Abstract
In addition to its roles in changes in the actin cytoskeleton and lipid metabolism at the plasma membrane, recent results suggest that Arf6 also participates in desensitization and internalization of G-protein-coupled receptors. The evidence to support this novel function for Arf6 is reviewed in this chapter.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Abdulaev, N. G., and Ridge, K. D. (1998). Light-induced exposure of the cytoplasmic end of transmembrane helix seven in rhodopsin. Proc. Natl. Acad. Sci., USA, 95, 12854–12859.
Abell, A. N. and Segaloff, D. L. (1997). Evidence for the direct involvement of transmembrane region 6 and the lutropin/choriogonadotropin receptor in activating Gs. J. Biol. Chem., 272, 14586–14591.
Altenbach, C., Cai, K., Khorana, H. G., and Hubbell, W. L. (1999). Structural features and light-dependent changes in the sequence 306–322 extending from helix VII to the palmitoylation sites in rhodopsin: a site-directed spin-labeling study. Biochemistry, 38, 7931–7937.
Anderson, W. B. and Jaworski, C. J. (1979). Isoproterenol-induced desensitization of adenylate cyclase responsiveness in a cell-free system. J. Biol. Chem., 254, 4596–4601.
Austin, C., Boehm, M., and Tooze, S. A. (2002). Site-specific cross-linking reveals a differential direct interaction of class 1, 2, and 3 ADP-ribosylation factors with adaptor protein complexes 1 and 3. Biochemistry, 41, 4669–4677.
Ballesteros, J. A., Jensen, A. D., Liapakis, G., Rasmussen, S. G., Shi, L., Gether, U., and Javitch, J. A. (2001). Activation of the beta 2-adrenergic receptor involves disruption of an ionic lock between the cytoplasmic ends of transmembrane segments 3 and 6. J. Biol. Chem., 276, 29171–29177.
Barak, L. S., Ferguson, S. S., Zhang, J., and Caron, M. G. (1997). A beta-arrestin/green fluorescent protein biosensor for detecting a G protein-coupled receptor activation. J. Biol. Chem., 272, 27497–27500.
Barak, L. S., Warabi, K., Feng, X., Caron, M. G., and Kwatra, M. M. (1999). Real-time visualization of the cellular redistribution of G protein-coupled receptor kinase 2 and beta-arrestin 2 during homologous desensitization of the substance P receptor. J. Biol. Chem., 274, 7565–7569.
Bennett, T. A., Maestas, D. C., and Prossnitz, E. R. (2000). Arrestin binding to the G protein-coupled N-formyl peptode receptor is regulated by the conserved “DRY” sequence. J. Biol. Chem., 275, 24590–24594.
Bhatnagar, A., Willins, D. L., Gray, J. A., Woods, J., Benovic, J. L., and Roth, B. L. (2001). The dynamin-dependent, arrestin-independent Internalization of 5-hydroxytryptamine 2A (5-HT2A) serotonin receptors reveals differential sorting of arrestins and 5-HT2 Areceptors during endocytosis. J. Biol. Chem., 276, 8269–8277.
Bockaert, J., Hunzicker-Dunn, M., and Birnbaumer, L. (1976). Hormone-stimulated desensitization of hormone-dependent adenylyl cyclase. J. Biol. Chem., 251, 2653–2663.
Bohn, L. M., Gainetdinov, R. R., Lin, F. T., Lefkowitz, R. J., and Caron, M. G. (2000). Muopioid receptor desensitization by beta-arrestin-2 determines morphine tolerance but not dependence. Nature, 408, 720–723.
Brown, F. D., Rozelle, A. L., Yin, H. L., Balla, T., and Donaldson, J. G. (2001). Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J. Cell. Biol., 154, 1007–1017.
Carmen, C. V. and Benovic, J. L. (1999). G-protein-coupled receptors: turn-ons and turn-offs. Curr. Opin. Neurobiol., 8, 335–344.
Caumont, A.-S., Galas, M.-C., Vitale, N., Aunis, D., and Bader, M.-F. (1998). Regulated exocytosis in chromaffin cells.Translocation of ARF6 stimulates a plasma membrane-associated phosphlipase D. J. Biol. Chem., 273, 1373–1379.
Cavenagh, M. M., Whitney, J. A., Carroll, K., Zhang, C., Boman, A. L., Rosenwald, A. G., Mellman, I., and Kahn, R. A. (1996). Intracellular distribution of Arf proteins in mammalian cells. J. Biol. Chem., 271, 21767–21774.
Celver, J., Vishnivetskiy, S. A., Chavkin, C., and Gurevich, V. V. (2002). Conservation of the phosphate-sensitive elements in the arrestin family of proteins. J. Biol. Chem., 277, 9043–9048.
Chen, W., Hu, L. A., Semenov, M. V., Yanagawa, S., Kikuchi, A., Lefkowitz, R. J., and Miller, W. E. (2001). β-Arrestinl modulates lymphoid enhancer factor transcriptional activity through interaction with phosphorylated dishevelled proteins. Proc. Natl. Acad. Sci., USA, 98, 14889–14894.
Cheng, Z.-J., Yu, Q.-M., Wu, Y.-L., Ma, L., and Pei, G. (1998). Selective interference of β-arrestin 1 with κ and δ but not μ opiod receptor/G protein coupling. J. Biol. Chem., 273, 24328–24333.
Claing, A., Chen, W., Miller, W. E., Vitale, N., Moss, J., Premont, R. T., and Lefkowitz, R. J. (2001). β arrestin-mediated ARF6 activation and β2-adrenergic receptor endocytosis. J. Biol. Chem. 276, 42509–42513.
Claing, A., Laporte, S. A., Caron, M. G., and Lefkowitz, R. J. (2002). Endocytosis of G protein-coupled receptors: roles of G protein-coupled receptor kinases and beta-arrestin proteins. Prog. Neurobiol., 66, 61–79.
Conner, D. A., Mathier, M. A., Mortensen, R. M., Christe, M., Vatner, S. F., Seidman, C. E., and Seidman, J. G. (1997). β-Arrestin1 knockout mice appear normal but demonstrate altered cardiac responses to β-adrenergic stimulation. Circ. Res., 81, 1021–1026.
D’Souza-Schorey, C., van Donselaar, E., Hsu, V. W., Yang, C., Stahl, P. D., and Peters, P. J. (1998). ARF6 targets recycling vesicles to the plasma membrane: insights from an ultrastructural investigation. J. Cell Biol., 140, 603–616.
Drake, M. T., Zhu, Y., and Kornfeld, S. (2000). The assembly of AP-3 adaptor complex-containing clathrin-coated vesicles on synthetic liposomes. Mol. Biol. Cell, 11, 3723–3736.
Dulin, N. O., Niu, J., Browning, D. D., Ye, R. D., and Voyno-Yasenetskaya, T. (2001). Cyclic AMP-independent Activation of Protein Kinase A by Vasoactive Peptides. J. Biol. Chem., 276, 20827–20830.
Ekstrom, R. C., Carney, E. M., Lamm, M. L. G., and Hunzicker-Dunn, M. (1992). Reversal of the desensitized state of pig ovarian follicular human choriogonadotropin-sensitive adenylylcyclase by guanosine 5′-0-(2-thiodiphosphate). J. Biol. Chem., 267, 22183–22189.
Ekstrom, R. C. and Hunzicker-Dunn, M. (1989). Homologous desensitization of ovarian luteinizing hormone/human chorionic gonadotropin-responsive adenylyl cyclase is dependent upon GTP. Endocrinology, 124, 956–963.
Ekstrom, R. C. and Hunzicker-Dunn, M. (1990). Opposing effects of ethanol on pig ovarian adenylyl cyclase desensitized by human choriogonadotropin or isoproterenol. Endocrinology., 127, 2578–2586.
Evans, N. A., Groarke, D. A., Warrack, J., Greenwood, C. J., Dodgson, K., Milligan, G., and Wilson, S. (2001). Visualizing differences in ligand-induced beta-arrestin-GFP interactions and trafficking between three recently characterized G protein-coupled receptors. J. Neurochem., 77, 476–485.
Ezra, E. and Salomon, Y. (1980). Mechanism of desensitization of adenylate cyclase by lutropin. J. Biol. Chem., 255, 653–658.
Ezra, E. and Salomon, Y. (1981). Mechanism of desensitization of adenylate cyclase by lutropin. J. Biol. Chem., 256, 5377–5382.
Ferguson, S. S. G. (2001). Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharm. Rev., 53, 1–24.
Ferguson, S. S. G., Barak, L. S., Zhang, J., and Caron, M. G. (1996). G-protein-coupled receptor regulation: role of G-protein-coupled receptor kinases and arrestins. Can. J. Physiol. Pharmacol., 74, 1094–1110.
Ferrari, S. L. and Bisello, A. (2001). Cellular distribution of constitutively active mutant parathyroid hormone (PTH)/PTH-related protein receptors and regulation of cyclic adenosine 3′,5′-monophosphate signaling by β-arrestin2. Mol. Endo., 15, 149–163.
Franco, M., Peters, P. J., Boretto, J., van Donselaar, E., Neri, A., D’Souza-Schorey, C., and Chavrier, P. (1999). EFA6, a sec7 domain-containing exchange factor for ARF6, coordinates membrane recycling and actin cytoskeleton organization. EMBO J., 18, 1480–1491.
Frank, S. R., Hatfield, J. C., and Casanova, J. E. (1998). Remodeling of the actin cytoskeleton is coordinately regulated by protein kinase C and the ADP-ribosylation factor nucleotide exchange factor ARNO. Mol. Biol. Cell, 9, 3133–3146.
Galas, M.-C., Helms, J. B., Vitale, N., Thierse, 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.
Godi, A., Pertile, P., Meyers, R., Marra, P., Di Tullio, G., Iurisci, C., Luini, A., Corda, D., and De Matteis, M. A. (1999). ARF mediates recruitment of Ptdins-4-OH kinase-β and stimulates synthesis of Ptdins(4,5)P2 on the golgi complex. Nature Cell Biol., 1, 280–287.
Goodman, O. B., Krupnick, J. G., Santini, F., Gurevich, V. V., Penn, R. B., Gagnon, A. W., Keen, J. H., and Benovic, J. L. (1996). β-arrestin acts as a clathrin adaptor in endocytosis of the β2-adrenergic receptor. Nature, 383, 447–450.
Gurevich, V. V. and Benovic, J. L. (1993). Visual arrestin interaction with rhodopsin. J. Biol. Chem., 268, 11628–11638.
Gurevich, V. V., Dion, S. B., Onorato, J. J., Ptasienski, J., Kim, C. M., Sterne-Marr, M., Hosey, M. M., and Benovic, J. L. (1995). Arrestin interactions with G protein-coupled receptors. J. Biol. Chem., 270, 720–731.
Honda, A., Nogami, M., Yokozeki, T., Yamazaki, M., Nakamura, H., Watanabe, H., Kawamoto, K., Nakayama, K., Morris, A. J., Frohman, M. A., and Kanaho, Y. (1999). Phosphatidylinositol 4-phosphate 4-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell, 99, 521–532.
Hunzicker-Dunn, M. (1981). Rabbit follicular adenylyl cyclase activity. II. Gonadotropin-induced desensitization in granulosa cells and follicle shells. Biol. Repro., 24, 279–286.
Iacovelli, L., Franchetti, R., Masini, N. M., and DeBlasi, A. (1996). GRK2 and β-arrestin1 as negative regulators of thyrotropin receptor-stimulated response. Mol. Endo., 10, 1138–1146.
Jackson, C. L. and Casanova, J. E. (2000). Turning on ARF: the Sec7 family of guanine-nucleotide-exchange factors. Trends Cell Biol., 10, 60–67.
Kahn, R. A., Randazzo, P., Serafini, T., Weiss, O., Rulka, C., Clark, J., Amherdt, M., Roller, P., Orci, L., and Rothman, J. E. (1992). The amino terminus of ADP-ribosylation factor (ARF) is a critical determinant of ARF activities and is a potent and specific inhibitor of protein transport. J. Biol. Chem., 267, 13039–13046.
Klein, U., Muller, C., Chu, P., Birnbaumer, M., and von Zastrow, M. (2001). Heterologous inhibition of G protein-coupled receptor endocytosis mediated by receptor-specific trafficking of beta-arrestins. J. Biol. Chem., 276, 17442–17447.
Knospe, V., Donoso, L. A., Banga, J. P., Yue, S., Kasp, E., and Gregerson, D. S. (1988). Epitope mapping of bovine retinal S-antigen with monoclonal antibodies. Eye Res., 7, 1137–1147.
Kohout, T. A., Lin, F. T., Perry, S. J., Conner, D. A., and Lefkowitz, R. J. (2001). β-Arrestin 1 and 2 differentially regulate heptahelical receptor signaling and trafficking. Proc. Natl. Acad. Sci., 98, 1601–1606.
Kovoor, A., Celvert, J., Abdryashitov, R. I., Chavkin, C., and Gurevich, V. V. (1999). Targeted construction of phosphorylation-independent beta-arrestin mutants with constitutive activity in cells. J. Biol. Chem., 274, 6831–6834.
Krupnick, J. G. and Benovic, J. L. (1998). The role of receptor kinases and arrestins in G protein-coupled receptor regulation. Annu. Rev. Pharmacol. Toxicol., 38, 289–319.
Lamm, M. L. G., Ekstrom, R. C., Maizels, E. T., Rajagopalan, R. M., and Hunzicker-Dunn, M. (1994). The effect of protein kinases on desensitization of the porcine follicular membrane luteinizing hormone/chorionic gonadotropin-sensitive adenylyl cyclase. Endocrinology, 134, 1745–1754.
Lamm, M. L. G. and Hunzicker-Dunn, M. (1994). Phosphorylation-independent desensitization of the luteinizing hormone/chorionic gonadotropin receptor in porcine follicular membranes. Mol. Endo., 8, 1537–1546.
Laporte, S. A., Oakley, R. H., Holt, J. A., Barak, L. S., and Caron, M. G. (2000). The interaction of β-arrestin with the AP-2 adaptor is required for clustring of β2-adrenergic receptor into clathrin-coated pits. J. Biol. Chem., 275, 23120–23126.
Laporte, S. A., Oakley, R., Zhang, J., Holt, J. A., Ferguson, S. S. G., Caron, M. G., and Barak, L. S. (1999). The β2-adrenergic receptor/β arrestin complex recruits the clathrin adaptor AP-2 during endocytosis. Proc. Natl. Acad. Sci., USA, 96, 3712–3717.
Lenhard, J. M., Kahn, R. A., and Stahl, P. D. (1992). Evidence for ADP-ribosylation factor (ARF) as a regulator of in vitro endosome-endosome fusion. J. Biol. Chem., 267, 13047–13052.
Lohse, M. J., Andexinger, S., Pitcher, J., Trukawinski, S., Codina, J., Faure, J.-P., Caron, M. G., and Lefkowitz, R. J. (1992). Receptor-specific desensitization with purified proteins. J. Biol. Chem., 267, 8558–8564.
Lohse, M. J., Benovic, J. L., Codina, J., Caron, M. G., and Lefkowitz, R. J. (1990). β-arrestin: a protein that regulates β-adrenergic receptor function. Science, 248, 1547–1550.
Marsh, J. M., Mills, T. M., and Lemaire, W. J. (1973). Preovulatory changes in the synthesis of cyclic AMP by rabbit Graafian follicles. Biochem. Biophys. Acta, 304, 197–202.
Min, L., Galet, C., and Ascoli, M. (2001). The association of arrestin-3 with the human lutropin/choriogonadotropin receptor depends mostly on receptor activation rather than on receptor phosphorylation. J. Biol. Chem., 277, 702–710.
Mukherjee, S., Casanova, J. E., and Hunzicker-Dunn, M. (2001). Desensitization of the luteinizing hormone/choriogonadotropin receptor in ovarian follicular membranes is inhibited by catalytically inactive ARNO. J. Biol. Chem., 276, 6524–6528.
Mukherjee, S., Gurevich, V. V., Jones, J. C. R., 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., USA, 97, 5901–5906.
Mukherjee, S., Gurevich, V. V., Preninger, A., Hamm, H. E., Bader, M. F., Fazleabas, A. T., Birnbaumer, L., and Hunzicker-Dunn, M. (2002). Aspartic acid 564 in the third cytoplasmic loop of luteinizing hormone/choriogonadotropin receptor is crucial for phosphorylation-independent interaction with arrestin2. J. Biol. Chem., 277, 17916–17927.
Mukherjee, S., Palczewski, K., Gurevich, V. V., Benovic, J. L., Banga, J. P., and Hunzicker-Dunn, M. (1999a). A direct role for arrestins in desensitization of the luteinizing hormone/choriogonadotropin receptor in porcine ovarian follicular membranes. Proc. Natl. Acad. Sci., USA, 96, 493–498.
Mukherjee, S., Palczewski, K., Gurevich, V. V., and Hunzicker-Dunn, M. (1999b). βarrestin-dependent desensitization of luteinizing hormone/choriogonadotropin receptor is prevented by a synthetic peptide corresponding to the third intracellular loop of the receptor. J. Biol. Chem., 274, 12984–12989.
Nagel, W., Zeitlmann, L., Schilcher, P., Geiger, C., Kolanus, J., and Kolanus, W. (1998). Phosphoinositide 3-OH kinase activates the beta2 integrin adhesion pathway and induces membrane recruitment of Cytohesin-1. J. Biol. Chem., 273, 14853–14861.
Oakley, R. H., Laporte, S. A., Holt, J. A., Caron, M. G., and Barak, L. S. (2000). Differential affinities of visual arrestin, β arrestin1, and β arrestin2 for G protein-coupled receptors delineate two major classes of receptors. J. Biol. Chem., 275, 17201–17210.
Paing, M. M., Stutts, A. B., Kohout, T. A., Lefkowitz, R. J., and Trejo, J. (2002). β-Arrestins regulate protease-activated receptor-1 desensitization but not internalization or Down-regulation. J. Biol. Chem., 277, 1292–1300.
Palczewski, K. (1994). Structure and functions of arrestins. Prot. Sci., 3, 1355–1361.
Pals-Rylaarsdam, R., Zu, Y., Witt-Enderby, P., and Benovic, J. L. (1995). Desensitization and internalization of the m2 muscarinic acetylcholine receptor are directed by independent mechanisms. J. Biol. Chem., 270, 29004–29011.
Peters, P. J., Gao, M., Gaschet, J., Ambach, A., van Donselaar, E., Traverse, J. F., Bos, E., Wolffe, E. J., and Hsu, V. W. (2001). Characterization of coated vesicles that participate in endocytic recycling. Traffic, 2, 885–895.
Peters, P. J., Hsu, V. W., Ooi, C. E., Finazzi, D., Teal, S. B., Oorschot, V., Donaldson, J. G., and Klausner, R. D. (1995). Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments. J. Cell. Biol., 128, 1003–1017.
Pierce, K. L., Lefkowitz, R. J., and Lefkowitz, R. J. (2001). Classical and new roles of β-arrestins in the regulation of G-protein coupled receptors. Nat. Rev. Neurosci., 2, 727–733.
Premont, R. T., Claing, A., Vitale, N., Freeman, J. L. R., Pitcher, J. A., Patton, W. A., Moss, J., Vaughan, M., and Lefkowitz, R. J. (1998). β2-adrenergic receptor regulation of GIT1, a G protein-coupled receptor kinase-associated ADP ribosylation factor GTPase-activating protein. Proc. Natl. Acad. Sci., USA, 95, 14082–14097.
Radhakrishna, H. and Donaldson, J. G. (1997). ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol., 139, 49–61.
Radhakrishna, H., Klausner, R. D., and Donaldson, J. G. (1996). Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. J. Cell Biol., 134, 935–947.
Rajagopalan-Gupta, R. M., Mukherjee, S., Zhu, X., Ho, Y.-K., Hamm, H., Birnbaumer, M., Birnbaumer, L., and Hunzicker-Dunn, M. (1999). Roles of Gi and Gq/11 in mediating desensitization of the luteinizing hormone/choriogonadotropin receptor in porcine ovarian follicular membranes. Endocrinology, 140, 1612–1621.
Roy, C., Guillon, G., and Jard, S. (1976). Hormone-dependent desensitization of vasopressin-sensitive adenylate cyclase. Biochem. Biophys. Res. Comm., 72, 1265–1270.
Salvador, L. M., Mukherjee, S., Kahn, R. A., Lamm, M. L. G., Fazleabas, A. T., Maizels, E. T., Bader, M.-F., Hamm, H., Rasenick, M. M., Casanova, J. E., and Hunzicker-Dunn, M. (2001). Activation of the luteinizing hormone/choriogonadotropin hormone receptor promotes ADP ribosylation factor (ARF) 6 activation in porcine ovarian follicular membranes. J. Biol. Chem., 276, 33773–33781.
Santini, F., Penn, R. B., Gagnon, A. W., Benovic, J. L., and Keen, J. H. (2000). Selective recruitment of arrestin-3 to clathrin coated pits upon stimulation of G protein-coupled receptors. J. Cell. Sci., 113, 2463–2470.
Schulz, A., Bruns, K., Henklein, P., Krause, G., Schubert, M., Gudermann, T., Wray, V., Schultz, G., and Schoneberg, T. (2000). Requirement of specific intrahelical interactions for stabilizing the inactive conformation of glycoprotein hormone receptors. J. Biol. Chem., 275, 37860–37869.
Shenker, A. (2002). Activating mutations of the lutropin/choriogonadotropin receptor in precocious puberty. Receptors Channels, 8, 3–18.
Troispoux, C., Guillou, F. E. J.-M., Firsov, D., Iacovelli, L., DeBlasi, A., Combarnous, Y., and Reiter, E. (2000). Involvement of G protein-coupled receptor kinases and arrrestins in desensitization to follicle sitmulating hromone action. Mol. Endo., 13, 1599–1614.
Wang, Z., Liu, X., and Ascoli, M. (1997). Phosphorylation of the lutropin/choriogonadotropin receptor facilitates uncoupling of the receptor from adenylyl cyclase and endocytosis of the bound hormone. Mol. Endo., 11, 183–192.
Zhu, X., Gudermann, T., Birnbaumer, M., and Birnbaumer, L. (1993). A luteinizing hormone receptor with a severely truncated cytoplasmic tail (LHR-ct628) desensitizes to the same degree as the full-length receptor. J. Biol. Chem., 268, 1723–1728.
Zhu, Y., Drake, M. T., and Kornfeld, S. (1999). ADP-ribosylation factor 1 dependent clathrincoat assembly on synthetic liposomes. Proc. Natl. Acad. Sci., USA, 96, 5013–5018.
Author information
Authors and Affiliations
Rights and permissions
Copyright information
© 2004 Springer Science + Business Media, Inc.
About this chapter
Cite this chapter
Hunzicker-Dunn, M. (2004). A Role for Arf6 in G Protein-coupled Receptor Desensitization. In: ARF Family GTPases. Proteins and Cell Regulation, vol 1. Springer, Dordrecht. https://doi.org/10.1007/1-4020-2593-9_15
Download citation
DOI: https://doi.org/10.1007/1-4020-2593-9_15
Publisher Name: Springer, Dordrecht
Print ISBN: 978-1-4020-1719-3
Online ISBN: 978-1-4020-2593-8
eBook Packages: Springer Book Archive