The role of PI3P phosphatases in the regulation of autophagy

FEBS Letters

Volumn 584, Issue 7, 2010, Pages 1313-1318

  Vergne, Isabelle ^a   Deretic, Vojo ^a  

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

Author keywords

Autophagy; Jumpy; MTMR14; Myotubularin; Phosphatase; PI3P

Indexed keywords

BECLIN 1; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHOPROTEIN PHOSPHATASE; POLYPHOSPHOINOSITIDE;

AUTOPHAGY; CELL FUNCTION; CENTRONUCLEAR MYOPATHY; GENE MUTATION; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; MAMMAL CELL; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; X CHROMOSOME LINKED DISORDER; ANIMAL; CHEMISTRY; GENERAL ASPECTS OF DISEASE; METABOLISM;

MAMMALIA;

ANIMALS; AUTOPHAGY; DISEASE; HUMANS; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHOPROTEIN PHOSPHATASES;

EID: 77950505030     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.02.054     Document Type: Review

References (58)

1. Petiot A., Ogier-Denis E., Blommaart E.F., Meijer A.J., Codogno P. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 2000, 275:992-998.
2. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D., Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939.
3. Tassa A., Roux M.P., Attaix D., Bechet D.M. Class III phosphoinositide 3-kinase-Beclin1 complex mediates the amino acid-dependent regulation of autophagy in C2C12 myotubes. Biochem. J. 2003, 376:577-586.
4. Itakura E., Kishi C., Inoue K., Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol. Biol. Cell 2008, 19:5360-5372.
5. Simonsen A., Tooze S.A. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J. Cell Biol. 2009, 186:773-782.
6. Nobukuni T., Joaquin M., Roccio M., Dann S.G., Kim S.Y., Gulati P., Byfield M.P., Backer J.M., Natt F., Bos J.L., et al. Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc. Natl. Acad. Sci. USA 2005, 102:14238-14243.
7. Byfield M.P., Murray J.T., Backer J.M. HVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. J. Biol. Chem. 2005, 280:33076-33082.
8. Lindmo K., Stenmark H. Regulation of membrane traffic by phosphoinositide 3-kinases. J. Cell Sci. 2006, 119:605-614.
9. de Lartigue J., Polson H., Feldman M., Shokat K., Tooze S.A., Urbe S., Clague M.J. PIKfyve regulation of endosome-linked pathways. Traffic 2009, 10:883-893.
10. Rusten T.E., Vaccari T., Lindmo K., Rodahl L.M., Nezis I.P., Sem-Jacobsen C., Wendler F., Vincent J.P., Brech A., Bilder D., et al. ESCRTs and Fab1 regulate distinct steps of autophagy. Curr. Biol. 2007, 17:1817-1825.
11. Clague M.J., Lorenzo O. The myotubularin family of lipid phosphatases. Traffic 2005, 6:1063-1069.
12. Laporte J., Bedez F., Bolino A., Mandel J.L. Myotubularins, a large disease-associated family of cooperating catalytically active and inactive phosphoinositides phosphatases. Hum. Mol. Genet. 2003, 12:R285-292. (Spec No. 2).
13. Robinson F.L., Dixon J.E. Myotubularin phosphatases: policing 3-phosphoinositides. Trends Cell Biol. 2006, 16:403-412.
14. Mochizuki Y., Majerus P.W. Characterization of myotubularin-related protein 7 and its binding partner, myotubularin-related protein 9. Proc. Natl. Acad. Sci. USA 2003, 100:9768-9773.
15. Tosch V., Rohde H.M., Tronchere H., Zanoteli E., Monroy N., Kretz C., Dondaine N., Payrastre B., Mandel J.L., Laporte J. A novel PtdIns3P and PtdIns(3, 5)P2 phosphatase with an inactivating variant in centronuclear myopathy. Hum. Mol. Genet. 2006, 15:3098-3106.
16. Shen J., Yu W.M., Brotto M., Scherman J.A., Guo C., Stoddard C., Nosek T.M., Valdivia H.H., Qu C.K. Deficiency of MIP/MTMR14 phosphatase induces a muscle disorder by disrupting Ca(2+) homeostasis. Nat. Cell Biol. 2009, 11:769-776.
17. Laporte J., Blondeau F., Buj-Bello A., Tentler D., Kretz C., Dahl N., Mandel J.L. Characterization of the myotubularin dual specificity phosphatase gene family from yeast to human. Hum. Mol. Genet. 1998, 7:1703-1712.
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. Bolino A., Marigo V., Ferrera F., Loader J., Romio L., Leoni A., Di Duca M., Cinti R., Cecchi C., Feltri M.L., et al. Molecular characterization and expression analysis of Mtmr2, mouse homologue of MTMR2, the myotubularin-related 2 gene, mutated in CMT4B. Gene 2002, 283:17-26.
20. Parrish W.R., Stefan C.J., Emr S.D. 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.
21. Nicot A.S., Laporte J. Endosomal phosphoinositides and human diseases. Traffic 2008, 9:1240-1249.
22. Buj-Bello A., Laugel V., Messaddeq N., Zahreddine H., Laporte J., Pellissier J.F., Mandel J.L. The lipid phosphatase myotubularin is essential for skeletal muscle maintenance but not for myogenesis in mice. Proc. Natl. Acad. Sci. USA 2002, 99:15060-15065.
23. Lorenzo O., Urbe S., Clague M.J. Systematic analysis of myotubularins: heteromeric interactions, subcellular localisation and endosome related functions. J. Cell Sci. 2006, 119:2953-2959.
24. Zou J., Chang S.C., Marjanovic J., Majerus P.W. MTMR9 increases MTMR6 enzyme activity, stability, and role in apoptosis. J. Biol. Chem. 2009, 284:2064-2071.
25. Berger P., Berger I., Schaffitzel C., Tersar K., Volkmer B., Suter U. Multi-level regulation of myotubularin-related protein-2 phosphatase activity by myotubularin-related protein-13/set-binding factor-2. Hum. Mol. Genet. 2006, 15:569-579.
26. Kim S.A., Vacratsis P.O., Firestein R., Cleary M.L., Dixon J.E. Regulation of myotubularin-related (MTMR)2 phosphatidylinositol phosphatase by MTMR5, a catalytically inactive phosphatase. Proc. Natl. Acad. Sci. USA 2003, 100:4492-4497.
27. Schaletzky J., Dove S.K., Short B., Lorenzo O., Clague M.J., Barr F.A. Phosphatidylinositol-5-phosphate activation and conserved substrate specificity of the myotubularin phosphatidylinositol 3-phosphatases. Curr. Biol. 2003, 13:504-509.
28. 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. USA 2003, 100:12177-12182.
29. Lorenzo O., Urbe S., Clague M.J. Analysis of phosphoinositide binding domain properties within the myotubularin-related protein MTMR3. J. Cell Sci. 2005, 118:2005-2012.
30. Choudhury P., Srivastava S., Li Z., Ko K., Albaqumi M., Narayan K., Coetzee W.A., Lemmon M.A., Skolnik E.Y. Specificity of the myotubularin family of phosphatidylinositol-3-phosphatase is determined by the PH/GRAM domain. J. Biol. Chem. 2006, 281:31762-31769.
31. MacKeigan J.P., Murphy L.O., Blenis J. Sensitized RNAi screen of human kinases and phosphatases identifies new regulators of apoptosis and chemoresistance. Nat. Cell Biol. 2005, 7:591-600.
32. Laporte J., Blondeau F., Gansmuller A., Lutz Y., Vonesch J.L., Mandel J.L. The PtdIns3P phosphatase myotubularin is a cytoplasmic protein that also localizes to Rac1-inducible plasma membrane ruffles. J. Cell Sci. 2002, 115:3105-3117.
33. Cao C., Backer J.M., Laporte J., Bedrick E.J., Wandinger-Ness A. Sequential actions of myotubularin lipid phosphatases regulate endosomal PI(3)P and growth factor receptor trafficking. Mol. Biol. Cell 2008, 19:3334-3346.
34. Chaussade C., Pirola L., Bonnafous S., Blondeau F., Brenz-Verca S., Tronchere H., Portis F., Rusconi S., Payrastre B., Laporte J., et al. 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.
35. Cao C., Laporte J., Backer J.M., Wandinger-Ness A., Stein M.P. Myotubularin lipid phosphatase binds the hVPS15/hVPS34 lipid kinase complex on endosomes. Traffic 2007, 8:1052-1067.
36. Dowling J.J., Vreede A.P., Low S.E., Gibbs E.M., Kuwada J.Y., Bonnemann C.G., Feldman E.L. Loss of myotubularin function results in T-tubule disorganization in zebrafish and human myotubular myopathy. PLoS Genet. 2009, 5:e1000372.
37. Al-Qusairi L., Weiss N., Toussaint A., Berbey C., Messaddeq N., Kretz C., Sanoudou D., Beggs A.H., Allard B., Mandel J.L., et al. T-tubule disorganization and defective excitation-contraction coupling in muscle fibers lacking myotubularin lipid phosphatase. Proc. Natl. Acad. Sci. USA 2009, 106:18763-18768.
38. Bolis A., Coviello S., Visigalli I., Taveggia C., Bachi A., Chishti A.H., Hanada T., Quattrini A., Previtali S.C., Biffi A., et al. Dlg1, Sec8, and Mtmr2 regulate membrane homeostasis in Schwann cell myelination. J. Neurosci. 2009, 29:8858-8870.
39. Vergne I., Roberts E., Elmaoued R.A., Tosch V., Delgado M.A., Proikas-Cezanne T., Laporte J., Deretic V. Control of autophagy initiation by phosphoinositide 3-phosphatase jumpy. EMBO J. 2009, 28:2244-2258.
40. Young A.R., Chan E.Y., Hu X.W., Kochl R., Crawshaw S.G., High S., Hailey D.W., Lippincott-Schwartz J., Tooze S.A. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J. Cell Sci. 2006, 119:3888-3900.
41. Reggiori F., Tucker K.A., Stromhaug P.E., Klionsky D.J. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev. Cell 2004, 6:79-90.
42. Srivastava S., Li Z., Lin L., Liu G., Ko K., Coetzee W.A., Skolnik E.Y. The phosphatidylinositol 3-phosphate phosphatase myotubularin- related protein 6 (MTMR6) is a negative regulator of the Ca2+-activated K+ channel KCa3.1. Mol. Cell Biol. 2005, 25:3630-3638.
43. Kim H.J., Soyombo A.A., Tjon-Kon-Sang S., So I., Muallem S. The Ca(2+) channel TRPML3 regulates membrane trafficking and autophagy. Traffic 2009, 10:1157-1167.
44. Hoyer-Hansen M., Bastholm L., Szyniarowski P., Campanella M., Szabadkai G., Farkas T., Bianchi K., Fehrenbacher N., Elling F., Rizzuto R., et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 2007, 25:193-205.
45. Gordon P.B., Holen I., Fosse M., Rotnes J.S., Seglen P.O. Dependence of hepatocytic autophagy on intracellularly sequestered calcium. J. Biol. Chem. 1993, 268:26107-26112.
46. Walker D.M., Urbe S., Dove S.K., Tenza D., Raposo G., Clague M.J. Characterization of MTMR3. an inositol lipid 3-phosphatase with novel substrate specificity. Curr. Biol. 2001, 11:1600-1605.
47. Taguchi-Atarashi, N., Hamasaki, M., Matsunaga, K., Omori, H., Ktistakis, N.T., Yoshimori, T. and Noda, T. Modulation of local PtdIns3P levels by the PI phosphatase MTMR3 regulates constitutive autophagy. Traffic. [Epub ahead of print].
48. Ferguson C.J., Lenk G.M., Meisler M.H. Defective autophagy in neurons and astrocytes from mice deficient in PI(3, 5)P2. Hum. Mol. Genet. 2009, 18:4868-4878.
49. Tronchere H., Laporte J., Pendaries C., Chaussade C., Liaubet L., Pirola L., Mandel J.L., Payrastre B. Production of phosphatidylinositol 5-phosphate by the phosphoinositide 3-phosphatase myotubularin in mammalian cells. J. Biol. Chem. 2004, 279:7304-7312.
50. Pendaries C., Tronchere H., Arbibe L., Mounier J., Gozani O., Cantley L., Fry M.J., Gaits-Iacovoni F., Sansonetti P.J., Payrastre B. PtdIns5P activates the host cell PI3-kinase/Akt pathway during Shigella flexneri infection. EMBO J. 2006, 25:1024-1034.
51. Berger, P., Tersar, K., Ballmer-Hofer, K. and Suter, U. (2009) The CMT4B disease-causing proteins MTMR2 and MTMR13/SBF2 regulate AKT signaling. J. Cell Mol. Med. [Epub ahead of print].
52. Pankiv S., Alemu E.A., Brech A., Bruun J.A., Lamark T., Overvatn A., Bjorkoy G., Johansen T. FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J. Cell. Biol. 2010, 188:253-269.
53. Nandurkar H.H., Layton M., Laporte J., Selan C., Corcoran L., Caldwell K.K., Mochizuki Y., Majerus P.W., Mitchell C.A. Identification of myotubularin as the lipid phosphatase catalytic subunit associated with the 3-phosphatase adapter protein, 3-PAP. Proc. Natl. Acad. Sci. USA 2003, 100:8660-8665.
54. Robinson F.L., Dixon J.E. 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.
55. Bolino A., Bolis A., Previtali S.C., Dina G., Bussini S., Dati G., Amadio S., Del Carro U., Mruk D.D., Feltri M.L., et al. Disruption of Mtmr2 produces CMT4B1-like neuropathy with myelin outfolding and impaired spermatogenesis. J. Cell Biol. 2004, 167:711-721.
56. Previtali S.C., Zerega B., Sherman D.L., Brophy P.J., Dina G., King R.H., Salih M.M., Feltri L., Quattrini A., Ravazzolo R., et al. Myotubularin-related 2 protein phosphatase and neurofilament light chain protein, both mutated in CMT neuropathies, interact in peripheral nerve. Hum. Mol. Genet. 2003, 12:1713-1723.
57. Zhang J., Wong C.H., Xia W., Mruk D.D., Lee N.P., Lee W.M., Cheng C.Y. Regulation of Sertoli-germ cell adherens junction dynamics via changes in protein-protein interactions of the N-cadherin-beta-catenin protein complex which are possibly mediated by c-Src and myotubularin-related protein 2: an in vivo study using an androgen suppression model. Endocrinology 2005, 146:1268-1284.
58. Plant P.J., Correa J., Goldenberg N., Bain J., Batt J. The inositol phosphatase MTMR4 is a novel target of the ubiquitin ligase Nedd4. Biochem. J. 2009, 419:57-63.