BCL-2 counteracts Doppel-induced apoptosis of prion-protein-deficient Purkinje cells in the Ngsk Prnp0/0 mouse

Developmental Neurobiology

Volumn 68, Issue 3, 2008, Pages 332-348

  Heitz, S ^a   Gautheron, V ^b   Lutz, Y ^c   Rodeau, J L ^a   Zanjani, H S ^b,d   Sugihara, I ^e   Bombarde, G ^a   Richard, F ^a   Fuchs, J P ^c   Vogel, M W ^d   Mariani, J ^b,f   Bailly, Y ^a  

^a Hopitaux Universitaires de Strasbourg   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSERM   (France)

^d MARYLAND PSYCHIATRIC RESEARCH CENTER   (United States)

^e TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^f HÔPITAL CHARLES FOIX   (France)

Author keywords

Apoptosis; BCL 2; Doppel; Neurodegeneration; Prion protein; Purkinje cell

Indexed keywords

DOPPEL PROTEIN; FRUCTOSE BISPHOSPHATE ALDOLASE; PRION PROTEIN; PROTEIN; PROTEIN BAX; PROTEIN BCL 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COMPARTMENTALIZATION; CELL DEATH; CELL SURVIVAL; CEREBELLUM CORTEX; CHRONIC INFLAMMATION; CONTROLLED STUDY; FEMALE; GENE DELETION; GENE OVEREXPRESSION; GLIA CELL; KNOCKOUT MOUSE; MALE; MOUSE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEOMICS; PURKINJE CELL; QUANTITATIVE ANALYSIS;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; CELL COUNT; CEREBELLUM; FRUCTOSE-BISPHOSPHATE ALDOLASE; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PRIONS; PROTO-ONCOGENE PROTEINS C-BCL-2; PURKINJE CELLS;

EID: 39349098259     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.20555     Document Type: Article

References (66)

1. Anderson L, Rossi D, Linehan J, Brandner S, Weissmann C. 2004. Transgene-driven expression of the doppel protein in Purkinje cells causes purkinje cell degeneration and motor impairment. Proc Natl Acad Sci USA 101:3644-3649.
2. Atarashi R, Sakaguchi S, Shigematsu K, Arima K, Okimura N, Yamaguchi N, Li A, et al. 2001. Abnormal activation of glial cells in the brains of prion protein-deficient mice ectopically expressing prion protein-like protein, PrPLP/Dpi. Mol Med 7:803-809.
3. Bailly Y, Haeberle AM, Blanquet-Grossard F, Chasserot-Golaz S, Grant N, Schulze T, Bombarde G, et al. 2004. Prion protein (PrPc) immunocytochemistry and expression of the green fluorescent protein reporter gene under control of the bovine PrP gene promoter in the mouse brain. J Comp Neurol 473:244-269.
4. Bailly Y, Schoen SW, Delhaye-Bouchaud N, Kreutzberg GW, Mariant J. 1995. 5′-Nucleotidase activity as a synaptic marker of parasagittal compartmentation in the mouse cerebellum. J Neurocytol 24:879-890.
5. Bounhar Y, Mann KK, Roucou X, LeBlanc AC. 2006. Prion protein prevents Bax-mediated cell death in the absence of other Bcl-2 family members in Saccharomyces cerevisiae. FEMS Yeast Res 6:1204-1212.
6. Bounhar Y, Zhang Y, Goodyer CG, LeBlanc A. 2001. Prion protein protects human neurons against Bax-mediated apoptosis. J Biol Chem 276:39145-39149
7. Büeler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, Weissmann C. 1993. Mice devoid of PrP are resistant to scrapie. Cell 73:1339-1347.
8. Cheng EH, Wei MC, Weiler S, Flavell RA, Mak TW, Lindsten T, Korsmeyer SJ. 2001. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX-and BAK-mediated mitochondrial apoptosis. Mol Cell 8:705-7011.
9. Chiesa R, Piccardo P, Ghetti B, Harris DA. 1998. Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron 21:1339-1351.
10. Cui T, Holme A, Sassoon J, Brown DR. 2003. Analysis of doppel protein toxicity. Mol Cell Neurosci 23:144-155.
11. Duchala CS, Shick HE, Garcia J, Deweese DM, Sun X, Stewart VJ, Macklin WB. 2004. The toppler mouse: A novel mutant exhibiting loss of Purkinje cells. J Comp Neurol 476:113-129.
12. Eisenman L, Hawkes R. 1993. Antigenic compartmentation in the mouse cerebellar cortex: Zebrin and HNK-1 reveal a complex, overlapping molecular topography. J Comp Neurol 335:586-605.
13. Flechsig E, Hegyi I, Leimeroth R, Zuniga A, Rossi D, Cozzio A, Schwarz P, et al. 2003. Expression of truncated PrP targeted to Purkinje cells of PrP knockout mice causes Purkinje cell death and ataxia. EMBO J 22:3095-3101.
14. Fournier JG, Escaig-Haye F, Grigoriev V. 2000. Ultrastructural localization of prion proteins: Physiological and pathological implications. Microsc Res Tech 50:76-88.
15. Giffard RG, Swanson RA. 2005. Ischemia-induced programmed cell death in astrocytes. Glia 50:299-306.
16. Gravel C, Eisenman L, Sasseville R, Hawkes R. 1987. Parasagittal organization of the rat cerebellar cortex: Direct correlation between antigenic Purkinje cell bands revealed by mabQ113 and the organization of the olivocerebellar projection. J Comp Neurol 265:294-310.
17. Gross A, McDonnell JM, Korsmeyer SJ. 1999. BCL-2 family members and the mitochondria in apoptosis. Genes Dev 13:1899-1911.
18. Hara A, Hirose Y, Wang A, Yoshimi N, Tanaka T, Mori H. 1996. Localization of Bax and Bcl-2 proteins, regulators of programmed cell death, in the human central nervous system. Virchows Arch 429:249-253.
19. Hawkes R, Leclerc N. 1987. Antigenic map of the rat cerebellar cortex: The distribution of parasagittal bands as revealed by monoclonal anti-Purkinje cell antibody mabQ113. J Comp Neurol 256:29-41.
20. Heitz S, Lutz Y, Rodeau J-L, Zanjani H, Gautheron V, Bombarde G, Richard F, et al. 2007. BAX contributes to doppel-induced apoptosis of prion protein-deficient Purkinje cells. Dev Neurobiol 67:670-686.
21. Hendry IA. 1976. A method to correct adequately for the change in neuronal size when estimating neuronal numbers after nerve growth factor treatment. J Neurocytol 5:337-349.
22. Herrup K, Sunter K. 1986. Cell lineage dependent and independent control of Purkinje cell number in the mammalian CNS: Further quantitative studies of lurcher chimeric mice. Dev Biol 117:417-427.
23. Hsu SM, Raine L, Fanger H. 1981. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase technics. J Histochem Cytochem 29:577-580.
24. Imura T, Shimohama S. 2000. Opposing effects of adenosine on the survival of glial cells exposed to chemical ischemia. J Neurosci Res 62:539-546.
25. Kurschner C, Morgan JI. 1995. The cellular prion protein (PrP) selectively binds to Bcl-2 in the yeast two-hybrid system. Brain Res Mol Brain Res 30:165-168.
26. Kuwahara C, Takeuchi A, Nishimura T, Haraguchi K, Kubosaki A, Matsumoto Y, Saeki K, et al. 1999. Prions prevent neuronal cell-line death. Nature 400:225-226.
27. Lee DC, Sakudo A, Kim CK, Nishimura T, Saeki K, Matsumoto Y, Yokoyama T, et al. 2006. Fusion of doppel to octapeptide repeat and N-terminal half of hydrophobic region of prion protein confers resistance to serum deprivation. Microbiol Immunol 50:203-209.
28. Li A, Barmada S, Roth K, Harris D. 2007. N-terminally deleted forms of the prion protein activate botch Bax-dependent and Bax-independent neurotoxic pathways. J Neurosci 27:852-859
29. Li A, Harris DA. 2005. Mammalian prion protein suppresses BAX-induced cell death in yeast. J Biol Chem 280:17430-17434.
30. Li A, Sakaguchi S, Ryuichiro A, Bhabesh CR, Ryota N, Kazuhiko A, Nobuhiko O, et al. 2000. Identification of a novel gene encoding a PrP-like protein expressed as chimeric transcripts fused to PrP exon 1/2 in ataxic mouse line with a disrupted PrP gene. Cell Mol Biol 20:553-567.
31. Ma J, Lindquist S. 2001. Wild-type PrP and a mutant associated with prion disease are subject to retrograde transport and proteasome degradation. Proc Natl Acad Sci USA 98:14955-14960.
32. Mallucci G, Dickinson A, Linehan J, Klöhn P-C, Brandner S, Collinge J. 2003. Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302:871-874.
33. Manson JC, Clarke AR, Hooper ML, Aitchison L, McConnell I, Hope J. 1994. 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol Neurobiol 8:121-127.
34. Martinou JC, Dubois-Dauphin M, Staple JK, Rodriguez I, Frankowski H, Missotten M, Albertini P, et al. 1994. Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13:1017-1030.
35. Massimino ML, Ballarin C, Bertolt A, Casonato S, Genovesi S, Negro A, Sorgato MC. 2004. Human doppel and prion protein share common membrane microdomains and internalization pathways. Int J Biochem Cell Biol 36:2016-2031.
36. Moore RC, Lee IT, Bouzamondo E, Silverman GL, Harisson PM, Strome R, Heinrich C, et al. 1999. Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein doppel. J Mol Biol 292:797-817.
37. Moore RC, Mastrangelo P, Bouzamondo E, Heinrich C, Legname G, Prusiner SB, Hood L, et al. 2001. Doppel-induced cerebellar degeneration in transgenic mice. Proc Natl Acad Sci USA. 98:15288-15293.
38. Moore RC, Redhead NJ, Selfridge J, Hope J, Manson JC, Melton DW. 1995. Double replacement gene targeting for the production of a series of mouse strains with different prion protein gene alterations. Biotechnology (NY) 13:999-1004.
39. Nishida N, Tremblay P, Sugimoto T, Shigematsu K, Shirabe S, Petromilli C, Erpel SP, et al. 1999. A mouse prion protein transgene rescues mice deficient for the prion protein gene from Purkinje cell degeneration and demyelination. Lab Invest 79:689-697.
40. Oltvai ZN, Milliman CL, Korsmeyer SJ. 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619.
41. Prusiner SB. 1998. Prions. Proc Natl Acad Sci USA 95:13363-13383.
42. Qin K, Coomaraswamy J, Mastrangelo P, Yang Y, Lugowski S, Petromilli C, Prusiner SB, et al. 2003. The PrP-like protein Doppel binds copper. J Biol Chem 278: 8888-8896.
43. Rossi D, Cozzio A, Flechsig E, Klein MA, Rulicke T, Aguzzi A, Weissmann C. 2001. Onset of ataxia and Purkinje cell loss in PrP null mice inversely correlated with Dpl level in brain. EMBO J 20:694-702.
44. Roucou X, Gains M, LeBlanc AC. 2004. Neuroprotective functions of prion protein. J Neurosci Res 75:153-161.
45. Roucou X, Giannopoulos PN, Zhang Y, Jodoin J, Goodyer CG, LeBlanc A. 2005. Cellular prion protein inhibits proapoptotic Bax conformational change in human neurons and in breast carcinoma MCF-7 cells. Cell Death Differ 12:783-795.
46. Roucou X, Guo Q, Zhang Y, Goodyer CG, LeBlanc AC. 2003. Cytosolic prion protein is not toxic and protects against Bax-mediated cell death in human primary neurons. J Biol Chem 278:40877-40881.
47. Sakaguchi S, Katamine S, Nishida N, Moriuchi R, Shigematsu K, Sugimoto T, Nakatani A, et al. 1996. Loss of cerebellar purkinje cells in aged mice homozygous for a disrupted PrP gene. Nature 380:528-531.
48. Sakaguchi S, Katamine S, Shigematsu K, Nakatani A, Moriuchi R, Nishida N, Kurokawa K, et al. 1995. Accumulation of proteinase K-resistant prion protein (PrP) is restricted by the expression level of normal PrP in mice inoculated with a mouse-adapted strain of the Creutzfeldt-Jakob disease agent. J Virol 69:7586-75892.
49. Sakudo A, Lee DC, Nakamura I, Taniuchi Y, Saeki K, Matsumoto Y, Itohara S, et al. 2005. Cell-autonomous PrP-Doppel interaction regulates apoptosis in PrP gene-deficient neuronal cells. Biochem Biophys Res Commun 333:448-454.
50. Shin C-M, Chung YH, Kim MJ, Shin DH, Kim YS, Gurney ME, Lee KW, et al. 2000. Immunohistochemical study on the distribution of Bcl-2 and Bax in the central nervous system of the transgenic mice expressing a human Cu/Zn SOD mutation. Brain Res 887:309-315.
51. Shmerling D, Hegyi I, Fischer M, Blattler T, Brandner S, Gotz J, Rulicke T, et al. 1998. Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions. Cell 93:203-214.
52. Silverman GL, Qin K, Moore RC, Yang Y, Mastrangelo P, Tremblay P, Prusiner SB, et al. 2000. Doppel is an N-glycosylated, glycosylphosphatidylinositol-anchored protein. Expression in testis and ectopic production in the brains of Prnp(0/0) mice predisposed to purkinje cell loss. J Biol Chem 275:26834-26841.
53. Sugihara I, Quy PN. 2007. Identification of aldolase C compartments in the mouse cerebellar cortex by olivocerebellar labelling. J Comp Neurol 500:1076-1092.
54. Sugihara I, Shinoda Y. 2004. Molecular, topographic, and functional organization of the cerebellar cortex: A study with combined aldolase C and olivocerebellar labeling. J Neurosci 24:8771-8785.
55. Tsujimoto Y, Croce CM. 1986. Analysis of the structure, transcripts, and protein products of bcl-2, the gene involved in human follicular lymphoma. Proc Natl Acad Sci USA 83:5214-5218.
56. Voogd J, Ruigrok TJ. 2004. The organization of the corticonuclear and olivocerebellar climbing fiber projections to the rat cerebellar vermis: The congruence of projection zones and the zebrin pattern. J Neurocytol 33:5-21.
57. Wassef M, Cholley B, Heizmann CW, Sotelo C. 1992. Development of the olivocerebellar projection in the rat. II. Matching of the developmental compartmentations of the cerebellum and inferior olive through the projection map. J Comp Neurol 323:537-550.
58. Weissmann C, Aguzzi A. 1999. PrP double causes trouble. Science 286:914-915.
59. Wetts R, Herrup K. 1982. Cerebellar Purkinje cells are descended from a small number of progenitors committed during early development: Quantitative analysis of lurcher chimeric mice. J Neurosci 2:1494-1498.
60. Wong BS, Liu T, Paisley D, Li R, Pan T, Chen SG, Perry G, et al. 2001. Induction of HO-1 and NOS in doppel-expressing mice devoid of PrP: Implications for doppel function. Mol Cell Neurosci 17:768-775.
61. Yamaguchi N, Sakaguchi S, Shigematsu K, Okimura N, Katamine S. 2004. Doppel-induced Purkinje cell death is stoichiometrically abrogated by prion protein. Biochem Biophys Res Commun 319:1247-1252.
62. Yedidia Y, Horontchik L, Tzaban S, Yanai A, Taraboulos A. 2001. Proteasomes and ubiquitin are involved in the turnover of the wild-type prion protein. EMBO J 20:5383-5391.
63. Yin XM, Oltvai ZN, Korsmeyer SJ. 1994. BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369:321-323.
64. Yokoyama T, Kimura KM, Ushiki Y, Yamada S, Morooka A, Nakashiba T, Sassa T, et al. 2001. In vivo conversion of cellular prion protein to pathogenic isoforms, as monitored by conformation-specific antibodies. J Biol Chem 276:11265-11271.
65. Zanjani H, Lemaigre-Dubreuil Y, Tillakaratne NJ, Blokhin A, McMahon RP, Tobin AJ, Vogel MW, et al. 2004. Cerebellar Purkinje cell loss in aging Hu-bcl-2 transgenic mice. J Comp Neurol 475:481-492.
66. Zanjani HS, Vogel MW, Delhaye-Bouchaud N, Martinou JC, Mariant J. 1996. Increased cerebellar Purkinje cell numbers in mice overexpressing a human bcl-2 transgene. J Comp Neurol 374:332-341.