Distinct spatial activation of intrinsic and extrinsic apoptosis pathways in natural scrapie: Association with prion-related lesions

Veterinary Research

Volumn 40, Issue 5, 2009, Pages

  Serrano, Carmen ^a   Lyahyai, Jaber ^a   Bolea, Rosa ^a   Varona, Luis ^a   Monleón, Eva ^a   Badiola, Juan J ^a   Zaragoza, Pilar ^a   Martín Burriel, Inmaculada ^a  

^a UNIVERSIDAD DE ZARAGOZA   (Spain)

Author keywords

Apoptosis; Extrinsic pathway; Mitochondrial pathway; Prion; Scrapie

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 3; CYTOKINE; FAS ANTIGEN; FAS LIGAND; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PRION PROTEIN; PROTEIN BAD; PROTEIN BAK; PROTEIN BCL 2; PROTEIN BCL X; PROTEIN BCL XL; PROTEIN MCL 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; RNA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN MITOCHONDRION; BRAIN REGION; CELL ACTIVATION; CELL DEATH; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PREFRONTAL CORTEX; PRION DISEASE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCRAPIE; SHEEP; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALIA; OVIS ARIES;

ANIMALS; APOPTOSIS; BRAIN; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; RNA; SCRAPIE; SHEEP;

EID: 67650976617     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1051/vetres/2009024     Document Type: Article

References (46)

1. Acin C., Martin-Burriel I., Monleon E., Rodellar C., Badiola J.J., Zaragoza P., PrP polymorphisms in Spanish sheep affected with natural scrapie, Vet. Rec. (2004) 155:370-372.
2. Bolea R., Monleon E., Schiller I., Raeber A.J., Acin C., Monzon M., et al., Comparison of immunohistochemistry and two rapid tests for detection of abnormal prion protein in different brain regions of sheep with typical scrapie, J. Vet. Diagn. Invest. (2005) 17:467-469. (Pubitemid 41414966)
3. Brenner C., Cadiou H., Vieira H.L., Zamzami N., Marzo I., Xie Z., et al., Bcl-2 and Bax regulate the channel activity of the mitochondrial adenine nucleotide translocator, Oncogene (2000) 19:329-336. (Pubitemid 30077332)
4. Budka H., Aguzzi A., Brown P., Brucher J.M., Bugiani O., Gullotta F., et al., Neuropathological diagnostic criteria for Creutzfeldt-Jakob disease (CJD) and other human spongiform encephalopathies (prion diseases), Brain Pathol. (1995) 5:459-466.
5. Cuconati A., Mukherjee C., Perez D., White E., DNA damage response and MCL-1 destruction initiate apoptosis in adenovirus-infected cells, Genes Dev. (2003) 17:2922-2932. (Pubitemid 37523156)
6. Choe W., Stoica G., Lynn W., Wong P.K., Neurodegeneration induced by MoMuLV-ts1 and increased expression of Fas and TNF-alpha in the central nervous system, Brain Res. (1998) 779:1-8. (Pubitemid 28039933)
7. Chou A.H., Yeh T.H., Kuo Y.L., Kao Y.C., Jou M.J., Hsu C.Y., et al., Polyglutamine-expanded ataxin-3 activates mitochondrial apoptotic pathway by upregulating Bax and downregulating Bcl-xL, Neurobiol. Dis. (2006) 21:333-345.
8. Diedrich J.F., Bendheim P.E., Kim Y.S., Carp R.I., Haase A.T., Scrapie-associated prion protein accumulates in astrocytes during scrapie infection, Proc. Natl. Acad. Sci. USA (1991) 88:375-379.
9. Elmore S., Apoptosis: a review of programmed cell death, Toxicol. Pathol. (2007) 35:495-516.
10. Ettaiche M., Pichot R., Vincent J.P., Chabry J., In vivo cytotoxicity of the prion protein fragment 106-126, J. Biol. Chem. (2000) 275:36487-36490.
11. Ferrer I., Puig B., Krupinsk J., Carmona M., Blanco R., Fas and Fas ligand expression in Alzheimer's disease, Acta Neuropathol. (2001) 102:121-131. (Pubitemid 32771659)
12. Gray F., Chretien F., Adle-Biassette H., Dorandeu A., Ereau T., Delisle M.B., et al., Neuronal apoptosis in Creutzfeldt-Jakob disease, J. Neuropathol. Exp. Neurol. (1999) 58:321-328.
13. Green D.R., Kroemer G., The pathophysiology of mitochondrial cell death, Science (2004) 305: 626-629.
14. Grell M., Zimmermann G., Hulser D., Pfizenmaier K., Scheurich P., TNF receptors TR60 and TR80 can mediate apoptosis via induction of distinct signal pathways, J. Immunol. (1994) 153:1963-1972. [15] Hardt M., Baron T., Groschup M.H., A comparative study of immunohistochemical methods for detecting abnormal prion protein with monoclonal and polyclonal antibodies, J. Comp. Pathol. (2000) 122:43-53. (Pubitemid 24256665)
15. Igney F.H., Krammer P.H., Death and anti-death: tumour resistance to apoptosis, Nat. Rev. Cancer (2002) 2:277-288.
16. Jamieson E., Jeffrey M., Ironside J.W., Fraser J.R., Apoptosis and dendritic dysfunction precede prion protein accumulation in 87V scrapie, Neuroreport (2001) 12:2147-2153. (Pubitemid 32646262)
17. Jia L., Srinivasula S.M., Liu F.T., Newland A.C., Fernandes-Alnemri T., Alnemri E.S., Kelsey S.M., Apaf-1 protein deficiency confers resistance to cytochrome c-dependent apoptosis in human leukemic cells, Blood (2001) 98:414-421.
18. Kim Y.S., Carp R.I., Callahan S., Wisniewski H.M., Incubation periods and histopathological changes in mice injected stereotaxically in different brain areas with the 87V scrapie strain, Acta Neuropathol. (Berl.) (1990) 80:388-392.
19. Kitamura Y., Shimohama S., Kamoshima W., Ota T., Matsuoka Y., Nomura Y., et al., Alteration of proteins regulating apoptosis, Bcl-2, Bcl-x, Bax, Bak, Bad, ICH-1 and CPP32, in Alzheimer's disease, Brain Res. (1998) 780:260-269.
20. Kroemer G., Zamzami N., Susin S.A., Mitochondrial control of apoptosis, Immunol. Today (1997) 18:44-51.
21. Lazarini F., Boussin F., Deslys J.P., Tardy M., Dormont D., Astrocyte gene expression in experimental mouse scrapie, J. Comp. Pathol. (1994) 111:87-98.
22. Liberski P.P., Sikorska B., Bratosiewicz-Wasik J., Gajdusek D.C., Brown P., Neuronal cell death in transmissible spongiform encephalopathies (prion diseases) revisited: from apoptosis to autophagy, Int. J. Biochem. Cell Biol. (2004) 36:2473-2490. (Pubitemid 39119760)
23. Lyahyai J., Bolea R., Serrano C., Vidal E., Pumarola M., Badiola J.J., et al., Differential expression and protein distribution of Bax in natural scrapie, Brain Res. (2007) 1180:111-120. (Pubitemid 350018739)
24. Martinez M., Fernandez-Vivancos E., Frank A., De la Fuente M., Hernanz A., Increased cerebrospinal fluid fas (Apo-1) levels in Alzheimer's disease. Relationship with IL-6 concentrations, Brain Res. (2000) 869:216-219.
25. Puig B., Ferrer I., Cell death signaling in the cerebellum in Creutzfeldt-Jakob disease, Acta Neuropathol. (2001) 102:207-215. (Pubitemid 32816140)
26. Roucou X., Giannopoulos P.N., Zhang Y., Jodoin J., Goodyer C.G., LeBlanc A., Cellular prion protein inhibits proapoptotic Bax conformational change in human neurons and in breast carcinoma MCF-7 cells, Cell Death Differ. (2005) 12:783-795. (Pubitemid 40945985)
27. Saas P., Boucraut J., QuiquerezA.L., SchnurigerV., Perrin G., Desplat-Jego S., et al., CD95 (Fas/Apo-1) as a receptor governing astrocyte apoptotic or inflammatory responses: a key role in brain inflammation? J. Immunol. (1999) 162:2326-2333. (Pubitemid 29288858)
28. Sajan F.D., Martiniuk F., Marcus D.L., Frey W.H. 2nd, Hite R., Bordayo E.Z., Freedman M.L., Apoptotic gene expression in Alzheimer's disease hippocampal tissue, Am. J. Alzheimers Dis. Other Demen. (2007) 22:319-328.
29. Sakudo A., Lee D.C., Saeki K., Matsumoto Y., Itohara S., Onodera T., Tumor necrosis factor attenuates prion protein-deficient neuronal cell death by increases in anti-apoptotic Bcl-2 family proteins, Biochem. Biophys. Res. Commun. (2003) 310: 725-729. (Pubitemid 37188680)
30. Santee S.M., Owen-Schaub L.B., Human tumor necrosis factor receptor p75/80 (CD120b) gene structure and promoter characterization, J. Biol. Chem. (1996) 271:21151-21159.
31. Sawada M., Brain cytokine network and novel characteristics of microglia, Nihon Shinkei Seishin Yakurigaku Zasshi (1999) 19:151-154 (in Japanese).
32. Shimizu S., Narita M., Tsujimoto Y., Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC, Nature (1999) 399:483-487. (Pubitemid 29258855)
33. Siso S., Puig B., Varea R., Vidal E., Acin C., Prinz M., et al., Abnormal synaptic protein expression and cell death in murine scrapie, Acta Neuropathol. (Berl.) (2002) 103:615-626.
34. Stobart M.J., Parchaliuk D., Simon S.L., Lemaistre J., Lazar J., Rubenstein R., Knox J.D., Differential expression of interferon responsive genes in rodent models of transmissible spongiform encephalopathy disease, Mol. Neurodegener. (2007) 2:5.
35. Stoka V., Turk V., Bredesen D.E., Differential regulation of the intrinsic pathway of apoptosis in brain and liver during ageing, FEBS Lett. (2006) 580:3739-3745. (Pubitemid 43902811)
36. Theil D., Fatzer R., Meyer R., Schobesberger M., Zurbriggen A., Vandevelde M., Nuclear DNA fragmentation and immune reactivity in bovine spongiform encephalopathy, J. Comp. Pathol. (1999) 121:357-367.
37. Van Everbroeck B., Dewulf E., Pals P., Lubke U., Martin J.J., Cras P., The role of cytokines, astrocytes, microglia and apoptosis in Creutzfeldt-Jakob disease, Neurobiol. Aging (2002) 23:59-64. (Pubitemid 34066536)
38. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F., Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes, Genome Biol. (2002) 3:RESEARCH0034.
39. Vargas F., Lujan L., Bolea R., Monleon E., Martin-Burriel I., Fernandez A., et al., Detection and clinical evolution of scrapie in sheep by 3rd eyelid biopsy, J. Vet. Intern. Med. (2006) 20:187-193. (Pubitemid 43219390)
40. Wang H.L., Yeh T.H., Chou A.H., Kuo Y.L., Luo L.J., He C.Y., et al., Polyglutamine-expanded ataxin-7 activates mitochondrial apoptotic pathway of cerebellar neurons by upregulating Bax and downregulating Bcl-x(L), Cell. Signal. (2006) 18:541-552.
41. Williams A., Lucassen P.J., Ritchie D., Bruce M., PrP deposition, microglial activation, and neuronal apoptosis in murine scrapie, Exp. Neurol. (1997) 144:433-438. (Pubitemid 27224571)
42. Wolf B.B., Schuler M., Li W., Eggers-Sedlet B., Lee W., Tailor P., et al., Defective cytochrome c-dependent caspase activation in ovarian cancer cell lines due to diminished or absent apoptotic protease activating factor-1 activity, J. Biol. Chem. (2001) 276:34244-34251.
43. Wyss-Coray T., Mucke L., Inflammation in neurodegenerative disease - a double-edged sword, Neuron (2002) 35:419-432. (Pubitemid 34879943)
44. Yakovlev A.G., Ota K., Wang G., Movsesyan V., Bao W.L., Yoshihara K., Faden A.I., Differential expression of apoptotic protease-activating factor-1 and caspase-3 genes and susceptibility to apoptosis during brain development and after traumatic brain injury, J. Neurosci. (2001) 21:7439-7446. (Pubitemid 32904942)
45. Yao M., Nguyen T.V., Pike C.J., Beta-amyloidinduced neuronal apoptosis involves c-Jun N-terminal kinase-dependent downregulation of Bcl-w, J. Neurosci. (2005) 25:1149-1158. (Pubitemid 40268956)
46. Zhou P., Qian L., Bieszczad C.K., Noelle R., Binder M., Levy N.B., Craig R.W., Mcl-1 in transgenic mice promotes survival in a spectrum of hematopoietic cell types and immortalization in the myeloid lineage, Blood (1998) 92:3226-3239. (Pubitemid 28492330)