Adenovirus-mediated gene transfer of inhibitors of apoptosis proteins delays apoptosis in cerebellar granule neurons

Journal of Neurochemistry

Volumn 72, Issue 1, 1999, Pages 292-301

  Simons, M ^a   Beinroth, S ^a   Gleichmann, M ^a   Liston, P ^b   Korneluk, R G ^b   MacKenzie, A E ^b   Bahr M ^a   Klockgether, T ^a   Robertson, G S ^c   Weller, M ^a   Schulz, J B ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b CHILDREN S HOSPITAL OF EASTERN ONTARIO   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Apoptosis; Caspases; Cerebellar granule neurons; Inhibitors of apoptosis

Indexed keywords

BETA GALACTOSIDASE; CASPASE; DIZOCILPINE; GLUTAMIC ACID; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; VIRUS VECTOR;

ADENOVIRUS; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CEREBELLUM; CONTROLLED STUDY; ENZYME ACTIVITY; GENE TRANSFER; GRANULE CELL; NERVE CELL NECROSIS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT;

ADENOVIRIDAE; ADENOVIRIDAE INFECTIONS; ANIMALS; APOPTOSIS; CASPASE 3; CASPASES; CELLS, CULTURED; CEREBELLUM; CYSTEINE PROTEINASE INHIBITORS; DNA FRAGMENTATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, VIRAL; GENE TRANSFER TECHNIQUES; IN SITU NICK-END LABELING; INHIBITOR OF APOPTOSIS PROTEINS; NEURONS; NEUROTOXINS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; VIRAL PROTEINS;

ADENOVIRIDAE; ANIMALIA; HEXAPODA; INTRACISTERNAL A-PARTICLES; UNIDENTIFIED BACULOVIRUS;

EID: 0032902337     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0720292.x     Document Type: Article

References (47)

1. Ambrosini G., Adida C., and Altieri D. C. (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat. Med. 3, 917-921.
2. Ankarcrona M., Dypbukt J. M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S. A., and Nicotera P. (1995) Glutamale-induced neuronal death: a succession of necrosis and apoptosis depending on mitochondrial function. Neuron 15, 961-973.
3. Armstrong R. C., Aja T. J., Hoang K. D., Gaur S., Bai X., Alnemri E. S., Litwack G., Karanewsky D. S., Fritz L. C., and Tomaselli K. J. (1997) Activation of the CED3/ICE-related protease CPP32 in cerebellar granule neurons undergoing apoptosis but not necrosis. J. Neurosci. 17, 553-562.
4. Boldin M. P., Goncharow T. M., Goltsev Y. V., and Wallach D. (1996) Involvement of MACH, a novel MORTI/FADD-interacting protease, in Fas/APO-1 and TNF receptor-induced cell death. Cell 85, 803-815.
5. Burgoyne R. D., Graham M. E., and Cambray D. M. (1993) Neurotrophic effects of NMDA receptor activation on developing cerebellar granule cells. J. Neurocytol. 22, 689-695.
6. Chu Z. L., McKinsey T. A., Liu L., Gentry J. J., Malim M. H., and Ballard D. W. (1997) Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-kappa B control. Proc. Natl. Acad. Sci. USA 94, 10057-10062.
7. Clem R. J. and Miller L. K. (1994) Control of programmed cell death by the baculovirus genes p35 and IAP. Mol. Cell. Biol. 14, 5212-5222.
8. Crook N, E., Clem R. J., and Miller L. K. (1993) An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol. 67, 2168-2174.
9. Deveraux Q. L., Takahashi R., Salvesen G. S., and Reed J. C. (1997) X-linked IAP is a direct inhibitor of cell-death proteases. Nature 388, 300-304.
10. D'Mello S. R., Galli C., Ciotti T., and Calissano P. (1993) Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin growth factor I and cAMP. Proc. Natl. Acad. Sci. USA 90, 10989-10993.
11. Du Y. S., Bales K. R., Dodel R. C., Hamilton-Byrd E., Horn J. W., Czilli D. L., Simmons L. K., Ni B. H., and Paul S. M. (1997) Activation of a caspase 3-related cysteine protease is required for glutamate-mediated apoptosis of cultered cerebellar granule neurons. Proc. Natl. Acad. Sci. USA 94, 11657-11662.
12. Duckett C. S., Nava V. E., Gedrich R. W., Clem R. J., VanDongen J. L., Gilfillan M. C., Shiels H., Hardwick J. M., and Thompson C. B. (1996) A conserved family of cellular genes related to the baculovirus IAP gene and encoding apoptosis inhibitors. EMBO J. 15, 2685-2694.
13. Eldadah B. A., Yakovlev A. G., and Faden A. I. (1997) The role of CED-3-related cysteine proteases in apoptosis of cerebellar granule cells. J. Neurosci. 17, 6105-6113.
14. Enari M., Hug H., and Nagata S. (1995) Involvement of an ICE-like protease in Fas-mediated apoptosis. Nature 375, 78-81.
15. Enari M., Sakahira H., Yokoyama H., Okawa K., Iwamatsu A., and Nagata S. (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391, 43-50.
16. Fritz J. D., Utz A. L., Hale N. M., Wu L., Powers A. C., Verdoorn T. A., and Robertson D. (1997) Gene-based neurotransmitter modulation in cerebellar granule neurons. J. Neurochem. 68, 204-212.
17. Gagliardini V., Fernandez P.-A., Lee R. K. K., Drexler H. C. A., Rotello R. J., Fishman M. C., and Yuan J. (1994) Prevention of vertebrate neuronal death by the crmA gene. Science 263, 826-828.
18. Galli C., Meucci O., Scorziella A., Werge T., Calissano P., and Schettini G. (1995) Apoptosis in cerebellar granule cells is blocked by high KCl, forskolin, and IGF-1 through distinct mechanisms of action: the involvement of intracellular calcium and RNA synthesis. J. Neurosci. 15, 1172-1179.
19. Gallo V., Kingsbury A., Balazs R., and Jorgensen O. S. (1987) The role of depolarization in the survival of cerebellar granule cells in culture. J. Neurosci. 7, 2203-2213.
20. Graham F. L. and van der Eb A. (1973) A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52, 456-467.
21. Hay B. A., Wassarman D. A., and Rubin G. M. (1995) Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83, 1253-1262.
22. Liston P., Roy N., Tamai K., Lefebvre C., Baird S., ChertonHorvat G., Farahani R., McLean M., Ikeda J. E., MacKenzie A., and Korneluk R. G. (1996) Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes. Nature 379, 349-353.
23. Loo D. T., Copani A., Pike C. J., Whittemore E. R., Walencewicz A. J., and Cotman C. W. (1993) Apoptosis is induced by β-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. USA 90, 7951-7955.
24. Los M., van de Craen M., Penning L. C., Schenk H., Westendorp M., Baeuerle P. A., Droge W., Krammer P. H., Fiers W., and Schulze-Osthoff K. (1995) Requirement of an ICE/CED-3 protease for FAS/APO-1-mediated apoptosis. Nature 275, 81-83.
25. Martinou I., Fernandez P.-A., Missotten M., White E., Allet B., Sadoul R., and Martinou J.-C. (1995) Viral proteins E1B19K and p35 protect sympathetic neurons from cell death induced by NGF deprivation. J. Cell Biol. 128, 201-208.
26. MillerT. M., Moulder K. L., Knudson C. M., Creedon D. J., Deshmukh M., Korsmeyer S. J., and Johnson E. M. (1997) Bax deletion further orders the cell death pathway in cerebellar granule cells and suggests a caspase-independent pathway to cell death. J. Cell Biol. 139, 205-217.
27. Miyake S., Makimura M., Kanegae Y., Harada S., Sato Y., Takamori K., Tokuda C., and Saito I. (1996) Efficient generation of recombinant adenoviruses using adenovirus DNA-terminal protein complex and a cosmid bearing the full-length virus genome. Proc. Natl. Acad. Sci. USA 93, 1320-1324.
28. Muzio M., Chinnaiyan A. M., Kisehkel F. C., O'Rourke K., Shevchenko A., Ni J., Scaffidi C., Bretz, J. D., Zhang M., Gentz R., Mann M., Krammer P. H., Peter M. E., and Dixit V. M. (1996) FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD 95 (Fas/APO-1) death-inducing signaling complex. Cell 85, 817-827.
29. Peng L., Juurlink B. H. J., and Hertz, L. (1991) Differences in transmitter release, morphology, and ischemia-induced cell injury between cerebellar granule cell cultures developing in the presence and in the absence of depolarizing potassium concentration. Dev. Brain Res. 63, 1-12.
30. Portera-Cailliau C. Hedreen J. C., Price D. L., and Koliatsos V. E. (1995) Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci. 15, 3775-3787.
31. Price J., Turner D., and Cepko C. (1987) Lineage analysis in the vertebrate nervous system by retrovirus-mediated gene transfer. Proc. Natl. Acad. Sci. USA 84, 156-160.
32. Rabizadeh S., Gralla E. B., Borchelt D. R., Gwinn R., Valentine J. S., Sisodia S., Wong P., Lee M., Hahn H., and Bredesen D. E. (1995) Mutations associated with amyotrophic lateral sclerosis convert superoxide dismutase from an antiapoptotic gene to a proapoptotic gene: studies in yeast and neural cells. Proc. Natl. Acad. Sci. USA 92, 3024-3028.
33. Rosenfeld M. A., Yoshimura K., Trapnell B. C., Yoneyama K., Rosenthal E. R., Dalemans W., Fukayama M., Bargon J., Stier L. E., and Stratford-Perricaudet L. (1992) In vivo transfer of the human cystic fibrosis transmembrane conductance regulator gene to the airway epithelium. Cell 68, 143-155.
34. Rothe M., Pan M. G., Henzel W. J., Ayres T. M., and Goeddel D. V. (1995) The TNFR2-TRAF signaling complex contains two novel proteins related to baculorival-inhihitor of apoptosis proteins. Cell 83, 1243-1252.
35. Roy N., Mahadevan M. S., McLean M., Shutler G., Yaraghi Z., Farahani R., Baird S., Besner-Johnston A., Lefebre C., Kang X., Salih M., Huguette A., Tamai K., Guan X., Ioannou P., Crawford T. O., de Jong P. J., Surth L., Ikeda J.-E., Korneluk R. G., and MacKenzie A. (1995) The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 80, 167-178.
36. Roy N., Deveraux Q. L., Takahashi R., Salvesen G. S., and Reed J. C. (1997) The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J. 16, 6914-6925.
37. Salvesen G. S. and Dixit V. M. (1997) Caspases: intracellular signaling by proteolysis. Cell 91, 443-446.
38. Schulz J. B., Weller M., and Klockgether T. (1996) Potassium deprivation-induced apoptosis of cerebellar granule neurons: a sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species. J. Neurosci. 16, 4696-4706.
39. Schulz J. B., Bremen D., Reed J. C., Lommatzsch J., Takayama S., Wüllner U., Löschmann P.-A., Klockgether T., and Weller M. (1997) Cooperative interception of neuronal apoptosis by BCL-2 and BAG-1 expression: prevention of caspase activation and reduced production of reactive oxygen species. J. Neurochem. 69, 2075-2086.
40. Slack R. S., Belliveau D. J., Rosenberg M., Atwal J., Lochmuller H., Aloys R., Haghighi A., Lach B., Seth P., Cooper E., and Miller F. D. (1996) Adenovirus-mediated gene transfer of the tumor suppressor, p53, induces apoptosis in postmitotic neurons. J. Cell Biol. 135, 1085-1096.
41. Uren A. G., Pakusch M., Hawkins C. J., Puls K. L., and Vaux D. L. (1996) Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or hind tumor necrosis factor receptor-associated factors. Proc. Natl. Acad. Sci. USA 93, 4974-4978.
42. Wang L., Miura M., Bergeron L., Zhu H., and Yuan J. (1994) Ice-I, an ICE/CED-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell 78, 739-750.
43. Weller M., Constam D. B., Malipiero U., and Fontana A. (1994a) Transforming growth factor-β2 induces apoptosis of murine T cell clones without down-regulating bcl-2 mRNA expression. Eur. J. Immunol. 24, 1293-1300.
44. Weller M., Montpied P., and Paul S. M. (1994b) NMDA receptor-mediated excitoprotection of cultured cerebellar granule neurons fails to alter glutamate-induced expression of c-fos and c-jun mRNAs. Mol. Brain Res. 22, 227-235.
45. 1β-converting enzyme-like proteases. Proc. Natl. Acad. Sci. USA 93, 14559-14563.
46. Xu D. G., Crocker S. J., Doucet J.-P., St. Jean M., Tamai K., Hakim A. M., Ikeda J.-E., Liston P., Thompson C. S., Korneluk R. G., MacKenzie A., and Robertson G. S. (1997) Elevation of neuronal expression of NAIP reduces ischemic damage in the rat hippocampus. Nat. Med. 3, 1-8.
47. Yan G.-M., Ni B., Weller M., Wood K., and Paul S. M. (1994) Depolarization or glutamate receptor activation blocks apoptotic cell death of cultured cerebellar granule neurons. Brain Res. 656, 43-51.