Expression of X-chromosome linked inhibitor of apoptosis protein in mature purkinje cells and in retinal bipolar cells in transgenic mice induces neurodegeneration

Neuroscience

Volumn 156, Issue 3, 2008, Pages 515-526

  Korhonen, L ^a,b   Hansson, I ^a   Maugras, C ^c,d   Wehrle, R ^c,d   Kairisalo, M ^a   Borgkvist, A ^e   Jokitalo, E ^f   Sotelo, C ^c,d,g   Fisone, G ^e   Dusart, I ^c,d   Lindholm, D ^a,b  

^a MINERVA FOUNDATION INSTITUTE FOR MEDICAL RESEARCH   (Finland)

^b UPPSALA UNIVERSITY   (Sweden)

^c CNRS   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e KAROLINSKA INSTITUTE   (Sweden)

^f UNIVERSITY OF HELSINKI   (Finland)

^g MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

ataxia; cerebellum; Jun N terminal kinase; Purkinje cell; retinal bipolar cells; XIAP

Indexed keywords

PROTEIN BAX; PROTEIN C JUN; X LINKED INHIBITOR OF APOPTOSIS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; CELL COUNT; CELL DEATH; CELL DEGENERATION; CELL ORGANELLE; CELL STRESS; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME PHOSPHORYLATION; GENE DELETION; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PURKINJE CELL; RETINA; RETINA BIPOLAR GANGLION CELL; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ATAXIA; BCL-2-ASSOCIATED X PROTEIN; BEHAVIOR, ANIMAL; CEREBELLUM; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, SCANNING; NERVE DEGENERATION; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-JUN; PURKINJE CELLS; RETINAL BIPOLAR CELLS; TRANSFECTION; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 53249109343     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.08.005     Document Type: Article

References (49)

1. Behrens A., Sibilia M., and Wagner E.F. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat Genet 21 (1999) 326-329
2. Bernstein M., and Lichtman J.W. Axonal atrophy: the retraction reaction. Curr Opin Neurobiol 9 (1999) 364-370
3. Borsello T., Croquelois K., Hornung J.P., and Clarke P.G. N-methyl-d-aspartate-triggered neuronal death in organotypic hippocampal cultures is endocytic, autophagic and mediated by the c-Jun N-terminal kinase pathway. Eur J Neurosci 18 (2003) 473-485
4. Buffo A., Zagrebelsky M., Huber A.B., Skerra A., Schwab M.E., Strata P., and Rossi F. Application of neutralizing antibodies against NI-35/250 myelin-associated neurite growth inhibitory proteins to the adult rat cerebellum induces sprouting of uninjured Purkinje cell axons. J Neurosci 20 (2000) 2275-2286
5. Carter R.J., Lione L.A., Humby T., Mangiarini L., Mahal A., Bates G.P., Dunnett S.B., and Morton A.J. Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J Neurosci 19 (1999) 3248-3257
6. Celio M.R. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35 (1990) 375-475
7. Cory S., and Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2 (2002) 647-656
8. Deveraux Q.L., Takahashi R., Salvesen G.S., and Reed J.C. X-linked IAP is a direct inhibitor of cell-death proteases. Nature 388 (1997) 300-304
9. Dong J., Li A., Yamaguchi N., Sakaguchi S., and Harris D.A. Doppel induces degeneration of cerebellar Purkinje cells independently of Bax. Am J Pathol 171 (2007) 599-607
10. Dumesnil-Bousez N., and Sotelo C. Early development of the lurcher cerebellum: Purkinje cell alterations and impairment of synaptogenesis. J Neurocytol 21 (1992) 506-529
11. Dusart I., and Sotelo C. Lack of Purkinje cell loss in adult rat cerebellum following protracted axotomy: degenerative changes and regenerative attempts of the severed axons. J Comp Neurol 347 (1994) 211-232
12. Dusart I., Guenet J.L., and Sotelo C. Purkinje cell death: Differences between developmental cell death and neurodegenerative death in mutant mice. Cerebellum 5 (2006) 163-173
13. Fan H., Favero M., and Vogel M.W. Elimination of Bax expression in mice increases cerebellar Purkinje cell numbers but not the number of granule cells. J Comp Neurol 436 (2001) 82-91
14. Feddersen R.M., Ehlenfeldt R., Yunis W.S., Clark H.B., and Orr H.T. Disrupted cerebellar cortical development and progressive degeneration of Purkinje cells in SV40 T antigen transgenic mice. Neuron 9 (1992) 955-966
15. Fernandez-Gonzalez A., La Spada A.R., Treadaway J., Higdon J.C., Harris B.S., Sidman R.L., Morgan J.I., and Zuo J. Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science 295 (2002) 1904-1906
16. Ghoumari A.M., Wehrle R., Bernard O., Sotelo C., and Dusart I. Implication of Bcl-2 and caspase-3 in age-related Purkinje cell death in murine organotypic culture: an in vitro model to study apoptosis. Eur J Neurosci 12 (2000) 2935-2949
17. Gonzales Curto G.G., Lara J.M., Parrilla M., Aijón J., and Velasco A. Modifications of the retina neuronal populations of the heterozygous mutant small eye mouse, the Sey(Dey). Brain Res 1127 (2007) 163-176
18. Haverkamp S., and Wässle H. Immunocytochemical analysis of the mouse retina. J Comp Neurol 424 (2000) 1-23
19. Herrup K., and Kuemerle B. The compartmentalization of the cerebellum. Annu Rev Neurosci 20 (1997) 61-90
20. Hogan B., Constantini F., and Lacy E. Manipulating the mouse embryo: a laboratory manual (1986), Cold Spring Harbor Press, Cold Spring Harbor, NY
21. Kairisalo M., Korhonen L., Blomgren K., and Lindholm D. X-linked inhibitor of apoptosis protein increases mitochondrial antioxidants through NF-κB activation. Biochem Biophys Res Commun 364 (2007) 138-144
22. Knudson C.M., Tung K.S., Tourtellotte W.G., Brown G.A., and Korsmeyer S.J. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270 (1995) 96-99
23. Korhonen L., Belluardo N., and Lindholm D. Regulation of X-chromosome linked inhibitor of apoptosis protein in kainic acid induced neuronal death in the rat hippocampus. Mol Cell Neurosci 17 (2001) 364-372
24. Korhonen L., Hansson I., Kukkonen J., Brännvall K., Kobayashi M., Takamatsu K., and Lindholm D. Hippocalcin protects against caspase-12-induced and age-dependent neuronal degeneration. Mol Cell Neurosci 28 (2005) 85-95
25. Li J., Ma Y., Teng Y.D., Zheng K., Vartanian T.K., Snyder E.Y., and Sidman R.L. Purkinje neuron degeneration in nervous (nr) mutant mice is mediated by a metabolic pathway involving excess tissue plasminogen activator. Proc Natl Acad Sci U S A 103 (2006) 7847-7852
26. Lindholm D., Castrén E., Tsoulfas P., Kolbeck R., da Penha Berzaghi M., Leingärtner A., Heisenberg C.P., Tessarollo L., Parada L.F., and Thoenen H. Neurotrophin-3 induced by tri-iodothyronine in cerebellar granule cells promotes Purkinje cell differentiation. J Cell Biol 122 (1993) 443-450
27. Lindholm D., Wootz H., and Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ 13 (2006) 385-392
28. Marin-Teva J.L., Dusart I., Colin C., Gervais A., van Rooijen N., and Mallat M. Microglia promote the death of developing Purkinje cells. Neuron 41 (2004) 535-547
29. Mullen R.J., Eicher E.M., and Sidman R.L. Purkinje cell degeneration, a new neurological mutation in the mouse. Proc Natl Acad Sci U S A 73 (1976) 208-212
30. Nusser Z., Sieghart W., Stephenson F.A., and Somogyi P. The alpha 6 subunit of the GABAA receptor is concentrated in both inhibitory and excitatory synapses on cerebellar granule cells. J Neurosci 16 (1996) 103-114
31. Oberdick J., Smeyne R.J., Mann J.R., Zachsa S., and Morgan J.L. A promoter that drives transgene expression in cerebellar Purkinje cells and retinal bipolar neurons. Science 248 (1990) 223-226
32. Orr H.T. Into the depths of ataxia. J Clin Invest 113 (2004) 505-507
33. Reijonen S., Putkonen N., Nørremølle A., Lindholm D., and Korhonen L. Inhibition of endoplasmic reticulum stress counteracts neuronal cell death and protein aggregation caused by N-terminal mutant huntingtin proteins. Exp Cell Res 314 (2008) 950-960
34. Sanna M.G., Duckett C.S., Richter B.W., Thompson C.B., and Ulevitch R.J. Selective activation of JNK1 is necessary for the anti-apoptotic activity of hILP. Proc Natl Acad Sci U S A 95 (1998) 6015-6020
35. Selimi F., Lohof A.M., Heitz S., Lalouette A., Jarvis C.I., Bailly Y., and Mariani J. Lurcher GRID2-induced death and depolarization can be dissociated in cerebellar Purkinje cells. Neuron 37 (2003) 813-819
36. Sotelo C. Axonal abnormalities in cerebellar Purkinje cells of the hyperspiny Purkinje cell mutant mouse. J Neurocytol 19 (1990) 737-755
37. Sotelo C. Cellular and genetic regulation of the development of the cerebellar system. Prog Neurobiol 72 (2004) 295-339
38. Sun W., Gould T.W., Newbern J., Milligan C., Choi S.Y., Kim H., and Oppenheim R.W. Phosphorylation of c-Jun in avian and mammalian motoneurons in vivo during programmed cell death: an early reversible event in the apoptotic cascade. J Neurosci 25 (2005) 5595-5603
39. Takei K., Mignery G.A., Mugnaini E., Sudhof T.C., and De Camilli P. Inositol 1,4,5-trisphosphate receptor causes formation of ER cisternal stacks in transfected fibroblasts and in cerebellar Purkinje cells. Neuron 12 (1994) 327-342
40. Trapp T., Korhonen L., Besselmann M., Martinez R., Mercer E.A., and Lindholm D. Transgenic mice overexpressing XIAP in neurons show better outcome after transient cerebral ischemia. Mol Cell Neurosci 23 (2003) 302-313
41. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., and Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287 (2000) 664-666
42. Vaux D.L., and Silke J. IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol 6 (2005) 287-297
43. Wassef M., Zanetta J.P., Brehier A., and Sotelo C. Transient biochemical compartmentalization of Purkinje cells during early cerebellar development. Dev Biol 111 (1985) 129-137
44. Whitfield J., Neame S.J., Paquet L., Bernard O., and Ham J. Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29 (2001) 629-643
45. Yu L.Y., Jokitalo E., Sun Y.F., Mehlen P., Lindholm D., Saarma M., and Arumae U. GDNF-deprived sympathetic neurons die via a novel nonmitochondrial pathway. J Cell Biol 163 (2003) 987-997
46. Yuan J., Lipinski M., and Degterev A. Diversity in the mechanisms of neuronal cell death. Neuron 40 (2003) 401-413
47. Yue Z., Horton A., Bravin M., DeJager P.L., Selimi F., and Heintz N. A novel protein complex linking the delta 2 glutamate receptor and autophagy: implications for neurodegeneration in lurcher mice. Neuron 35 (2002) 921-933
48. Zanjani H.S., Vogel M., Delhaye-Bouchaud N., Martinou J.C., and Mariani J. Increased cerebellar Purkinje cell numbers in mice overexpressing a human bcl-2 transgene. J Comp Neurol 374 (1996) 332-341
49. Zuo J., De Jager P.L., Takahashi K.A., Jiang W., Linden D.J., and Heintz N. Neurodegeneration in lurcher mice caused by mutation in delta2 glutamate receptor gene. Nature 388 (1997) 769-777