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Department of Anatomy and Neurobiology, University of Kentucky College of Medicine, Lexington, Kentucky 40536
Address all correspondence and requests for reprints to: Lothar Jennes, Ph.D., Department of Anatomy and Neurobiology, University of Kentucky College of Medicine, 430 Health Science Research Building, Lexington, Kentucky 40536. E-mail: ljenn0{at}pop.uky.edu.
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Tissue preparation for in situ hybridization
Deeply anesthetized female rats were decapitated, and the brains were rapidly removed and frozen on dry ice. Twelve-micron-thick coronal sections were prepared through the medial septum-diagonal band complex to the mammary bodies, mounted onto positively charged SuperFrost Plus slides (CMS, Houston, TX), and stored at -80 C until use. Immediately before in situ hybridization, the slides were equilibrated to room temperature, fixed for 5 min in 4% paraformaldehyde, followed by a 2-min rinse in 0.1 M sodium phosphate buffer (pH 7.4). The slides were acetylated for 10 min in 0.1 M triethanolamine (pH 8.0) and 0.25% acetic anhydride, then dehydrated and air-dried.
Riboprobe preparation
The partial cDNA sequence of rat VGluT2 was obtained by RT-PCR from rat brain total RNA using two oligonucleotide primers (forward primer, 5'-cgaaagatcatgaactgcggg-3'; reverse primer, 5'-gcccaaggttgcttctctcc-3') and cloned into pCRII-TOPO vector (Invitrogen, Carlsbad, CA). The cDNA sequence corresponds to nucleotides 1615–1979 of GenBank entry AF271235 (submitted by Drs. H. Mashima and T. Kojima).
cRNA riboprobe was synthesized by in vitro transcription in the presence of HindIII-linearized VGluT2 plasmid, 35S-labeled UTP, and T7 RNA polymerase.
In situ hybridization
The above brain sections were hybridized overnight at 55 C with the 35S-labeled cRNA riboprobe (1 x 106 cpm/section) diluted in hybridization cocktail containing 20 mM Tris-HCl (pH 7.4), 1 mM EDTA, 300 mM NaCl, 50% (vol/vol) deionized formamide, 10% (vol/vol) dextran sulfate, 1x Denhardt’s solution, and 100 mM dithiothreitol. After 16 h, sections were rinsed twice for 10 min each time in 2x SSC (1x SSC = 0.25 M NaCl and 0.015 M sodium citrate, pH 7.2) containing 10 mM dithiothreitol at 22 C, treated with ribonuclease A (20 µg/ml) for 30 min at 37 C, washed with 1x SSC for 15 min at room temperature, and washed twice with 0.1x SSC at 63 C for 30 min each time. Finally, the sections were rinsed in 0.1x SSC at room temperature, quickly dehydrated, and air-dried. Slides were exposed to BIO-MAX MR x-ray film (Kodak, Rochester, NY) for 1–2 wk.
Tissue preparation for immunohistochemistry
For immunohistochemical experiments, 10 animals were perfusion-fixed under anesthesia with PBS (0.1 M, pH 7.4), followed by 4% paraformaldehyde and 7.5% saturated picric acid in PBS, and the brains were removed and postfixed in the above fixative overnight at 4 C. Serial 40-µm coronal Vibratome (St. Louis, MO) sections were collected from the hypothalamus, infiltrated with cryoprotectant (18), and stored at -20 C. Five animals received an intracerebroventricular injection of colchicine (100 µg/10 µl/animal) 2 d before perfusion fixation.
Immunocytochemistry
Vibratome sections were equilibrated to room temperature, washed in Tris-HCl buffer (0.05 M; pH 7.6), and treated with the blocking buffer (10% normal horse serum, 0.2% Triton X-100, and 0.1% sodium azide in Tris-HCl) for 1 h at room temperature. Sections were then incubated overnight at room temperature in affinity-purified rabbit or guinea pig anti-VGLUT2 antibody (1:1000). After several washes with Tris-HCl buffer, sections were incubated 1 h in affinity-purified, biotinylated donkey antirabbit IgG, or antiguinea pig antibody (1:400; Jackson ImmunoResearch Laboratories, West Grove, PA), washed again in Tris-HCl buffer, and exposed for 1 h to avidin-biotin peroxidase complex (Elite, Vector Laboratories, Inc., Burlingame, CA). After two 10-min washes in Tris-HCl buffer, sections were stained for 10 min in Tris-HCl buffer containing 50 mg diaminobenzidine and 5 µl H2O2 (30%). For dual labeling studies, sections were exposed overnight to rabbit anti-VGLUT2 and monoclonal antisynaptophysin antibody (Sigma-Aldrich, St. Louis, MO; 1:1,000). After two 10-min washes, sections were incubated in affinity-purified, cross-absorbed second antibodies that were labeled with Texas Red or fluorescein isothiocyanate (1:100; Jackson ImmunoResearch Laboratories). For triple labeling studies, sections were exposed overnight to rabbit anti-VGLUT2, monoclonal antisynaptophysin, and guinea pig anti-GnRH (GP6–4; 1:1,000); washed twice for 10 min each time; and incubated in affinity-purified, cross-absorbed second antibodies that were labeled with Texas Red, fluorescein isothiocyanate, or Cy5 (1:100; Jackson ImmunoResearch Laboratories). Fluorescent-labeled sections were examined with a confocal microscope (Leica Corp., Rockleigh, NJ) using sequential scanning settings.
Specificity controls included absorption with antigen (VGLUT2 and GnRH peptides), omission of the primary antibodies, and extensive tests of cross-reactivities of the second antibodies. All control experiments resulted in the absence of staining.
VGLUT2 antibodies
Antibodies were raised is rabbits and guinea pig against a synthetic decapeptide unique to the C terminus of VGLUT2. The peptide was coupled to hemocyanin via glutaraldehyde, and 100 µg of this antigen were injected per immunization cycle. Resulting antibodies were affinity-purified and tested for their specificity by Western blot analysis using cortical and thalamic/hypothalamic tissue, immunohistochemistry, and absorption with the synthetic antigen peptide. An example of a Western blot is shown in Fig. 1
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). In the medial septum, most heavily labeled cells were located in the lateral aspects of this nucleus, and this band of cells extended through the vertical limb of the diagonal band into the horizontal limb. This distribution pattern continued caudally to the organum vasculosum of the lamina terminalis (OVLT), which is very heavily labeled with the VGLUT2 cRNA probe (Fig. 2, B and C).
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). The central part and the ventral aspects of the medial preoptic nucleus, medial part, were strongly labeled, whereas further caudally the remaining portion of the medial preoptic nucleus and the lateral preoptic area were sparsely labeled (Fig. 2, E and F). At this level, VGLUT2 mRNA-containing cells continued to be present in the horizontal diagonal band and ventral portion of the lateral septum.
At the anterior level, the supraoptic and paraventricular nuclei were moderately labeled. In the paraventricular nucleus, both magnocellular and parvocellular portions showed hybridization signal that was strongest in the medial and dorsal parvocellular part (Fig. 2G). The periventricular nucleus was only lightly labeled. The lateroanterior hypothalamic nucleus contained many intensely labeled cells, and slightly fewer cells were seen in the anterior hypothalamic area, ventrolateral hypothalamic nucleus, and lateral hypothalamic area (Fig. 2H).
At the tuberal level, the posterior periventricular nucleus was unlabeled, whereas the arcuate nucleus contained moderate levels of hybridization signal throughout its rostrocaudal extent. The ventromedial nucleus was heavily labeled, whereas the dorsomedial nucleus exhibited slightly lighter signal (Fig. 2I). The lateral and dorsal hypothalamic areas contained patches of moderately labeled cells.
The mammillary complex contained large amounts of VGLUT2 mRNA. Thus, both the dorsal and ventral premammillary nuclei, the median portion of the medial mammillary nucleus, as well as the supramammillary nucleus were very heavily labeled in contrast to the medial and lateral portions, which contained only moderate amounts of signal (Fig. 2J). The lateral hypothalamus contained patches of moderately labeled cells. The results are summarized in Table 1.
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Beginning rostrally, a few immunoreactive cells were seen in the ventral part of the lateral septum, medial septum, and diagonal band (Fig. 3A). In contrast, numerous positive cells surrounded the organum vasculosum of the lamina terminalis in a distribution pattern reminiscent of a triangle with the base formed by the ventral surface of the brain and the apex reaching into the vertical limb of the diagonal band (Fig. 3B).
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, C and D). The medial preoptic complex contained slightly fewer immunoreactive cells in the anterodorsal and medial preoptic subunits, and only a few cells were seen in the lateral preoptic area.
At the anterior level, a few positive cells were detected in the periventricular nucleus, the caudal portion of the medial preoptic nucleus, and the anterior hypothalamic nucleus. Here, a strand of labeled cells appeared to be aligned in a ventrolateral orientation next to the lateral hypothalamus that extended from the fornix to the supraoptic nucleus. In contrast, most neurons of the supraoptic and the parvo- as well as magnocellular paraventricular nuclei contained immunoreactive VGLUT2 (Fig. 3, E–H). The suprachiasmatic nucleus was unlabeled, as was the lateral hypothalamus.
In the tuberal region many immunoreactive cells were present in the dorsal hypothalamic area, and fewer and less densely stained cells were seen in the dorsomedial, ventromedial, and arcuate nuclei. Only a few cells were identified in the lateral hypothalamus. In the mammillary complex, labeled cells were seen only in the lateral and medial mammillary nuclei.
Fibers.
VGLUT2-immunoreactive fibers had a punctuate appearance and were present in very large numbers throughout the septum-hypothalamus. At the light microscopic level, it appeared that immunoreactive puncta were juxtaposed to almost every neuron in the brain regions examined. There were, however, small regional differences in the number of immunoreactive puncta. Thus, the medial septum, most parts of the lateral septum, and the vertical limb of the diagonal band contained fewer VGLUT2-immunoreactive puncta compared with the horizontal limb of the diagonal band, the ventral part of the lateral septum, as well as the lambdoid region (Fig. 3A). The preoptic area was very heavily labeled, especially the periventricular preoptic nucleus, the anteroventral periventricular nucleus, and the region surrounding the organum vasculosum of the lamina terminalis (Fig. 3B). In the anterior hypothalamus, the supraoptic, paraventricular, and suprachiasmatic nuclei contained less abundant VGLUT2-containing puncta compared with the anterior hypothalamic nucleus. In the tuberal region, immunoreactive puncta were seen in high density in the ventromedial, dorsomedial, and arcuate nuclei as well as in the external layer of the median eminence and the posterior pituitary (Fig. 3, I and J). The mammillary complex did not contain VGLUT2-immunoreactive puncta, whereas the lateral hypothalamus contained a comparatively moderate number of VGLUT2-immunoreactive fibers throughout its extent. The results are summarized in Table 1.
Dual immunohistochemistry for VGLUT2 and synaptophysin showed that many VGLUT2-immunoreactive puncta were colocalized with synaptophysin immunoreactivity. Examples of colocalizations of VGLUT2 and synaptophysin in the ventromedial nucleus and the median eminence are shown in Fig. 4, A–F.
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, A–D).
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-aminobutyric acid. VGLUT proteins are present in the areas of the brain that are known to be glutamatergic, and VGLUTs are localized to synaptic vesicles, as has been shown with electron microscopic immunohistochemistry and by differential centrifugation followed by Western blot analysis (8, 10). In addition, we observed colocalization of VGLUT2 protein with synaptophysin, which further indicates that this transporter is preferentially directed to presynaptic terminals. The results of the present study confirm and extend the data reported by Kaneko et al. (16) and show that VGLUT2 protein is present in numerous neurites in all regions of the septum and hypothalamus, which suggests that glutamate-containing presynaptic terminals are, from an anatomical point of view, in a position to affect almost every neuron in these brain regions. These data thus support the hypothesis that glutamate is the major excitatory neurotransmitter in the hypothalamus and participates in the regulation of probably all neuroendocrine systems (1). As a typical example of a neuroendocrine system, we examined GnRH perikarya in the medial septum-diagonal band and showed that these neurons were closely apposed by many VGLUT2-immunoreactive boutons, many of which contained synaptophysin. In addition to numerous axo-somatic contacts between VGLUT2-immunoreactive terminals and their target neurons, we identified VGLUT 2 protein in axon terminals in the external layer of the median eminence, which is the site where all hypophysiotropic hormones are released into the primary plexus of the hypothalamo-hypohyseal vasculature (20). The presence of VGLUT2 in this layer of the median eminence suggests that glutamate can stimulate the release of neurohormones from neighboring axon terminals into the blood, thus exerting a final control over coordinated neurohormone release. This view is supported by the findings that many neuroendocrine axon terminals in the median eminence contain glutamate receptor subunits, such as the N-methyl-D,L-aspartate or kainate subunits (21, 22, 23). Thus, glutamate released from the VGLUT2-positive axon terminals could bind to and activate these ion channels, which would cause the release of neurohormones. Furthermore, glutamate released in the external layer of the median eminence could enter the fenestrated capillaries of the primary plexus and act on the anterior pituitary cells directly. Such a direct stimulatory action of glutamate has been demonstrated for GH- and PRL-secreting cells, which release their hormone in response to the addition of glutamate in vitro (24, 25).
An examination of the distribution of VGLUT2 mRNA indicates that many neuroendocrine neurons probably coexpress glutamate in addition to neuropeptides. Thus, the magnocellular neurons of the supraoptic (SON) and paraventricular (PVN) nuclei, which synthesize oxytocin or vasopressin, also express VGLUT2 mRNA and protein, as do certain cells in the parvocellular paraventricular nucleus that house the neurons that synthesize CRH. Previous studies have shown that many neurosecretory neurons in these nuclei are sensitive to glutamate (26, 27), and it was thought that most excitatory input originates from intrahypothalamic sites near the SON or PVN (28). The possibility that glutamatergic neurons could also reside inside the SON and PVN was first substantiated by electrophysiological studies that measured fast excitatory postsynaptic potentials in isolated nuclei that were blocked by glutamate receptor antagonists (29). The results of the present study confirm the existence of such intranuclear glutamatergic neurons as well as a strong glutamatergic innervation of these neurosecretory neurons, and they raise the possibility that, in fact, certain oxytocin-, vasopressin-, or CRH-synthesizing neurons are also glutamatergic. This view is supported by the finding that the size and location of the VGLUT2-immunoreactive neurons correspond well to the magnocellular oxytocin- and vasopressin-positive neurons in the supraoptic and paraventricular nuclei as well as to the CRH neurons in the parvocellular paraventricular nucleus. Similarly, the arcuate nucleus, which houses a large number of neuroendocrine cells that synthesize, among many others, somatostatin, dopamine, or neuropeptide Y, contains many VGLUT2 mRNA-expressing neurons, and, based upon the numbers and location of the glutamatergic neuron, it can be expected that many of the aminergic and peptidergic neurons in the arcuate nucleus coexpress glutamate as neurotransmitter, as has been shown for the catecholaminergic neurons in the brainstem (30). Future dual labeling experiments are needed to determine the exact phenotype of the glutamatergic neurons in these brain regions.
A comparison of the distribution of VGLUT2 mRNA with the distribution of the different ionotropic glutamate receptor subunit mRNAs suggests that many glutamatergic cells are themselves regulated by glutamate (31). For instance, in the ventromedial nucleus most neurons express VGLUT2 mRNA as well as large amounts of N-methyl-D,L-aspartate, 
-amino-3 hydroxy-5 methyl-4 isoxazole proprionic acid, and kainate subunit mRNAs. Similarly in the preoptic region, the AVPV and the median preoptic nuclei express most ionotropic glutamate receptor subunits as well as VGLUT2 mRNA. An exception to this scheme appears to be the suprachiasmatic nucleus, which expresses all known ionotropic glutamate receptor subunits (31), but not VGLUT2 mRNA. This finding indicates that the suprachiasmatic nucleus receives its extensive glutamatergic input from the retina and other brain regions and not from intranuclear glutamatergic neurons, and that the output of this nucleus is mediated by neurotransmitters other than glutamate.
Up until now no data have been available on the promotor region of the VGLUT2 gene and the regulation of VGLUT2 expression. However, based upon the distribution of steroid hormone receptor protein (32) and mRNAs (33) and VGLU2 mRNA in the hypothalamus, we predict that VGLUT2 expression is, at least in certain hypothalamic regions, regulated by gonadal and adrenal steroids. For instance, many neurons in the AVPV, arcuate nucleus, and ventromedial nucleus contain estrogen receptor-, and it is known that estradiol regulates the synthesis of many neurotransmitters/hormones as well as receptor proteins in these cells. Similarly, the neurons in the supraoptic and paraventricular nucleus express estrogen receptor-ß (34), and because many of these neurons are in the same location as GLUT2-containing cells, it is likely that steroid hormones could regulate the glutamate transporter expression.
In summary, the results show that glutamatergic neurons as identified by the presence of VGLUT2 mRNA and VGLUT2 protein are widely distributed throughout the septum-hypothalamus in a distinct pattern, suggesting that glutamatergic neurons participate in the control of probably all neuroendocrine systems and that many glutamatergic cells probably express other neuropeptides or monoamines. Detailed studies are needed to determine the precise phenotypes of the glutamatergic neurons as well as their regulation by neurotransmitters and steroid hormones.
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Footnotes |
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Abbreviations: AVPV, Anteroventral periventricular nucleus; OVLT, organum vasculosum laminae terminalis; PVN, paraventricular nucleus; SON, supraoptic nucleus; SSC, standard saline citrate; VGLUT, vesicular glutamate transporter.
Received August 29, 2002.
Accepted for publication October 31, 2002.
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and -ß mRNA in the rat central nervous system. J Comp Neurol 388:507–525[CrossRef][Medline]
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