Huntingtin mediates dendritic transport of β-actin mRNA in rat neurons

Scientific Reports

Volumn 1, Issue , 2011, Pages

  Ma, Bin ^a,b   Savas, Jeffrey N ^a,c   Yu, Man Shan ^a   Culver, Brady P ^a   Chao, Moses V ^a   Tanese, Naoko ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; HAP1 PROTEIN, RAT; HUNTINGTIN PROTEIN, RAT; IMP1 PROTEIN, RAT; KIF5A PROTEIN, RAT; KINESIN; MESSENGER RNA; MOLECULAR MOTOR; NERVE PROTEIN; NUCLEAR PROTEIN; RNA BINDING PROTEIN; SMALL INTERFERING RNA;

ACTIVE TRANSPORT; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BRAIN; CELL CULTURE; CELL GRANULE; DENDRITE; DRUG ANTAGONISM; FEMALE; GENE SILENCING; GENETICS; METABOLISM; MICROTUBULE; NERVE CELL; RAT; SIGNAL TRANSDUCTION; WISTAR RAT;

ACTINS; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; BRAIN; CELLS, CULTURED; CYTOPLASMIC GRANULES; DENDRITES; DYNEINS; FEMALE; GENE KNOCKDOWN TECHNIQUES; KINESIN; MICROTUBULES; MODELS, NEUROLOGICAL; MOLECULAR MOTOR PROTEINS; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; RATS; RATS, WISTAR; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84859770244     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep00140     Document Type: Article

References (51)

1. Borrell-Pages, M., Zala, D., Humbert, S. & Saudou, F. Huntington's disease: from huntingtin function and dysfunction to therapeutic strategies. Cell Mol Life Sci 63, 2642-2660 (2006). (Pubitemid 44800717)
2. Caviston, J. P. & Holzbaur, E. L. Huntingtin as an essential integrator of intracellular vesicular trafficking. Trends Cell Biol 19, 147-155 (2009).
3. Gauthier, L. R. et al. Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 118, 127-138 (2004). (Pubitemid 38902819)
4. Gunawardena, S. et al. Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 40, 25-40 (2003). (Pubitemid 37222462)
5. Bramham, C. R. & Wells, D. G. Dendritic mRNA: transport, translation and function. Nat Rev Neurosci 8, 776-789 (2007). (Pubitemid 47462112)
6. Hirokawa, N. mRNA transport in dendrites: RNA granules, motors, and tracks. J Neurosci 26, 7139-7142 (2006).
7. Martin, K. C. & Zukin, R. S. RNA trafficking and local protein synthesis in dendrites: an overview. J Neurosci 26, 7131-7134 (2006).
8. Kang, H. & Schuman, E. M. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273, 1402-1406 (1996). (Pubitemid 26296531)
9. Huber, K. M., Kayser, M. S. & Bear, M. F. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288, 1254-1257 (2000).
10. Loya, C. M., Van Vactor, D. & Fulga, T. A. Understanding neuronal connectivity through the post-transcriptional toolkit. Genes Dev 24, 625-635 (2010).
11. Doyle, M. & Kiebler, M. A. Mechanisms of dendritic mRNA transport and its role in synaptic tagging. The EMBO journal 30, 3540-3552 (2011).
12. Blichenberg, A. et al. Identification of a cis-acting dendritic targeting element in MAP2 mRNAs. J Neurosci 19, 8818-8829 (1999). (Pubitemid 30226703)
13. Bassell, G. J. et al. Sorting of beta-actin mRNA and protein to neurites and growth cones in culture. J Neurosci 18, 251-265 (1998). (Pubitemid 28046786)
14. Blichenberg, A. et al. Identification of a cis-acting dendritic targeting element in the mRNA encoding the alpha subunit of Ca21/calmodulin-dependent protein kinase II. Eur J Neurosci 13, 1881-1888 (2001). (Pubitemid 32537214)
15. Zhang, H. L. et al. Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron 31, 261-275 (2001). (Pubitemid 32762979)
16. Lyford, G. L. et al. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14, 433-445 (1995).
17. Zeitelhofer, M., Macchi, P. & Dahm, R. Perplexing bodies: The putative roles of P-bodies in neurons. RNA Biol 5, 244-248 (2008).
18. Mikl, M., Vendra, G. & Kiebler, M. A. Independent localization of MAP2, CaMKIIalpha and beta-actin RNAs in low copy numbers. EMBO reports 12, 1077-1084 (2011).
19. Tubing, F. et al. Dendritically localized transcripts are sorted into distinct ribonucleoprotein particles that display fast directional motility along dendrites of hippocampal neurons. J Neurosci 30, 4160-4170 (2010).
20. Zeitelhofer, M. et al. Dynamic interaction between P-bodies and transport ribonucleoprotein particles in dendrites of mature hippocampal neurons. J Neurosci 28, 7555-7562 (2008).
21. Carson, J. H., Cui, H. & Barbarese, E. The balance of power in RNA trafficking. Curr Opin Neurobiol 11, 558-563 (2001). (Pubitemid 32938286)
22. Kanai, Y., Dohmae, N. & Hirokawa, N. Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43, 513-525 (2004). (Pubitemid 39094678)
23. Brendza, R. P., Serbus, L. R., Duffy, J. B. & Saxton, W. M. Afunction for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 289, 2120-2122 (2000).
24. Savas, J. N. et al. Huntington's disease protein contributes to RNA-mediated gene silencing through association with Argonaute and P bodies. Proc Natl Acad Sci USA 105, 10820-10825 (2008).
25. Savas, J. N. et al. Arole for huntington disease protein in dendritic RNAgranules. J Biol Chem 285, 13142-13153 (2010).
26. Kislauskis, E. H., Li, Z., Singer, R. H. & Taneja, K. L. Isoform-specific 39-untranslated sequences sort alpha-cardiac and beta-cytoplasmic actin messenger RNAs to different cytoplasmic compartments. J Cell Biol 123, 165-172 (1993). (Pubitemid 23284872)
27. Rook, M. S., Lu, M. & Kosik, K. S. CaMKIIalpha 39 untranslated region-directed mRNA translocation in living neurons: visualization by GFP linkage. J Neurosci 20, 6385-6393 (2000).
28. Li, X. J. & Li, S. H. HAP1 and intracellular trafficking. Trends Pharmacol Sci 26, 1-3 (2005).
29. Twelvetrees, A. E. et al. Delivery of GABAARs to synapses is mediated by HAP1-KIF5 and disrupted by mutant huntingtin. Neuron 65, 53-65 (2010).
30. Kloc, M., Zearfoss, N. R. & Etkin, L. D. Mechanisms of subcellular mRNA localization. Cell 108, 533-544 (2002). (Pubitemid 34260878)
31. Daigle, N. & Ellenberg, J. LambdaN-GFP: an RNA reporter system for live-cell imaging. Nat Methods 4, 633-636 (2007). (Pubitemid 47202473)
32. Stokin, G. B. & Goldstein, L. S. Axonal transport and Alzheimer's disease. Annu Rev Biochem 75, 607-627 (2006). (Pubitemid 44118045)
33. Gunawardena, S. & Goldstein, L. S. Polyglutamine diseases and transport problems: deadly traffic jams on neuronal highways. Arch Neurol 62, 46-51 (2005). (Pubitemid 40105035)
34. Harjes, P. & Wanker, E. E. The hunt for huntingtin function: interaction partners tell many different stories. Trends Biochem Sci 28, 425-433 (2003). (Pubitemid 36976745)
35. Eom, T., Antar, L. N., Singer, R. H. & Bassell, G. J. Localization of a beta-actin messenger ribonucleoprotein complex with zipcode-binding protein modulates the density of dendritic filopodia and filopodial synapses. J Neurosci 23, 10433-10444 (2003). (Pubitemid 37444620)
36. Epstein, E. et al. Dynein light chain binding to a 39-untranslated sequence mediates parathyroid hormone mRNA association with microtubules. J Clin Invest 105, 505-512 (2000). (Pubitemid 30127251)
37. Vale, R. D. Themolecular motor toolbox for intracellular transport. Cell 112, 467-480 (2003). (Pubitemid 36263080)
38. Colin, E. et al. Huntingtin phosphorylation acts as a molecular switch for anterograde/retrograde transport in neurons. Embo J 27, 2124-2134 (2008).
39. Her, L. S. & Goldstein, L. S. Enhanced sensitivity of striatal neurons to axonal transport defects induced by mutant huntingtin. J Neurosci 28, 13662-13672 (2008).
40. Pineda, J. R. et al. Genetic and pharmacological inhibition of calcineurin corrects the BDNF transport defect in Huntington's disease. Mol Brain 2, 33 (2009).
41. DeBoer, S. R. et al. Conventional kinesin holoenzymes are composed of heavy and light chain homodimers. Biochemistry 47, 4535-4543 (2008).
42. Sasaki, Y. et al. Phosphorylation of zipcode binding protein 1 is required for brainderived neurotrophic factor signaling of local beta-actin synthesis and growth cone turning. J Neurosci 30, 9349-9358 (2010).
43. Metzler, M. et al. Phosphorylation of huntingtin at Ser421 in YAC128 neurons is associated with protection of YAC128 neurons from NMDA-mediated excitotoxicity and is modulated by PP1 and PP2A. J Neurosci 30, 14318-14329 (2010).
44. Jeong, H. et al. Acetylation targets mutant huntingtin to autophagosomes for degradation. Cell 137, 60-72 (2009).
45. Prigge, J. R. & Schmidt, E. E. HAP1 can sequester a subset of TBP in cytoplasmic inclusions via specific interaction with the conserved TBP(CORE).BMC Mol Biol 8, 76 (2007).
46. King, S. J., Brown, C. L., Maier, K. C., Quintyne, N. J. & Schroer, T. A. Analysis of the dynein-dynactin interaction in vitro and in vivo. Mol Biol Cell 14, 5089-5097 (2003). (Pubitemid 37484822)
47. Bannai, H. et al. An RNA-interacting protein, SYNCRIP (heterogeneous nuclear ribonuclear protein Q1/NSAP1) is a component of mRNA granule transported with inositol 1, 4, 5-trisphosphate receptor type 1 mRNA in neuronal dendrites. J Biol Chem 279, 53427-53434 (2004). (Pubitemid 40051847)
48. Darzacq, X. et al. Stepwise RNP assembly at the site of H/ACA RNA transcription in human cells. J Cell Biol 173, 207-218 (2006).
49. Wilson, A. C., Freiman, R. N., Goto, H., Nishimoto, T. & Herr, W. VP16 targets an amino-terminal domain of HCF involved in cell cycle progression. Mol Cell Biol 17, 6139-6146 (1997). (Pubitemid 27411123)
50. Ma, B. et al. Localization of BDNF mRNA with the Huntington's disease protein in rat brain. Mol Neurodegener 5, 22 (2010).
51. Osten, P. et al. The AMPA receptor GluR2 C terminus can mediate a reversible, ATP-dependent interaction with NSF and alpha-and beta-SNAPs. Neuron 21, 99-110 (1998). (Pubitemid 28355695)