Lowe syndrome protein Ocrl1 is translocated to membrane ruffles upon Rac GTPase activation: A new perspective on Lowe syndrome pathophysiology

Human Molecular Genetics

Volumn 14, Issue 11, 2005, Pages 1441-1448

  Faucherre, Adèle ^a   Desbois, Pierrette ^a   Nagano, Fumiko ^b   Satre, Véronique ^c   Lunardi, Joël ^c   Gacon, Gérard ^a   Dorseuil, Olivier ^a  

^a INSTITUT COCHIN   (France)

^b INSTITUT CURIE   (France)

^c GRENOBLE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; OCULOCEREBRORENAL 1 PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOPROTEIN PHOSPHATASE; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CELL MIGRATION; CELL STRAIN COS7; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE MUTATION; GENE TRANSLOCATION; HUMAN; IMMUNODETECTION; LOWE SYNDROME; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; COS CELLS; ENZYME ACTIVATION; EPIDERMAL GROWTH FACTOR; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN TRANSPORT; RAC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 20444464060     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddi153     Document Type: Article

References (32)

1. Attree, O., Olivos, I.M., Okabe, I., Bailey, L.C., Nelson, D.L., Lewis, R.A., McInnes, R.R. and Nussbaum, R.L. (1992) The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase. Nature, 358, 239-242.
2. Peck, J., Douglas, G.T., Wu, C.H. and Burbelo, P.D. (2002) Human RhoGAP domain-containing proteins: structure, function and evolutionary relationships. FEBS Lett., 528, 27-34.
3. Zhang, X., Jefferson, A.B., Auethavekiat, V. and Majerus, P.W. (1995) The protein deficient in Lowe syndrome is a phosphatidylinositol-4,5-bisphosphate 5-phosphatase. Proc. Natl Acad. Sci. USA, 92, 4853-4856.
4. Suchy, S.F., Olivos-Glander, I.M. and Nussbaum, R.L. (1995) Lowe syndrome, a deficiency of phosphatidylinositol 4,5-bisphosphate 5-phosphatase in the Golgi apparatus. Hum. Mol. Genet., 4, 2245-2250.
5. Zhang, X., Hartz, P.A., Philip, E., Racusen, L.C. and Majerus, P.W. (1998) Cell lines from kidney proximal tubules of a patient with Lowe syndrome lack OCRL inositol polyphosphate 5-phosphatase and accumulate phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem., 273, 1574-1582.
6. Wenk, M.R., Lucast, L., Di Paolo, G., Romanelli, A.J., Suchy, S.F., Nussbaum, R.L., Cline, G.W., Shulman, G.I., McMurray, W. and De Camilli, P. (2003) Phosphoinositide profiling in complex lipid mixtures using electrospray ionization mass spectrometry. Nat. Biotechnol., 21, 813-817.
7. Raucher, D., Stauffer, T., Chen, W., Shen, K., Guo, S., York, J.D., Sheetz, M.P. and Meyer, T. (2000) Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell, 100, 221-228.
8. Payrastre, B., Missy, K., Giuriato, S., Bodin, S., Plantavid, M. and Gratacap, M. (2001) Phosphoinositides: key players in cell signalling, in time and space. Cell Signal., 13, 377-387.
9. Dressman, M.A., Olivos-Glander, I.M., Nussbaum, R.L. and Suchy, S.F. (2000) Ocrl1, a PtdIns(4,5)P(2) 5-phosphatase, is localized to the trans-Golgi network of fibroblasts and epithelial cells. J. Histochem. Cytochem., 48, 179-190.
10. Ungewickell, A.J. and Majerus, P.W. (1999) Increased levels of plasma lysosomal enzymes in patients with Lowe syndrome. Proc. Natl Acad. Sci. USA, 96, 13342-13344.
11. Ungewickell, A., Ward, M.E., Ungewickell, E. and Majerus, P.W. (2004) The inositol polyphosphate 5-phosphatase Ocrl associates with endosomes that are partially coated with clathrin. Proc. Natl Acad. Sci. USA, 101, 13501-13506.
12. Suchy, S.F. and Nussbaum, R.L. (2002) The deficiency of PIP2 5-phosphatase in Lowe syndrome affects actin polymerization. Am. J. Hum. Genet., 71, 1420-1427.
13. Lin, T., Orrison, B.M., Suchy, S.F., Lewis, R.A. and Nussbaum, R.L. (1998) Mutations are not uniformly distributed throughout the OCRL1 gene in Lowe syndrome patients. Mol. Genet. Metab., 64, 58-61.
14. Loovers, H.M., Veenstra, K., Snippe, H., Pesesse, X., Erneux, C. and van Haastert, P.J. (2003) A diverse family of inositol 5-phosphatases playing a role in growth and development in Dictyostelium discoideum. J. Biol. Chem., 278, 5652-5658.
15. Faucherre, A., Desbois, P., Satre, V., Lunardi, J., Dorseuil, O. and Gacon, G. (2003) Lowe syndrome protein OCRL1 interacts with Rac GTPase in the trans-Golgi network. Hum. Mol. Genet., 12, 2449-2456.
16. van Aelst, L. and D'Souza-Schorey, C. (1997) Rho GTPases and signaling networks. Genes. Dev., 11, 2295-2322.
17. Etienne-Manneville, S. and Hall, A. (2002) Rho GTPases in cell biology. Nature, 420, 629-635.
18. Takai, Y., Sasaki, T. and Matozaki, T. (2001) Small GTP-binding proteins. Physiol. Rev., 81, 153-208.
19. Ridley, A.J., Paterson, H.F., Johnston, C.L., Diekmann, D. and Hall, A. (1992) The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell, 70, 401-410.
20. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science, 279, 509-514.
21. Monnier, N., Satre, V., Lerouge, E., Berthoin, F. and Lunardi, J. (2000) OCRL1 mutation analysis in French Lowe syndrome patients: implications for molecular diagnosis strategy and genetic counseling. Hum. Mutat., 16, 157-165.
22. Singer, A.J. and Clark, R.A. (1999) Cutaneous wound healing. N. Engl. J. Med., 341, 738-746.
23. Li, W., Fan, J., Chen, M., Guan, S., Sawcer, D., Bokoch, G.M. and Woodley, D.T. (2004) Mechanism of human dermal fibroblast migration driven by type I collagen and platelet-derived growth factor-BB. Mol. Biol. Cell, 15, 294-309.
24. Heldin, C.H. and Westermark, B. (1999) Mechanism of action and in vivo role of platelet-derived growth factor. Physiol. Rev., 79, 1283-1316.
25. Wang, Y.J., Wang, J., Sun, H.Q., Martinez, M., Sun, Y.X., Macia, E., Kirchhausen, T., Albanesi, J.P., Roth, M.G. and Yin, H.L. (2003) Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell, 114, 299-310.
26. Pendaries, C., Tronchere, H., Plantavid, M. and Payrastre, B. (2003) Phosphoinositide signaling disorders in human diseases. FEBS Lett., 546, 25-31.
27. Watt, S.A., Kular, G., Fleming, I.N., Downes, C.P. and Lucocq, J.M. (2002) Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta1. Biochem. J., 363, 657-666.
28. Gurung, R., Tan, A., Ooms, L.M., McGrath, M.J., Huysmans, R.D., Munday, A.D., Prescott, M., Whisstock, J.C. and Mitchell, C.A. (2003) Identification of a novel domain in two mammalian inositol-polyphosphate 5-phosphatases that mediates membrane ruffle localization. The inositol 5-phosphatase skip localizes to the endoplasmic reticulum and translocates to membrane ruffles following epidermal growth factor stimulation. J. Biol. Chem., 278, 11376-11385.
29. Ijuin, T., Mochizuki, Y., Fukami, K., Funaki, M., Asano, T. and Takenawa, T. (2000) Identification and characterization of a novel inositol polyphosphate 5-phosphatase. J. Biol. Chem., 275, 10870-10875.
30. Insall, R.H. and Weiner, O.D. (2001) PIP3, PIP2, and cell movement - similar messages, different meanings? Dev. Cell, 1, 743-747.
31. Hilpela, P., Vartiainen, M.K. and Lappalainen, P. (2004) Regulation of the actin cytoskeleton by PI(4,5)P2 and PI(3,4,5)P3. Curr. Top. Microbiol. Immunol., 282, 117-163.
32. van Aelst, L. and Symons, M. (2002) Role of Rho family GTPases in epithelial morphogenesis. Genes Dev., 16, 1032-1054.