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BDNF and trkB mRNA Expression in Neurons of the Neonatal Mouse Barrel Field Cortex: Normal Development and Plasticity after Cauterizing Facial Vibrissae

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Abstract

Development of the central somatosensory system is profoundly modulated by the sensory periphery. Cauterization of facial whiskers alters the segregation pattern of barrels in rodents only during a few days just after birth (critical period). Although a molecular basis of the segregation of barrel neurons and the critical period for the anatomical plasticity observed in layer IV barrel neuron is not clear yet, the accumulating evidence suggests that neurotrophins modulate synaptic connections including central nervous system. In this study, we showed by in situ hybridization that mouse barrel side neurons express brain-derived neurotrophic factor (BDNF) mRNA and both catalytic and non-catalytic forms of trkB mRNA. Cautery of row C vibrissae on the right side of the face within 24 h after birth (post natal day 0, PND0) reduced the expression of BDNF and trkB mRNA from the division region between the contralateral row C barrels at PND7. The vibrissae in row A, C, and E were cauterized at PND0 followed by quantitative RT-PCR for BDNF and trkB mRNA with total RNA isolated from the barrel region at PND7. The result showed that BDNF, but not trkB, mRNA was increased several-fold in the contralateral barrel region. These data suggest that the expression of BDNF mRNA is differentially regulated between injured barrels and actively innervated barrels. The differential expression of the mRNA encoding neurotrophins and their receptors may be important in regulating the injury-dependent re-segregation of barrels.

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REFERENCES

  1. Hubel, D. H. 1982. Exploration of the primary visual cortex, 1955–78. Nature 299:515–524.

    Google Scholar 

  2. LeVay, S., Wiesel, T. N., and Hubel, D. H. 1980. The development of ocular dominance columns in normal and visually deprived monkeys. J. Comp. Neurol. 191:1–51.

    Google Scholar 

  3. Snider, W. D. 1994. Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77:627–638.

    Google Scholar 

  4. Glass, D. J., Nye, S. H., Hantzopoulos, P., Macchi, M. J., Squinto, S. P., Goldfarb, M., and Yancopoulos, G. D. 1991. TrkB mediates BDNF/NT-3-dependent survival and proliferation in fibroblasts lacking the low affinity NGF receptor. Cell 66:405–413.

    Google Scholar 

  5. Soppet, D., Escandon, E., Maragos, J., Middlemas, D. S., Reid, S. W., Blair, J., Burton, L. E., Stanton, B. R., Kaplan, D. R., Hunter, T., Nikolics, K., and Parada, L. F. 1991. The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65:895–903.

    Google Scholar 

  6. Barbacid, M., Lamballe, F., Pulido, D., and Klein, R. 1991. The trk family of tyrosine protein kinase receptors. Biochim. Biophys. Acta 1072:115–127.

    Google Scholar 

  7. Lindholm, D., Castren, E., Berzaghi, M., Blochl, A., and Thoenen, H. 1994. Activity-dependent and hormonal regulation of neurotrophin mRNA levels in the brain—implications for neuronal plasticity. J. Neurobiol. 25:1362–1372.

    Google Scholar 

  8. Katz, L. C., and Shatz, C. J. 1996. Synaptic activity and the construction of cortical circuits. Science 274:1133–1138.

    Google Scholar 

  9. Durham, D., and Woolsey, T. A. 1984. Effects of neonatal whisker lesions on mouse central trigeminal pathways. J. Comp. Neurol. 223:424–447.

    Google Scholar 

  10. Woolsey, T. A., and Wann, J. R. 1976. Areal changes in mouse cortical barrels following vibrissal damage at different postnatal ages. J. Comp. Neurol. 170:53–66.

    Google Scholar 

  11. Harris, R. M., and Woolsey, T. A. 1981. Dendritic plasticity in mouse barrel cortex following postnatal vibrissa follicle damage. J. Comp. Neurol. 196:357–376.

    Google Scholar 

  12. Fox, K. 1992. A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J. Neurosci. 12:1826–1838.

    Google Scholar 

  13. McCasland, J. S., Bernardo, K. L., Probst, K. L., and Woolsey, T. A. 1992. Cortical local circuit axons do not mature after early deafferentation. Proc. Natl. Acad. Sci. USA 89:1832–1836.

    Google Scholar 

  14. Diamond, M. E., Huang, W., and Ebner, F. F. 1994. Laminar comparison of somatosensory cortical plasticity. Science 265: 1885–1888.

    Google Scholar 

  15. Li, Y., Erzurumlu, R. S., Chen, C., Jhaveri, S., and Tonegawa, S. 1994. Whisker-related neuronal patterns fail to develop in the trigeminal brainstem nuclei of NMDAR1 knockout mice. Cell 76: 427–437.

    Google Scholar 

  16. Kutusuwada, T., Sakimura, K., Manabe, T., Takayama, C., Katakura, N., Kushiya, E., Natsume, R., Watanabe, M., Inoue, Y., Yagi, T., Aizawa, S., Arakawa, M., Takahashi, T., Nakamura, Y., Mori, H., and Mishina, M. 1996. Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor ε2 subunit mutant mice. Neuron 16:333–344.

    Google Scholar 

  17. Schlaggar, B. L., Fox, K., and O'Leary, D. D. Postsynaptic control of plasticity in developing somatosensory cortex. Nature 364:623–626.

  18. Crair, M. C., and Malenka, R. C. 1995. A critical period for long-term potentiation at thalamocortical synapses. Nature 375:325–328.

    Google Scholar 

  19. Cabelli, R. J., Hohn, A., and Shatz, C. J. 1995. Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 267:1662–1666.

    Google Scholar 

  20. Riddle, D., Lo, D., and Katz, L. NT-4-mediated rescue of lateral geniculate neurons from effects of monocular deprivation. Nature 378:189–191.

  21. Prakash, N., Cohen-Cory, S., and Frostig, R. D. 1996. Rapid and opposite effects of BDNF and NGF on the functional organization of the adult cortex in vivo. Nature 381:702–706.

    Google Scholar 

  22. Lohof, A. M., Ip, N. Y., and Poo, M.-m. 1993. Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363:350–353.

    Google Scholar 

  23. Kang, H., and Schuman, E. M. 1995. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267:1658–1662.

    Google Scholar 

  24. Levine, E. S., Dreyfus, C. F., Black, I. B., and Plummer, M. R. 1995. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl. Aca. Sci. USA 92:8074–8077.

    Google Scholar 

  25. Strominger, R. N., and Woolsey, T. A. 1987. Templates for locating the whisker area in fresh flattened mouse and rat cortex. J. Neurosci. Methods 22:113–118.

    Google Scholar 

  26. Klein, R., Parada, L. F., Coulier, F., and Barbacid, M. 1989. trkB, a novel tyrosine protein kinase receptor expressed during mouse neural development. EMBO J. 8:3701–3709.

    Google Scholar 

  27. Klein, R., Conway, D., Parada, L. F., and Barbacid, M. 1990. The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 61:647–656.

    Google Scholar 

  28. Chomczynski, P., and Sacchi, N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol chloroform extraction. Anal. Biochem. 162:156–159.

    Google Scholar 

  29. Masana, Y., Wanaka, A., Kato, H., Asai, T., and Tohyama, M. 1993. Localization of trkB mRNA in postnatal brain development. J. Neurosci. Res. 35:468–479.

    Google Scholar 

  30. Allendoerfer, K. L., Cabelli, R. J., Escandon, E., Kaplan, D. R., Nikolics, K., and Shatz, C. J. 1994. Regulation of neurotrophin receptors during the maturation of the mammalian visual system. J. Neurosci. 14:1795–1811.

    Google Scholar 

  31. Mcallister, A., Lo, D., and Katz, L. 1995. Neurotrophins regulate dendritic growth in developing visual-cortex. Neuron 15:791–803.

    Google Scholar 

  32. Crossin, K. L., Hoffman, S., Tan, S. S., and Edelman, G. M. 1989. Cytotactin and its proteoglycan ligand mark structural and functional boundaries in somatosensory cortex of the early postnatal mouse. Dev. Biol. 136:381–392.

    Google Scholar 

  33. Erzurumlu, R. S., Jhaveri, S., and Benowitz, L. I. 1990. Transient patterns of GAP-43 expression during the formation of barrels in the rat somatosensory cortex. J. Comp. Neurol. 292:443–456.

    Google Scholar 

  34. Woolsey, T. A., Dierker, M. L., and Wann, D. F. 1975. Mouse SmI cortex: qualitative and quantitative classification of golgi-impregnated barrel neurons. Proc. Natl. Acad. Sci. USA 72:2165–2169.

    Google Scholar 

  35. White, E. L. 1978. Identified neurons in mouse Sml cortex which are postsynaptic to thalamocortical axon terminals: a combined Golgi-electron microscopic and degeneration study. J. Comp. Neurol. 181:627–661.

    Google Scholar 

  36. Rocamora, N., Welker, E., Pascual, M., and Soriano, E. 1996. Upregulation of BDNF mRNA expression in the barrel cortex of adult mice after sensory stimulation. J. Neurosci. 16:4411–4419.

    Google Scholar 

  37. Zafra, F., Lindholm, D., Castren, E., Hartikka, J., and Thoenen, H. 1992. Regulation of brain-derived neurotrophic factor and nerve growth factor mRNA in primary cultures of hippocampal neurons and astrocytes. J. Neurosci. 12:4793–4799.

    Google Scholar 

  38. Schlaggar, B. L., and O'Leary, D. D. 1993. Patterning of the barrel field in somatosensory cortex with implications for the specification of neocortical areas. Perspect. Dev. Neurobiol. 1:81–91.

    Google Scholar 

  39. Ernfors, P., Rosario, C. M., Merlio, J. P., Grant, G., Aldskogius, H., and Persson, H. 1993. Expression of mRNAs for neurotrophin receptors in the dorsal root ganglion and spinal cord during development and following peripheral or central axotomy. Mol. Brain Res. 17:217–226.

    Google Scholar 

  40. Sebert, M. E., and Shooter, E. M. 1993. Expression of mRNA for neurotrophic factors and their receptors in the rat dorsal root ganglion and sciatic nerve following nerve injury. J. Neurosci. Res. 36:357–367.

    Google Scholar 

  41. Henderson, T. A., Rhoades, R. W., Bennett-Clarke, C. A., Osborne, P. A., Johnson, E. M., and Jacquin, M. F. 1993. NGF augmentation rescues trigeminal ganglion and principalis neurons, but not brainstem or cortical whisker patterns, after infraorbital nerve injury at birth. J Comp. Neurol. 336:243–260.

    Google Scholar 

  42. Ernfors, P., Lee, K.-F., and Jaenlsch, R. 1994. Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368:147–150.

    Google Scholar 

  43. Jones, K. R., Farinas, I., Backus, C., and Reichardt, L. F. 1994. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76: 989–999.

    Google Scholar 

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Authors and Affiliations

  1. Division of Biochemistry and Cellular Biology, National Institute of Neuroscience, 4-1-1 Ogawahigashi, Kodaira, Tokyo, 187, Japan

    Tryambak Deo Singh, Kiyonobu Mizuno, Tomoko Kohno & Shun Nakamura

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  1. Tryambak Deo Singh
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  2. Kiyonobu Mizuno
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  3. Tomoko Kohno
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  4. Shun Nakamura
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Correspondence to Shun Nakamura.

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Singh, T.D., Mizuno, K., Kohno, T. et al. BDNF and trkB mRNA Expression in Neurons of the Neonatal Mouse Barrel Field Cortex: Normal Development and Plasticity after Cauterizing Facial Vibrissae. Neurochem Res 22, 791–797 (1997). https://doi.org/10.1023/A:1022075508176

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