The calcium-sensing receptor changes cell shape via a β-arrestin-1-ARNO-ARF6-ELMO protein network

Journal of Cell Science

Volumn 120, Issue 15, 2007, Pages 2489-2497

  Bouschet, Tristan ^a,c   Martin, Stéphane ^a   Kanamarlapudi, Venkateswarlu ^b,d   Mundell, Stuart ^b   Henley, Jeremy M ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^d SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

arrestin 1; ARF6; ARNO; Calcium sensing receptor; Cytoskeleton; ELMO

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; ARF NUCLEOTIDE BINDING SITE OPENER PROTEIN; BETA ARRESTIN 1; BINDING PROTEIN; CALCIUM; CALCIUM SENSING RECEPTOR; ENGULFMENT AND CELL MOTILITY PROTEIN; G PROTEIN COUPLED RECEPTOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL SHAPE; CELL STRUCTURE; CHEMOTAXIS; CONTROLLED STUDY; CYTOSKELETON; EXTRACELLULAR CALCIUM; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RECEPTOR BINDING; SIGNAL TRANSDUCTION;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADP-RIBOSYLATION FACTORS; ARRESTINS; CALCIUM; CELL LINE; CELL MEMBRANE; CELL MOVEMENT; CELL SHAPE; GTPASE-ACTIVATING PROTEINS; HUMANS; RECEPTORS, CALCIUM-SENSING;

EID: 34548246116     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03469     Document Type: Article

References (35)

1. Adams, G. B., Chabner, K. T., Alley, I. R., Olson, D. P., Szczepiorkowski, Z. M., Poznansky, M. C., Kos, C. H., Pollak, M. R., Brown, E. M. and Scadden, D. T. (2006). Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature 439, 599-603.
2. Ahn, S., Nelson, C. D., Garrison, T. R., Miller, W. E. and Lefkowitz, R. J. (2003). Desensitization, intemalization, and signaling functions of beta-arrestins demonstrated by RNA interference. Proc. Natl. Acad. Sci. USA 100, 1740-1744.
3. Ashby, M. C., De La Rue, S. A., Ralph, G. S., Uney, J., Collingridge, G. L. and Henley, J. M. (2004). Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J. Neurosci. 24, 5172-5176.
4. Bhattacharya, M., Anborgh, P. H., Babwah, A. V., Dale, L. B., Dobransky, T., Benovic, J. L., Feldman, R. D., Verdi, J. M., Rylett, R. J. and Ferguson, S. S. (2002). Beta-arrestins regulate a Ral-GDS Ral effector pathway that mediates cytoskeletal reorganization. Nat. Cell Biol. 4, 547-555.
5. Bouschet, T. and Henley, J. M. (2005). Calcium as an extracellular signalling molecule: Perspectives on the Calcium Sensing Receptor in the brain. C. R. Biol. 328, 691-700.
6. Bouschet, T., Martin, S. and Henley, J. M. (2005). Receptor-activity-modifying proteins are required for forward trafficking of the calcium-sensing receptor to the plasma membrane. J. Cell Sci. 118, 4709-4720.
7. Brown, E. M. and MacLeod, R. J. (2001). Extracellular calcium sensing and extracellular calcium signaling. Physiol. Rev. 81 239-297.
8. Claing, A., Chen, W., Miller, W. E., Vitale, N., Moss, J., Premont, R. T. and Lefkowitz, R. J. (2001). beta-Arrestin-mediated ADP-ribosylation factor 6 activation and beta 2-adrenergic receptor endocytosis. J. Biol. Chem. 276, 42509-42513.
9. Dale, L. B., Bhattacharya, M., Seachrist, J. L., Anborgh, P. H. and Ferguson, S. S. (2001). Agonist-stimulated and tonic internalization of metabotropic glutamate receptor la in human embryonic kidney 293 cells: Agonist-stimulated endocytosis is beta-arrestinl isoform-specific. Mol. Pharmacol. 60, 1243-1253.
10. 2+-sensing receptor induces Rho kinase-mediated actin stress fiber assembly and altered cell morphology, but not in response to aromatic amino acids. Am. J. Physiol. 290, C1543-C1551.
11. Fong, A. M., Premont, R. T., Richardson, R. M., Yu, Y. R., Lefkowitz, R. J. and Patel, D. D. (2002). Defective lymphocyte chemotaxis in beta-arrestin2- and GRK6-deficient mice. Proc. Natl. Acad Sci. USA 99, 7478-7483.
12. Ge, L., Ly, Y., Hollenberg, M. and DeFea, K. (2003). A beta-arrestin-dependent scaffold is associated with prolonged MAPK activation in pseudopodia during protease-activated receptor-2-induced chemotaxis. J. Biol. Chem. 278, 34418-34426.
13. Ge, L., Shenoy, S. K., Lefkowitz, R. J. and DeFea, K. (2004). Constitutive protease-activated receptor-2-mediated migration of MDA MB-231 breast cancer cells requires both beta-arrestin-1 and -2. J. Biol. Chem. 279, 55419-55424.
14. Giannone, G., Dubin-Thaler, B. J., Dobereiner, H. G., Kieffer, N., Bresnick, A. R. and Sheetz, M. P. (2004). Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116, 431-443.
15. Godwin, S. L. and Soltoff, S. P. (1997). Extracellular calcium and platelet-derived growth factor promote receptor-mediated chemotaxis in osteoblasts through different signaling pathways. J. Biol. Chem. 272, 11307-11312.
16. Gumienny, T. L., Brugnera, E., Tosello-Trampont, A. C., Kinchen, J. M., Haney, L. B., Nishiwaki, K., Walk, S. F., Nemergut, M. E., Macara, I. G., Francis, R. et al. (2001). CED-12/ELMO, a novel member of the CrkII/Dockl80/Rac pathway, is required for phagocytosis and cell migration. Cell 107, 27-41.
17. Hofer, A. M. and Brown, E. M. (2003). Extracellular calcium sensing and signalling. Nat. Rev. Mol. Cell Biol. 4, 530-538.
18. Kraynov, V. S., Chamberlain, C., Bokoch, G. M., Schwartz, M. A., Slabaugh, S. and Hahn, K. M. (2000). Localized Rac activation dynamics visualized in living cells. Science 290, 333-337.
19. Krupnick, J. G., Santini, F., Gagnon, A. W., Keen, J. H. and Benovic, J. L. (1997). Modulation of the arrestin-clathrin interaction in cells. Characterization of beta-arrestin dominant-negative mutants. J. Biol. Chem. 272, 32507-32512.
20. Lefkowitz, R. J. and Whalen, E. J. (2004). beta-arrestins: Traffic cops of cell signaling. Curr. Opin- Cell Biol. 16, 162-168.
21. Lohse, M. J., Benovic, J. L., Codina, J., Caron, M. G. and Lefkowitz, R. J. (1990). beta-Arrestin: A protein that regulates beta-adrenergic receptor function. Science 248, 1547-1550.
22. Lorenz, S., Frenzel, R., Paschke, R., Breitwieser, G. E. and Miedlich, S. U. (2007). Functional desensitization of the extrarellular calcium-sensing receptor is regulated via distinct mechanisms: Role of G protein-coupled receptor kinases, protein kinase c and beta-arrestins. Endocrinology 148, 2398-2404.
23. 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. et al. (2000). The ADP ribosylation factor nucleotide exchange factor ARNO promotes beta-arrestin release necessary for luteinizing hormone/choriogonadotropin receptor desensitization. Proc. Natl. Acad. Sci. USA 97, 5901-5906.
24. Olszak, I. T., Poznansky, M. C., Evans, R. H., Olson, D., Kos, C., Pollak, M. R., Brown, E. M. and Scadden, D. T. (2000). Extracellular calcium elicits a chemokinetic response from monocytes in vitro and in vivo. J. Clin. Invest. 105, 1299-1305.
25. Pi, M., Oakley, R. H., Gesty-Palmer, D., Cruickshank, R. D., Spurney, R. F., Luttrell, L. M. and Quarles, L. D. (2005). Beta-arrestin- and G protein receptor kinase-mediated calcium-sensing receptor desensitization. Mol. Endocrinol. 19, 1078-1087.
26. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003). Cell migration: Integrating signals from front to back. Science 302, 1704-1709.
27. Ruat, M., Molliver, M. E., Snowman, A. M. and Snyder, S. H. (1995). Calcium sensing receptor: Molecular cloning in rat and localization to nerve terminals. Proc. Natl. Acad Sci. USA 92 3161-3165.
28. Santy, L. C. and Casanova, J. E. (2001). Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J. Cell Biol. 154, 599-610.
29. Santy, L. C., Ravichandran, K. S. and Casanova, J. E. (2005). The DOCK180/Elmo complex couples ARNO-mediated Arf6 activation to the downstream activation of Racl. Curr. Biol. 15, 1749-1754.
30. Scott, M. G., Pierotti, V., Storez, H., Lindberg, E., Thuret, A., Muntaner, O., Labbe-Jullie, C., Pitcher, J. A. and Marullo, S. (2006). Cooperative regulation of extracellular signal-regulated kinase activation and cell shape change by filamin A and (beta)-arrestins. Mol. Cell. Biol. 26, 3432-3445.
31. Small, J. V., Stradal, T., Vignal, E. and Rottner, K. (2002). The lamellipodium: Where motility begins. Trends Cell Biol. 12, 112-120.
32. Sun, Y., Cheng, Z., Ma, L. and Pei, G. (2002). Beta-arrestin2 is critically involved in CXCR4-mediated chemotaxis, and this is mediated by its enhancement of p38 MAPK activation. J. Biol. Chem. 277 49212-49219.
33. Venkateswarlu, K., Oatey, P. B., Tavare, 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.
34. Walker, J. K., Fong, A. M., Lawson, B. L., Savov, J. D., Patel, D. D., Schwartz, D. A. and Lefkowitz, R. J. (2003). Beta-arrestin-2 regulates the development of allergic asthma. J. Clin. Invest. 112 566-574.
35. Yudowski, G. A., Puthenveedu, M. A. and von Zastrow, M. (2006). Distinct modes of regulated receptor insertion to the somatodendritic plasma membrane. Nat. Neurosci. 9, 622-627.