The 5-phosphatase OCRL mediates retrograde transport of the mannose 6-phosphate receptor by regulating a Rac1-cofilin signalling module

Human Molecular Genetics

Volumn 21, Issue 23, 2012, Pages 5019-5038

  Van Rahden, Vanessa A ^a   Brand, Kristina ^a   Najm, Juliane ^a,c   Heeren, Joerg ^a   Pfeffer, Suzanne R ^b   Braulke, Thomas ^a   Kutsche, Kerstin ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COFILIN; IODINE 125; LYSOSOME ENZYME; PHOSPHATASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; RAC1 PROTEIN; SOMATOMEDIN B RECEPTOR; SYNAPTOJANIN;

ARTICLE; CELL LYSATE; CONGENITAL CATARACT; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; GENE; GENE MUTATION; HELA CELL; HUMAN; HUMAN CELL; INTERNALIZATION; ISOTOPE LABELING; KIDNEY TUBULE DISORDER; LOWE SYNDROME; MENTAL DEFICIENCY; MUSCLE HYPOTONIA; OCRL GENE; PATHOPHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; TRANS GOLGI NETWORK; X CHROMOSOME LINKED DISORDER;

ACTIN DEPOLYMERIZING FACTORS; ARYLSULFONATES; CATHEPSIN D; ENDOSOMES; FIBROBLASTS; HEK293 CELLS; HELA CELLS; HUMANS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; OCULOCEREBRORENAL SYNDROME; P21-ACTIVATED KINASES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN TRANSPORT; RAC1 GTP-BINDING PROTEIN; RECEPTOR, IGF TYPE 2; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANS-GOLGI NETWORK;

EID: 84869065602     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds343     Document Type: Article

References (81)

1. Lowe, C.U., Terrey, M. and Mac, L.E. (1952) Organic-aciduria, decreased renal ammonia production, hydrophthalmos, and mental retardation; a clinical entity. AMA Am. J. Dis. Child., 83, 164-184.
2. Loi, M. (2006) Lowe syndrome. Orphanet J. Rare Dis., 1, 16.
3. Bockenhauer, D., Bokenkamp, A., van't Hoff, W., Levtchenko, E., Kist-van Holthe, J.E., Tasic, V. and Ludwig, M. (2008) Renal phenotype in Lowe Syndrome: a selective proximal tubular dysfunction. Clin. J. Am. Soc. Nephrol., 3, 1430-1436.
4. 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.
5. Nussbaum, R.L., Orrison, B.M., Janne, P.A., Charnas, L. and Chinault, A.C. (1997) Physical mapping and genomic structure of the Lowe syndrome gene OCRL1. Hum. Genet., 99, 145-150.
6. Johnson, J.M., Castle, J., Garrett-Engele, P., Kan, Z., Loerch, P.M., Armour, C.D., Santos, R., Schadt, E.E., Stoughton, R. and Shoemaker, D.D. (2003) Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science, 302, 2141-2144.
7. Schmid, A.C., Wise, H.M., Mitchell, C.A., Nussbaum, R. and Woscholski, R. (2004) Type II phosphoinositide 5-phosphatases have unique sensitivities towards fatty acid composition and head group phosphorylation. FEBS Lett., 576, 9-13.
8. 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.
9. Mao, Y., Balkin, D.M., Zoncu, R., Erdmann, K.S., Tomasini, L., Hu, F., Jin, M.M., Hodsdon, M.E. and De Camilli, P. (2009) A PH domain within OCRL bridges clathrin-mediated membrane trafficking to phosphoinositide metabolism. EMBO J., 28, 1831-1842.
10. Ponting, C.P. (2006) A novel domain suggests a ciliary function for ASPM, a brain size determining gene. Bioinformatics, 22, 1031-1035.
11. Erdmann, K.S., Mao, Y., McCrea, H.J., Zoncu, R., Lee, S., Paradise, S., Modregger, J., Biemesderfer, D., Toomre, D. and De Camilli, P. (2007) A role of the Lowe syndrome protein OCRL in early steps of the endocytic pathway. Dev. Cell, 13, 377-390.
12. Lichter-Konecki, U., Farber, L.W., Cronin, J.S., Suchy, S.F. and Nussbaum, R.L. (2006) The effect of missense mutations in the RhoGAP-homology domain on ocrl1 function. Mol. Genet. Metab., 89, 121-128.
13. Hyvola, N., Diao, A., McKenzie, E., Skippen, A., Cockcroft, S. and Lowe, M. (2006) Membrane targeting and activation of the Lowe syndrome protein OCRL1 by rab GTPases. EMBO J., 25, 3750-3761.
14. 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.
15. Faucherre, A., Desbois, P., Nagano, F., Satre, V., Lunardi, J., Gacon, G. and Dorseuil, O. (2005) Lowe syndrome protein Ocrl1 is translocated to membrane ruffles upon Rac GTPase activation: a new perspective on Lowe syndrome pathophysiology. Hum. Mol. Genet., 14, 1441-1448.
16. Coon, B.G., Mukherjee, D., Hanna, C.B., Riese, D.J. 2nd, Lowe, M. and Aguilar, R.C. (2009) Lowe syndrome patient fibroblasts display Ocrl1-specific cell migration defects that cannot be rescued by the homologous Inpp5b phosphatase. Hum. Mol. Genet., 18, 4478-4491.
17. Ben El Kadhi, K., Roubinet, C., Solinet, S., Emery, G. and Carreno, S. (2011) The inositol 5-phosphatase dOCRL controls PI(4,5)P2 homeostasis and is necessary for cytokinesis. Curr. Biol., 21, 1074-1079.
18. Dambournet, D., Machicoane, M., Chesneau, L., Sachse, M., Rocancourt, M., El Marjou, A., Formstecher, E., Salomon, R., Goud, B. and Echard, A. (2011) Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat. Cell Biol., 13, 981-988.
19. Kühbacher, A., Dambournet, D., Echard, A., Cossart, P. and Pizarro-Cerda, J. (2012) The phosphatidylinositol 5-phosphatase oculocerebrorenal syndrome of Lowe protein (OCRL) controls actin dynamics during early steps of Listeria monocytogenes infection. J. Biol. Chem., 287, 13128-13136.
20. Vicinanza, M., Di Campli, A., Polishchuk, E., Santoro, M., Di Tullio, G., Godi, A., Levtchenko, E., De Leo, M.G., Polishchuk, R., Sandoval, L. et al. (2011) OCRL controls trafficking through early endosomes via PtdIns4,5P-dependent regulation of endosomal actin. EMBO J., 30, 4970-4985.
21. 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.
22. Choudhury, R., Diao, A., Zhang, F., Eisenberg, E., Saint-Pol, A., Williams, C., Konstantakopoulos, A., Lucocq, J., Johannes, L., Rabouille, C. et al. (2005) Lowe syndrome protein OCRL1 interacts with clathrin and regulates protein trafficking between endosomes and the trans-Golgi network. Mol. Biol. Cell, 16, 3467-3479.
23. Noakes, C.J., Lee, G. and Lowe, M. (2011) The PH domain proteins IPIP27A and B link OCRL1 to receptor recycling in the endocytic pathway. Mol. Biol. Cell, 22, 606-623.
24. Swan, L.E., Tomasini, L., Pirruccello, M., Lunardi, J. and De Camilli, P. (2010) Two closely related endocytic proteins that share a common OCRL-binding motif with APPL1. Proc. Natl Acad. Sci. USA, 107, 3511-3516.
25. 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.
26. Norden, A.G., Gardner, S.C., Van't Hoff, W. and Unwin, R.J. (2008) Lysosomal enzymuria is a feature of hereditary Fanconi syndrome and is related to elevated CI-mannose-6-P-receptor excretion. Nephrol. Dial. Transplant., 23, 2795-2803.
27. Braulke, T. and Bonifacino, J.S. (2009) Sorting of lysosomal proteins. Biochim. Biophys. Acta, 1793, 605-614.
28. Cui, S., Guerriero, C.J., Szalinski, C.M., Kinlough, C.L., Hughey, R.P. and Weisz, O.A. (2010) OCRL1 function in renal epithelial membrane traffic. Am. J. Physiol. Renal Physiol., 298, F335-F345.
29. Choudhury, R., Noakes, C.J., McKenzie, E., Kox, C. and Lowe, M. (2009) Differential clathrin binding and subcellular localization of OCRL1 splice isoforms. J. Biol. Chem., 284, 9965-9973.
30. Itin, C., Rancano, C., Nakajima, Y. and Pfeffer, S.R. (1997) A novel assay reveals a role for soluble N-ethylmaleimide-sensitive fusion attachment protein in mannose 6-phosphate receptor transport from endosomes to the trans Golgi network. J. Biol. Chem., 272, 27737-27744.
31. Ha, S.A., Torabinejad, J., DeWald, D.B., Wenk, M.R., Lucast, L., De Camilli, P., Newitt, R.A., Aebersold, R. and Nothwehr, S.F. (2003) The synaptojanin-like protein Inp53/Sjl3 functions with clathrin in a yeast TGN-to-endosome pathway distinct from the GGA protein-dependent pathway. Mol. Biol. Cell, 14, 1319-1333.
32. Malecz, N., McCabe, P.C., Spaargaren, C., Qiu, R., Chuang, Y. and Symons, M. (2000) Synaptojanin 2, a novel Rac1 effector that regulates clathrin-mediated endocytosis. Curr. Biol., 10, 1383-1386.
33. Olivos-Glander, I.M., Janne, P.A. and Nussbaum, R.L. (1995) The oculocerebrorenal syndrome gene product is a 105-kD protein localized to the Golgi complex. Am. J. Hum. Genet., 57, 817-823.
34. 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.
35. 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.
36. Garcia, P., Gupta, R., Shah, S., Morris, A.J., Rudge, S.A., Scarlata, S., Petrova, V., McLaughlin, S. and Rebecchi, M.J. (1995) The pleckstrin homology domain of phospholipase C-delta 1 binds with high affinity to phosphatidylinositol 4,5-bisphosphate in bilayer membranes. Biochemistry, 34, 16228-16234.
37. Yin, H.L. and Janmey, P.A. (2003) Phosphoinositide regulation of the actin cytoskeleton. Annu. Rev. Physiol., 65, 761-789.
38. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K. and Narumiya, S. (1999) Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science, 285, 895-898.
39. Manser, E., Leung, T., Salihuddin, H., Zhao, Z.S. and Lim, L. (1994) A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature, 367, 40-46.
40. Kligys, K., Claiborne, J.N., DeBiase, P.J., Hopkinson, S.B., Wu, Y., Mizuno, K. and Jones, J.C. (2007) The slingshot family of phosphatases mediates Rac1 regulation of cofilin phosphorylation, laminin-332 organization, and motility behavior of keratinocytes. J. Biol. Chem., 282, 32520-32528.
41. Zaidi, N., Maurer, A., Nieke, S. and Kalbacher, H. (2008) Cathepsin D: a cellular roadmap. Biochem. Biophys. Res. Commun., 376, 5-9.
42. Riederer, M.A., Soldati, T., Shapiro, A.D., Lin, J. and Pfeffer, S.R. (1994) Lysosome biogenesis requires Rab9 function and receptor recycling from endosomes to the trans-Golgi network. J. Cell Biol., 125, 573-582.
43. Williams, C., Choudhury, R., McKenzie, E. and Lowe, M. (2007) Targeting of the type II inositol polyphosphate 5-phosphatase INPP5B to the early secretory pathway. J. Cell Sci., 120, 3941-3951.
44. Janne, P.A., Suchy, S.F., Bernard, D., MacDonald, M., Crawley, J., Grinberg, A., Wynshaw-Boris, A., Westphal, H. and Nussbaum, R.L. (1998) Functional overlap between murine Inpp5b and Ocrl1 may explain why deficiency of the murine ortholog for OCRL1 does not cause Lowe syndrome in mice. J. Clin. Invest., 101, 2042-2053.
45. Sahagian, G.G. and Neufeld, E.F. (1983) Biosynthesis and turnover of the mannose 6-phosphate receptor in cultured Chinese hamster ovary cells. J. Biol. Chem., 258, 7121-7128.
46. Seaman, M.N. (2004) Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol., 165, 111-122.
47. Meyer, C., Eskelinen, E.L., Guruprasad, M.R., von Figura, K. and Schu, P. (2001) Mu 1A deficiency induces a profound increase in MPR300/IGF-II receptor internalization rate. J. Cell Sci., 114, 4469-4476.
48. Ganley, I.G., Espinosa, E. and Pfeffer, S.R. (2008) A syntaxin 10-SNARE complex distinguishes two distinct transport routes from endosomes to the trans-Golgi in human cells. J. Cell Biol., 180, 159-172.
49. Progida, C., Cogli, L., Piro, F., De Luca, A., Bakke, O. and Bucci, C. (2010) Rab7b controls trafficking from endosomes to the TGN. J. Cell Sci., 123, 1480-1491.
50. 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.
51. Allen, P.G. (2003) Actin filament uncapping localizes to ruffling lamellae and rocketing vesicles. Nat. Cell Biol., 5, 972-979.
52. Guerriero, C.J., Weixel, K.M., Bruns, J.R. and Weisz, O.A. (2006) Phosphatidylinositol 5-kinase stimulates apical biosynthetic delivery via an Arp2/3-dependent mechanism. J. Biol. Chem., 281, 15376-15384.
53. Arber, S., Barbayannis, F.A., Hanser, H., Schneider, C., Stanyon, C.A., Bernard, O. and Caroni, P. (1998) Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature, 393, 805-809.
54. Gorbatyuk, V.Y., Nosworthy, N.J., Robson, S.A., Bains, N.P., Maciejewski, M.W., Dos Remedios, C.G. and King, G.F. (2006) Mapping the phosphoinositide-binding site on chick cofilin explains how PIP2 regulates the cofilin-actin interaction. Mol. Cell, 24, 511-522.
55. Pandey, D., Goyal, P., Dwivedi, S. and Siess, W. (2009) Unraveling a novel Rac1-mediated signaling pathway that regulates cofilin dephosphorylation and secretion in thrombin-stimulated platelets. Blood, 114, 415-424.
56. Harrington, A.W., St Hillaire, C., Zweifel, L.S., Glebova, N.O., Philippidou, P., Halegoua, S. and Ginty, D.D. (2011) Recruitment of actin modifiers to TrkA endosomes governs retrograde NGF signaling and survival. Cell, 146, 421-434.
57. Erlmann, P., Schmid, S., Horenkamp, F.A., Geyer, M., Pomorski, T.G. and Olayioye, M.A. (2009) DLC1 activation requires lipid interaction through a polybasic region preceding the RhoGAP domain. Mol. Biol. Cell, 20, 4400-4411.
58. Crompton, A.M., Foley, L.H., Wood, A., Roscoe, W., Stokoe, D., McCormick, F., Symons, M. and Bollag, G. (2000) Regulation of Tiam1 nucleotide exchange activity by pleckstrin domain binding ligands. J. Biol. Chem., 275, 25751-25759.
59. Bollag, G. and McCormick, F. (1991) Differential regulation of rasGAP and neurofibromatosis gene product activities. Nature, 351, 576-579.
60. Chuang, T.H., Bohl, B.P. and Bokoch, G.M. (1993) Biologically active lipids are regulators of Rac.GDI complexation. J. Biol. Chem., 268, 26206-26211.
61. Zheng, Y., Glaven, J.A., Wu, W.J. and Cerione, R.A. (1996) Phosphatidylinositol 4,5-bisphosphate provides an alternative to guanine nucleotide exchange factors by stimulating the dissociation of GDP from Cdc42Hs. J. Biol. Chem., 271, 23815-23819.
62. Heo, W.D., Inoue, T., Park, W.S., Kim, M.L., Park, B.O., Wandless, T.J. and Meyer, T. (2006) PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science, 314, 1458-1461.
63. Jaffer, Z.M. and Chernoff, J. (2002) p21-activated kinases: three more join the Pak. Int. J. Biochem. Cell Biol., 34, 713-717.
64. Webb, B.A., Zhou, S., Eves, R., Shen, L., Jia, L. and Mak, A.S. (2006) Phosphorylation of cortactin by p21-activated kinase. Arch. Biochem. Biophys., 456, 183-193.
65. Poupon, V., Girard, M., Legendre-Guillemin, V., Thomas, S., Bourbonniere, L., Philie, J., Bright, N.A. and McPherson, P.S. (2008) Clathrin light chains function in mannose phosphate receptor trafficking via regulation of actin assembly. Proc. Natl Acad. Sci. USA, 105, 168-173.
66. Wen, P.J., Osborne, S.L., Zanin, M., Low, P.C., Wang, H.T., Schoenwaelder, S.M., Jackson, S.P., Wedlich-Soldner, R., Vanhaesebroeck, B., Keating, D.J. et al. (2011) Phosphatidylinositol(4,5)bisphosphate coordinates actin-mediated mobilization and translocation of secretory vesicles to the plasma membrane of chromaffin cells. Nat. Commun., 2, 491.
67. Morel, E., Parton, R.G. and Gruenberg, J. (2009) Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev. Cell, 16, 445-457.
68. Salvarezza, S.B., Deborde, S., Schreiner, R., Campagne, F., Kessels, M.M., Qualmann, B., Caceres, A., Kreitzer, G. and Rodriguez-Boulan, E. (2009) LIM kinase 1 and cofilin regulate actin filament population required for dynamin-dependent apical carrier fission from the trans-Golgi network. Mol. Biol. Cell, 20, 438-451.
69. von Blume, J., Alleaume, A.M., Cantero-Recasens, G., Curwin, A., Carreras-Sureda, A., Zimmermann, T., van Galen, J., Wakana, Y., Valverde, M.A. and Malhotra, V. (2011) ADF/cofilin regulates secretory cargo sorting at the TGN via the Ca2+ ATPase SPCA1. Dev. Cell, 20, 652-662.
70. von Blume, J., Duran, J.M., Forlanelli, E., Alleaume, A.M., Egorov, M., Polishchuk, R., Molina, H. and Malhotra, V. (2009) Actin remodeling by ADF/cofilin is required for cargo sorting at the trans-Golgi network. J. Cell Biol., 187, 1055-1069.
71. Ito, W., Ishiguro, H. and Kurosawa, Y. (1991) A general method for introducing a series of mutations into cloned DNA using the polymerase chain reaction. Gene, 102, 67-70.
72. Wimplinger, I., Morleo, M., Rosenberger, G., Iaconis, D., Orth, U., Meinecke, P., Lerer, I., Ballabio, A., Gal, A., Franco, B. et al. (2006) Mutations of the mitochondrial holocytochrome c-type synthase in X-linked dominant microphthalmia with linear skin defects syndrome. Am. J. Hum. Genet., 79, 878-889.
73. Marschner, K., Kollmann, K., Schweizer, M., Braulke, T. and Pohl, S. (2011) A key enzyme in the biogenesis of lysosomes is a protease that regulates cholesterol metabolism. Science, 333, 87-90.
74. Stoorvogel, W., Geuze, H.J. and Strous, G.J. (1987) Sorting of endocytosed transferrin and asialoglycoprotein occurs immediately after internalization in HepG2 cells. J. Cell Biol., 104, 1261-1268.
75. McFarlane, A.S. (1958) Efficient trace-labelling of proteins with iodine. Nature, 182, 53.
76. Heeren, J., Weber, W. and Beisiegel, U. (1999) Intracellular processing of endocytosed triglyceride-rich lipoproteins comprises both recycling and degradation. J. Cell Sci., 112, 349-359.
77. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
78. Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193, 265-275.
79. Braulke, T., Gartung, C., Hasilik, A. and von Figura, K. (1987) Is movement of mannose 6-phosphate-specific receptor triggered by binding of lysosomal enzymes? J. Cell Biol., 104, 1735-1742.
80. Sincock, P.M., Ganley, I.G., Krise, J.P., Diederichs, S., Sivars, U., O'Connor, B., Ding, L. and Pfeffer, S.R. (2003) Self-assembly is important for TIP47 function in mannose 6-phosphate receptor transport. Traffic, 4, 18-25.
81. Ganley, I.G., Carroll, K., Bittova, L. and Pfeffer, S. (2004) Rab9 GTPase regulates late endosome size and requires effector interaction for its stability. Mol. Biol. Cell, 15, 5420-5430.