Prion protein impairs kinesin-driven transport

Biochemical and Biophysical Research Communications

Volumn 425, Issue 4, 2012, Pages 788-793

  Nieznanska, Hanna ^a   Dudek, Elzbieta ^a,b   Zajkowski, Tomasz ^a   Szczesna, Ewa ^a   Kasprzak, Andrzej A ^a   Nieznanski, Krzysztof ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Division spindle; Kinesin; Microtubule; Prion disease; Prion protein

Indexed keywords

KINESIN; MOLECULAR MOTOR; PRION PROTEIN; TUBULIN;

ARTICLE; CELL STRUCTURE; CYTOTOXICITY; MICROTUBULE; MITOSIS SPINDLE; NONHUMAN; OLIGOMERIZATION; PRION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN TRANSPORT;

ANIMALS; CELL DIVISION; KINESIN; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PC12 CELLS; PRIONS; PROTEIN TRANSPORT; RATS; TUBULIN;

EID: 84865974206     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.07.153     Document Type: Article

References (47)

1. Prusiner S.B. Prions. Proc. Natl. Acad. Sci. USA 1998, 95:13363-13383.
2. Novitskaya V., Makarava N., Sylvester I., Bronstein I.B., Baskakov I.V. Amyloid fibrils of mammalian prion protein induce axonal degeneration in NTERA2-derived terminally differentiated neurons. J. Neurochem. 2007, 102:398-407.
3. Ermolayev V., Friedrich M., Nozadze R., Cathomen T., Klein M.A., Harms G.S., Flechsig E. Ultramicroscopy reveals axonal transport impairments in cortical motor neurons at prion disease. Biophys. J. 2009, 96:3390-3398.
4. Goldstein L.S. Do disorders of movement cause movement disorders and dementia?. Neuron 2003, 40:415-425.
5. Gunawardena S., Goldstein L.S. Polyglutamine diseases and transport problems: deadly traffic jams on neuronal highways. Arch. Neurol. 2005, 62:46-51.
6. Stokin G.B., Goldstein L.S. Axonal transport and Alzheimer's disease. Annu. Rev. Biochem. 2006, 75:607-627.
7. Roy S., Zhang B., Lee V.M., Trojanowski J.Q. Axonal transport defects: a common theme in neurodegenerative diseases. Acta Neuropathol. 2005, 109:5-13.
8. Dixit R., Ross J.L., Goldman Y.E., Holzbaur E.L. Differential regulation of dynein and kinesin motor proteins by tau. Science 2008, 319:1086-1089.
9. Nieznanski K., Nieznanska H., Skowronek K.J., Osiecka K.M., Stepkowski D. Direct interaction between prion protein and tubulin. Biochem. Biophys. Res. Commun. 2005, 334:403-411.
10. Nieznanski K., Podlubnaya Z.A., Nieznanska H. Prion protein inhibits microtubule assembly by inducing tubulin oligomerization. Biochem. Biophys. Res. Commun. 2006, 349:391-399.
11. Osiecka K.M., Nieznanska H., Skowronek K.J., Karolczak J., Schneider G., Nieznanski K. Prion protein region 23-32 interacts with tubulin and inhibits microtubule assembly. Proteins 2009, 77:279-296.
12. Nieznanski K. Interactions of prion protein with intracellular proteins: so many partners and no consequences?. Cell. Mol. Neurobiol. 2010, 30:653-666.
13. Keshet G.I., Bar-Peled O., Yaffe D., Nudel U., Gabizon R. The cellular prion protein colocalizes with the dystroglycan complex in the brain. J. Neurochem. 2000, 75:1889-1897.
14. 2-terminal cellular prion protein fragment. Biochem. Biophys. Res. Commun. 2004, 313:818-823.
15. Hachiya N.S., Watanabe K., Yamada M., Sakasegawa Y., Kaneko K. Anterograde and retrograde intracellular trafficking of fluorescent cellular prion protein. Biochem. Biophys. Res. Commun. 2004, 315:802-807.
16. Li X.L., Wang G.R., Jing Y.Y., Pan M.M., Dong C.F., Zhou R.M., Wang Z.Y., Shi Q., Gao C., Dong X.P. Cytosolic PrP induces apoptosis of cell by disrupting microtubule assembly. J. Mol. Neurosci. 2011, 43:316-325.
17. Dong C.F., Shi S., Wang X.F., An R., Li P., Chen J.M., Wang X., Wang G.R., Shan B., Zhang B.Y., Han J., Dong X.P. The N-terminus of PrP is responsible for interacting with tubulin and fCJD related PrP mutants possess stronger inhibitive effect on microtubule assembly in vitro. Arch. Biochem. Biophys. 2008, 470:83-92.
18. Gray E.G. Spongiform encephalopathy: a neurocytologist's viewpoint with a note on Alzheimer's disease. Neuropathol. Appl. Neurobiol. 1986, 12:149-172.
19. Morillas M., Swietnicki W., Gambetti P., Surewicz W.K. Membrane environment alters the conformational structure of the recombinant human prion protein. J. Biol. Chem. 1999, 274:36859-36865.
20. Zahn R., von Schroetter C., Wuthrich K. Human prion proteins expressed in Escherichia coli and purified by high-affinity column refolding. FEBS Lett. 1997, 417:400-404.
21. Kocik E., Skowronek K.J., Kasprzak A.A. Interactions between subunits in heterodimeric Ncd molecules. J. Biol. Chem. 2009, 284:35735-35745.
22. Mandelkow E.M., Herrmann M., Ruhl U. Tubulin domains probed by limited proteolysis and subunit-specific antibodies. J. Mol. Biol. 1985, 185:311-327.
23. Castoldi M., Popov A.V. Purification of brain tubulin through two cycles of polymerization-depolymerization in a high-molarity buffer. Protein Expr. Purif. 2003, 32:83-88.
24. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
25. Osiecka K.M., Nieznanska H., Skowronek K.J., Jozwiak J., Nieznanski K. Tau inhibits tubulin oligomerization induced by prion protein. Biochim. Biophys. Acta 1813, 2011:1845-1853.
26. Fellous A., Francon J., Lennon A.M., Nunez J. Microtubule assembly in vitro. Purification of assembly-promoting factors. Eur. J. Biochem. 1977, 78:167-174.
27. Lindwall G., Cole R.D. The purification of tau protein and the occurrence of two phosphorylation states of tau in brain. J. Biol. Chem. 1984, 259:12241-12245.
28. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
29. Lundberg P., Magzoub M., Lindberg M., Hällbrink M., Jarvet J., Eriksson L.E., Langel U., Gräslund A. Cell membrane translocation of the N-terminal (1-28) part of the prion protein. Biochem. Biophys. Res. Commun. 2002, 299:85-90.
30. McVicker D.P., Chrin L.R., Berger C.L. The nucleotide-binding state of microtubules modulates kinesin processivity and the ability of Tau to inhibit kinesin-mediated transport. J. Biol. Chem. 2011, 286:42873-42880.
31. Hegde R.S., Mastrianni J.A., Scott M.R., DeFea K.A., Tremblay P., Torchia M., DeArmond S.J., Prusiner S.B., Lingappa V.R. A transmembrane form of the prion protein in neurodegenerative disease. Science 1998, 279:827-834.
32. Ma J., Wollmann R., Lindquist S. Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science 2002, 298:1781-1785.
33. Grenier C., Bissonnette C., Volkov L., Roucou X. Molecular morphology and toxicity of cytoplasmic prion protein aggregates in neuronal and non-neuronal cells. J. Neurochem. 2006, 97:1456-1466.
34. Stahl N., Borchelt D.R., Prusiner S.B. Differential release of cellular and scrapie prion proteins from cellular membranes by phosphatidylinositol-specific phospholipase C. Biochemistry 1990, 29:5405-5412.
35. Mironov A., Latawiec D., Wille H., Bouzamondo-Bernstein E., Legname G., Williamson R.A., Burton D., DeArmond S.J., Prusiner S.B., Peters P.J. Cytosolic prion protein in neurons. J. Neurosci. 2003, 23:7183-7193.
36. Yost C.S., Lopez C.D., Prusiner S.B., Myers R.M., Lingappa V.R. Non-hydrophobic extracytoplasmic determinant of stop transfer in the prion protein. Nature 1990, 343:669-672.
37. Kim S.J., Rahbar R., Hegde R.S. Combinatorial control of prion protein biogenesis by the signal sequence and transmembrane domain. J. Biol. Chem. 2001, 276:26132-26140.
38. Chakrabarti O., Ashok A., Hegde R.S. Prion protein biosynthesis and its emerging role in neurodegeneration. Trends Biochem. Sci. 2009, 34:287-295.
39. Zanusso G., Petersen R.B., Jin T., Jing Y., Kanoush R., Ferrari S., Gambetti P., Singh N. Proteasomal degradation and N-terminal protease resistance of the codon 145 mutant prion protein. J. Biol. Chem. 1999, 274:23396-23404.
40. Heske J., Heller U., Winklhofer K.F., Tatzelt J. The C-terminal globular domain of the prion protein is necessary and sufficient for import into the endoplasmic reticulum. J. Biol. Chem. 2004, 279:5435-5443.
41. Ma J., Lindquist S. Wild-type PrP and a mutant associated with prion disease are subject to retrograde transport and proteasome degradation. Proc. Natl. Acad. Sci. USA 2001, 98:14955-14960.
42. Kristiansen M., Deriziotis P., Dimcheff D.E., Jackson G.S., Ovaa H., Naumann H., Clarke A.R., van Leeuwen F.W., Menéndez-Benito V., Dantuma N.P., Portis J.L., Collinge J., Tabrizi S.J. Disease-associated prion protein oligomers inhibit the 26S proteasome. Mol. Cell 2007, 26:175-188.
43. Miesbauer M., Rambold A.S., Winklhofer K.F., Tatzelt J. Targeting of the prion protein to the cytosol: mechanisms and consequences. Curr. Issues Mol. Biol. 2009, 12:109-118.
44. Rambold A.S., Miesbauer M., Rapaport D., Bartke T., Baier M., Winklhofer K.F., Tatzelt J. Association of Bcl-2 with misfolded prion protein is linked to the toxic potential of cytosolic PrP. Mol. Biol. Cell 2006, 17:3356-3368.
45. Chakrabarti O., Hegde R.S. Functional depletion of mahogunin by cytosolically exposed prion protein contributes to neurodegeneration. Cell 2009, 137:1136-1147.
46. Morel E., Fouquet S., Strup-Perrot C., Thievend C.P., Petit C., Loew D., Faussat A.M., Yvernault L., Pincon-Raymond M., Chambaz J., Rousset M., Thenet S., Clair C. The cellular prion protein PrP is involved in the proliferation of epithelial cells and in the distribution of junction-associated proteins. PLoS ONE 2008, 3:e3000.
47. Leuba G., Saini K., Savioz A., Charnay Y. Early-onset familial Alzheimer disease with coexisting beta-amyloid and prion pathology. JAMA 2000, 283:1689-1691.