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Defective Membrane Remodeling in Neuromuscular Diseases: Insights from Animal Models


Proteins involved in membrane remodeling play an essential role in a plethora of cell functions including endocytosis and intracellular transport. Defects in several of them lead to human diseases. Myotubularins, amphiphysins, and dynamins are all proteins implicated in membrane trafficking and/or remodeling. Mutations in myotubularin, amphiphysin 2 (BIN1), and dynamin 2 lead to different forms of centronuclear myopathy, while mutations in myotubularin-related proteins cause Charcot-Marie-Tooth neuropathies. In addition to centronuclear myopathy, dynamin 2 is also mutated in a dominant form of Charcot-Marie-Tooth neuropathy. While several proteins from these different families are implicated in similar diseases, mutations in close homologues or in the same protein in the case of dynamin 2 lead to diseases affecting different tissues. This suggests (1) a common molecular pathway underlying these different neuromuscular diseases, and (2) tissue-specific regulation of these proteins. This review discusses the pathophysiology of the related neuromuscular diseases on the basis of animal models developed for proteins of the myotubularin, amphiphysin, and dynamin families. A better understanding of the common mechanisms between these neuromuscular disorders will lead to more specific health care and therapeutic approaches.


Vyšlo v časopise: Defective Membrane Remodeling in Neuromuscular Diseases: Insights from Animal Models. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002595
Kategorie: Review
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002595

Souhrn

Proteins involved in membrane remodeling play an essential role in a plethora of cell functions including endocytosis and intracellular transport. Defects in several of them lead to human diseases. Myotubularins, amphiphysins, and dynamins are all proteins implicated in membrane trafficking and/or remodeling. Mutations in myotubularin, amphiphysin 2 (BIN1), and dynamin 2 lead to different forms of centronuclear myopathy, while mutations in myotubularin-related proteins cause Charcot-Marie-Tooth neuropathies. In addition to centronuclear myopathy, dynamin 2 is also mutated in a dominant form of Charcot-Marie-Tooth neuropathy. While several proteins from these different families are implicated in similar diseases, mutations in close homologues or in the same protein in the case of dynamin 2 lead to diseases affecting different tissues. This suggests (1) a common molecular pathway underlying these different neuromuscular diseases, and (2) tissue-specific regulation of these proteins. This review discusses the pathophysiology of the related neuromuscular diseases on the basis of animal models developed for proteins of the myotubularin, amphiphysin, and dynamin families. A better understanding of the common mechanisms between these neuromuscular disorders will lead to more specific health care and therapeutic approaches.


Zdroje

1. De MatteisMALuiniA 2011 Mendelian disorders of membrane trafficking. N Engl J Med 365 927 938

2. van WijngaardenGKFleuryPBethlemJMeijerAE 1969 Familial “myotubular” myopathy. Neurology 19 901 908

3. LaporteJHuLJKretzCMandelJLKioschisP 1996 A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast. Nat Genet 13 175 182

4. SenderekJBergmannCWeberSKetelsenUPSchorleH 2003 Mutation of the SBF2 gene, encoding a novel member of the myotubularin family, in Charcot-Marie-Tooth neuropathy type 4B2/11p15. Hum Mol Genet 12 349 356

5. AzzedineHBolinoATaiebTBiroukNDi DucaM 2003 Mutations in MTMR13, a new pseudophosphatase homologue of MTMR2 and Sbf1, in two families with an autosomal recessive demyelinating form of Charcot-Marie-ooth disease associated with early-onset glaucoma. Am J Hum Genet 72 1141 1153

6. BolinoAMugliaMConfortiFLLeGuernESalihMA 2000 Charcot-Marie-Tooth type 4B is caused by mutations in the gene encoding myotubularin-related protein-2. Nat Genet 25 17 19

7. SuterUSchererS 2003 Disease mechanisms in inherited neuropathies. Nat Rev Neurosci 4 714 726

8. NicotASLaporteJ 2008 Endosomal phosphoinositides and human diseases. Traffic 9 1240 1249

9. Di PaoloGDe CamilliP 2006 Phosphoinositides in cell regulation and membrane dynamics. Nature 443 651 657

10. VicinanzaMD'AngeloGDi CampliADe MatteisMA 2008 Phosphoinositides as regulators of membrane trafficking in health and disease. Cell Mol Life Sci 65 2833 2841

11. LaporteJBedezFBolinoAMandelJ-L 2003 Myotubularins, a large disease-associated family of cooperating catalytically active and inactive phosphoinositides phosphatases. Hum Mol Genet 12 285 292

12. BegleyMJDixonJE 2005 The structure and regulation of myotubularin phosphatases. Curr Opin Struct Biol 15 614 620

13. CuiXDe VivoISlanyRMiyamotoAFiresteinR 1998 Association of SET domain and myotubularin-related proteins modulates growth control. Nat Genet 18 331 337

14. LaporteJBlondeauFBuj-BelloATentlerDKretzC 1998 Characterization of the myotubularin dual specificity phosphatase gene family from yeast to human. Hum Mol Genet 7 1703 1712

15. ZouJChangSMarjanovicJMajerusP 2009 MTMR9 increases MTMR6 enzyme activity, stability, and role in apoptosis. J Biol Chem 2009 284 2064 2071

16. NandurkarHHLaytonMLaporteJSelanCCorcoranL 2003 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 100 8660 8665

17. MochizukiYMajerusPW 2003 Characterization of myotubularin-related protein 7 and its binding partner, myotubularin-related protein 9. Proc Natl Acad Sci U S A 100 9768 9773

18. KimSAVacratsisPOFiresteinRClearyMLDixonJE 2003 Regulation of myotubularin-related (MTMR)2 phosphatidylinositol phosphatase by MTMR5, a catalytically inactive phosphatase. Proc Natl Acad Sci U S A 100 4492 4497

19. RobinsonFLDixonJE 2005 The phosphoinositide-3-phosphatase MTMR2 associates with MTMR13, a membrane-associated pseudophosphatase also mutated in type 4B Charcot-Marie-Tooth disease. J Biol Chem 280 31699 31707

20. VelichkovaMJuanJKadandalePJeanSRibeiroI 2010 Drosophila Mtm and class II PI3K coregulate a PI(3)P pool with cortical and endolysosomal functions. J Cell Biol 190 407 425

21. RibeiroIYuanLTanentzapfGDowlingJJKigerA 2011 Phosphoinositide regulation of integrin trafficking required for muscle attachment and maintenance. PLoS Genet 7 e1001295 doi:10.1371/journal.pgen.1001295

22. LaporteJBlondeauFBuj-BelloAMandelJL 2001 The myotubularin family: from genetic disease to phosphoinositide metabolism. Trends Genet 17 221 228

23. WishartMJTaylorGSSlamaJTDixonJE 2001 PTEN and myotubularin phosphoinositide phosphatases: bringing bioinformatics to the lab bench. Curr Opin Cell Biol 13 172 181

24. XueYFaresHGrantBLiZRoseAM 2003 Genetic analysis of the myotubularin family of phosphatases in caenorhabditis elegans. J Biol Chem 278 34380 34386

25. FaresHGreenwaldI 2001 Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants. Genetics 159 133 145

26. DangHLiZSkolnikEYFaresH 2004 Disease-related myotubularins function in endocytic traffic in Caenorhabditis elegans. Mol Biol Cell 15 189 196

27. SilhankovaMPortFHarterinkMBaslerKKorswagenHC 2010 Wnt signalling requires MTM-6 and MTM-9 myotubularin lipid-phosphatase function in Wnt-producing cells. EMBO J 29 4094 4105

28. ZouWLuQZhaoDLiWMapesJ 2009 Caenorhabditis elegans myotubularin MTM-1 negatively regulates the engulfment of apoptotic cells. PLoS Genet 5 e1000679 doi:10.1371/journal.pgen.1000679

29. NeukommLJNicotASKinchenJMAlmendingerJPintoSM 2011 The phosphoinositide phosphatase MTM-1 regulates apoptotic cell corpse clearance through CED-5-CED-12 in C. elegans. Development 138 2003 2014

30. DowlingJJVreedeAPLowSEGibbsEMKuwadaJY 2009 Loss of myotubularin function results in T-tubule disorganization in zebrafish and human myotubular myopathy. PLoS Genet 5 e1000372 doi:10.1371/journal.pgen.1000372

31. RobbSASewryCADowlingJJFengLCullupT 2011 Impaired neuromuscular transmission and response to acetylcholinesterase inhibitors in centronuclear myopathies. Neuromuscul Disord 21 379 386

32. ShenJYuWMBrottoMSchermanJAGuoC 2009 Deficiency of MIP/MTMR14 phosphatase induces a muscle disorder by disrupting Ca(2+) homeostasis. Nat Cell Biol 11 769 776

33. HniaKKretzCAmoasiiLBohmJLiuX 2011 Primary T-tubule and autophagy defects in the phosphoinositide phosphatase Jumpy/MTMR14 knockout mice muscle. Adv Enzyme Regul In press

34. Buj-BelloALaugelVMessaddeqNZahreddineHLaporteJ 2002 The lipid phosphatase myotubularin is essential for skeletal muscle maintenance but not for myogenesis in mice. Proc Natl Acad Sci U S A 99 15060 15065

35. Al-QusairiLWeissNToussaintABerbeyCMessaddeqN 2009 T-tubule disorganization and defective excitation-contraction coupling in muscle fibers lacking myotubularin lipid phosphatase. Proc Natl Acad Sci U S A 106 18763 18768

36. ToussaintACowlingBSHniaKMohrMOldforsA 2011 Defects in amphiphysin 2 (BIN1) and triads in several forms of centronuclear myopathies. Acta Neuropathol 121 253 266

37. BeggsAHBohmJSneadEKozlowskiMMaurerM 2010 MTM1 mutation associated with X-linked myotubular myopathy in Labrador Retrievers. Proc Natl Acad Sci U S A 107 14697 14702

38. HniaKTronchereHTomczakKKAmoasiiLSchultzP 2011 Myotubularin controls desmin intermediate filament architecture and mitochondrial dynamics in human and mouse skeletal muscle. J Clin Invest 121 70 85

39. Buj-BelloAFougerousseFSchwabYMessaddeqNSpehnerD 2008 AAV-mediated intramuscular delivery of myotubularin corrects the myotubular myopathy phenotype in targeted murine muscle and suggests a function in plasma membrane homeostasis. Hum Mol Genet 17 2132 2143

40. BolinoABolisAPrevitaliSCDinaGBussiniS 2004 Disruption of Mtmr2 produces CMT4B1-like neuropathy with myelin outfolding and impaired spermatogenesis. J Cell Biol 167 711 721

41. BolisACovielloSBussiniSDinaGPardiniC 2005 Loss of Mtmr2 phosphatase in Schwann cells but not in motor neurons causes Charcot-Marie-Tooth type 4B1 neuropathy with myelin outfoldings. J Neurosci 25 8567 8577

42. BonneickSBoentertMBergerPAtanasoskiSManteiN 2005 An animal model for Charcot-Marie-Tooth disease type 4B1. Hum Mol Genet 14 3685 3695

43. TersarKBoentertMBergerPBonneickSWessigC 2007 Mtmr13/Sbf2-deficient mice: an animal model for CMT4B2. Hum Mol Genet 16 2991 3001

44. RobinsonFLNiesmanIRBeiswengerKKDixonJE 2008 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 105 4916 4921

45. BergerPBergerISchaffitzelCTersarKVolkmerB 2006 Multi-level regulation of myotubularin-related protein-2 phosphatase activity by myotubularin-related protein-13/set-binding factor-2. Hum Mol Genet 15 569 579

46. NicotASToussaintAToschVKretzCWallgren-PetterssonC 2007 Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy. Nat Genet 39 1134 1139

47. BohmJYisUOrtacRCakmakciHKurulSH 2010 Case report of intrafamilial variability in autosomal recessive centronuclear myopathy associated to a novel BIN1 stop mutation. Orphanet J Rare Dis 5 35

48. PeterBJKentHMMillsIGVallisYButlerPJ 2004 BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303 495 499

49. Wechsler-ReyaRSakamuroDZhangJDuhadawayJPrendergastGC 1997 Structural analysis of the human BIN1 gene. Evidence for tissue-specific transcriptional regulation and alternate RNA splicing. J Biol Chem 272 31453 31458

50. Wechsler-ReyaRJElliottKJPrendergastGC 1998 A role for the putative tumor suppressor Bin1 in muscle cell differentiation. Mol Cell Biol 18 566 575

51. LeeEMarcucciMDaniellLPypaertMWeiszOA 2002 Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297 1193 1196

52. De CamilliPThomasACofiellRFolliFLichteB 1993 The synaptic vesicle-associated protein amphiphysin is the 128-kD autoantigen of Stiff-Man syndrome with breast cancer. J Exp Med 178 2219 2223

53. RazzaqARobinsonIMMcMahonHTSkepperJNSuY 2001 Amphiphysin is necessary for organization of the excitation-contraction coupling machinery of muscles, but not for synaptic vesicle endocytosis in Drosophila. Genes Dev 15 2967 2979

54. PantSSharmaMPatelKCaplanSCarrC 2009 AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling. Nat Cell Biol 11 1399 1410

55. MullerAJBakerJFDuHadawayJBGeKFarmerG 2003 Targeted disruption of the murine Bin1/Amphiphysin II gene does not disable endocytosis but results in embryonic cardiomyopathy with aberrant myofibril formation. Mol Cell Biol 23 4295 4306

56. Di PaoloGSankaranarayananSWenkMRDaniellLPeruccoE 2002 Decreased synaptic vesicle recycling efficiency and cognitive deficits in amphiphysin 1 knockout mice. Neuron 33 789 804

57. KusumiNWatanabeMYamadaHLiSAKashiwakuraY 2007 Implication of amphiphysin 1 and dynamin 2 in tubulobulbar complex formation and spermatid release. Cell Struct Funct 32 101 113

58. BitounMMaugenreSJeannetPYLaceneEFerrerX 2005 Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat Genet 37 1207 1209

59. ZuchnerSNoureddineMKennersonMVerhoevenKClaeysK 2005 Mutations in the pleckstrin homology domain of dynamin 2 cause dominant intermediate Charcot-Marie-Tooth disease. Nat Genet 37 289 294

60. BitounMBevilacquaJAEymardBPrudhonBFardeauM 2009 A new centronuclear myopathy phenotype due to a novel dynamin 2 mutation. Neurology 72 93 95

61. BitounMBevilacquaJAPrudhonBMaugenreSTaratutoAL 2007 Dynamin 2 mutations cause sporadic centronuclear myopathy with neonatal onset. Ann Neurol 62 666 670

62. Echaniz-LagunaANicotASCarreSFranquesJTranchantC 2007 Subtle central and peripheral nervous system abnormalities in a family with centronuclear myopathy and a novel dynamin 2 gene mutation. Neuromuscul Disord 17 955 959

63. SchesslJMedneLHuYZouYBrownMJ 2007 MRI in DNM2-related centronuclear myopathy: evidence for highly selective muscle involvement. Neuromuscul Disord 17 28 32

64. PraefckeGJMcMahonHT 2004 The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5 133 147

65. JonesSMHowellKEHenleyJRCaoHMcNivenMA 1998 Role of dynamin in the formation of transport vesicles from the trans-Golgi network. Science 279 573 577

66. McNivenMACaoHPittsKRYoonY 2000 The dynamin family of mechanoenzymes: pinching in new places. Trends Biochem Sci 25 115 120

67. DurieuxACPrudhonBGuicheneyPBitounM 2010 Dynamin 2 and human diseases. J Mol Med 88 339 350

68. RamaswamiMKrishnanKRB.K 1994 Intermediates in synaptic vesicle recycling revealed by optical imaging of Drosophila neuromuscular junctions. Neuron 13 363 375

69. KosakaTIkedaK 1983 Reversible blockage of membrane retrieval and endocytosis in the garland cell of the temperature-sensitive mutant of Drosophila melanogaster, shibirets1. J Cell Biol 97 499 507

70. EstesPSRoosJvan der BliekAKellyRBKrishnanKS 1996 Traffic of dynamin within individual Drosophila synaptic boutons relative to compartment-specific markers. J Neurosci 16 5443 5456

71. TsuruharaTKoenigJIkedaK 1990 Synchronized endocytosis studied in the oocyte of a temperature-sensitive mutant of Drosophila melanogaster. Cell Tissue Res 259 199 207

72. JohnsonERingoJDowseH 2001 Dynamin, encoded by shibire, is central to cardiac function. J Exp Zool 289 81 89

73. ClarkSGShurlandDLMeyerowitzEMBargmannCIvan der BliekAM 1997 A dynamin GTPase mutation causes a rapid and reversible temperature-inducible locomotion defect in C. elegans. Proc Natl Acad Sci U S A 94 10438 10443

74. LabrousseAShurlandDvan der BliekA 1998 Contribution of the GTPase domain to the subcellular localization of dynamin in the nematode Caenorhabditis elegans. Mol Biol Cell 9 3227 3239

75. YuXOderaSChuangCHLuNZhouZ 2006 C. elegans Dynamin mediates the signaling of phagocytic receptor CED-1 for the engulfment and degradation of apoptotic cells. Dev Cell 10 743 757

76. NakayamaYShivasJPooleDSquirrellJKulkoskiJ 2009 Dynamin participates in the maintenance of anterior polarity in the Caenorhabditis elegans embryo. Dev Cell 16 889 900

77. FergusonSMBrasnjoGHayashiMWolfelMCollesiC 2007 A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316 570 574

78. RaimondiAFergusonSMLouXArmbrusterMParadiseS 2011 Overlapping role of dynamin isoforms in synaptic vesicle endocytosis. Neuron 70 1100 1114

79. PattersonEEMinorKMTchernatynskaiaAVTaylorSMSheltonGD 2008 A canine DNM1 mutation is highly associated with the syndrome of exercise-induced collapse. Nat Genet 40 1235 1239

80. FergusonSMRaimondiAParadiseSShenHMesakiK 2009 Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev Cell 17 811 822

81. DurieuxACVignaudAPrudhonBViouMTBeuvinM 2010 A centronuclear myopathy-dynamin 2 mutation impairs skeletal muscle structure and function in mice. Hum Mol Genet 19 4820 4836

82. CowlingBSToussaintAAmoasiiLKoebelPFerryA 2011 Increased expression of wild-type or a centronuclear myopathy mutant of dynamin 2 in skeletal muscle of adult mice leads to structural defects and muscle weakness. Am J Pathol 178 2224 2235

83. ReillyMMMurphySMLauraM 2011 Charcot-Marie-Tooth disease. J Peripher Nerv Syst 16 1 14

84. Hernandez-DeviezDJMartinSLavalSHLoHPCooperST 2006 Aberrant dysferlin trafficking in cells lacking caveolin or expressing dystrophy mutants of caveolin-3. Hum Mol Genet 15 129 142

85. KlingeLHarrisJSewryCCharltonRAndersonL 2010 Dysferlin associates with the developing T-tubule system in rodent and human skeletal muscle. Muscle Nerve 41 166 173

86. WangLBarylkoBByersCRossJAJamesonDM 2010 Dynamin 2 mutants linked to centronuclear myopathies form abnormally sTable polymers. J Biol Chem 285 22753 22757

87. KennistonJALemmonMA 2010 Dynamin GTPase regulation is altered by PH domain mutations found in centronuclear myopathy patients. Embo J 29 3054 3067

88. OwenDJWiggePVallisYMooreJDEvansPR 1998 Crystal structure of the amphiphysin-2 SH3 domain and its role in the prevention of dynamin ring formation. Embo J 17 5273 5285

89. BolinoAMarigoVFerreraFLoaderJRomioL 2002 Molecular characterization and expression analysis of Mtmr2, mouse homologue of MTMR2, the Myotubularin-related 2 gene, mutated in CMT4B. Gene 283 17 26

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