Disruption of endocytic trafficking in frontotemporal dementia with CHMP2B mutations

Human Molecular Genetics

Volumn 19, Issue 11, 2010, Pages 2228-2238

  Urwin, Hazel ^a   Authier, Astrid ^a   Nielsen, Jorgen E ^b,c   Metcalf, Daniel ^a   Powell, Caroline ^a   Froud, Kristina ^a   Malcolm, Denise S ^a   Holm, Ida ^d,e   Johannsen, Peter ^c   Brown, Jeremy ^f   Fisher, Elizabeth M C ^a   van der Zee, Julie ^g,h   Bruyland, Marc ⁱ   Van Broeckhoven, Christine ^g,h   Collinge, John ^a   Brandner, Sebastian ^a   Futter, Clare ^j   Isaacs, Adrian M ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c Rigshospitalet   (Denmark)

^d RANDERS REGIONAL HOSPITAL   (Denmark)

^e AARHUS UNIVERSITY HOSPITAL   (Denmark)

^f ADDENBROOKE S HOSPITAL   (United Kingdom)

^g DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^h UNIVERSITY OF ANTWERP   (Belgium)

ⁱ Laboratory of Neurogenetics Institute Born Bunge University of Antwerp ^*  (Belgium)

^j UNIVERSITY COLLEGE LONDON   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MUTANT PROTEIN; PROTEIN CHMP2B; RAB7 PROTEIN; UNCLASSIFIED DRUG; CHMP2B PROTEIN, HUMAN; ESCRT PROTEIN; NERVE PROTEIN;

ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DISEASE COURSE; ENDOSOME; FIBROBLAST; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LYSOSOME; NERVE CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; CELL LINE; DENMARK; ELECTRON MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENETICS; IMMUNOHISTOCHEMISTRY; MEMBRANE FUSION; METABOLISM; MULTIVESICULAR BODY; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY; PEDIGREE; PHYSIOLOGY; PROTEIN TRANSPORT; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE; DENMARK; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; FRONTOTEMPORAL DEMENTIA; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; LYSOSOMES; MEMBRANE FUSION; MICROSCOPY, ELECTRON; MULTIVESICULAR BODIES; MUTATION; NERVE TISSUE PROTEINS; PEDIGREE; PROTEIN TRANSPORT;

EID: 77953583994     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq100     Document Type: Article

References (46)

1. Snowden, J.S., Neary, D. and Mann, D.M. (2002) Frontotemporal dementia. Br. J. Psychiatry, 180, 140-143.
2. Lindquist, S.G., Braedgaard, H., Svenstrup, K., Isaacs, A.M. and Nielsen, J.E. (2008) Frontotemporal dementia linked to chromosome 3 (FTD-3)-current concepts and the detection of a previously unknown branch of the Danish FTD-3 family. Eur. J. Neurol., 15, 667-670.
3. Gydesen, S., Brown, J.M., Brun, A., Chakrabarti, L., Gade, A., Johannsen, P., Rossor, M., Thusgaard, T., Grove, A., Yancopoulou, D. et al. (2002) Chromosome 3 linked frontotemporal dementia (FTD-3). Neurology, 59, 1585-1594.
4. Skibinski, G., Parkinson, N.J., Brown, J.M., Chakrabarti, L., Lloyd, S.L., Hummerich, H., Nielsen, J.E., Hodges, J.R., Spillantini, M.G., Thusgaard, T. et al. (2005) Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat. Genet., 37, 806-808.
5. Momeni, P., Rogaeva, E., Van, D.V., Yuan, W., Grafman, J., Tierney, M., Huey, E., Bell, J., Morris, C.M., Kalaria, R.N. et al. (2006) Genetic variability in CHMP2B and frontotemporal dementia. Neurodegener. Dis., 3, 129-133.
6. van der Zee, J., Urwin, H., Engelborghs, S., Bruyland, M., Vandenberghe, R., Dermaut, B., De, P.T., Peeters, K., Santens, P., De Deyn, P.P. et al. (2008) CHMP2B C-truncating mutations in frontotemporal lobar degeneration are associated with an aberrant endosomal phenotype in vitro. Hum. Mol. Genet., 17, 313-322.
7. Urwin, H., Ghazi-Noori, S., Collinge, J. and Isaacs, A. (2009) The role of CHMP2B in frontotemporal dementia. Biochem. Soc. Trans., 37, 208-212.
8. Katzmann, D.J., Odorizzi, G. and Emr, S.D. (2002) Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell. Biol., 3, 893-905.
9. Holm, I.E., Englund, E., Mackenzie, I.R., Johannsen, P. and Isaacs, A.M. (2007) A reassessment of the neuropathology of frontotemporal dementia linked to chromosome 3. J. Neuropathol. Exp. Neurol., 66, 884-891.
10. Rohrer, J.D., Ahsan, R.L., Isaacs, A.M., Nielsen, J.E., Ostergaard, L., Scahill, R., Warren, J.D., Rossor, M.N., Fox, N.C. and Johannsen, P. (2009) Presymptomatic generalized brain atrophy in frontotemporal dementia caused by CHMP2B mutation. Dement. Geriatr. Cogn. Disord., 27, 182-186.
11. Eskildsen, S.F., Ostergaard, L.R., Rodell, A.B., Ostergaard, L., Nielsen, J.E., Isaacs, A.M. and Johannsen, P. (2009) Cortical volumes and atrophy rates in FTD-3 CHMP2B mutation carriers and related non-carriers. Neuroimage, 45, 713-721.
12. Eden, E.R., White, I.J. and Futter, C.E. (2009) Down-regulation of epidermal growth factor receptor signalling within multivesicular bodies. Biochem. Soc. Trans., 37, 173-177.
13. Futter, C.E., Pearse, A., Hewlett, L.J. and Hopkins, C.R. (1996) Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell. Biol., 132, 1011-1023.
14. Rink, J., Ghigo, E., Kalaidzidis, Y. and Zerial, M. (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell, 122, 735-749.
15. Bache, K.G., Stuffers, S., Malerod, L., Slagsvold, T., Raiborg, C., Lechardeur, D., Walchli, S., Lukacs, G.L., Brech, A. and Stenmark, H. (2006) The ESCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. Mol. Biol. Cell, 17, 2513-2523.
16. Shim, J.H., Xiao, C., Hayden, M.S., Lee, K.Y., Trombetta, E.S., Pypaert, M., Nara, A., Yoshimori, T., Wilm, B., Erdjument-Bromage, H. et al. (2006) CHMP5 is essential for late endosome function and down-regulation of receptor signaling during mouse embryogenesis. J. Cell. Biol., 172, 1045-1056.
17. Hanson, P.I., Roth, R., Lin, Y. and Heuser, J.E. (2008) Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J. Cell. Biol., 180, 389-402.
18. Saksena, S., Wahlman, J., Teis, D., Johnson, A.E. and Emr, S.D. (2009) Functional reconstitution of ESCRT-III assembly and disassembly. Cell, 136, 97-109.
19. Teis, D., Saksena, S. and Emr, S.D. (2008) Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation. Dev. Cell, 15, 578-589.
20. Wollert, T., Wunder, C., Lippincott-Schwartz, J. and Hurley, J.H. (2009) Membrane scission by the ESCRT-III complex. Nature, 458, 172-177.
21. Shim, S., Kimpler, L.A. and Hanson, P.I. (2007) Structure/function analysis of four core ESCRT-III proteins reveals common regulatory role for extreme C-terminal domain. Traffic, 8, 1068-1079.
22. Zamborlini, A., Usami, Y., Radoshitzky, S.R., Popova, E., Palu, G. and Gottlinger, H. (2006) Release of autoinhibition converts ESCRT-III components into potent inhibitors of HIV-1 budding. Proc. Natl Acad. Sci. USA, 103, 19140-19145.
23. Lin, Y., Kimpler, L.A., Naismith, T.V., Lauer, J.M. and Hanson, P.I. (2005) Interaction of the mammalian endosomal sorting complex required for transport (ESCRT) III protein hSnf7-1 with itself, membranes, and the AAA+ ATPase SKD1. J. Biol. Chem., 280, 12799-12809.
24. Whitley, P., Reaves, B.J., Hashimoto, M., Riley, A.M., Potter, B.V. and Holman, G.D. (2003) Identification of mammalian Vps24p as an effector of phosphatidylinositol 3,5-bisphosphate-dependent endosome compartmentalization. J. Biol. Chem., 278, 38786-38795.
25. Obita, T., Saksena, S., Ghazi-Tabatabai, S., Gill, D.J., Perisic, O., Emr, S.D. and Williams, R.L. (2007) Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4. Nature, 449, 735-739.
26. Stuchell-Brereton, M.D., Skalicky, J.J., Kieffer, C., Karren, M.A., Ghaffarian, S. and Sundquist, W.I. (2007) ESCRT-III recognition by VPS4 ATPases. Nature, 449, 740-744.
27. 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.
28. 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.
29. Luzio, J.P., Pryor, P.R. and Bright, N.A. (2007) Lysosomes: fusion and function. Nat. Rev. Mol. Cell. Biol., 8, 622-632.
30. Wu, C., Lai, C.F. and Mobley, W.C. (2001) Nerve growth factor activates persistent Rap1 signaling in endosomes. J. Neurosci., 21, 5406-5416.
31. Ginty, D.D. and Segal, R.A. (2002) Retrograde neurotrophin signaling: Trk-ing along the axon. Curr. Opin. Neurobiol., 12, 268-274.
32. Zhou, P., Porcionatto, M., Pilapil, M., Chen, Y., Choi, Y., Tolias, K.F., Bikoff, J.B., Hong, E.J., Greenberg, M.E. and Segal, R.A. (2007) Polarized signaling endosomes coordinate BDNF-induced chemotaxis of cerebellar precursors. Neuron, 55, 53-68.
33. Hibbert, A.P., Kramer, B.M., Miller, F.D. and Kaplan, D.R. (2006) The localization, trafficking and retrograde transport of BDNF bound to p75NTR in sympathetic neurons. Mol. Cell. Neurosci., 32, 387-402.
34. Kantamneni, S., Holman, D., Wilkinson, K.A., Correa, S.A., Feligioni, M., Ogden, S., Fraser, W., Nishimune, A. and Henley, J.M. (2008) GISP binding to TSG101 increases GABA receptor stability by down-regulating ESCRT-mediated lysosomal degradation. J. Neurochem., 107, 86-95.
35. Kantamneni, S., Holman, D., Wilkinson, K.A., Nishimune, A. and Henley, J.M. (2009) GISP increases neurotransmitter receptor stability by down-regulating ESCRT-mediated lysosomal degradation. Neurosci. Lett., 452, 106-110.
36. Ahmad, S.T., Sweeney, S.T., Lee, J.A., Sweeney, N.T. and Gao, F.B. (2009) Genetic screen identifies serpin5 as a regulator of the toll pathway and CHMP2B toxicity associated with frontotemporal dementia. Proc. Natl Acad. Sci. USA, 106, 12168-12173.
37. Okun, E., Griffioen, K.J., Lathia, J.D., Tang, S.C., Mattson, M.P. and Arumugam, T.V. (2009) Toll-like receptors in neurodegeneration. Brain Res. Rev., 59, 278-292.
38. Gordon, P.B. and Seglen, P.O. (1988) Prelysosomal convergence of autophagic and endocytic pathways. Biochem. Biophys. Res. Commun., 151, 40-47.
39. Klionsky, D.J. and Ohsumi, Y. (1999) Vacuolar import of proteins and organelles from the cytoplasm. Annu. Rev. Cell. Dev. Biol., 15, 1-32.
40. Tooze, J., Hollinshead, M., Ludwig, T., Howell, K., Hoflack, B. and Kern, H. (1990) In exocrine pancreas, the basolateral endocytic pathway converges with the autophagic pathway immediately after the early endosome. J. Cell. Biol., 111, 329-345.
41. Lee, J.A., Beigneux, A., Ahmad, S.T., Young, S.G. and Gao, F.B. (2007) ESCRT-III Dysfunction causes autophagosome accumulation and neurodegeneration. Curr. Biol., 17, 1561-1567.
42. Lee, J.A. and Gao, F.B. (2008) Roles of ESCRT in autophagy-associated neurodegeneration. Autophagy, 4, 230-232.
43. Filimonenko, M., Stuffers, S., Raiborg, C., Yamamoto, A., Malerod, L., Fisher, E.M.C., Isaacs, A., Brech, A., Stenmark, H. and Simonsen, A. (2007) Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J. Cell. Biol., 179, 485-500.
44. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H. et al. (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature, 441, 885-889.
45. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E. et al. (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature, 441, 880-884.
46. Isaacs,A.M.,Powell,C.,Webb,T.E.,Linehan,J.M.,Collinge,J.andBrandner, S. (2008) Lack of TAR-DNA binding protein-43 (TDP-43) pathology in human prion diseases. Neuropathol. Appl. Neurobiol., 34, 446-456.