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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Central nervous system control of food intake
Schwartz, M. W., Woods, S. C., Porte, D., Seeley, R. J., & Baskin, D. G. (2000) · Nature · doi:10.1038/35007534 · Cited by 6,451
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Herman, J. P., & Cullinan, W. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10069-2 · Cited by 2,270
Brain Maps: Structure of the Rat Brain
Swanson, L. W. (1992) · Medical Entomology and Zoology · Cited by 1,878
Localization of neuronal and glial glutamate transporters
Rothstein, J. D., Martin, L. J., Levey, A. I., Dykes‐Hoberg, M., Jin, L., Wu, D. M., Nash, N. R., & Kuncl, R. W. (1994) · Neuron · doi:10.1016/0896-6273(94)90038-8 · Cited by 1,703
Brain maps: structure of the rat brain
Guillery, R. W. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90187-q · Cited by 1,669
The Expression of Vesicular Glutamate Transporters Defines Two Classes of Excitatory Synapse
Fremeau, R. T., Troyer, M. D., Pahner, I., Nygaard, G. O., Tran, C. H., Reimer, R. J., Bellocchio, E. E., Fortin, D. L., Storm‐Mathisen, J., & Edwards, R. H. (2001) · Neuron · doi:10.1016/s0896-6273(01)00344-0 · Cited by 1,266
Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons
Takamori, S., Rhee, J. S., Rosenmund, C., & Jahn, R. (2000) · Nature · doi:10.1038/35025070 · Cited by 862
Cerebral hemisphere regulation of motivated behavior
Swanson, L. W. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02905-x · Cited by 846
Regional expression of a gene encoding a neuron-specific Na+-dependent inorganic phosphate cotransporter (DNPI) in the rat forebrain
Hisano, S., Hoshi, K., Ikeda, Y., Maruyama, D., Kanemoto, M., Ichijo, H., Kojima, I., Takeda, J., & Nogami, H. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(00)00194-7 · Cited by 806

Show all 53 references

Research works printed but not linked: 3

Storm‐Mathisen J, 1995, CNS neurotransmitters and neuromodulators: glutamate, 1
Swanson LW, 1987, Integrated systems of the CNS, Part I: Hypothalamus, hippocampus, amygdala, retina, 1
Wisden W, 2000, Handbook of chemical neuroanatomy: Glutamate, 99

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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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