Identification and structural analysis of C-terminally truncated collapsin response mediator protein-2 in a murine model of prion diseases

Proteome Science

Volumn 8, Issue , 2010, Pages

  Shinkai Ouchi, Fumiko ^a   Yamakawa, Yoshio ^a   Hara, Hideyuki ^a   Tobiume, Minoru ^a   Nishijima, Masahiro ^a,b   Hanada, Kentaro ^a   Hagiwara, Ken'ichi ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; MESSENGER RNA; SERINE;

AMINO ACID SEQUENCE; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DENDRITE; ELECTROSPRAY MASS SPECTROMETRY; EXPERIMENTAL MODEL; FEMALE; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; NERVE CELL; NERVE FIBER; NEURITE; NONHUMAN; NORTHERN BLOTTING; PATHOGENESIS; PRION DISEASE; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; TWO DIMENSIONAL ELECTROPHORESIS; WESTERN BLOTTING;

MURINAE; MUS; SCRAPIE PRION; WALLERIA;

EID: 77957993127     PISSN: None     EISSN: 14775956     Source Type: Journal    
DOI: 10.1186/1477-5956-8-53     Document Type: Article

References (52)

1. Prusiner SB, . (Ed) Prion biology and diseases 2004, Cold Spring Harbor: Cold Spring Harbor Laboratory Press, (Ed).
2. Hogan RN, Baringer JR, Prusiner SB. Scrapie infection diminishes spines and increases varicosities of dendrites in hamsters: a quantitative Golgi analysis. J Neuropathol Exp Neurol 1987, 46:461-473. 10.1097/00005072-198707000-00005, 3598605.
3. Jeffrey M, Halliday WG, Bell J, Johnston AR, MacLeod NK, Ingham C, Sayers AR, Brown DA, Fraser JR. Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapie-infected murine hippocampus. Neuropathol Appl Neurobiol 2000, 26:41-54. 10.1046/j.1365-2990.2000.00216.x, 10736066.
4. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science 1982, 216:136-144. 10.1126/science.6801762, 6801762.
5. Mironov A, 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.
6. Linden R, Martins VR, Prado MA, Cammarota M, Izquierdo I, Brentani RR. Physiology of the prion protein. Physiol Rev 2008, 88:673-728. 10.1152/physrev.00007.2007, 18391177.
7. Büeler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, Weissmann C. Mice devoid of PrP are resistant to scrapie. Cell 1993, 73:1339-1347. 10.1016/0092-8674(93)90360-3, 8100741.
8. Soto C. Unfolding the role of protein misfolding in neurodegenerative diseases. Nat Rev Neurosci 2003, 4:49-60. 10.1038/nrn1007, 12511861.
9. Riemer C, Neidhold S, Burwinkel M, Schwarz A, Schultz J, Krätzschmar J, Mönning U, Baier M. Gene expression profiling of scrapie-infected brain tissue. Biochem Biophys Res Commun 2004, 323:556-564. 10.1016/j.bbrc.2004.08.124, 15369787.
10. Brown AR, Rebus S, McKimmie CS, Robertson K, Williams A, Fazakerley JK. Gene expression profiling of the preclinical scrapie-infected hippocampus. Biochem Biophys Res Commun 2005, 334:86-95. 10.1016/j.bbrc.2005.06.060, 15992767.
11. Skinner PJ, Abbassi H, Chesebro B, Race RE, Reilly C, Haase AT. Gene expression alterations in brains of mice infected with three strains of scrapie. BMC Genomics 2006, 7:114. 10.1186/1471-2164-7-114, 1475852, 16700923.
12. Xiang W, Hummel M, Mitteregger G, Pace C, Windl O, Mansmann U, Kretzschmar HA. Transcriptome analysis reveals altered cholesterol metabolism during the neurodegeneration in mouse scrapie model. J Neurochem 2007, 102:834-847. 10.1111/j.1471-4159.2007.04566.x, 17437544.
13. Sorensen G, Medina S, Parchaliuk D, Phillipson C, Robertson C, Booth SA. Comprehensive transcriptional profiling of prion infection in mouse models reveals networks of responsive genes. BMC Genomics 2008, 9:114. 10.1186/1471-2164-9-114, 2294129, 18315872.
14. Greenwood AD, Horsch M, Stengel A, Vorberg I, Lutzny G, Maas E, Schädler S, Erfle V, Beckers J, Schätzl H, Leib-Mösch C. Cell line dependent RNA expression profiles of prion-infected mouse neuronal cells. J Mol Biol 2005, 349:487-500. 10.1016/j.jmb.2005.03.076, 15896347.
15. Chich JF, Schaeffer B, Bouin AP, Mouthon F, Labas V, Larramendy C, Deslys JP, Grosclaude J. Prion infection-impaired functional blocks identified by proteomics enlighten the targets and the curing pathways of an anti-prion drug. Biochim Biophys Acta 2007, 1774:154-167.
16. Goshima Y, Nakamura F, Strittmatter P, Strittmatter SM. Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 1995, 376:509-514. 10.1038/376509a0, 7637782.
17. Wang LH, Strittmatter SM. A family of rat CRMP genes is differentially expressed in the nervous system. J Neurosci 1996, 16:6197-6207.
18. Byk T, Ozon S, Sobel A. The Ulip family phosphoproteins. Eur J Biochem 1998, 254:14-24. 10.1046/j.1432-1327.1998.2540014.x, 9652388.
19. Kamata T, Subleski M, Hara Y, Yuhki N, Kung H, Copeland NG, Jenkins NA, Yoshimura T, Modi W, Copeland TD. Isolation and characterization of a bovine neural specific protein (CRMP-2) cDNA homologous to unc-33, a C. elegans gene implicated in axonal outgrowth and guidance. Mol Brain Res 1998, 54:219-236. 10.1016/S0169-328X(97)00332-X, 9555025.
20. Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, Kaibuchi K. GSK-3β regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 2005, 120:137-149. 10.1016/j.cell.2004.11.012, 15652488.
21. Shinagawa M, Takahashi K, Sasaki S, Doi S, Goto H, Sato G. Characterization of scrapie agent isolated from sheep in Japan. Microbiol Immunol 1985, 29:543-551.
22. Inoue Y, Yamakawa Y, Sakudo A, Kinumi T, Nakamura Y, Matsumoto Y, Saeki K, Kamiyama T, Onodera T, Nishijima M. Infection route-independent accumulation of splenic abnormal prion protein. Jpn J Infect Dis 2005, 58:78-82.
23. Diedrich J, Wietgrefe S, Zupancic M, Staskus K, Retzel E, Haase AT, Race R. The molecular pathogenesis of astrogliosis in scrapie and Alzheimer's disease. Microb Pathog 1987, 2:435-442. 10.1016/0882-4010(87)90050-7, 3507557.
24. Gray BC, Skipp P, O'Connor VM, Perry VH. Increased expression of glial fibrillary acidic protein fragments and μ-calpain activation within the hippocampus of prion-infected mice. Biochem Soc Trans 2006, 34:51-54. 10.1042/BST0340051, 16417481.
25. Kumar Y, Khachane A, Belwal M, Das S, Somsundaram K, Tatu U. ProteoMod: A new tool to quantitate protein post-translational modifications. Proteomics 2004, 4:1672-1683. 10.1002/pmic.200300778, 15174136.
26. Zhu K, Zhao J, Lubman DM, Miller FR, Barder TJ. Protein pI shifts due to posttranslational modifications in the separation and characterization of proteins. Anal Chem 2005, 77:2745-2755. 10.1021/ac048494w, 15859589.
27. Zhuo S, Clemens JC, Hakes DJ, Barford D, Dixon JE. Expression, purification, crystallization, and biochemical characterization of a recombinant protein phosphatase. J Biol Chem 1993, 268:17754-17761.
28. Breci LA, Tabb DL, Yates JR, Wysocki VH. Cleavage N-terminal to proline: analysis of a database of peptide tandem mass spectra. Anal Chem 2003, 75:1963-1971. 10.1021/ac026359i, 12720328.
29. Gu Y, Hamajima N, Ihara Y. Neurofibrillary tangle-associated collapsin response mediator protein-2 (CRMP-2) is highly phosphorylated on Thr-509, Ser-518, and Ser-522. Biochemistry 2000, 39:4267-4275. 10.1021/bi992323h, 10757975.
30. Yuasa-Kawada J, Suzuki R, Kano F, Ohkawara T, Murata M, Noda M. Axonal morphogenesis controlled by antagonistic roles of two CRMP subtypes in microtubule organization. Eur J Neurosci 2003, 17:2329-2343. 10.1046/j.1460-9568.2003.02664.x, 12814366.
31. Rogemond V, Auger C, Giraudon P, Becchi M, Auvergnon N, Belin MF, Honnorat J, Moradi-Améli M. Processing and nuclear localization of CRMP2 during brain development induce neurite outgrowth inhibition. J Biol Chem 2008, 283:14751-14761. 10.1074/jbc.M708480200, 18332147.
32. Bretin S, Reibel S, Charrier E, Maus-Moatti M, Auvergnon N, Thevenoux A, Glowinski J, Rogemond V, Prémont J, Honnorat J, Gauchy C. Differential expression of CRMP1, CRMP2A, CRMP2B, and CRMP5 in axons or dendrites of distinct neurons in the mouse brain. J Comp Neurol 2005, 486:1-17. 10.1002/cne.20465, 15834957.
33. Quinn CC, Chen E, Kinjo TG, Kelly G, Bell AW, Elliott RC, McPherson PS, Hockfield S. TUC-4b, a novel TUC family variant, regulates neurite outgrowth and associates with vesicles in the growth cone. J Neurosci 2003, 23:2815-2823.
34. Bretin S, Rogemond V, Marin P, Maus M, Torrens Y, Honnorat J, Glowinski J, Prémont J, Gauchy C. Calpain product of WT-CRMP2 reduces the amount of surface NR2B NMDA receptor subunit. J Neurochem 2006, 98:1252-1265. 10.1111/j.1471-4159.2006.03969.x, 16787405.
35. Zhang Z, Ottens AK, Sadasivan S, Kobeissy FH, Fang T, Hayes RL, Wang KK. Calpain-mediated collapsin response mediator protein-1, -2, and -4 proteolysis after neurotoxic and traumatic brain injury. J Neurotrauma 2007, 24:460-472. 10.1089/neu.2006.0078, 17402852.
36. Touma E, Kato S, Fukui K, Koike T. Calpain-mediated cleavage of collapsin response mediator protein (CRMP)-2 during neurite degeneration in mice. Eur J Neurosci 2007, 26:3368-3381. 10.1111/j.1460-9568.2007.05943.x, 18052987.
37. Kobeissy FH, Ottens AK, Zhang Z, Liu MC, Denslow ND, Dave JR, Tortella FC, Hayes RL, Wang KK. Novel differential neuroproteomics analysis of traumatic brain injury in rats. Mol Cell Proteomics 2006, 5:1887-1898. 10.1074/mcp.M600157-MCP200, 16801361.
38. Jiang SX, Kappler J, Zurakowski B, Desbois A, Aylsworth A, Hou ST. Calpain cleavage of collapsin response mediator proteins in ischemic mouse brain. Eur J Neurosci 2007, 26:801-809. 10.1111/j.1460-9568.2007.05715.x, 17672855.
39. Katano T, Mabuchi T, Okuda-Ashitaka E, Inagaki N, Kinumi T, Ito S. Proteomic identification of a novel isoform of collapsin response mediator protein-2 in spinal nerves peripheral to dorsal root ganglia. Proteomics 2006, 6:6085-6094. 10.1002/pmic.200600300, 17051644.
40. Tompa P, Buzder-Lantos P, Tantos A, Farkas A, Szilágyi A, Bánóczi Z, Hudecz F, Friedrich P. On the sequential determinants of calpain cleavage. J Biol Chem 2004, 279:20775-20785. 10.1074/jbc.M313873200, 14988399.
41. Cuerrier D, Moldoveanu T, Davies PL. Determination of peptide substrate specificity for μ-calpain by a peptide library-based approach: the importance of primed side interactions. J Biol Chem 2005, 280:40632-40641. 10.1074/jbc.M506870200, 16216885.
42. Auvergnon N, Reibel S, Touret M, Honnorat J, Baron T, Giraudon P, Bencsik A. Altered expression of CRMPs in the brain of bovine spongiform encephalopathy-infected mice during disease progression. Brain Res 2009, 1261:1-6. 10.1016/j.brainres.2009.01.006, 19401179.
43. Stenmark P, Ogg D, Flodin S, Flores A, Kotenyova T, Nyman T, Nordlund P, Kursula P. The structure of human collapsin response mediator protein 2 a regulator of axonal growth. J Neurochem 2007, 101:906-917. 10.1111/j.1471-4159.2006.04401.x, 17250651.
44. Kim CL, Umetani A, Matsui T, Ishiguro N, Shinagawa M, Horiuchi M. Antigenic characterization of an abnormal isoform of prion protein using a new diverse panel of monoclonal antibodies. Virology 2004, 320:40-51. 10.1016/j.virol.2003.10.026, 15003861.
45. Shevchenko A, Wilm M, Vorm O, Mann M. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 1996, 68:850-858. 10.1021/ac950914h, 8779443.
46. Yanagisawa Y, Sato Y, Asahi-Ozaki Y, Ito E, Honma R, Imai J, Kanno T, Kano M, Akiyama H, Sata T, Shinkai-Ouchi F, Yamakawa Y, Watanabe S, Katano H. Effusion and solid lymphomas have distinctive gene and protein expression profiles in ananimal model of primary effusion lymphoma. J Pathol 2006, 209:464-473. 10.1002/path.2012, 16741895.
47. Protein Prospector program developed by the University of California, San Francisco, Mass Spectrometry Facility. , http://prospector.ucsf.edu/prospector/cgi-bin/msform.cgi?form=msfitstandard
48. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567. 10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2, 10612281.
49. ExPaSy Protemics Server, Compute pI/MW tool. , http://kr.expasy.org/tools/pi_tool.html
50. Obenauer JC, Cantley LC, Yaffe MB. Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 2003, 31:3635-3641. 10.1093/nar/gkg584, 168990, 12824383.
51. Nielsen AL, Holm IE, Johansen M, Bonven B, Jørgensen P, Jørgensen AL. A new splice variant of glial fibrillary acidic protein, GFAPε, interacts with the presenilin proteins. J Biol Chem 2002, 277:29983-29991. 10.1074/jbc.M112121200, 12058025.
52. Pappin DJ, Hojrup P, Bleasby AJ. Rapid identification of proteins by peptide-mass fingerprinting. Curr Biol 1993, 3:327-332. 10.1016/0960-9822(93)90195-T, 15335725.