Khandekar Durga, Dahunsi Debolanle O, Manzanera Esteve Isaac V, Reid Sonya, Rathmell Jeffrey C, Titze Jens, Tiriveedhi Venkataswarup
Department of Biological Sciences, Tennessee State University, Nashville, TN 37209, USA.
Department Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
Biology (Basel). 2022 May 25;11(6):810. doi: 10.3390/biology11060810.
Immune checkpoint inhibitor (ICI) therapy has revolutionized the breast cancer treatment landscape. However, ICI-induced systemic inflammatory immune-related adverse events (irAE) remain a major clinical challenge. Previous studies in our laboratory and others have demonstrated that a high-salt (HS) diet induces inflammatory activation of CD4+T cells leading to anti-tumor responses. In our current communication, we analyzed the impact of dietary salt modification on therapeutic and systemic outcomes in breast-tumor-bearing mice following anti-cytotoxic T-lymphocyte-associated protein 4 (CTLA4) monoclonal antibody (mAb) based ICI therapy. As HS diet and anti-CTLA4 mAb both exert pro-inflammatory activation of CD4+T cells, we hypothesized that a combination of these would lead to enhanced irAE response, while low-salt (LS) diet through blunting peripheral inflammatory action of CD4+T cells would reduce irAE response. We utilized an orthotopic murine breast tumor model by injecting Py230 murine breast cancer cells into syngeneic C57Bl/6 mice. In an LS diet cohort, anti-CTLA4 mAb treatment significantly reduced tumor progression (day 35, 339 ± 121 mm3), as compared to isotype mAb (639 ± 163 mm3, p < 0.05). In an HS diet cohort, treatment with anti-CTLA4 reduced the survival rate (day 80, 2/15) compared to respective normal/regular salt (NS) diet cohort (8/15, p < 0.05). Further, HS plus anti-CTLA4 mAb caused an increased expression of inflammatory cytokines (IFNγ and IL-1β) in lung infiltrating and peripheral circulating CD4+T cells. This inflammatory activation of CD4+T cells in the HS plus anti-CTLA4 cohort was associated with the upregulation of inflammasome complex activity. However, an LS diet did not induce any significant irAE response in breast-tumor-bearing mice upon treatment with anti-CTLA4 mAb, thus suggesting the role of high-salt diet in irAE response. Importantly, CD4-specific knock out of osmosensitive transcription factor NFAT5 using CD4cre/creNFAT5flox/flox transgenic mice caused a downregulation of high-salt-mediated inflammatory activation of CD4+T cells and irAE response. Taken together, our data suggest that LS diet inhibits the anti-CTLA4 mAb-induced irAE response while retaining its anti-tumor efficacy.
免疫检查点抑制剂(ICI)疗法彻底改变了乳腺癌的治疗格局。然而,ICI诱导的全身性炎症性免疫相关不良事件(irAE)仍然是一个重大的临床挑战。我们实验室和其他机构之前的研究表明,高盐(HS)饮食会诱导CD4+T细胞的炎症激活,从而引发抗肿瘤反应。在我们当前的交流中,我们分析了饮食盐分改变对携带乳腺肿瘤的小鼠在基于抗细胞毒性T淋巴细胞相关蛋白4(CTLA4)单克隆抗体(mAb)的ICI治疗后的治疗效果和全身结果的影响。由于HS饮食和抗CTLA4 mAb都会对CD4+T细胞产生促炎激活作用,我们假设将两者结合会导致更强的irAE反应,而低盐(LS)饮食通过减弱CD4+T细胞的外周炎症作用会降低irAE反应。我们通过将Py230小鼠乳腺癌细胞注射到同基因C57Bl/6小鼠中建立了原位小鼠乳腺肿瘤模型。在LS饮食组中,与同型mAb相比,抗CTLA4 mAb治疗显著降低了肿瘤进展(第35天,339±121立方毫米)(同型mAb组为639±163立方毫米,p<0.05)。在HS饮食组中,与各自的正常/常规盐(NS)饮食组相比,抗CTLA4治疗降低了生存率(第80天,2/15)(NS饮食组为8/15,p<0.05)。此外,HS加抗CTLA4 mAb导致肺浸润和外周循环CD4+T细胞中炎性细胞因子(IFNγ和IL-1β)的表达增加。HS加抗CTLA4组中CD4+T细胞的这种炎症激活与炎性小体复合物活性的上调有关。然而,如果给携带乳腺肿瘤的小鼠喂食LS饮食并给予抗CTLA4 mAb治疗,则不会诱导任何显著的irAE反应,这表明高盐饮食在irAE反应中的作用。重要的是,使用CD4cre/creNFAT5flox/flox转基因小鼠对渗透压敏感转录因子NFAT5进行CD4特异性敲除,导致高盐介导的CD4+T细胞炎症激活和irAE反应下调。综上所述,我们的数据表明,LS饮食在保留其抗肿瘤疗效的同时,抑制了抗CTLA4 mAb诱导的irAE反应。
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