Phosphorylation of C3a Receptor at Multiple Sites Mediates Desensitization, β-Arrestin-2 Recruitment and Inhibition of NF-κB Activity in Mast Cells
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{"title"=>"Phosphorylation of C3a Receptor at Multiple Sites Mediates Desensitization, β-Arrestin-2 Recruitment and Inhibition of NF-κB Activity in Mast Cells", "type"=>"journal", "authors"=>[{"first_name"=>"Kshitij", "last_name"=>"Gupta", "scopus_author_id"=>"57195437619"}, {"first_name"=>"Hariharan", "last_name"=>"Subramanian", "scopus_author_id"=>"13105794200"}, {"first_name"=>"Andreas", "last_name"=>"Klos", "scopus_author_id"=>"7006704994"}, {"first_name"=>"Hydar", "last_name"=>"Ali", "scopus_author_id"=>"35599375200"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84867544941", "doi"=>"10.1371/journal.pone.0046369", "sgr"=>"84867544941", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"23077507", "issn"=>"19326203", "pui"=>"365864417"}, "id"=>"6bef8f92-bc2b-3f71-9e27-ab52e8811fe3", "abstract"=>"BACKGROUND: Phosphorylation of G protein coupled receptors (GPCRs) by G protein coupled receptor kinases (GRKs) and the subsequent recruitment of β-arrestins are important for their desensitization. Using shRNA-mediated gene silencing strategy, we have recently shown that GRK2, GRK3 and β-arrestin-2 promote C3a receptor (C3aR) desensitization in human mast cells. We also demonstrated that β-arrestin-2 provides an inhibitory signal for NF-κB activation. C3aR possesses ten potential phosphorylation sites within its carboxyl terminus but their role on desensitization, β-arrestin recruitment and NF-κB activation has not been determined.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: We utilized a site directed mutagenesis approach in transfected HEK293 cells to determine the role of receptor phosphorylation on β-arrestin-2 recruitment and RBL-2H3 cells for functional studies. We found that although Ala substitution of Ser475/479, Thr480/481 residues resulted in 58±3.8% decrease in agonist-induced C3aR phosphorylation there was no change in β-arrestin-2 binding or receptor desensitization. By contrast, Ala substitution of Thr463, Ser465, Thr466 and Ser470 led to 40±1.3% decrease in agonist-induced receptor phosphorylation but this was associated with 74±2.4% decreases in β-arrestin-2 binding, significantly reduced desensitization and enhanced NF-κB activation. Combined mutation of these Ser/Thr residues along with Ser459 (mutant MT7), resulted in complete loss of receptor phosphorylation and β-arrestin-2 binding. RBL-2H3 cells expressing MT7 responded to C3a for greater Ca(2+) mobilization, degranulation and NF-κB activation when compared to the wild-type receptor. Interestingly, co-expression of MT7 with a constitutively active mutant of β-arrestin (R169E) inhibited C3a-induced degranulation by 28±2.4% and blocked NF-κB activation by 80±2.4%.\\n\\nCONCLUSION/SIGNIFICANCE: This study demonstrates that although C3a causes phosphorylation of its receptor at multiple sites, Ser459, Thr463, Ser465, Thr466 and Ser470 participate in C3aR desensitization, β-arrestin-2 recruitment and inhibition of NF-κB activity. Furthermore, β-arrestin-2 inhibits C3a-induced NF-κB activation via receptor desensitization-dependent and independent pathways.", "link"=>"http://www.mendeley.com/research/phosphorylation-c3a-receptor-multiple-sites-mediates-desensitization-%CE%B2arrestin2-recruitment-inhibiti", "reader_count"=>10, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>2, "Student > Ph. D. Student"=>1, "Student > Master"=>2, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>2, "Student > Ph. D. Student"=>1, "Student > Master"=>2, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>5, "Medicine and Dentistry"=>2, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>5}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/558238"], "description"=>"<p>(A) Schematic representation of the carboxyl-terminal domain of C3aR (WT) and mutants MT1–MT7 used for phosphorylation studies. (B) HEK293 cells transiently expressing HA-tagged C3aR or mutants were labeled with <sup>32</sup>P and exposed to buffer or C3a (100 nM, 37°C for 5 min), lysed and immunoprecipitated with anti-HA-antibody, resolved by 10% SDS-PAGE and transferred onto nitrocellulose membrane. Blots were then visualized by autoradiography to determine the extent of receptor phosphorylation. Western blotting was performed with anti-C3aR antibody to determine receptor expression (bottom panel). A representative blot from three independent experiments is shown. (C) Western blotting was performed with anti-C3aR antibody to determine receptor expression. Bars represent phosphorylation of C3aR and mutants normalized to respective total receptor expression. Data represent the mean ± SEM from three independent experiments. Statistical significance was determined by two way ANOVA with Bonferroni's post-hoc test. * indicates p<0.05 and ** indicates p<0.001.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Immune system proteins", "immunology", "Immune system", "Complement system", "Allergy and hypersensitivity", "Molecular cell biology", "Signal transduction", "Signaling cascades", "Calcium signaling cascade", "Protein kinase signaling cascade", "Signaling in cellular processes", "G-protein signaling", "Transmembrane signaling", "Signaling in selected disciplines", "Immunological signaling", "Membrane receptor signaling", "phosphorylation", "sites"], "article_id"=>228704, "categories"=>["Biological Sciences"], "users"=>["Kshitij Gupta", "Hariharan Subramanian", "Andreas Klos", "Hydar Ali"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046369.g001", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characterization_of_phosphorylation_sites_in_C3aR_/228704", "title"=>"Characterization of phosphorylation sites in C3aR.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 21:40:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/559061"], "description"=>"<p>(A) RBL-2H3 cells expressing MT7 were transiently transfected with GFP, βarrestin-2-GFP, or R169E-βarrestin-GFP. Cells were then stimulated with C3a (100 nM) for 30 min, and β-hexosaminidase release was determined. (B) Cells were also stimulated with C3a (100 nM) for 6 h, and NF-κB luciferase activity was determined. The data presented are mean ± SEM of three separate experiments performed in triplicate. Statistical significance was determined by two way ANOVA with Bonferroni's post-hoc test and unpaired two-tailed <i>t</i> test. * indicates p<0.05 ** indicates p<0.001.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Immune system proteins", "immunology", "Immune system", "Complement system", "Allergy and hypersensitivity", "Molecular cell biology", "Signal transduction", "Signaling cascades", "Calcium signaling cascade", "Protein kinase signaling cascade", "Signaling in cellular processes", "G-protein signaling", "Transmembrane signaling", "Signaling in selected disciplines", "Immunological signaling", "Membrane receptor signaling", "mutant", "inhibits", "c3a-degranulation"], "article_id"=>229536, "categories"=>["Biological Sciences"], "users"=>["Kshitij Gupta", "Hariharan Subramanian", "Andreas Klos", "Hydar Ali"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046369.g008", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Constitutively_active_mutant_of_946_arrestin_inhibits_C3a_degranulation_and_NF_954_B_activation_/229536", "title"=>"Constitutively active mutant of β-arrestin inhibits C3a-degranulation and NF-κB activation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 21:45:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/558524"], "description"=>"<p>RBL-2H3 Cells stably expressing either C3aR or mutants were exposed to buffer or different concentrations of C3a (1, 10, and 100 nM) and percent degranulation (β-hexosaminidase release) was determined. Data represent the mean ± SEM from three independent experiments. Statistical significance was determined by two way ANOVA with Bonferroni's post-hoc test. * indicates p<0.05 and ** indicates p<0.001.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Immune system proteins", "immunology", "Immune system", "Complement system", "Allergy and hypersensitivity", "Molecular cell biology", "Signal transduction", "Signaling cascades", "Calcium signaling cascade", "Protein kinase signaling cascade", "Signaling in cellular processes", "G-protein signaling", "Transmembrane signaling", "Signaling in selected disciplines", "Immunological signaling", "Membrane receptor signaling", "receptor", "phosphorylation", "c3a-induced"], "article_id"=>228986, "categories"=>["Biological Sciences"], "users"=>["Kshitij Gupta", "Hariharan Subramanian", "Andreas Klos", "Hydar Ali"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046369.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_receptor_phosphorylation_on_C3a_induced_degranulation_/228986", "title"=>"Effects of receptor phosphorylation on C3a-induced degranulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 21:42:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/558627"], "description"=>"<p>(A) Carboxyl terminus of WT-C3aR and a point mutant of Ser459 to Ala (MT8) are shown. (B). RBL-2H3 cells stably expressing either C3aR or MT8 were loaded with Indo-1 (1 µM) and Ca<sup>2+</sup> mobilization response following stimulation with C3a (100 nM) was determined. A representative traces from three independent experiments are shown. (B) Cells were exposed to buffer or C3a (100 nM) and percent degranulation (β-hexosaminidase release) was determined. Data represent the mean ± SEM from three independent experiments.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Immune system proteins", "immunology", "Immune system", "Complement system", "Allergy and hypersensitivity", "Molecular cell biology", "Signal transduction", "Signaling cascades", "Calcium signaling cascade", "Protein kinase signaling cascade", "Signaling in cellular processes", "G-protein signaling", "Transmembrane signaling", "Signaling in selected disciplines", "Immunological signaling", "Membrane receptor signaling", "ser459", "c3a-induced", "mobilization"], "article_id"=>229095, "categories"=>["Biological Sciences"], "users"=>["Kshitij Gupta", "Hariharan Subramanian", "Andreas Klos", "Hydar Ali"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046369.g004", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Role_of_Ser459_on_C3a_induced_Ca_2_mobilization_and_degranulation_/229095", "title"=>"Role of Ser459 on C3a-induced Ca<sup>2+</sup> mobilization and degranulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 21:42:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/558746"], "description"=>"<p>(A) HEK-293 cells transiently transfected with Flag-βarrestin-2 and HA-tagged WT-C3aR, or indicated C3aR mutants were exposed to buffer or C3a (100 nM) for 5 min. After chemical cross-linking with disuccinimidyl suberate (DSS), HA-tagged receptors were immunoprecipitated and probed with anti-Flag antibody (<i>Upper panel</i>). The membrane was then stripped and reprobed with anti-C3aR monoclonal antibody (<i>Middle panel</i>). Whole cell lysates were analyzed by Western blotting with anti-Flag antibodies to ensure equivalent expression of β-arrestin-2 in all samples (<i>Lower panel</i>). A representative blot from three independent experiments is shown. (B) Co-immunoprecipitation of β-arrestin-2 was quantified by densitometry using Image J software. Statistical significance was determined by one way ANOVA with Bonferroni's post-hoc test. * indicates p<0.05 and ** indicates p<0.001.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Immune system proteins", "immunology", "Immune system", "Complement system", "Allergy and hypersensitivity", "Molecular cell biology", "Signal transduction", "Signaling cascades", "Calcium signaling cascade", "Protein kinase signaling cascade", "Signaling in cellular processes", "G-protein signaling", "Transmembrane signaling", "Signaling in selected disciplines", "Immunological signaling", "Membrane receptor signaling", "c3ar", "phosphorylation"], "article_id"=>229217, "categories"=>["Biological Sciences"], "users"=>["Kshitij Gupta", "Hariharan Subramanian", "Andreas Klos", "Hydar Ali"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046369.g005", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Role_of_C3aR_phosphorylation_on_946_arrestin_2_recruitment_/229217", "title"=>"Role of C3aR phosphorylation on β-arrestin-2 recruitment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 21:43:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/558390"], "description"=>"<p>(A, B and C) RBL-2H3 cells stably expressing C3aR (Dark line) or mutants MT1, MT2 and MT7 (Red line) were loaded with Indo-1 (1 µM) and Ca<sup>2+</sup> mobilization response following stimulation with C3a (100 nM) was determined. (D) Shows peak Ca<sup>2+</sup> mobilization at 105–160 sec after stimulation. Data represent the mean ± SEM from three independent experiments. Statistical significance was determined by unpaired two-tailed <i>t</i> test * indicates p<0.05 ** indicates p<0.001.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Immune system proteins", "immunology", "Immune system", "Complement system", "Allergy and hypersensitivity", "Molecular cell biology", "Signal transduction", "Signaling cascades", "Calcium signaling cascade", "Protein kinase signaling cascade", "Signaling in cellular processes", "G-protein signaling", "Transmembrane signaling", "Signaling in selected disciplines", "Immunological signaling", "Membrane receptor signaling", "receptor", "phosphorylation", "c3a-induced", "mobilization", "rbl-2h3"], "article_id"=>228861, "categories"=>["Biological Sciences"], "users"=>["Kshitij Gupta", "Hariharan Subramanian", "Andreas Klos", "Hydar Ali"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046369.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_receptor_phosphorylation_on_C3a_induced_Ca_2_mobilization_in_RBL_2H3_cells_/228861", "title"=>"Effects of receptor phosphorylation on C3a-induced Ca<sup>2+</sup> mobilization in RBL-2H3 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 21:41:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/558975"], "description"=>"<p>RBL-2H3 cells stably expressing receptors (WT-C3aR, MT1, MT2, or MT7) were transiently transfected with NF-κB luciferase reporter gene construct. (A) Cells were stimulated with C3a (100 nM, 6 h) and NF-κB-dependent transcriptional activity was determined in cell lysates. Data presented are relative luciferase activity normalized to Renilla luciferase activity as is expressed as relative luciferase units. (B) Cells were stimulated with C3a (100 nM, 6 h) and CCL2 production was determined in the supernatant by ELISA. Data shown are mean ± SEM of three experiments performed in triplicate. Statistical significance was determined by two way ANOVA with Bonferroni's post-hoc test and unpaired two-tailed <i>t</i> test. * indicates p<0.05 ** indicates p<0.001.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Immune system proteins", "immunology", "Immune system", "Complement system", "Allergy and hypersensitivity", "Molecular cell biology", "Signal transduction", "Signaling cascades", "Calcium signaling cascade", "Protein kinase signaling cascade", "Signaling in cellular processes", "G-protein signaling", "Transmembrane signaling", "Signaling in selected disciplines", "Immunological signaling", "Membrane receptor signaling", "mutants", "mt1", "mt7", "enhanced", "c3a-induced", "activation", "ccl2"], "article_id"=>229437, "categories"=>["Biological Sciences"], "users"=>["Kshitij Gupta", "Hariharan Subramanian", "Andreas Klos", "Hydar Ali"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046369.g007", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_C3aR_mutants_MT1_and_MT7_show_enhanced_C3a_induced_NF_954_B_activation_and_CCL2_generation_/229437", "title"=>"C3aR mutants MT1 and MT7 show enhanced C3a-induced NF-κB activation and CCL2 generation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 21:44:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/558875"], "description"=>"<p>Cells stably expressing either WT-C3aR (A) or its mutants (B–D) were exposed to buffer (−C3a) or C3a (+C3a, 100 nM) for 5 min at 37°C. Cells were washed and C3aR expression was analyzed by flow cytometry. A representative histogram for each mutant from three independent experiments is shown. (E) Bar graph shows internalization of wild type and mutant C3aR expressed as the percentage loss of C3aR following exposure to C3a. Data represent the mean ± SEM from three experiments. Statistical significance was determined by two way ANOVA with Bonferroni's post-hoc test. * indicates p<0.05, ** indicates p<0.001.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Immune system proteins", "immunology", "Immune system", "Complement system", "Allergy and hypersensitivity", "Molecular cell biology", "Signal transduction", "Signaling cascades", "Calcium signaling cascade", "Protein kinase signaling cascade", "Signaling in cellular processes", "G-protein signaling", "Transmembrane signaling", "Signaling in selected disciplines", "Immunological signaling", "Membrane receptor signaling", "receptor", "internalization", "rbl-2h3", "cells", "expressing", "c3ar"], "article_id"=>229345, "categories"=>["Biological Sciences"], "users"=>["Kshitij Gupta", "Hariharan Subramanian", "Andreas Klos", "Hydar Ali"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046369.g006", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Agonist_induced_receptor_internalization_in_RBL_2H3_cells_expressing_C3aR_and_mutants_/229345", "title"=>"Agonist-induced receptor internalization in RBL-2H3 cells expressing C3aR and mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 21:44:01"}

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Relative Metric

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