Disease mutations in Rab7 result in unregulated nucleotide exchange and inappropriate activation

Human Molecular Genetics

Volumn 19, Issue 6, 2010, Pages 1033-1047

  McCray, Brett A ^a,b   Skordalakes, Emmanuel ^c   Taylor, J Paul ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c WISTAR INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATE; LEUCINE; PHENYLALANINE; RAB7 PROTEIN;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GENE ACTIVATION; GENE INACTIVATION; GENE MUTATION; HUMAN; HUMAN CELL; HYDROLYSIS; MUTANT; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION;

AMINO ACID SUBSTITUTION; BINDING SITES; CELL LINE; CHARCOT-MARIE-TOOTH DISEASE; CYTOPLASMIC VESICLES; ENZYME ACTIVATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; GUANOSINE TRIPHOSPHATE; HUMANS; INTRACELLULAR MEMBRANES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTANT PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS;

EID: 77950686629     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp567     Document Type: Article

References (57)

1. Sasaki, T., Kikuchi, A., Araki, S., Hata, Y., Isomura, M., Kuroda, S. and Takai, Y. (1990) Purification and characterization from bovine brain cytosol of a protein that inhibits the dissociation of GDP from and the subsequent binding of GTP to smg p25A, a ras p21-like GTP-binding protein. J. Biol. Chem., 265, 2333-2337.
2. Rak, A., Pylypenko, O., Durek, T., Watzke, A., Kushnir, S., Brunsveld, L., Waldmann, H., Goody, R.S. and Alexandrov, K. (2003) Structure of Rab GDP-dissociation inhibitor in complex with prenylated YPT1 GTPase. Science, 302, 646-650.
3. Sato, Y., Fukai, S., Ishitani, R. and Nureki, O. (2007) Crystal structure of the Sec4p.Sec2p complex in the nucleotide exchanging intermediate state. Proc. Natl Acad. Sci. USA, 104, 8305-8310.
4. Ullrich, O., Stenmark, H., Alexandrov, K., Huber, L.A., Kaibuchi, K., Sasaki, T., Takai, Y. and Zerial, M. (1993) Rab GDP dissociation inhibitor as a general regulator for the membrane association of rab proteins. J. Biol. Chem., 268, 18143-18150.
5. Feng, Y., Press, B. and Wandinger-Ness, A. (1995) Rab 7: an important regulator of late endocytic membrane traffic. J. Cell Biol., 131, 1435-1452.
6. Bucci, C., Thomsen, P., Nicoziani, P., McCarthy, J. and van Deurs, B. (2000) Rab7: a key to lysosome biogenesis. Mol. Biol. Cell, 11, 467-480.
7. Harrison, R.E., Bucci, C., Vieira, O.V., Schroer, T.A. and Grinstein, S. (2003) Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol. Cell. Biol., 23, 6494-6506.
8. Vitelli, R., Santillo, M., Lattero, D., Chiariello, M., Bifulco, M., Bruni, C.B. and Bucci, C. (1997) Role of the small GTPase Rab7 in the late endocytic pathway. J. Biol. Chem., 272, 4391-4397.
9. Saxena, S., Bucci, C., Weis, J. and Kruttgen, A. (2005) The small GTPase Rab7 controls the endosomal trafficking and neuritogenic signaling of the nerve growth factor receptor TrkA. J. Neurosci., 25, 10930-10940.
10. Ceresa, B.P. and Bahr, S.J. (2006) rab7 activity affects epidermal growth factor:epidermal growth factor receptor degradation by regulating endocytic trafficking from the late endosome. J. Biol. Chem., 281, 1099-1106.
11. Gutierrez, M.G., Munafo, D.B., Beron, W. and Colombo, M.I. (2004) Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J. Cell Sci., 117, 2687-2697.
12. Jager, S., Bucci, C., Tanida, I., Ueno, T., Kominami, E., Saftig, P. and Eskelinen, E.L. (2004) Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci., 117, 4837-4848.
13. Deinhardt, K., Salinas, S., Verastegui, C., Watson, R., Worth, D., Hanrahan, S., Bucci, C. and Schiavo, G. (2006) Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron, 52, 293-305.
14. Zweifel, L.S., Kuruvilla, R. and Ginty, D.D. (2005) Functions and mechanisms of retrograde neurotrophin signalling. Nat. Rev. Neurosci., 6, 615-625.
15. Barisic, N., Claeys, K.G., Sirotkovic-Skerlev, M., Lofgren, A., Nelis, E., De Jonghe, P. and Timmerman, V. (2008) Charcot-Marie-Tooth disease: a clinico-genetic confrontation. Ann. Hum. Genet., 72, 416-441.
16. Zuchner, S. and Vance, J.M. (2006) Mechanisms of disease: a molecular genetic update on hereditary axonal neuropathies. Nat. Clin. Pract. Neurol., 2, 45-53.
17. Houlden, H., King, R.H., Muddle, J.R., Warner, T.T., Reilly, M.M., Orrell, R.W. and Ginsberg, L. (2004) A novel RAB7 mutation associated with ulcero-mutilating neuropathy. Ann. Neurol., 56, 586-590.
18. 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. (2003) Mutations in the small GTP-ase late endosomal protein RAB7 cause Charcot-Marie-Tooth type 2B neuropathy. Am. J. Hum. Genet., 72, 722-727.
19. Meggouh, F., Bienfait, H.M., Weterman, M.A., de Visser, M. and Baas, F. (2006) Charcot-Marie-Tooth disease due to a de novo mutation of the RAB7 gene. Neurology, 67, 1476-1478.
20. Auer-Grumbach, M., De Jonghe, P., Wagner, K., Verhoeven, K., Hartung, H.P. and Timmerman, V. (2000) Phenotype-genotype correlations in a CMT2B family with refined 3q13-q22 locus. Neurology, 55, 1552-1557.
21. Spinosa, M.R., Progida, C., De Luca, A., Colucci, A.M., Alifano, P. and Bucci, C. (2008) Functional characterization of Rab7 mutant proteins associated with Charcot-Marie-Tooth type 2B disease. J. Neurosci., 28, 1640-1648.
22. Rak, A., Pylypenko, O., Niculae, A., Pyatkov, K., Goody, R.S. and Alexandrov, K. (2004) Structure of the Rab7:REP-1 complex: insights into the mechanism of Rab prenylation and choroideremia disease. Cell, 117, 749-760.
23. Romero Rosales, K., Peralta, E.R., Guenther, G.G., Wong, S.Y. and Edinger, A.L. (2009) Rab7 activation by growth factor withdrawal contributes to the induction of apoptosis. Mol. Biol. Cell, 20, 2831-2840.
24. Regazzi, R., Kikuchi, A., Takai, Y. and Wollheim, C.B. (1992) The small GTP-binding proteins in the cytosol of insulin-secreting cells are complexed to GDP dissociation inhibitor proteins. J. Biol. Chem., 267, 17512-17519.
25. Andres, D.A., Seabra, M.C., Brown, M.S., Armstrong, S.A., Smeland, T.E., Cremers, F.P. and Goldstein, J.L. (1993) cDNA cloning of component A of Rab geranylgeranyl transferase and demonstration of its role as a Rab escort protein. Cell, 73, 1091-1099.
26. Cantalupo, G., Alifano, P., Roberti, V., Bruni, C.B. and Bucci, C. (2001) Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes. EMBO J., 20, 683-693.
27. Mizuno, K., Kitamura, A. and Sasaki, T. (2003) Rabring7, a novel Rab7 target protein with a RING finger motif. Mol. Biol. Cell, 14, 3741-3752.
28. Stein, M.P., Feng, Y., Cooper, K.L., Welford, A.M. and Wandinger-Ness, A. (2003) Human VPS34 and p150 are Rab7 interacting partners. Traffic, 4, 754-771.
29. Johansson, M., Lehto, M., Tanhuanpaa, K., Cover, T.L. and Olkkonen, V.M. (2005) The oxysterol-binding protein homologue ORP1L interacts with Rab7 and alters functional properties of late endocytic compartments. Mol. Biol. Cell, 16, 5480-5492.
30. Rojas, R., van Vlijmen, T., Mardones, G.A., Prabhu, Y., Rojas, A.L., Mohammed, S., Heck, A.J., Raposo, G., van der Sluijs, P. and Bonifacino, J.S. (2008) Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol., 183, 513-526.
31. Jordens, I., Fernandez-Borja, M., Marsman, M., Dusseljee, S., Janssen, L., Calafat, J., Janssen, H., Wubbolts, R. and Neefjes, J. (2001) The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol., 11, 1680-1685.
32. Patterson, G.H. and Lippincott-Schwartz, J. (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science, 297, 1873-1877.
33. Wilkin, M., Tongngok, P., Gensch, N., Clemence, S., Motoki, M., Yamada, K., Hori, K., Taniguchi-Kanai, M., Franklin, E., Matsuno, K. et al. (2008) Drosophila HOPS and AP-3 complex genes are required for a Deltex-regulated activation of notch in the endosomal trafficking pathway. Dev, Cell, 15, 762-772.
34. Entchev, E.V., Schwabedissen, A. and Gonzalez-Gaitan, M. (2000) Gradient formation of the TGF-beta homolog Dpp. Cell, 103, 981-991.
35. Traut, T.W. (1994) Physiological concentrations of purines and pyrimidines. Mol. Cell. Biochem., 140, 1-22.
36. Johansson, M., Rocha, N., Zwart, W., Jordens, I., Janssen, L., Kuijl, C., Olkkonen, V.M. and Neefjes, J. (2007) Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor betalll spectrin. J. Cell Biol., 176, 459-471.
37. Brickner, J.H. and Fuller, R.S. (1997) SOI1 encodes a novel, conserved protein that promotes TGN-endosomal cycling of Kex2p and other membrane proteins by modulating the function of two TGN localization signals. J. Cell Biol., 139, 23-36.
38. Kuriyama, H., Asakawa, S., Minoshima, S., Maruyama, H., Ishii, N., Ito, K., Gejyo, F., Arakawa, M., Shimizu, N. and Kuwano, R. (2000) Characterization and chromosomal mapping of a novel human gene, ANKHZN. Gene, 253, 151-160.
39. Hanna, M.C. and Blackstone, C. (2009) Interaction of the SPG21 protein ACP33/maspardin with the aldehyde dehydrogenase ALDH16A1. Neurogenetics, 10, 217-228.
40. Soussan, L., Burakov, D., Daniels, M.P., Toister-Achituv, M., Porat, A., Yarden, Y. and Elazar, Z. (1999) ERG30, a VAP-33-related protein, functions in protein transport mediated by COPI vesicles. J. Cell Biol., 146, 301-311.
41. Rocha, N., Kuijl, C., van der Kant, R., Janssen, L., Houben, D., Janssen, H., Zwart, W. and Neefjes, J. (2009) Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150 Glued and late endosome positioning. J. Cell Biol., 185, 1209-1225.
42. Nishimura, A.L., Mitne-Neto, M., Silva, H.C., Richieri-Costa, A., Middleton, S., Cascio, D., Kok, F., Oliveira, J.R., Gillingwater, T., Webb, J. et al. (2004) A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am. J. Hum. Genet., 75, 822-831.
43. Simpson, M.A., Cross, H., Proukakis, C., Pryde, A., Hershberger, R., Chatonnet, A., Patton, M.A. and Crosby, A.H. (2003) Maspardin is mutated in mast syndrome, a complicated form of hereditary spastic paraplegia associated with dementia. Am. J. Hum. Genet., 73, 1147-1156.
44. van den Hurk, J.A., van de Pol, T.J., Molloy, C.M., Brunsmann, F., Ruther, K., Zrenner, E., Pinckers, A.J., Pawlowitzki, I.H., Bleeker-Wagemakers, E.M., Wieringa, B. et al. (1992) Detection and characterization of point mutations in the choroideremia candidate gene by PCR-SSCP analysis and direct DNA sequencing. Am. J. Hum. Genet., 50, 1195-1202.
45. Seabra, M.C., Brown, M.S. and Goldstein, J.L. (1993) Retinal degeneration in choroideremia: deficiency of rab geranylgeranyl transferase. Science, 259, 377-381.
46. D'Adamo, P., Menegon, A., Lo Nigro, C., Grasso, M., Gulisano, M., Tamanini, F., Bienvenu, T., Gedeon, A.K., Oostra, B., Wu, S.K. et al. (1998) Mutations in GDI1 are responsible for X-linked non-specific mental retardation. Nat. Genet., 19, 134-139.
47. Puls, I., Jonnakuty, C., LaMonte, B.H., Holzbaur, E.L., Tokito, M., Mann, E., Floeter, M.K., Bidus, K., Drayna, D., Oh, S.J. et al. (2003) Mutant dynactin in motor neuron disease. Nat. Genet., 33, 455-456.
48. Ikeda, Y., Dick, K.A., Weatherspoon, M.R., Gincel, D., Armbrust, K.R., Dalton, J.C., Stevanin, G., Durr, A., Zuhlke, C., Burk, K. et al. (2006) Spectrin mutations cause spinocerebellar ataxia type 5. Nat. Genet., 38, 184-190.
49. Cardoso, C., Leventer, R.J., Ward, H.L., Toyo-Oka, K., Chung, J., Gross, A., Martin, C.L., Allanson, J., Pilz, D.T., Olney, A.H. et al. (2003) Refinement of a 400-kb critical region allows genotypic differentiation between isolated lissencephaly, Miller-Dieker syndrome, and other phenotypes secondary to deletions of 17p13.3. Am. J. Hum. Genet., 72, 918-930.
50. Nixon, R.A., Yang, D.S. and Lee, J.H. (2008) Neurodegenerative lysosomal disorders: a continuum from development to late age. Autophagy, 4, 590-599.
51. Einarsdottir, E., Carlsson, A., Minde, J., Toolanen, G., Svensson, O., Solders, G., Holmgren, G., Holmberg, D. and Holmberg, M. (2004) A mutation in the nerve growth factor beta gene (NGFB) causes loss of pain perception. Hum. Mol. Genet., 13, 799-805.
52. Indo, Y., Tsuruta, M., Hayashida, Y., Karim, M.A., Ohta, K., Kawano, T., Mitsubuchi, H., Tonoki, H., Awaya, Y. and Matsuda, I. (1996) Mutations in the TRKA/NGF receptor gene in patients with congenital insensitivity to pain with anhidrosis. Nat. Genet., 13, 485-488.
53. Potterton, E., Briggs, P., Turkenburg, M. and Dodson, E. (2003) A graphical user interface to the CCP4 program suite. Acta Crystallogr. D. Biol. Crystallogr., 59, 1131-1137.
54. Cowtan, K. (1994) A CCP4 density modification package. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography, 31, 34-38.
55. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D. Biol. Crystallogr., 60, 2126-2132.
56. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S. et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D. Biol. Crystallogr., 54, 905-921.
57. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D. Biol. Crystallogr., 53, 240-255.