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Immunocytochemical Localization of Nitric Oxide Synthase-containing Neurons in Mouse and Rabbit Visual Cortex and Co-Localization with Calcium-binding Proteins  

Lee, Jee-Eun (Department of Biology, College of Natural Sciences, Kyungpook National University)
Jeon, Chang-Jin (Department of Biology, College of Natural Sciences, Kyungpook National University)
Publication Information
Molecules and Cells / v.19, no.3, 2005 , pp. 408-417 More about this Journal
Abstract
Nitric oxide (NO) occurs in various types of cells in the central nervous system. We studied the distribution and morphology of neuronal nitric oxide synthase (NOS)-containing neurons in the visual cortex of mouse and rabbit with antibody immunocytochemistry. We also compared this labeling to that of calbindin D28K, calretinin, and parvalbumin. Staining for NOS was seen both in the specific layers and in selective cell types. The densest concentration of intense anti-NOS immunoreactive (IR) neurons was found in layer VI, while the weak anti-NOS-IR neurons were found in layer II/III in both animals. The NOS-IR neurons varied in morphology. The large majority of NOS-IR neurons were round or oval cells with many dendrites coursing in all directions. Two-color immunofluorescence revealed that only 16.7% of the NOS-IR cells were double-labeled with calbindin D28K in the mouse visual cortex, while more than half (51.7%) of the NOS-IR cells were double-labeled with calretinin and 25.0% of the NOS-IR cells were double-labeled with parvalbumin in mouse. By contrast, 92.4% of the NOS-IR neurons expressed calbindin D28K while only 2.5% of the NOS-IR neurons expressed calretinin in the rabbit visual cortex. In contrast with the mouse, none of the NOS-IR cells in the rabbit visual cortex were double-labeled with parvalbumin. The results indicate that neurons in the visual cortex of both animals express NOS in specific layers and cell types, which do not correlate with the expression of calbindin D28K, calretinin or parvalbumin between the two animals.
Keywords
Calcium-binding Protein; Immunocytochemistry; Localization; Nitric Oxide Synthase; Visual Cortex;
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1 Bredit, D. S. and Snyder, S. M. (1990) Isolation of nitric synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA 87, 682-685
2 Daff, S. (2003) Calmodulin-dependent regulation of mammalian nitric oxide synthase. Biochem. Soc. Trans. 31, 502-505   DOI
3 Ferrante, R. J., Kowall, N. W., Beal, M. F., Richardson Jr, E. P., Bird, E. D., et al. (1985) Selective sparing of a class of striatal neurons in Huntington's disease. Science 230, 561-563   DOI
4 Iritani, S., Niizato, K., and Emson, P. C. (2001) Relationship of calbindin D28K-immunoreactive cells and neuropathological changes in the hippocampal formation of Alzheimer's disease. Neuropathology 21, 162-167   DOI   ScienceOn
5 Jilge, B. (1991) The rabbit: a diurnal or a nocturnal animal? J. Exp. Anim. Sci. 34, 170-183
6 Kowianski, P., Morys, J. M., Wojcik, S., Dziewiatkowski, J., and Morys, J. (2003) Co-localisation of NOS with calciumbinding proteins during the postnatal development of the rat claustrum. Folia Morphol. 62, 211-214
7 Li, H. and Poulos, T. L. (2005) Structure-function studies on nitric oxide synthase. J. Inorg. Biochem. 99, 293-305   DOI   ScienceOn
8 Van Damme, K., Massie, A., Vandesande, F., and Arckens, L. (2003) Distribution of the AMPA2 glutamate receptor subunit in adult cat visual cortex. Brain Res. 960, 1-8   DOI   ScienceOn
9 Wu, Y. and Parent, A. (2000) Striatal interneurons expressing calretinin, parvalbumin or NADPH-diaphorase: a comparative study in the rat, monkey and human. Brain Res. 863, 182-191   DOI   ScienceOn
10 Cha, C. I., Uhm, M. R., Shin, D. H., Chung, Y. H., and Baik, S. H. (1998) Immunocytochemical study on the distribution of NOS-immunoreactive neurons in the cerebral cortex of aged rats. NeuroReport 9, 2171-2174   DOI   ScienceOn
11 Kang, Y.-S., Park, W.-M., Lim, J.-K., Kim, S,-Y., and Jeon, C.-J. (2002) Changes of calretinin, calbindin D28K and parvalbumin immunoreactive neurons in the superficial layers of the hamster superior colliculus following monocular enucleation. Neurosci. Lett. 330, 104-108   DOI   ScienceOn
12 Yan, X. X. and Garey, L. J. (1997) Morphological diversity of nitric oxide synthesizing neurons in mammalian cerebral cortex. J. Hirnforsch. 38, 165-172
13 Heizmann, C. W., Rohrenbeck, J., and Kamphuis, W. (1990) Parvalbumin, molecular and functional aspects. Adv. Exp. Med. Biol. 269, 57-66
14 Norris, P. J., Faull, R. L., and Emson, P. C. (1996) Neuronal nitric oxide synthase (nNOS) mRNA expression and NADPHdiaphorase staining in the frontal cortex, visual cortex and hippocampus of control and Alzheimer's disease brains. Brain Res. Mol. 41, 36-49   DOI   ScienceOn
15 Xiao, Y.-M., Diao, Y.-C., and So, K.-F. (1996) A morphological study of neurons expressing NADPH diaphorase activity in the visual cortex of the Golden hamster. Brain Behav. Evol. 48, 221-230   DOI
16 Park, H.-J., Kong, J.-H., Kang, Y.-S., Park, W.-M., Jeong, S.-A., et al. (2002) The distribution and morphlology of calbindin D28k-, calretinin-immunoreactive neurons in the visual cortex of mouse. Mol. Cells 14, 143-149
17 Rogers, J., Khan, M., and Ellis, J. (1990) Calretinin: a gene for a novel calcium-binding protein expressed principally in neuron. J. Cell Biol. 105, 1343-1353
18 Soares-Mota, M., Henze, I., and Mendez-Otero, R. (2001) Nitric oxide synthase-positive neurons in the rat superior colliculus: colocalization of NOS with NMDAR1 glutamate receptor, GABA, and parvalbumin. J. Neurosic. Res. 64, 501-507   DOI   ScienceOn
19 Megías, M., Verduga, R., Fernández-Viadero, C., and Crespo, D. (1997) Neurons co-localizing calretinin immunoreactivity and reduced nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) activity in the hippocampus and dentate gyrus of the rat. Brain Res. 744, 112-120   DOI   ScienceOn
20 Goldstein, I, M., Ostwald, P., and Roth, S. (1996) Nitric oxide: a review of its role in retinal function and disease. Vision Res. 36, 2979-2994   DOI   ScienceOn
21 Yousef, T., Neubacher, U., Eysel, U. T., and Volgushev, M. (2004) Nitric oxide synthase in rat visual cortex: an immunohistochemical study. Brain Res. Protoc. 13, 57-67   DOI   ScienceOn
22 Lüth, H.-J., Hedlich, A., Hilbig, H., Winkelmann, E., and Mayer, B. (1994) Morphological analyses of NADPH-diaphorase/ nitric oxide synthase positive structures in human visual cortex. J. Neurocytol. 23, 770-782   DOI
23 Bertini, G., Peng, Z.-C., and Bentivoglio, M. (1996) The chemical heterogeneity of cortical interneurons: nitric oxide synthase vs. calbindin and parvalbumin immunoreactivity in the rat. Brain Res. Bull. 39, 261-266   DOI   ScienceOn
24 He, Y., Hof, P. R., Janssen, W. G., Vissavajjhala, P., and Morrison, J. H. (2001) AMPA GluR2 subunit is differentially distributed on GABAergic neurons and pyramidal cells in the macaque monkey visual cortex. Brain Res. 921, 60-67   DOI   ScienceOn
25 Heizmann, C. W. and Braun, K. (1995) Calcium Regulation by Calcium-binding proteins in Neurodegenerative Disorders, Springer-Verlag, New York
26 Gutierrez-Igarza, K., Fogarty, D. J., Perez-Cerda, F., Donate- Oliver, F., Albus, K., et al. (1996) Localization of AMPAselective glutamate receptor subunits in the adult cat visual cortex. Vis. Neurosci. 13, 61-72   DOI
27 Simonian, N. A. and Coyle, J. T. (1996) Oxidative stress in neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol. 36, 83-106   DOI   ScienceOn
28 Park, H.-J., Lee, S.-N., Lim, H.-R., Kong, J.-H., and Jeon, C.-J. (2000) Calcium-binding protein calbindin D28K, calretinin, and parvalbumin immunoreactivity in the rabbit visual cortex. Mol. Cells 10, 206-212   DOI
29 Hong, S.-K., Kim, J.-Y., and Jeon, C.-J. (2002) Immunocytochemical localization of calretinin in the superficial layers of the cat superior colliculus. Neurosci. Res. 44, 325-335   DOI   ScienceOn
30 Jeon, C.-J., Pyun, J.-K., and Yang, H.-W. (1998) Calretinin and calbindin D28K immunoreactivity in the superficial layers of the rabbit superior colliculus. Neuroreport 9, 3847-3852   DOI   ScienceOn
31 Aoki, C. S., Fenstemaker, S., Lubin, M., and Go, C.-G. (1993) Nitric oxide synthase in the visual cortex of monocular monkeys as revealed by light and electron microscopic immunocytochemistry. Brain Res. 620, 97-113   DOI   ScienceOn
32 Xu, L., Tanigawa, H., and Fujita, I. (2003) Distribution of alphaamino- 3-hydroxy-5-methyl-4-isoxazolepropionate-type glutamate receptor subunits (GluR2/3) along the ventral visual pathway in the monkey. J. Comp. Neurol. 456, 396-407   DOI   ScienceOn
33 Demeulemeester, H., Arckens, L., Vandesande, F., Orban, G. A., Heizmann, C. W., et al. (1991) Calcium-binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex. Exp. Brain Res. 84, 538-544
34 Lee, J.-E., Ahn, C.-H., Lee, J.-Y., Chung, E.-S., and Jeon, C.-J. (2004) Nitric oxide synthase and calcium-binding proteincontaining neurons in the hamster visual cortex. Mol. Cells 18, 30-39
35 Schäfer, B. W. and Heizmann, C. W. (1996) The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem. Sci. 21, 134-140
36 Snyder, S. H., Jaffrey, S. R., and Zakhary, R. (1998) Nitric oxide and carbon monoxide: parallel roles as neural messengers. Brain Res. Rev. 28, 167
37 Jinno, S., Kinukawa, N., and Kosaka, T. (2001) Morphometric multivariate analysis of GABAergic neurons containing calretinin and neuronal nitric oxide synthase in the mouse hippocampus. Brain Res. 900, 195-204   DOI   ScienceOn
38 Johannes, S., Reif, A., Senitz, D., Riederer, P., and Lauer, M. (2003) NADPH-diaphorase staining reveals new types of interneurons in human putamen. Brain Res. 980, 92-99   DOI   ScienceOn
39 Kiss, J. P. (2000) Role of nitric oxide in the regulation of monoaminergic neurotransmission. Brain Res. Bull. 52, 459-466   DOI   ScienceOn
40 Zhang, J. and Snyder, S. H. (1995) Nitric oxide in the nervous system. Annu. Rev. Pharmacol. Toxicol. 35, 213-233   DOI   ScienceOn
41 Gonchar, Y. and Burkhalter, A. (1997) Three distint families of GABAergic neurons in rat visual cortex. Cereb. Cortex 7, 347-358   DOI   ScienceOn
42 Sandell, J. H. (1986) NADPH-diaphorase histochemistry in the macaque striate cortex. J. Comp. Neurol. 251, 388-397   DOI   ScienceOn
43 Wiencken, A. E. and Casagrande, V. A. (2000) The distribution of NADPH diaphorase and nitric oxide synthetase (NOS) in relation to the functional compartments of areas V1 and V2 of primate visual cortex. Cereb. Cortex 10, 499-511   DOI   ScienceOn
44 Baimbridge, K. G., Celio, M. R., and Rogers, J. H. (1992) Calcium- binding proteins in the nervous system. Trends Neurosci. 15, 303-307   DOI   ScienceOn
45 Park, H.-J., Hong, S.-K., Kong, J.-H., and Jeon, C.-J. (1999) Localization of calcium-binding protein parvalbumin-immunoreactive neurons in mouse and hamster visual cortex. Mol. Cells 9, 542-547
46 Dawson, V. L. and Dawson, T. M. (1996) Nitric oxide actions in neurochemistry. Neurochem. Int. 29, 97-110   DOI   ScienceOn