Alteration of NF-κB activity leads to mitochondrial apoptosis after infection with pathological prion protein

Cellular Microbiology

Volumn 9, Issue 9, 2007, Pages 2202-2217

  Bourteele, Soizic ^a   Oesterle, Katja ^a   Weinzierl, Andreas O ^b   Paxian, Stephan ^c,d   Riemann, Marc ^c,e   Schmid, Roland M ^c   Planz, Oliver ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 9; IMMUNOGLOBULIN ENHANCER BINDING 1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING 2 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NUCLEIC ACID BINDING PROTEIN; PRION PROTEIN; PROTEIN BCL 3; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BCL2L1 PROTEIN, MOUSE; NFKB1 PROTEIN, MOUSE; NFKB2 PROTEIN, MOUSE; ONCOPROTEIN; PROTEIN BCL X; PROTO ONCOGENE PROTEIN BCL 3; PROTO-ONCOGENE PROTEIN BCL-3;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; GENE DELETION; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC TRANSCRIPTION; IN VITRO STUDY; MITOCHONDRION; MOUSE; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; PRION DISEASE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; UPREGULATION; ANIMAL; BRAIN; C57BL MOUSE; CELL LINE; CYTOLOGY; ENZYME ACTIVATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY;

MUS;

ANIMALS; APOPTOSIS; BCL-X PROTEIN; BRAIN; CASPASE 3; CASPASE 9; CELL LINE; ENZYME ACTIVATION; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; NF-KAPPA B P50 SUBUNIT; NF-KAPPA B P52 SUBUNIT; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; PRPSC PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 34547868484     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2007.00950.x     Document Type: Article

References (45)

1. 2+ accumulation. Proc Natl Acad Sci USA 92: 9328-9332.
2. Barkett, M., Xue, D., Horvitz, H.R., and Gilmore, T.D. (1997) Phosphorylation of I kappa B-alpha inhibits its cleavage by caspase CPP32 in vitro. J Biol Chem 272: 29419-29422.
3. Bate, C., Salmona, M., Diomede, L., and Williams, A. (2004) Squalestatin cures prion-infected neurons and protects against prion neurotoxicity. J Biol Chem 279: 14983-14990.
4. Betz, U.A., Vosshenrich, C.A., Rajewsky, K., and Muller, W. (1996) Bypass of lethality with mosaic mice generated by Cre-loxP-mediated recombination. Curr Biol 6: 1307-1316.
5. Bhakar, A.L., Tannis, L.L., Zeindler, C., Russo, M.P., Jobin, C., Park, D.S., et al. (2002) Constitutive nuclear factor-kappaB activity is required for central neuron survival. J Neurosci 22: 8466-8475.
6. Bonizzi, G., and Karin, M. (2004) The two NF-kappa B activation pathways and their role in innate and adaptive immunity. Trends Immunol 25: 280-288.
7. Bosque, P.J., and Prusiner, S.B. (2000) Cultured cell sublines highly susceptible to prion infection. J Virol 74: 4377-4386.
8. Bours, V., Franzoso, G., Azarenko, V., Park, S., Kanno, T., Brown, K., and Siebenlist, U. (1993) The oncoprotein Bcl-3 directly transactivates through Kappa-B motifs via association with DNA-binding P50B homodimers. Cell 72: 729-739.
9. Bourteele, S., Oesterle, K., Pleschka, S., Unterstab, G., Ehrhardt, C., Wolff, T., et al. (2005) Constitutive activation of the transcription factor NF-kappa B results in impaired Borna disease virus replication. J Virol 79: 6043-6051.
10. Brown, A.R., Webb, J., Rebus, S., Walker, R., Williams, A., and Fazakerley, J.K. (2003) Inducible cytokine gene expression in the brain in the ME7/CV mouse model of scrapie is highly restricted, is at a strikingly low level relative to the degree of gliosis and occurs only late in disease. J Gen Virol 84: 2605-2611.
11. Coulpier, M., Messiaen, S., Hamel, R., Fernandez de Marco, M., Lilin, T., and Eloit, M. (2006) Bax deletion does not protect neurons from BSE-induced death. Neurobiol Dis 23: 603-611.
12. Cronier, S., Laude, H., and Peyrin, J.M. (2004) Prions can infect primary cultured neurons and astrocytes and promote neuronal cell death. Proc Natl Acad Sci USA 101: 12271-12276.
13. Dhantapani, K.M., Wade, F.M., Wakade, C., Mahesesh, V.B., and Brann, D.W. (2005) Neuroprotection by stem cell factor in rat cortical neurons involves AKT and NFkappaB. J Neurochem 95: 9-19.
14. Fabrizi, C., Silei, V., Menegazzi, M., Salmona, M., Bugiani, O., Tagliavini, F., et al. (2001) The stimulation of inducible nitric-oxide synthase by the prion protein fragment 106-126 in human microglia is tumor necrosis factor-alpha-dependent and involves p38 mitogen-activated protein kinase. J Biol Chem 276: 25692-25696.
15. Giese, A., Groschup, M.H., Hess, B., and Kretzschmar, H.A. (1995) Neuronal cell-death in scrapie-infected mice is due to apoptosis. Brain Pathol 5: 213-221.
16. Glasgow, J., and Perez-Polo, R. (2000) One path to cell death in the nervous system. Neurochem Res 25: 1373-1383.
17. Greenwood, A.D., Horsch, M., Stengel, A., Vorberg, I., Lutzny, G., Maas, E., et al. (2005) Cell line dependent RNA expression profiles of prion-infected mouse neuronal cells. J Mol Biol 349: 487-500.
18. Herrmann, O., Baumann, B., de Lorenzi, R., Muhammad, S., Zhang, W., Kleesiek, J., et al. (2005) IKK mediates ischemia-induced neuronal death. Nat Med 11: 1322-1329.
19. Hetz, C., and Soto, C. (2003) Protein misfolding and disease: The case of prion disorders. Cell Mol Life Sci 60: 133-143.
20. Hetz, C., Russelakis-Carneiro, M., Maundrell, K., Castilla, J., and Soto, C. (2003) Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. EMBO J 22: 5435-5445.
21. Hetz, C., Russelakis-Carneiro, M., Wälchi, S., Carboni, S., Vial-Knecht, E., Maundrell, K., et al. (2005) The disulfide isomerase Grp58 is a protective factor against prion neurotoxicity. J Neurosci 25: 2793-2802.
22. Hill, A.F., Joiner, S., Linehan, J., Desbruslais, M., Lantos, P.L., and Collinge, J. (2000) Species barrier-independent prion replication in apparently resistant species. Proc Natl Acad Sci USA 97: 10248-10253.
23. Inta, I., Paxian, S., Maegele, I., Zhang, W., Pizzi, M., Spano, P., et al. (2006) Bim and Nora are candidates to mediate the deleterious effect of the NF-kappa B subunit RelA in cerebral ischemia. J Neurosci 26: 12896-12903.
24. Kaltschmidt, B., Uherek, M., Wellman, H., Volk, B., and Kaltschmidt, C. (1999) Inhibition of NF-kappa-B potentiates amyloid beta-mediated neuronal apoptosis. Proc Natl Acad Sci USA 96: 9409-9414.
25. Kaltschmidt, C., Kaltschmidt, B., and Baeuerle, P.A. (1995) Stimulation of ionotropic glutamate receptors activates transcription factor NF-Kappa-B in primary neurons. Proc Natl Acad Sci USA 92: 9618-9622.
26. Karin, M., and Lin, A. (2002) NF-kappa-B at the crossroads of life and death. Nat Immunol 3: 221-227.
27. Kastenbauer, S., and Ziegler-Heitbrock, H.W.L. (1999) NF-kappa-B1 (p50) is upregulated in lipopolysaccharide tolerance and can block tumor necrosis factor gene expression. Infect Immun 67: 1553-1559.
28. Kim, J.I., Ju, W.K., Choi, J.H., Kim, J., Choi, E.K., Carp, R.I., etal. (1999) Expression of cytokine genes and increased nuclear factor-kappa-B activity in the brains of scrapie-infected mice. Mol Brain Res 73: 17-27.
29. Kristiansen, M., Messenger, M.J., Klöhn, P.C., Brandner, S., Wadsworth, J.D.F., Collinge, J., and Tabrizi, S.J. (2005) Disease-related prion protein forms aggresomes in neuronal cells leading to caspase activation and apoptosis. J Biol Chem 280: 38851-38861.
30. Kroemer, G. (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 3: 614-620.
31. Li, A., Barmada, S.J., Roth, K.A., and Harris, D.A. (2007) N-terminally deleted forms of the prion protein activate both Bax-dependent and Bax-independent neurotoxic pathways. J Neurosci 27: 852-859.
32. Liptay, S., Fulda, S., Schanbacher, M., Bourteele, S., Ferri, K.F., Kroemer, G., et al. (2002) Molecular mechanisms of sulfasalazine-induced T-cell apoptosis. Br J Pharmacol 137: 608-620.
33. Lucassen, P.J., Williams, A., Chung, W.C., and Fraser, H. (1995) Detection of apoptosis in murine scrapie. Neurosci Lett 198: 185-188.
34. Mallucci, G., Dickinson, A., Linehan, J., Klöhn, P.C., Brandner, S., and Collinge, J. (2003) Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302: 871-874.
35. Mattson, M.P., Goodman, Y., Luo, H., Fu, W., and Furukawa, K. (1997) Activation of NF-kappa-B protects hippocampal neurons against oxidative stress-induced apoptosis: Evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J Neurosci Res 49: 681-697.
36. Mattson, M.P., and Culmsee, C., Yu, Z.F., and Camandola, S. (2000) Roles of nuclear factor kappa B in neuronal survival and plasticity. J Neurochem 74: 443-456.
37. Nilsen, J., and Brinton, R.D. (2004) Mitochondria as therapeutic targets of estrogen action in the central nervous system. Curr Drug Targets CNS Neurol Disord 3: 297-313.
38. O'Donovan, C.N., Tobin, D., and Cotter, T.G. (2001) Prion protein fragment PrP-(106-126) induces apoptosis via mitochondrial disruption in human neuronal SH-SY5Y cells. J Biol Chem 276: 43516-43523.
39. Olschlager, V., Pleschka, S., Fischer, T., Rziha, H.J., Wurzer, W., Stitz, L., et al. (2004) Lung-specific expression of active Raf kinase results in increased mortality of influenza A virus-infected mice. Oncogene 23: 6639-6646.
40. Pahl, H.L. (1999) Activators and target genes of Rel/NF-kappa B transcription factors. Oncogene 18: 6853-6866.
41. Paxian, S., Merkle, H., Riemann, M., Wilda, M., Adler, G., Hameister, H., et al. (2002) Abnormal organogenesis of Peyer's patches in mice deficient for NF-kappa B1, NF-kappa B2, and Bcl-3. Gastroenterology 122: 1853-1868.
42. Polster, B.M., and Fiskum, G. (2004) Mitochondrial mechanisms of neural cell apoptosis. J Neurochem 90: 1281-1289.
43. Riemann, M., Endres, R., Liptay, S., Pfeffer, K., and Schmid, R.M. (2005) The I kappa B protein Bcl-3 negatively regulates transcription of the IL-10 gene in macrophages. J Immunol 175: 3560-3568.
44. Shi, Y. (2002) Mechanism of caspase activation and inhibition during apoptosis. Mol Cell 9: 459-470.
45. Shishodia, S., Amin, H.M., Lai, R., and Aggarwal, B.B. (2005) Curcumin (diferuloylmethane) inhibits constitutive NF-kappa B activation, induces G1/S arrest, suppresses proliferation, and induces apoptosis in mantle cell lymphoma. Biochem Pharmacol 70: 700-713.