Gandhi Hetvi, Worch Remigiusz, Kurgonaite Kristina, Hintersteiner Martin, Schwille Petra, Bökel Christian, Weidemann Thomas
BIOTEC/Biophysics, Technische Universität Dresden, Dresden, Germany.
BIOTEC/Biophysics, Technische Universität Dresden, Dresden, Germany; Institute of Physics, Polish Academy of Sciences, Warsaw, Poland.
Biophys J. 2014 Dec 2;107(11):2515-27. doi: 10.1016/j.bpj.2014.07.077.
It has long been established that dimerization of Interleukin-4 receptor (IL-4R) subunits is a pivotal step for JAK/STAT signal transduction. However, ligand-induced complex formation at the surface of living cells has been challenging to observe. Here we report an experimental assay employing trisNTA dyes for orthogonal, external labeling of eGFP-tagged receptor constructs that allows the quantification of receptor heterodimerization by dual-color fluorescence cross-correlation spectroscopy. Fluorescence cross-correlation spectroscopy analysis at the plasma membrane shows that IL-4R subunit dimerization is indeed a strictly ligand-induced process. Under conditions of saturating cytokine occupancy, we determined intramembrane dissociation constants (K(d,2D)) of 180 and 480 receptors per μm(2) for the type-2 complexes IL-4:IL-4Rα/IL-13Rα1 and IL-13:IL-13Rα1/IL-4Rα, respectively. For the lower affinity type-1 complex IL-4:IL-4Rα/IL-2Rγ, we estimated a K(d,2D) of ∼1000 receptors per μm(2). The receptor densities required for effective dimerization thus exceed the typical, average expression levels by several orders of magnitude. In addition, we find that all three receptor subunits accumulate rapidly within a subpopulation of early sorting and recycling endosomes stably anchored just beneath the plasma membrane (cortical endosomes, CEs). The receptors, as well as labeled IL-4 and trisNTA ligands are specifically trafficked into CEs by a constitutive internalization mechanism. This may compensate for the inherent weak affinities that govern ligand-induced receptor dimerization at the plasma membrane. Consistently, activated receptors are also concentrated at the CEs. Our observations thus suggest that receptor trafficking may play an important role for the regulation of IL-4R-mediated JAK/STAT signaling.
长期以来人们已经确定,白细胞介素4受体(IL-4R)亚基的二聚化是JAK/STAT信号转导的关键步骤。然而,在活细胞表面观察配体诱导的复合物形成一直具有挑战性。在此,我们报告了一种实验方法,该方法使用三氮杂环壬四乙酸(trisNTA)染料对eGFP标记的受体构建体进行正交、外部标记,从而能够通过双色荧光互相关光谱法对受体异二聚化进行定量。质膜处的荧光互相关光谱分析表明,IL-4R亚基二聚化确实是一个严格由配体诱导的过程。在细胞因子占据饱和的条件下,我们分别测定了IL-4:IL-4Rα/IL-13Rα1和IL-13:IL-13Rα1/IL-4Rα这两种2型复合物每μm²的膜内解离常数(K(d,2D))为180和480个受体。对于亲和力较低的1型复合物IL-4:IL-4Rα/IL-2Rγ,我们估计其K(d,2D)约为每μm²1000个受体。有效二聚化所需的受体密度因此比典型的平均表达水平高出几个数量级。此外,我们发现所有三个受体亚基都在早期分选和再循环内体的一个亚群中迅速积累,这些内体稳定地锚定在质膜下方(皮质内体,CEs)。受体以及标记的IL-4和trisNTA配体通过组成型内化机制特异性地转运到CEs中。这可能弥补了在质膜上控制配体诱导受体二聚化的内在弱亲和力。一致地,活化的受体也集中在CEs处。因此,我们的观察结果表明,受体转运可能在IL-4R介导的JAK/STAT信号传导调节中发挥重要作用。