Huntingtin is required for ER-to-Golgi transport and for secretory vesicle fusion at the plasma membrane

DMM Disease Models and Mechanisms

Volumn 7, Issue 12, 2014, Pages 1335-1340

  Brandstaetter, Hemma ^a   Kruppa, Antonina J ^a   Buss, Folma ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

ER; Exocytosis; Golgi; Huntingtin; Vesicle fusion

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; HUMAN GROWTH HORMONE; HUNTINGTIN; GREEN FLUORESCENT PROTEIN; HTT PROTEIN, HUMAN; HUNTINGTON PROTEIN, MOUSE; NERVE PROTEIN; NUCLEAR PROTEIN; PROTEIN BINDING; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ARTICLE; CELL FUSION; CELL MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EXOCYTOSIS; FIBROBLAST; GENE SILENCING; GOLGI COMPLEX; HELA CELL LINE; HOMOZYGOTE; HUMAN; HUNTINGTON CHOREA; IMMUNOBLOTTING; MICROSCOPY; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SECRETORY PATHWAY; SECRETORY VESICLE; TRANS GOLGI NETWORK; ANIMAL; DISEASE MODEL; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

MUS;

ANIMALS; CELL MEMBRANE; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM; FIBROBLASTS; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HOMOZYGOTE; HUMANS; HUNTINGTON DISEASE; MICE; MICROSCOPY, FLUORESCENCE; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; SECRETORY VESICLES; TRANS-GOLGI NETWORK;

EID: 84919619341     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.017368     Document Type: Article

References (37)

1. Arribat, Y., Bonneaud, N., Talmat-Amar, Y., Layalle, S., Parmentier, M. L. and Maschat, F. (2013). A huntingtin peptide inhibits polyQ-huntingtin associated defects. PLoS ONE 8, e68775.
2. Bond, L. M., Peden, A. A., Kendrick-Jones, J., Sellers, J. R. and Buss, F. (2011). Myosin VI and its binding partner optineurin are involved in secretory vesicle fusion at the plasma membrane. Mol. Biol. Cell 22, 54-65.
3. Borrell-Pagès, M., Zala, D., Humbert, S. and Saudou, F. (2006). Huntington's disease: from huntingtin function and dysfunction to therapeutic strategies. Cell. Mol. Life Sci. 63, 2642-2660.
4. Caviston, J. P. and Holzbaur, E. L. (2009). Huntingtin as an essential integrator of intracellular vesicular trafficking. Trends Cell Biol. 19, 147-155.
5. Caviston, J. P., Ross, J. L., Antony, S. M., Tokito, M. and Holzbaur, E. L. (2007). Huntingtin facilitates dynein/dynactin-mediated vesicle transport. Proc. Natl. Acad. Sci. USA 104, 10045-10050.
6. Di Figlia, M., Sapp, E., Chase, K. O., Davies, S. W., Bates, G. P., Vonsattel, J. P. and Aronin, N. (1997). Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277, 1990-1993.
7. Duyao, M. P., Auerbach, A. B., Ryan, A., Persichetti, F., Barnes, G. T., McNeil, S. M., Ge, P., Vonsattel, J. P., Gusella, J. F., Joyner, A. L. et al. (1995). Inactivation of the mouse Huntington's disease gene homolog Hdh. Science 269, 407-410.
8. Engelender, S., Sharp, A. H., Colomer, V., Tokito, M. K., Lanahan, A., Worley, P., Holzbaur, E. L. and Ross, C. A. (1997). Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued subunit of dynactin. Hum. Mol. Genet. 6, 2205-2212.
9. Gauthier, L. R., Charrin, B. C., Borrell-Pagès, M., Dompierre, J. P., Rangone, H., Cordelières, F. P., De Mey, J., MacDonald, M. E., Lessmann, V., Humbert, S. et al. (2004). Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 118, 127-138.
10. Gordon, D. E., Bond, L. M., Sahlender, D. A. and Peden, A. A. (2010). A targeted siRNA screen to identify SNAREs required for constitutive secretion in mammalian cells. Traffic 11, 1191-1204.
11. Gupta, V., Palmer, K. J., Spence, P., Hudson, A. and Stephens, D. J. (2008). Kinesin-1 (uKHC/KIF5B) is required for bidirectional motility of ER exit sites and efficient ER-to-Golgi transport. Traffic 9, 1850-1866.
12. Harjes, P. and Wanker, E. E. (2003). The hunt for huntingtin function: interaction partners tell many different stories. Trends Biochem. Sci. 28, 425-433.
13. Hattula, K. and Peränen, J. (2000). FIP-2, a coiled-coil protein, links Huntingtin to Rab8 and modulates cellular morphogenesis. Curr. Biol. 10, 1603-1606.
14. Imarisio, S., Carmichael, J., Korolchuk, V., Chen, C. W., Saiki, S., Rose, C., Krishna, G., Davies, J. E., Ttofi, E., Underwood, B. R. et al. (2008). Huntington's disease: from pathology and genetics to potential therapies. Biochem. J. 412, 191-209.
15. Kreitzer, G., Marmorstein, A., Okamoto, P., Vallee, R. and Rodriguez-Boulan, E. (2000). Kinesin and dynamin are required for post-Golgi transport of a plasmamembrane protein. Nat. Cell Biol. 2, 125-127.
16. Lee, M. C. S., Miller, E. A., Goldberg, J., Orci, L. and Schekman, R. (2004). Bidirectional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20, 87-123.
17. Li, S. H. and Li, X. J. (2004). Huntingtin-protein interactions and the pathogenesis of Huntington's disease. Trends Genet. 20, 146-154.
18. Li, X. J. and Li, S. H. (2005). HAP1 and intracellular trafficking. Trends Pharmacol. Sci. 26, 1-3.
19. Li, X. J., Li, S. H., Sharp, A. H., Nucifora, F. C., Jr, Schilling, G., Lanahan, A., Worley, P., Snyder, S. H. and Ross, C. A. (1995). A huntingtin-associated protein enriched in brain with implications for pathology. Nature 378, 398-402.
20. Lippincott-Schwartz, J., Cole, N. B., Marotta, A., Conrad, P. A. and Bloom, G. S. (1995). Kinesin is the motor for microtubule-mediated Golgi-to-ER membrane traffic. J. Cell Biol. 128, 293-306.
21. Nasir, J., Floresco, S. B., O'Kusky, J. R., Diewert, V. M., Richman, J. M., Zeisler, J., Borowski, A., Marth, J. D., Phillips, A. G. and Hayden, M. R. (1995). Targeted disruption of the Huntington's disease gene results in embryonic lethality and behavioral and morphological changes in heterozygotes. Cell 81, 811-823.
22. Palmer, K. J., Hughes, H. and Stephens, D. J. (2009). Specificity of cytoplasmic dynein subunits in discrete membrane-trafficking steps. Mol. Biol. Cell 20, 2885-2899.
23. Pineda, J. R., Pardo, R., Zala, D., Yu, H., Humbert, S. and Saudou, F. (2009). Genetic and pharmacological inhibition of calcineurin corrects the BDNF transport defect in Huntington's disease. Mol. Brain 2, 33.
24. Presley, J. F., Cole, N. B., Schroer, T. A., Hirschberg, K., Zaal, K. J. and Lippincott-Schwartz, J. (1997). ER-to-Golgi transport visualized in living cells. Nature 389, 81-85.
25. Roghi, C. and Allan, V. J. (1999). Dynamic association of cytoplasmic dynein heavy chain 1a with the Golgi apparatus and intermediate compartment. J. Cell Sci. 112, 4673-4685.
26. Sahlender, D. A., Roberts, R. C., Arden, S. D., Spudich, G., Taylor, M. J., Luzio, J. P., Kendrick-Jones, J. and Buss, F. (2005). Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J. Cell Biol. 169, 285-295.
27. Saleh, A. A., Bhadra, A. K. and Roy, I. (2014). Cytotoxicity of mutant huntingtin fragment in yeast can be modulated by the expression level of wild type huntingtin fragment. ACS Chem. Neurosci. 5, 205-215.
28. Sathasivam, K., Amaechi, I., Mangiarini, L. and Bates, G. (1997). Identification of an HD patient with a (CAG)180 repeat expansion and the propagation of highly expanded CAG repeats in lambda phage. Hum. Genet. 99, 692-695.
29. Schulte, J. and Littleton, J. T. (2011). The biological function of the Huntingtin protein and its relevance to Huntington's Disease pathology. Curr Trends Neurol. 5, 65-78.
30. Shirasaki, D. I., Greiner, E. R., Al-Ramahi, I., Gray, M., Boontheung, P., Geschwind, D. H., Botas, J., Coppola, G., Horvath, S., Loo, J. A. et al. (2012). Network organization of the huntingtin proteomic interactome in mammalian brain. Neuron 75, 41-57.
31. Snell, R. G., MacMillan, J. C., Cheadle, J. P., Fenton, I., Lazarou, L. P., Davies, P., MacDonald, M. E., Gusella, J. F., Harper, P. S. and Shaw, D. J. (1993). Relationship between trinucleotide repeat expansion and phenotypic variation in Huntington's disease. Nat. Genet. 4, 393-397.
32. Squitieri, F., Cannella, M. and Simonelli, M. (2002). CAG mutation effect on rate of progression in Huntington's disease. Neurol. Sci. 23 Suppl. 2, S107-S108.
33. Stanek, L. M., Sardi, S. P., Mastis, B. M., Richards, A. R., Treleaven, C. M., Taksir, T. V., Misra, K., Cheng, S. H. and Shihabuddin, L. S. (2014). Silencing mutant huntingtin by AAV-mediated RNAi ameliorates disease manifestations in the YAC128 mouse model of Huntington's disease. Hum. Gene Ther. 25, 461-474.
34. Stauber, T., Simpson, J. C., Pepperkok, R. and Vernos, I. (2006). A role for kinesin-2 in COPI-dependent recycling between the ER and the Golgi complex. Curr. Biol. 16, 2245-2251.
35. Wang, L., Lin, F., Wang, J., Wu, J., Han, R., Zhu, L., Difiglia, M. and Qin, Z. (2012). Expression of mutant N-terminal huntingtin fragment (htt552-100Q) in astrocytes suppresses the secretion of BDNF. Brain Res. 1449, 69-82.
36. Zala, D., Colin, E., Rangone, H., Liot, G., Humbert, S. and Saudou, F. (2008). Phosphorylation of mutant huntingtin at S421 restores anterograde and retrograde transport in neurons. Hum. Mol. Genet. 17, 3837-3846.
37. Zeitlin, S., Liu, J. P., Chapman, D. L., Papaioannou, V. E. and Efstratiadis, A. (1995). Increased apoptosis and early embryonic lethality in mice nullizygous for the Huntington's disease gene homologue. Nat. Genet. 11, 155-163.