Cerebellar purkinje cell loss in heterozygous Rora+/- mice: A longitudinal study

Journal of Neurogenetics

Volumn 20, Issue 1-2, 2006, Pages 1-17

  Doulazmi, Mohamed ^a,b   Capone, Francesca ^a,b   Frederic, Florence ^a,b   Boukhtouche, Joëlle ^a,b   Lemaigre Dubreuil, Yolande ^a,b   Mariani, Jean ^a,b,c  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

^c HÔPITAL CHARLES FOIX   (France)

Author keywords

Aging; Cerebellum; Mutant mice; Neuronal death; Staggerer locus

Indexed keywords

RETINOIC ACID RECEPTOR; RETINOIC ACID RECEPTOR RELATED ORPHAN RECEPTOR ALPHA; UNCLASSIFIED DRUG;

AGE; AGING; ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATAXIA; CELL LOSS; CEREBELLUM; CEREBELLUM DEGENERATION; CONTROLLED STUDY; GENE; GENE DELETION; GENE MUTATION; GENETIC ASSOCIATION; HETEROZYGOTE; LIFESPAN; LIGAND BINDING; LONGITUDINAL STUDY; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PURKINJE CELL; QUALITATIVE ANALYSIS; RORA GENE; STAGGERER GENE; WILD TYPE;

AGING; ANIMALS; CELL COUNT; CELL DEATH; CELL SIZE; FEMALE; GENOTYPE; HETEROZYGOTE; IMMUNOHISTOCHEMISTRY; LONGITUDINAL STUDIES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 1; PURKINJE CELLS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, RETINOIC ACID; TRANS-ACTIVATORS;

ANIMALIA; ATAXIA;

EID: 33745712817     PISSN: 01677063     EISSN: 15635260     Source Type: Journal    
DOI: 10.1080/01677060600685832     Document Type: Article

References (44)

1. Akashi, M. & Takumi, T. (2005). The orphan nuclear receptor RORalpha regulates circadian transcription of the mammalian core-clock Bmal1. Nature Struct. Molec. Biol. 12, 441-448.
2. Andersen, B.B., Korbo, L., & Pakkenberg, B. (1992). A quantitative study of the human cerebellum with unbiased stereological techniques. J. Comp. Neurol. 326, 549-560.
3. Becker-Andre, M., Andre, E., & DeLamarter, J.F. (1993). Identification of nuclear receptor mRNAs by RT-PCR amplification of conserved zinc-finger motif sequences. Biochem. Biophys. Res. Commun. 194, 1371-1379.
4. Boukhtouche, F., Janmaat, S., Vodjdani, G., Gautheron, V., Mallet, J., Dusart, I., & Mariani, J. (2006a). Retinoid-related orphan receptor alpha controls the early steps of Purkinje cell dendritic differentiation. J. Neurosci. 26, 1531-1538.
5. Boukhtouche, F., Mariani, J., & Tedgui, A. (2004). The "CholesteROR" protective pathway in the vascular system. Arterioscler. Thromb. Vasc. Biol. 24, 637-643.
6. Boukouche, F., Vodjdani, G., Jarvis, C.I., Bakouche, J., Staels, B., Mallet, J., Mariani, J., Lemaigre-Dubreuil, Y., & Brugg, B. (2006b). hRORa1 overexpression protects neurons against oxidative stress-induced apoptosis. J. Neurochem. 96, 1778-1789.
7. Crusio, W.E. (2004). Flanking gene and genetic background problems in genetically manipulated mice. Biol. Psychiatry 56, 381-385.
8. Doulazmi, M., Frederic, F., Capone, F., Becker-Andre, M., Delhaye-Bouchaud, N., & Mariani, J. (2001). A comparative study of Purkinje cells in two RORalpha gene mutant mice: staggerer and RORalpha(-/-). Devel. Brain Res. 127, 165-174.
9. Doulazmi, M., Frederic, F., Lemaigre-Dubreuil, Y., Hadj-Sahraoui, N., Delhaye-Bouchaud, N., & Mariani, J. (1999). Cerebellar Purkinje cell loss during life span of the heterozygous staggerer mouse (Rora(+)/Rora(sg)) is gender-related. J. Comp. Neurol. 411, 267-273.
10. Dussault, I., Fawcett, D., Matthyssen, A., Bader, J.A., & Giguere, V. (1998). Orphan nuclear receptor ROR alpha-deficient mice display the cerebellar defects of staggerer. Mech. Devel. 70, 147-153.
11. Dussault, I. & Giguere, V. (1997). Differential regulation of the N-myc protooncogene by ROR alpha and RVR, two orphan members of the superfamily of nuclear hormone receptors. Molec. Cell. Biol. 17, 1860-1867.
12. Dzhagalov, I., Zhang, N., & He, Y.W. (2004). The roles of orphan nuclear receptors in the development and function of the immune system. Cell. Molec. Immunol. 1, 401-407.
13. Emery, P. & Reppert, S.M. (2004). A rhythmic Ror. Neuron 43, 443-446.
14. Frederic, F., Chianale, C., Oliver, C., & Mariani, J. (2006). Enhanced endocrine response to novel environment stress and lack of corticosterone circadian rhythm in staggerer (Rora sg/sg) mutant mice. J. Neurosci. Res. 83, 1525-1532.
15. Giguere, V., Beatty, B., Squire, J., Copeland, N.G., & Jenkins, N.A. (1995). The orphan nuclear receptor ROR alpha (RORA) maps to a conserved region of homology on human chromosome 15q21-q22 and mouse chromosome 9. Genomics 28, 596-598.
16. Giguere, V., Tini, M., Flock, G., Ong, E., Evans, R.M., & Otulakowski, G. (1994). Isoform-specific amino-terminal domains dictate DNA-binding properties of ROR alpha, a novel family of orphan hormone nuclear receptors. Genes Devel. 8, 538-553.
17. Gold, D.A., Baek, S.H., Schork, N.J., Rose, D.W., Larsen, D.D., Sachs, B.D., Rosenfeld, M.G., & Hamilton, B.A. (2003). RORalpha coordinates reciprocal signaling in cerebellar development through sonic hedgehog and calcium-dependent pathways. Neuron 40, 1119-1131.
18. Gold, D.A., Gent, P.M., & Hamilton, B.A. (2006). RORalpha in genetic control of cerebellum development: 50 staggering years. Brain Res. Epub ahead of print, PMID: 16427031.
19. Guillaumond, F., Dardente, H., Giguere, V., & Cermakian, N. (2005). Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J. Biol. Rhythms 20, 391-403.
20. Hadj-Sahraoui, N., Frederic, F., Delhaye-Bouchaud, N., & Mariani, J. (1996). Gender effect on Purkinje cell loss in the cerebellum of the heterozygous reeler mouse. J. Neurogenet. 11, 45-58.
21. Hadj-Sahraoui, N., Frederic, F., Zanjani, H., Herrup, K., Delhaye-Bouchaud, N., & Mariani, J. (1997). Purkinje cell loss in heterozygous staggerer mutant mice during aging. Devel. Brain Res. 98, 1-8.
22. Hamilton, B.A., Frankel, W.N., Kerrebrock, A.W., Hawkins, T.L., FitzHugh, W., Kusumi, K., Russell, L.B., Mueller, K.L., van Berkel, V., Birren, B.W., Kruglyak, L., & Lander, E.S. (1996). Disruption of the nuclear hormone receptor RORalpha in staggerer mice. Nature 379, 736-739.
23. Hendry, I.A. (1976). A method to correct adequately for the change in neuronal size when estimating neuronal numbers after nerve growth factor treatment. J. Neurocytol. 5, 337-349.
24. Herrup, K. & Mullen, R.J. (1979a). Regional variation and absence of large neurons in the cerebellum of the staggerer mouse. Brain Res. 172, 1-12.
25. Herrup, K. & Mullen, R.J. (1979b). Staggerer chimeras: intrinsic nature of Purkinje cell defects and implications for normal cerebellar development. Brain Res. 178, 443-457.
26. Herrup, K., Shojaeian-Zanjani, H., Panzini, L., Sunter, K., & Mariani, J. (1996). The numerical matching of source and target populations in the CNS: the inferior olive to Purkinje cell projection. Brain Res Dev Brain Res. 96, 28-35.
27. Ino, H. (2004). Immunohistochemical characterization of the orphan nuclear receptor ROR alpha in the mouse nervous system. J. Histochem. Cytochem. 52, 311-323.
28. Jarvis, C.I., Staels, B., Brugg, B., Lemaigre-Dubreuil, Y., Tedgui, A., & Mariani, J. (2002). Age-related phenotypes in the staggerer mouse expand the RORalpha nuclear receptor's role beyond the cerebellum. Molec. Cell. Endocrinol. 186, 1-5.
29. Kallen, J., Schlaeppi, J.M., Bitsch, F., Delhon, I., & Fournier, B. (2004). Crystal structure of the human RORalpha Ligand binding domain in complex with cholesterol sulfate at 2.2 A. J. Biol. Chem. 279, 14033-14038.
30. Kallen, J.A., Schlaeppi, J.M., Bitsch, F., Geisse, S., Geiser, M., Delhon, I., & Fournier, B. (2002). X-ray structure of the hRORalpha LBD at 1.63 A: structural and functional data that cholesterol or a cholesterol derivative is the natural ligand of RORalpha. Structure 10, 1697-1707.
31. Landis, D.M. & Sidman, R.L. (1978). Electron microscopic analysis of postnatal histogenesis in the cerebellar cortex of staggerer mutant mice. J. Comp. Neurol. 179, 831-863.
32. Lau, P., Bailey, P., Dowhan, D.H., & Muscat, G.E. (1999). Exogenous expression of a dominant negative RORalpha1 vector in muscle cells impairs differentiation: RORalpha1 directly interacts with p300 and myoD. Nucleic Acids Res. 27, 411-420.
33. Matsui, T. (1997). Transcriptional regulation of a Purkinje cell-specific gene through a functional interaction between ROR alpha and RAR. Genes Cells 2, 263-272.
34. Matysiak-Scholze, U. & Nehls, M. (1997). The structural integrity of ROR alpha isoforms is mutated in staggerer mice: cerebellar coexpression of ROR alphal and ROR alpha4. Genomics 43, 78-84.
35. Meyer, T., Kneissel, M., Mariani, J., & Fournier, B. (2000). In vitro and in vivo evidence for orphan nuclear receptor RORalpha function in bone metabolism. Proc. Nat. Acad. Sci. US 97, 9197-9202.
36. Sato, T.K., Panda, S., Miraglia, L.J., Reyes, T.M., Rudic, R.D., McNamara, P., Naik, K. A., FitzGerald, G.A., Kay, S.A., & Hogenesch, J.B. (2004). A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 43, 527-537.
37. Sidman, R.L., Lane, P.W., & Dickie, M.M. (1962). Staggerer, a new mutation in the mouse affecting the cerebellum. Science 137, 610-612.
38. Steinmayr, M., Andre, E., Conquet, F., Rondi-Reig, L., Delhaye-Bouchaud, N., Auclair, N., Daniel, H., Crepel, F., Mariani, J., Sotelo, C., & Becker-Andre, M. (1998). Staggerer phenotype in retinoid-related orphan receptor alpha-deficient mice. Proc. Nat. Acad. Sci. US 95, 3960-3965.
39. Ueda, H.R., Hayashi, S., Chen, W., Sano, M., Machida, M., Shigeyoshi, Y., Iino, M., & Hashimoto, S. (2005). System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nature Genet. 37, 187-192.
40. Vogel, M.W., Sinclair, M., Qiu, D., & Fan, H. (2000). Purkinje cell fate in staggerer mutants: agenesis versus cell death. J. Neurobiol. 42, 323-337.
41. Vogel, M.W., 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.
42. Williams, R.W. & Rakic, P. (1988). Three-dimensional counting: an accurate and direct method to estimate numbers of cells in sectioned material. J. Comp. Neurol. 278, 344-352.
43. Zanjani, H.S., Mariani, J., Delhaye-Bouchaud, N., & Herrup, K. (1992). Neuronal cell loss in heterozygous staggerer mutant mice: a model for genetic contributions to the aging process. Devel. Brain Res. 67, 153-160.
44. Zhu, Y., McAvoy, S., Kuhn, R., & Smith, D.I. (2006). RORA, a large common fragile site gene, is involved in cellular stress response. Oncogene 25, 2901-2908.