Department of Mathematics, University of Pittsburgh, Pittsburgh, PA 15260, USA.
J Theor Biol. 2013 Oct 7;334:173-86. doi: 10.1016/j.jtbi.2013.05.028. Epub 2013 Jun 11.
Human malaria can be caused by the parasite Plasmodium falciparum that is transmitted by female Anopheles mosquitoes. "Immunological crosstalk" between the mammalian and anopheline hosts for Plasmodium functions to control parasite numbers. Key to this process is the mammalian cytokine transforming growth factor-β1 (TGF-β1). In mammals, TGF-β1 regulates inducible nitric oxide (NO) synthase (iNOS) both positively and negatively. In some settings, high levels of NO activate latent TGF-β1, which in turn suppresses iNOS expression. In the mosquito, ingested TGF-β1 induces A. stephensi NOS (AsNOS), which limits parasite development and which in turn is suppressed by activation of the mosquito homolog of the mitogen-activated protein kinases MEK and ERK. Computational models linking TGF-β1, AsNOS, and MEK/ERK were developed to provide insights into this complex biology. An initial Boolean model suggested that, as occurs in mammalian cells, MEK/ERK and AsNOS would oscillate upon ingestion of TGF-β1. An ordinary differential equation (ODE) model further supported the hypothesis of TGF-β1-induced multiphasic behavior of MEK/ERK and AsNOS. To achieve this multiphasic behavior, the ODE model was predicated on the presence of constant levels of TGF-β1 in the mosquito midgut. Ingested TGF-β1, however, did not exhibit this behavior. Accordingly, we hypothesized and experimentally verified that ingested TGF-β1 induces the expression of the endogenous mosquito TGF-β superfamily ligand As60A. Computational simulation of these complex, cross-species interactions suggested that TGF-β1 and NO-mediated induction of As60A expression together may act to maintain multiphasic AsNOS expression via MEK/ERK-dependent signaling. We hypothesize that multiphasic behavior as represented in this model allows the mosquito to balance the conflicting demands of parasite killing and metabolic homeostasis in the face of damaging inflammation.
人类疟疾可由疟原虫引起,疟原虫通过雌性按蚊传播。哺乳动物和按蚊宿主之间的“免疫串扰”有助于控制寄生虫数量。这个过程的关键是哺乳动物细胞因子转化生长因子-β1(TGF-β1)。在哺乳动物中,TGF-β1 既正向又负向调节诱导型一氧化氮合酶(iNOS)。在某些情况下,高水平的一氧化氮会激活潜伏的 TGF-β1,进而抑制 iNOS 的表达。在蚊子中,摄入的 TGF-β1 诱导 A. stephensi NOS(AsNOS),从而限制寄生虫的发育,而蚊子中丝裂原活化蛋白激酶 MEK 和 ERK 的同源物的激活又会抑制 AsNOS 的表达。为了深入了解这一复杂的生物学特性,建立了将 TGF-β1、AsNOS 和 MEK/ERK 联系起来的计算模型。一个初步的布尔模型表明,与哺乳动物细胞中发生的情况一样,摄入 TGF-β1 后,MEK/ERK 和 AsNOS 会发生振荡。进一步的常微分方程(ODE)模型支持了 MEK/ERK 和 AsNOS 被 TGF-β1 诱导呈多相性的假说。为了实现这种多相行为,ODE 模型假设在蚊子中肠中 TGF-β1 的水平保持不变。然而,摄入的 TGF-β1 并没有表现出这种行为。因此,我们假设并通过实验验证,摄入的 TGF-β1 诱导内源性蚊子 TGF-β 超家族配体 As60A 的表达。对这些复杂的、跨物种相互作用的计算模拟表明,TGF-β1 和 NO 介导的 As60A 表达诱导一起可能通过 MEK/ERK 依赖性信号通路共同作用,维持 AsNOS 表达的多相性。我们假设,这种模型中所代表的多相行为使蚊子能够在面对破坏性炎症时平衡杀死寄生虫和代谢平衡的相互冲突的需求。