Anatomy and Cell Biology

Korean Association of Anatomists (대한해부학회)
권호 표지
DOI QR코드

DOI QR Code

Differential regulation of Purkinje cell dendritic spines in rolling mouse Nagoya ($tg^{rol}/tg^{rol}$), P/Q type calcium channel (${\alpha}1_A/Ca_v2.1$) mutant

  • Oda, Sen-Ich (Laboratory of Animal Management, School of Agricultural Science, Nagoya University) ;
  • Lee, Kea-Joo (Department of Anatomy, College of Medicine and Human Genetics, Korea University) ;
  • Arii, Tatsuo (Section of Brain Structure, Center for Brain Experiment) ;
  • Imoto, Keiji (Department of Information Physiology, National Institute for Physiological Sciences) ;
  • Hyun, Byung-Hwa (Genetic Resource Center, Korea Research Institute of Bioscience and Biotechnology, KRIBB) ;
  • Park, In-Sung (Department of Anatomy, College of Medicine and Human Genetics, Korea University) ;
  • Kim, Hyun (Department of Anatomy, College of Medicine and Human Genetics, Korea University) ;
  • Rhyu, Im-Joo (Department of Anatomy, College of Medicine and Human Genetics, Korea University)
  • Received : 2010.05.10
  • Accepted : 2010.08.26
  • Published : 2010.09.30
⟨ Previous Next ⟩

Abstract

Voltage dependent calcium channels (VDCC) participate in regulation of neuronal $Ca^{2+}$. The Rolling mouse Nagoya ($Cacna1a^{tg-rol}$) is a spontaneous P/Q type VDCC mutant, which has been suggested as an animal model for some human neurological diseases such as autosomal dominant cerebellar ataxia (SCA6), familial hemiplegic migraine and episodic ataxia type-2. Morphology of Purkinje cell (PC) dendritic spine is suggested to be regulated by signal molecules such as $Ca^{2+}$ and by interactions with afferent inputs. The amplitude of excitatory postsynaptic current was decreased in parallel fiber (PF) to PC synapses, whereas apparently increased in climbing fiber (CF) to PC synapses in rolling mice Nagoya. We have studied synaptic morphology changes in cerebella of this mutant strain. We previously found altered synapses between PF varicosity and PC dendritic spines. To study dendritic spine plasticity of PC in the condition of insufficient P/Q type VDCC function, we used high voltage electron microscopy (HVEM). We measured the density and length of PC dendritic spines at tertiary braches. We observed statistically a significant decrease in spine density as well as shorter spine length in rolling mice compared to wild type mice at tertiary dendritic braches. In proximal PC dendrites, however, there were more numerous dendritic spines in rolling mice Nagoya. The differential regulation of rolling PC spines at tertiary and proximal dendrites in rolling mice Nagoya suggests that two major excitatory afferent systems may be regulated reciprocally in the cerebellum of rolling mouse Nagoya.

Keywords

References

  1. Austin MC, Schultzberg M, Abbott LC, et al. (1992). Expression of tyrosine hydroxylase in cerebellar Purkinje neurons of the mutant tottering and leaner mouse. Brain Res Mol Brain Res 15: 227-240 https://doi.org/10.1016/0169-328X(92)90113-P
  2. Cicale M, Ambesi-Impiombato A, Cimini V, et al. (2002). Decreased gene expression of calretinin and ryanodine receptor type 1 in tottering mice. Brain Res Bull 59: 53-58 https://doi.org/10.1016/S0361-9230(02)00841-9
  3. Ertel EA, Campbell KP, Harpold MM, et al. (2000). Nomenclature of voltage-gated calcium channels. Neuron 25: 533-535 https://doi.org/10.1016/S0896-6273(00)81057-0
  4. Ghosh A, Greenberg ME. (1995).Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268: 239-247 https://doi.org/10.1126/science.7716515
  5. Hama K, Arii T, Kosaka T. (1989). Three-dimensional morphometrical study of dendritic spines of the granule cell in the rat dentate gyrus with HVEM stereo images. J Electron Microsc Tech 12: 80-87 https://doi.org/10.1002/jemt.1060120203
  6. Hama K, Kosaka T. (1979). Purkinje cell and related neurons and glial cells under high voltage electron microscopy. In Zimmerman HM, ed. Progress in neuropathology. New York, Raven Press, 61-77
  7. Harris KM, Stevens JK. (1988). Dendritic spines of rat cerebellar Purkinje cells: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 8: 4455-4469
  8. Huang CM, Brown N, Huang RH. (1999). Age-related changes in the cerebellum: parallel fibers. Brain Res 840: 148-152 https://doi.org/10.1016/S0006-8993(99)01707-2
  9. Isaacs KR, Abbott LC. (1995). Cerebellar volume decreases in the tottering mouse are specific to the molecular layer. Brain Res Bull 36: 309-314 https://doi.org/10.1016/0361-9230(94)00207-H
  10. Jun K, Piedras-Renteria ES, Smith SM, et al. (1999). Ablation of P/Q-type Ca(2+) channel currents, altered synaptic transmission, and progressive ataxia in mice lacking the alpha(1A)-subunit. Proc Natl Acad Sci USA 96: 15245-15250 https://doi.org/10.1073/pnas.96.26.15245
  11. Lee KJ, Kim H, Kim TS, Park SH, Rhyu IJ. (2004). Morphological analysis of spine shapes of Purkinje cell dendrites in the rat cerebellum using high-voltage electron microscopy. Neurosci Lett 359: 21-24 https://doi.org/10.1016/j.neulet.2004.01.071
  12. Llinas RR. (1988). The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242: 1654-1664 https://doi.org/10.1126/science.3059497
  13. Matsushita K, Wakamori M, Rhyu IJ, et al. (2002). Bidirectional alterations in cerebellar synaptic transmission of tottering and rolling Ca2+ channel mutant mice. J Neurosci 22: 4388-4398
  14. Mori Y, Wakamori M, Oda S, et al. (2000). Reduced voltage sensitivity of activation of P/Q-type Ca2+ channels is associated with the ataxic mouse mutation rolling Nagoya (tg(rol)). J Neurosci 20: 5654-5662
  15. Oda S. (1973). The observation of rolling mouse Nagoya (rol), a new neurological mutant, and its maintenance (author's transl). Jikken Dobutsu 22: 281-288
  16. Ophoff RA, Terwindt GM, Vergouwe MN, et al. (1996). Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca2+ channel gene CACNL1A4. Cell 87: 543-552 https://doi.org/10.1016/S0092-8674(00)81373-2
  17. Palay SL, Chan-Palay V. (1974). Cerebellar cortex - cytology and organization. New York, Berlin, Springer-Verlag
  18. Pietrobon D. (2002). Calcium channels and channelopathies of the central nervous system. Mol Neurobiol 25: 31-50 https://doi.org/10.1385/MN:25:1:031
  19. Rhyu IJ, Abbott LC, Walker DB, Sotelo C. (1999a). An ultrastructural study of granule cell/Purkinje cell synapses in tottering (tg/tg), leaner (tg(la)/tg(la)) and compound heterozygous tottering/leaner (tg/tg(la)) mice. Neuroscience 90: 717-728 https://doi.org/10.1016/S0306-4522(98)00518-1
  20. Rhyu IJ, Cho TH, Lee NJ, Uhm CS, Kim H, Suh YS. (1999b). Magnetic resonance image-based cerebellar volumetry in healthy Korean adults. Neurosci Lett 270: 149-152 https://doi.org/10.1016/S0304-3940(99)00487-5
  21. Rhyu IJ, Nahm SS, Hwang SJ, et al. (2003). Altered neuronal nitric oxide synthase expression in the cerebellum of calcium channel mutant mice. Brain Res 977: 129-140 https://doi.org/10.1016/S0006-8993(03)02403-X
  22. Rhyu IJ, Oda S, Uhm CS, Kim H, Suh YS, Abbott LC. (1999c). Morphologic investigation of rolling mouse Nagoya (tg(rol)/tg(rol)) cerebellar Purkinje cells: an ataxic mutant, revisited. Neurosci Lett 266: 49-52 https://doi.org/10.1016/S0304-3940(99)00254-2
  23. Segal I, Korkotian I, Murphy DD. (2000). Dendritic spine formation and pruning: common cellular mechanisms? Trends Neurosci 23: 53-57 https://doi.org/10.1016/S0166-2236(99)01499-X
  24. Strata P, Morando L, Bravin M, Rossi F. (2000). Dendritic spine density in Purkinje cells. Trends Neurosci 23: 198
  25. Suh YS, Oda S, Kang YH, Kim H, Rhyu IJ. (2002). Apoptotic cell death of cerebellar granule cells in rolling mouse Nagoya. Neurosci Lett 325: 1-4 https://doi.org/10.1016/S0304-3940(02)00216-1
  26. Tsien RW, Tsien RY. (1990). Calcium channels, stores, and oscillations. Annu Rev Cell Biol 6: 715-760 https://doi.org/10.1146/annurev.cb.06.110190.003435
  27. Vecellio M, Schwaller B, Meyer M, Hunziker W, Celio MR. (2000). Alterations in Purkinje cell spines of calbindin D-28 k and parvalbumin knock-out mice. Eur J Neurosci 12: 945-954 https://doi.org/10.1046/j.1460-9568.2000.00986.x
  28. Westenbroek RE, Sakurai T, Elliott EM, et al. (1995). Immunochemical identification and subcellular distribution of the alpha 1A subunits of brain calcium channels. J Neurosci 15: 6403-6418
  29. Wheeler DB, Randall A, Tsien RW. (1994). Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science 264: 107-111 https://doi.org/10.1126/science.7832825
  30. Zhuchenko O, Bailey J, Bonnen P, et al. (1997). Autosomal dominant cerebellar ataxia (SCA6) associated with small polyglutamine expansions in the alpha 1A-voltage-dependent calcium channel. Nat Genet 15: 62-69 https://doi.org/10.1038/ng0197-62
  31. Zwingman TA, Neumann PE, Noebels JL, Herrup K. (2001). Rocker is a new variant of the voltage-dependent calcium channel gene Cacnala. J Neurosci 21: 1169-1178

Cited by

  1. Comprehensive Review of Golgi Staining Methods for Nervous Tissue vol.47, pp.2, 2010, https://doi.org/10.9729/am.2017.47.2.63
  2. High Voltage Electron Microscopic Image of Red Blood Cell in the Blood Vessel of Mouse Brain vol.47, pp.2, 2017, https://doi.org/10.9729/am.2017.47.2.75
  3. Bergman glial cell morphology under the high voltage Electron microscope vol.49, pp.None, 2019, https://doi.org/10.1186/s42649-019-0007-3
  4. Cerebellar developmental deficits underlie neurodegenerative disorder spinocerebellar ataxia type 23 vol.31, pp.2, 2010, https://doi.org/10.1111/bpa.12905