- Email: [email protected]
The distribution of neuropeptide Y and brain-derived neurotrophic factor immunoreactivity in hippocampal formation of the monkey and rat
Brain Research 852 Ž2000. 475–478 www.elsevier.comrlocaterbres
Short communication
The distribution of neuropeptide Y and brain-derived neurotrophic factor immunoreactivity in hippocampal formation of the monkey and rat Shuji Iritani a
a, )
, Kazuhiro Niizato a , Hiroyuki Nawa b , Kenji Ikeda
c
Department of Psychiatry, Tokyo Metropolitan Matsuzawa Hospital, 2-1-1 Kamikitazawa, Setagayaku, Tokyo 156-0057, Japan b Department of Molecular Biology, Brain Research Institute, Niigata UniÕersity, Niigata 010-8585, Japan c Department of Neuropathology, Tokyo Institute of Psychiatry, Setagayaku, Tokyo 156-8585, Japan Accepted 14 September 1999
Abstract The distribution of neuropeptide Y ŽNPY. and Brain-Derived Neurotrophic Factor ŽBDNF. in the hippocampal formation of monkey and rat brains was studied immunohistochemically. The NPY–neuronal system is more highly developed in the monkey compared to that in the rat. The distribution of NPY-positive products was coincident with that of abundant BDNF-positive deposits. These observations suggest that the role of BDNF and the interaction of BDNF–NPY may differ between species. q 2000 Elsevier Science B.V. All rights reserved. Keywords: BDNF; Neuropeptide Y; Hippocampus; Immunohistochemistry
BDNF, one of neurotrophic factor group, significantly influences synaptic plasticity andror construction in the central nervous system ŽCNS. w3x, and BDNF may be concerned not only with construction of the neuron network, but also with the regulation of neurotransmitters such as acetylcholine or NPY w2,15x. While NPY is abundantly distributed in the CNS w1x, although the precise role of NPY is still unknown. However, it would involve many complex functions w16x. The development and differentiation of NPY neuronal systems induced by BDNF is thought to be very important for mental activity. In this study, we investigated the distribution of NPY and BDNF immunoreactivity in the hippocampal formation of the monkey and the rat. Five male Japanese monkeys Ž Macaca fuscata fuscata. and nine male Wistar rats were used. The procedure used was the same as that in the previous study w7x. Briefly, the animals were perfused with Zamboni solution w17x under deep anesthesia. The brains were immediately removed, and 30-mm thick sections were cut. The sections were incubated: Ž1. in a polyclonal anti-BDNF ŽNiigata Brain Institute, Niigata Univ.. or in a polyclonal anti-NPY ŽResearch Biochemicals Interna)
Corresponding author. Laboratory of Molecular Neuroscience, Department of Neurobiology, The Babraham Institute, cro Dr. Piers Emson, Babraham, Cambridge CB2 4AT, UK. Fax: q81-3-3329-7586; e-mail: [email protected]
tional. overnight, Ž2. in a medium containing biotinylated anti-universal Žrat, rabbit. IgG ŽVecstain. and then Ž3. in an avidin–biotin peroxidase complex. Finally, the sections were reacted with diaminobenzidine. Control studies were conducted under the same procedure as above except that prior to immunocytochemical labeling, the diluted antiBDNF or anti-NPY was preabsorbed with BDNF ŽSigma. or NPY ŽSigma., respectively. As a result, dense NPY-positive immunoreactivity was observed throughout the hippocampus of the monkey, especially in the field of CA4, SP Žstratum pyramidalis. and SR Žstratum radiatum. of the area CA2 and CA3, SLM Žstratum lacunosum–moleculare. of the CA1 area, and in the parahippocampal cortex ŽFig. 1A–D.. In the rat brain, positive cell bodies were relatively abundant in the CA1– CA4 although fewer positive fibers were observed compared to that in the monkey ŽFig. 1E–H.. For the most part, these findings do not contradict the observation in the previous study w6,10x. The NPY-containing neuronal network is more highly developed in the hippocampal formation of the monkey compared to that of the rat, especially in the CA4 field, the CA3 subfield Žmossy fiber region. and parahippocampal cortex. BDNF-positive immunoreactivity was observed throughout the hippocampus of the monkey, relatively abundant in the CA4 field and in the SR in the CA3 field Žso-called granule cell projection of the mossy fiber region.. Abundant BDNF-positive cell
0006-8993r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 0 6 - 8 9 9 3 Ž 9 9 . 0 2 1 3 9 - 3
476
S. Iritani et al.r Brain Research 852 (2000) 475–478
Fig. 1. NPY immunoreactivity in the hippocampal formation of monkey and rat. ŽA. Low power magnification of immunoreactivity of the monkey. The bracketed area ŽB. is shown in the following photograph. Bar s 0.5 mm. ŽB. Positive cell bodies and fibers in SP and SR in the CA3. Bar s 100 mm. ŽC. A dense network in the parahippocampal cortex. Bar s 100 mm. ŽD. Positive fibers in the upper layer of the parahippocampal cortex. Bar s 100 mm. ŽE. Low power magnification photograph of immunoreactivity of the rat. The bracketed area ŽF. is indicated in the following photograph. Bar s 0.7 mm. ŽF. Positive cell bodies in SP and fibers in SR in the CA3. Bar s 100 mm. ŽG. Network of fiber in the entorhinal cortex. Bar s 100 mm. ŽH. Positive fibers and cell bodies in the middle–deep layer of the entorhinal cortex. Bar s 100 mm. Abbreviations: SM Žstratum moleculare..
S. Iritani et al.r Brain Research 852 (2000) 475–478
477
Fig. 2. BDNF immunoreactivity in the hippocampal formation of monkey and rat. ŽA. Low power magnification of the monkey. The bracketed area ŽB. is shown in the following photograph. Bar s 0.5 mm. ŽB. Abundant immunoreactive dots in SR in the CA3. Bar s 100 mm. ŽC. Positive cell bodies in layer IV in the parahippocampal cortex. Control study of the same region in the right corner. Bar s 100 mm. ŽD. Low power magnification photograph of BDNF immunoreactivity in the rat. The bracketed area ŽE. is indicated in the following photograph. Bar s 0.5 mm. ŽE. Relatively intensely labeled cell bodies in SP in the CA1. Bar s 100 mm. ŽF. Weakly labeled positive cell bodies in the middle layer in the entorhinal cortex. Bar s 200 mm. Abbreviations: SO Žstratum oriens..
478
S. Iritani et al.r Brain Research 852 (2000) 475–478
bodies were observed throughout the layer in the parahippocampal cortex ŽFig. 2A–C.. In the rat brain, BDNFweakly labeled cell bodies and dots were seen in the field of CA4, and relatively intense labeling of cell bodies was seen in the SP of the CA1–CA3 area. Weakly positive cell bodies were noted in the middle layer of the entorhinal cortex ŽFig. 2D–F.. The distribution of BDNF-immunoreactive products was nearly in accordance with that of NPY immunoreactivity in both animal species. This observation may coincide with the fact that BDNF up-regulates NPY-expression in the CNS w4x, and may also increase NPY derive through activation of GABAergic neurons w14x. In the recent study, it was reported that the presence of BDNF affected the neuropeptide protein levels in postnatal hippocampal interneurons w12x. Moreover, it was observed that the biosynthesis of NPY by granule cells and transport to the CA3rmossy fiber subfield was demonstrated by the radiolabel-infusion technique in vivo w13x. Electrophysiologically, NPY has been shown to inhibit presynaptic transmission in the CA3 subfield w9x. Although most of these previous studies used rodent materials, the interaction of BDNF and NPY may be significantly involved in neurotransmission andror electrophysiological function in these regions even in primates, as shown in this study. In the pyramidal cell layer of CA1–CA3 in the rat hippocampus, many pyramidal cell bodies in these regions contained BDNF. This observation was not confirmed in the monkey. In the CA1 area of the rat brain, BDNF induced LTP Žlong-term potentiation. without repeated stimulation w8x. In the brains of BDNF gene knock-out mice, LTP was hardly induced in this area w11x. BDNF might be important for LTP induction in the rodent hippocampus. BDNF would act differently at each developmental stage w5x, and would affect neurons differently according to their localization w2x. Similarly, this study presumes that the functions of BDNF might differ between species.
References w1x T.E. Adrian, J.M. Allen, S.R. Bloom, M.A. Ghatei, M.N. Rossor, G.W. Roberts, T.J. Crow, K. Tatemoto, J.M. Polak, Neuropeptide Y distribution in human brain, Nature 306 Ž1983. 584–586.
w2x R.F. Alderson, A.L. Alterman, Y.A. Barde, R.M. Lindsay, Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture, Neuron 5 Ž1990. 297–306. w3x R.J. Cabelli, A. Hohn, C.J. Shatz, Inhibition of ocular dominance column formation by infusion of NT-4r5 or BDNF, Science 267 Ž1995. 1662–1666. w4x J. Carnahan, H. Nawa, Regulation of neuropeptide expression in the brain by neurotrophins. Potential role in vivo, Mol. Neurobiol. 10 Ž1995. 135–149. w5x S.D. Croll, S.J. Wiegand, K.D. Anderson, R.M. Lindsay, H. Nawa, Regulation of neuropeptides in adult rat forebrain by the neurotrophins BDNF and NGF, Eur. J. Neurosci. 6 Ž1994. 1343–1353. w6x M.E. de Quidt, P.C. Emson, Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system: II. Immunohistochemical analysis, Neuroscience 18 Ž1986. 545–618. w7x S. Iritani, M. Fujii, K. Satoh, The distribution of substance P in the cerebral cortex and hippocampal formation: an immunohistochemical study in the monkey and rat, Brain Res. Bull. 22 Ž1989. 295–303. w8x H.J. Kang, E.M. Schuman, Neurotrophin-induced modulation of synaptic transmission in the adult hippocampus, J. Physiol. ŽParis. 89 Ž1995. 11–22. w9x G.J. Klapstein, W.F. Colmers, On the sites of presynaptic inhibition by neuropeptide Y in rat hippocampus in vitro, Hippocampus 3 Ž1993. 103–111. w10x C. Kohler, L. Eriksson, S. Davies, V. Chan-Palay, Neuropeptide Y innervation of the hippocampal region in the rat and monkey brain, J. Comp. Neurol. 244 Ž1986. 384–400. w11x M. Korte, P. Carroll, E. Wolf, G. Brem, H. Thoenen, T. Bonhoeffer, Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor, Proc. Natl. Acad. Sci. U. S. A. 92 Ž1995. 8856–8860. w12x S. Marty, B. Onteniente, BDNF and NT-4 differentiate two pathways in the modulation of neuropeptide protein levels in postnatal hippocampal interneurons, Eur. J. Neurosci. 11 Ž1999. 1647–1656. w13x J.B. McCarthy, M. Walker, J. Pierce, P. Camp, J.D. White, Biosynthesis and metabolism of native and oxidized neuropeptide Y in the hippocampal mossy fiber system, J. Neurochem. 70 Ž1998. 1950– 1963. w14x H. Nawa, Y. Bessho, J. Carnahan, S. Nakanishi, K. Mizuno, Regulation of neuropeptide expression in cultured cerebral cortical neurons by brain-derived neurotrophic factor, J. Neurochem. 60 Ž1993. 772– 775. w15x H. Nawa, M.A. Pelleymounter, J. Carnahan, Intraventricular administration of BDNF increases neuropeptide expression in newborn rat brain, J. Neurosci. 14 Ž1994. 3751–3765. w16x J. Scuvee-Moreau, Peptides in the brain, Acta Psychiatr. Belg. 83 Ž1983. 375–382. w17x L. Zamboni, C. De Martino, Buffered picric-acid formaldehyde: a new rapid fixative for electron microscopy, J. Cell Biol. 35 Ž1967. 148.
Short communication
The distribution of neuropeptide Y and brain-derived neurotrophic factor immunoreactivity in hippocampal formation of the monkey and rat Shuji Iritani a
a, )
, Kazuhiro Niizato a , Hiroyuki Nawa b , Kenji Ikeda
c
Department of Psychiatry, Tokyo Metropolitan Matsuzawa Hospital, 2-1-1 Kamikitazawa, Setagayaku, Tokyo 156-0057, Japan b Department of Molecular Biology, Brain Research Institute, Niigata UniÕersity, Niigata 010-8585, Japan c Department of Neuropathology, Tokyo Institute of Psychiatry, Setagayaku, Tokyo 156-8585, Japan Accepted 14 September 1999
Abstract The distribution of neuropeptide Y ŽNPY. and Brain-Derived Neurotrophic Factor ŽBDNF. in the hippocampal formation of monkey and rat brains was studied immunohistochemically. The NPY–neuronal system is more highly developed in the monkey compared to that in the rat. The distribution of NPY-positive products was coincident with that of abundant BDNF-positive deposits. These observations suggest that the role of BDNF and the interaction of BDNF–NPY may differ between species. q 2000 Elsevier Science B.V. All rights reserved. Keywords: BDNF; Neuropeptide Y; Hippocampus; Immunohistochemistry
BDNF, one of neurotrophic factor group, significantly influences synaptic plasticity andror construction in the central nervous system ŽCNS. w3x, and BDNF may be concerned not only with construction of the neuron network, but also with the regulation of neurotransmitters such as acetylcholine or NPY w2,15x. While NPY is abundantly distributed in the CNS w1x, although the precise role of NPY is still unknown. However, it would involve many complex functions w16x. The development and differentiation of NPY neuronal systems induced by BDNF is thought to be very important for mental activity. In this study, we investigated the distribution of NPY and BDNF immunoreactivity in the hippocampal formation of the monkey and the rat. Five male Japanese monkeys Ž Macaca fuscata fuscata. and nine male Wistar rats were used. The procedure used was the same as that in the previous study w7x. Briefly, the animals were perfused with Zamboni solution w17x under deep anesthesia. The brains were immediately removed, and 30-mm thick sections were cut. The sections were incubated: Ž1. in a polyclonal anti-BDNF ŽNiigata Brain Institute, Niigata Univ.. or in a polyclonal anti-NPY ŽResearch Biochemicals Interna)
Corresponding author. Laboratory of Molecular Neuroscience, Department of Neurobiology, The Babraham Institute, cro Dr. Piers Emson, Babraham, Cambridge CB2 4AT, UK. Fax: q81-3-3329-7586; e-mail: [email protected]
tional. overnight, Ž2. in a medium containing biotinylated anti-universal Žrat, rabbit. IgG ŽVecstain. and then Ž3. in an avidin–biotin peroxidase complex. Finally, the sections were reacted with diaminobenzidine. Control studies were conducted under the same procedure as above except that prior to immunocytochemical labeling, the diluted antiBDNF or anti-NPY was preabsorbed with BDNF ŽSigma. or NPY ŽSigma., respectively. As a result, dense NPY-positive immunoreactivity was observed throughout the hippocampus of the monkey, especially in the field of CA4, SP Žstratum pyramidalis. and SR Žstratum radiatum. of the area CA2 and CA3, SLM Žstratum lacunosum–moleculare. of the CA1 area, and in the parahippocampal cortex ŽFig. 1A–D.. In the rat brain, positive cell bodies were relatively abundant in the CA1– CA4 although fewer positive fibers were observed compared to that in the monkey ŽFig. 1E–H.. For the most part, these findings do not contradict the observation in the previous study w6,10x. The NPY-containing neuronal network is more highly developed in the hippocampal formation of the monkey compared to that of the rat, especially in the CA4 field, the CA3 subfield Žmossy fiber region. and parahippocampal cortex. BDNF-positive immunoreactivity was observed throughout the hippocampus of the monkey, relatively abundant in the CA4 field and in the SR in the CA3 field Žso-called granule cell projection of the mossy fiber region.. Abundant BDNF-positive cell
0006-8993r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 0 6 - 8 9 9 3 Ž 9 9 . 0 2 1 3 9 - 3
476
S. Iritani et al.r Brain Research 852 (2000) 475–478
Fig. 1. NPY immunoreactivity in the hippocampal formation of monkey and rat. ŽA. Low power magnification of immunoreactivity of the monkey. The bracketed area ŽB. is shown in the following photograph. Bar s 0.5 mm. ŽB. Positive cell bodies and fibers in SP and SR in the CA3. Bar s 100 mm. ŽC. A dense network in the parahippocampal cortex. Bar s 100 mm. ŽD. Positive fibers in the upper layer of the parahippocampal cortex. Bar s 100 mm. ŽE. Low power magnification photograph of immunoreactivity of the rat. The bracketed area ŽF. is indicated in the following photograph. Bar s 0.7 mm. ŽF. Positive cell bodies in SP and fibers in SR in the CA3. Bar s 100 mm. ŽG. Network of fiber in the entorhinal cortex. Bar s 100 mm. ŽH. Positive fibers and cell bodies in the middle–deep layer of the entorhinal cortex. Bar s 100 mm. Abbreviations: SM Žstratum moleculare..
S. Iritani et al.r Brain Research 852 (2000) 475–478
477
Fig. 2. BDNF immunoreactivity in the hippocampal formation of monkey and rat. ŽA. Low power magnification of the monkey. The bracketed area ŽB. is shown in the following photograph. Bar s 0.5 mm. ŽB. Abundant immunoreactive dots in SR in the CA3. Bar s 100 mm. ŽC. Positive cell bodies in layer IV in the parahippocampal cortex. Control study of the same region in the right corner. Bar s 100 mm. ŽD. Low power magnification photograph of BDNF immunoreactivity in the rat. The bracketed area ŽE. is indicated in the following photograph. Bar s 0.5 mm. ŽE. Relatively intensely labeled cell bodies in SP in the CA1. Bar s 100 mm. ŽF. Weakly labeled positive cell bodies in the middle layer in the entorhinal cortex. Bar s 200 mm. Abbreviations: SO Žstratum oriens..
478
S. Iritani et al.r Brain Research 852 (2000) 475–478
bodies were observed throughout the layer in the parahippocampal cortex ŽFig. 2A–C.. In the rat brain, BDNFweakly labeled cell bodies and dots were seen in the field of CA4, and relatively intense labeling of cell bodies was seen in the SP of the CA1–CA3 area. Weakly positive cell bodies were noted in the middle layer of the entorhinal cortex ŽFig. 2D–F.. The distribution of BDNF-immunoreactive products was nearly in accordance with that of NPY immunoreactivity in both animal species. This observation may coincide with the fact that BDNF up-regulates NPY-expression in the CNS w4x, and may also increase NPY derive through activation of GABAergic neurons w14x. In the recent study, it was reported that the presence of BDNF affected the neuropeptide protein levels in postnatal hippocampal interneurons w12x. Moreover, it was observed that the biosynthesis of NPY by granule cells and transport to the CA3rmossy fiber subfield was demonstrated by the radiolabel-infusion technique in vivo w13x. Electrophysiologically, NPY has been shown to inhibit presynaptic transmission in the CA3 subfield w9x. Although most of these previous studies used rodent materials, the interaction of BDNF and NPY may be significantly involved in neurotransmission andror electrophysiological function in these regions even in primates, as shown in this study. In the pyramidal cell layer of CA1–CA3 in the rat hippocampus, many pyramidal cell bodies in these regions contained BDNF. This observation was not confirmed in the monkey. In the CA1 area of the rat brain, BDNF induced LTP Žlong-term potentiation. without repeated stimulation w8x. In the brains of BDNF gene knock-out mice, LTP was hardly induced in this area w11x. BDNF might be important for LTP induction in the rodent hippocampus. BDNF would act differently at each developmental stage w5x, and would affect neurons differently according to their localization w2x. Similarly, this study presumes that the functions of BDNF might differ between species.
References w1x T.E. Adrian, J.M. Allen, S.R. Bloom, M.A. Ghatei, M.N. Rossor, G.W. Roberts, T.J. Crow, K. Tatemoto, J.M. Polak, Neuropeptide Y distribution in human brain, Nature 306 Ž1983. 584–586.
w2x R.F. Alderson, A.L. Alterman, Y.A. Barde, R.M. Lindsay, Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture, Neuron 5 Ž1990. 297–306. w3x R.J. Cabelli, A. Hohn, C.J. Shatz, Inhibition of ocular dominance column formation by infusion of NT-4r5 or BDNF, Science 267 Ž1995. 1662–1666. w4x J. Carnahan, H. Nawa, Regulation of neuropeptide expression in the brain by neurotrophins. Potential role in vivo, Mol. Neurobiol. 10 Ž1995. 135–149. w5x S.D. Croll, S.J. Wiegand, K.D. Anderson, R.M. Lindsay, H. Nawa, Regulation of neuropeptides in adult rat forebrain by the neurotrophins BDNF and NGF, Eur. J. Neurosci. 6 Ž1994. 1343–1353. w6x M.E. de Quidt, P.C. Emson, Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system: II. Immunohistochemical analysis, Neuroscience 18 Ž1986. 545–618. w7x S. Iritani, M. Fujii, K. Satoh, The distribution of substance P in the cerebral cortex and hippocampal formation: an immunohistochemical study in the monkey and rat, Brain Res. Bull. 22 Ž1989. 295–303. w8x H.J. Kang, E.M. Schuman, Neurotrophin-induced modulation of synaptic transmission in the adult hippocampus, J. Physiol. ŽParis. 89 Ž1995. 11–22. w9x G.J. Klapstein, W.F. Colmers, On the sites of presynaptic inhibition by neuropeptide Y in rat hippocampus in vitro, Hippocampus 3 Ž1993. 103–111. w10x C. Kohler, L. Eriksson, S. Davies, V. Chan-Palay, Neuropeptide Y innervation of the hippocampal region in the rat and monkey brain, J. Comp. Neurol. 244 Ž1986. 384–400. w11x M. Korte, P. Carroll, E. Wolf, G. Brem, H. Thoenen, T. Bonhoeffer, Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor, Proc. Natl. Acad. Sci. U. S. A. 92 Ž1995. 8856–8860. w12x S. Marty, B. Onteniente, BDNF and NT-4 differentiate two pathways in the modulation of neuropeptide protein levels in postnatal hippocampal interneurons, Eur. J. Neurosci. 11 Ž1999. 1647–1656. w13x J.B. McCarthy, M. Walker, J. Pierce, P. Camp, J.D. White, Biosynthesis and metabolism of native and oxidized neuropeptide Y in the hippocampal mossy fiber system, J. Neurochem. 70 Ž1998. 1950– 1963. w14x H. Nawa, Y. Bessho, J. Carnahan, S. Nakanishi, K. Mizuno, Regulation of neuropeptide expression in cultured cerebral cortical neurons by brain-derived neurotrophic factor, J. Neurochem. 60 Ž1993. 772– 775. w15x H. Nawa, M.A. Pelleymounter, J. Carnahan, Intraventricular administration of BDNF increases neuropeptide expression in newborn rat brain, J. Neurosci. 14 Ž1994. 3751–3765. w16x J. Scuvee-Moreau, Peptides in the brain, Acta Psychiatr. Belg. 83 Ž1983. 375–382. w17x L. Zamboni, C. De Martino, Buffered picric-acid formaldehyde: a new rapid fixative for electron microscopy, J. Cell Biol. 35 Ž1967. 148.