ARF6 activated by the LHCG receptor through the cytohesin family of guanine nucleotide exchange factors mediates the receptor internalization and signaling

Journal of Biological Chemistry

Volumn 287, Issue 24, 2012, Pages 20443-20455

  Kanamarlapudi, Venkateswarlu ^a   Thompson, Aiysha ^a   Kelly, Eamonn ^b   Bernal, Andrés López ^b  

^a SWANSEA UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADP-RIBOSYLATION FACTORS; CLATHRINS; DOMINANT-NEGATIVE MUTANTS; DYNAMIN; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HETEROTRIMERIC G-PROTEIN; INHIBITORY PEPTIDES; INTACT CELLS; MUTANT PROTEINS; PHARMACOLOGICAL INHIBITORS; PHOSPHATIDYLINOSITOL; SIGNALING PATHWAYS; WORTMANNIN;

PEPTIDES;

CHEMICAL ACTIVATION;

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CHORIONIC GONADOTROPIN RECEPTOR; CLATHRIN; CYCLIC AMP; CYTOHESIN PROTEIN; DYNAMIN; DYNASORE; GALLEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; LUTEINIZING HORMONE CHORIONIC GONADOTROPIN RECEPTOR; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN INHIBITOR; QS 11; SECIN H3; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; WORTMANNIN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ADP-RIBOSYLATION FACTORS; CHORIONIC GONADOTROPIN; CLATHRIN; CYCLIC AMP; DYNAMINS; GELSOLIN; GTPASE-ACTIVATING PROTEINS; HUMANS; NM23 NUCLEOSIDE DIPHOSPHATE KINASES; PEPTIDE FRAGMENTS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; RECEPTORS, LH; SIGNAL TRANSDUCTION;

EID: 84861623717     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.362087     Document Type: Article

References (58)

1. Oldham, W. M., and Hamm, H. E. (2008) Heterotrimeric G protein activation by G-protein-coupled receptors. Nat. Rev. Mol. Cell Biol. 9, 60-71
2. Smrcka, A. V. (2008) G protein βγ subunits: central mediators of G protein- coupled receptor signaling. Cell Mol. Life Sci. 65, 2191-2214
3. Taniguchi, C. M., Emanuelli, B., and Kahn, C. R. (2006) Critical nodes in signaling pathways: insights into insulin action. Nat. Rev. Mol. Cell Biol. 7, 85-96 (Pubitemid 43278292)
4. Hawkins, P. T., and Stephens, L. R. (2007) PI3Kγ is a key regulator of inflammatory responses and cardiovascular homeostasis. Science 318, 64-66 (Pubitemid 47538006)
5. Okada, T., Kawano, Y., Sakakibara, T., Hazeki, O., and Ui, M. (1994) Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin. J. Biol. Chem. 269, 3568-3573
6. Ascoli, M., Fanelli, F., and Segaloff, D. L. (2002) The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr. Rev. 23, 141-174 (Pubitemid 34299022)
7. Wang, H., Segaloff, D. L., and Ascoli, M. (1991) Lutropin/ choriogonadotropin down-regulates its receptor by both receptor-mediated endocytosis and a cAMP-dependent reduction in receptor mRNA. J. Biol. Chem. 266, 780-785 (Pubitemid 21907183)
8. Hanyaloglu, A. C., and von Zastrow, M. (2008) Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu. Rev. Pharmacol. Toxicol. 48, 537-568 (Pubitemid 351738163)
9. Gurevich, V. V., and Gurevich, E. V. (2006) The structural basis of arrestin- mediated regulation of G-protein-coupled receptors. Pharmacol. Ther. 110, 465-502
10. Min, L., and Ascoli, M. (2000) Effect of activating and inactivating mutations on the phosphorylation and trafficking of the human lutropin/choriogonadotropin receptor. Mol. Endocrinol. 14, 1797-1810
11. Hunzicker-Dunn, M., Gurevich, V. V., Casanova, J. E., and Mukherjee, S. (2002) ARF6: a newly appreciated player in G protein-coupled receptor desensitization. FEBS Lett. 521, 3-8 (Pubitemid 34628447)
12. Moss, J., and Vaughan, M. (1998) Molecules in the ARF orbit. J. Biol. Chem. 273, 21431-21434 (Pubitemid 28405306)
13. Donaldson, J. G., Finazzi, D., and Klausner, R. D. (1992) Brefeldin A inhibits Golgi membrane-catalyzed exchange of guanine nucleotide onto ARF protein. Nature 360, 350-352 (Pubitemid 23000673)
14. Zeeh, J. C., Zeghouf, M., Grauffel, C., Guibert, B., Martin, E., Dejaegere, A., and Cherfils, J. (2006) Dual specificity of the interfacial inhibitor brefeldin a for arf proteins and sec7 domains. J. Biol. Chem. 281, 11805-11814 (Pubitemid 43855440)
15. Hafner, M., Schmitz, A., Grüne, I., Srivatsan, S. G., Paul, B., Kolanus, W., Quast, T., Kremmer, E., Bauer, I., and Famulok, M. (2006) Inhibition of cytohesins by SecinH3 leads to hepatic insulin resistance. Nature 444, 941-944 (Pubitemid 46025008)
16. Zhang, Q., Major, M. B., Takanashi, S., Camp, N. D., Nishiya, N., Peters, E. C., Ginsberg, M. H., Jian, X., Randazzo, P. A., Schultz, P. G., Moon, R. T., and Ding, S. (2007) Small-molecule synergist of the Wnt/β-catenin signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 104, 7444-7448 (Pubitemid 47185925)
17. Venkateswarlu, K., Oatey, P. B., Tavaré, J. M., Jackson, T. R., and Cullen, P. J. (1999) Identification of centaurin-α1 as a potential in vivo phosphatidylinositol 3,4,5-trisphosphate-binding protein that is functionally homologous to the yeast ADP-ribosylation factor (ARF) GTPase-activating protein, Gcs1. Biochem. J. 340, 359-363 (Pubitemid 29286552)
18. Venkateswarlu, K., Gunn-Moore, F., Oatey, P. B., Tavaré, J. M., and Cullen, P. J. (1998) Nerve growth factor- and epidermal growth factor-stimulated translocation of the ADP-ribosylation factor-exchange factor GRP1 to the plasma membrane of PC12 cells requires activation of phosphatidylinositol 3-kinase and the GRP1 pleckstrin homology domain. Biochem. J. 335, 139-146
19. Venkateswarlu, K., Oatey, P. B., Tavaré, J. M., and Cullen, P. J. (1998) Insulin-dependent translocation of ARNO to the plasma membrane of adipocytes requires phosphatidylinositol 3-kinase. Curr. Biol. 8, 463-466 (Pubitemid 28181124)
20. Cullen, P. J., and Venkateswarlu, K. (1999) Potential regulation of ADP-ribosylation factor 6 signaling by phosphatidylinositol 3,4,5-trisphosphate. Biochem. Soc Trans. 27, 683-689 (Pubitemid 29412514)
21. Venkateswarlu, K., and Cullen, P. J. (2000) Signalling via ADP-ribosylation Factor G lies downstream of phosphatidylinositide 3-kinase. Biochem. J. 345, 719-724 (Pubitemid 30099104)
22. Claing, A. (2004) Regulation ofGprotein-coupled receptor endocytosis by ARF6 GTP-binding proteins. Biochem. Cell Biol. 82, 610-617
23. Venkateswarlu, K., Brandom, K. G., and Lawrence, J. L. (2004) Centaurin-alpha1 is an in vivo phosphatidylinositol 3,4,5-trisphosphate- dependent GTPase-activating protein for ARF6 that is involved in actin cytoskeleton organization. J. Biol. Chem. 279, 6205-6208 (Pubitemid 38248750)
24. Lawrence, J., Mundell, S. J., Yun, H., Kelly, E., and Venkateswarlu, K. (2005) Centaurin-α1, an ADP-ribosylation factor 6 GTPase-activating protein, inhibits β2-adrenoceptor internalization. Mol. Pharmacol. 67, 1822-1828 (Pubitemid 41007763)
25. Venkateswarlu, K. (2003) Interaction protein for cytohesin exchange factors 1 (IPCEF1) binds cytohesin 2 and modifies its activity. J. Biol. Chem. 278, 43460-43469
26. Benmerah, A., Bayrou, M., Cerf-Bensussan, N., and Dautry-Varsat, A. (1999) Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112, 1303-1311 (Pubitemid 29243453)
27. Volpicelli-Daley, L. A., Li, Y., Zhang, C. J., and Kahn, R. A. (2005) Isoform-selective effects of the depletion of ADP-ribosylation factors 1-5 on membrane traffic. Mol. Biol. Cell 16, 4495-4508 (Pubitemid 41416436)
28. Hashimoto, S., Onodera, Y., Hashimoto, A., Tanaka, M., Hamaguchi, M., Yamada, A., and Sabe, H. (2004) Requirement for Arf6 in breast cancer invasive activities. Proc. Natl. Acad. Sci. U.S.A. 101, 6647-6652 (Pubitemid 38586028)
29. Venkateswarlu, K. (2005) Analysis of the interaction between cytohesin 2 and IPCEF1. Methods Enzymol. 404, 252-266
30. Galas, M. C., Helms, J. B., Vitale, N., Thiersé, D., Aunis, D., and Bader, M. F. (1997) Regulated exocytosis in chromaffin cells. A potential role for a secretory granule-associated ARF6 protein. J. Biol. Chem. 272, 2788-2793 (Pubitemid 27053323)
31. Derossi, D., Chassaing, G., and Prochiantz, A. (1998) Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol. 8, 84-87 (Pubitemid 28056816)
32. Kagan, J. C., and Medzhitov, R. (2006) Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125, 943-955 (Pubitemid 43795199)
33. Klausner, R. D., Donaldson, J. G., and Lippincott-Schwartz, J. (1992) Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116, 1071-1080
34. Abel, K., Anderson, R. A., and Shears, S. B. (2001) Phosphatidylinositol and inositol phosphate metabolism. J. Cell Sci. 114, 2207-2208 (Pubitemid 32633692)
35. Stephens, L., Smrcka, A., Cooke, F. T., Jackson, T. R., Sternweis, P. C., and Hawkins, P. T. (1994) A novel phosphoinositide 3 kinase activity in myeloid- derived cells is activated by G protein βγ subunits. Cell 77, 83-93 (Pubitemid 24184690)
36. Naga Prasad, S. V., Barak, L. S., Rapacciuolo, A., Caron, M. G., and Rockman, H. A. (2001) Agonist-dependent recruitment of phosphoinositide 3-kinase to the membrane by β-adrenergic receptor kinase 1. A role in receptor sequestration. J. Biol. Chem. 276, 18953-18959
37. Yano, H., Nakanishi, S., Kimura, K., Hanai, N., Saitoh, Y., Fukui, Y., Nonomura, Y., and Matsuda, Y. (1993) Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem. 268, 25846-25856 (Pubitemid 23358203)
38. Lehmann, D. M., Seneviratne, A. M., and Smrcka, A. V. (2008) Small molecule disruption of G protein βγ subunit signaling inhibits neutrophil chemotaxis and inflammation. Mol. Pharmacol. 73, 410-418 (Pubitemid 351159211)
39. Bonacci, T. M., Mathews, J. L., Yuan, C., Lehmann, D. M., Malik, S., Wu, D., Font, J. L., Bidlack, J. M., and Smrcka, A. V. (2006) Differential targeting of Gβγ-subunit signaling with small molecules. Science 312, 443-446
40. Venkateswarlu, K., Gunn-Moore, F., Tavaré, J. M., and Cullen, P. J. (1999) EGF-and NGF-stimulated translocation of cytohesin-1 to the plasma membrane of PC12 cells requires PI 3-kinase activation and a functional cytohesin-1 PH domain. J. Cell Sci. 112, 1957-1965 (Pubitemid 29338820)
41. Lazari, M. F., Bertrand, J. E., Nakamura, K., Liu, X., Krupnick, J. G., Benovic, J. L., and Ascoli, M. (1998) Mutation of individual serine residues in the C-terminal tail of the lutropin/choriogonadotropin receptor reveal distinct structural requirements for agonist-induced uncoupling and agonist- induced internalization. J. Biol. Chem. 273, 18316-18324 (Pubitemid 28334756)
42. D'Souza-Schorey, C., and Chavrier, P. (2006) ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358
43. Palacios, F., Schweitzer, J. K., Boshans, R. L., and D'Souza-Schorey, C. (2002) ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nat. Cell Biol. 4, 929-936 (Pubitemid 35469422)
44. Krauss, M., Kinuta, M., Wenk, M. R., De Camilli, P., Takei, K., and Haucke, V. (2003) ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Iγ. J. Cell Biol. 162, 113-124 (Pubitemid 36859539)
45. Paleotti, O., Macia, E., Luton, F., Klein, S., Partisani, M., Chardin, P., Kirchhausen, T., and Franco, M. (2005) The small G-protein Arf6GTP recruits the AP-2 adaptor complex to membranes. J. Biol. Chem. 280, 21661-21666 (Pubitemid 40805736)
46. Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C., and Kirchhausen, T. (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850 (Pubitemid 43779110)
47. Fu, H., Björkman, L., Janmey, P., Karlsson, A., Karlsson, J., Movitz, C., and Dahlgren, C. (2004) The two neutrophil members of the formylpeptide receptor family activate the NADPH-oxidase through signals that differ in sensitivity to a gelsolin-derived phosphoinositide-binding peptide. BMC Cell Biol. 5, 50
48. Bhaskaran, R. S., and Ascoli, M. (2005) The post-endocytotic fate of the gonadotropin receptors is an important determinant of the desensitization of gonadotropin responses. J. Mol. Endocrinol. 34, 447-457 (Pubitemid 40585194)
49. Poupart, M. E., Fessart, D., Cotton, M., Laporte, S. A., and Claing, A. (2007) ARF6 regulates angiotensin II type 1 receptor endocytosis by controlling the recruitment of AP-2 and clathrin. Cell Signal. 19, 2370-2378 (Pubitemid 47361691)
50. Claing, A., Chen, W., Miller, W. E., Vitale, N., Moss, J., Premont, R. T., and Lefkowitz, R. J. (2001) β-Arrestin-mediated ADP-ribosylation factor 6 activation and β2-adrenergic receptor endocytosis. J. Biol. Chem. 276, 42509-42513
51. Houndolo, T., Boulay, P. L., and Claing, A. (2005) G protein-coupled receptor endocytosis in ADP-ribosylation factor 6-depleted cells. J. Biol. Chem. 280, 5598-5604 (Pubitemid 40280038)
52. Svensson, H. G., West, M. A., Mollahan, P., Prescott, A. R., Zaru, R., and Watts, C. (2008) A role for ARF6 in dendritic cell podosome formation and migration. Eur. J. Immunol. 38, 818-828
53. Frank, S., Upender, S., Hansen, S. H., and Casanova, J. E. (1998) ARNO is a guanine nucleotide exchange factor for ADP-ribosylation factor 6. J. Biol. Chem. 273, 23-27 (Pubitemid 28042170)
54. Mukherjee, S., Gurevich, V. V., Jones, J. C., Casanova, J. E., Frank, S. R., Maizels, E. T., Bader, M. F., Kahn, R. A., Palczewski, K., Aktories, K., and Hunzicker-Dunn, M. (2000) The ADP ribosylation factor nucleotide exchange factor ARNO promotes β-arrestin release necessary for luteinizing hormone/choriogonadotropin receptor desensitization. Proc. Natl. Acad. Sci. U.S.A. 97, 5901-5906 (Pubitemid 30367496)
55. Rameh, L. E., and Cantley, L. C. (1999) The role of phosphoinositide 3-kinase lipid products in cell function. J. Biol. Chem. 274, 8347-8350 (Pubitemid 29164617)
56. Fazioli, F., Minichiello, L., Matoskova, B., Wong, W. T., and Di Fiore, P. P. (1993) eps15, a novel tyrosine kinase substrate, exhibits transforming activity. Mol. Cell. Biol. 13, 5814-5828 (Pubitemid 23260682)
57. Chen, H., Slepnev, V. I., Di Fiore, P. P., and De Camilli, P. (1999) The interaction of epsin and Eps15 with the clathrin adaptor AP-2 is inhibited by mitotic phosphorylation and enhanced by stimulation-dependent dephosphorylation in nerve terminals. J. Biol. Chem. 274, 3257-3260 (Pubitemid 29077157)
58. Di Fiore, P. P., and De Camilli, P. (2001) Endocytosis and signaling. an inseparable partnership. Cell 106, 1-4