Arginylation Regulates Intracellular Actin Polymer Level by Modulating Actin Properties and Binding of Capping and Severing Proteins

Saha, Swati; Mundia, Maureen M.; Zhang, Fangliang; Demers, Ryan W.; Korobova, Farida; Svitkina, Tatyana; Perieteanu, Alex A. PerieteanuA.A.; Dawson, John F.; Kashina, Anna

doi:10.1091/mbc.e09-09-0829

Cited by 90 publications

(87 citation statements)

References 50 publications

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“…A significant proportion of β-actin protein at the leading lamella prior to cell-cell contact and adherens junction assembly is posttranslationally arginylated, preventing tight packing and consequently favoring branched filament polymerization (Karakozova et al 2006). In contrast, linear actin filaments, required to stabilize and anchor adherens junction complexes, are assembled from nonarginylated β-actin monomers (Saha et al 2010). Consequently, we hypothesize that the monomer required for linear actin filament polymerization at cell contact sites during adherens junction assembly are products of locally translated β-actin.…”

Section: Discussionmentioning

confidence: 99%

“…For example, E-cadherin directly regulates actin filament polymerization during the contact initiation stage of epithelial adherens junction assembly by binding and localizing Arp2/3 complexes to cellcell contact sites (Kovacs et al 2002b). Also during the contact initiation stage of adherens junction assembly, post-translationally arginylated-β-actin monomers polymerize into branched filament arrays driving lamellar protrusion in areas with high concentrations of activated Arp2/3 complexes (Kovacs et al 2002a;Karakozova et al 2006;Saha et al 2010). Thereafter, E-cadherin homophilic interactions stimulate accumulation of other actin-binding proteins including formin, mDia, and Ena/Vasp to the contact zone, where they stimulate linear filament polymerization to drive contact expansion (Sahai and Marshall 2002;Kobielak et al 2004; 3 Scott et al 2006;Carramusa et al 2007).…”

Section: Introductionmentioning

confidence: 99%

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The β-actin mRNA zipcode regulates epithelial adherens junction assembly but not maintenance

Gutierrez

Eromobor

Petrie

et al. 2014

RNA

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Epithelial cell-cell contact stimulates actin cytoskeleton remodeling to down-regulate branched filament polymerization-driven lamellar protrusion and subsequently to assemble linear actin filaments required for E-cadherin anchoring during adherens junction complex assembly. In this manuscript, we demonstrate that de novo protein synthesis, the β-actin 3 ′ UTR, and the β-actin mRNA zipcode are required for epithelial adherens junction complex assembly but not maintenance. Specifically, we demonstrate that perturbing cell-cell contact-localized β-actin monomer synthesis causes epithelial adherens junction assembly defects. Consequently, inhibiting β-actin mRNA zipcode/ZBP1 interactions with β-actin mRNA zipcode antisense oligonucleotides, to intentionally delocalize β-actin monomer synthesis, is sufficient to perturb adherens junction assembly following epithelial cell-cell contact. Additionally, we demonstrate active RhoA, the signal required to drive zipcode-mediated β-actin mRNA targeting, is localized at epithelial cell-cell contact sites in a β-actin mRNA zipcode-dependent manner. Moreover, chemically inhibiting Src kinase activity prevents the local stimulation of β-actin monomer synthesis at cell-cell contact sites while inhibiting epithelial adherens junction assembly. Together, these data demonstrate that epithelial cell-cell contact stimulates β-actin mRNA zipcode-mediated monomer synthesis to spatially regulate actin filament remodeling, thereby controlling adherens junction assembly to modulate cell and tissue adhesion.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The β-actin mRNA zipcode regulates epithelial adherens junction assembly but not maintenance

Gutierrez

Eromobor

Petrie

et al. 2014

RNA

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“…When one then compares this to the reported specificity of the Ubr proteins, it appears that the yeast UBR1 protein exhibits a low specificity for acidic penultimate residues (Choi et al 2010), such that Ate1 products in yeast are suboptimal substrates for UBR1. Further investigations may reveal this apparent dichotomy may be to tune the half-life of protein substrates or may correlate with emerging alternative roles for protein arginylation (Cha-Molstad et al 2015;Cornachione et al 2014;Jiang et al 2016;Saha et al 2010;Zhang et al 2015).…”

Section: Recent Work Bymentioning

confidence: 99%

Emerging branches of the N-end rule pathways are revealing the sequence complexities of N-termini dependent protein degradation

Eldeeb

Leitao

Fahlman

2018

Biochem. Cell Biol.

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The N-end rule links the identity of the N-terminal amino acid of a protein to its in vivo half life as some N-terminal residues confer metabolic instability to a protein via their recognition by the cellular machinery that targets them for degradation. Since its discovery, the N-end rule has generally been defined as set of rules of whether an N-terminal residue is stabilizing or not.However, recent studies are revealing that the N-terminal code of amino acids conferring protein instability is more complex than previously appreciated as recent investigations are revealing that the identity of adjoining downstream residues can also influence the metabolic stability of N-end rule substrate. This is exemplified by the recent discovery of a new branch of N-end rule pathways that target proteins bearing N-terminal proline. In addition, recent investigations are demonstrating that the molecular machinery in N-termini dependent protein degradation may also target proteins for lysosomal degradation, in addition to proteasome dependent degradation.Herein, we describe some of the recent advances in N-end rule pathways discuss some of the implications regarding the emerging additional sequence requirements.

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“…Intriguingly, in many cases the destabilizing effect of arginylation on the corresponding target proteins in mouse was lacking and most arginylated N-terminal amino acids were not classical destabilizing residues in the context of the N-end rule pathway (23). In fact, arginylation of mammalian proteins can increase stability and influence oligomerization (25,26). In contrast, arginylation of glutamic acid residues can also target proteins via p62 (Sequestosome-1) binding to autophagy-mediated degradation in mammalian cell lines (27).…”

mentioning

confidence: 99%

Identification of Targets and Interaction Partners of Arginyl-tRNA Protein Transferase in the Moss Physcomitrella patens

Hoernstein

Mueller

Fiedler

et al. 2016

Molecular & Cellular Proteomics

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Protein arginylation is a posttranslational modification of both N-terminal amino acids of proteins and sidechain carboxylates and can be crucial for viability and physiology in higher eukaryotes. The lack of arginylation causes severe developmental defects in moss, affects the low oxygen response in Arabidopsis thaliana and is embryo lethal in Drosophila and in mice. Although several studies investigated impact and function of the responsible enzyme, the arginyltRNA protein transferase (ATE) in plants, identification of arginylated proteins by mass spectrometry was not hitherto achieved. In the present study, we report the identification of targets and interaction partners of ATE in the model plant Physcomitrella patens by mass spectrometry, employing two different immuno-affinity strategies and a recently established transgenic ATE:GUS reporter line (Schuessele et al., 2016 New Phytol., DOI: 10.1111/nph.13656). Here we use a commercially available antibody against the fused reporter protein (␤-glucuronidase) to pull down ATE and its interacting proteins and validate its in vivo interaction with a class I small heatshock protein via Fö rster resonance energy transfer (FRET). Additionally, we apply and modify a method that already successfully identified arginylated proteins from mouse proteomes by using custom-made antibodies specific for N-terminal arginine. As a result, we identify four arginylated proteins from Physcomitrella patens with high confidence.

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Arginylation Regulates Intracellular Actin Polymer Level by Modulating Actin Properties and Binding of Capping and Severing Proteins

Cited by 90 publications

References 50 publications

The β-actin mRNA zipcode regulates epithelial adherens junction assembly but not maintenance

The β-actin mRNA zipcode regulates epithelial adherens junction assembly but not maintenance

Emerging branches of the N-end rule pathways are revealing the sequence complexities of N-termini dependent protein degradation

Identification of Targets and Interaction Partners of Arginyl-tRNA Protein Transferase in the Moss Physcomitrella patens

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