OCRL-mutated fibroblasts from patients with Dent-2 disease exhibit INPP5B-independent phenotypic variability relatively to Lowe syndrome cells

Human Molecular Genetics

Volumn 24, Issue 4, 2015, Pages 994-1006

  Montjean, Rodrick ^a,b   Aoidi, Rifdat ^a,b   Desbois, Pierrette ^a,b   Rucci, Julien ^a,b   Trichet, Michaël ^a,b   Salomon, Rémi ^c   Rendu, John ^d   Fauré, Julien ^d   Lunardi, Joël ^d   Gacon, Gérard ^a,b   Billuart, Pierre ^a,b   Dorseuil, Olivier ^a,b  

^a INSTITUT COCHIN   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

^d GRENOBLE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; F ACTIN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN INPP5B; PROTEIN OCRL 1; SYNAPTOJANIN; UNCLASSIFIED DRUG; ACTIN; OCRL PROTEIN, HUMAN; PHOSPHATASE; PHOSPHOINOSITIDE 5-PHOSPHATASE;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ALLELE; ARTICLE; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CLINICAL FEATURE; COMPARATIVE STUDY; CONTROLLED STUDY; DENT 2 DISEASE; DENT DISEASE; FRAMESHIFT MUTATION; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; LOWE SYNDROME; MALE; MISSENSE MUTATION; PHENOTYPE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; STRESS FIBER; AMINO ACID SUBSTITUTION; CELL CULTURE; EUKARYOTIC FLAGELLUM; FIBROBLAST; GENETICS; METABOLISM; MUTATION; NEPHROLITHIASIS; PATHOLOGY; PROTEIN TRANSPORT; X CHROMOSOME LINKED DISORDER;

ACTINS; AMINO ACID SUBSTITUTION; CELLS, CULTURED; CILIA; FIBROBLASTS; GENETIC DISEASES, X-LINKED; HUMANS; MUTATION; NEPHROLITHIASIS; OCULOCEREBRORENAL SYNDROME; PHENOTYPE; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN TRANSPORT;

EID: 84922441970     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu514     Document Type: Article

References (61)

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. Hichri, H., Rendu, J., Monnier, N., Coutton, C., Dorseuil, O., Poussou, R.V., Baujat, G., Blanchard, A., Nobili, F., Ranchin, B. et al. (2011) From Lowe syndrome to Dent disease: correlations between mutations of the OCRL1 gene and clinical and biochemical phenotypes. Hum. Mutat., 32, 379-388.
3. Fisher, S.E., van Bakel, I., Lloyd, S.E., Pearce, S.H., Thakker, R.V. and Craig, I.W. (1995) Cloning and characterization of CLCN5, the human kidney chloride channel gene implicated in Dent disease (an X-linked hereditary nephrolithiasis). Genomics, 29, 598-606.
4. Cho, H.Y., Lee, B.H., Choi, H.J., Ha, I.S., Choi, Y. and Cheong, H.I. (2008) Renal manifestations of Dent disease and Lowe syndrome. Pediatr. Nephrol., 23, 243-249.
5. Hoopes, R.R. Jr, Shrimpton, A.E., Knohl, S.J., Hueber, P., Hoppe, B., Matyus, J., Simckes, A., Tasic, V., Toenshoff, B., Suchy, S.F. et al. (2005) Dent Disease with mutations in OCRL1. Am. J. Hum. Genet., 76, 260-267.
6. Sekine, T., Nozu, K., Iyengar, R., Fu, X.J., Matsuo, M., Tanaka, R., Iijima, K., Matsui, E., Harita, Y., Inatomi, J. et al. (2007) OCRL1 mutations in patients with Dent disease phenotype in Japan. Pediatr. Nephrol., 22, 975-980.
7. Shrimpton, A.E., Hoopes, R.R. Jr, Knohl, S.J., Hueber, P., Reed, A.A., Christie, P.T., Igarashi, T., Lee, P., Lehman, A., White, C. et al. (2009) OCRL1 mutations in Dent 2 patients suggest a mechanism for phenotypic variability. Nephron. Physiol., 112, p27-p36.
8. Utsch, B., Bokenkamp, A., Benz, M.R., Besbas, N., Dotsch, J., Franke, I., Frund, S., Gok, F., Hoppe, B., Karle, S. et al. (2006) NovelOCRL1mutations in patients with the phenotype of Dent disease. Am. J. Kidney Dis., 48, 942 e941-914.
9. Mehta, Z.B., Pietka, G. and Lowe, M. (2014) The cellular and physiological functions of the Lowe syndrome protein OCRL1. Traffic, 15, 471-487.
10. Zhang, X., Jefferson, A.B., Auethavekiat, V. andMajerus, P.W. (1995) The protein deficient inLowe syndrome is a phosphatidylinositol-4, 5-bisphosphate 5-phosphatase. Proc. Natl. Acad. Sci. U. S. A., 92, 4853-4856.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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 andOCRLphosphatase remodel lipids and F-actin for successful cytokinesis. Nat. Cell. Biol., 13, 981-988.
16. 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.
17. 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.
18. Noakes, C.J., Lee, G. and Lowe, M. (2011) ThePHdomain proteins IPIP27A andBlinkOCRL1to receptor recycling in the endocytic pathway. Mol. Biol. Cell., 22, 606-623.
19. Rodriguez-Gabin, A.G., Ortiz, E., Demoliner, K., Si, Q., Almazan, G. and Larocca, J.N. (2010) Interaction of Rab31 and OCRL-1in oligodendrocytes: its role in transport of mannose 6-phosphate receptors. J. Neurosci. Res., 88, 589-604.
20. Ungewickell, A., Hugge, C., Kisseleva, M., Chang, S.C., Zou, J., Feng, Y., Galyov, E.E., Wilson, M. and Majerus, P.W. (2005) The identification and characterization of two phosphatidylinositol-4, 5-bisphosphate 4-phosphatases. Proc. Natl. Acad. Sci. U S A., 102, 18854-18859.
21. 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.
22. 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.
23. 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.
24. Coon, B.G., Hernandez, V., Madhivanan, K., Mukherjee, D., Hanna, C.B., Barinaga-Rementeria Ramirez, I., Lowe, M., Beales, P.L. and Aguilar, R.C. (2012) The Lowe syndrome protein OCRL1 is involved in primary cilia assembly. Hum. Mol. Genet., 21, 1835-1847.
25. 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.
26. 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.
27. 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(2)-dependent regulation of endosomal actin. EMBO J., 30, 4970-4985.
28. Luo, N., West, C.C., Murga-Zamalloa, C.A., Sun, L., Anderson, R.M., Wells, C.D., Weinreb, R.N., Travers, J.B., Khanna, H. and Sun, Y. (2012) OCRLlocalizes to the primary cilium: anewrole for cilia inLowesyndrome. Hum. Mol. Genet., 21, 3333-3344.
29. Rbaibi, Y., Cui, S., Mo, D., Carattino, M., Rohatgi, R., Satlin, L.M., Szalinski, C.M., Swanhart, L.M., Folsch, H., Hukriede, N.A. et al. (2012) OCRL1 modulates cilia length in renal epithelial cells. Traffic, 13, 1295-1305.
30. Ramirez, I.B., Pietka, G., Jones, D.R., Divecha, N., Alia, A., Baraban, S.C., Hurlstone, A.F. and Lowe, M. (2012) Impaired neural development in a zebrafish model for Lowe syndrome. Hum. Mol. Genet., 21, 1744-1759.
31. Pirruccello, M. and De Camilli, P. (2012) Inositol 5-phosphatases: insights from the Lowe syndrome protein OCRL. Trends Biochem. Sci., 37, 134-143.
32. 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 forOCRL1does not causeLowesyndrome in mice. J. Clin. Invest., 101, 2042-2053.
33. Luo, N., Kumar, A., Conwell, M., Weinreb, R.N., Anderson, R. and Sun, Y. (2013) Compensatory role of inositol 5-phosphatase INPP5B to OCRL in primary cilia formation in oculocerebrorenal syndrome of Lowe. PLoS One, 8, e66727.
34. Chabaa, L., Monnier, N., Dahri, S., Jorio, M., Lunardi, J. and Chabraoui, L. (2006) [Oculo-cerebro-renal Lowe syndrome: clinical, biochemical and molecular studies in a Moroccan patient]. Ann. Biol. Clin. (Paris), 64, 53-59.
35. Monnier, N., Satre, V., Lerouge, E., Berthoin, F. andLunardi, J. (2000) OCRL1 mutationanalysis inFrenchLowesyndromepatients: implications formolecular diagnosis strategy and genetic counseling. Hum. Mutat., 16, 157-165.
36. Satre, V., Monnier, N., Berthoin, F., Ayuso, C., Joannard, A., Jouk, P.S., Lopez-Pajares, I., Megabarne, A., Philippe, H.J., Plauchu, H. et al. (1999) Characterization of a germline mosaicism in families with Lowe syndrome, and identification of seven novel mutations in the OCRL1 gene. Am. J. Hum. Genet., 65, 68-76.
37. Chou, Y.Y., Chao, S.C., Chiou, Y.Y. and Lin, S.J. (2005) Identification of OCRL1 mutations in two Taiwanese Lowe syndrome patients. Acta. Paediatr. Taiwan, 46, 226-229.
38. Kawano, T., Indo, Y., Nakazato, H., Shimadzu, M. and Matsuda, I. (1998) Oculocerebrorenal syndrome of Lowe: three mutations in the OCRL1 gene derived from three patients with different phenotypes. Am. J. Med. Genet., 77, 348-355.
39. Delous, M., Hellman, N.E., Gaude, H.M., Silbermann, F., Le Bivic, A., Salomon, R., Antignac, C. and Saunier, S. (2009) Nephrocystin-1 and nephrocystin-4 are required for epithelial morphogenesis and associate with PALS1/PATJ and Par6. Hum. Mol. Genet., 18, 4711-4723.
40. Doughman, R.L., Firestone, A.J., Wojtasiak, M.L., Bunce, M.W. and Anderson, R.A. (2003) Membrane ruffling requires coordination between type Ialpha phosphatidylinositol phosphate kinase andRac signaling. J. Biol. Chem., 278, 23036-23045.
41. 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.
42. Fraley, T.S., Tran, T.C., Corgan, A.M., Nash, C.A., Hao, J., Critchley, D.R. and Greenwood, J.A. (2003) Phosphoinositide binding inhibits alpha-actinin bundling activity. J. Biol. Chem., 278, 24039-24045.
43. He, B., Xi, F., Zhang, X., Zhang, J. and Guo, W. (2007) Exo70 interacts with phospholipids and mediates the targeting of the exocyst to the plasma membrane. EMBO J., 26, 4053-4065.
44. Liu, J., Zuo, X., Yue, P. and Guo, W. (2007) Phosphatidylinositol 4, 5-bisphosphate mediates the targeting of the exocyst to the plasma membrane for exocytosis in mammalian cells. Mol. Biol. Cell., 18, 4483-4492.
45. Zuo, X., Guo, W. and Lipschutz, J.H. (2009) The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro. Mol. Biol. Cell., 20, 2522-2529.
46. Hammond, G.R., Fischer, M.J., Anderson, K.E., Holdich, J., Koteci, A., Balla, T. and Irvine, R.F. (2012) PI4P and PI(4, 5)P2 are essential but independent lipid determinants of membrane identity. Science, 337, 727-730.
47. Hammond, G.R., Schiavo, G. and Irvine, R.F. (2009) Immunocytochemical techniques reveal multiple, distinct cellular pools of PtdIns4P and PtdIns(4, 5)P(2). Biochem. J., 422, 23-35.
48. Fukuda, M., Kanno, E., Ishibashi, K. and Itoh, T. (2008) Large scale screening for novel rab effectors reveals unexpected broad Rab binding specificity. Mol. Cell. Proteomics, 7, 1031-1042.
49. Nadif Kasri, N. and Van Aelst, L. (2008) Rho-linked genes and neurological disorders. Pflugers Arch., 455, 787-797.
50. Weber, G.F. and Menko, A.S. (2006) Actin filament organization regulates the induction of lens cell differentiation and survival. Dev. Biol., 295, 714-729.
51. Grove, M., Demyanenko, G., Echarri, A., Zipfel, P.A., Quiroz, M.E., Rodriguiz, R.M., Playford, M., Martensen, S.A., Robinson, M.R., Wetsel, W.C. et al. (2004) ABI2-deficient mice exhibit defective cell migration, aberrant dendritic spine morphogenesis, and deficits in learning and memory. Mol. Cell. Biol., 24, 10905-10922.
52. Rohatgi, R., Milenkovic, L. and Scott, M.P. (2007) Patched1 regulates hedgehog signaling at the primary cilium. Science, 317, 372-376.
53. Schneider, L., Clement, C.A., Teilmann, S.C., Pazour, G.J., Hoffmann, E.K., Satir, P. and Christensen, S.T. (2005) PDGFRalphaalpha signaling is regulated through the primary cilium in fibroblasts. Curr. Biol., 15, 1861-1866.
54. Raghavan, V., Rbaibi, Y., Pastor-Soler, N.M., Carattino, M.D. andWeisz, O.A. (2014) Shear stress-dependent regulation of apical endocytosis in renal proximal tubule cellsmediated by primary cilia.Proc.Natl. Acad. Sci.U. S.A., 111, 8506-8511.
55. Kumamoto, N., Gu, Y., Wang, J., Janoschka, S., Takemaru, K., Levine, J. and Ge, S. (2012) A role for primary cilia in glutamatergic synaptic integration of adult-born neurons. Nat. Neurosci., 15, 399-405, S391.
56. Loi, M. (2006) Lowe syndrome. Orphanet J. Rare. Dis., 1, 16.
57. Suchy, S.F., Cronin, J.C. and Nussbaum, R.L. (2009) Abnormal bradykinin signalling in fibroblasts deficient in the PIP(2) 5-phosphatase, ocrl1. J. Inherit. Metab. Dis., 32, 280-288.
58. Oertner, T.G. and Matus, A. (2005) Calcium regulation of actin dynamics in dendritic spines. Cell. Calcium, 37, 477-482.
59. Gupta, P.D., Johar, K. and Vasavada, A. (2004) Causative and preventive action of calcium in cataracto-genesis. Acta Pharmacol. Sin., 25, 1250-1256.
60. 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.
61. 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.