In vivo analysis reveals different apoptotic pathways in pre- and postmigratory cerebellar granule cells of rabbit

Journal of Neurobiology

Volumn 60, Issue 4, 2004, Pages 437-452

  Lossi, Laura ^a   Gambino, Graziana ^a   Mioletti, Silvia ^a   Merighi, Adalberto ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Apoptosis; Cell cycle; Cerebellum; Checkpoint kinase; Programmed cell death; Retinoblastoma protein

Indexed keywords

CASPASE 3; CASPASE 7; CASPASE 9; CHECKPOINT KINASE 1; DNA FRAGMENT; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN KINASE; PROTEIN P85; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE; CELL MATURATION; CELL MIGRATION; CEREBELLUM; ELECTRON MICROSCOPY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GRANULE CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MICROSCOPY; NEWBORN; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; RABBIT; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CASPASE 3; CASPASES; CELL CYCLE; CELL DIFFERENTIATION; CELL MOVEMENT; CEREBELLAR CORTEX; GENES, CDC; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; PHOSPHORYLATION; PROTEIN KINASES; PROTEINS; RABBITS; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 4243198219     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.20032     Document Type: Article

References (67)

1. Allsopp TE, McLuckie J, Kerr LE, Macleod M, Sharkey J, Kelly JS. 2000. Caspase 6 activity initiates caspase 3 activation in cerebellar granule cell apoptosis. Cell Death Differ 7:984-993.
2. Alnemri ES, Livingston JN, Nicholson DW, Salvesen G, Thomberry NA, Wong WW, Yuan J. 1996. Human ICE/CED-3 protease nomenclature. Cell 87:171-181.
3. Altman J. 1972. Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer. J Comp Neurol 145:353-398.
4. Altman J, Bayer SA. 1997. Development of the cerebellar system in relation to its evolution, structure and functions. Boca Raton: CRC Press. 783 p.
5. Arendt T. 2001. Alzheimer's disease as a disorder of mechanisms underlying structural brain self-organization. Neuroscience 102:723-765.
6. Arendt T. 2002. Dysregulation of neuronal differentiation and cell cycle control in Alzheimer's disease. J Neural Transm Suppl 66:77-85.
7. Bartek J, Lukas J. 2001. Mammalian G1- and S-phase checkpoints in response to DNA damage. Curr Opin Cell Biol 13:738-747.
8. Borner C, Monney L. 1999. Apoptosis without caspases: an inefficient molecular guillotine? Cell Death Differ 6:497-507.
9. Boutillier AL, Trinh E, Loeffler JP. 2000. Caspase-dependent cleavage of the retinoblastoma protein is an early step in neuronal apoptosis. Oncogene 19:2171-2178.
10. Brodal A. 1940. The cerebellum of rabbit: a topographical atlas of the folia as revealed in transverse sections. J Comp Neurol 72:63-81.
11. Bu B, Li J, Davies P, Vincent I. 2002. Deregulation of cdk5, hyperphosphorylation, and cytoskeletal pathology in the Niemann-Pick type C murine model. J Neurosci 22:6515-6525.
12. Bulavin DV, Amundson SA, Fornace AJ. 2002. p38 and Chk1 kinases: different conductors for the G(2)/M checkpoint symphony. Curr Opin Genet Dev 12:92-97.
13. Busser J, Geldmacher DS, Herrup K. 1998. Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J Neurosci 18:2801-2807.
14. Callaghan DA, Dong L, Callaghan SM, Hou YX, Dagnino L, Slack RS. 1999. Neural precursor cells differentiating in the absence of Rb exhibit delayed terminal mitosis and deregulated E2F 1 and 3 activity. Dev Biol 207:257-270.
15. Calof AL, Hagiwara N, Holcomb JD, Mumm JS, Shou J. 1996. Neurogenesis and cell death in olfactory epithelium. J Neurobiol 30:67-81.
16. Chen Y, McPhie DL, Hirschberg J, Neve RL. 2000. The amyloid precursor protein-binding protein APP-BP1 drives the cell cycle through the S-M checkpoint and causes apoptosis in neurons. J Biol Chem 275:8929-8935.
17. Copani A, Condorelli F, Caruso A, Vancheri C, Sala A, Giuffrida Stella AM, Canonico PL, Nicoletti F, Sortino MA. 1999. Mitotic signaling by beta-amyloid causes neuronal death. FASEB J 13:2225-2234.
18. Dou QP, An B. 1998. RB and apoptotic cell death. Front Biosci 3:d419-d430.
19. Dranovsky A, Vincent I, Gregori L, Schwarzman A, Colflesh D, Enghild J, Strittmatter W, Davies P, Goldgaber D. 2001. Cdc2 phosphorylation of nucleolin demarcates mitotic stages and Alzheimer's disease pathology. Neurobiol Aging 22:517-528.
20. Elward K, Gasque P. 2003. "Eat me" and "don't eat me" signals govern the innate immune response and tissue repair in the CNS: emphasis on the critical role of the complement system. Mol Immunol 40:85-94.
21. m1 ganglioside. Involvement of Trk neurotrophin receptors. J Biol Chem 270:3074-3080.
22. Fraser A, Evan G. 1996. A license to kill. Cell 85:781-784.
23. Gerhardt E, Kugler S, Leist M, Beier C, Berliocchi L, Volbracht C, Weller M, Bahr M, Nicotera P, Schulz JB. 2001. Cascade of caspase activation in potassium-deprived cerebellar granule neurons: targets for treatment with peptide and protein inhibitors of apoptosis. Mol Cell Neurosci 17:717-731.
24. Gould E, McEwen BS. 1993. Neuronal birth and death. Curr Opin Neurobiol 3:676-682.
25. Gundersen HJG, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, et al. 1988. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Acta Pathol Microbiol Immunol Scand 96:379-394.
26. Ha HC, Snyder SH. 2000. Poly(ADP-ribose) polymerase-1 in the nervous system. Neurobiol Dis 7:225-239.
27. Hatten ME. 1990. Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci 13:179-184.
28. Herrup K, Busser JC. 1995. The induction of multiple cell cycle events precedes target-related neuronal death. Development 121:2385-2395.
29. Katchanov J, Harms C, Gertz K, Hauck L, Waeber C, Hirt L, Priller J, von HR, Bruck W, Hormagl H, et al. 2001. Mild cerebral ischemia induces loss of cyclin-dependent kinase inhibitors and activation of cell cycle machinery before delayed neuronal cell death. J Neurosci 21:5045-5053.
30. Lee EY, Hu N, Yuan SS, Cox LA, Bradley A, Lee WH, Herrup K. 1994. Dual roles of the retinoblastoma protein in cell cycle regulation and neuron differentiation. Genes Dev 8:2008-2021.
31. Liu DX, Greene LA. 2001. Neuronal apoptosis at the G1/S cell cycle checkpoint. Cell Tissue Res 305:217-228.
32. Lossi L, Ghidella S, Marroni P, Merighi A. 1995. The neurochemical maturation of the rabbit cerebellum. J Anat 187:709-722.
33. Lossi L, Mioletti S, Merighi A. 2002. Synapse-independent and synapse-dependent apoptosis of cerebellar granule cells in postnatal rabbits occur at two subsequent but partly overlapping developmental stages. Neuroscience 112:509-523.
34. Lundberg AS, Weinberg RA. 1998. Functional inactivation of the retinoblastoma protein requires sequential modification by at least two distinct cyclin-cdk complexes. Mol Cell Biol 18:753-761.
35. Lynch T, Vasilakos JP, Raser K, Keane KM, Shivers BD. 1997. Inhibition of the interleukin-1 beta converting enzyme family rescues neurons from apoptotic death. Mol Psychiatry 2:227-238.
36. Magnus T, Chan A, Savill J, Toyka KV, Gold R. 2002. Phagocytotic removal of apoptotic, inflammatory lymphocytes in the central nervous system by microglia and its functional implications. J Neuroimmunol 130:1-9.
37. Melo J, Toczyski D. 2002. A unified view of the DNA-damage checkpoint. Curr Opin Cell Biol 14:237-245.
38. Migheli A, Piva R, Casolino S, Atzori C, Dlouhy SR, Ghetti B. 1999. A cell cycle alteration precedes apoptosis of granule cell precursors in the weaver mouse cerebellum. Am J Pathol 155:365-373.
39. Oppenheim RW. 1985. Naturally occurring cell death during neural development. Trends Neurosci 8:487-493.
40. Oppenheim RW. 1991. Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
41. Padmanabhan J, Park DS, Greene LA, Shelanski ML. 1999. Role of cell cycle regulatory proteins in cerebellar granule neuron apoptosis. J Neurosci 19:8747-8756.
42. Park DS, Morris EJ, Greene LA, Geller HM. 1997. G1/S cell cycle blockers and inhibitors of cyclin-dependent kinases suppress camptothecin-induced neuronal apoptosis. J Neurosci 17:1256-1270.
43. Raff MC, Barres BA, Burne JF, Coles HSR, Ishizaki Y, Jacobson MD. 1994. Programmed cell death and the control of cell survival. Philos Trans R Soc Lond [Biol] 345:265-268.
44. Rakic P. 1971. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electron microscopic study in Macacus rhesus. J Comp Neurol 141:283-312.
45. Rakic P. 2000. Radial unit hypothesis of neocortical expansion. Novartis Found Symp 228:42-52.
46. Ramuz O, Isnardon D, Devilard E, Charafe-Jauffret E, Hassoun J, Birg F, Xerri L. 2003. Constitutive nuclear localization and initial cytoplasmic apoptotic activation of endogenous caspase-3 evidenced by confocal microscopy. Int J Exp Pathol 84:75-81.
47. Rhind N, Russell P. 2000. Chk1 and Cds1: linchpins of the DNA damage and replication checkpoint pathways. J Cell Sci 113:3889-3896.
48. Sastry PS, Rao K. 2000. Apoptosis in the nervous system. J Neurochem 74:1-20.
49. Selimi F, Doughty M, Delhaye-Bouchaud N, Mariani J. 2000. Target-related and intrinsic neuronal death in Lurcher mutant mice are both mediated by caspase-3 activation. J Neurosci 20:992-1000.
50. Slack RS, El Bizri H, Wong J, Belliveau DJ, Miller FD. 1998. A critical temporal requirement for the retinoblastoma protein family during neuronal determination. J Cell Biol 140:1497-1509.
51. Smith S. 2001. The world according to PARP. Trends Biochem Sci 26:174-179.
52. Sommer L, Rao M. 2002. Neural stem cells and regulation of cell number. Progr Neurobiol 66:1-18.
53. Srinivasan A, Roth KA, Sayers RO, Schindler KS, Wong AM, Fritz LC, Tomaselli KJ. 1998. In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system. Cell Death Differ 5:1004-1016.
54. Stefanis L, Park DS, Friedman WJ, Greene LA. 1999. Caspase-dependent and -independent death of camptothecin-treated embryonic cortical neurons. J Neurosci 19:6235-6247.
55. Stennicke HR, Salvesen GS. 1999. Catalytic properties of the caspases. Cell Death Differ 6:1054-1059.
56. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, et al. 1999. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446.
57. Tan X, Wang JY. 1998. The caspase-RB connection in cell death. Trends Cell Biol 8:116-120.
58. Tanabe H, Eguchi Y, Shimizu S, Martinou JC, Tsujimoto Y. 1998. Death-signalling cascade in mouse cerebellar granule neurons. Eur J Neurosci 10:1403-1411.
59. Thornberry NA, Lazebnik Y. 1998. Caspases: enemies within. Science 281:1312-1316.
60. Vincent I, Rosado M, Davies P. 1996. Mitotic mechanisms in Alzheimer's disease? J Cell Biol 132:413-425.
61. Walworth NC. 2000. Cell-cycle checkpoint kinases: checking in on the cell cycle. Curr Opin Cell Biol 12:697-704.
62. Walworth NC. 2001. DNA damage: Chk1 and Cdc25, more than meets the eye. Curr Opin Genet Dev 11:78-82.
63. Wood KA, Dipasquale B, Youle RJ. 1993. In situ labeling of granule cells for apoptosis-associated DNA fragmentation reveals different mechanisms of cell loss in developing cerebellum. Neuron 11:621-632.
64. Yoshikawa K. 2000. Cell cycle regulators in neural stem cells and postmitotic neurons. Neurosci Res 37:1-14.
65. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL. 2002. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297:259-263.
66. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. 1993. The C. elegans cell death gene ced-9 encodes a protein similar to mammalian interleukin-1beta converting enzyme. Cell 75:641-652.
67. Zarkowska T, Mittnacht S. 1997. Differential phosphorylation of the retinoblastoma protein by G1/S cyclin-dependent kinases. J Biol Chem 272:12738-12746.