Adaptor protein2 (AP2) orchestrates CXCR2-mediated cell migration

Traffic

Volumn 15, Issue 4, 2014, Pages 451-469

  Raman, Dayanidhi ^a,b   Sai, Jiqing ^a,b   Hawkins, Oriana ^a,b   Richmond, Ann ^a,b  

^a DEPARTMENT OF VETERANS AFFAIRS   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AP2; AP2 2; AP2 2; Chemotaxis; CXCR2; Internalization; PIP2 patches

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN 2; BETA ARRESTIN 1; CHEMOKINE RECEPTOR CXCR2; CLATHRIN; INTERLEUKIN 8; MEMBRANE PHOSPHOLIPID; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL; UNCLASSIFIED DRUG; PRIMER DNA;

ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL STRAIN HL 60; CHEMOTAXIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENDOCYTOSIS; HUMAN; HUMAN CELL; HYDROPHOBICITY; INTERNALIZATION; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; STABLE TRANSFECTION; GENETICS; HEK293 CELL LINE; HL 60 CELL LINE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS;

ADAPTOR PROTEIN COMPLEX 2; BASE SEQUENCE; CHEMOTAXIS; DNA PRIMERS; ENDOCYTOSIS; HEK293 CELLS; HL-60 CELLS; HUMANS; MUTAGENESIS, SITE-DIRECTED; RECEPTORS, INTERLEUKIN-8B;

EID: 84896755845     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12154     Document Type: Article

References (60)

1. Arai H, Charo IF. Differential regulation of G-protein-mediated signaling by chemokine receptors. J Biol Chem 1996;271:21814-21819.
2. Addison CL, Daniel TO, Burdick MD, Liu H, Ehlert JE, Xue YY, Buechi L, Walz A, Richmond A, Strieter RM. The CXC chemokine receptor 2, CXCR2, is the putative receptor for ELR+CXC chemokine-induced angiogenic activity. J Immunol 2000;165:5269-5277.
3. Devalaraja RM, Nanney LB, Du J, Qian Q, Yu Y, Devalaraja MN, Richmond A. Delayed wound healing in CXCR2 knockout mice. J Invest Dermatol 2000;115:234-244.
4. Matsuo Y, Raimondo M, Woodward TA, Wallace MB, Gill KR, Tong Z, Burdick MD, Yang Z, Strieter RM, Hoffman RM, Guha S. CXC-chemokine/CXCR2 biological axis promotes angiogenesis in vitro and in vivo in pancreatic cancer. Int J Cancer 2009;125:1027-1037.
5. Raman D, Baugher PJ, Thu YM, Richmond A. Role of chemokines in tumor growth. Cancer Lett 2007;256:137-165.
6. Strieter RM, Burdick MD, Mestas J, Gomperts B, Keane MP, Belperio JA. Cancer CXC chemokine networks and tumour angiogenesis. Eur J Cancer 2006;42:768-778.
7. Fan GH, Yang W, Wang XJ, Qian Q, Richmond A. Identification of a motif in the carboxyl terminus of CXCR2 that is involved in adaptin 2 binding and receptor internalization. Biochemistry 2001;40:791-800.
8. Traub LM. Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 2009;10:583-596.
9. Sai J, Fan GH, Wang D, Richmond A. The C-terminal domain LLKIL motif of CXCR2 is required for ligand-mediated polarization of early signals during chemotaxis. J Cell Sci 2004;117(Pt 23):5489-5496.
10. Collins BM, McCoy AJ, Kent HM, Evans PR, Owen DJ. Molecular architecture and functional model of the endocytic AP2 complex. Cell 2002;109:523-535.
11. Honing S, Ricotta D, Krauss M, Spate K, Spolaore B, Motley A, Robinson M, Robinson C, Haucke V, Owen DJ. Phosphatidylinositol-(4, 5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol Cell 2005;18:519-531.
12. Gaidarov I, Keen JH. Membrane targeting of endocytic adaptors: cargo and lipid do it together. Dev Cell 2005;8:801-802.
13. Kwiatkowska K. One lipid, multiple functions: how various pools of PI(4, 5)P(2) are created in the plasma membrane. Cell Mol Life Sci 2010;67:3927-3946.
14. Jackson LP, Kelly BT, McCoy AJ, Gaffry T, James LC, Collins BM, Honing S, Evans PR, Owen DJ. A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 2010;141:1220-1229.
15. Gaidarov I, Chen Q, Falck JR, Reddy KK, Keen JH. A functional phosphatidylinositol 3, 4, 5-trisphosphate/phosphoinositide binding domain in the clathrin adaptor AP-2 alpha subunit. Implications for the endocytic pathway. J Biol Chem 1996;271:20922-20929.
16. Gaidarov I, Keen JH. Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits. J Cell Biol 1999;146:755-764.
17. Abe N, Inoue T, Galvez T, Klein L, Meyer T. Dissecting the role of PtdIns(4, 5)P2 in endocytosis and recycling of the transferrin receptor. J Cell Sci 2008;121(Pt 9):1488-1494.
18. Rohde G, Wenzel D, Haucke V. A phosphatidylinositol (4, 5)-bisphosphate binding site within mu2-adaptin regulates clathrin-mediated endocytosis. J Cell Biol 2002;158:209-214.
19. Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 2003;72:395-447.
20. Krauss M, Kukhtina V, Pechstein A, Haucke V. Stimulation of phosphatidylinositol kinase type I-mediated phosphatidylinositol (4, 5)-bisphosphate synthesis by AP-2mu-cargo complexes. Proc Natl Acad Sci USA 2006;103:11934-11939.
21. Haas M, Askari A, Xie Z. Involvement of Src and epidermal growth factor receptor in the signal-transducing function of Na+/K+-ATPase. J Biol Chem 2000;275:27832-27837.
22. Kozik P, Francis RW, Seaman MN, Robinson MS. A screen for endocytic motifs. Traffic 2010;11:843-855.
23. Doray B, Lee I, Knisely J, Bu G, Kornfeld S. The gamma/sigma1 and alpha/sigma2 hemicomplexes of clathrin adaptors AP-1 and AP-2 harbor the dileucine recognition site. Mol Biol Cell 2007;18:1887-1896.
24. Sai J, Walker G, Wikswo J, Richmond A. The IL sequence in the LLKIL motif in CXCR2 is required for full ligand-induced activation of Erk, Akt, and chemotaxis in HL60 cells. J Biol Chem 2006;281:35931-35941.
25. Barwe SP, Anilkumar G, Moon SY, Zheng Y, Whitelegge JP, Rajasekaran SA, Rajasekaran AK. Novel role for Na, K-ATPase in phosphatidylinositol 3-kinase signaling and suppression of cell motility. Mol Biol Cell 2005;16:1082-1094.
26. Mueller SG, White JR, Schraw WP, Lam V, Richmond A. Ligand-induced desensitization of the human CXC chemokine receptor-2 is modulated by multiple serine residues in the carboxyl-terminal domain of the receptor. J Biol Chem 1997;272:8207-8214.
27. Ben-Baruch A, Grimm M, Bengali K, Evans GA, Chertov O, Wang JM, Howard OM, Mukaida N, Matsushima K, Oppenheim JJ. The differential ability of IL-8 and neutrophil-activating peptide-2 to induce attenuation of chemotaxis is mediated by their divergent capabilities to phosphorylate CXCR2 (IL-8 receptor B). J Immunol 1997;158:5927-5933.
28. Gurevich VV, Richardson RM, Kim CM, Hosey MM, Benovic JL. Binding of wild type and chimeric arrestins to the m2 muscarinic cholinergic receptor. J Biol Chem 1993;268:16879-16882.
29. Cheng ZJ, Zhao J, Sun Y, Hu W, Wu YL, Cen B, Wu GX, Pei G. Beta-arrestin differentially regulates the chemokine receptor CXCR4-mediated signaling and receptor internalization, and this implicates multiple interaction sites between beta-arrestin and CXCR4. J Biol Chem 2000;275:2479-2485.
30. Wu G, Krupnick JG, Benovic JL, Lanier SM. Interaction of arrestins with intracellular domains of muscarinic and alpha2-adrenergic receptors. J Biol Chem 1997;272:17836-17842.
31. Wu N, Macion-Dazard R, Nithianantham S, Xu Z, Hanson SM, Vishnivetskiy SA, Gurevich VV, Thibonnier M, Shoham M. Soluble mimics of the cytoplasmic face of the human V1-vascular vasopressin receptor bind arrestin2 and calmodulin. Mol Pharmacol 2006;70:249-258.
32. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25years of image analysis. Nat Methods 2012;9:671-675.
33. Motley AM, Berg N, Taylor MJ, Sahlender DA, Hirst J, Owen DJ, Robinson MS. Functional analysis of AP-2 alpha and mu2 subunits. Mol Biol Cell 2006;17:5298-5308.
34. Ricotta D, Conner SD, Schmid SL, von Figura K, Honing S. Phosphorylation of the AP2 mu subunit by AAK1 mediates high affinity binding to membrane protein sorting signals. J Cell Biol 2002;156:791-795.
35. Kelly BT, McCoy AJ, Spate K, Miller SE, Evans PR, Honing S, Owen DJ. A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 2008;456:976-979.
36. Zhao X, Greener T, Al-Hasani H, Cushman SW, Eisenberg E, Greene LE. Expression of auxilin or AP180 inhibits endocytosis by mislocalizing clathrin: evidence for formation of nascent pits containing AP1 or AP2 but not clathrin. J Cell Sci 2001;114(Pt 2):353-365.
37. Lau AW, Chou MM. The adaptor complex AP-2 regulates post-endocytic trafficking through the non-clathrin Arf6-dependent endocytic pathway. J Cell Sci 2008;121(Pt 24):4008-4017.
38. Fraile-Ramos A, Kohout TA, Waldhoer M, Marsh M. Endocytosis of the viral chemokine receptor US28 does not require beta-arrestins but is dependent on the clathrin-mediated pathway. Traffic 2003;4:243-253.
39. Chen B, Dores MR, Grimsey N, Canto I, Barker BL, Trejo J. Adaptor protein complex-2 (AP-2) and epsin-1 mediate protease-activated receptor-1 internalization via phosphorylation- and ubiquitination-dependent sorting signals. J Biol Chem 2011;286:40760-40770.
40. Owen DJ, Vallis Y, Pearse BM, McMahon HT, Evans PR. The structure and function of the beta 2-adaptin appendage domain. EMBO J 2000;19:4216-4227.
41. Schmid EM, Ford MG, Burtey A, Praefcke GJ, Peak-Chew SY, Mills IG, Benmerah A, McMahon HT. Role of the AP2 beta-appendage hub in recruiting partners for clathrin-coated vesicle assembly. PLoS Biol 2006;4:e262.
42. Thapa N, Anderson RA. PIP2 signaling, an integrator of cell polarity and vesicle trafficking in directionally migrating cells. Cell Adh Migr 2012;6:409-412.
43. Raman D, Neel NF, Sai J, Mernaugh RL, Ham AJ, Richmond AJ. Characterization of chemokine receptor CXCR2 interacting proteins using a proteomics approach to define the CXCR2 "chemosynapse". Methods Enzymol 2009;460:315-330.
44. Montagnac G, Meas-Yedid V, Irondelle M, Castro-Castro A, Franco M, Shida T, Nachury MV, Benmerah A, Olivo-Marin JC, Chavrier P. alphaTAT1 catalyses microtubule acetylation at clathrin-coated pits. Nature 2013;502:567-570.
45. Sai J, Raman D, Liu Y, Wikswo J, Richmond A. Parallel phosphatidylinositol 3-kinase (PI3K)-dependent and Src-dependent pathways lead to CXCL8-mediated Rac2 activation and chemotaxis. J Biol Chem 2008;283:26538-26547.
46. Wong K, Pertz O, Hahn K, Bourne H. Neutrophil polarization: spatiotemporal dynamics of RhoA activity support a self-organizing mechanism. Proc Natl Acad Sci USA 2006;103:3639-3644.
47. Van Keymeulen A, Wong K, Knight ZA, Govaerts C, Hahn KM, Shokat KM, Bourne HR. To stabilize neutrophil polarity, PIP3 and Cdc42 augment RhoA activity at the back as well as signals at the front. J Cell Biol 2006;174:437-445.
48. Onsum MD, Wong K, Herzmark P, Bourne HR, Arkin AP. Morphology matters in immune cell chemotaxis: membrane asymmetry affects amplification. Phys Biol 2006;3:190-199.
49. Carlton JG, Cullen PJ. Coincidence detection in phosphoinositide signaling. Trends Cell Biol 2005;15:540-547.
50. Ahle S, Mann A, Eichelsbacher U, Ungewickell E. Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO J 1988;7:919-929.
51. Keen JH. Clathrin and associated assembly and disassembly proteins. Annu Rev Biochem 1990;59:415-438.
52. Haucke V, Wenk MR, Chapman ER, Farsad K, De Camilli P. Dual interaction of synaptotagmin with mu2- and alpha-adaptin facilitates clathrin-coated pit nucleation. EMBO J 2000;19:6011-6019.
53. Montagnac G, de Forges H, Smythe E, Gueudry C, Romao M, Salamero J, Chavrier P. Decoupling of activation and effector binding underlies ARF6 priming of fast endocytic recycling. Curr Biol 2011;21:574-579.
54. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007;8:603-612.
55. Sauvonnet N, Dujeancourt A, Dautry-Varsat A. Cortactin and dynamin are required for the clathrin-independent endocytosis of gammac cytokine receptor. J Cell Biol 2005;168:155-163.
56. Neel NF, Sai J, Ham AJ, Sobolik-Delmaire T, Mernaugh RL, Richmond A. IQGAP1 is a novel CXCR2-interacting protein and essential component of the "chemosynapse". PLoS One 2011;6:e23813.
57. Schraufstatter IU, Chung J, Burger M. IL-8 activates endothelial cell CXCR1 and CXCR2 through Rho and Rac signaling pathways. Am J Physiol Lung Cell Mol Physiol 2001;280:L1094-L1103.
58. Nesterov A, Carter RE, Sorkina T, Gill GN, Sorkin A. Inhibition of the receptor-binding function of clathrin adaptor protein AP-2 by dominant-negative mutant mu2 subunit and its effects on endocytosis. EMBO J 1999;18:2489-2499.
59. Raman D, Sai J, Neel NF, Chew CS, Richmond A. LIM and SH3 protein-1 modulates CXCR2-mediated cell migration. PLoS One 2010;5:e10050.
60. Smith AL, Friedman DB, Yu H, Carnahan RH, Reynolds AB. ReCLIP (reversible cross-link immuno-precipitation): an efficient method for interrogation of labile protein complexes. PLoS One 2011;6:e16206.