Chemerin C9 peptide induces receptor internalization through a clathrin-independent pathway

Acta Pharmacologica Sinica

Volumn 35, Issue 5, 2014, Pages 653-663

  Zhou, Jun Xian ^a   Liao, Dan ^a   Zhang, Shuo ^a   Cheng, Ni ^b   He, Hui Qiong ^a   Ye, Richard D ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

calcium flux; chemerin; CMKLR1; endocytosis; ERK phosphorylation; GPCR; receptor internalization; receptor trafficking

Indexed keywords

ALANINE; CALCIUM ION; CHEMERIN; CHEMERIN C9; CLATHRIN; CMKLR1 RECEPTOR; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR KINASE; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; CALCIUM; CHEMOKINE RECEPTOR; CMKLR1 PROTEIN, HUMAN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL SURFACE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; HEK293 CELL LINE; HELA CELL LINE; HETEROLOGOUS EXPRESSION; IN VITRO STUDY; INTERNALIZATION; INTRACELLULAR SIGNALING; LEUKEMIA CELL LINE; MAST CELL LEUKEMIA; NONHUMAN; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; RAT; SITE DIRECTED MUTAGENESIS; ANIMAL; CELL LINE; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CALCIUM; CELL LINE; CELL LINE, TUMOR; CLATHRIN; ENDOCYTOSIS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; LEUKEMIA, BASOPHILIC, ACUTE; PHOSPHORYLATION; RATS; RECEPTORS, CHEMOKINE; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84908674697     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2013.198     Document Type: Article

References (40)

1. Gantz I, Konda Y, Yang YK, Miller DE, Dierick HA, Yamada T. Molecular cloning of a novel receptor (CMKLR1) with homology to the chemotactic factor receptors. Cytogenet Cell Genet 1996; 74: 286-90.
2. Samson M, Edinger AL, Stordeur P, Rucker J, Verhasselt V, Sharron M, et al. ChemR23, a putative chemoattractant receptor, is expressed in monocyte-derived dendritic cells and macrophages and is a coreceptor for SIV and some primary HIV-1 strains. Eur J Immunol 1998; 28: 1689-700.
3. Wittamer V, Franssen JD, Vulcano M, Mirjolet JF, Le Poul E, Migeotte I, et al . Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluids. J Exp Med 2003; 198: 977-85.
4. Meder W, Wendland M, Busmann A, Kutzleb C, Spodsberg N, John H, et al. Characterization of human circulating TIG2 as a ligand for the orphan receptor ChemR23. FEBS Lett 2003; 555: 495-9.
5. Bondue B, Wittamer V, Parmentier M. Chemerin and its receptors in leukocyte trafficking, inflammation and metabolism. Cytokine Growth Factor Rev 2011; 22: 331-8.
6. Zabel BA, Allen SJ, Kulig P, Allen JA, Cichy J, Handel TM, et al . Chemerin activation by serine proteases of the coagulation, fibrinolytic, and inflammatory cascades. J Biol Chem 2005; 280: 34661-6.
7. Guillabert A, Wittamer V, Bondue B, Godot V, Imbault V, Parmentier M, et al. Role of neutrophil proteinase 3 and mast cell chymase in chemerin proteolytic regulation. J Leukoc Biol 2008; 84: 1530-8.
8. Wittamer V, Bondue B, Guillabert A, Vassart G, Parmentier M, Communi D. Neutrophil-mediated maturation of chemerin: a link between innate and adaptive immunity. J Immunol 2005; 175: 487-93.
9. Vermi W, Riboldi E, Wittamer V, Gentili F, Luini W, Marrelli S, et al. Role of ChemR23 in directing the migration of myeloid and plasmacytoid dendritic cells to lymphoid organs and inflamed skin. J Exp Med 2005; 201: 509-15.
10. Parolini S, Santoro A, Marcenaro E, Luini W, Massardi L, Facchetti F, et al. The role of chemerin in the colocalization of NK and dendritic cell subsets into inflamed tissues. Blood 2007; 109: 3625-32.
11. Arita M, Ohira T, Sun YP, Elangovan S, Chiang N, Serhan CN. Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation. J Immunol 2007; 178: 3912-7.
12. Goralski KB, McCarthy TC, Hanniman EA, Zabel BA, Butcher EC, Parlee SD, et al. Chemerin, a novel adipokine that regulates adipogenesis and adipocyte metabolism. J Biol Chem 2007; 282: 28175-88.
13. Bozaoglu K, Bolton K, McMillan J, Zimmet P, Jowett J, Collier G, et al. Chemerin is a novel adipokine associated with obesity and metabolic syndrome. Endocrinology 2007; 148: 4687-94.
14. Wittamer V, Gregoire F, Robberecht P, Vassart G, Communi D, Parmentier M. The C-terminal nonapeptide of mature chemerin activates the chemerin receptor with low nanomolar potency. J Biol Chem 2004; 279: 9956-62.
15. Luangsay S, Wittamer V, Bondue B, De Henau O, Rouger L, Brait M, et al. Mouse ChemR23 is expressed in dendritic cell subsets and macrophages, and mediates an anti-inflammatory activity of chemerin in a lung disease model. J Immunol 2009; 183: 6489-99.
16. Shimamura K, Matsuda M, Miyamoto Y, Yoshimoto R, Seo T, Tokita S. Identification of a stable chemerin analog with potent activity toward ChemR23. Peptides 2009; 30: 1529-38.
17. Cash JL, Hart R, Russ A, Dixon JP, Colledge WH, Doran J, et al . Synthetic chemerin-derived peptides suppress inflammation through ChemR23. J Exp Med 2008; 205: 767-75.
18. Cash JL, Christian AR, Greaves DR. Chemerin peptides promote phagocytosis in a ChemR23- and Syk-dependent manner. J Immunol 2010; 184: 5315-24.
19. Koenig JA, Edwardson JM. Endocytosis and recycling of G protein-coupled receptors. Trends Pharmacol Sci 1997; 18: 276-87.
20. von Zastrow M. Mechanisms regulating membrane trafficking of G protein-coupled receptors in the endocytic pathway. Life Sci 2003; 74: 217-24.
21. Ostrom RS, Insel PA. The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br J Pharmacol 2004; 143: 235-45.
22. Tardif M, Mery L, Brouchon L, Boulay F. Agonist-dependent phosphorylation of N-formylpeptide and activation peptide from the fifth component of C (C5a) chemoattractant receptors in differentiated HL60 cells. J Immunol 1993; 150: 3534-45.
23. Prossnitz ER, Kim CM, Benovic JL, Ye RD. Phosphorylation of the N-formyl peptide receptor carboxyl terminus by the G protein-coupled receptor kinase, GRK2. J Biol Chem 1995; 270: 1130-7.
24. Ferguson SS, Downey WE 3rd, Colapietro AM, Barak LS, Ménard L, Caron MG. Role of beta-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science 1996; 271: 363-6.
25. Zabel BA, Nakae S, Zuniga L, Kim JY, Ohyama T, Alt C, et al. Mast cell-expressed orphan receptor CCRL2 binds chemerin and is required for optimal induction of IgE-mediated passive cutaneous anaphylaxis. J Exp Med 2008; 205: 2207-20.
26. Monnier J, Lewen S, O'Hara E, Huang K, Tu H, Butcher EC, et al . Expression, regulation, and function of atypical chemerin receptor CCRL2 on endothelial cells. J Immunol 2012; 189: 956-67.
27. Phonphok Y, Rosenthal KS. Stabilization of clathrin coated vesicles by amantadine, tromantadine and other hydrophobic amines. FEBS Lett 1991; 281: 188-90.
28. Tse SM, Furuya W, Gold E, Schreiber AD, Sandvig K, Inman RD, et al. Differential role of actin, clathrin, and dynamin in Fc gamma receptor-mediated endocytosis and phagocytosis. J Biol Chem 2003; 278: 3331-8.
29. McGookey DJ, Fagerberg K, Anderson RG. Filipin-cholesterol complexes form in uncoated vesicle membrane derived from coated vesicles during receptor-mediated endocytosis of low density lipoprotein. J Cell Biol 1983; 96: 1273-8.
30. Schnitzer JE, Oh P, Pinney E, Allard J. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol 1994; 127: 1217-32.
31. Benovic JL, Kuhn H, Weyand I, Codina J, Caron MG, Lefkowitz RJ. Functional desensitization of the isolated beta-adrenergic receptor by the beta-adrenergic receptor kinase: potential role of an analog of the retinal protein arrestin (48-kDa protein). Proc Natl Acad Sci U S A 1987; 84: 8879-82.
32. Lohse MJ, Benovic JL, Codina J, Caron MG, Lefkowitz RJ. beta-Arrestin: a protein that regulates beta-adrenergic receptor function. Science 1990; 248: 1547-50.
33. Rapacciuolo A, Suvarna S, Barki-Harrington L, Luttrell LM, Cong M, Lefkowitz RJ, et al. Protein kinase A and G protein-coupled receptor kinase phosphorylation mediates beta-1 adrenergic receptor endocytosis through different pathways. J Biol Chem 2003; 278: 35403-11.
34. Xue Y, Li A, Wang L, Feng H, Yao X. PPSP: prediction of PK-specific phosphorylation site with Bayesian decision theory. BMC Bioinformatics 2006; 7: 163.
35. Barak LS, Tiberi M, Freedman NJ, Kwatra MM, Lefkowitz RJ, Caron MG. A highly conserved tyrosine residue in G protein-coupled receptors is required for agonist-mediated beta 2-adrenergic receptor sequestration. J Biol Chem 1994; 269: 2790-5.
36. Daaka Y, Luttrell LM, Ahn S, Della Rocca GJ, Ferguson SS, Caron MG, et al. Essential role for G protein-coupled receptor endocytosis in the activation of mitogen-activated protein kinase. J Biol Chem 1998; 273: 685-8.
37. Schramm NL, Limbird LE. Stimulation of mitogen-activated protein kinase by G protein-coupled alpha(2)-adrenergic receptors does not require agonist-elicited endocytosis. J Biol Chem 1999; 274: 24935-40.
38. Kim SJ, Kim MY, Lee EJ, Ahn YS, Baik JH. Distinct regulation of internalization and mitogen-activated protein kinase activation by two isoforms of the dopamine D2 receptor. Mol Endocrinol 2004; 18: 640-52.
39. Barnea G, Strapps W, Herrada G, Berman Y, Ong J, Kloss B, et al. The genetic design of signaling cascades to record receptor activation. Proc Natl Acad Sci U S A 2008; 105: 64-9.
40. Del Prete A, Bonecchi R, Vecchi A, Mantovani A, Sozzani S. CCRL2, a fringe member of the atypical chemoattractant receptor family. Eur J Immunol 2013; 43: 1418-22.