Myotubularin lipid phosphatase binds the hVPS15/hVPS34 lipid kinase complex on endosomes

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Volumn 8, Issue 8, 2007, Pages 1052-1067

  Cao, Canhong ^a   Laporte, Jocelyn ^b,c,d,e,f   Backer, Jonathan M ^g   Wandinger Ness, Angela ^a   Stein, Mary Pat ^h  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c INSERM   (France)

^d CNRS   (France)

^e UNIVERSITÉ DE STRASBOURG   (France)

^f l'alimentation et l'Environnement   (France)

^g ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^h CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Charcot Marie Tooth neuropathy; Endocytosis; Phosphatidylinositol 3 phosphatase or 3 kinase; Rab GTPase; X linked myotubular myopathy

Indexed keywords

ADAPTOR PROTEIN; EARLY ANTIGEN; ESTERASE; GLYCEROPHOSPHOLIPID; MYOTUBULARIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHATIDYLINOSITOL 3,5 BIPHOSPHATE; RAB PROTEIN; RAB5 PROTEIN; RAB7 PROTEIN; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING 15 PROTEIN; VACUOLAR PROTEIN SORTING 34 PROTEIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL MEMBRANE; CENTRONUCLEAR MYOPATHY; COMPLEX FORMATION; CONTROLLED STUDY; ENDOSOME; ENZYME BINDING; ENZYME DEGRADATION; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; IN VIVO STUDY; INTRACELLULAR TRANSPORT; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NEUROMUSCULAR DISEASE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SKELETAL MUSCLE; WILD TYPE; X CHROMOSOME LINKED DISORDER;

ANIMALS; CELL LINE; CRICETINAE; ENDOSOMES; PHOSPHOTRANSFERASES; PROTEIN BINDING; PROTEIN-TYROSINE-PHOSPHATASE; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 34447543013     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2007.00586.x     Document Type: Article

References (64)

1. Laporte J, Guiraud-Chaumeil C, Vincent MC, Mandel JL, Tanner SM, Liechti-Gallati S, Wallgren-Pettersson C, Dahl N, Kress W, Bolhuis PA, Fardeau M, Samson F, Bertini E. Mutations in the MTM1 gene implicated in X-linked myotubular myopathy. ENMC International Consortium on Myotubular Myopathy. European Neuro-Muscular Center. Hum Mol Genet 1997; 6: 1505-1511.
2. Dang H, Li Z, Skolnik EY, Fares H. Disease-related myotubularins function in endocytic traffic in Caenorhabditis elegans. Mol Biol Cell 2004; 15: 189-196.
3. Bolino A, Muglia M, Conforti FL, LeGuern E, Salih MA, Georgiou DM, Christodoulou K, Hausmanowa-Petrusewicz I, Mandich P, Schenone A, Gambardella A, Bono F, Quattrone A, Devoto M, Monaco AP. Charcot-Marie-Tooth type 4B is caused by mutations in the gene encoding myotubularin-related protein-2. Nat Genet 2000; 25: 17-19.
4. Azzedine H, Bolino A, Taieb T, Birouk N, Di Duca M, Bouhouche A, Benamou S, Mrabet A, Hammadouche T, Chkili T, Gouider R, Ravazzolo R, Brice A, Laporte J, LeGuern E. Mutations in MTMR13, a new pseudophosphatase homologue of MTMR2 and Sbf1, in two families with an autosomal recessive demyelinating form of Charcot-Marie-Tooth disease associated with early-onset glaucoma. Am J Hum Genet 2003; 72: 1141-1153.
5. Laporte J, Bedez F, Bolino A, Mandel JL. Myotubularins, a large disease-associated family of cooperating catalytically active and inactive phosphoinositides phosphatases. Hum Mol Genet 2003; 12: R285-R292.
6. Wishart MJ, Dixon JE. PTEN and myotubularin phosphatases: From 3-phosphoinositide dephosphorylation to disease. Trends Cell Biol 2002; 12: 579-585.
7. Kim SA, Vacratsis PO, Firestein R, Cleary ML, Dixon JE. Regulation of myotubularin-related (MTMR)2 phosphatidylinositol phosphatase by MTMR5, a catalytically inactive phosphatase. Proc Natl Acad Sci U S A 2003; 100: 4492-4497.
8. Mochizuki Y, Majerus PW. Characterization of myotubularin-related protein 7 and its binding partner, myotubularin-related protein 9. Proc Natl Acad Sci U S A 2003; 100: 9768-9773.
9. Nandurkar HH, Layton M, Laporte J, Selan C, Corcoran L, Caldwell KK, Mochizuki Y, Majerus PW, Mitchell CA. Identification of myotubularin as the lipid phosphatase catalytic subunit associated with the 3-phosphatase adapter protein, 3-PAP. Proc Natl Acad Sci U S A 2003; 100: 8660-8665.
10. Cui X, De Vivo I, Slany R, Miyamoto A, Firestein R, Cleary ML. Association of SET domain and myotubularin-related proteins modulates growth control. Nat Genet 1998; 18: 331-337.
11. Berger P, Schaffitzel C, Berger I, Ban N, Suter U. 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 2003; 100: 12177-12182.
12. Robinson FL, Dixon JE. The phosphoinositide-3-phosphatase MTMR2 associates with MTMR13, a membrane-associated pseudophosphatase also mutated in type 4B Charcot-Marie-Tooth disease. J Biol Chem 2005; 280: 31699-31707.
13. Tsujita K, Itoh T, Ijuin T, Yamamoto A, Shisheva A, Laporte J, Takenawa T. Myotubularin regulates the function of the late endosome through the GRAM domain-phosphatidylinositol 3,5-bisphosphate interaction. J Biol Chem 2004; 279: 13817-13824.
14. Laporte J, Blondeau F, Buj-Bello A, Tentler D, Kretz C, Dahl N, Mandel JL. Characterization of the myotubularin dual specificity phosphatase gene family from yeast to human. Hum Mol Genet 1998; 7: 1703-1712.
15. Blondeau F, Laporte J, Bodin S, Superti-Furga G, Payrastre B, Mandel JL. Myotubularin, a phosphatase deficient in myotubular myopathy, acts on phosphatidylinositol 3-kinase and phosphatidylinositol 3-phosphate pathway. Hum Mol Genet 2000; 9: 2223-2229.
16. Taylor GS, Maehama T, Dixon JE. Myotubularin, a protein tyrosine phosphatase mutated in myotubular myopahty, dephosphorylates the lipid second messenger, phosphatidylinositol 3-phosphate. Proc Natl Acad Sci U S A 2000; 97: 8910-8915.
17. Walker DM, Urbe S, Dove SK, Tenza D, Raposo G, Clague MJ. Characterization of MTMR3. An inositol lipid 3-phosphatase with novel substrate specificity. Curr Biol 2001; 11: 1600-1605.
18. Berger P, Bonneick S, Willi S, Wymann M, Suter U. Loss of phosphatase activity in myotubularin-related protein 2 is associated with Charcot-Marie-Tooth disease type 4B1. Hum Mol Genet 2002; 11: 1569-1579.
19. Tronchere H, Laporte J, Pendaries C, Chaussade C, Liaubet L, Pirola L, Mandel JL, Payrastre B. Production of phosphatidylinositol 5-phosphate by the phosphoinositide 3-phosphatase myotubularin in mammalian cells. J Biol Chem 2004; 279: 7304-7312.
20. Gillooly DJ, Morrow IC, Linsay M, Gould R, Bryant NJ, Gaullier J-M, Parton RG, Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 2000; 19: 4577-4588.
21. Cooke FT. Phosphatidylinositol 3,5-bisphosphate: Metabolism and function. Arch Biochem Biophys 2002; 407: 143-151.
22. Gaullier JM, Simonsen A, D'Arrigo A, Bremnes B, Stenmark H, Aasland R. FYVE fingers bind PtdIns(3)P. Nature 1998; 394: 432-433.
23. Stenmark H, Aasland R, Toh BH, D'Arrigo A. Endosomal localization of the autoantigen EEA1 is mediated by a zinc-binding FYVE finger. J Biol Chem 1996; 271: 24048-24054.
24. Stenmark H, Aasland R. FYVE-finger proteins-effectors of an inositol lipid. J Cell Sci 1999; 112: 4175-4183.
25. Misra S, Miller GJ, Hurley JH. Recognizing phosphatidylinositol 3-phosphate. Cell 2001; 107: 559-562.
26. Bache KG, Brech A, Mehlum A, Stenmark H. Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J Cell Biol 2003; 162: 435-442.
27. Clague MJ, Urbe S. Hrs function: Viruses provide the clue. Trends Cell Biol 2003; 13: 603-606.
28. Futter CE, Collinson LM, Backer JM., Hopkins CR. Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J Cell Biol 2001; 155: 1251-1264.
29. Petiot A, Faure J, Stenmark H, Gruenberg J. PI3P signaling regulates receptor sorting but not transport in the endosomal pathway. J Cell Biol 2003; 162: 971-979.
30. Volinia S, Dhand R, Vanhaesebroeck B, MacDougall LK, Stein R, Zvelebil MJ, Domin J, Panaretou C, Waterfield MD. A human phosphatidylinositol 3-kinase complex related to the yeast Vps34p-Vps15p protein sorting system. EMBO J 1995; 14: 3339-3348.
31. Christoforidis S, Miaczynska M, Ashma K, Wilm M, Zhao L, Yip S-C, Waterfield MD, Backer JM, Zerial M. Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol 1999; 1: 249-252.
32. Stein MP, Feng Y, Cooper KL, Welford AM, Wandinger-Ness A. Human VPS34 and p150 are Rab7 interacting partners. Traffic 2003; 4: 754-771.
33. Siddhanta U, McIlroy J, Shah A, Zhang Y, Backer JM. Distinct roles for the p110alpha and hVPS34 phosphatidylinositol 3′-kinases in vesicular trafficking, regulation of the actin cytoskeleton, and mitogenesis. J Cell Biol 1998; 143: 1647-1659.
34. Ikonomov OC, Sbrissa D, Shisheva A. Mammalian cell morphology and endocytic membrane homeostasis require enzymatically active phosphoinositide 5-kinase PIKfyve. J Biol Chem 2001; 276: 26141-26147.
35. Gary JD, Wurmser AE, Bonangelino CJ, Weisman LS, Emr SD. Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J Cell Biol 1998; 143: 65-79.
36. Wurmser AE, Emr SD. Phosphoinositide signaling and turnover: PtdIns(3)P, a regulator of membrane traffic, is transported to the vacuole and degraded by a process that requires lumenal vacuolar hydrolase activities. EMBO J 1998; 17: 4930-4942.
37. Ikonomov OC, Sbrissa D, Foti M, Carpentier JL, Shisheva A. PIKfyve controls fluid phase endocytosis but not recycling/degradation of endocytosed receptors or sorting of procathepsin D by regulating multivesicular body morphogenesis. Mol Biol Cell 2003; 14: 4581-4591.
38. Murray JT, Panaretou C, Stenmark H, Miaczynska M, Backer JM. Role of Rab5 in the recruitment of hVps34/p150 to the early endosome. Traffic 2002; 3: 416-427.
39. Parrish WR, Stefan CJ, Emr SD. Essential role for the myotubularin-related phosphatase Ymr1p and the synaptojanin-like phosphatases Sjl2p and Sjl3p in regulation of phosphatidylinositol 3-phosphate in yeast. Mol Biol Cell 2004; 15: 3567-3579.
40. Shin HW, Hayashi M, Christoforidis S, Lacas-Gervais S, Hoepfner S, Wenk MR, Modregger J, Uttenweiler-Joseph S, Wilm M, Nystuen A, Frankel WN, Solimena M, De Camilli P, Zerial M. An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J Cell Biol 2005; 170: 607-618.
41. Stein M-P, Cao C, Tessema M, Feng Y, Romero E, Welford A, Wandinger-Ness A. Interaction and functional analyses of human VPS34/p150 phosphatidylinositol 3-kinase complex with Rab7. In: Balch W, Hall A, editors. Methods in Enzymology. New York: Elsevier Inc.; 2005, pp. 628-649.
42. Panaretou C, Domin J, Cockcroft S, Waterfield MD. Characterization of p150, an adapter protein for the human phosphatidylinositol (PtdIns) 3-kinase. Substrate presentation by phosphatidylinositol transfer protein to the p150.Ptdins 3-kinase complex. J Biol Chem 1997; 272: 2477-2485.
43. Chaussade C, Pirola L, Bonnafous S, Blondeau F, Brenz-Verca S, Tronchere H, Portis F, Rusconi S, Payrastre B, Laporte J, Van Obberghen E. Expression of myotubularin by an adenoviral vector demonstrates its function as a phosphatidylinositol 3-phosphate [PtdIns(3)P] phosphatase in muscle cell lines: Involvement of PtdIns(3)P in insulin-stimulated glucose transport. Mol Endocrinol 2003; 17: 2448-2460.
44. Willingham MC. An alternative fixation-processing method for preembedding ultrastructural immunocytochemistry of cytoplasmic antigens: The GBS (glutaraldehyde-borohydride-saponin) procedure. J Histochem Cytochem 1983; 31: 791-798.
45. Goldenthal KL, Hedman K, Chen JW, August JT, Willingham MC. Postfixation detergent treatment for immunofluorescence suppresses localization of some integral membrane proteins. J Histochem Cytochem 1985; 33: 813-820.
46. Patki V, Virbasius J, Lane WS, Toh BH, Shpetner HS, Corvera S. Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase. Proc Natl Acad Sci U S A 1997; 94: 7326-7330.
47. Schaletzky J, Dove SK, Short B, Lorenzo O, Clague MJ, Barr FA. Phosphatidylinositol-5-phosphate activation and conserved substrate specificity of the myotubularin phosphatidylinositol 3-phosphatases. Curr Biol 2003; 13: 504-509.
48. Sonnichsen B, De Renzis S, Nielsen E, Rietdork J, Zerial M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of rab4, rab5, and rab11. J Cell Biol 2000; 149: 901-913.
49. Feng Y, Press B, Chen W, Zimmerman J, Wandinger-Ness A. Expression and properties of Rab7 in endosome function. In: Hall A, editor. Methods in Enzymology. San Diego: Academic Press; 2001, pp. 175-187.
50. Press B, Feng Y, Hoflack B, Wandinger-Ness A. Mutant Rab7 causes the accumulation of cathepsin D and cation-independent mannose 6-phosphate receptor in an early endocytic compartment. J Cell Biol 1998; 140: 1075-1089.
51. Vonderheit A, Helenius A. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 2005; 3: E233.
52. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005; 122: 735-749.
53. Kim SA, Taylor GS, Torgersen KM, Dixon JE. Myotubularin and MTMR2, phosphatidylinositol 3-phosphatases mutated in myotubular myopathy and type 4B Charcot-Marie-Tooth disease. J Biol Chem 2002; 277: 4526-4531.
54. Laporte J, Blondeau F, Gansmuller A, Lutz Y, Vonesch JL, Mandel JL. The PtdIns3P phosphatase myotubularin is a cytoplasmic protein that also localizes to Rac1-inducible plasma membrane ruffles. J Cell Sci 2002; 115: 3105-3117.
55. Feng Y, Press B, Wandinger-Ness A. Rab 7: An important regulator of late endocytic membrane traffic. J Cell Biol 1995; 131: 1435-1452.
56. Bucci C, Wandinger-Ness A, Lutcke A, Chiariello M, Bruni CB, Zerial M. Rab5a is a common component of the apical and basolateral endocytic machinery in polarized epithelial cells. Proc Natl Acad Sci U S A 1994; 91: 5061-5065.
57. Qiu Y, Xu X, Wandinger-Ness A, Dalke DP, Pierce SK. Separation of subcellular compartments containing distinct functional forms of MHC class II. J Cell Biol 1994; 125: 595-605.
58. Waite RL, Sentry JW, Stenmark H, Toh BH. Autoantibodies to a novel early endosome antigen 1. Clin Immunol Immunopathol 1998; 86: 81-87.
59. Willingham MC. Electron microscopic immunocytochemical localization of intracellular antigens in cultured cells: The EGS and ferritin bridge procedures. Histochem J 1980; 12: 419-434.
60. Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 1990; 62: 317-329.
61. Estrada-Garcia T, Craxton A, Kirk CJ, Michell RH. A salt-activated inositol 1,3,4,5-tetrakisphosphate 3-phosphatase at the inner surface of the human erythrocyte membrane. Proc Biol Sci 1991; 244: 63-68.
62. Ohsaki Y, Maeda T, Fujimoto T. Fixation and permeabilization protocol is critical for the immunolabeling of lipid droplet proteins. Histochem Cell Biol 2005; 124: 445-452.
63. Taylor GS, Liu Y, Baskerville C, Charbonneau H. The activity of Cdc14p, an oligomeric dual specificity protein phosphatase from Saccharomyces cerevisiae, is required for cell cycle progression. J Biol Chem 1997; 272: 24054-24063.
64. Stein M-P, Dong J, Wandinger-Ness A. Rab proteins and endocytic trafficking: Potential targets for therapeutic intervention. Advanced Drug Delivery Reviews 2003; 55: 1421-1437.