Cited by 241Neuroscience and Neuropharmacology ResearchRegulation of Appetite and ObesityAmino Acid Enzymes and Metabolism

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Distribution of vesicular glutamate transporter mRNA in rat hypothalamus

Ziegler, Dana R., Cullinan, William E., Herman, James P.·2002·Journal of Comparative Neurology

DOI 10.1002/cne.10257

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Abstract

Two isoforms of the vesicular glutamate transporter, VGLUT1 and VGLUT2, were recently cloned and biophysically characterized. Both VGLUT1 and VGLUT2 specifically transport glutamate into synaptic vesicles, making them definitive markers for neurons using glutamate as a neurotransmitter. The present study takes advantage of the specificity of the vesicular transporters to afford the first detailed map of putative glutamatergic neurons in the rat hypothalamus. In situ hybridization analysis was used to map hypothalamic distributions of VGLUT1 and VGLUT2 mRNAs. VGLUT2 is clearly the predominant vesicular transporter mRNA found in the hypothalamus; rich expression can be documented in regions regulating energy balance (ventromedial hypothalamus), neuroendocrine function (preoptic nuclei), autonomic tone (posterior hypothalamus), and behavioral/homeostatic integration (lateral hypothalamus, mammillary nuclei). Expression of VGLUT1 is decidedly more circumspect and is confined to relatively weak labeling in lateral hypothalamic regions, neuroendocrine nuclei, and the suprachiasmatic nucleus. Importantly, dual-label analysis revealed no incidence of colocalization of VGLUT1 or VGLUT2 mRNAs in glutamic acid decarboxylase (GAD) 65-positive neurons, indicating that GABA neurons do not express either transporter. Our data support a major role for hypothalamic glutamatergic neurons in regulation of all aspects of hypothalamic function.

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Hrabovszky, E., Kalló, I., Turi, G. F., May, K., Wittmann, G., Fekete, C., & Liposits, Z. (2006) · Endocrinology · doi:10.1210/en.2005-1229 · Cited by 26
“• VGLUT2 in Adenohypophysis Endocrinology, August 2006, 147(8):3818–3825 3821”
BackgroundInfluential
Layer-Specific Vesicular Glutamate Transporter 1 Immunofluorescence Levels Delineate All Layers of the Human Hippocampus Including the Stratum lucidum
Woelfle, S., & Boeckers, T. M. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.789903 · Cited by 23
Effect of relative social rank within a social hierarchy on neural activation in response to familiar or unfamiliar social signals
Lee, W., Dowd, H. N., Nikain, C., Dwortz, M. F., Yang, E., & Curley, J. P. (2021) · Scientific Reports · doi:10.1038/s41598-021-82255-8 · Cited by 29
The hypothalamic ventral premammillary nucleus: A key site in leptin's regulation of reproduction
Leshan, R. L., & Pfaff, D. W. (2014) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2014.08.008 · Cited by 25
Glutamatergic neurons say NO in the nucleus tractus solitarii
Lin, L. (2009) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2009.02.002 · Cited by 24
“The physiologic relevance of this finding requires further investigation, but it is noteworthy that VGluT1 and VGluT2 are often distributed in a complementary fashion in the central nervous system in rat (Herzog et al., 2001; Ziegler et al., 2001; Kaneko and Fujiyama, 2002).”
Background
Neurobiological characteristics underlying metabolic differences between males and females
Chowen, J. A., Freire‐Regatillo, A., & Argente, J. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.09.001 · Cited by 24
Amyloid‐beta1–42 induced glutamatergic receptor and transporter expression changes in the mouse hippocampus
Yeung, J. H. Y., Guzmán, B. C., Palpagama, T. H., Ethiraj, J., Zhai, Y., Tate, W. P., Peppercorn, K., Waldvogel, H. J., Faull, R. L. M., & Kwakowsky, A. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15099 · Cited by 24
Presence of vesicular glutamate transporter‐2 in hypophysiotropic somatostatin but not growth hormone‐releasing hormone neurons of the male rat
Hrabovszky, E., Turi, G. F., & Liposits, Z. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04076.x · Cited by 23
“To confirm VGLUT2 hybridization specificity in positive control experiments, the ‘VGLUT2-879’ probe was replaced with the ‘VGLUT2-734’ probe kindly provided by Dr J. P. Herman (Ziegler et al., 2002; Hrabovszky et al., 2004b, 2005), targeting a nonoverlapping segment (bases 1704–2437) of VGLUT2 mRNA.”
Method
Single-cell multiplex qPCR evidence for sex-dimorphic glutamate decarboxylase, estrogen receptor, and 5′-AMP-activated protein kinase alpha subunit mRNA expression by ventromedial hypothalamic nucleus GABAergic neurons
Ali, M. H., Alshamrani, A. A., Napit, P. R., & Briski, K. P. (2022) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2022.102132 · Cited by 22
Area-specific analysis of the distribution of hypothalamic neurons projecting to the rat ventral tegmental area, with special reference to the GABAergic and glutamatergic efferents
Kalló, I., Molnár, C. S., Szöke, S., Fekete, C., Hrabovszky, E., & Liposits, Z. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00112 · Cited by 21
“, 1993) and VGLUT1 (Ziegler et al., 2002) expression, respectively.”
Defining the caudal hypothalamic arcuate nucleus with a focus on anorexic excitatory neurons
van den Pol, A. N., Acuna, C., Davis, J. N., Huang, H., & Zhang, X. (2019) · The Journal of Physiology · doi:10.1113/jp277152 · Cited by 20
“A previous in situ hybridization study reported strong expression of vGluT2 in various hypothalamic nuclei, but noted “no vGluT2 expression was seen in the arcuate nucleus” (Ziegler et al. 2002).”
Background
Regulation and neurochemical identity of melanin‐concentrating hormone neurones in the preoptic area of lactating mice
Teixeira, P. D. S., Wasinski, F., Lima, L. B., Frazão, R., Bittencourt, J. C., & Donato, J. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12818 · Cited by 21
Synaptic contacts of vesicular glutamate transporter 2 fibres on chemically identified neurons of the hypothalamic suprachiasmatic nucleus of the rat
Kiss, J. Z., Csáki, Á., Csaba, Z., & Halász, B. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06463.x · Cited by 21
“In addition, there are VGluT2 (Kiss et al., 2007) and VGluT1 mRNA-containing neurons in the cell group (Ziegler et al., 2002).”
Background
VGLUT‐VGAT expression delineates functionally specialised populations of vasopressin‐containing neurones including a glutamatergic perforant path‐projecting cell group to the hippocampus in rat and mouse brain
Zhang, L., Hernández, V. S., Zetter, M. A., & Eiden, L. E. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12831 · Cited by 19
“(A) PVN (1) PVN (1) PVN (1) ZI (6) AN (4) SON (3) AN (4) SON (3) BNSTam (5) Ascending axonal expression Opt Ch SCN (2) BNSTpl (7) PVN (1) SON (3) AON (17) BNSTpl (7) SON (3) LH (8)/ZI (6) VTA (9)AN (4)LH (8) MOB- CeA (13) CEnt (15) CEnt (15) CeA (13) BLA PC (18) VLEnt (14)STIA (12) CeA (13) CeA (13) STIA (12) CEnt ZI(…”
Influential
Posterior lateral hypothalamic axon terminals are in contact with trigeminal premotor neurons in the parvicellular reticular formation of the rat medulla oblongata
Notsu, K., Tsumori, T., Yokota, S., Sekine, J., & Yasui, Y. (2008) · Brain Research · doi:10.1016/j.brainres.2008.09.076 · Cited by 19
“VGLUT has been considered to be a much better marker for glutamatergic neurons (Kaneko and Fujiyama, 2002), and it has been reported that LHA neurons express predominantly VGLUT2 mRNA and additionally VGLUT1 mRNA (Ziegler et al., 2002).”
Blockade of TrkB receptors in the nucleus accumbens prior to heterotypic stress alters corticotropin-releasing hormone (CRH), vesicular glutamate transporter 2 (vGluT2) and glucocorticoid receptor (GR) within the mesolimbic pathway
Azogu, I., & Plamondon, H. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.02.012 · Cited by 20
“Neurons in these areas express markers for the vesicular glutamate transporters (vGluTs) 1, 2, and 3 (Fremeau et al., 2002; Ziegler et al., 2002), which for the most part act to facilitate glutamate release and provide high-affinity reuptake for released glutamate (Fremeau et al.”
High expression of hippocampal glutamic acid decarboxylase 67 mediates hypersensitivity of the hypothalamic-pituitary-adrenal axis in response to prenatal caffeine exposure in rats
Xu, D., Zhang, C., He, X., Guo, Z., Hu, D., Lu, J., Cheng, S., & Wang, H. (2017) · Toxicology Letters · doi:10.1016/j.toxlet.2017.10.019 · Cited by 19
Hypoglycemia: Role of Hypothalamic Glucose-Inhibited (GI) Neurons in Detection and Correction
Zhou, C., Teegala, S. B., Khan, B. A., Gonzalez, C., & Routh, V. H. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00192 · Cited by 19
“The VMH possesses high expression of mRNA encoding the vesicular glutamate transporter VGLUT2, a marker for glutamate neurons (Ziegler et al., 2002).”
Background
Vasopressinergic network abnormalities potentiate conditioned anxious state of rats subjected to maternal hyperthyroidism
Zhang, L., Medina‐Pizarro, M., Hernández, V. S., Estrada, F. S., & Vega‐González, A. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.03.059 · Cited by 19
Antagonism of orexin receptors in the posterior hypothalamus reduces hypoglossal and cardiorespiratory excitation from the perifornical hypothalamus
Stettner, G. M., & Kubin, L. K. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00965.2012 · Cited by 19
Activity-Dependent Modulation of Neurotransmitter Innervation to Vasopressin Neurons of the Supraoptic Nucleus
Mueller, N. K., Di, S., Paden, C. M., & Herman, J. P. (2004) · Endocrinology · doi:10.1210/en.2004-0539 · Cited by 18
Inhalation of a racemic mixture (R,S)-linalool by rats experiencing restraint stress alters neuropeptide and MHC class I gene expression in the hypothalamus
Yoshida, K., Yamamoto, N., Fujiwara, S., Kamei, A., Abe, K., & Nakamura, A. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.05.046 · Cited by 17
“SLC17A6 (VGLUT2) specifically transports glutamate into synaptic vesicles (40).”
Background
Vesicular glutamate transporter 2 protein and mRNA containing neurons in the hypothalamic suprachiasmatic nucleus of the rat
Kiss, J. Z., Halász, B., Csáki, Á., Liposits, Z., & Hrabovszky, E. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2007.07.023 · Cited by 17
“The number of VGluT2 immunopositive neurons we detected was very limited, and therefore the positive cells could easily be overlooked, particularly if one did not focus exclusively on the SCN, but studied a larger brain region such as the hypothalamus as did Ziegler et al. [ 59 ] and Lin et al. [34].”
Background
Co-localization of corticotropin-releasing factor and vesicular glutamate transporters within axon terminals of the rat dorsal raphe nucleus
Waselus, M., & Bockstaele, E. J. V. (2007) · Brain Research · doi:10.1016/j.brainres.2007.08.014 · Cited by 17
LMO4 Is Essential for Paraventricular Hypothalamic Neuronal Activity and Calcium Channel Expression to Prevent Hyperphagia
Zaman, T., Zhou, X. C., Pandey, N. R., Qin, Z., Keyhanian, K., Wen, K., Courtney, R. D., Stewart, A. F. R., & Chen, H. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3419-13.2014 · Cited by 16
“PVH neurons are excitatory glutamatergic neurons (Ziegler et al., 2002; Rosin et al., 2003; Hrabovszky et al., 2005; Hur and Zaborszky, 2005; Stocker et al., 2006).”
Identification of neural cells activated by mating stimulus in the periaqueductal gray in female rats
Yamada, S., & Kawata, M. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00421 · Cited by 16
“The upstream and downstream primers were 5′-CTT CTT GGT GCT TGC AGT GG and 5′-GGA CGA ATG GCC TGA ATG GA, respectively (Ziegler et al., 2002).”
BackgroundMethodInfluential
The Structural and Electrophysiological Properties of Progesterone Receptor-Expressing Neurons Vary along the Anterior-Posterior Axis of the Ventromedial Hypothalamus and Undergo Local Changes across the Reproductive Cycle
Dias, I. C., Gutiérrez‐Castellanos, N., Ferreira, L., & Lima, S. Q. (2021) · eNeuro · doi:10.1523/eneuro.0049-21.2021 · Cited by 16
“The VMH is organized in a core of glutamatergic neurons (Ziegler et al 2002, Yamamoto et al 2018) and a surrounding shell with higher density of GABAergic neurons (Yamamoto et al 2018).”
Pharmacotherapy to enhance arousal: what is known and what is not
ZAFONTE, R. D., Hammond, F. M., Dennison, A. C., & Chew, E. (2009) · Progress in brain research · doi:10.1016/s0079-6123(09)17720-8 · Cited by 16
“Similarly to the RF, there is evidence of both glutamate (Ziegler et al., 2002) and GABA (Decavel et al.”
Background
Expression of Vesicular Glutamate Transporter 2 (vGluT2) on Large Dense-Core Vesicles within GnRH Neuroterminals of Aging Female Rats
Yin, W., Sun, Z., Mendenhall, J. M., Walker, D. M., Riha, P. D., Bezner, K. S., & Gore, A. C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129633 · Cited by 16
“No vGluT1 immunoreactivity was found at either the light or electron microscopic level in the median eminence; however immunofluorescent labeling was seen clearly in the cortex, suggesting that the failure to detect vGluT1 in the median eminence is due to its absence in this latter region, and consistent with other re…”
Result
Differential Effects of Dietary MSG on Hippocampal Dependent Memory Are Mediated by Diet
Holton, K. F., Hargrave, S. L., & Davidson, T. L. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00968 · Cited by 14
“Furthermore, arginine vasopressin-containing neurons in the hypothalamus have been shown to be glutamatergic neurons (Ziegler et al., 2002).”
Background
Evidence for a glutamatergic input to pontine preganglionic neurons of the superior salivatory nucleus in rat
Lin, L.-H., Agassandian, K., Fujiyama, F., Kaneko, T., & Talman, W. T. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(03)00033-4 · Cited by 15
Gene expression profiling of the SCN in young and old rhesus macaques
Eghlidi, D. H., Luna, S. L., Brown, D. I., Garyfallou, V. T., Kohama, S. G., & Urbanski, H. F. (2018) · Journal of Molecular Endocrinology · doi:10.1530/jme-18-0062 · Cited by 14
Responses to cholecystokinin in the ventromedial nucleus of the rat hypothalamus in vivo
Sabatier, N., & Leng, G. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07144.x · Cited by 14
“In particular, most neurons in the VMN are glutamatergic (Ziegler et al., 2002; Meister, 2007), and express SF-1 (Tong et al.”
Background
The Presynaptic Protein Mover Is Differentially Expressed Across Brain Areas and Synapse Types
Wallrafen, R., & Dresbach, T. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00058 · Cited by 13
A subset of thalamocortical projections to the retrosplenial cortex possesses two vesicular glutamate transporter isoforms, VGluT1 and VGluT2, in axon terminals and somata
Oda, S., Funato, H., Sato, F., Adachi‐Akahane, S., Ito, M., Takase, K., & Kuroda, M. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23519 · Cited by 13
“VGluT2 mRNA is expressed predominantly in these subcortical sources (Fremeau et al., 2001; Ziegler et al, 2002; Lin et al., 2003; Barroso-Chinea et al., 2007).”
Background
Neuropeptide Y – Its role in human performance and extreme environments
Kienast, C., Gunga, H., & Steinach, M. (2019) · REACH · doi:10.1016/j.reach.2019.100032 · Cited by 12
Coexpression of the mu‐opioid receptor splice variant MOR1C and the vesicular glutamate transporter 2 (VGLUT2) in rat central nervous system
Schnell, S. A., & Wessendorf, M. W. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21712 · Cited by 12
“This hypothesis is supported by the observations that VGLUT2 mRNA (Ziegler et al., 2002) and MOR1C mRNA Fig.”
Result
Discrete melanocortin-sensitive neuroanatomical pathway linking the ventral premmamillary nucleus to the paraventricular hypothalamus
Gautron, L., Cravo, R. M., Elmquist, J. K., & Elias, C. F. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.02.024 · Cited by 12
“…our anatomical observations, these nerve terminals principally originate from the PMv. Notably, the vast majority of PMv neurons is glutamatergic (Ziegler et al., 2002, Donato et al., 2010), which suggests that MC4-R in PMv neurons might contribute to the stimulatory effects of melanocortin…”
Background
Origin of thyrotropin-releasing hormone neurons that innervate the tuberomammillary nuclei
Sánchez‐Jaramillo, E., Wittmann, G., Menyhért, J., Singru, P. S., Gómez-González, G. B., Sánchez-Islas, E., Yáñez-Recendis, N., Pimentel, J. A., León‐Olea, M., Gereben, B., et al. (2022) · Brain Structure and Function · doi:10.1007/s00429-022-02527-5 · Cited by 11
Sex-specific prefrontal-hypothalamic control of behavior and stress responding
Schaeuble, D., Wallace, T., Pace, S. A., Hentges, S. T., & Myers, B. (2023) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2023.106413 · Cited by 12
Estrogen-responsive neural circuits governing male and female mating behavior in mice
Yu, Z., Zha, X., & Xu, X. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102749 · Cited by 12
Tangential Intrahypothalamic Migration of the Mouse Ventral Premamillary Nucleus and Fgf8 Signaling
López-González, L., Alonso, A., Garcı́a-Calero, E., Puelles, E., & Puelles, L. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.676121 · Cited by 11
Neurocircuit regulation of the hypothalamo–pituitary–adrenocortical stress response – an overview
Herman, J. P., Mueller, N. K., Figueiredo, H. F., & Cullinan, W. E. (2005) · Techniques in the behavioral and neural sciences · doi:10.1016/s0921-0709(05)80023-9 · Cited by 11
The influence of dorsomedial hypothalamic nucleus on contralateral paraventricular nucleus in NMDA-mediated cardiovascular responses
Gören, M. Z., Yananlı, H. R., Berkman, K., Onat, F., & Aker, R. G. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02241-8 · Cited by 10
Immunoelectron Microscopic Characterization of Vasopressin-Producing Neurons in the Hypothalamo-Pituitary Axis of Non-Human Primates by Use of Formaldehyde-Fixed Tissues Stored at −25 °C for Several Years
Otubo, A., Maejima, S., Oti, T., Satoh, K., Ueda, Y., Morris, J. F., Sakamoto, T., & Sakamoto, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179180 · Cited by 8
“It has been reported that rodent AVP neurons use glutamate as a neurotransmitter [16,17,35,36].”
Background
Hippocampal CA field neurogenesis after pilocarpine insult: The hippocampal fissure as a neurogenic niche
Zhang, L., Hernández, V. S., Estrada, F. S., & Luján, R. (2014) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2014.02.002 · Cited by 9

Authors: Ziegler, D. R., Cullinan, W. E., & Herman, J. P.
Affiliations: University of Kentucky (US)
Marquette University (US)
Corresponding author: Herman, James P.
ORCID: Herman, James P.
Venue: Journal of Comparative Neurology
Publisher: Wiley
Published: 2002-05-21
Volume: 448
Issue: 3
Pages: 217-229
ISSN: 0021-9967 (ISSN-L)
1096-9861
DOI: 10.1002/cne.10257
OpenAlex: W1977741133
Cited by: 241
References: 53
Citations by year: 2026: 1 · 2025: 1 · 2024: 4 · 2023: 10 · 2022: 8 · 2021: 10 · 2020: 5 · 2019: 12 · 2018: 14 · 2017: 10 · 2016: 11 · 2015: 11 · 2014: 9 · 2013: 12 · 2012: 9
FWCI: 5.25
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Comparative Neurology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r29mh056577-05, 5f31mh011980-02, 5r03mh060819-03)
National Institute of Mental Health (MH 60819, MH49698, MH56577, MH 11980)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
Keywords: vesicular glutamate transporter, VGLUT1, VGLUT2, hypothalamus, glutamatergic neurons, glutamatergic neurotransmission, mRNA distribution, ventromedial hypothalamus, suprachiasmatic nucleus, lateral hypothalamus, mammillary nuclei, GABAergic neurons, energy balance, neuroendocrine function, autonomic regulation
MeSH terms: Animals, Carrier Proteins, Gene Expression Regulation, Glutamate Decarboxylase, Hypothalamus, Male, Synaptic Transmission, Neurons, RNA, Messenger, Synaptic Vesicles, Biomarkers, Rats, Sprague-Dawley, In Situ Hybridization, Glutamic Acid, Membrane Transport Proteins, Vesicular Transport Proteins, Vesicular Glutamate Transport Protein 1, Vesicular Glutamate Transport Protein 2, Rats

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Distribution of vesicular glutamate transporter mRNA in rat hypothalamus

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