A cell cycle alteration precedes apoptosis of granule cell precursors in the weaver mouse cerebellum

American Journal of Pathology

Volumn 155, Issue 2, 1999, Pages 365-373

  Migheli, Antonio ^a   Piva, Roberto ^a   Casolino, Stefania ^a   Atzori, Cristiana ^a   Dlouhy, Stephen R ^b   Ghetti, Bernardino ^b,c  

^a UNIVERSITY OF TURIN   (Italy)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INDIANA UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN D; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLINE; GUANINE NUCLEOTIDE BINDING PROTEIN; ION CHANNEL; POTASSIUM CHANNEL; POTASSIUM ION; PROTEIN P27;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE; CONTROLLED STUDY; DNA DEGRADATION; DOPAMINERGIC NERVE CELL; GRANULE CELL; MISSENSE MUTATION; MOUSE; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

EID: 0032777993     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)65133-4     Document Type: Article

References (56)

1. Rakic P, Sidman RL: Organization of cerebellar cortex secondary to deficit of granule cells in weaver mutant mice. J Comp Neurol 1973, 152:133-162
2. Schmidt MJ, Sawyer BD, Perry KW, Fuller RW, Foreman MM, Ghetti B: Dopamine deficiency in the weaver mutant mouse. J Neurosci 1982, 2:376-380
3. Verina T, Tang X, Fitzpatrick L, Norton J, Vogelweid C, Ghetti B: Degeneration of Sertoli and spermatogenic cells in homozygous and heterozygous weaver mice. J Neurogenet 1995, 9:251-265
4. Patil N, Cox DR, Bhat D, Faham M, Myers RM, Peterson AS: A potassium channel mutation in weaver mice implicates membrane excitability in granule cell differentiation. Nat Genet 1995, 11:126-129
5. Surmeier DJ, Mermelstein PG, Goldowitz D: The weaver mutation of GIRK2 results in a loss of inwardly rectifying K+ current in cerebellar granule cells: Proc Natl Acad Sci USA 1996, 93:11191-11195
6. Rossi P, De Filippi G, Armano S, Taglieti V, D'Angelo E: The weaver mutation causes a loss of inward rectifier current regulation in premigratory granule cells of the mouse cerebellum. J Neurosci 1998, 18:3537-3547
7. + channel and rescue of weaver granule cells. Neuron 1996, 16:941-952
8. + channels. Science 1996, 272:1950-1953
9. Silverman SK, Kofuji P, Dougherty DA, Davidson N, Lester HA: A regenerative link in the ionic fluxes through the weaver potassium channel underlies the pathophysiology of the mutation. Proc Natl Acad Sci USA 1996, 93:15429-15434
10. + channels. Neuron 1996, 16:321-331
11. Tong Y, Wei J, Zhang S, Strong JA, Dlouhy SR, Hodes ME, Ghetti B, Yu L: The weaver mutation changes the ion selectivity of the affected inwardly rectifying potassium channel GIRK2. FEBS Lett 1996, 390: 63-68
12. Fox AP, Dlouhy S, Ghetti B, Hurley JH, Nucifora PGP. Nelson DJ, Won L, Heller A: Altered responses to potassium in cerebellar neurons from weaver heterozygote mice. Exp Brain Res 1998, 123:298-306
13. Gillardon F, Bäurle J, Grüsser-Cornhels U, Zimmermann M: DNA fragmentation and activation of c-Jun in the cerebellum of mutant mice (weaver, Purkinje cell degeneration). NeuroReport 1995, 6:1766-1768
14. Migheli A, Attanasio A, Lee WH, Bayer SA, Ghetti B: Detection of apoptosis in weaver cerebellum by electron microscopic in situ endlabeling of fragmented DNA. Neurosci Lett 1995, 199:53-56
15. Wüllner U, Löschmann PA, Weller M, Klockgether T: Apoptotic cell death in the cerebellum of mutant weaver and lurcher mice. Neurosci Lett 1995, 200:109-112
16. Migheli A. Piva R, Wei J, Attanasio A, Casolino S, Hodes ME, Dlouhy SR, Bayer SA, Ghetti B: Diverse cell death pathways result from a single missense mutation in weaver mouse. Am J Pathol 1997, 151: 1629-1638
17. Oo TF, Blazeski R, Harrison SMW, Henchcliffe C, Mason CA, Roffler-Tarlov SK, Burke RE: Neuron death in the substantia nigra of weaver mouse occurs late in development and is non apoptotic. J Neurosci 1996, 16:6134-6145
18. Wood KA, Dipasquale B, Youle RJ: In situ labeling of granule cells for apoptosis-associated DNA fragmentation reveals different mechanisms of cell loss in the developing cerebellum. Neuron 1993, 11: 621-632
19. Smeyne RJ, Goldowitz D: Development and death of external granular layer cells in the weaver mouse cerebellum: a quantitative study. J Neurosci 1989, 9:1608-1620
20. Rezai Z, Yoon CH: Abnormal rate of granule cell migration in the cerebellum of 'weaver' mutant mice. Dev Biol 1972, 29:17-26
21. Sotelo C, Changeux JP: Bergmann fibres and granular cell migration in the cerebellum of homozygous weaver mutant mouse. Brain Res 1974, 77:484-491
22. Gao W-Q, Liu X-L, Hatten ME: The weaver gene encodes a nonautonomous signal for CNS neuronal differentiation. Cell 1992, 68:841-854
23. Maricich SM, Soha J, Trenkner E. Herrup K: Failed cell migration and death of Purkinje cells and deep nuclear neurons in the weaver cerebellum. J Neurosci 1997, 17:3675-3683
24. Oppenheim R: Cell death during development of the nervous system. Annu Rev Neurosci 1991, 14:453-501
25. Linden R: The survival of developing neurons: a review of afferent control. Neuroscience 1994, 58:671-682
26. Ross ME: Cell division and the nervous system: regulating the cell cycle from neural differentiation to death. Trends Neurosci 1996, 19:62-68
27. King KL, Cidlowski JA: Cell cycle regulation and apoptosis. Annu Rev Physiol 1998, 60:601-617
28. Freeman RS, Estus S, Johnson EM: Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of cyclin D1 during programmed cell death. Neuron 1994, 12:343-355
29. Meikrantz W, Gisselbrecht S, Tam SW, Schlegel R: Activation of cyclin A-dependent protein kinases during apoptosis. Proc Natl Acad Sci USA 1994, 91:3754-3758
30. Herrup K, Busser JC: The induction of multiple cell cycle events precedes target-related neuronal death. Development 1995, 121: 2385-2395
31. Gil-Gomez G, Berns A, Brady HJM: A link between cell cycle and cell death: Bax and Bcl-2 modulate Cdk2 activation during thymocyte apoptosis. EMBO J 1998, 17:7209-7218
32. Kranenburg O, van der Eb AJ, Zantema A: Cyclin D1 is an essential mediator of apoptotic neuronal cell death. EMBO J 1996, 15:46-54
33. Park DS, Levine B. Ferrari G, Greene LA: Cyclin dependent kinase inhibitors and dominant negative cyclin dependent kinase 4 and 6 promote survival of NGF-deprived sympathetic neurons. J Neurosci 1997, 17:8975-8983
34. Park DS, Morris EJ, Stefanis L, Troy CM, Shelanski ML, Geller HM, Greene LA: Multiple pathways of neuronal death induced by DNA-damaging agents, NGF deprivation, and oxidative stress. J Neurosci 1998, 18:830-840
35. Bravo R, Frank R, Blundell PA, Macdonald Bravo H: Cyclin/PCNA is the auxiliary protein of DNA polymerase-6. Nature 1987, 326:515-517
36. Johnson DG, Walker CL: Cyclins and cell cycle checkpoints. Annu Rev Pharmacol Toxicol 1999, 39:295-312
37. kip1 alters the response of cells to mitogen and is part of a cell-intrinsic timer that arrests the cell cycle and initiates differentiation. Curr Biol 1998, 8:431-440
38. Migheli A, Cavalla P, Marino S, Schiffer D: Detection of apoptosis in normal and pathologic nervous tissue after in situ end-labeling of DNA strand breaks. J Neuropathol Exp Neurol 1994, 53:606-616
39. Bayer SA, Wills KB, Wei J, Feng Y, Dlouhy SR, Hodes ME, Verina T, Ghetti B: Phenotypic effects of the weaver gene are evident in the embryonic cerebellum but not in the ventral midbrain. Dev Brain Res 1996, 96:130-137
40. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685
41. Fujita S, Shimada M, Nakamura T: H3-thymidine autoradiographic studies on the cell proliferation, and differentiation in the external, and the internal granular layers of the mouse cerebellum: J Comp Neurol 1966, 128:191-208
42. Janec E, Burke RE: Naturally occurring cell death during postnatal development of the substantia nigra pars compacta of rat. Mol Cell Neurosci 1993, 4:30-35
43. Shambaugh GE, Lee RJ, Watanabe G, Erfurth F, Karnezis AN, Koch AE, Haines GK, Halloran M, Brody BA, Pestell RG: Reduced cyclin D1 expression in the cerebella of nutritionally deprived rats correlates with developmental delay and decreased cellular DNA synthesis. J Neuropathol Exp Neurol 1996, 55:1009-1020
44. Wüllner U, lsenmann S, Gleichmann M, Klockgether T, Bahr M: Expression of neurotrophins and neurotrophin receptors in the cerebellum of mutant weaver and lurcher mice. Brain Res Dev Brain Res 1998, 110:1-6
45. Shivji MKK, Kenny MK, Wood RD: Proliferating cell nuclear antigen is required for DNA excision repair. Cell 1992, 69:367-374
46. Yamaguchi H, Hosokawa K, Jiang ZL, Takahashi A, Ikehara T, Miyamoto H: Arrest of cell cycle progression of HeLa cells in the early G1 phase in K(+)-depleted conditions and its recovery upon addition of insulin and LDL. J Cell Biochem 1993, 53:13-20
47. Cui H, Bulleit RF: Potassium chloride inhibits proliferation of cerebellar granule neuron progenitors. Brain Res Dev Brain Res 1998, 106: 129-135
48. Miller TM, Johnson EM: Metabolic and genetic analyses of apoptosis in potassium/serum-deprived rat cerebellar granule cells. J Neurosci 1996, 16:7487-7495
49. Brüggemann A, Stühmer W, Pardo LA: Mitosis-promoting factor-mediated suppression of a cloned delayed rectifier potassium channel expressed in Xenopus oocytes. Proc Natl Acad Sci USA 1997, 94: 537-542
50. Ramsdell JS: Voltage-dependent calcium channels regulate GH4 pituitary cell proliferation at two stages of the cell cycle. J Physiol 1991, 146:197-206
51. McShea A, Harris PL, Webster KR, Wahl AF, Smith MA: Abnormal expression of the cell cycle regulators P16 and CDK4 in Alzheimer's disease. Am J Pathol 1997, 1939, 150:1933
52. Clarke PGH: Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 1990, 181:195-213
53. Perry G, Nunomura A, Smith MA: A suicide note from Alzheimer disease neurons? Nat Med 1998, 4:897-898
54. Sanguinetti MC, Spector PS: Potassium channelopathies. Neuropharmacology 1997, 36:755-762
55. Gordon N: Episodic ataxia and channelopathies. Brain Dev 1998, 20:9-13
56. Rose MR: Neurological channelopathies. Br Med J 1998, 316:1104-1105