Department of Neurology and , 2 Department of Anatomy, Albert Szent-Györgyi Medical and Pharmaceutical Center, University of Szeged, Hungary and , 1 Department of Biochemistry, Wakayama Medical College, Wakayama, Japan
Address correspondence to Anita E. Csillik, Department of Neurology, Semmelweis utca 6, Szeged, Hungary. Email: knyihar{at}nepsy.szote.u-szeged.hu.
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Abstract |
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Introduction |
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As the only known endogenous N-methyl-D-aspartate (NMDA) receptor antagonist, kynurenic acid displays a neuroprotective effect in neurodegenerative diseases (Du et al., 1992; Nozaki and Beal, 1992
; Knyihár-Csillik et al., 1999
). Kynurenic acid is known to be produced by the activity of the enzyme kynurenin aminotransferase (KAT). According to the studies of Guidetti et al. (Guidetti et al., 1997
), there are two subtypes of this enzyme KAT-I and KAT-II with distinctive properties. KAT-I, identical with glutamine transaminase K, has an optimal pH of 9.5, prefers pyruvate as a cosubstrate and is inhibited by glutamine. KAT-II, identical with L-
-aminoadipate transaminase, has an optimal pH of 7.0, shows no preference for pyruvate and is essentially insensitive to inhibition by glutamine. While the presence of KAT-II mRNA in the brain has been identified with Northern blot analysis (Okuno et al., 1991
), to date, antibodies for immunohistochemical localization are only available against KAT-I (Knyihár-Csillik et al., 1999
). Therefore, in the present study we examined KAT-I immunoreactivity in the cells of the subplate and its remnants in rat embryos, newborn rats and rat pups, at the light and electron microscopic level. Since migration of nerve cells has been proposed to be regulated by NMDA receptors (Komuro and Rakic, 1993
), we also studied the expression of the NMDA receptor subtype R2A, and its relation to KAT-I expression in the cells of the subplate. At the same time, we compared the existence of KAT-I immunoreactivity to those of several known markers of the subplate, such as parvalbumin (PV), neuropeptide Y (NPY), nitric oxide synthase (NOS) and the
7-subunit of the nicotinic acetylcholine receptor (nAChR).
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Materials and Methods |
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Essentially the same technique was used for the visualization of PV, NOS and NPY immunoreactivity. The PV antibody raised in mouse (Sigma-Aldrich, St Louis, MO) was diluted to 1:20 000; the bNOS antibody raised in mouse (Sigma-Aldrich) was diluted to 1:3000; the NPY antibody raised in rabbit (Sigma-Aldrich) was diluted to 1:2000.
For the detection of the a7-subunit of nAChR, biotinylated -bungaro-toxin (Molecular Probes, Eugene, OR) was used at a dilution of 1:2000.
KAT-I, PV, NOS, NPY and nAChR immunoreactivity was visualized with diaminobenzidine to which hydrogen peroxide had been added (3 µl of 30% H2O2 to 10 ml of 0.05% diaminobenzidine). Sections were dehydrated in a graded series of ethanol and processed in carbolxylene. Slides were coverslipped with Permount (Fisher, Fair Lawn, NJ).
The specificity of the immunohistochemical reaction was assessed by means of one of the following treatments: (i) Omission of the first (specific) antiserum. (ii) Use of normal rabbit serum instead of the specific antiserum. (iii) Treatment according to the avidinbiotin complex method, from which one of the steps had been omitted. (iv) Preabsorbtion of the specific antibody with pure rat kidney KAT-I (Okuno et al., 1990) at 4°C for 24 h. None of these specimens showed any immunoreactivity.
Immunocytochemical Localization of the R2A Subunit of the NMDA Receptor
Fixation, preparation and sectioning of the brain was carried out exactly as previously described, except that postfixation in PLP was performed only for 1 h at 4°C. Microscopic analysis of NMDA-R2A immunolabeling showed that the best NR2A labeling with minimal background could be achieved by fixation with periodatelysineparaformaldehyde for 1 h. After sectioning either with a vibrotome or with a cryostat, primary antibody incubation with anti-NR2A serum (RBI Research Biochemicals International, Natick, MA) diluted to 1:200 in Tris-buffered saline (TBS) containing 2% NGS, was carried out overnight at 4°C, followed by 1 h incubation at room temperature. The samples were washed three times for 5 min in TBS (pH 8.2) containing 1% NGS. For immunogold labeling, sections were treated with 1 nm gold-labeled goat anti-rabbit IgG (H+L) 1 ml gelatine (IGSS) quality (Amersham Life Sciences, UK) diluted to 1:20 in TBS (pH 8.2) containing 0.4% lysine, 0.1% gelatine and 1% NGS, for 90 min at room temperature. After incubation, sections were rinsed 3 x 15 min in TBS (pH 8.2) containing 1% NGS, and 3 x 5 min in distilled water. This was followed by 1020 min silver intensification. The silver enhancement solution was prepared by mixing equal parts of Enhancer and Initiator of the IntenSE M kit (Amersham Life Sciences). After the silver enhancement process, which was monitored under a microscope with bright-field illumination, specimens were rinsed 3 x 5 min in excess distilled water. Sections were dehydrated in a graded series of ethanol and processed in carbolxylene. Slides were coverslipped with Permount (Fisher).
Combined KAT-I Immunohistochemistry and ImmunogoldSilver Staining Method on the Same Section
Sections of the subplate were double labeled for KAT-I and NMDA-R2A. Sections were labeled for NMDA-R2A with the immunogoldsilver staining method as described above, then they were immunolabeled for KAT-I with the ABC method. Sections were photographed on Leitz Diaplan and Nikon Nomarski microscopes.
Double Staining of KAT-I and Parvalbumin Immunoreactivity
Cryostat sections (30 mm thick) of the subplate were incubated in the cocktail medium containing KAT-I antiserum (dilution 1:1500) and parvalbumin antiserum (dilution 1:20 000). After 48 h incubation at 4°C KAT-I was visualized with diaminobenzidine (DAB) using the ABC technique and PV was visualized with NickelDAB, using the PAP method.
Electron Microscopy
For electron microscopic immunohistochemistry, KAT-I and NMDA R2A were visualized in Vibratome sections (50 mm), which were treated in the same manner as the light microscopic specimens. After 30 min of osmic acid fixation followed by dehydration, the sections were flat-embedded on liquid release-pretreated slides in Durcupan ACM. Relevant areas were excised with a razor blade under a microscope, remounted to pre-polymerized blocks and sectioned with a diamond knife on a Reichert Ultrotome. Serial sections of silver interference colour were collected on copper slot grids and stained with lead citrate and uranyl acetate. Sections were examined and photographed using a Zeiss Opton 902 electron microscope.
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Results |
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The cells of the subplate expressed the R2A subunit of the NMDA receptor (Fig. 3a). Using the goldsilver labeling method, the grains representing the receptor were found to be present in the cytoplasm as well as on the surface of subplate cells. It could readily be demonstrated, especially if using the Nomarski optics, that neither the nucleus nor the nucleolus contained any silver grains; they were restricted partly to the cytoplasm and partly to the surface of the cells (Figs. 3b,c
). In between the cells presenting NMDA receptors on their surfaces, non-reactive cells could also be seen.
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The presence of KAT-I immunoreactivity characterized the subplate during the embryonic period of the developing rat cortex from E16 to E21 and during the postnatal (P) period P1P7. PV immunoreactivity and NOS were present in sub-plate cells from E16 to P10. However, the localization and morphological appearance of PV- and NOS-immunoreactive cells differed considerably from that of KAT-I-immunoreactive cell populations. The fusiform PV- and NOS-immunopositive cells were located above KAT-I cells and exhibited a rich arborization of neuronal processes directed against the cortical plate (Fig. 5ad). Double staining clearly delineated the KAT-I- and PV-immunoreactive sublayers of the subplate (Fig. 5g
), which proves that different cell populations express KAT-I and PV without any trace of coexistence. On the other hand, NPY immunoreactivity was characteristic of the subplate only during the postnatal period from P7 to P10 (Fig. 5e
). We found expression of the
7-subunit of nAChR in the spherical (mostly unipolar) subplate cells from E16 until postnatal day P10 (Fig. 5f
). The
7-subunit of nAChR was also present in embryonic Cajal Retzius cells.
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Discussion |
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Due to the importance of the subplate for normal development of the cerebral cortex, several attempts have been made to find specific markers and morphoregulatory molecules that characterize its function. A fibronectin-like molecule was found both in the developing cerebral cortex and in the subplate zone (Chun and Shatz, 1988), and the antigen SP1 could be successfully used to analyze the fate of the cells constituting the subplate (Wahle et al., 1994
). Also, cells of the subplate zone were shown to exhibit strong, transient immunoreactivity of the nerve growth factor-inducible gene VGF (Lombardo et al., 1995
), which reflects the presence of the antigen in axon terminals originating from thalamic neurons. Since the transmitter nitric oxide also characterizes the subplate (Derer and Derer, 1993
; Luth et al., 1995
; Yan and Ribak, 1997
; Fatemi et al., 1998
; Judas et al., 1999
; Downen et al., 1999
), attempts were made to designate NOS, an enzyme readily accessible for immuno-histochemical studies, as the specific marker substance of the subplate. Finally, transient immunoglobulin-like molecules (Dunn et al., 1995
) and the sulfoglucuronyl carbohydrate-binding protein-1 (Nair et al., 1998
) was observed in immature neurons of the subplate. Also, calcium-binding proteins like PV (Hogan and Berman, 1994
; Honig et al., 1996
) and calbindin-D (Berger et al., 1993
; Hogan and Berman, 1994
) were shown to be present in the subplate. The PV-immunoreactive interneurons follow an inside-out pattern of maturation of cortical laminae (Hogan and Berman, 1994
). According to Honig et al. (Honig et al., 1996
) molecular markers are expressed in spatial and temporal patterns that characterize humans, non-human primates, carnivores and rodents. According to Finney et al. (Finney et al., 1998
), subplate neurons provide a major glutamatergic synaptic input to the cortical plate. Remnants of the subplate neuronal population comprise the interstitial cells of adult cortical white matter (Dunn et al., 1995
).
In our present studies, we found that KAT-I is not only a novel marker for the localization of the subplate, but also a marker that seems to have important functional aspects, since kynurenic acid, the product of kynurenine aminotransferase (KAT-I) is, as far as is currently known, the only endogenous antagonist of NMDA receptors. In this capacity, KAT-I contributes to neuronal protection against the cytotoxic effect of endogenous excito-toxins (Schwarcz et al., 1984, 1992
).
According to our present studies, the morphological entity of the subplate does not represent a homogeneous cell population. This is especially striking in double-stained specimens where the PV- and the KAT-I-expressing cell populations appear in different colours (Fig. 5g). Cells expressing PV, NOS and NPY appear to migrate to the cortical plate. At the same time, cells displaying KAT-I and the nicotinic AChR seem rather to stay in loco and support the guiding of corticothalamic and thalamo-cortical pathways.
The role of KAT-I is transient, since later, during the course of development, as the subplate cells enter the process of programmed cell death (Kostovic and Rakic, 1980; Al-Ghoul and Miller, 1989
; Ferrer et al., 1990
), this enzyme disappears. This again is in complete harmony with the role of KAT-I as proposed earlier. According to recent investigations, the neurodevelopmental origin of schizophrenia once again seems to hold its ground (Bloom, 1993
), as follows from the studies of Akbarian et al. (Akbarian et al., 1993
, 1996
). Dysfunctions of the NMDA receptors seem to play a crucial role in the development of numerous neurological and psychiatric diseases, including epilepsy, Parkinsons disease, Alzheimers disease, depression, post-traumatic stress disorder, alcoholism and schizophrenia (Heresco-Levy and Javitt, 1998
), while those of calcium-binding proteins are supposed to be involved in the development of hydrocephalus (Ulfig et al., 2001
). Further investigations may shed light on the role of dysfunctioning and surviving KAT-I-containing subplate neurons in structural and functional irregularities of the cerebral cortex. In this respect, it seems to be of major importance that kynurenic acid, the product of the enzyme KAT, inhibits
7-nicotinic receptor activity (Hilmas et al., 2001
), since the a7-nicotinic receptor, a ligand-gated ion channel that admits calcium ions into cells, has various developmental roles (Freedman et al., 2000
). It has to be assumed that in the course of normal development, a7-nicotinic receptor and kynurenic acid are in a delicate equilibrium. Our observation that the a7-nicotinic receptor is present in the subplate and in CajalRetzius cells (Meyer et al., 1999
) seems to be closely related to the developmental role of
7-nicotinic receptor, the malfunction of which has recently been implicated in the developmental pathogenesis of schizophrenia (Freedman et al., 2000
). Recent studies in this laboratory, performed in collaboration with gynecologists and psychiatrists on human embryos, may prove or disprove the validity of this assumption.
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Acknowledgments |
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