Matar Caline G, Anthony Neil R, O'Flaherty Brigid M, Jacobs Nathan T, Priyamvada Lalita, Engwerda Christian R, Speck Samuel H, Lamb Tracey J
Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, Georgia, United States of America; Microbiology and Molecular Genetics Graduate Program, Laney Graduate School, Emory University, Atlanta, Georgia, United States of America.
Division of Pediatric Infectious Disease, Department of Pediatrics, Emory University School of Medicine, Emory Children's Centre, Atlanta, Georgia, United States of America.
PLoS Pathog. 2015 May 21;11(5):e1004858. doi: 10.1371/journal.ppat.1004858. eCollection 2015 May.
Immunity to non-cerebral severe malaria is estimated to occur within 1-2 infections in areas of endemic transmission for Plasmodium falciparum. Yet, nearly 20% of infected children die annually as a result of severe malaria. Multiple risk factors are postulated to exacerbate malarial disease, one being co-infections with other pathogens. Children living in Sub-Saharan Africa are seropositive for Epstein Barr Virus (EBV) by the age of 6 months. This timing overlaps with the waning of protective maternal antibodies and susceptibility to primary Plasmodium infection. However, the impact of acute EBV infection on the generation of anti-malarial immunity is unknown. Using well established mouse models of infection, we show here that acute, but not latent murine gammaherpesvirus 68 (MHV68) infection suppresses the anti-malarial humoral response to a secondary malaria infection. Importantly, this resulted in the transformation of a non-lethal P. yoelii XNL infection into a lethal one; an outcome that is correlated with a defect in the maintenance of germinal center B cells and T follicular helper (Tfh) cells in the spleen. Furthermore, we have identified the MHV68 M2 protein as an important virus encoded protein that can: (i) suppress anti-MHV68 humoral responses during acute MHV68 infection; and (ii) plays a critical role in the observed suppression of anti-malarial humoral responses in the setting of co-infection. Notably, co-infection with an M2-null mutant MHV68 eliminates lethality of P. yoelii XNL. Collectively, our data demonstrates that an acute gammaherpesvirus infection can negatively impact the development of an anti-malarial immune response. This suggests that acute infection with EBV should be investigated as a risk factor for non-cerebral severe malaria in young children living in areas endemic for Plasmodium transmission.
在恶性疟原虫流行传播地区,据估计,在感染1 - 2次后可产生对非脑型重症疟疾的免疫力。然而,每年仍有近20%的感染儿童死于重症疟疾。多种风险因素被认为会加重疟疾病情,其中之一是与其他病原体的共同感染。撒哈拉以南非洲地区的儿童在6个月大时,血清中爱泼斯坦 - 巴尔病毒(EBV)呈阳性。这个时间点与保护性母体抗体的消退以及对原发性疟原虫感染的易感性相重叠。然而,急性EBV感染对抗疟疾免疫产生的影响尚不清楚。利用成熟的小鼠感染模型,我们在此表明,急性而非潜伏性的鼠γ - 疱疹病毒68(MHV68)感染会抑制对二次疟疾感染的抗疟疾体液反应。重要的是,这导致了原本非致命的约氏疟原虫XNL感染转变为致命感染;这一结果与脾脏中生发中心B细胞和T滤泡辅助细胞(Tfh)维持缺陷相关。此外,我们已确定MHV68 M2蛋白是一种重要的病毒编码蛋白,它可以:(i)在急性MHV68感染期间抑制抗MHV68体液反应;(ii)在共同感染情况下观察到的抗疟疾体液反应抑制中起关键作用。值得注意的是,与M2基因缺失突变体MHV68共同感染可消除约氏疟原虫XNL的致死性。总体而言,我们的数据表明急性γ - 疱疹病毒感染会对抗疟疾免疫反应的发展产生负面影响。这表明,对于生活在疟原虫传播流行地区的幼儿,应将急性EBV感染作为非脑型重症疟疾的一个风险因素进行研究。