Nitric oxide-factor, which regulates proliferation and apoptosis in the adult brain of amur sturgeon <i>Acipenser schrenckii</i> — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Nitric oxide-factor, which regulates proliferation and apoptosis in the adult brain of amur sturgeon <i>Acipenser schrenckii</i>
A.V. Zhyrmunskii Institute of Marine Biology, Far East Division, Russian Academy of Sciences, Vladivostok, Russia
,
St.Petersburg State University, St. Petersburg, Russia
1 A.V. Zhyrmunskii Institute of Marine Biology, Far East Division, Russian Academy of Sciences, Vladivostok, Russia
2 St.Petersburg State University, St. Petersburg, Russia
The distribution of proliferative zones, NO-producing cells and apoptosis areas in the medulla oblongata, cerebellum, optic tectum, thalamus and hypothalamus of Amur sturgeon Acipenser schrenckii was investigated, using techniques of immunoperoxidase staining of proliferating cell nuclear antigen (PCNA), neuronal nitric oxide synthase and TU-NEL-labeling of fragmented DNA. It has been established, that in the sturgeon brain NO can act both as a cytotoxic proapoptogenic factor, and as a factor, which stimulates cell proliferation. The presence of NO-producing elements in somato- and viscerosensory areas of medulla oblongata, tectum, cerebellum and thalamus suppose, that in these brain areas NO constitutes apoptogenic factor, which induces the cells death in a territory of postmitotic neuroblasts, renders controlling effect on development and differentiating of chemosensory, visual, motor and hypophysotropic brain areas in postnatal ontogenesis. Maximal proliferating activity and high concentration of NO-ergic cells were revealed in external layers, adjoining to the medullar, cerebellar and tectum membranes, that allow to suppose NO participation in postnatal morphogenesis of these brain structures as a factor, which regulates cell proliferation. In sensory centers (tectum and nuclei of the V, VII, and X nerves), significantly varying ratios of intensities of proliferation and apoptosis were found; this is indicative of dissimilar rates of growth and differentiation in visual and chemosensory centers of the sturgeon brain. Presence of NO-producing elements in the PCNA- immuno-labeling and TUNEL-labeling brain areas allow to consider NO as a factor, which balances processes of proliferation and apoptosis in the sturgeon brain.
KeywordsAdult NeurogenesisNitric OxideApoptosisSturgeonNeoteniaDevelopment of Sensory Systems
Zupanc, G.K.H., Hinsch, K., Gagr, F.H. (2005). Proliferation, migration, neuronal differentiation and long-term survival of new cells in the adult zebrafish brain. J. Comp. Neurol. 488, 290–319. http://onlinelibrary.wiley.com/doi:10.1002/cne.20571
Grandel, H., Kaslin, J., Ganz, J., Wenzel, I., Brand, M. (2006). Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev. Biol. 295, 263–77. http://dx.doi.org/10.1016/j.ydbio.2006.03.040
Soutschek, J.,and Zupanc, G.K.H. (1996). Apoptosis in the cerebellum of adult teleost fish, Apteronotus leptorhynchus. Dev. Brain Res. 97, 279–286. http://dx.doi.org/10.1016/j.ydbio.2006.03.040
Ampatzis, К., Dermon, С. (2007). Sex differences in adult cell proliferation within the zebrafish (Danio rerio) cerebellum. Eur. J. Neurosci. 25, 1030-1040. doi: 10.1111/j.1460-9568.2007.05366.x
Arevalo, R., Alonso, J.R., Garcia-Ojeda, E., Brinón, J.G., Crespo, C., Aijón, J. (1995). NADPH-diaphorase in the central nervous system of the tench (Tinca tinca L., 1758). J. Comp. Neurol. 352, 398-420. http://onlinelibrary.wiley.com/doi/10.1002/cne.903520307
Bruning, G., Katzbach, R., Mayer, B. (1995). Histochemical and immunocytochemical localization of nitric oxide synthase in the central nervous system of the goldfish, Carassius auratus. J Comp Neurol. 358, 353-382. http://onlinelibrary.wiley.com/doi/10.1002/cne.903580305
Villani, L., Guarnieri, T. (1995). Localization of NADPH-diaphorese in the goldfish brain. Brain Res. 679, 261-266. http://dx.doi.org/10.1016/0006-8993(95)00240-Q
Virgilli, M., Poli, A., Beraudi, A., Giuliani, A., Villani, L. (2001). Regional distribution of nitric oxide synthase and NADPH-diaphorase activities in the central nervous system of teleost. Brain Res. 901, 202-207. http://dx.doi.org/10.1016/S0006-8993(01)02357-5
Bordieri, L., Persichini, T., Venturini, G., Cioni, C. (2003). Expression of nitric oxide synthase in the preoptic-hypothalamo-hypophyseal system of the teleost Oreochromis niloticus. Brain Behav Evol. 62, 43-55. doi: 10.1159/000071959
Jadhao, A.G., Malz, C.R. (2004). Nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase activity in the brain of a cichlid fish, with remarkable findings in the entopeduncular nucleus: a histochemical study. J Chem Neuroanat. 27, 75-86. http://dx.doi.org/10.1016/j.jchemneu.2003.12.001
Perez, S.E., Adrio, F., Rodriguez, M.A., Rodriguez-Moldes, I., Anadon, R. (1996). NADPH-diaphorase histochemistry reveals oligodendrocytes in the rainbow trout (teleosts). Neurosci. Lett. 205, 83-86. http://dx.doi.org/10.1016/0304-3940(96)12379-X
Ma, P.M. (1993). Tanycytes in the sunfish brain: NADPH-diaphorase histochemistry and regional distribution. J. Comp. Neurol. 336, 77-95. http://onlinelibrary.wiley.com/doi/10.1002/cne.903360107
Holmqvist, B., Ellingsen, B., Forsell, J., Zhdanova, I., Alm, P. (2003). The early ontogeny of neuronal nitric oxide synthase systems in the zebrafish. J. Exp. Biol. 207, 923-935. doi: 10.1242/jeb.00845
Oqura, T., Nakayama, N., Fujisawa, H., Esumi, H. (1996). Neuronal nitric oxide synthase expression in neuronal cell differentiation. Neurosci. Lett. 204, 89-92. http://dx.doi.org/10.1016/0304-3940(96)12324-7
Cuodhi, B. (2001). Glial cells: basic components of clusters of supramedullary neurons in pufferfish. J. Neurocytol. 30, 503-513. doi: 10.1023/A:1015641201599
Villani, L. (1999). Development of NADPH-diaphorase in the central nervous system of the cichlid fish Tilapia mariae. Brain Behav. Evol. 54, 147-158. doi: 10.1159/000006619
Holmqvist, B., Ekstrom, P. (1997). Subcellular localization of neuronal nitric oxide synthase in the brain of a teleost; an immunoelectron and confocal microscopical study. Brain Res. 745, 67-82. http://dx.doi.org/10.1016/S0006-8993(96)01128-6
Merkulov, G. A. (1969) Course of Pathological/Histological Technique [in Russian], Meditsina, Leningrad. 423 p.
Fritsche, R., Schwerte, T., Peltser, B. (2000). Nitric oxide and vascular reactivity in developing zebrafish, Danio rerio. Am. J. Phisiol. Reg. Int. Comp. Physiol. 279, 2200-2207. http://ajpregu.physiology.org/content/279/6/R2200
Devades, M., Liu, Z., Kaneda, M., Arai, K., Matsukawa, T., Kato, S. (2001). Changes in NADPH diphorase expression in the fish visual system during optic nerve regeneration and retinal development. Neurosci. Res. 40, 359-365. http://dx.doi.org/10.1016/S0168-0102(01)00251-6
Holmqvist, B., Ellingsen, B., Alm, P., Forsell, J., Oyan, A., Goksoyr, A., Fjose, A., Seo, H. (2000). Identification and distribution of nitric oxide synthase in the brain of adult zebrafish. Neurosci Lett. 292, 119-122. http://dx.doi.org/10.1016/S0304-3940(00)01460-9
Wulliman, M.F., Knipp, S. (2000). Proliferation patterns changes in the zebrafish brain from embryonic through early postembryonic stages. Anat. Embriol. 202, 385-400. http://www.springerlink.com/content/yahxhg9tvvq64clm doi: 10.1007/s004290000115
Mize, R.R., Dawson, T.M., Dawson, V.L., Friedlander, M.J. (1998). Nitric oxide in brain development, plasticity and disease. Progress in Brain Research. Amsterdam: Elsevier Science, 118, 1-302.
Puenova, N., Scheinker, V., Cline, H., Enikolopov, G. (2001). Nitric oxide is an essential negative regulator of cell proliferation in Xenopus brain. J. Neurosci. 21, 8809-8818. http://www.jneurosci.org/content/21/22/8809.
Sturrock, R.R. (1981) An electron microscopic study of the development of the ependyma of the central canal of the mouse spinal cord. J. Anat. 132, 119-136. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1233400
Abbate, F., Laura, R., Muglia, U., Bronzetti, P. (1993) Differentiation of ependymal surface of lateral ventricles in fetus and newborn rabbits: observations by SEM. Anat. Histol. Embriol. 22, 348-254. http://www.ncbi.nlm.nih.gov/pubmed/8129170
Bicker, G. (2005). Stop and go with NO: nitric oxide as regulator of cell motility in simple brains. BioEssays. 27, 495-505. http://onlinelibrary.wiley.com/doi/10.1002/bies.20221
Romero-Grimaldi, C., Moreno-Lуpez, B., Estrada, C. (2008) Age-dependent effect of nitric oxide on subventricular zone and olfactory bulb neural precursor proliferation. J. Comp. Neurol., 506, 339–346. http://onlinelibrary.wiley.com/doi/10.1002/cne.21556
Islam, A.T., Kuraoka, A., Kawabuchi, M. (2003) Morphological basis of nitric oxide production and its correlation with the polysialylated precursor cells in the dentate gyrus of the adult guinea pig hippocampus. Anat. Sci. Int., 78, 98-103. http://www.springerlink.com/content/q484550176361710
Moreno-Lopez, B., Noval J.A., Gonzalez-Bonet L.G., Estrada C. (2000). Morphological bases for a role of nitric oxide in adult neurogenesis. Brain Res. 869, 244-250. http://dx.doi.org/10.1016/S0006-8993(00)02474-4
Kalinichenko, S. G., and Matveeva N. Yu. (2008). Morphological Characteristics of Apoptosis and Its Significance in Neurogenesis. Neurosci. Behav. Physiol. 38(4), 333-344. doi: 10.1007/s11055-008-0046-7
Reutov, V. P. (2000). Medical-biological aspects of the nitric oxide and superoxide anion radical cycles. Vest. Ross. Akad. Med. Nauk, 4, 35–41. http://www.ncbi.nlm.nih.gov/pubmed/10832412
Beckman, J.S. (1996). The physiology and pathophysiological chemistry of nitric oxide. Nitric oxide: principles and actions. San Diego: Acafemic Pressw, 1-82.
Estvez, A.G., Spear, N., Manuel, S.M. (1998). Nitric oxide and superoxide contribute to motor neuron apoptosis induced by trophic factor deprivation. J. Neurosci. 18, 923-931. http://www.jneurosci.org/content/18/3/923
Brune, B., Sandau, K., Von Kneten A. (1998) Apoptotic cell death and nitric oxide: mechanisms of activation and antagonistic signal pathways (review). Biokhimiya, 63(7), 966–975. http://www.ncbi.nlm.nih.gov/pubmed/9721334
Zupank, G.K.H. (2009). Towards brain repair: Insights from teleost fish. Seminars in Cell & Devel. Biol. 20, 683-690. http://dx.doi.org/10.1016/j.semcdb.2008.12.001
Pushchina, E.V., Fleishman, M. Yu., Timoshin, S.S. (2007) Proliferative zones in the brain of the Amur sturgeon fry. Interaction with neuromeres and migration of secondary matrix zones. Rus. J. Dev. Biol. 38, 286-293. http://www.ncbi.nlm.nih.gov/pubmed/18038653
Zupank, G.K.H. (1999). Neurogenesis, cell death and regeneration in the adult gymnotiform brain. J. Exp. Biol. 202, 1435-1446. http://jeb.biologists.org/content/202/10/1435.long
Pushchina, E.V. (2007). Nitric oxide-ergic organization of medullar cranial nuclei in teleost fishes. Tsitologiia. 49(6), 471-83. http://www.ncbi.nlm.nih.gov/pubmed/17802744
Pushchina, E.V., Varaksin, A.A. (2001). Argyrophilic and nitric oxidergic bipolar neurons in cerebellum of the opisthocentrus Pholidapus dybowskii. J. Evol. Biochem. and Physiol. 37(5), 569-575. http://www.ncbi.nlm.nih.gov/pubmed/11771249
Ikenaga, T., Yoshida, M., Uematsu, K. (2006). Cerebellar efferent neurons in teleost fish. Cerebellum. 5, 268–274. http://www.springerlink.com/content/h82731v07j781700
Brandst?tter, R., Kotrschal, K. (1990). Brain growth patterns in four European cyprinid fish species (Cyprinidae, Teleostei): roach (Rutilus rutilus), bream (Abramis brama), common carp (Cyprinus carpio) and sabre carp (Pelecus cultratus). Brain Behav. Evol. 35, 195–211. http://www.ncbi.nlm.nih.gov/pubmed/2379081
Marcus, R.C., Delaney, C.L., Easter, S.S. (1999). Neurogenesis in the visual system of embryonic and adult zebrafish (Danio rerio). Vis. Neurosci. 16, 417–424. http://www.ncbi.nlm.nih.gov/pubmed/10349963
Kubota, R., Hokoc, J. N., Moshiri, A., McGuire, C., Reh, T.A. (2002). A comparative study of neurogenesis in the retinal ciliary marginal zone of homeothermic vertebrates. Brain Res. Dev. Brain Res. 134, 31–41. http://dx.doi.org/10.1016/S0165-3806(01)00287-5
Rakic, P. (2004). Neuroscience: immigration denied. Nature. 427, 685–686. http://www.nature.com/nature/journal/v427/n6976/full/427685a.html
Song, H., Kempermann. G., Overstreet Wadiche, L., Zhao, C., Schinder, A.F., Bischofberger, J. (2005). New neurons in the adult mammalian brain: synaptogenesis and functional integration. J. Neurosci. 25, 10366–10368. http://www.jneurosci.org/content/25/45/10366.
Lledo, P. M., Alonso, M., Grubb, M. S. (2006). Adult neurogenesis and functional plasticity in neuronal circuits. Nat. Rev. Neurosci. 7, 179–193. http://www.nature.com/nrn/journal/v7/n3/full/nrn1867.html.