Physiological role of the cellular prion protein (PrPc): Protein profiling study in two cell culture systems

Journal of Proteome Research

Volumn 7, Issue 7, 2008, Pages 2681-2695

  Ramljak, Sanja ^a   Asif, Abdul R ^a   Armstrong, Victor W ^a   Wrede, Arne ^a   Groschup, Martin H ^b   Buschmann, Anne ^b   Schulz Schaeffer, Walter ^a   Bodemer, Walter ^c   Zerr, Inga ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^c GERMAN PRIMATE CENTER   (Germany)

Author keywords

Cellular prion protein; Function; Human embryonic kidney 293 cells; Prion protein deficient cells; Proteome

Indexed keywords

PRION PROTEIN; PROTEIN; PROTEOME;

ALZHEIMER DISEASE; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL PROTECTION; CELL STRAIN HEK293; CELL STRESS; CONTROLLED STUDY; ENERGY METABOLISM; HOMEOSTASIS; HUMAN; HUMAN CELL; MOUSE; NEUROPATHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; UPREGULATION; ANIMAL; BIOSYNTHESIS; CELL LINE; COMPARATIVE STUDY; CYTOLOGY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; NERVE CELL; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; APOPTOSIS; CELL LINE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION PROFILING; HUMANS; MICE; NEURONS; PRPC PROTEINS; UP-REGULATION;

EID: 51649087972     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr7007187     Document Type: Article

References (58)

1. Kuwahara, C.; Takeuchi, A. M.; Nishimura, T.; Haraguchi, K.; Kubosaki, A.; Matsumoto, Y.; Saeki, K.; Yokoyama, T.; Itohara, S.; Onodera, T. Prions prevent neuronal cell-line death. Nature 1999, 400, 225-226.
2. Bounhar, Y.; Zhang, Y.; Goodyer, C. G.; LeBlanc, A. C. Prion protein protects human neurons against Bax-mediated apoptosis. J. Biol. Chem. 2001, 276, 39145-39149.
3. Panel, E.; Sunyach, C.; Alves da Costa, C.; Bourdon, J, C.; Vincent, B.; Checler, F. Primary cultured neurons devoid of cellular prion display lower responsiveness to staurosporine through the control of p53 at both transcriptional and post-transcriptional levels. J. Biol. Chem. 2004, 279, 612-618.
4. Brown, D. R.; Schulz-Schaeffer, W. J.; Schmidt, B.; Kretzschmar, H. Prion protein-deficient cells show altered response to oxidative stress due to decreased SOD-1 activity. Exp. Neurol. 1997, 146, 104-112.
5. Wong, B. S.; Liu, T.; Li, R.; Pan, T.; Petersen, R. B.; Smith, M. A.; Gambetti, P.; Perry, G.; Manson, J. C.; Brown, D. R.; Sy, M. S. Increased levels of oxidative stress markers detected in the brains of mice devoid of prion protein. J. Neurochem. 2001, 76, 565-572.
6. Brown, D. R.; Qin, K.; Herms, J. W.; Madlung, A.; Manson, J.; Strome, R.; Fraser, P. E.; 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.
7. Pauly, P. C.; Harris, D. A. Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 1998, 273, 33107-33110.
8. Mouillet-Richard, S.; Ermonval, M.; Chebassier, G; Laplanche, J. L.; Lehmann, S.; Launay, J. M.; Kellermann, O. Signal transduction through prion protein. Science 2000, 289, 1925-1928.
9. Chiarini, L. B.; Freitas, A. R.; Zanata, S. M.; Berntani, R. R.; Martins, V. R.; Linden, R. Cellular prion protein transduces neuroprotective signals. EMBO J. 2002, 21, 3317-3326.
10. Zanata, S. M.; Lopes, M. H.; Mercadante, A. F.; Hajj, G. N.; Chiarini, L. B.; Nomizo, R.; Freitas, A. R.; Cabral, A. L.; Lee, K. S.; Juliano, M. A.; De Oliveira, E.; Jachieri, S. G.; Burlingame, A.; Huang, L.; Linden, R.; Brentani, R. R.; Martins, V. R. Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO ]. 2002, 21, 3307-3316.
11. Walz, R.; Amaral, O. B.; Rockenbach, I. C.; Roesler, R.; Izquierdo, I.; Cavalheiro, E. A.; Martins, V. R.; Brentani, R. R. Increased sensitivity to seizures in mice lacking cellular prion protein. Epilepsia 1999, 40, 1679-1682.
12. McLennan, N. F.; Brennan, P. M.; McNeill, A.; Davies, I.; Fother-ingham, A.; Rennison, K. A.; Ritchie, D.; Brannan, F.; Head, M. W.; Ironside, J. W.; Williams, A.; Bell, J. E. Prion protein accumulation and neuroprotection in hypoxic brain damage. Am. J. Pathol. 2004, 165, 227-235.
13. c after focal cerebral ischemia and influence of lesion severity. Neurosci. Lett. 2004, 372, 146-150.
14. Westaway, D.; DeArmond, S. J.; Cayetano-Canlas, J.; Groth, D.; Foster, D.; Yang, S. L.; Torchia, M.; Carlson, G. A.; Prusiner, S. B. Degeneration of skeletal muscle.; peripheral nerves and the central nervous system in transgenic mice overexpressing wild-type prion proteins. Cell 1994, 76, 117-129.
15. Huang, S.; Liang, J.; Zheng, M.; Li, X.; Wang, M.; Wang, P.; Vanegas, D.; Wu, D.; Chakraborty, B.; Hays, A. P.; Chen, K.; Chen, S. G.; Booth, S.; Cohen, M.; Gambetti, P.; Kong, Q. Inducible overexpression of wild-type prion protein in the muscles leads to a primary myopathy in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 6800-6805.
16. Satoh, J.; Kuroda, Y.; Katamine, S. Gene expression profile in prion protein-deficient fibroblasts in culture. Am. J. Pathol. 2000, 157, 9-68.
17. Satoh, J.; Yamamura, T. Gene expression profile following stable expression of the cellular prion protein. Cell. Mol. Neurobiol. 2004, 24, 793-814.
18. artinez, T.; Pascual, A. Identification of genes differentially expressed in SH-SY5Y neuroblastoma cells exposed to the prion peptide 106-126. Eur. J. Neurosci. 2007, 26, 51-59.
19. Strom, A.; Diecke, S.; Hunsmann, G.; Stuke, A. W. Identification of prion protein binding proteins by combined use of far-Western immunoblotting, two dimensional gel electrophoresis and mass spectrometry. Proteomics 2006, 6, 26-34.
20. Petrakis, S.; Sklaviadis, T. Identification of proteins with high affinity for refolded and native PrPc. Proteomics 2006, 6, 6476-6484.
21. Büeler, H.; Aguzzi, A.; Sailer, A.; Greiner, R. A.; Autenried, P.; Aguet, M.; Weissmann, C. Mice devoid of PrP are resistent to scrapie. Cell 1993, 73, 1339-1347.
22. Blum, H.; Beier, H.; Gross, H. J. Improved silver staining of plant proteins.; RNA and DNA in polyacrylamide gels. Electrophoresis 1987, 8, 93-99.
23. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68, 850-858.
24. Asif, A. R.; Oellerich, M.; Armstrong, V. W.; Riemenschneider, B.; Monod, M.; Reichard, U. Proteome of conidial surface associated proteins of Aspergillus fumigatus reflecting potential vaccine candidates and allergens. J. Proteome Res. 2006, 5, 954-962.
25. Krasemann, S.; Jurgens, T.; Bodemer, W. Generation of monoclonal antibodies against prion proteins with an unconventional nucleic acid-based immunization strategy. J. Biotechnol. 1999, 73, 119-129.
26. Ma, J.; Wollmann, R.; Lindquist, S. Neurotoxicity and neurode- generation when PrP accumulates in the cytosol. Science 2002, 298, 1781-1785.
27. Sunyach, C.; Cisse, M. A.; da Costa, C. A.; Vincent, B.; Checler, F. The C-terminal products of cellular prion protein processing, CI and C2, exert distinct influence on p53-dependent staurosporine-induced caspase-3 activation. J. Biol. Chem. 2007, 282, 1956-1963.
28. Yan, S. D.; Fu, J.; Soto, C.; Chen, X.; Zhu, FL; Al-Mohanna, F.; Collison, K.; Zhu, A.; Stern, E.; Saido, T.; Tohyama, M.; Ogawa, S.; Roher, A.; Stern, D. An intracellular protein that binds amyloid-β peptide and mediates neurotoxicity in Alzheimer's disease. Nature 1997, 389, 689-695.
29. Frackowiak, J.; Mazur-Kolecka, B.; Kaczmarski, W.; Dickson, D. Deposition of Alzheimer's vascular amyloid-beta is associated with decreased expression of brain L-3-hydroxyacyl-coenzyme A dehydrogenase ERAB. Brain Res. 2001, 907, 44-53.
30. Tieu, K.; Perier, C.; Vila, M.; Caspersen, C.; Zhang, H. P.; Teismann, P.; Jackson-Lewis, V.; Stern, D. M.; Yan, S. D.; Przedborski, S. L-3-hydroxyacyl-CoA dehydrogenase II protects in a model of Parkinson's disease. Ann. Neurol. 2004, 56, 51-60.
31. Schapira, A. H.; Cooper, J. M.; Dexter, D.; Clark, J. B.; Jenner, P.; Marsden, C. D. Mitochondrial complex I deficiency in Parkinson's disease. J. Neurochem. 1990, 54, 823-827.
32. Coskun, P. E.; Beal, M. F.; Wallace, D. C. Alzheimer's brains harbor somatic mtDNA control-region mutations that suppress mitochondrial transcription and replication. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 10726-10731.
33. Xiang, W.; Windl, O.; Westner, I. M.; Neumann, M.; Zerr, I.; Lederer, R. M.; Kretzschmar, H. A Cerebral gene expression profiles in sporadic Creutzfeldt-Jakob disease. Ann. Neurol. 2005, 58, 242-257.
34. Stabler, S. M.; Ostrowski, L. L.; Janicki, S. M.; Monteiro, M. J. A myristoylated calcium-binding protein that preferentially interacts with the Alzheimer's disease presenilin 2 protein. J. Cell. Biol. 1999,145, 1277-1292.
35. Jastrzêbska, B.; Filipek, A.; Nowicka, D.; Kaczmarek, L.; Kuünicki, J. Calcyclin S100A6 binding protein CacyBP is highly expressed in brain neurons. J. Histochem. Cytochem. 2000, 48, 1195-1202.
36. Wu, J.; Tan, X.; Peng, X.; Yuan, J.; Qiang, B. Translocation and phosphorylation of calcyclin binding protein during retinoic acid-induced neuronal differentiation of neuroblastoma SH-SY5Y cells. J. Biochem. Mol. Biol. 2003, 36, 354-358.
37. Liang, J.; Luo, G.; Ning, X.; Shi, Y.; Zhai, H.; Sun, S.; Jin, H.; Liu, Z.; Zhang, F.; Lu, Y.; Zhao, Y.; Chen, X; Zhang, H.; Guo, X.; Wu, K.; Fan, D. Differential expression of calcium-related genes in gastric cancer cells transfected with cellular prion protein. Biochem. Cell Biol. 2007, 85, 375-383.
38. Paitel, E.; Alves da Costa, C.; Vilette, D.; Grassi, J.; Checler, F. Overexpression of PrPc triggers caspase 3 activation: potentiation by proteasome inhibitors and blockade by anti-PrP antibodies. J. Neurochem. 2002, 83, 1208-1214.
39. Sitia, R.; Braakman, I. Quality control in the endoplasmic reticulum protein factory. Nature 2003, 426, 891-894.
40. Schonberger, S. J.; Edgar, P. F.; Kydd, R.; Faull, R. L.; Cooper, G. J. Proteomic analysis of the brain in Alzheimer's disease, molecular phenotype of a complex disease process. Proteomics 2001, 1, 1519-1528.
41. Liang, J.; Pan, Y.; Zhang, D.; Guo, C.; Shi, Y.; Wang, J.; Chen, Y.; Wang, X.; Liu, J.; Guo, X.; Chen, Z.; Qiao, T.; Fan, D. Cellular prion protein promotes proliferation and Gl/S transition of human gastric cancer cells SGC7901 and AGS. FASEB J. 2007, 21, 2247-2256.
42. Lopes, C. S.; Sampaio, P.; Williams, B.; Goldberg, M.; Sunkel, C. E. The Drosophila Bub3 protein is required for the mitotic checkpoint and for normal accumulation of cyclins during G2 and early stages of mitosis. J. Cell Sci. 2005, 118, 187-198.
43. Junge, W.; Lill, H.; Engelbrecht, S. ATP synthase, an electrochemical transducer with rotatory mechanics. Trends Biochem. Sci. 1997, 22, 420-423.
44. Schagger, H.; Ohm, T. G. Human diseases with defects in oxidative phosphorylation. 2. FIFO ATP-synthase defects in Alzheimer disease revealed by blue native polyacrylamide gel electrophoresis. Eur. J. Biochem. 1995, 227, 916-921.
45. Gerke, V.; Moss, S. E. Annexins, from structure to function. Physiol. Rev. 2002, 82, 331-371.
46. Negrutskii, B. S.; El'skaya, A. V. Eukaryotic translation elongation factor 1 alpha: structure; expression; functions; and possible role in aminoacyl-tRNA channeling. Prog. Nucleic Acid Res. Mol. Biol. 1998, 60, 47-78.
47. Shiina, N.; Gotoh, Y.; Kubomura, N.; Iwamatsu, A.; Nishida, E. Microtubule severing by elongation factor 1 alpha. Science 1994, 266, 282-285.
48. Sakudo, A.; Lee, D. C.; Saeki, K.; Nakamura, Y.; Inoue, K.; Matsumoto, Y.; Itohara, S.; Onodera, T. Impairment of superoxide dismutase activation by N-terminally truncated prion protein PrP in PrP deficient neuronal cell line. Biochem. Biophys. Res. Commun. 2003, 308, 660-667.
49. Han, S.; Zhang, K. H.; Lu, P. H.; Xu, X. M. Effects of annexins II and V on survival of neurons and astrocytes in vitro. Acta Pharmacol. Sin. 2004, 25, 602-610.
50. Strom, A.; Wang, G. S.; Reimer, R.; Finegood, D. T.; Scott, F. W. Pronounced cytosolic aggregation of cellular prion protein in ancreatic β-cells in response to hyperglycemia. Lab. Invest. 2007, 87, 139-149.
51. Schmidt, H.; Otto, M.; Niedmann, P.; Cepek, L.; Schroter, A.; Kretzschmar, H. A.; Poser, S. CSF lactate dehydrogenase activity in patients with Creutzfeldt-Jakob disease exceeds that in other dementias. Dement. Geriatr. Cogn. Disord. 2004, 17, 204-206.
52. Mehlen, P.; Kretz-Remy, C.; Preville, X.; Arrigo, A. P. Human hsp27, Drosophila hsp27 and human alphaB Crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFalpha -induced cell death. EMBO J. 1996, 15, 2695-2706.
53. Bruey, J. M.; Ducasse, C.; Bonniaud, P.; Ravagnan, L.; Susin, S. A.; Diaz-Latoud, C.; Gurbuxani, S.; Arrigo, A. P.; Kroemer, G.; Solary, E.; Garrido, C. Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat. Cell Biol. 2000, 2, 645-652.
54. Kim, B. H.; Lee, H. G.; Choi, J. K.; Kim, J. I.; Choi, E. K.; Carp, R. I.; Kim, Y. S. The cellular prion protein PrPc prevents apoptotic neuronal cell death and mitochondrial dysfunction induced by serum deprivation. Mol. Brain Res. 2004, 124, 40-50.
55. Burd, C. G.; Dreyfuss, G. Conserved structures and diversity of functions of RNA-binding proteins. Science 1994, 265, 615-621.
56. Pinol-Roma, S.; Dreyfuss, G. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 1992, 355, 730-732.
57. Radulescu, R. T.; Korth, C. Prion function and dysfunction: A structure-based scenario. Med. Hypotheses 1996, 46, 225-228.
58. Banki, K.; Hutter, E.; Colombo, E.; Gonchoroff, N. J.; Perl, A. Glutathione levels and sensitivity to apoptosis are regulated by changes in transaldolase expression. J. Biol. Chem. 1996, 271, 32994-33001.