Cooperativity of membrane-protein and protein–protein interactions control membrane remodeling by epsin 1 and affects clathrin-mediated endocytosis

Kroppen, Benjamin; Teske, Nelli; Yambire, King Faisal; Denkert, Niels; Mukherjee, Indrani; Tarasenko, Daryna; Jaipuria, Garima; Zweckstetter, Markus; Milošević, Ira; Steinem, Claudia; Meinecke, Michael

doi:10.1007/s00018-020-03647-z

Cited by 8 publications

(3 citation statements)

References 51 publications

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“…Previous studies reported the use of Dyn K44A [ 34 , 50 , 72 ] and Pitstop2 [ 51 , 73 , 74 ] as means by which to investigate the clathrin-mediated pathway. In addition to the significant changes in BILF1 internalization induced by the inhibitors, we also observed an increase in receptor expression after the addition of Dyn K44A.…”

Section: Discussionmentioning

confidence: 99%

Patterns of human and porcine gammaherpesvirus-encoded BILF1 receptor endocytosis

Mavri¹,

Glišić

Senćanski

et al. 2023

Cell Mol Biol Lett

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Background The viral G-protein-coupled receptor (vGPCR) BILF1 encoded by the Epstein–Barr virus (EBV) is an oncogene and immunoevasin and can downregulate MHC-I molecules at the surface of infected cells. MHC-I downregulation, which presumably occurs through co-internalization with EBV-BILF1, is preserved among BILF1 receptors, including the three BILF1 orthologs encoded by porcine lymphotropic herpesviruses (PLHV BILFs). This study aimed to understand the detailed mechanisms of BILF1 receptor constitutive internalization, to explore the translational potential of PLHV BILFs compared with EBV-BILF1. Methods A novel real-time fluorescence resonance energy transfer (FRET)-based internalization assay combined with dominant-negative variants of dynamin-1 (Dyn K44A) and the chemical clathrin inhibitor Pitstop2 in HEK-293A cells was used to study the effect of specific endocytic proteins on BILF1 internalization. Bioluminescence resonance energy transfer (BRET)-saturation analysis was used to study BILF1 receptor interaction with β-arrestin2 and Rab7. In addition, a bioinformatics approach informational spectrum method (ISM) was used to investigate the interaction affinity of BILF1 receptors with β-arrestin2, AP-2, and caveolin-1. Results We identified dynamin-dependent, clathrin-mediated constitutive endocytosis for all BILF1 receptors. The observed interaction affinity between BILF1 receptors and caveolin-1 and the decreased internalization in the presence of a dominant-negative variant of caveolin-1 (Cav S80E) indicated the involvement of caveolin-1 in BILF1 trafficking. Furthermore, after BILF1 internalization from the plasma membrane, both the recycling and degradation pathways are proposed for BILF1 receptors. Conclusions The similarity in the internalization mechanisms observed for EBV-BILF1 and PLHV1-2 BILF1 provide a foundation for further studies exploring a possible translational potential for PLHVs, as proposed previously, and provides new information about receptor trafficking. Graphical Abstract

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Section: Discussionmentioning

confidence: 99%

Patterns of human and porcine gammaherpesvirus-encoded BILF1 receptor endocytosis

Mavri¹,

Glišić

Senćanski

et al. 2023

Cell Mol Biol Lett

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“…Given that epsins themselves are able to induce membrane curvature 50 , 51 , it was possible that impaired CCS invagination resulted from compromised localization of epsins in the presence of CK-666. To test this possibility, we applied CK-666 or DMSO to Ptk2 cells ectopically expressing mCherry-CLC and EGFP-epsin1 and imaged cells by TIRF microscopy (Fig.…”

Section: Resultsmentioning

confidence: 99%

Actin polymerization promotes invagination of flat clathrin-coated lattices in mammalian cells by pushing at lattice edges

et al. 2022

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Clathrin-mediated endocytosis (CME) requires energy input from actin polymerization in mechanically challenging conditions. The roles of actin in CME are poorly understood due to inadequate knowledge of actin organization at clathrin-coated structures (CCSs). Using platinum replica electron microscopy of mammalian cells, we show that Arp2/3 complex-dependent branched actin networks, which often emerge from microtubule tips, assemble along the CCS perimeter, lack interaction with the apical clathrin lattice, and have barbed ends oriented toward the CCS. This structure is hardly compatible with the widely held “apical pulling” model describing actin functions in CME. Arp2/3 complex inhibition or epsin knockout produce large flat non-dynamic CCSs, which split into invaginating subdomains upon recovery from Arp2/3 inhibition. Moreover, epsin localization to CCSs depends on Arp2/3 activity. We propose an “edge pushing” model for CME, wherein branched actin polymerization promotes severing and invagination of flat CCSs in an epsin-dependent manner by pushing at the CCS boundary, thus releasing forces opposing the intrinsic curvature of clathrin lattices.

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“…This, in turn, lowers the energy barrier to induce membrane curvature (Steinem and Meinecke 2020). The mechanism of decreasing lateral membrane tension and generation of curvature depends on AH insertion and the lipid-specific oligomerization of the ENTH domain (Kroppen et al 2020). It therefore seems reasonable to assume that ENTH-dependent membrane remodeling relies on different molecular mechanisms that combine cooperativity of protein-lipid and protein-protein interactions.…”

Section: Epsin1mentioning

confidence: 99%

Protein-dependent membrane remodeling in mitochondrial morphology and clathrin-mediated endocytosis

Tarasenko

Meinecke

2021

Eur Biophys J

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Cellular membranes can adopt a plethora of complex and beautiful shapes, most of which are believed to have evolved for a particular physiological reason. The closely entangled relationship between membrane morphology and cellular physiology is strikingly seen in membrane trafficking pathways. During clathrin-mediated endocytosis, for example, over the course of a minute, a patch of the more or less flat plasma membrane is remodeled into a highly curved clathrin-coated vesicle. Such vesicles are internalized by the cell to degrade or recycle plasma membrane receptors or to take up extracellular ligands. Other, steadier, membrane morphologies can be observed in organellar membranes like the endoplasmic reticulum or mitochondria. In the case of mitochondria, which are double membrane-bound, ubiquitous organelles of eukaryotic cells, especially the mitochondrial inner membrane displays an intricated ultrastructure. It is highly folded and consequently has a much larger surface than the mitochondrial outer membrane. It can adopt different shapes in response to cellular demands and changes of the inner membrane morphology often accompany severe diseases, including neurodegenerative- and metabolic diseases and cancer. In recent years, progress was made in the identification of molecules that are important for the aforementioned membrane remodeling events. In this review, we will sum up recent results and discuss the main players of membrane remodeling processes that lead to the mitochondrial inner membrane ultrastructure and in clathrin-mediated endocytosis. We will compare differences and similarities between the molecular mechanisms that peripheral and integral membrane proteins use to deform membranes.

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Cooperativity of membrane-protein and protein–protein interactions control membrane remodeling by epsin 1 and affects clathrin-mediated endocytosis

Cited by 8 publications

References 51 publications

Patterns of human and porcine gammaherpesvirus-encoded BILF1 receptor endocytosis

Patterns of human and porcine gammaherpesvirus-encoded BILF1 receptor endocytosis

Actin polymerization promotes invagination of flat clathrin-coated lattices in mammalian cells by pushing at lattice edges

Protein-dependent membrane remodeling in mitochondrial morphology and clathrin-mediated endocytosis

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