Selective and regulated gene expression in murine Purkinje cells by in utero electroporation

European Journal of Neuroscience

Volumn 36, Issue 7, 2012, Pages 2867-2876

  Nishiyama, Jun ^a,c   Hayashi, Yukari ^a,b   Nomura, Toshihiro ^a,b   Miura, Eriko ^a,b   Kakegawa, Wataru ^a,b   Yuzaki, Michisuke ^a,b  

^a KEIO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cerebellum; Mouse; Retinoid related orphan receptor ; staggerer

Indexed keywords

BASSOON; CRE RECOMBINASE; CYAN FLUORESCENT PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; FLUORESCENT DYE; RED FLUORESCENT PROTEIN; RETINOID RELATED ORPHAN RECEPTOR ALPHA; SYNAPSE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CEREBELLUM CORTEX; CONTROLLED STUDY; ELECTROPORATION; GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; IN UTERO ELECTROPORATION; IN VIVO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; NEURAL STEM CELL; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PURKINJE CELL; RORALPHA1 GEN; SYNAPTIC TRANSMISSION; TRANSGENE;

ANIMALS; ELECTROPORATION; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VECTORS; MEMBRANE POTENTIALS; MICE; MICE, NEUROLOGIC MUTANTS; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 1; PREGNANCY; PROMOTER REGIONS, GENETIC; PURKINJE CELLS; SYNAPTIC TRANSMISSION; TRANSFECTION; TRANSGENES;

EID: 84867032981     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08203.x     Document Type: Article

References (48)

1. Agudo, M., Trejo, J.L., Lim, F., Avila, J., Torres-Aleman, I., Diaz-Nido, J. & Wandosell, F. (2002) Highly efficient and specific gene transfer to Purkinje cells in vivo using a herpes simplex virus I amplicon. Hum. Gene Ther., 13, 665-674.
2. Altman, J. & Bayer, S.A. (1997). Development of the Cerebellar System: in Relation to its Evolution, Structure and Functions. CRC Press, Boca Raton, FL.
3. Barnabe-Heider, F., Meletis, K., Eriksson, M., Bergmann, O., Sabelstrom, H., Harvey, M.A., Mikkers, H. & Frisen, J. (2008) Genetic manipulation of adult mouse neurogenic niches by in vivo electroporation. Nat. Methods, 5, 189-196.
4. Berrebi, A.S., Morgan, J.I. & Mugnaini, E. (1990) The Purkinje cell class may extend beyond the cerebellum. J. Neurocytol., 19, 643-654.
5. Bonnin, A., Torii, M., Wang, L., Rakic, P. & Levitt, P. (2007) Serotonin modulates the response of embryonic thalamocortical axons to netrin-1. Nat. Neurosci., 10, 588-597.
6. Boukhtouche, F., Doulazmi, M., Frederic, F., Dusart, I., Brugg, B. & Mariani, J. (2006) RORalpha, a pivotal nuclear receptor for Purkinje neuron survival and differentiation: from development to ageing. Cerebellum, 5, 97-104.
7. De Vry, J., Martinez-Martinez, P., Losen, M., Temel, Y., Steckler, T., Steinbusch, H.W., De Baets, M.H. & Prickaerts, J. (2010) In vivo electroporation of the central nervous system: a non-viral approach for targeted gene delivery. Prog. Neurobiol., 92, 227-244.
8. tom Dieck, S., Sanmarti-Vila, L., Langnaese, K., Richter, K., Kindler, S., Soyke, A., Wex, H., Smalla, K.H., Kampf, U., Franzer, J.T., Stumm, M., Garner, C.C. & Gundelfinger, E.D. (1998) Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals. J. Cell Biol., 142, 499-509.
9. 2+channels. Proc. Natl. Acad. Sci. USA, 99, 14458-14463.
10. 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.
11. Hashimoto, M. & Mikoshiba, K. (2003) Mediolateral compartmentalization of the cerebellum is determined on the 'birth date' of Purkinje cells. J. Neurosci., 23, 11342-11351.
12. Hashimoto, M., Aruga, J., Hosoya, Y., Kanegae, Y., Saito, I. & Mikoshiba, K. (1996) A neural cell-type-specific expression system using recombinant adenovirus vectors. Hum. Gene Ther., 7, 149-158.
13. Hirai, H. (2008) Progress in transduction of cerebellar Purkinje cells in vivo using viral vectors. Cerebellum, 7, 273-278.
14. Ito, M. (1989) Long-term depression. Annu. Rev. Neurosci., 12, 85-102.
15. Kaemmerer, W.F., Reddy, R.G., Warlick, C.A., Hartung, S.D., McIvor, R.S. & Low, W.C. (2000) In vivo transduction of cerebellar Purkinje cells using adeno-associated virus vectors. Mol. Ther., 2, 446-457.
16. Kakegawa, W., Miyazaki, T., Kohda, K., Matsuda, K., Emi, K., Motohashi, J., Watanabe, M. & Yuzaki, M. (2009) The N-terminal domain of GluD2 (GluRdelta2) recruits presynaptic terminals and regulates synaptogenesis in the cerebellum in vivo. J. Neurosci., 29, 5738-5748.
17. Kakegawa, W., Miyoshi, Y., Hamase, K., Matsuda, S., Matsuda, K., Kohda, K., Emi, K., Motohashi, J., Konno, R., Zaitsu, K. & Yuzaki, M. (2011) D-serine regulates cerebellar LTD and motor coordination through the delta2 glutamate receptor. Nat. Neurosci., 14, 603-611.
18. Kawauchi, D. & Saito, T. (2008) Transcriptional cascade from Math1 to Mbh1 and Mbh2 is required for cerebellar granule cell differentiation. Dev. Biol., 322, 345-354.
19. Kawauchi, D., Taniguchi, H., Watanabe, H., Saito, T. & Murakami, F. (2006) Direct visualization of nucleogenesis by precerebellar neurons: involvement of ventricle-directed, radial fibre-associated migration. Development, 133, 1113-1123.
20. Kohda, K., Kakegawa, W., Matsuda, S., Nakagami, R., Kakiya, N. & Yuzaki, M. (2007) The extreme C-terminus of GluRdelta2 is essential for induction of long-term depression in cerebellar slices. Eur. J. Neurosci., 25, 1357-1362.
21. Kolk, S.M., de Mooij-Malsen, A.J. & Martens, G.J. (2011) Spatiotemporal molecular approach of in utero electroporation to functionally decipher endophenotypes in neurodevelopmental disorders. Front. Mol. Neurosci., 4, 37.
22. 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.
23. Lau, P., Nixon, S.J., Parton, R.G. & Muscat, G.E. (2004) RORalpha regulates the expression of genes involved in lipid homeostasis in skeletal muscle cells: caveolin-3 and CPT-1 are direct targets of ROR. J. Biol. Chem., 279, 36828-36840.
24. Matsuda, T. & Cepko, C.L. (2004) Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc. Natl. Acad. Sci. USA, 101, 16-22.
25. Matsuda, T. & Cepko, C.L. (2007) Controlled expression of transgenes introduced by in vivo electroporation. Proc. Natl. Acad. Sci. USA, 104, 1027-1032.
26. Miale, I.L. & Sidman, R.L. (1961) An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp. Neurol., 4, 277-296.
27. Miyazaki, T., Fukaya, M., Shimizu, H. & Watanabe, M. (2003) Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum. Eur. J. Neurosci., 17, 2563-2572.
28. Nakagawa, S., Watanabe, M., Isobe, T., Kondo, H. & Inoue, Y. (1998) Cytological compartmentalization in the staggerer cerebellum, as revealed by calbindin immunohistochemistry for Purkinje cells. J. Comp. Neurol., 395, 112-120.
29. Navarro-Quiroga, I., Chittajallu, R., Gallo, V. & Haydar, T.F. (2007) Long-term, selective gene expression in developing and adult hippocampal pyramidal neurons using focal in utero electroporation. J. Neurosci., 27, 5007-5011.
30. Oberdick, J., Smeyne, R.J., Mann, J.R., Zackson, S. & Morgan, J.I. (1990) A promoter that drives transgene expression in cerebellar Purkinje and retinal bipolar neurons. Science, 248, 223-226.
31. Pierce, E.T. (1967) Histogenesis of the dorsal and ventral cochlear nuclei in the mouse. An autoradiographic study. J. Comp. Neurol., 131, 27-54.
32. Saito, T. & Nakatsuji, N. (2001) Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev. Biol., 240, 237-246.
33. Sidman, R.L., Lane, P.W. & Dickie, M.M. (1962) Staggerer, a new mutation in the mouse affecting the cerebellum. Science, 137, 610-612.
34. Slemmer, J.E., De Zeeuw, C.I. & Weber, J.T. (2005) Don't get too excited: mechanisms of glutamate-mediated Purkinje cell death. Prog. Brain Res., 148, 367-390.
35. Smeyne, R.J., Oberdick, J., Schilling, K., Berrebi, A.S., Mugnaini, E. & Morgan, J.I. (1991) Dynamic organization of developing Purkinje cells revealed by transgene expression. Science, 254, 719-721.
36. Soha, J.M. & Herrup, K. (1995) Stunted morphologies of cerebellar Purkinje cells in lurcher and staggerer mice are cell-intrinsic effects of the mutant genes. J. Comp. Neurol., 357, 65-75.
37. Sotelo, C. & Dusart, I. (2009) Intrinsic versus extrinsic determinants during the development of Purkinje cell dendrites. Neuroscience, 162, 589-600.
38. Tabata, H. & Nakajima, K. (2001) Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience, 103, 865-872.
39. Takayama, K., Torashima, T., Horiuchi, H. & Hirai, H. (2008) Purkinje-cell-preferential transduction by lentiviral vectors with the murine stem cell virus promoter. Neurosci. Lett., 443, 7-11.
40. Tamada, A., Kumada, T., Zhu, Y., Matsumoto, T., Hatanaka, Y., Muguruma, K., Chen, Z., Tanabe, Y., Torigoe, M., Yamauchi, K., Oyama, H., Nishida, K. & Murakami, F. (2008) Crucial roles of Robo proteins in midline crossing of cerebellofugal axons and lack of their up-regulation after midline crossing. Neural Dev., 3, 29.
41. Terashima, T., Miwa, A., Kanegae, Y., Saito, I. & Okado, H. (1997) Retrograde and anterograde labeling of cerebellar afferent projection by the injection of recombinant adenoviral vectors into the mouse cerebellar cortex. Anat. Embryol. (Berl), 196, 363-382.
42. Tomomura, M., Rice, D.S., Morgan, J.I. & Yuzaki, M. (2001) Purification of Purkinje cells by fluorescence-activated cell sorting from transgenic mice that express green fluorescent protein. Eur. J. Neurosci., 14, 57-63.
43. Torashima, T., Okoyama, S., Nishizaki, T. & Hirai, H. (2006) In vivo transduction of murine cerebellar Purkinje cells by HIV-derived lentiviral vectors. Brain Res., 1082, 11-22.
44. Wang, V.Y. & Zoghbi, H.Y. (2001) Genetic regulation of cerebellar development. Nat. Rev. Neurosci., 2, 484-491.
45. Wang, V.Y., Rose, M.F. & Zoghbi, H.Y. (2005) Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron, 48, 31-43.
46. Wu, Z., Yang, H. & Colosi, P. (2010) Effect of genome size on AAV vector packaging. Mol. Ther., 18, 80-86.
47. Yuzaki, M. (2005) Transgenic rescue for characterizing orphan receptors: a review of delta2 glutamate receptor. Transgenic Res., 14, 117-121.
48. Zimmermann, T., Rietdorf, J. & Pepperkok, R. (2003) Spectral imaging and its applications in live cell microscopy. FEBS Lett., 546, 87-92.