Survival of interneurons and parallel fiber synapses in a cerebellar cortex deprived of Purkinje cells: Studies in the double mutant mouse Grid2 Lc/+;Bax-/-

Journal of Comparative Neurology

Volumn 497, Issue 4, 2006, Pages 622-635

  Zanjani, S Hadi ^a   Selimi, Fekrije ^a   Vogel, Michael W ^c   Haeberlé, Anne Marie ^b   Boeuf, Julien ^b   Mariani, Jean ^a   Bailly, Yannick J ^b  

^a Groupe Enzymologie Moléculaire et Fonctionnelle   (France)

^b CNRS   (France)

^c MARYLAND PSYCHIATRIC RESEARCH CENTER   (United States)

Author keywords

Autophagy; Cerebellum; Interneuron; Neuronal death; Synapse

Indexed keywords

4 AMINOBUTYRIC ACID; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL DEATH; CELL SURVIVAL; CEREBELLUM CORTEX; ELECTRON MICROSCOPY; GENE; GENE MUTATION; GRANULE CELL; IMMUNOGOLD LABELING; INTERNEURON; MORPHOMETRICS; MOUSE; NERVE ENDING; NEUROPIL; NONHUMAN; OLIVARY NUCLEUS; PRIORITY JOURNAL; PURKINJE CELL; SYNAPSE; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; AUTOPHAGY; BCL-2-ASSOCIATED X PROTEIN; CELL COMMUNICATION; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CEREBELLAR CORTEX; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERNEURONS; MALE; MICE; MICE, KNOCKOUT; MICE, NEUROLOGIC MUTANTS; MICROSCOPY, ELECTRON, TRANSMISSION; NERVE GROWTH FACTORS; NEUROGLIA; PURKINJE CELLS; RECEPTORS, GLUTAMATE; SYNAPSES; UP-REGULATION;

EID: 33745138533     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21017     Document Type: Article

References (46)

1. Baader SL, Schilling ML, Rosengarten B, Pretsch W, Teutsch HF, Oberdick J, Schilling K. 1996. Purkinje cell lineage and the topographic organization of the cerebellar cortex: a view from X inactivation mosaics. Dev Biol 174:393-406.
2. Bailly YJ, Schoen SW, Mariani J, Kreutzberg GW, Delhaye-Bouchaud N. 1998. Immature chemodifferentiation of Purkinje cell synapses revealed by 5′-nucleotidase ecto-enzyme activity in the cerebellum of the reeler mouse. Synapse 29:279-292.
3. Caddy KWT, Biscoe TJ. 1979. Structural and quantitative studies on the normal CH3 and lurcher mutant mouse. Philos Trans R Soc Lond B 287:167-201.
4. Dahmane N, Ruiz-i-Altaba A. 1999 Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126:3089-3100.
5. De Biasi S, Vitellaro-Zuccarello L, Bernardi P, Valtschanoff JG, Weinberg RJ. 1994. Ultrastructural and immunocytochemical characterization of primary afferent terminals in the rat cuneate nucleus. J Comp Neurol 347:275-287.
6. Deckwerth TL, Elliott JL, Knudson CM, Johnson EMJ, Snider WD, Korsmeyer SJ. 1996. BAX is required forneuronal death after trophic factor deprivation and during development. Neuron 17:401-411.
7. Doughty ML, De Jager PL, Korsmeyer SJ, Heintz N. 2000. Neurodegeneration in Lurcher mice occurs via multiple cell death pathways. J Neurosci 20:3687-3694.
8. Dumesnil-Bousez N, Sotelo C. 1992. Early development of the Lurcher cerebellum: Purkinje cell alterations and impairment of synaptogenesis. J Neurocytol 21:506-529.
9. Fan H, Favero M, Vogel MW. 2001. Elimination of Bax expression in mice increases cerebellar Purkinje cell numbers but not the number of granule cells. J Comp Neurol 436:82-91.
10. Hawkes R, Faulkner-Jones B, Tam P, Tan S-S. 1998. Pattern formation in the cerebellum of murine embryonic stem cell chimeras. Eur J Neurosci 10:790-793.
11. Heckroth JA, Eisenman LM. 1988. The olivocerebellar projection in lurcher mutant mice. Neurosci Lett 85:199-204.
12. Heckroth JA, Goldowitz D, Eisenman LM. 1990. Olivocerebellar fiber maturation in normal and lurcher mutant mice: defective development in lurcher. J Comp Neurol 291:415-430.
13. Herrup K, Sunter K. 1987. Numerical matching during cerebellar development: quantitative analysis of granule cell dentil in staggerer mouse chimeras. J Neurosci 7:829-836.
14. Kashiwabushi N, Ikuda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y, Aizawa S, Mishina M. 1995. Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluRd2 mutant mice. Cell 81: 245-252.
15. Knudson CM, Tung KSK, Tourtelotte WG, Brown AJ, Korsmeyer SJ. 1995. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:90-99.
16. Larramendi LM, Victor T. 1967. Synapses on the Purkinje cell spines in the mouse. An electron microscopic study. Brain Res 5:15-30.
17. Lemkey-Johnston N, Larramendi L. 1968. Types and distribution of synapses upon basket and stellate cells of the mouse cerebellum: an electron microscopic study. J Comp Neurol 134:73-112.
18. Mariani J, Crepel F, Mikoshiha K, Changeux JP, Sotelo C. 1977. Anatomical, physiological and biochemical studies of the cerebellum from reeler mutant mouse. Philos Trans R Soc Lond 281:1-28.
19. Mathis L, Bonnerot C, Puelles L, Nicolas J-F. 1997. Retrospective clonal analysis of the cerebellum using genetics lacZ/lacZ mouse mosaics. Development 124:4089-4104.
20. Messner A, Eisenherg B, Martin DL. 1988. The role of timing and cell interactions in cerebellar development. In: Swann JW, Messer A, editors. Disorders of the developing nervous system: changing views on their origins, diagnoses, and treatments. New York: Alan R. Liss. p 111-123.
21. Norman D, Feng L, Gubbay J, Chan E, Heintz N. 1995. The lurcher gene induces apoptotic death in cerebellar Purkinje cells. Development, 121: 1183-1193.
22. Phillips RJS. 1960. Lurcher a new gene linkage group XI of the house mouse. J Genet 57:35-42.
23. Rossi F, Jankovski A, Sotelo C. 1995. Target neuron controls the integrity of afferent axon phenotype: a study on the Purkinje cell-climbing fiber system in cerebellar mutant mice. J Neurosci 15:2040-2056.
24. Selimi F, Vogel MW, Mariani J. 2000. Bax inactivatiou in lurcher mutants rescues cerebellar granule cells but not Purkinje cells or inferior olivary neurons. J Neurosci 20:5339-5345.
25. Selimi F, Lohof AM, Heitz S, Lalouette A, Jarvis CI, Bailly Y, Mariani J. 2003. Lurcher GRID2-induced death and depolarization can he dissociated in cerebellar Purkinje cells. Neuron 37:813-819.
26. Smeyne RJ, Chu T, Lewin A, Bian F, Crisman SS, Kunsch C, Lira SA, Oberdick J. 1995. Local control of granule cell generation by cerebellar Purkinje cells. Mech Cell Neurosci 6:230-251.
27. Sonmez E, Herrup K. 1984. Role of staggerer gene in determining cell number in cerebellar cortex. II. Granule cell death and persistence of the external granule cell layer in young mouse chimeras. Dev Brain Res 12:271-283.
28. Sotelo C. 1991. Cerebellar synaptogenesis: mutant mice-neuronal grafting. J Physiol Paris 85:134-144.
29. Sotelo C, Changeux J-P. 1974. Transsynaptic degeneration en cascade in the cerebellar cortex of staggerer mutant mice. Brain Res 67:519-526.
30. Sotelo C, Triller A. 1979. Fate of presynaptic afferents to Purkinje cells in the adult nervous mutant mouse: a model to study presynaptic stabilization. Brain Res 175:11-36.
31. Takagishi Y, Yamamura H. 1989. Purkinje cell abnormalities and synaptogonesis in genetically jaundiced rats (Gann rats). Brain Res 492:116-128.
32. Vogel MW, Herrup K. 1993. A theoretical and experimental examination of cell lineage relationships among cerebellar Purkinje cells in the mouse. Dev Biol 156:49-68.
33. Vogel MW, Sunter K, Herrup K. 1989. Numerical matching between granule and Purkinje cells in lurcher chimeric mice: a hypothesis for the trophic rescue of granule cells from target related cell death. J Neurosci 9:3454-3462.
34. Wallace WA. 1999. Purkinje-cell-derived sonic hedgehog granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr Biol 9:445-448.
35. Wechsler-Reya RJ, Scott MP. 1999. Control of neural precursor proliferation in the cerebellum by sonic hedgehog. 22:103-114.
36. Wetts R, Herrup K. 1982a. Interaction of granule, Purkinje, and inferior olivary neurons in Lurcher chimeric mice. I. Qualitative studies. J Embryol Exp Morphol 68:87-98.
37. Wetts R, Herrup K. 1982b. Interaction of granule, Purkinje, and inferior olivary neurons in Lurcher chimeric mice. II. Granule cell death. Brain Res 250:358-362.
38. Wetts R, Herrup K. 1982c. Cerebellar Purkinje cells are descended from a small number of progenitors committed during early development. Qualitative analysis of lurcher chimeric mice. J Neurosci 2:1494-1498.
39. Wetts R, Herrup K. 1983. Direct correlation between Purkinje and granule cell number in the cerebella of lurcher chimeras and wild-type mice. Dev Brain Res 10:41-47.
40. White FA, Keller-Peck CR, Knudson M, Korsmeyer SJ, Snider WD. 1998. Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J Neurosci 18:1428-1439.
41. Wüllner U, Weller M, Schulz J, Krajewski S, Reed J, Klockgether S. 1998. Bcl-2, Bax and Bcl-x expression in neuronal apoptosis: a study of mutant weaver and lurcher mice. Acta Neuropathol 96:233-238.
42. Yue Z, Horton A, Bravin M, DeJager PL, Selimi P, Heintz N. 2002. A novel protein complex linking the delta 2 glutamate receptor and autophagy: implication for neurodegeneration in lurcher mice. Neuron 35:921-933.
43. Zanjani HS, Vogel MW, Delhaye-Bouchaud N, Martinou JC, Mariani J. 1996. Increased cerebellar Purkinje cell numbers in mice ovorexpressing a human bcl-2 transgene. J Comp Neurol 374:332-341.
44. Zanjani HS, Vogel MW, Delhaye-Bouchaud N, Martinou JC, Mariani J. 1997. Increased olivary neuron and cerebellar granule cell numbers in transgenic mice overexpressing a human bcl-2 transgene. J Neurobiol 32:502-516.
45. Zanjani HS, Lemaigre-Dubreuil Y, Tillakaratae NJ, Blokhin A, McMahon RP, Tobin AJ, Vogel MW, Mariani J. 2004. Cerebellar Purkinje cell loss in aging Hu-Bcl-2 transgenic mice. J Comp Neurol 475:481-492.
46. Zuo J, De Jager PL, Takahashi KA, Jiang W, Linden DJ, Heintz N. 1997. Neurodegeneration in Lurcher mice caused by mutation in delta2 glutamate receptor gene. Nature 388:769-773.