de Moraes Luciana V, Dechavanne Sebastien, Sousa Patrícia M, Barateiro André, Cunha Sónia F, Nunes-Silva Sofia, Lima Flávia A, Murillo Oscar, Marinho Claudio R F, Gangnard Stephane, Srivastava Anand, Braks Joanna A, Janse Chris J, Gamain Benoit, Franke-Fayard Blandine, Penha-Gonçalves Carlos
Instituto Gulbenkian de Ciência, Oeiras, Portugal
Inserm UMR_1134, Paris, France.
Infect Immun. 2016 May 24;84(6):1761-1774. doi: 10.1128/IAI.01207-15. Print 2016 Jun.
Plasmodium falciparum infection during pregnancy leads to abortions, stillbirth, low birth weight, and maternal mortality. Infected erythrocytes (IEs) accumulate in the placenta by adhering to chondroitin sulfate A (CSA) via var2CSA protein exposed on the P. falciparum IE membrane. Plasmodium berghei IE infection in pregnant BALB/c mice is a model for severe placental malaria (PM). Here, we describe a transgenic P. berghei parasite expressing the full-length var2CSA extracellular region (domains DBL1X to DBL6ε) fused to a P. berghei exported protein (EMAP1) and characterize a var2CSA-based mouse model of PM. BALB/c mice were infected at midgestation with different doses of P. berghei-var2CSA (P. berghei-VAR) or P. berghei wild-type IEs. Infection with 10(4) P. berghei-VAR IEs induced a higher incidence of stillbirth and lower fetal weight than P. berghei At doses of 10(5) and 10(6) IEs, P. berghei-VAR-infected mice showed increased maternal mortality during pregnancy and fetal loss, respectively. Parasite loads in infected placentas were similar between parasite lines despite differences in maternal outcomes. Fetal weight loss normalized for parasitemia was higher in P. berghei-VAR-infected mice than in P. berghei-infected mice. In vitro assays showed that higher numbers of P. berghei-VAR IEs than P. berghei IEs adhered to placental tissue. Immunization of mice with P. berghei-VAR elicited IgG antibodies reactive to DBL1-6 recombinant protein, indicating that the topology of immunogenic epitopes is maintained between DBL1-6-EMAP1 on P. berghei-VAR and recombinant DBL1-6 (recDBL1-6). Our data suggested that impairments in pregnancy caused by P. berghei-VAR infection were attributable to var2CSA expression. This model provides a tool for preclinical evaluation of protection against PM induced by approaches that target var2CSA.
孕期感染恶性疟原虫会导致流产、死产、低出生体重和孕产妇死亡。受感染的红细胞(IEs)通过疟原虫IE膜上暴露的var2CSA蛋白与硫酸软骨素A(CSA)结合,从而在胎盘中积聚。怀孕的BALB/c小鼠感染伯氏疟原虫IE是严重胎盘疟疾(PM)的一个模型。在此,我们描述了一种转基因伯氏疟原虫寄生虫,它表达与伯氏疟原虫输出蛋白(EMAP1)融合的全长var2CSA细胞外区域(结构域DBL1X至DBL6ε),并对基于var2CSA的PM小鼠模型进行了表征。在妊娠中期,用不同剂量的伯氏疟原虫-var2CSA(P. berghei-VAR)或伯氏疟原虫野生型IEs感染BALB/c小鼠。与伯氏疟原虫相比,感染10⁴个伯氏疟原虫-VAR IEs会导致更高的死产发生率和更低的胎儿体重。在10⁵和10⁶个IEs剂量下,感染伯氏疟原虫-VAR的小鼠分别在孕期出现更高的孕产妇死亡率和胎儿丢失率。尽管母体结局存在差异,但不同寄生虫株感染的胎盘内寄生虫载量相似。与感染伯氏疟原虫的小鼠相比,感染伯氏疟原虫-VAR的小鼠经寄生虫血症校正后的胎儿体重减轻更高。体外试验表明,与伯氏疟原虫IEs相比,更多数量的伯氏疟原虫-VAR IEs黏附于胎盘组织。用伯氏疟原虫-VAR免疫小鼠可诱导产生对DBL1-6重组蛋白有反应的IgG抗体,这表明伯氏疟原虫-VAR上的DBL1-6-EMAP1与重组DBL1-6(recDBL1-6)之间免疫原性表位的拓扑结构得以保留。我们的数据表明,伯氏疟原虫-VAR感染导致的妊娠损伤归因于var2CSA的表达。该模型为针对var2CSA的方法诱导的抗PM保护作用的临床前评估提供了一个工具。