Literature DB >> 25468331

Dynamics and interaction of interleukin-4 receptor subunits in living cells.

Hetvi Gandhi1, Remigiusz Worch2, Kristina Kurgonaite3, Martin Hintersteiner4, Petra Schwille5, Christian Bökel3, Thomas Weidemann6.   

Abstract

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.
Copyright © 2014 Biophysical Society. Published by Elsevier Inc. All rights reserved.

Entities:  

Mesh:

Substances:

Year:  2014        PMID: 25468331      PMCID: PMC4255262          DOI: 10.1016/j.bpj.2014.07.077

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   4.033


  48 in total

Review 1.  Molecular phylogeny within type I cytokines and their cognate receptors.

Authors:  Jean-Louis Boulay; John J O'Shea; William E Paul
Journal:  Immunity       Date:  2003-08       Impact factor: 31.745

2.  Analysis of binding reactions by fluorescence recovery after photobleaching.

Authors:  Brian L Sprague; Robert L Pego; Diana A Stavreva; James G McNally
Journal:  Biophys J       Date:  2004-06       Impact factor: 4.033

3.  Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway.

Authors:  C Lamaze; A Dujeancourt; T Baba; C G Lo; A Benmerah; A Dautry-Varsat
Journal:  Mol Cell       Date:  2001-03       Impact factor: 17.970

4.  The high-affinity interaction of human IL-4 and the receptor alpha chain is constituted by two independent binding clusters.

Authors:  Jin-Li Zhang; Irina Simeonowa; Yonghong Wang; Walter Sebald
Journal:  J Mol Biol       Date:  2002-01-18       Impact factor: 5.469

Review 5.  Structure, binding, and antagonists in the IL-4/IL-13 receptor system.

Authors:  Thomas D Mueller; Jin-Li Zhang; Walter Sebald; Albert Duschl
Journal:  Biochim Biophys Acta       Date:  2002-11-11

6.  Functional epitope of common gamma chain for interleukin-4 binding.

Authors:  Jin-Li Zhang; Manfred Buehner; Walter Sebald
Journal:  Eur J Biochem       Date:  2002-03

7.  Jak3-independent trafficking of the common gamma chain receptor subunit: chaperone function of Jaks revisited.

Authors:  Sigrun R Hofmann; Albert Q Lam; Stephan Frank; Yong-Jie Zhou; Haydeé L Ramos; Yuka Kanno; Davide Agnello; Richard J Youle; John J O'Shea
Journal:  Mol Cell Biol       Date:  2004-06       Impact factor: 4.272

8.  Long term association of the cytokine receptor gp130 and the Janus kinase Jak1 revealed by FRAP analysis.

Authors:  Bernd Giese; Chi-King Au-Yeung; Andreas Herrmann; Sandra Diefenbach; Claude Haan; Andrea Küster; Saskia B Wortmann; Christoph Roderburg; Peter C Heinrich; Iris Behrmann; Gerhard Müller-Newen
Journal:  J Biol Chem       Date:  2003-07-23       Impact factor: 5.157

9.  Interleukin-4 and interleukin-13 signaling connections maps.

Authors:  Ann E Kelly-Welch; Erica M Hanson; Mark R Boothby; Achsah D Keegan
Journal:  Science       Date:  2003-06-06       Impact factor: 47.728

10.  Characterization of the human B cell stimulatory factor 1 receptor.

Authors:  L S Park; D Friend; H M Sassenfeld; D L Urdal
Journal:  J Exp Med       Date:  1987-08-01       Impact factor: 14.307

View more
  15 in total

1.  Kinetics of cytokine receptor trafficking determine signaling and functional selectivity.

Authors:  Jonathan Martinez-Fabregas; Stephan Wilmes; Luopin Wang; Majid Kazemian; Suman Mitra; Ignacio Moraga; Maximillian Hafer; Elizabeth Pohler; Juliane Lokau; Christoph Garbers; Adeline Cozzani; Paul K Fyfe; Jacob Piehler
Journal:  Elife       Date:  2019-11-27       Impact factor: 8.140

2.  MHC I Expression Regulates Co-clustering and Mobility of Interleukin-2 and -15 Receptors in T Cells.

Authors:  Gábor Mocsár; Julianna Volkó; Daniel Rönnlund; Jerker Widengren; Péter Nagy; János Szöllősi; Katalin Tóth; Carolyn K Goldman; Sándor Damjanovich; Thomas A Waldmann; Andrea Bodnár; György Vámosi
Journal:  Biophys J       Date:  2016-07-12       Impact factor: 4.033

3.  Estrogen Signaling Contributes to Sex Differences in Macrophage Polarization during Asthma.

Authors:  Aleksander Keselman; Xi Fang; Preston B White; Nicola M Heller
Journal:  J Immunol       Date:  2017-07-31       Impact factor: 5.422

4.  Quantifying membrane protein oligomerization with fluorescence cross-correlation spectroscopy.

Authors:  Megan J Kaliszewski; Xiaojun Shi; Yixuan Hou; Ryan Lingerak; Soyeon Kim; Paul Mallory; Adam W Smith
Journal:  Methods       Date:  2018-02-13       Impact factor: 3.608

Review 5.  Targeting IL4/IL4R for the treatment of epithelial cancer metastasis.

Authors:  Katherine Venmar Bankaitis; Barbara Fingleton
Journal:  Clin Exp Metastasis       Date:  2015-09-18       Impact factor: 5.150

6.  Nanoconjugation prolongs endosomal signaling of the epidermal growth factor receptor and enhances apoptosis.

Authors:  L Wu; F Xu; B M Reinhard
Journal:  Nanoscale       Date:  2016-07-14       Impact factor: 7.790

7.  Ligand-induced type II interleukin-4 receptor dimers are sustained by rapid re-association within plasma membrane microcompartments.

Authors:  David Richter; Ignacio Moraga; Hauke Winkelmann; Oliver Birkholz; Stephan Wilmes; Markos Schulte; Michael Kraich; Hella Kenneweg; Oliver Beutel; Philipp Selenschik; Dirk Paterok; Martynas Gavutis; Thomas Schmidt; K Christopher Garcia; Thomas D Müller; Jacob Piehler
Journal:  Nat Commun       Date:  2017-07-14       Impact factor: 14.919

8.  Instructive roles for cytokine-receptor binding parameters in determining signaling and functional potency.

Authors:  Ignacio Moraga; David Richter; Stephan Wilmes; Hauke Winkelmann; Kevin Jude; Christoph Thomas; Megan M Suhoski; Edgar G Engleman; Jacob Piehler; K Christopher Garcia
Journal:  Sci Signal       Date:  2015-11-10       Impact factor: 8.192

9.  Diffusion of Single-Pass Transmembrane Receptors: From the Plasma Membrane into Giant Liposomes.

Authors:  Remigiusz Worch; Zdenek Petrášek; Petra Schwille; Thomas Weidemann
Journal:  J Membr Biol       Date:  2016-11-08       Impact factor: 1.843

10.  Relationship Between Homodimeric Glucocorticoid Receptor and Transcriptional Regulation Assessed via an In Vitro Fluorescence Correlation Spectroscopy-Microwell System.

Authors:  Sho Oasa; Shintaro Mikuni; Johtaro Yamamoto; Tsumugi Kurosaki; Daisuke Yamashita; Masataka Kinjo
Journal:  Sci Rep       Date:  2018-05-10       Impact factor: 4.379

View more

北京卡尤迪生物科技股份有限公司 © 2022-2023.