Multiple regulatory mechanisms for the Dictyostelium Roco protein GbpC

Journal of Biological Chemistry

Volumn 287, Issue 4, 2012, Pages 2749-2758

  Kortholt, Arjan ^a   Van Egmond, Wouter N ^a   Plak, Katarzyna ^a   Bosgraaf, Leonard ^a   Keizer Gunnink, Ineke ^a   Van Haastert, Peter J M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN CYTOSKELETON; CELL BOUNDARY; CELLULAR LOCALIZATION; CELLULAR MEMBRANES; CHEMOATTRACTANTS; CYCLASES; DICTYOSTELIUM; FUNCTIONAL ACTIVITIES; HETEROTRIMERIC G PROTEINS; IN-VITRO; IN-VIVO; KINASE ACTIVITY; KINASE DOMAINS; MEMBRANE ASSOCIATION; MULTI DOMAINS; MULTIPLE INPUTS; OSMOTIC SHOCKS; REGULATORY MECHANISM; RESTING CELLS; SIGNALING CASCADES;

BIOCHEMISTRY; CELL MEMBRANES; CHEMICAL ACTIVATION; CYTOLOGY; ENZYMES; PHOSPHOLIPIDS;

PROTEINS;

CYCLIC AMP; CYCLIC GMP; GUANYLATE CYCLASE; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; PHOSPHOLIPID; PROTEIN GBPC; PROTEIN ROCO; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; BIOLOGICAL ACTIVITY; CELL MEMBRANE; CELLULAR DISTRIBUTION; CHEMOTAXIS; CONTROLLED STUDY; CYTOPLASM; DICTYOSTELIUM; IN VITRO STUDY; IN VIVO STUDY; MUTATION; NONHUMAN; OSMOTIC STRESS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

CELL MEMBRANE; CYCLIC AMP; CYCLIC GMP; CYTOPLASM; DICTYOSTELIUM; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; SECOND MESSENGER SYSTEMS;

DICTYOSTELIUM;

EID: 84856077085     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.315739     Document Type: Article

References (44)

1. Lees, A. J., Hardy, J., and Revesz, T. (2009) Parkinson's disease. Lancet 373, 2055-2066
2. Paisán-Ruíz, C., Jain, S., Evans, E. W., Gilks, W. P., Simón, J., van der Brug, M., López, de Munain, A., Aparicio, S., Gil, A. M., Khan, N., Johnson, J., Martinez, J. R., Nicholl, D., Carrera, I. M., Pena, A. S., de Silva, R., Lees, A., Martí-Massó, J. F., Pérez-Tur, J., Wood, N. W., and Singleton, A. B. (2004) Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron 44, 595-600
3. Zimprich, A., Biskup, S., Leitner, P., Lichtner, P., Farrer, M., Lincoln, S., Kachergus, J., Hulihan, M., Uitti, R. J., Calne, D. B., Stoessl, A. J., Pfeiffer, R. F., Patenge, N., Carbajal, I. C., Vieregge, P., Asmus, F., Müller-Myhsok, B., Dickson, D. W., Meitinger, T., Strom, T. M., Wszolek, Z. K., and Gasser, T. (2004) Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44, 601-607 (Pubitemid 39531225)
4. Bosgraaf, L., and Van Haastert, P. J. (2003) Roc, a Ras/GTPase domain in complex proteins. Biochim. Biophys. Acta 1643, 5-10 (Pubitemid 37494887)
5. Marín, I., van Egmond, W. N., and van Haastert, P. J. (2008) The Roco protein family. A functional perspective. FASEB J. 22, 3103-3110
6. Cookson, M. R., and Bandmann, O. (2010) Parkinson's disease. Insights from pathways. Hum. Mol. Genet. 19, R21-R27
7. Cookson, M. R. (2010) The role of leucine-rich repeat kinase 2 (LRRK2) in Parkinson's disease. Nat. Rev. Neurosci. 11, 791-797
8. Bosgraaf, L., Russcher, H., Smith, J. L., Wessels, D., Soll, D. R., and Van Haastert, P. J. (2002) A novel cGMP signalling pathway mediating myosin phosphorylation and chemotaxis in Dictyostelium. EMBO J. 21, 4560-4570 (Pubitemid 34984343)
9. van Egmond, W. N., and van Haastert, P. J. (2010) Characterization of the Roco protein family in Dictyostelium discoideum. Eukaryot. Cell 9, 751-761
10. Goldberg, J. M., Bosgraaf, L., Van Haastert, P. J., and Smith, J. L. (2002) Identification of four candidate cGMP targets in Dictyostelium. Proc. Natl. Acad. Sci. U.S.A. 99, 6749-6754 (Pubitemid 34526203)
11. Araki, T., van Egmond, W. N., van Haastert, P. J., and Williams, J. G. (2010) Dual regulation of a Dictyostelium STAT by cGMP and Ca2+ signalling. J. Cell Sci. 123, 837-841
12. Kuwayama, H., Ecke, M., Gerisch, G., and Van Haastert, P. J. (1996) Protection against osmotic stress by cGMP-mediated myosin phosphorylation. Science 271, 207-209 (Pubitemid 26033301)
13. Veltman, D. M., and van Haastert, P. J. (2008) The role of cGMP and the rear of the cell in Dictyostelium chemotaxis and cell streaming. J. Cell Sci. 121, 120-127 (Pubitemid 351265709)
14. van Egmond, W. N., Kortholt, A., Plak, K., Bosgraaf, L., Bosgraaf, S., Keizer-Gunnink, I., and van Haastert, P. J. (2008) Intramolecular activation mechanism of the Dictyostelium LRRK2 homolog Roco protein GbpC. J. Biol. Chem. 283, 30412-30420
15. Iaccarino, C., Crosio, C., Vitale, C., Sanna, G., Carrì, M. T., and Barone, P. (2007) Apoptotic mechanisms in mutant LRRK2-mediated cell death. Hum. Mol. Genet. 16, 1319-1326 (Pubitemid 47055127)
16. Berger, Z., Smith, K. A., and Lavoie, M. J. (2010) Membrane localization of LRRK2 is associated with increased formation of the highly active LRRK2 dimer and changes in its phosphorylation. Biochemistry 49, 5511-5523
17. Nichols, R. J., Dzamko, N., Morrice, N. A., Campbell, D. G., Deak, M., Ordureau, A., Macartney, T., Tong, Y., Shen, J., Prescott, A. R., and Alessi, D. R. (2010) 14-3-3 binding to LRRK2 is disrupted by multiple Parkinson's disease-associated mutations and regulates cytoplasmic localization. Biochem. J. 430, 393-404
18. Sen, S., Webber, P. J., and West, A. B. (2009) Dependence of leucine-rich repeat kinase 2 (LRRK2) kinase activity on dimerization. J. Biol. Chem. 284, 36346-36356
19. Bosgraaf, L., Keizer-Gunnink, I., and Van Haastert, P. J. (2008) PI3-kinase signaling contributes to orientation in shallow gradients and enhances speed in steep chemoattractant gradients. J. Cell Sci. 121, 3589-3597
20. Bosgraaf, L., van Haastert, P. J., and Bretschneider, T. (2009) Analysis of cell movement by simultaneous quantification of local membrane displacement and fluorescent intensities using Quimp2. Cell Motil. Cytoskeleton 66, 156-165
21. Konijn, T. M. (1970) Microbiological assay of cyclic 3′,5′- AMP. Experientia 26, 367-369
22. Veltman, D. M., and Van Haastert, P. J. (2006) Guanylyl cyclase protein and cGMP product independently control front and back of chemotaxing Dictyostelium cells. Mol. Biol. Cell 17, 3921-3929 (Pubitemid 44330876)
23. Veltman, D. M., Keizer-Gunnik, I., and Van Haastert, P. J. (2008) Four key signaling pathways mediating chemotaxis in Dictyostelium discoideum. J. Cell Biol. 180, 747-753 (Pubitemid 351397774)
24. Araki, T., Tsujioka, M., Abe, T., Fukuzawa, M., Meima, M., Schaap, P., Morio, T., Urushihara, H., Katoh, M., Maeda, M., Tanaka, Y., Takeuchi, I., and Williams, J. G. (2003) A STAT-regulated, stress-induced signalling pathway in Dictyostelium. J. Cell Sci. 116, 2907-2915 (Pubitemid 36926980)
25. Van Haastert, P. J., and Devreotes, P. N. (2004) Chemotaxis. Signalling the way forward. Nat. Rev. Mol. Cell Biol. 5, 626-634
26. Roelofs, J., and Van Haastert, P. J. (2002) Characterization of two unusual guanylyl cyclases from Dictyostelium. J. Biol. Chem. 277, 9167-9174 (Pubitemid 34952995)
27. Liao, X. H., Majithia, A., Huang, X., and Kimmel, A. R. (2008) Growth control via TOR kinase signaling, an intracellular sensor of amino acid and energy availability, with cross-talk potential to proline metabolism. Amino Acids 35, 761-770
28. Begley, M. J., Taylor, G. S., Kim, S. A., Veine, D. M., Dixon, J. E., and Stuckey, J. A. (2003) Crystal structure of a phosphoinositide phosphatase, MTMR2. Insights into myotubular myopathy and Charcot-Marie-Tooth syndrome. Mol. Cell 12, 1391-1402 (Pubitemid 38037009)
29. Berger, P., Schaffitzel, C., Berger, I., Ban, N., and Suter, U. (2003) Membrane association of myotubularin-related protein 2 is mediated by a pleckstrin homology-GRAM domain and a coiled-coil dimerization module. Proc. Natl. Acad. Sci. U.S.A. 100, 12177-12182 (Pubitemid 37271534)
30. de Rooij, J., Rehmann, H., van Triest, M., Cool, R. H., Wittinghofer, A., and Bos, J. L. (2000) Mechanism of regulation of the Epac family of cAMP-dependent RapGEFs. J. Biol. Chem. 275, 20829-20836 (Pubitemid 30457676)
31. Tsujita, K., Itoh, T., Ijuin, T., Yamamoto, A., Shisheva, A., Laporte, J., and Takenawa, T. (2004) Myotubularin regulates the function of the late endosome through the gram domain-phosphatidylinositol 3,5-bisphosphate interaction. J. Biol. Chem. 279, 13817-13824 (Pubitemid 38468913)
32. Weeks, G., and Herring, F. G. (1980) The lipid composition and membrane fluidity of Dictyostelium discoideum plasma membranes at various stages during differentiation. J. Lipid Res. 21, 681-686
33. Kamimura, Y., Xiong, Y., Iglesias, P. A., Hoeller, O., Bolourani, P., and Devreotes, P. N. (2008) PIP3-independent activation of TorC2 and PKB at the cell's leading edge mediates chemotaxis. Curr. Biol. 18, 1034-1043
34. Chen, L., Iijima, M., Tang, M., Landree, M. A., Huang, Y. E., Xiong, Y., Iglesias, P. A., and Devreotes, P. N. (2007) PLA2 and PI3K/PTEN pathways act in parallel to mediate chemotaxis. Dev. Cell 12, 603-614 (Pubitemid 46523645)
35. Greggio, E., Jain, S., Kingsbury, A., Bandopadhyay, R., Lewis, P., Kaganovich, A., van der Brug, M. P., Beilina, A., Blackinton, J., Thomas, K. J., Ahmad, R., Miller, D. W., Kesavapany, S., Singleton, A., Lees, A., Harvey, R. J., Harvey, K., and Cookson, M. R. (2006) Kinase activity is required for the toxic effects of mutant LRRK2/dardarin. Neurobiol. Dis. 23, 329-341 (Pubitemid 44097032)
36. Guo, L., Gandhi, P. N., Wang, W., Petersen, R. B., Wilson-Delfosse, A. L., and Chen, S. G. (2007) The Parkinson's disease-associated protein, leucine-rich repeat kinase 2 (LRRK2), is an authentic GTPase that stimulates kinase activity. Exp. Cell Res. 313, 3658-3670 (Pubitemid 47404550)
37. Ito, G., Okai, T., Fujino, G., Takeda, K., Ichijo, H., Katada, T., and Iwatsubo, T. (2007) GTP binding is essential to the protein kinase activity of LRRK2, a causative gene product for familial Parkinson's disease. Biochemistry 46, 1380-1388 (Pubitemid 46208485)
38. Lewis, P. A., Greggio, E., Beilina, A., Jain, S., Baker, A., and Cookson, M. R. (2007) The R1441C mutation of LRRK2 disrupts GTP hydrolysis. Biochem. Biophys. Res. Commun. 357, 668-671 (Pubitemid 46653831)
39. Li, X., Tan, Y. C., Poulose, S., Olanow, C. W., Huang, X. Y., and Yue, Z. (2007) Leucine-rich repeat kinase 2 (LRRK2)/PARK8 possesses GTPase activity that is altered in familial Parkinson's disease R1441C/G mutants. J. Neurochem. 103, 238-247 (Pubitemid 47404210)
40. Luzón-Toro, B., Rubio de la Torre, E., Delgado, A., Pérez-Tur, J., and Hilfiker, S. (2007) Mechanistic insight into the dominant mode of the Parkinson's disease-associated G2019S LRRK2 mutation. Hum. Mol. Genet. 16, 2031-2039 (Pubitemid 47354886)
41. West, A. B., Moore, D. J., Biskup, S., Bugayenko, A., Smith, W. W., Ross, C. A., Dawson, V. L., and Dawson, T. M. (2005) Parkinson's disease-associated mutations in leucine-rich repeat kinase 2 augment kinase activity. Proc. Natl. Acad. Sci. U.S.A. 102, 16842-16847 (Pubitemid 41688864)
42. West, A. B., Moore, D. J., Choi, C., Andrabi, S. A., Li, X., Dikeman, D., Biskup, S., Zhang, Z., Lim, K. L., Dawson, V. L., and Dawson, T. M. (2007) Parkinson's disease-associated mutations in LRRK2 link enhanced GTP-binding and kinase activities to neuronal toxicity. Hum. Mol. Genet. 16, 223-232 (Pubitemid 46179004)
43. Gasper, R., Meyer, S., Gotthardt, K., Sirajuddin, M., and Wittinghofer, A. (2009) It takes two to tango. Regulation of G proteins by dimerization. Nat. Rev. Mol. Cell Biol. 10, 423-429
44. Gotthardt, K., Weyand, M., Kortholt, A., Van Haastert, P. J., and Wittinghofer, A. (2008) Structure of the Roc-COR domain tandem of C. tepidum, a prokaryotic homologue of the human LRRK2 Parkinson kinase. EMBO J. 27, 2239-2249