NET formation. We hypothesize that B-1a cells clear NETs to prevent sepsis-induced injury. Sepsis in mice was induced by injecting 1 × 107 and 5 × 107 colony-forming units of Escherichia coli intraperitoneally. After 4 and 20 h, we assessed the number of B-1a cells in the peritoneal cavity using flow cytometry. Our results showed that the number of peritoneal B-1a cells was significantly decreased in E. coli sepsis mice. Importantly, replenishing B-1a cells via intraperitoneal injection in sepsis mice significantly decreased NETs in peritoneal neutrophils. We also observed a decrease in serum inflammation and injury markers and a significant increase in the overall survival rate in B-1a cell-treated septic mice. To understand the mechanism, we cocultured bone marrow-derived neutrophils with peritoneal B-1a cells in a contact or noncontact condition using an insert and stimulated them with eCIRP. After 4 h, we found that eCIRP significantly increased NET formation in bone marrow-derived neutrophils. Interestingly, we observed that B-1a cells inhibited NETs by 67% in a contact-dependent manner. Surprisingly, when B-1a cells were cultured in inserts, there was no significant decrease in NET formation, suggesting that direct cell-to-cell contact is crucial for this inhibitory effect. We further determined that B-1a cells promoted NET phagocytosis, and this was mediated through natural IgM, as blocking the IgM receptor attenuated the engulfment of NETs by B-1a cells. Finally, we identified that following their engulfment, NETs were localized into the lysosomal compartment for lysis. Thus, our study suggests that B-1a cells decrease NET content in eCIRP-treated neutrophils and E. coli sepsis mice.
B-1a 细胞是 B 淋巴细胞的一种调节亚群,能够产生天然 IgM 和白细胞介素-10。中性粒细胞胞外诱捕网(NETs)在病原体防御中起着至关重要的作用,但在脓毒症中过度形成会导致进一步的炎症和组织损伤。在脓毒症中,细胞外冷诱导 RNA 结合蛋白(eCIRP)作为一种损伤相关分子模式被释放出来诱导 NET 形成。我们假设 B-1a 细胞可以清除 NET 以防止脓毒症引起的损伤。通过向小鼠腹腔内注射 1×107 和 5×107 个大肠杆菌菌落形成单位来诱导脓毒症。在 4 和 20 小时后,我们使用流式细胞术评估腹腔内 B-1a 细胞的数量。结果表明,大肠杆菌脓毒症小鼠腹腔内 B-1a 细胞的数量显著减少。重要的是,在脓毒症小鼠中通过腹腔内注射补充 B-1a 细胞可显著减少腹腔中性粒细胞中的 NET。我们还观察到血清炎症和损伤标志物减少,并且 B-1a 细胞治疗的脓毒症小鼠的总生存率显著提高。为了了解机制,我们在接触或非接触条件下,使用插入物将骨髓来源的中性粒细胞与腹腔内 B-1a 细胞共培养,并使用 eCIRP 刺激它们。4 小时后,我们发现 eCIRP 显著增加了骨髓来源的中性粒细胞中 NET 的形成。有趣的是,我们观察到 B-1a 细胞以接触依赖的方式将 NET 抑制了 67%。令人惊讶的是,当 B-1a 细胞在插入物中培养时,NET 的形成并没有显著减少,这表明直接的细胞间接触对于这种抑制作用至关重要。我们进一步确定 B-1a 细胞促进了 NET 的吞噬作用,并且这是通过天然 IgM 介导的,因为阻断 IgM 受体减弱了 B-1a 细胞对 NET 的吞噬作用。最后,我们发现 NET 被 B-1a 细胞吞噬后被定位到溶酶体区室进行裂解。因此,我们的研究表明,B-1a 细胞减少了 eCIRP 处理的中性粒细胞和大肠杆菌脓毒症小鼠中的 NET 含量。