Apoptosis of undifferentiated progenitors and granule cell precursors in the postnatal human cerebellar cortex correlates with expression of BCLl-2, ICE, and CPP32 proteins

Journal of Comparative Neurology

Volumn 399, Issue 3, 1998, Pages 359-372

  Lossi, Laura ^a   Zagzag, David ^b   Greco, M Alba ^b   Merighi, Adalberto ^a,c  

^a UNIVERSITY OF TURIN   (Italy)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^c I 10126   (Italy)

Author keywords

Cell proliferation; Cerebellum; DNA fragmentation; Postnatal development; Programmed cell death

Indexed keywords

ANTIBODY; BETA TUBULIN; CYCLINE; DNA FRAGMENT; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEIN BCL 2; VIMENTIN;

ADULT; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBELLUM CORTEX; CHILD; CONTROLLED STUDY; GRANULE CELL; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; INFANT; NEWBORN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 0032575996     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1096-9861(19980928)399:3<359::aid-cne5>3.0.co;2-%23     Document Type: Article

References (79)

1. Abe-Dohmae, S., N. Harada, K. Yamada, and R. Tanaka (1993) bcl-2 gene is highly expressed during neurogenesis in the central nervous system. Biochem. Biophys. Res. Commun. 191:915-921.
2. Alnemri, E.S., J.N. Livingston, D.W. Nicholson, G. Salvesen, N.A. Thornberry, W.W. Wong, and J. Yuan (1996) Human ICE/CED-3 protease nomenclature. Cell 87:171-181.
3. Altman, J. and S.A. Bayer (1997) Development of the Cerebellar System in Relation to its Evolution, Structure and Functions. Boca Raton: CRC Press.
4. Alvarez-Otero, R., C. Sotelo, and R.M. Alvarado-Mallart (1993) Chick/quail chimeras with partial cerebellar grafts: An analysis of the origin and migration of cerebellar cells. J. Comp. Neurol. 333:597-615.
5. Beppu, T., Y. Ishida, H. Arai, T. Wada, N. Uesugi, and K. Sasaki (1994) Identification of S-phase cells with PC10 antibody to proliferating cell nuclear antigen (PCNA) by flow cytometric analysis. J. Histochem. Cytochem. 42:1177-1182.
6. Carrio, R., M. Lopez-Hoyos, J. Jimeno, M.A. Benedict, R. Merino, A. Benito, J.L. Fernandez-Luna, G. Nunez, J.A. Garcia-Porrero, and J. Merino (1996) A1 demonstrates restricted tissue distribution during embryonic development and functions to protect against cell death. Am. J. Pathol. 149:2133-2142.
7. Castren, E., Y. Ohga, M.P. Berzaghi, G. Tzimaagiorgis, H. Thoenen, and D. Lindholm (1994) bcl-2 messenger RNA is localized in neurons of the developing and adult rat brain. Neuroscience 61:165-177.
8. Chien, C.-L., C.A. Mason, and R.K.H. Liem (1996) α-Internexin is the only neuronal intermediate filament expressed in developing cerebellar granule neurons. J. Neurobiol. 29:304-318.
9. Chitteden, T., E. Harrington, R. O'Connor, G. Evan, and B. Guild (1995) Induction of apoptosis by the Bcl-2 homologue Bax. Nature 374:733-736.
10. Cleary, M.L., S.D. Smith, and J. Sklar (1986) Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/immunoglobulin transcript resulting from the (14;18) translocation. Cell 47:19-28.
11. Cochard, P. and D. Paulin (1984) Initial expression of neurofilaments and vimentin in central and peripheral nervous system of the mouse embryo in vivo. J. Neurosci. 4:2080-2094.
12. Cowan, W.M., J.W. Fawcett, D.D.M. O'Leary, and B.B. Stanfield (1984) Regressive events in neurogenesis. Science 225:1258-1265.
13. Cunningham, T.J. (1982) Naturally occurring neuron death and its regulation by developing neural pathways. Int. Rev. Cytol. 74:163-186.
14. Didenko, V.V. and P.J. Hornsby (1996) Presence of double-strand breaks with single base 3′ overhangs in cells undergoing apoptosis but not necrosis. J. Cell Biol. 135:1369-1376
15. Feddersen, R.M., R. Ehlenfeldt, W.S. Yunis, H.B. Clark, and H.T. Orr (1991) Disrupted cerebellar cortical development and progressive degeneration of Purkinje cells in SV40 T antigen transgenic mice. Neuron 9:955-966.
16. Fernandez-Alnemri, T., G. Litwack, and E.S. Alnemri (1994) CPP32, a novel human apoptotic protein with homology to Caenorahbitis elegans cell death protein Ced-3 and mammalian interleukin-1-beta-converting enzyme. J. Biol. Chem. 269:30761-30764.
17. Fraser, A. and G. Evan (1996) A license to kill. Cell 85:781-784.
18. Fritsch, P., H. Richard-Le Naour, S. Denis, and F. Ménétrier (1994) Kinetics of radiation-induced apoptosis in the cerebellum of 14-day-old rats after acute or during continuous exposure. Int. J. Radiat. Biol. 66:111-117.
19. Gagliardini, V., P-A. Fernandez, R.K.K. Lee, H.C.A. Drexler, R.J. Rotello, M.C. Fishman, and J. Yuan (1994) Prevention of vertebrate neuronal death by the crmA gene. Science 263:826-828.
20. Galli, C., O. Meucci, A. Scorziello, T.M. Werge, P. Calissano, and G. Schettino (1995) Apoptosis in cerebellar granule cells is blocked by high KCl, forskolin, and IGF-1 through distinct mechanisms of action: The involvment of intracellular calcium and RNA synthesis. J. Neurosci. 15:1172-1179.
21. Gao, W.Q. and M.E. Hatten (1994) Immortalizing oncogenes subvert the establishment of granule cell identity in developing cerebellum. Development 120:1059-1070.
22. Gavrieli, Y., Y. Sherman, and S.A. Ben-Sasson (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
23. Gerdes, J., U. Schwab, H. Lemke, and H. Stein (1983) Production of a mouse monoclonal antibody reactive with a human antigen associated with cell proliferation. Int. J. Cancer 31:13-20.
24. Glucksmann, P.D. (1951) Cell deaths in normal vertebrate ontogeny. Biol. Rev. 26:59-86.
25. Gonzales-Garcia, M., I. Garcia, L. Ding, S. O'Shea, L.H. Boise, C.B. Thompson, and G. Nunez (1995) Bcl-x is expressed in embryonic and postnatal neural tissues and functions to prevent neuronal cell death. Proc. Natl. Acad. Sci. USA 92:4304-4308.
26. Gundersen, H.J.G., T.F. Bendtsen, L. Korbo, N. Marcussen, A. Moller, K. Nielsen, J.R. Nyengaard, B. Pakkenberg, F.B. Sorensen, A. Vesterby, and J.M. West (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Acta Pathol. Microbiol. Immunol. Scand. 96:379-394.
27. Hallonet, M.E., M.A. Teillet, and N.M. Le-Douarin (1990) A new approach to the development of the cerebellum provided by the quail-chick marker system. Development 108:19-31.
28. Hara, A., Y. Hirose, A. Wang, N. Yoshimi, T. Tanaka, and H. Mori (1996) Localization of Bax and Bcl-2 proteins, regulators of programmed cell death, in the human central nervous system. Virchows Arch. 429:249-253.
29. Hatten, M.E. (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.
30. Hengartner, M.O. and H.R. Horvitz (1994) Programmed cell death in Caenorhabditis elegans. Curr. Opin. Cell Biol. 4:581-586.
31. Hengartner, M.O., R.E. Ellis, and H.R. Horvitz (1992) C.elegans gene ced-9 protects cells from programmed cell death. Nature 356:494-499.
32. Ito, M. (1984) The Cerebellum and Neuronal Control. New York: Raven Press.
33. Jacobson, M. (1991) Developmental Neurobiology. New York: Plenum Press.
34. Kaplan, M.P., S.S.M. Chin, K.H. Fliegner, and R.K.H. Liem (1990) α-Internexin, a novel neuronal intermediate filament protein, precedes the low molecular weight neurofilament protein (NF-L) in the developing rat brain. J. Neurosci. 10:2735-2748.
35. Kerr, J.F., A.H. Wyllie, and A.R. Currie (1972) Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J Cancer 26:239-257.
36. Komuro, H. and P. Rakic (1995) Dynamics of granule cell migration: A confocal microscopic study in acute cerebellar slice preparations. J. Neurosci. 15:1110-1120.
37. Krajewski, S., S. Bodrug, M. Krajewska, A. Shabaik, R. Gascoyne, K. Berean, and J.C. Reed (1995) Immunohistochemical analysis of McI-1-protein in human tissues. Differential regulation of Mcl-1 and Bcl-2 protein production suggests a unique role for Mcl-1 in control of programmed cell death in vivo. Am. J. Pathol. 146:1309-1319.
38. Krajewski, S., M. Krajewska, and J.C. Reed (1996) Immunohistochemical analysis of in vitro patterns of Bax expression, a proapototic member of the Bcl-2 protein family. Cancer Res. 56:2849-2855.
39. Krueger, B.K., J.F. Burne, and M.C. Raff (1995) Evidence for large-scale astrocyte death in the developing cerebellum. J. Neurosci. 15:3366-3374.
40. Kuida, K., J.A. Lippke, G. Ku, M.W. Harding, D.J. Livingston, M.S. Su, and R.A. Flavell (1995) Altered cytokine export and apoptosis in mice deficient in interleukine-1-beta converting enzyme. Science 267:2000-2003.
41. Kuida, K., T. Zheng, S. Na, C. Kuan, D. Yang, H. Karasuyama, P. Rakic, and R.A. Flavell (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384:368-370.
42. Lamaigre-Dubreuil, Y., B. Brugg, C. Chianale, N. Delhaye-Bouchaud, and J. Mariani (1996) Over-expression of interleukin-1-beta-converting enzyme in staggerer cerebellum. NeuroReport 7:1777-1780.
43. Lange, W. (1975) Cell number and cell density in the cerebellar cortex of man and some other mammals. Cell Tissue Res. 157:115-124.
44. Lendahl, U., L.B. Zimmerman, and R.D.G. McKay (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585-595.
45. Levine, J.M., F. Stincone, and Y-S. Lee (1993) Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7:307-321.
46. Li, P., H. Allen, S.K. Banerjee, S. Franklin, L. Herzog, C. Johnston, J. McDowell, M. Paskind, L. Rodman, J. Salfeld, E. Towne, D. Tracey, S. Wardwell, F.-H. Wei, W.W. Wong, R. Kamen, and T. Seshadri (1995) Mice deficcient in IL-1 beta converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxin shock. Cell 80:401-411.
47. Martin, S.J. and D.R. Green (1995) Protease activation during apoptosis: Death by a thousand cuts? Cell 82:349-352.
48. Menezes, J.R.L. and M.B. Luskin (1994) Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J. Neurosci. 14:5399-5416.
49. Merry, D.E., D.J. Veis, W.F. Hickey, and S.J. Korsmeyer (1994) Bcl-2 protein expression is widespread in developing nervous system and retained in the adult PNS. Development 120:301-311.
50. Migheli, A., A. Attanasio, W.H. Lee, S.A. Bayer, and B. Ghetti (1995) Detection of apoptosis in weaver cerebellum by electron microscopic in situ end-labeling of fragmented DNA. Neurosci. Lett. 199:53-56.
51. Milligan, C.E., D. Prevette, H. Yaginuma, S. Homma, C. Cardwell, L.C. Fritz, K.J. Tomaselli, R.W. Oppenheim, and L.M. Schwartz (1995) Peptide inhibitors of the ICE protease family arrest programmed cell death of motoneurons in vivo and in vitro. Neuron 15:385-393.
52. Murtomäki, S., E. Trenkner, J.M. Wright, O. Saksela, and P. Liesi (1995) Increased proteolytic activity of the granule neurons may contribute to neuronal death in the weaver mouse cerebellum. Dev. Biol. 168:635-648.
53. Oppenheim, R.W. (1985) Naturally occurring cell death during neural development. Trends Neurosci. 8:487-493.
54. Osborn, M., M. Altamannsberger, E. Debus, and K. Weber (1984a) Conventional and monoclonal antibodies to intermediate filament proteins in human tumor diagnosis. In: Cancer Cells 1. The Transformed Phenotype. Cold Spring Harbor, NY: Cold Spring Harbor Laboratories, pp. 191-200.
55. Osborn, M., E. Debus, and K. Weber (1984b) Monoclonal antibodies specific for vimentin. Eur. J. Cell Biol. 34:137-143.
56. Perry, V.H., Z. Henderson, and R. Linden (1983) Postnatal changes in retinal ganglion cells and optic nerve axon populations in the pigmented rat. J. Comp. Neurol. 219:356-368.
57. Pixley, S.K.R. and J. De Vellis (1984) Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Dev. Brain Res. 15:201-209.
58. Posmantur, R., K. McGinnis, R. Nadimpalli, R.B. Gilbertsen, and K.W. Wang (1997) Characterization of CPP32-like protease activity following apoptotic challenge in SH-SY5Y neuroblastoma cells. J. Neurochem. 68:2328-2337.
59. Raaf, J. and J. W. Kernohan (1944) A study of the external granular layer in the cerebellum. Am. J. Anat. 75:151-172.
60. Raff, M.C., B.A. Barres, J.F. Burne, H.S.R. Coles, Y. Ishizaki, and M.D. Jacobson (1994) Programmed cell death and the control of cell survival. Phil. Trans. R. Soc. Lond. (Biol.) 345:265-268.
61. 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.
62. Ryder, E.F. and C.L. Cepko (1994) Migration patterns of clonally related granule cells and their progenitors in the developing chick cerebellum. Neuron 12:1011-1029.
63. Sasaki, K., A. Kurose, Y. Ishida, and M. Matsuta (1994) Estimation of S-phase fraction in tumor tissue sections by immunohistochemical staining of PCNA. J. Histochem. Cytochem. 42:957-960.
64. Saunders, J.V. (1966) Death in embryonic systems. Science 154:604-612.
65. Smeyne, R.J., T. Chu, A. Lewin, F.S. Bian, S. Crisman, C. Kunsch, S.A. Lira, and J. Oberdick (1995) Local control of granule cell generation by cerebellar Purkinje cells. Mol. Cell. Neurosci. 6:230-251.
66. Sohma, O., M. Mizuguchi, S. Takashima, M. Yamada, K. Ikeda, and S. Ohta (1996) High espression of Bcl-x protein in the developing human cerebellar cortex. J. Neurosci. Res. 43:175-182.
67. Takahashi, T. and V.S. Caviness, Jr. (1993) PCNA-binding to DNA at the G1/S transition in proliferating cells of the developing cerebral wall. J. Neurocytol. 22:1096-1102.
68. Takahashi, T, R.S. Nowakowski, and V.S. Caviness, Jr. (1993) Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J. Neurosci. 13:820-833.
69. Takahashi, T., R.S. Nowakowski, and V.S. Caviness, Jr. (1994) Mode of cell proliferation in the developing mouse neocortex. Proc. Natl. Acad. Sci. USA 91:375-379.
70. Waseem, N.H. and D.P. Lane (1990) Monoclonal antibody analysis of the proliferating cell nuclear antigen (PCNA). Structural conversation and the detection of a nucleolar form. J. Cell Sci. 96:121-129.
71. Wood, K.A. and R.J. Youle (1995) The role of free radicals and p53 in neuron apoptosis in vivo. J. Neurosci. 15:5851-5857.
72. Wood, K.A., B. Dipasquale, and R.J. Youle (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.
73. Wüllner, U., PA. Löschmann, M. Weller, and T. Klockgether (1995) Apoptotic cell death in the cerebellum of mutant weaver and lurcher mice. Neurosci. Lett. 200:109-112.
74. Wyllie, A.H. (1980) Glucocorticoid-induced tymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555-556.
75. Yachnis, A.T., L.B. Rorke, V.M.-Y Lee, and J.Q. Trojanowski (1993) Expression of neuronal and glial polypeptides during histogenesis of the human cerebellar cortex including observations on the dentate nucleus. J. Comp. Neurol. 334:356-369.
76. Yin, X.-M., Z.N. Oltvai, and S.J. Korsmeyer (1994) BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369:321-323.
77. Yuan, J. and H.R. Horvitz (1990) The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death. Dev. Biol. 138:33-41.
78. Yuan, J., S. Shaham, S. Ledoux, H.M. Ellis, and H.R. Horvitz (1993) The C. elegans cell death gene ced-9 encodes a protein similar to mammalian interleukin-1beta converting enzyme. Cell 75:641-652.
79. Zhang L. and J.E. Goldman (1996) Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron 16:47-54.