Endosomal Phosphoinositides and Human Diseases

Abstract

Phosphoinositides (PIs) are lipid second messengers implicated in signal transduction and membrane trafficking. Seven distinct PIs can be synthesized by phosphorylation of the inositol ring of phosphatidylinositol (PtdIns), and their metabolism is accurately regulated by PI kinases and phosphatases. Two of the PIs, PtdIns3 P and PtdIns(3,5) P 2 , are present on intracellular endosomal compartments, and several studies suggest that they have a role in membrane remodeling and trafficking. We refer to them as ‘endosomal PIs’. An increasing number of human genetic diseases including myopathy and neuropathies are associated to mutations in enzymes regulating the turnover of these endosomal PIs. The PtdIns3 P and PtdIns(3,5) P 2 3‐phosphatase myotubularin gene is mutated in X‐linked centronuclear myopathy, whereas its homologs MTMR2 and MTMR13 and the PtdIns(3,5) P 2 5‐phosphatase SAC3/FIG4 are implicated in Charcot–Marie–Tooth peripheral neuropathies. Mutations in the gene encoding the PtdIns3 P 5‐kinase PIP5K3/PIKfyve have been found in patients affected with François–Neetens fleck corneal dystrophy. This review presents the roles of the endosomal PIs and their regulators and proposes defects of membrane remodeling as a common pathological mechanism for the corresponding diseases.

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81. 81.

    Senderek J, Bergmann C, Weber S, Ketelsen UP, Schorle H, Rudnik-Schoneborn S, Buttner R, Buchheim E, Zerres K. Mutation of the SBF2 gene, encoding a novel member of the myotubularin family, in Charcot-Marie-Tooth neuropathy type 4B2/11p15. Hum Mol Genet. 2003;12:349-356.

    Not in our library10.1093/hmg/ddg030

82. 82.

    Hirano R, Takashima H, Umehara F, Arimura H, Michizono K, Okamoto Y, Nakagawa M, Boerkoel CF, Lupski JR, Osame M, Arimura K. SET binding factor 2 (SBF2) mutation causes CMT4B with juvenile onset glaucoma. Neurology. 2004;63:577-580.

    Not in our library10.1212/01.wnl.0000133211.40288.9a

83. 83.

    Robinson FL, Niesman IR, Beiswenger KK, Dixon JE. Loss of the inactive myotubularin-related phosphatase Mtmr13 leads to a Charcot-Marie-Tooth 4B2-like peripheral neuropathy in mice. Proc Natl Acad Sci U S A. 2008;105:4916-4921.

    Not in our library10.1073/pnas.0800742105

84. 84.

    Tersar K, Boentert M, Berger P, Bonneick S, Wessig C, Toyka KV, Young P, Suter U. Mtmr13/Sbf2-deficient mice: an animal model for CMT4B2. Hum Mol Genet. 2007;16:2991-3001.

    Not in our library10.1093/hmg/ddm257

85. 85.

    Laporte J, Hu LJ, Kretz C, Mandel JL, Kioschis P, Coy JF, Klauck SM, Poustka A, Dahl N. A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast. Nat Genet. 1996;13:175-182.

    Not in our library10.1038/ng0696-175

86. 86.

    Biancalana V, Caron O, Gallati S, Baas F, Kress W, Novelli G, D’Apice MR, Lagier-Tourenne C, Buj-Bello A, Romero NB, Mandel JL. Characterisation of mutations in 77 patients with X-linked myotubular myopathy, including a family with a very mild phenotype. Hum Genet. 2003;112:135-142.

    Not in our library10.1007/s00439-002-0869-1

87. 87.

    Laporte J, Biancalana V, Tanner SM, Kress W, Schneider V, Wallgren-Pettersson C, Herger F, Buj-Bello A, Blondeau F, Liechti-Gallati S, Mandel JL. MTM1 mutations in X-linked myotubular myopathy. Hum Mutat. 2000;15:393-409.

    Not in our library10.1002/(sici)1098-1004(200005)15:5<393::aid-humu1>3.0.co;2-r

88. 88.

    Laporte J, Kress W, Mandel JL. Diagnosis of X-linked myotubular myopathy by detection of myotubularin. Ann Neurol. 2001;50:42-46.

    Not in our library10.1002/ana.1033

89. 89.

    Buj-Bello A, Laugel V, Messaddeq N, Zahreddine H, Laporte J, Pellissier JF, Mandel JL. The lipid phosphatase myotubularin is essential for skeletal muscle maintenance but not for myogenesis in mice. Proc Natl Acad Sci U S A. 2002;99:15060-15065.

    Not in our library10.1073/pnas.212498399

90. 90.

    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.

    Not in our library10.1091/mbc.e03-08-0605

91. 91.

    Cao C, Laporte J, Backer JM, Wandinger-Ness A, Stein MP. Myotubularin lipid phosphatase binds the hVPS15/hVPS34 lipid kinase complex on endosomes. Traffic. 2007;8:1052-1067.

    Not in our library10.1111/j.1600-0854.2007.00586.x

92. 92.

    Fili N, Calleja V, Woscholski R, Parker PJ, Larijani B. Compartmental signal modulation: Endosomal phosphatidylinositol 3-phosphate controls endosome morphology and selective cargo sorting. Proc Natl Acad Sci U S A. 2006;103:15473-15478.

    Not in our library10.1073/pnas.0607040103

93. 93.

    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.

    Not in our library10.1074/jbc.m111087200

94. 94.

    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.

    Not in our library10.1242/jcs.115.15.3105

95. 95.

    Bolino A, Marigo V, Ferrera F, Loader J, Romio L, Leoni A, Di Duca M, Cinti R, Cecchi C, Feltri ML, Wrabetz L, Ravazzolo R, Monaco AP. Molecular characterization and expression analysis of Mtmr2, mouse homologue of MTMR2, the Myotubularin-related 2 gene, mutated in CMT4B. Gene. 2002;283:17-26.

    Not in our library10.1016/s0378-1119(01)00876-9

96. 96.

    Zuchner S, Noureddine M, Kennerson M, Verhoeven K, Claeys K, De Jonghe P, Merory J, Oliveira SA, Speer MC, Stenger JE, Walizada G, Zhu D, Pericak-Vance MA, Nicholson G, Timmerman V, et al. Mutations in the pleckstrin homology domain of dynamin 2 cause dominant intermediate Charcot-Marie-Tooth disease. Nat Genet. 2005;37:289-294.

    Not in our library10.1038/ng1514

97. 97.

    Street VA, Bennett CL, Goldy JD, Shirk AJ, Kleopa KA, Tempel BL, Lipe HP, Scherer SS, Bird TD, Chance PF. Mutation of a putative protein degradation gene LITAF/SIMPLE in Charcot-Marie-Tooth disease 1C. Neurology. 2003;60:22-26.

    Not in our library10.1212/wnl.60.1.22

98. 98.

    Verhoeven K, De Jonghe P, Coen K, Verpoorten N, Auer-Grumbach M, Kwon JM, FitzPatrick D, Schmedding E, De Vriendt E, Jacobs A, Van Gerwen V, Wagner K, Hartung HP, Timmerman V. Mutations in the small GTP-ase late endosomal protein RAB7 cause Charcot-Marie-Tooth type 2B neuropathy. Am J Hum Genet. 2003;72:722-727.

    Not in our library10.1086/367847

99. 99.

    Bitoun M, Maugenre S, Jeannet PY, Lacene E, Ferrer X, Laforet P, Martin JJ, Laporte J, Lochmuller H, Beggs AH, Fardeau M, Eymard B, Romero NB, Guicheney P. Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat Genet. 2005;37:1207-1209.

    Not in our library10.1038/ng1657

100. 100.

     Nicot AS, Toussaint A, Tosch V, Kretz C, Wallgren-Pettersson C, Iwarsson E, Kingston H, Garnier JM, Biancalana V, Oldfors A, Mandel JL, Laporte J. Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy. Nat Genet. 2007;39:1134-1139.

     Not in our library10.1038/ng2086

Cited by papers we hold 3

• Endosomal PI(3)P regulation by the COMMD/CCDC22/CCDC93 (CCC) complex controls membrane protein recycling · 2019
  No notice
• Phosphoinositides, Major Actors in Membrane Trafficking and Lipid Signaling Pathways · 2017
  No notice
• Loss of Myotubularin Function Results in T-Tubule Disorganization in Zebrafish and Human Myotubular Myopathy · 2009
  No notice

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