Charcot-Marie-Tooth 2B mutations in rab7 cause dosage-dependent neurodegeneration due to partial loss of function

eLife

Volumn 2013, Issue 2, 2013, Pages

  Cherry, Smita ^a   Jin, Eugene Jennifer ^a   Özel, Mehmet Neset ^a   Lu, Zhiyuan ^b   Agi, Egemen ^a   Wang, Dong ^a   Jung, Wei Hung ^c   Epstein, Daniel ^a   Meinertzhagen, Ian A ^b   Chan, Chih Chiang ^a,c   Robin Hiesinger, P ^a,d  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b DALHOUSIE UNIVERSITY   (Canada)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RAB7 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHARCOT MARIE TOOTH 2B GENE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DROSOPHILA; ELECTROPHYSIOLOGY; ELECTRORETINOGRAPHY; GENE; GENE EXPRESSION; GENE MUTATION; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; NERVE DEGENERATION; NEUROMUSCULAR SYNAPSE; NEUROPATHY; NONHUMAN; PHOTORECEPTOR; POLYMERASE CHAIN REACTION; PROTEIN DEGRADATION; SENSORY NERVE CELL; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

CHARCOT-MARIE-TOOTH DISEASE; HUMANS; MALE; MIDDLE AGED; NEUROFIBROMATOSES; NEUROFIBROMATOSIS 1; PERIPHERAL NERVOUS SYSTEM NEOPLASMS; SPINAL NERVE ROOTS;

EID: 84890407183     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01064.001     Document Type: Article

References (45)

1. Basuray S, Mukherjee S, Romero EG, Seaman MN, Wandinger-Ness A. 2013. Rab7 mutants associated with Charcot-Marie-Tooth disease cause delayed growth factor receptor transport and altered endosomal and nuclear signaling. J Biol Chem 288:1135-49. doi: 10.1074/jbc.M112.417766.
2. Bischof J, Maeda RK, Hediger M, Karch F, Basler K. 2007. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci USA 104:3312-7. doi: 10.1073/pnas.0611511104.
3. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-15.
4. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B. 2000. Rab7: a key to lysosome biogenesis. Mol Biol Cell 11:467-80. doi: 10.1091/mbc.11.2.467.
5. Chan CC, Scoggin S, Hiesinger PR, Buszczak M. 2012. Combining recombineering and ends-out homologous recombination to systematically characterize Drosophila gene families: rab GTPases as a case study. Commun Integr Biol 5:179-83. doi: 10.4161/cib.18788.
6. Chan CC, Scoggin S, Wang D, Cherry S, Dembo T, Greenberg B, et al. 2011. Systematic discovery of Rab GTPases with synaptic functions in Drosophila. Curr Biol 21:1704-15. doi: 10.1016/j.cub.2011.08.058.
7. Chinchore Y, Mitra A, Dolph PJ. 2009. Accumulation of rhodopsin in late endosomes triggers photoreceptor cell degeneration. PLOS Genet 5:e1000377. doi: 10.1371/journal.pgen.1000377.
8. Chotard C, Leung W, Salecker I. 2005. glial cells missing and gcm2 cell autonomously regulate both glial and neuronal development in the visual system of Drosophila. Neuron 48:237-51. doi: 10.1016/j.neuron.2005.09.019.
9. Cogli L, Progida C, Lecci R, Bramato R, Kruttgen A, Bucci C. 2010. CMT2B-associated Rab7 mutants inhibit neurite outgrowth. Acta Neuropathol 120:491-501. doi: 10.1007/s00401-010-0696-8.
10. Cogli L, Progida C, Thomas CL, Spencer-Dene B, Donno C, Schiavo G, et al. 2013. Charcot-Marie-Tooth type 2B disease-causing RAB7A mutant proteins show altered interaction with the neuronal intermediate filament peripherin. Acta Neuropathol 125:257-72. doi: 10.1007/s00401-012-1063-8.
11. Coombe PE. 1986. The large monopolar cells L1 and L2 are responsible for ERG transients in Drosophila. J Comp Physiol A 159:655-65. doi: 10.1007/BF00612038.
12. De Luca A, Progida C, Spinosa MR, Alifano P, Bucci C. 2008. Characterization of the Rab7K157N mutant protein associated with Charcot-Marie-Tooth type 2B. Biochem Biophys Res Commun 372:283-7. doi: 10.1016/j.bbrc.2008.05.060.
13. Dermaut B, Norga KK, Kania A, Verstreken P, Pan H, Zhou Y, et al. 2005. Aberrant lysosomal carbohydrate storage accompanies endocytic defects and neurodegeneration in Drosophila benchwarmer. J Cell Biol 170:127-39. doi: 10.1083/jcb.200412001.
14. Elliott JL, Kwon JM, Goodfellow PJ, Yee WC. 1997. Hereditary motor and sensory neuropathy IIB: clinical and electrodiagnostic characteristics. Neurology 48:23-8. doi: 10.1212/WNL.48.1.23.
15. Fabian-Fine R, Verstreken P, Hiesinger PR, Horne JA, Kostyleva R, Zhou Y, et al. 2003. Endophilin promotes a late step in endocytosis at glial invaginations in Drosophila photoreceptor terminals. J Neurosci 23:10732-44.
16. Haberman A, Williamson WR, Epstein D, Wang D, Rina S, Meinertzhagen IA, et al. 2012. The synaptic vesicle SNARE neuronal Synaptobrevin promotes endolysosomal degradation and prevents neurodegeneration. J Cell Biol 196:261-76. doi: 10.1083/jcb.201108088.
17. Houlden H, King RH, Muddle JR, Warner TT, Reilly MM, Orrell RW, et al. 2004. A novel RAB7 mutation associated with ulcero-mutilating neuropathy. Ann Neurol 56:586-90. doi: 10.1002/ana.20281.
18. Imlach W, McCabe BD. 2009. Electrophysiological methods for recording synaptic potentials from the NMJ of Drosophila larvae. J Vis Exp doi: 10.3791/1109.
19. Kawamura N, Sun-Wada GH, Aoyama M, Harada A, Takasuga S, Sasaki T, et al. 2012. Delivery of endosomes to lysosomes via microautophagy in the visceral endoderm of mouse embryos. Nature Commun 3:1071. doi: 10.1038/ncomms2069.
20. Kinchen JM, Doukoumetzidis K, Almendinger J, Stergiou L, Tosello-Trampont A, Sifri CD, et al. 2008. A pathway for phagosome maturation during engulfment of apoptotic cells. Nat Cell Biol 10:556-66. doi: 10.1038/ncb1718.
21. Kwon JM, Elliott JL, Yee WC, Ivanovich J, Scavarda NJ, Moolsintong PJ, et al. 1995. Assignment of a second Charcot-Marie-Tooth type II locus to chromosome 3q. Am J Hum Genet 57:853-8.
22. Lloyd TE, Atkinson R, Wu MN, Zhou Y, Pennetta G, Bellen HJ. 2002. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108:261-9. doi: 10.1016/S0092-8674(02)00611-6.
23. McCray BA, Skordalakes E, Taylor JP. 2010. Disease mutations in Rab7 result in unregulated nucleotide exchange and inappropriate activation. Hum Mol Genet 19:1033-47. doi: 10.1093/hmg/ddp567.
24. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. 2003. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302:1765-8. doi: 10.1126/science.1089035.
25. Meggouh F, Bienfait HM, Weterman MA, de Visser M, Baas F. 2006. Charcot-Marie-Tooth disease due to a de novo mutation of the RAB7 gene. Neurology 67:1476-8. doi: 10.1212/01.wnl.0000240068.21499.f5.
26. Mehta SQ, Hiesinger PR, Beronja S, Zhai RG, Schulze KL, Verstreken P, et al. 2005. Mutations in Drosophila sec15 reveal a function in neuronal targeting for a subset of exocyst components. Neuron 46:219-32. doi: 10.1016/j.neuron.2005.02.029.
27. Meinertzhagen IA. 1996. Ultrastructure and quantification of synapses in the insect nervous system. J Neurosci Methods 69:59-73. doi: 10.1016/S0165-0270(96)00021-0.
28. Mukhopadhyay A, Barbieri AM, Funato K, Roberts R, Stahl PD. 1997a. Sequential actions of Rab5 and Rab7 regulate endocytosis in the Xenopus oocyte. J Cell Biol 136:1227-37. doi: 10.1083/jcb.136.6.1227.
29. Mukhopadhyay A, Funato K, Stahl PD. 1997b. Rab7 regulates transport from early to late endocytic compartments in Xenopus oocytes. J Biol Chem 272:13055-9. doi: 10.1074/jbc.272.20.13055.
30. Newsome TP, Asling B, Dickson BJ. 2000. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127:851-60.
31. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A. 2010. Identification of the switch in early-to-late endosome transition. Cell 141:497-508. doi: 10.1016/j.cell.2010.03.011.
32. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. 2005. Rab conversion as a mechanism of progression from early to late endosomes. Cell 122:735-49. doi: 10.1016/j.cell.2005.06.043.
33. Schultz ML, Tecedor L, Chang M, Davidson BL. 2011. Clarifying lysosomal storage diseases. Trends Neurosci 34:401-10. doi: 10.1016/j.tins.2011.05.006.
34. Skorobogata O, Rocheleau CE. 2012. RAB-7 antagonizes LET-23 EGFR signaling during vulva development in Caenorhabditis elegans. PLOS ONE 7:e36489. doi: 10.1371/journal.pone.0036489.
35. Spinosa MR, Progida C, De Luca A, Colucci AM, Alifano P, Bucci C. 2008. Functional characterization of Rab7 mutant proteins associated with Charcot-Marie-Tooth type 2B disease. J Neurosci 28:1640-8. doi: 10.1523/JNEUROSCI.3677-07.2008.
36. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF. 1994. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol A 175:179-91. doi: 10.1007/BF00215114.
37. Sweeney ST, Davis GW. 2002. Unrestricted synaptic growth in spinster-a late endosomal protein implicated in TGF-beta-mediated synaptic growth regulation. Neuron 36:403-16. doi: 10.1016/S0896-6273(02)01014-0.
38. Verhoeven K, De Jonghe P, Coen K, Verpoorten N, Auer-Grumbach M, Kwon JM, et al. 2003. Mutations in the small GTP-ase late endosomal protein RAB7 cause Charcot-Marie-Tooth type 2B neuropathy. Am J Hum Genet 72:722-7. doi: 10.1086/367847.
39. Wang D, Chan CC, Cherry S, Hiesinger PR. 2012. Membrane trafficking in neuronal maintenance and degeneration. Cell Mol Life Sci 70:2919-34. doi: 10.1007/s00018-012-1201-4.
40. Wang D, Hiesinger PR. 2012. Autophagy, neuron-specific degradation and neurodegeneration. Autophagy 8:711-3. doi: 10.4161/auto.19660.
41. Williamson WR, Hiesinger PR. 2010. Preparation of developing and adult Drosophila brains and retinae for live imaging. J Vis Exp doi: 10.3791/1936.
42. Williamson WR, Wang D, Haberman AS, Hiesinger PR. 2010. A dual function of V0-ATPase a1 provides an endolysosomal degradation mechanism in Drosophila melanogaster photoreceptors. J Cell Biol 189:885-99. doi: 10.1083/jcb.201003062.
43. Yamauchi J, Torii T, Kusakawa S, Sanbe A, Nakamura K, Takashima S, et al. 2010. The mood stabilizer valproic acid improves defective neurite formation caused by Charcot-Marie-Tooth disease-associated mutant Rab7 through the JNK signaling pathway. J Neurosci Res 88:3189-97. doi: 10.1002/jnr.22460.
44. Zhang J, Schulze KL, Hiesinger PR, Suyama K, Wang S, Fish M, et al. 2007. Thirty-one flavors of Drosophila rab proteins. Genetics 176:1307-22. doi: 10.1534/genetics.106.066761.
45. Zhang K, Fishel Ben Kenan R, Osakada Y, Xu W, Sinit RS, Chen L, et al. 2013. Defective axonal transport of Rab7 GTPase results in dysregulated trophic signaling. J Neurosci 33:7451-62. doi: 10.1523/JNEUROSCI.4322-12.2013.