Charcot marie tooth 2B peripheral sensory neuropathy: How Rab7 mutations impact NGF signaling?

International Journal of Molecular Sciences

Volumn 18, Issue 2, 2017, Pages

  Liu, Harry ^a   Wu, Chengbiao ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Autophagy; Axons; CMT2B; Lysosomes; Mutations; NGF; Peripheral sensory neuropathy; Rab7

Indexed keywords

GUANOSINE TRIPHOSPHATASE; NERVE GROWTH FACTOR; OXYSTEROL BINDING PROTEIN RELATED PROTEIN 1L; PEPTIDES AND PROTEINS; PROTEIN TYROSINE KINASE A; RAB INTERACTING LYSOSOMAL PROTEIN; RAB7 PROTEIN; RABRING7 PROTEIN; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING ASSOCIATED PROTEIN 13; LYSOZYME; RAB PROTEIN;

AUTOPHAGY; CELL MIGRATION; GAIN OF FUNCTION MUTATION; GENE MUTATION; GENETIC ASSOCIATION; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; LOSS OF FUNCTION MUTATION; MISSENSE MUTATION; NERVE FIBER DEGENERATION; NONHUMAN; PATHOGENESIS; POINT MUTATION; PROTEIN DEGRADATION; REVIEW; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; AXON; CHEMISTRY; GENETIC ASSOCIATION STUDY; GENETICS; METABOLISM; MUTATION;

AXONS; CHARCOT-MARIE-TOOTH DISEASE; GENETIC ASSOCIATION STUDIES; HUMANS; MURAMIDASE; MUTATION; NERVE GROWTH FACTOR; RAB GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 85012000465     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms18020324     Document Type: Review

References (69)

1. Barisic, N.; Claeys, K.G.; Sirotković-Skerlev, M.; Löfgren, A.; Nelis, E.; de Jonghe, P.; Timmerman, V. Charcot-Marie-Tooth disease: A clinico-genetic confrontation. Ann. Hum. Genet. 2008, 72, 416–441.
2. Auer-Grumbach, M. Hereditary sensory neuropathies. Drugs Today 2004, 40, 385–394.
3. Auer-Grumbach, M.; De Jonghe, P.; Verhoeven, K.; Timmerman, V.; Wagner, K.; Hartung, H.P.; Nicholson, G.A. Autosomal dominant inherited neuropathies with prominent sensory loss and mutilations: A review. Arch. Neurol. 2003, 60, 329–334.
4. Auer-Grumbach, M.; De Jonghe, P.; Wagner, K.; Verhoeven, K.; Hartung, H.P.; Timmerman, V. Phenotype-genotype correlations in a CMT2B family with refined 3q13-q22 locus. Neurology 2000, 55, 1552–1557.
5. Auer-Grumbach, M.; Mauko, B.; Auer-Grumbach, P.; Pieber, T.R. Molecular genetics of hereditary sensory neuropathies. Neuromol. Med. 2006, 8, 147–158.
6. Auer-Grumbach, M.; Wagner, K.; Timmerman, V.; De Jonghe, P.; Hartung, H.P. Ulcero-mutilating neuropathy in an Austrian kinship without linkage to hereditary motor and sensory neuropathy IIB and hereditary sensory neuropathy I loci. Neurology 2000, 54, 45–52.
7. Gutmann, L.; Shy, M. Update on Charcot-Marie-Tooth disease. Curr. Opin. Neurol. 2015, 5, 462–467.
8. Mathis, S.; Goizet, C.; Tazir, M.; Magdelaine, C.; Lia, A.S.; Magy, L.; Vallat, J.M. Charcot-Marie-Tooth diseases: An update and some new proposals for the classification. J. Med. Genet. 2015.
9. Ekins, S.; Litterman, N.K.; Arnold, R.J.; Burgess, R.W.; Freundlich, J.S.; Gray, S.J.; Higgins, J.J.; Langley, B.; Willis, D.E.; Notterpek, L.; et al. A brief review of recent Charcot-Marie-Tooth research and priorities. F1000 Res. 2015, 4, 53.
10. Chartier-Harlin, M.C.; Kachergus, J.; Roumier, C.; Mouroux, V.; Douay, X.; Lincoln, S.; Levecque, C.; Larvor, L.; Andrieux, J.; Hulihan, M.; et al. α-synuclein locus duplication as a cause of familial Parkinson’s disease. Lancet 2004, 364, 1167–1169.
11. Harding, A.E.; Thomas, P.K. The clinical features of hereditary motor and sensory neuropathy types I and II. Brain 1980, 103, 259–280.
12. Bird, T.D. Charcot-Marie-Tooth Neuropathy Type 2; University of Washington: Seattle, WA, USA, 1993.
13. Gemignani, F.; Marbini, A. Charcot-Marie-Tooth disease (CMT): Distinctive phenotypic and genotypic features in CMT type 2. J. Neurol. Sci. 2001, 184, 1–9.
14. Kwon, J.M.; Elliott, J.L.; Yee, W.C.; Ivanovich, J.; Scavarda, N.J.; Moolsintong, P.J.; Goodfellow, P.J. Assignment of a second Charcot-Marie-Tooth type II locus to chromosome 3q. Am. J. Hum. Genet. 1995, 57, 853–858.
15. Lus, G.; Nelis, E.; Jordanova, A.; Löfgren, A.; Cavallaro, T.; Ammendola, A.; Melone, M.A.B.; Rizzuto, N.; Timmerman, V.; Cotrufo, R.; et al. Charcot-Marie-Tooth disease with giant axons: A clinicopathological and genetic entity. Neurology 2003, 61, 988–990.
16. Marrosu, M.G.; Vaccargiu, S.; Marrosu, G.; Vannelli, A.; Cianchetti, C.; Muntoni, F. Charcot-Marie-Tooth disease type 2 associated with mutation of the myelin protein zero gene. Neurology 1998, 50, 1397–1401.
17. Meggouh, F.; Bienfait, H.M.; Weterman, M.A.; de Visser, M.; Baas, F. Charcot-Marie-Tooth disease due to a de novo mutation of the Rab7 gene. Neurology 2006, 67, 1476–1478.
18. Mersiyanova, I.V.; Perepelov, A.V.; Polyakov, A.V.; Sitnikov, V.F.; Dadali, E.L.; Oparin, R.B.; Petrin, A.N.; Evgrafov, O.V. A new variant of Charcot-Marie-Tooth disease type 2 is probably the result of a mutation in the neurofilament-light gene. Am. J. Hum. Genet. 2000, 67, 37–46.
19. Mathis, S.; Magy, L.; Vallat, J.M. Therapeutic options in Charcot-Marie-Tooth diseases. Expert Rev. Neurother. 2015, 15, 355–366.
20. Jerath, N.U.; Shy, M.E. Hereditary motor and sensory neuropathies: Understanding molecular pathogenesis could lead to future treatment strategies. Biochim. Biophys. Acta 2015, 1852, 667–678.
21. Brennan, K.M.; Bai, Y.; Shy, M.E. Demyelinating CMT—What’s known, what’s new and what’s in store? Neurosci. Lett. 2015, 596, 14–26.
22. Fridman, V.; Bundy, B.; Reilly, M.M.; Pareyson, D.; Bacon, C.; Burns, J.; Day, J.; Feely, S.; Finkel, R.S.; Grider, T.; et al. CMT subtypes and disease burden in patients enrolled in the Inherited Neuropathies Consortium natural history study: A cross-sectional analysis. J. Neurol. Neurosurg. Psychiatry 2015, 86, 873–878.
23. Bennett, C.L.; Chance, P.F. Molecular pathogenesis of hereditary motor, sensory and autonomic neuropathies. Curr. Opin. Neurol. 2001, 14, 621–627.
24. Vance, J.M.; Speer, M.C.; Stajich, J.M.; West, S.; Wolpert, C.; Gaskell, P.; Lennon, F.; Tim, R.M.; Rozear, M.; Othmane, K.B. Misclassification and linkage of hereditary sensory and autonomic neuropathy type 1 as Charcot-Marie-Tooth disease, type 2B. Am. J. Hum. Genet. 1996, 59, 258–262.
25. Verpoorten, N.; De Jonghe, P.; Timmerman, V. Disease mechanisms in hereditary sensory and autonomic neuropathies. Neurobiol. Dis. 2006, 21, 247–255.
26. Skre, H. Genetic and clinical aspects of Charcot-Marie-Tooth’s disease. Clin. Genet. 1974, 6, 98–118.
27. Reilly, M.M. Classification and diagnosis of the inherited neuropathies. Ann. Indian Acad. Neurol. 2009, 12, 80–88.
28. Wang, X.; Han, C.; Liu, W.; Wang, P.; Zhang, X. A novel Rab7 mutation in a Chinese family with Charcot-Marie-Tooth type 2B disease. Gene 2014, 534, 431–434.
29. Dawkins, J.L.; Hulme, D.J.; Brahmbhatt, S.B.; Auer-Grumbach, M.; Nicholson, G.A. Mutations in SPTLC1, encoding serine palmitoyltransferase, long chain base subunit-1, cause hereditary sensory neuropathy type I. Nat. Genet. 2001, 27, 309–312.
30. Bucci, C.; Thomsen, P.; Nicoziani, P.; McCarthy, J.; van Deurs, B. Rab7: A key to lysosome biogenesis. Mol. Biol. Cell 2000, 11, 467–480.
31. Cai, H.; Reinisch, K.; Ferro-Novick, S. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev. Cell. 2007, 12, 671–682.
32. Grosshans, B.L.; Ortiz, D.; Novick, P. Rabs and their effectors: Achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. USA 2006, 103, 11821–11827.
33. Zhang, K.; Kenan, R.F.B.; Osakada, Y.; Xu, W.; Sinit, R.S.; Chen, L.; Zhao, X.; Chen, J.Y.; Cui, B.; Wu, C. Defective axonal transport of Rab7 GTPase results in dysregulated trophic signaling. J. Neurosci. 2013, 33, 7451–7462.
34. Houlden, H.; King, R.H.; Muddle, J.R.; Warner, T.T.; Reilly, M.M.; Orrell, R.W.; Ginsberg, L. A novel Rab7 mutation associated with ulcero-mutilating neuropathy. Ann. Neurol. 2004, 56, 586–590.
35. Verhoeven, K.; De Jonghe, P.; Coen, K.; Verpoorten, N.; Auer-Grumbach, M.; Kwon, J.M.; FitzPatrick, D.; Schmedding, E.; De Vriendt, E.; Jacobs, A.; et al. Mutations in the small GTPase late endosomal protein Rab7 cause Charcot-Marie-Tooth type 2B neuropathy. Am. J. Hum. Genet. 2003, 72, 722–727.
36. Cogli, L.; Piro, F.; Bucci, C. Rab7 and the CMT2B disease. Biochem. Soc. Trans. 2009, 37, 1027–1031.
37. McCray, B.A.; Skordalakes, E.; Taylor, J.P. Disease mutations in Rab7 result in unregulated nucleotide exchange and inappropriate activation. Hum. Mol. Genet. 2010, 19, 1033–1047.
38. Cogli, L.; Progida, C.; Lecci, R.; Bramato, R.; Krüttgen, A.; Bucci, C. CMT2B-associated Rab7 mutants inhibit Neurite outgrowth. Acta Neuropathol. 2010, 120, 491–501.
39. Spinosa, M.R.; Progida, C.; De Luca, A.; Colucci, A.M.R.; Alifano, P.; Bucci, C. Functional characterization of Rab7 mutant proteins associated with Charcot-Marie-Tooth type 2B disease. J. Neurosci. 2008, 28, 1640–1648.
40. Cogli, L.; Progida, C.; Thomas, C.L.; Spencer-Dene, B.; Donno, C.; Schiavo, G.; Bucci, C. Charcot-Marie-Tooth type 2B disease-causing Rab7a mutant proteins show altered interaction with the neuronal intermediate filament peripherin. Acta Neuropathol. 2013, 125, 257–272.
41. Cherry, S.; Jin, E.J.; Özel, M.N.; Lu, Z.; Agi, E.; Wang, D.; Jung, W.H.; Epstein, D.; Meinertzhagen, I.A.; Chan, C.C.; et al. Charcot-Marie-Tooth 2B mutations in Rab7 cause dosage-dependent neurodegeneration due to partial loss of function. Elife 2013, 2, e01064.
42. Wu, M.; Wang, T.; Loh, E.; Hong, W.; Song, H. Structural basis for recruitment of RILP by small GTPase Rab7. EMBO J. 2005, 24, 1491–1501.
43. Ponomareva, O.Y.; Eliceiri, K.W.; Halloran, M.C. Charcot-Marie-Tooth 2b associated Rab7 mutations cause axon growth and guidance defects during vertebrate sensory neuron development. Neural Dev. 2016, 11, 2.
44. Saxena, S.; Bucci, C.; Weis, J.; Kruttgen, A. The small GTPase Rab7 controls the endosomal trafficking and neuritogenic signaling of the nerve growth factor receptor TrkA. J. Neurosci. 2005, 25, 10930–10940.
45. BasuRay, S.; Mukherjee, S.; Romero, E.; Wilson, M.C.; Wandinger-Ness, A. Rab7 mutants associated with Charcot-Marie-Tooth disease exhibit enhanced NGF-stimulated signaling. PLoS ONE 2010, 5, e15351.
46. Cogli, L.; Progida, C.; Bramato, R.; Bucci, C. Vimentin phosphorylation and assembly are regulated by the small GTPase Rab7a. Biochim. Biophys. Acta 2013, 1833, 1283–1293.
47. Mizuno, K.; Kitamura, A.; Sasaki, T. Rabring7, a novel Rab7 target protein with a RING finger motif. Mol. Biol. Cell 2003, 14, 3741–3752.
48. Taub, N.; Teis, D.; Ebner, H.L.; Hess, M.W.; Huber, L.A. Late endosomal traffic of the epidermal growth factor receptor ensures spatial and temporal fidelity of mitogen-activated protein kinase signaling. Mol. Biol. Cell 2007, 18, 4698–4710.
49. Bottger, G.; Nagelkerken, B.; van der Sluijs, P. Rab4 and Rab7 define distinct nonoverlapping endosomal compartments. J. Biol. Chem. 1996, 271, 29191–29197.
50. Seals, D.F.; Eitzen, G.; Margolis, N.; Wickner, W.T.; Price, A. A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proc. Natl. Acad. Sci. USA 2000, 97, 9402–9407.
51. Wurmser, A.E.; Sato, T.K.; Emr, S.D. New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J. Cell Biol. 2000, 151, 551–562.
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. Russell, M.R.; Nickerson, D.P.; Odorizzi, G. Molecular mechanisms of late endosome morphology, identity and sorting. Curr. Opin. Cell. Biol. 2006, 18, 422–428.
54. Cantalupo, G.; Alifano, P.; Roberti, V.; Bruni, C.B.; Bucci, C. Rab-interacting lysosomal protein (RILP): The Rab7 effector required for transport to lysosomes. EMBO J. 2001, 20, 683–693.
55. Jordens, I.; Fernandez-Borja, M.; Marsman, M.; Dusseljee, S.; Janssen, L.; Calafat, J.; Janssen, H.; Wubbolts, R.; Neefjes, J. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 2001, 11, 1680–1685.
56. Progida, C.; Malerød, L.; Stuffers, S.; Brech, A.; Bucci, C.; Stenmark, H. RILP is required for the proper morphology and function of late endosomes. J. Cell Sci. 2007, 120, 3729–3737.
57. Johansson, M.; Rocha, N.; Zwart, W.; Jordens, I.; Janssen, L.; Kuijl, C.; Olkkonen, V.M.; Neefjes, J. Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor betalll spectrin. J. Cell Biol. 2007, 176, 459–471.
58. Nakada-Tsukui, K.; Saito-Nakano, Y.; Ali, V.; Nozaki, T. A retromerlike complex is a novel Rab7 effector that is involved in the transport of the virulence factor cysteine protease in the enteric protozoan parasite Entamoeba histolytica. Mol. Biol. Cell 2005, 16, 5294–5303.
59. Rojas, R.; van Vlijmen, T.; Mardones, G.A.; Prabhu, Y.; Rojas, A.L.; Mohammed, S.; Heck, A.J.; Raposo, G.; van der Sluijs, P.; Bonifacino, J.S. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol. 2008, 183, 513–526.
60. Sakane, A.; Hatakeyama, S.; Sasaki, T. Involvement of Rabring7 in EGF receptor degradation as an E3 ligase. Biochem. Biophys. Res. Commun. 2007, 357, 1058–1064.
61. Janssens, K.; Goethals, S.; Atkinson, D.; Ermanoska, B.; Fransen, E.; Jordanova, A.; Auer-Grumbach, M.; Asselbergh, B.; Timmerman, V. Human Rab7 mutation mimics features of Charcot-Marie-Tooth neuropathy type 2B in Drosophila. Neurobiol. Dis. 2014, 65, 211–219.
62. Seaman, M.N.; Harbour, M.E.; Tattersall, D.; Read, E.; Bright, N. Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5. J. Cell Sci. 2009, 122, 2371–2382.
63. Harrison, M.S.; Hung, C.S.; Liu, T.T.; Christiano, R.; Walther, T.C.; Burd, C.G. A mechanism for retromer endosomal coat complex assembly with cargo. Proc. Natl. Acad. Sci. USA 2014, 111, 267–272.
64. BasuRay, S.; Mukherjee, S.; Romero, E.G.; Seaman, M.N.; Wandinger-Ness, A. Rab7 mutants associated with Charcot-Marie-Tooth disease cause delayed growth factor receptor transport and altered endosomal and nuclear signaling. J. Biol. Chem. 2013, 288, 1135–1149.
65. Choudhury, A.; Dominguez, M.; Puri, V.; Sharma, D.K.; Narita, K.; Wheatley, C.L.; Marks, D.L.; Pagano, R.E. Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J. Clin. Investig. 2002, 109, 1541–1550.
66. Beilina, A.; Rudenko, I.N.; Kaganovich, A.; Civiero, L.; Chau, H.; Kalia, S.K.; Kalia, L.V.; Lobbestael, E.; Chia, R.; Ndukwe, K.; et al. Unbiased screen for interactors of leucine-rich repeat kinase 2 supports a common pathway for sporadic and familial Parkinson disease. Proc. Natl. Acad. Sci. USA 2014, 111, 2626–2631.
67. Satake, W.; Nakabayashi, Y.; Mizuta, I.; Hirota, Y.; Ito, C.; Kubo, M.; Kawaguchi, T.; Tsunoda, T.; Watanabe, M.; Takeda, A.; et al. Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson’s disease. Nat. Genet. 2009, 41, 1303–1307.
68. Simon-Sanchez, J.; Schulte, C.; Bras, J.M.; Sharma, M.; Gibbs, J.R.; Berg, D.; Paisan-Ruiz, C.; Lichtner, P.; Scholz, S.W.; Hernandez, D.G.; et al. Genome-wide association study reveals genetic risk underlying Parkinson’s disease. Nat. Genet. 2009, 41, 1308–1312.
69. MacLeod, D.A.; Rhinn, H.; Kuwahara, T.; Zolin, A.; Di Paolo, G.; McCabe, B.D.; Marder, K.S.; Honig, L.S.; Clark, L.N.; Small, S.A.; et al. RAB7L1 interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson’s disease risk. Neuron 2013, 77, 425–439.