Prion protein region 23-32 interacts with tubulin and inhibits microtubule assembly

Proteins: Structure, Function and Bioinformatics

Volumn 77, Issue 2, 2009, Pages 279-296

  Osiecka, Katarzyna M ^a,b   Nieznanska, Hanna ^a   Skowronek, Krzysztof J ^a   Karolczak, Justyna ^a,c   Schneider, Gabriela ^a   Nieznanski, Krzysztof ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b POSTGRADUATE SCHOOL OF MOLECULAR MEDICINE   (Poland)

^c WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

Author keywords

Crosslinking; Electron microscopy; Microtubule; Oligomerization; Prion protein; Protein protein interactions; Tubulin

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN; COPPER ION; PRION PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; HUMAN; HUMAN CELL; MICROTUBULE ASSEMBLY; OLIGOMERIZATION; PRION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BINDING SITES; CELL LINE; CYTOSKELETON; EPITHELIAL CELLS; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULES; MOLECULAR SEQUENCE DATA; OLIGOPEPTIDES; PRIONS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION; TUBULIN;

EID: 70349448466     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22435     Document Type: Article

References (77)

1. Prusiner SB. Prions. Proc Natl Acad Sci USA 1998;95:13363-13383.
2. Bendheim PE, Brown HR, Rudelli RD, Scala LJ, Goller NL, Wen GY, Kascsak RJ, Cashman NR, Bolton DC. Nearly ubiquitous tissue distribution of the scrapie agent precursor protein. Neurology 1992;42:149-156.
3. Turk E, Teplow DB, Hood LE, Prusiner SB. Purification and properties of the cellular and scrapie hamster prion protein. Eur J Biochem 1988;176:21-30. (Pubitemid 18213510)
4. Kim SJ, Rahbar R, Hegde RS. Combinatorial control of prion protein biogenesis by the signal sequence and transmembrane domain. J Biol Chem 2001;276:26132-26140. (Pubitemid 37412825)
5. Stewart RS, Drisaldi B, Harris DA. A transmembrane form of the prion protein contains an uncleaved signal peptide and is retained in the endoplasmic reticulum. Mol Biol Cell 2001;12:881-889. (Pubitemid 33051985)
6. Stahl N, Borchelt DR, Hsiao K, Prusiner SB. Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 1987;51:229-240.
7. Haraguchi T, Fisher S, Olofsson S, Endo T, Groth D, Tarentino A, Borchelt DR, Teplow D, Hood L, Burlingame A, Lycke E, Kobata A, Prusiner SB. Asparagine-linked glycosylation of the scrapie and cellular prion proteins. Arch Biochem Biophys 1989;274:1-13.
8. Chen SG, Teplow DB, Parchi P, Teller JK, Gambetti P, Autilio-Gambetti L. Truncated forms of the human prion protein in normal brain and in prion diseases. J Biol Chem 1995;270:19173-19180.
9. Jimenez-Huete A, Lievens PM, Vidal R, Piccardo P, Ghetti B, Tagliavini F, Frangione B, Prelli F. Endogenous proteolytic cleavage of normal and disease-associated isoforms of the human prion protein in neural and non-neural tissues. Am J Pathol 1998;153:1561-1572. (Pubitemid 28509913)
10. Stahl N, Borchelt DR, Prusiner SB. Differential release of cellular and scrapie prion proteins from cellular membranes by phosphatidylinositol-specific phospholipase C. Biochemistry 1990;29:5405-5412. (Pubitemid 20193950)
11. Hegde RS, Mastrianni JA, Scott MR, DeFea KA, Tremblay P, Torchia M, DeArmond SJ, Prusiner SB, Lingappa VR. A transmembrane form of the prion protein in neurodegenerative disease. Science 1998;279:827-834. (Pubitemid 28106269)
12. Holscher C, Bach UC, Dobberstein B. Prion protein contains a second endoplasmic reticulum targeting signal sequence located at its C terminus. J Biol Chem 2001;276:13388-13394. (Pubitemid 37385272)
13. Mironov A, Jr, Latawiec D, Wille H, Bouzamondo-Bernstein E, Legname G, Williamson RA, Burton D, DeArmond SJ, Prusiner SB, Peters PJ. Cytosolic prion protein in neurons. J Neurosci 2003;23:7183-7193.
14. Hegde RS, Tremblay P, Groth D, DeArmond SJ, Prusiner SB, Lingappa VR. Transmissible and genetic prion diseases share a common pathway of neurodegeneration. Nature 1999;402:822-826. (Pubitemid 30012530)
15. Kim SJ, Hegde RS. Cotranslational partitioning of nascent prion protein into multiple populations at the translocation channel. Mol Biol Cell 2002;13:3775-3786.
16. 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. (Pubitemid 43725584)
17. Hornshaw MP, McDermott JR, Candy JM. Copper binding to the N-terminal tandem repeat regions of mammalian and avian prion protein. Biochem Biophys Res Commun 1995;207:621-629.
18. Brown DR, Qin K, Herms JW, Madlung A, Manson J, Strome R, Fraser PE, Kruck T, von Bohlen A, Schulz-Schaeffer W, Giese A, Westaway D, Kretzschmar H. The cellular prion protein binds copper in vivo. Nature 1997;390:684-687. (Pubitemid 28016355)
19. Büeler H, Fischer M, Lang Y, Fluethmann H, Lipp H-P, De Armond SJ, Prusiner SB, Aguet M, Weissmann C. Normal development and behavior of mice lacking the neuronal cell-surface Pr P protein. Nature 1992;356:577-582.
20. Manson JC, Clarke AR, Hooper ML, Aitchison L, McConnell I, Hope J. 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol Neurobiol 1994;8:121-127.
21. Keshet GI, 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. (Pubitemid 30783494)
22. Han J, Zhang J, Yao H, Wang X, Li F, Chen L, Gao C, Gao J, Nie K, Zhou W, Dong X. Study on interaction between microtubule associated protein tau and prion protein. Sci China C Life Sci 2006;49:473-479. (Pubitemid 44562896)
23. Vana K, Zuber C, Nikles D, Weiss S. Novel aspects of prions, their receptor molecules, and innovative approaches for TSE therapy. Cell Mol Neurobiol 2007;27:107-128. (Pubitemid 46169898)
24. Hachiya NS, Watanabe K, Sakasegawa Y, Kaneko K. Microtubules-associated intracellular localization of the NH2-terminal cellular prion protein fragment. Biochem Biophys Res Commun 2004;313:818-823. (Pubitemid 38021904)
25. Brown DR, Schmidt B, Kretzschmar HA. Prion protein fragment interacts with PrP-deficient cells. J Neurosci Res 1998;52:260-267. (Pubitemid 28196643)
26. Nieznanski K, Nieznanska H, Skowronek KJ, Osiecka KM, Stepkowski D. Direct interaction between prion protein and tubulin. Biochem Biophys Res Commun 2005;334:403-411. (Pubitemid 40982382)
27. Hachiya NS, 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. (Pubitemid 38249374)
28. Nieznanski K, Podlubnaya ZA, Nieznanska H. Prion protein inhibits microtubule assembly by inducing tubulin oligomerization. Biochem Biophys Res Commun 2006;349:391-399. (Pubitemid 44331804)
29. Nogales E. Structural insights into microtubule function. Annu Rev Biochem 2000;69:277-302.
30. Amos LA, Schlieper D. Microtubules and maps. Adv Protein Chem 2005;71:257-298.
31. Arnal I, Heichette C, Diamantopoulos GS, Chrétien D. CLIP-170/tubulin-curved oligomers coassemble at microtubule ends and promote rescues. Curr Biol 2004;14:2086-2095. (Pubitemid 39623189)
32. Schneider G, Nieznanski K, Kilanczyk E, Bieganowski P, Kuznicki J, Filipek A. CacyBP/SIP interacts with tubulin in neuroblastoma NB2a cells and induces formation of globular tubulin assemblies. Biochim Biophys Acta 2007;1773:1628-1636. (Pubitemid 350018916)
33. Jourdain L, Curmi P, Sobel A, Pantaloni D, Carlier MF. Stathmin: a tubulin-sequestering protein which forms a ternary T2S complex with two tubulin molecules. Biochemistry 1997;36:10817-10821. (Pubitemid 27396235)
34. Maccioni RB, Rivas CI, Vera JC. Differential interaction of synthetic peptides from the carboxyl-terminal regulatory domain of tubulin with microtubule-associated proteins. EMBO J 1988;7:1957-1963.
35. Al-Bassam J, Ozer RS, Safer D, Halpain S, Milligan RA. MAP2 and tau bind longitudinally along the outer ridges of microtubule protofilaments. J Cell Biol 2002;157:1187-1196. (Pubitemid 34847789)
36. Cross D, Dominguez J, Maccioni RB, Avila J. MAP-1 and MAP-2 binding sites at the C-terminus of beta-tubulin. Studies with synthetic tubulin peptides. Biochemistry 1991;30:4362-4366.
37. Melki R, Kerjan P, Waller JP, Carlier MF, Pantaloni D. Interaction of microtubule-associated proteins with microtubules: yeast lysyl- and valyl-tRNA synthetases and tau 218-235 synthetic peptide as model systems. Biochemistry 1991;30:11536-11545.
38. Taylor DR, Watt NT, Perera WS, Hooper NM. Assigning functions to distinct regions of the N-terminus of the prion protein that are involved in its copper-stimulated, clathrin-dependent endocytosis. J Cell Sci 2005;118:5141-5153.
39. Solforosi L, Bellon A, Schaller M, Cruite JT, Abalos GC, Williamson RA. Toward molecular dissection of PrPC-PrPSc interactions. J Biol Chem 2007;282:7465-7471.
40. Lau AL, Yam AY, Michelitsch MM, Wang X, Gao C, Goodson RJ, Shimizu R, Timoteo G, Hall J, Medina-Selby A, Coit D, McCoin C, Phelps B, Wu P, Hu C, Chien D, Peretz D. Characterization of prion protein (PrP)-derived peptides that discriminate full-length PrPSc from PrPC. Proc Natl Acad Sci USA 2007;104:11551-11556. (Pubitemid 47175050)
41. Löfgren K, Wahlström A, Lundberg P, Langel U, Gräslund A, Bedecs K. Antiprion properties of prion protein-derived cell-penetrating peptides. FASEB J 2008;22:2177-2184. (Pubitemid 351948637)
42. Morillas M, Swietnicki W, Gambetti P, Surewicz WK. Membrane environment alters the conformational structure of the recombinant human prion protein. J Biol Chem 1999;274:36859-36865. (Pubitemid 30016751)
43. 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. (Pubitemid 27511631)
44. Bradford MM. 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.
45. Mandelkow EM, Herrmann M, Ruhl U. Tubulin domains probed by limited proteolysis and subunit-specific antibodies. J Mol Biol 1985;185:311-327. (Pubitemid 16250033)
46. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. Protein identification and analysis tools on the ExPASy server. In: Walker JM, editor. The proteomics protocols handbook. Totowa: Humana Press; 2005. pp 571-607.
47. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-685.
48. Carraway KL, Koshland DE, Jr. Carbodiimide modification of proteins. Methods Enzymol 1972;25B:616-623.
49. Rezaei H, Marc D, Choiset Y, Takahashi M, Hui Bon Hoa G, Haertlé T, Grosclaude J, Debey P. High yield purification and physicochemical properties of full-length recombinant allelic variants of sheep prion protein linked to scrapie susceptibility. Eur J Biochem 2000;267:2833-2839. (Pubitemid 30321328)
50. Lundberg P, Magzoub M, Lindberg M, Hällbrink M, Jarvet J, Eriksson LE, 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.
51. Redeker V, Melki R, Promé D, Le Caer JP, Rossier J. Structure of tubulin C-terminal domain obtained by subtilisin treatment. The major alpha and beta tubulin isotypes from pig brain are glutamylated. FEBS Lett 1992;313:185-192.
52. Sackett DL, Bhattacharyya B, Wolff J. Tubulin subunit carboxyl termini determine polymerization efficiency. J Biol Chem 1985;260:43-45. (Pubitemid 15165276)
53. Serrano L, Wandosell F, de la Torre J, Avila J. Effect of specific proteolytic cleavages on tubulin polymer formation. Biochem J 1988;252:683-691. (Pubitemid 18153507)
54. Kirchner K, Mandelkow EM. Tubulin domains responsible for assembly of dimers and protofilaments. EMBO J 1985;4:2397-2402.
55. Dong CF, Shi S, Wang XF, An R, Li P, Chen JM, Wang X, Wang GR, Shan B, Zhang BY, Han J, Dong XP. 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.
56. Wolff J. Promotion of microtubule assembly by oligocations: cooperativity between charged groups. Biochemistry 1998;37:10722-10729. (Pubitemid 28357873)
57. Miura T, Hori IA, Takeuchi H. Metal-dependent alpha-helix formation promoted by the glycine-rich octapeptide region of prion protein. FEBS Lett 1996;396:248-252. (Pubitemid 26377833)
58. Brown DR. Altered toxicity of the prion protein peptide PrP106-126 carrying the Ala(117)->Val mutation. Biochem J 2000;346: 785-791.
59. Epple G, Langfeld K, Baier M, Holzhütter HG, Schleuning WD, Köttgen E, Gessner R, Praus M. Both lysine-clusters of the NH2-terminal prion-protein fragment PrP23-110 are essential for t-PA mediated plasminogen activation. Thromb Haemost 2004;91:465-472. (Pubitemid 38396868)
60. Li A, Harris DA. Mammalian prion protein suppresses Bax-induced cell death in yeast. J Biol Chem 2005;280:17430-17434. (Pubitemid 41389214)
61. Lysek DA, Wüthrich K. Prion protein interaction with the C-terminal SH3 domain of Grb2 studied using NMR and optical spectroscopy. Biochemistry 2004;43:10393-10399. (Pubitemid 39079313)
62. Gu Y, Hinnerwisch J, Fredricks R, Kalepu S, Mishra RS, Singh N. Identification of cryptic nuclear localization signals in the prion protein. Neurobiol Dis 2003;12:133-149. (Pubitemid 36349405)
63. Moreno FJ, Bagnat M, Lim F, Avila J. OP18/stathmin binds near the C-terminus of tubulin and facilitates GTP binding. Eur J Biochem 1999;262:557-562. (Pubitemid 29266069)
64. Tucker C, Goldstein LS. Probing the kinesin-microtubule interaction. J Biol Chem 1997;272:9481-9488.
65. Hagiwara H, Yorifuji H, Sato-Yoshitake R, Hirokawa N. Competition between motor molecules (kinesin and cytoplasmic dynein) and fibrous microtubule-associated proteins in binding to microtubules. J Biol Chem 1994;269:3581-3589. (Pubitemid 24237684)
66. Lopez LA, Sheetz MP. Steric inhibition of cytoplasmic dynein and kinesin motility by MAP2. Cell Motil Cytoskeleton 1993;24:1-16.
67. Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, Mandelkow E. Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J Cell Biol 1998;143:777-794. (Pubitemid 28512571)
68. Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, Mandelkow E. Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J 2002;21:4896-4905.
69. Nogales E, Whittaker M, Milligan RA, Downing KH. High-resolution model of the microtubule. Cell 1999;96:79-88.
70. Larcher JC, Boucher D, Lazereg S, Gros F, Denoulet P. Interaction of kinesin motor domains with alpha- and beta-tubulin subunits at a tau-independent binding site. Regulation by polyglutamylation. J Biol Chem 1996;271:22117- 22124. (Pubitemid 26303842)
71. Bonnet C, Boucher D, Lazereg S, Pedrotti B, Islam K, Denoulet P, Larcher JC. Differential binding regulation of microtubule-associated proteins MAP1A. MAP1B, and MAP2 by tubulin polyglutamylation. J Biol Chem 2001;276:12839-12848. (Pubitemid 37385203)
72. Saoudi Y, Paintrand I, Multigner L, Job D. Stabilization and bundling of subtilisin-treated microtubules induced by microtubule associated proteins. J Cell Sci 1995;108:357-367.
73. Chau MF, Radeke MJ, de Inés C, Barasoain I, Kohlstaedt LA, Feinstein SC. The microtubule-associated protein tau cross-links to two distinct sites on each alpha and beta tubulin monomer via separate domains. Biochemistry 1998;37:17692-17703. (Pubitemid 29023924)
74. Thorn KS, Ubersax JA, Vale RD. Engineering the processive run length of the kinesin motor. J Cell Biol 2000;151:1093-1100.
75. Folker ES, Baker BM, Goodson HV. Interactions between CLIP-170, tubulin, and microtubules: implications for the mechanism of CLIP-170 plus-end tracking behavior. Mol Biol Cell 2005;11:5373-5384.
76. Gustke N, Steiner B, Mandelkow EM, Biernat J, Meyer HE, Goedert M, Mandelkow E. The Alzheimer-like phosphorylation of tau protein reduces microtubule binding and involves Ser-Pro and Thr-Pro motifs. FEBS Lett 1992;307:199-205.
77. Morel E, Fouquet S, Strup-Perrot C, Thievend CP, Petit C, Loew D, Faussat AM, 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.