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Expression of the Transcription Factor Pax6 in the Lobe of the Facial Nerve of the Carp Brain

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Neurophysiology Aims and scope

Using immunoperoxidase labeling, we examined the distribution of the transcription factor Pax6 in the unpaired lobe of the facial nerve (lobus impar nervi facialis, LINF) of the brain of adult individuals of the carp (Cyprinus carpio). A significant fraction of the cells with expression of the Pax6 protein was localized in the dorsal, lateral, and basal zones of the external LINF layer. Cells with intense Pax6-positivity were usually of a rounded or slightly elongated shape; in most cases they were not grouped. The average diameter of most labelled cells was 5.8 to 9.6 μm; in the basal zone, some cells were larger (mean diameter up to 11.4 μm). The density of localization of Pax6-positive cells within basal zones of the external LINF layer was noticeably greater than that in the dorsal and lateral portions of the above layer. Within the internal LINF layer, cells with a relatively high content of Pax6 were observed, but the optical density of the immunolabelled substance in cells of this layer was several times lower than that in the external layer. Labelled cells in the internal LINF layer formed significant spatial accumulations (niches) separated by regions with no immunonepositivity. Cross-sectional areas of such niches varied from about 460 to 2070 μm2. A considerable part of the cells localized in the internal layer should probably be considered units in the course of migration. Basal regions of the LINF probably represent the most significant region where post-embryonic (“adult”) neurogenesis is realized within this brain structure. Here, cells are formed de novo (mostly in the external layer of the matrix zone), migrate, and undergo differentiation.

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References

  1. N. G. Andreyeva and D. K. Obukhov, Evolutionary Morphology of the Nervous System of Vertebrates, Lan’, St. Petersburg (1999).

    Google Scholar 

  2. P. Ekström, C. M. Johnsson, and L. M. Ohlin, “Ventricular proliferation zones in the brain of an adult teleost fish and their relation to neuromeres and migration zones,” J. Comp. Neurol., 436, 92-110 (2001).

    Article  PubMed  Google Scholar 

  3. G. K. Zupanc, “Neurogenesis, cell death and regeneration in the adult gymnotiform brain,” J. Exp. Biol., 202, 1435-1446 (1999).

    CAS  PubMed  Google Scholar 

  4. J. A. Thompson and М. Ziman, “Pax genes during neural development and their potential role in neuroregeneration,” J. Prog. Neurobiol., 94 , 334-351 (2011).

    Article  Google Scholar 

  5. J. Altman and Е. Das, “Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats,” J. Comp. Neurol., 124, 319-336 (1965).

    Article  CAS  PubMed  Google Scholar 

  6. W. Kirsche, “Überpostembryonale matrix zonen im gehirnverschiedener vertebraten und deren beziehung zur hirnbauplanlehre,” Z. Mikrosk.-Anat. Forsh., 77, 313-406 (1967).

    CAS  Google Scholar 

  7. W. Richter and D. Kranz, “Autoradiographische untersuchungenüber die abhängigkeit des 3H-thymidinindex vom lebensalter in den matrixzonen des telencephalons von Lebistesreticulatus (Teleostei),” Z. Mikrosk.-Anat. Forsh., 81, 530-554 (1970).

    CAS  Google Scholar 

  8. P. Johns, “Formation of photoreceptors in larval and adult goldfish,” J. Neurosci., 2, 178-198 (1982).

    CAS  PubMed  Google Scholar 

  9. P. A. Raymond, S. S. Easter, and J. A. Burnham, “Postembryonic growth of the optic tectum in goldfish. II. Modulation of cell proliferation by retinal fiber input,” J. Neurosci., 3, 1092-1099 (1983).

    CAS  PubMed  Google Scholar 

  10. G. K. Zupanc, K. Hinsch, and F. H. Gage, “Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain,” J. Comp. Neurol., 488, 290-319 (2005).

    Article  PubMed  Google Scholar 

  11. G. K. Zupanc and M. M. Zupanc, “Birth and migration of neurons in the central posterior/prepace- maker nucleus during adulthood in weakly electric knifefish,” Proc. Natl. Acad. Sci. USA, 89, 9539-9543 (1992).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. R. S. Rajendran, M. M. Zupanc, and A. Lösche, “Numerical chromosome variation and mitotic segregation defect in the adult brain of teleost fish,” Dev. Neurobiol., 67, 1334-1347 (2007).

    Article  PubMed  Google Scholar 

  13. G. K. Zupanc and R. Ott, “Cell proliferation after lesions in the cerebellum of adult teleost fish: time course, origin, and type of new cells produced,” Exp. Neurol., 160, 78-87 (1999).

    Article  CAS  PubMed  Google Scholar 

  14. G. K. Zupanc and I. Horschke, “Proliferation zones in the brain of adult gymnotiform fish: a quantitative mapping study,” J. Comp. Neurol., 353, 213-233 (1995).

    Article  CAS  PubMed  Google Scholar 

  15. K. Hinsch and G. K. Zupanc, “Generation and long-term persistence of new neurons in the adult zebrafish brain: a quantitative analysis,” Neuroscience, 146, 679-696 (2007).

    Article  CAS  PubMed  Google Scholar 

  16. C. Lois and A. Alvarez-Buylla, “Long-distance neuronal migration in the adult mammalian brain,” Science, 264, 1145-114 (1994).

    Article  CAS  PubMed  Google Scholar 

  17. R. W. Williams, “Mapping genes that modulate brain development: a quantitative genetic approach,” Mouse Brain Dev., 30, 21-49 (2000).

    Article  CAS  Google Scholar 

  18. H. A. Cameron and R. D. McKay, “Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus,” J. Comp. Neurol., 435, 406-417 (2001).

    Article  CAS  PubMed  Google Scholar 

  19. S. Herculano-Houzel and R. Lent, “Isotropic fractionator: a simple, rapid method for the quantification of total cell and neuron numbers in the brain,” J. Neurosci., 25, 2518-2521 (2005).

    Article  CAS  PubMed  Google Scholar 

  20. E. Pouwels, “On the development of the cerebellum of the trout, Salmo gairdneri: I. Patterns of cell migration,” Anat. Embryol., 152, 291-308 (1978).

    Article  CAS  PubMed  Google Scholar 

  21. А. B. Butler, “Topography and topology of the teleost telencephalon: a paradoxon resolved,” Neurosci. Lett., 293, 95-98 (2000).

    Article  CAS  PubMed  Google Scholar 

  22. M. Portavella, B. Torres, and C. Salas, “Avoidance response in goldfish: emotional and temporal involvement of medial and lateral telencephalicpallium,” J. Neurosci., 24, 2335-2342 (2004).

    Article  CAS  PubMed  Google Scholar 

  23. G. K. Zupanc, “Neurogenesis and neuronal regeneration in the adult fish brain,” J. Comp. Physiol., 192, 649-670 (2006).

    Article  CAS  Google Scholar 

  24. C. Redies, “Modularity in vertebrate brain development and evolution,” BioEssays, 23, 1100-1111 (2001).

    Article  CAS  PubMed  Google Scholar 

  25. C. Soukkarieh, E. Agius, and C. Soula, “Pax2 regulates neuronal-glia cell fate choice in the embryonic optic nerve,” Dev. Biol., 303, 800-813 (2007).

    Article  CAS  PubMed  Google Scholar 

  26. M. Horie and K. Sango, “Subpial neuronal migration in the medulla oblongata of Pax-6-deficient rats,” Eur. J. Neurosci., 17, 49-57 (2003).

    Article  PubMed  Google Scholar 

  27. R. Meech, P. Kallunki, and G. M. Edelman, “A binding site for homeodomain and Pax proteins is necessary for L1 cell adhesion molecule gene expression by Pax-6 and bone morphogenetic proteins,” Proc. Natl. Acad. Sci. USA, 96, 2420-2425 (1999).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. D. Caric, D. Gooday, and R. E. Hill, “Determination of the migratory capacity of embryonic cortical cells lacking the transcription factor Pax6,” Development, 124, 5087- 5096 (1997).

    CAS  PubMed  Google Scholar 

  29. S. Kanakubo, T. Nomura, K. Yamamura, et al., “Abnormal migration and distribution of neural crest cells in Pax6 heterozygous mutant eye, a model for human eye diseases,” Genes Cells, 11, 919-933 (2006).

    Article  CAS  PubMed  Google Scholar 

  30. R. H. Duparc, M. Abdouh, and J. David, “Pax6 controls the proliferation rate of neuroepithelial progenitors from the mouse optic vesicle,” Dev. Biol., 301, 374-387 (2007).

    Article  CAS  PubMed  Google Scholar 

  31. T. Marquardt, R. Ashery-Padan, and N. Andrejewski, “Pax6 is required for the multipotent state of retinal progenitor cells,” Cell, 105, 43-55 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. N. A. Zaghloul, “Alterations of rx1 and pax6 expression levels at neural plate stages differentially affect the production of retinal cell types and maintenance of retinal stem cell qualities,” Dev. Biol., 306, 222-240 (2007).

    Article  CAS  PubMed  Google Scholar 

  33. M. Maekawa, N. Takashima, and Y. Arai, “Pax6 is required for production and maintenance of progenitor cells in postnatal hippocampal neurogenesis,” Genes Cells, 10, 1001-1014 (2005).

    Article  CAS  PubMed  Google Scholar 

  34. M. Kohwi, N. Osumi, and J. L. Rubenstein, “Pax6 is required for making species subpopulations of granule and periglomerularneorones in the olfactory bulb,” J. Neurosci., 25, 6997-7003 (2005).

    Article  CAS  PubMed  Google Scholar 

  35. M. Sugimori, M. Nagao, N. Bertrand, et al., “Combinatorial actions of patterning and HLH transcription factors in the spatiotemporal control of neurogenesis and gliogenesis in the developing spinal cord,” Development, 134, 1617-1629 (2007).

    Article  CAS  PubMed  Google Scholar 

  36. T. C. Tuoc, K. Radyushkin, A. B Tonchev, et al., “Selective cortical layering abnormalities and behavioral deficits in cortex-specific Pax6 knock-out mice,” J. Neurosci., 29, 8335-8349 (2009).

    Article  CAS  PubMed  Google Scholar 

  37. N. Haubst, J. Berger, and V. Radjendirane, “Molecular dissection of Pax6 function: the specific roles of the paired domain and homeodomain in brain development,” Development, 131, 6131-6140 (2004).

    Article  CAS  PubMed  Google Scholar 

  38. H. Nakazaki, A. C. Reddy, and B. L. Mania-Farnell, “Key basic helix-loop-helix transcription factor genes Hes1 and Ngn2 are regulated by Pax3 during mouse embryonic development,” Dev. Biol., 316, 510-523 (2008).

    Article  CAS  PubMed  Google Scholar 

  39. M. F. Wullimann, “The central nervous system,” in: The Physiology of Fishes, Boca Raton, CRS Press, New York (1998), pp. 245-282.

  40. J. D. Burrill, L. Moran, and M. D. Goulding, “PAX2 is expressed in multiple spinal cord interneurons, including a population of EN1+ interneurons that require PAX6 for their development,” Development, 124, 4493-4503

  41. E. Charytonowicz, I. Matushansky, and M. Castillo- Martin, “Alternate PAX3 and PAX7 C-terminal isoforms in myogenic differentiation and sarcomagenesis,” Clin. Trans. Oncol., 13, 194-203 (2011).

  42. J. K. Gerber, T. Richter, and E. Kremmer, “Progressive loss of PAX9 expression correlates with increasing malignancy of dysplastic and cancerous epithelium of the human oesophagus,” J. Pathol., 197, 293-297 (2002).

    Article  CAS  PubMed  Google Scholar 

  43. G. K. Zupanc, Adult Neurogenesis in Teleost Fish, Springer, Tokio (2012).

    Google Scholar 

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Authors and Affiliations

  1. Zhirmunskii Institute of Marine Biology, Far East Division of the Russian Academy of Sciences, Vladivostok, Russia

    M. E. Stukaneva & E. V. Pushchina

  2. Bogomolets Institute of Physiology, National Academy of Sciences of Ukraine, Kyiv, Ukraine

    E. V. Pushchina

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  1. M. E. Stukaneva
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Correspondence to E. V. Pushchina.

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Stukaneva, M.E., Pushchina, E.V. Expression of the Transcription Factor Pax6 in the Lobe of the Facial Nerve of the Carp Brain. Neurophysiology 47, 277–286 (2015). https://doi.org/10.1007/s11062-015-9534-x

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