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Anatomy of an Endogenous Antagonist: Relationship between Agouti-Related Protein and Proopiomelanocortin in Brain
Open accessAbstract
Agouti-related protein (AGRP) is a recently discovered orexigenic neuropeptide that inhibits the binding and action of alpha-melanocyte-stimulating hormone derived from proopiomelanocortin (POMC) at the melanocortin 3 receptor (MC3R) and melanocortin 4 receptor (MC4R) and has been proposed to function primarily as an endogenous melanocortin antagonist. To better understand the interplay between the AGRP and melanocortin signaling systems, we compared their nerve fiber distributions with each other by immunohistochemistry and their perikarya distribution with MC3R and MC4R by double in situ hybridization. Although deriving from distinct cell groups, AGRP and melanocortin terminals project to identical brain areas. Both AGRP and melanocortin neurons selectively express the MC3R, which provides a neuroanatomical basis for a dual-input circuit with biological amplification and feedback inhibition. These studies highlight a broader complexity in POMC-mediated behavior in the brain.
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“Neurons expressing agouti-related protein (AgRP) are found exclusively in the ARC [20]”
From Chronic unpredictable stress induces depression-related behaviors by suppressing AgRP neuron activity (2021) · cites this paper as [20]
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“However, available anatomical evidence suggests that AgRP neurons may functionally interact with the mesolimbic pathway [20, 62, 86], which has been implicated in depression [56].”
From Chronic unpredictable stress induces depression-related behaviors by suppressing AgRP neuron activity (2021) · cites this paper as [20]
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“As AgRP neurons project to multiple brain regions involved in stress reactivity and reward processing [20, 62, 86], it is not clear which downstream targets may be contributing to the effects of AgRP neurons on depression-related behaviors.”
From Chronic unpredictable stress induces depression-related behaviors by suppressing AgRP neuron activity (2021) · cites this paper as [20]
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“Another candidate downstream target of AgRP neurons is the bed nucleus of the stria terminalis (BNST) [20, 62], which has emerged as a key player in stress-related disorders [90, 91].”
From Chronic unpredictable stress induces depression-related behaviors by suppressing AgRP neuron activity (2021) · cites this paper as [20]
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BackgroundVoluntary exercise improves hypothalamic and metabolic function in obese mice
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“Melanocortin agonist POMC-expressing neurons have been identified as coexpressing cocaine- and amphetamine-regulated transcript (CART) (41), the MC3R (42, 43), leptin receptors (44, 45), and the neuropeptide Y (NPY) Y1 receptor (46).”
BackgroundProteins Activate Satiety-Related Neuronal Pathways in the Brainstem and Hypothalamus of Rats3
Faipoux, R., Tomé, D., Gougis, S., Darcel, N., & Fromentin, G. (2008) · Journal of Nutrition · doi:10.1093/jn/138.6.1172 · Cited by 72
“Neurons in this area are principally regulated by 2 types of signals: 1) circulating nutrients and/or hormones; and 2) other brain areas involved in the regulation of food intake, especially NPY/AgRP neurons in the ARC.”
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“Recently, the MC3 receptor was identified on the AgRP neuron [45], but α-MSH secreted from POMC may become one of the candidate substances controlling the activation of the NPY/AgRP neuron in future studies.”
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“…dashed lines represent the mean differences between the methods and small dashed lines, mean 2 S.D. at A SPE T Journals on A ugust 18, 2017 jpet.aspetjournals.org D ow nloaded from tory autoreceptors on pro-opiomelanocortin neurons of the arcuate nucleus of the hypothalamus (Bagnol et al., 1999).”
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Agouti-Related Protein 2 Is a New Player in the Teleost Stress Response System
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Regulation of energy rheostasis by the melanocortin-3 receptor
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“These data sup port a role of MC3R specifically expressed in ARC neurons in medi ating the homeostatic responses shown here.”
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MacNeil, D. J., Howard, A. D., Guan, X.-M., Fong, T. M., Nargund, R. P., Bednarek, M. A., Goulet, M. T., Weinberg, D. H., Strack, A. M., Marsh, D. J., et al. (2002) · European Journal of Pharmacology · doi:10.1016/s0014-2999(02)01425-5 · Cited by 64
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“MelanocortinMC3 receptor is expressedwidely within the CNSwith abundant expression in the proopiomelanocortin and NPY neurons of the arcuate nucleus (Bagnol et al., 1999; Mounien et al., 2005).”
Role of melanocortin signaling in the regulation of the hypothalamic–pituitary–thyroid (HPT) axis
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“Moreover, AgRP, endogenous antagonist of MCRs, has high affinity for both these receptors [41,42], reflecting a differential regulation of the metabolic response and food consumption [7,42,52].”
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“In contrast, the role of this neuronal population in the control of SNA had been largely unexplored, despite recent evidence that NPY acts in the PVN to inhibit SNA (4, 5, 26) and that NPY/ AgRP neurons project to the PVN (9, 16, 19).”
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“MC3R mRNA has been co-localized to both AgRP and POMC neurons in a rostrocaudal gradient in the arcuate nucleus [56].”
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“through the presence of MC3 receptors on NPY neurons (64)”
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“In the viral POMC-ChR2 mice, CLARITY processing showed that Arc POMC neurons project to a number of brain regions (SI Appendix, Table S1), consistent with previous anatomical studies (46, 47).”
ResultSelf-citationEllacott, K. L. J., Halatchev, I. G., & Cone, R. D. (2005) · Peptides · doi:10.1016/j.peptides.2005.02.031 · Cited by 51
Integration of sensory information via central thermoregulatory leptin targets
Rezai-Zadeh, K. P., & Münzberg, H. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.02.014 · Cited by 52
“Within this POA>DMH/DHA>rRPa>BAT neuronal pathway leptin receptor (LepRb) expressing neurons are found in the POA and DMH/DHA, but not the rRPa.”
BackgroundInfluentialHypothalamic regulation of appetite
Simpson, K. A., Martin, N. M., & Bloom, S. R. (2008) · Expert Review of Endocrinology & Metabolism · doi:10.1586/17446651.3.5.577 · Cited by 49
“Gastroenterology 124(5), 1325–1336 (2003). Batterham RL, Le Roux CW, Cohen MA 206”
BackgroundCentral Melanocortins Regulate the Motivation for Sucrose Reward
Pandit, R., van der Zwaal, E. M., Luijendijk, M. C. M., Brans, M. A. D., van Rozen, A. J., Ophuis, R. J. A. O., Vanderschuren, L. J. M. J., Adan, R. A. H., & la Fleur, S. E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0121768 · Cited by 48
Polymorphisms and mutations in the melanocortin-3 receptor and their relation to human obesity
Demidowich, A. P., Jun, J. Y., & Yanovski, J. A. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.03.018 · Cited by 50
“In the rostral arcuate nucleus, MC3R mRNA is expressed in about 40% of POMC neurons and >50% of NPY/AGRP neurons [29, 30].”
BackgroundRaposinho, P., White, R. B., & Aubert, M. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.00962.x · Cited by 52
Agouti-related protein increases food hoarding more than food intake in Siberian hamsters
Day, D. E., & Bartness, T. J. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00284.2003 · Cited by 47
Loos, R. J. F., Rankinen, T., Rice, T., Rao, D. C., Leon, A. S., Skinner, J. S., Bouchard, C., & Argyropoulos, G. A. (2005) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/82.5.1097 · Cited by 47
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Participation of the central melanocortin system in metabolic regulation and energy homeostasis
Jeong, J. K., Kim, J. G., & Lee, B. J. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1650-z · Cited by 49
“Particularly in the ARC, MC3R is produced both by POMC- and AgRP/NPY-ergic neurons [102, 103].”
BackgroundMelanocortin control of energy balance: evidence from rodent models
Jonghe, B. C. D., Hayes, M. R., & Bence, K. K. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0707-5 · Cited by 50
“expressed in about half of POMC [184, 185] and AgRP [185] cells located in the rostral section of ARC, while no”
BackgroundSergi, D., & Williams, L. M. (2019) · Nutrition Reviews · doi:10.1093/nutrit/nuz056 · Cited by 48
van den Top, M., Lyons, D. J., Lee, K., Coderre, E., Renaud, L. P., & Spanswick, D. C. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.09.059 · Cited by 45
Goyal, S. N., Kokare, D. M., Ct, C., & Subhedar, N. K. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.09.004 · Cited by 46
β-MSH: a functional ligand that regulated energy homeostasis via hypothalamic MC4-R?
Harrold, J. A., Widdowson, P. S., & Williams, G. (2003) · Peptides · doi:10.1016/s0196-9781(03)00054-8 · Cited by 46
The central melanocortin system and the regulation of energy balance
Lee, M. (2007) · Frontiers in Bioscience · doi:10.2741/2366 · Cited by 45
“Centrally, the MC3-R localizes to the limbic system and hypothalamus, where it is expressed within the arcuate nucleus on both POMC and AGRP neurons and may mediate crosstalk between these neurons (4, 101).”
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Age‐Associated Changes in Hypothalamic and Pituitary Neuroendocrine Gene Expression in the Rat
Kappeler, L., Gourdji, D., Zizzari, P., Bluet‐Pajot, M., & Epelbaum, J. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01039.x · Cited by 44
Alpha-Melanocyte-Stimulating Hormone-Mediated Appetite Regulation in the Central Nervous System
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Trotta, M., Bello, E. P., Alsina, R., Tavella, M. B., Ferrán, J. L., Rubinstein, M., & Bumaschny, V. F. (2020) · Molecular Metabolism · doi:10.1016/j.molmet.2020.100985 · Cited by 45
Obesity: basic science and medical aspects relevant to anaesthetists
Cheah, M. H., & Kam, P. C. A. (2005) · Anaesthesia · doi:10.1111/j.1365-2044.2005.04229.x · Cited by 42
Plasticity of the Melanocortin System: Determinants and Possible Consequences on Food Intake
Nuzzaci, D., Laderrière, A., Lemoine, A., Nédélec, E., Pénicaud, L., Rigault, C., & Bénani, A. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00143 · Cited by 44
Novel Aspects of Brown Adipose Tissue Biology
Heeren, J., & Münzberg, H. (2012) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2012.11.004 · Cited by 43
The Anorexigenic Fatty Acid Synthase Inhibitor, C75, Is a Nonspecific Neuronal Activator
Takahashi, K. A., Smart, J. L., Liu, H., & Cone, R. D. (2003) · Endocrinology · doi:10.1210/en.2003-0337 · Cited by 42
Astrocytes: new targets of melanocortin 4 receptor actions
Caruso, C. M., Carniglia, L., Durand, D., Scimonelli, T. N., & Lasaga, M. (2013) · Journal of Molecular Endocrinology · doi:10.1530/jme-13-0064 · Cited by 42
“1992); from there, POMC neurons project throughout the brain (Bagnol et al. 1999).”
Backgrounda-MSH enhances activity-based anorexia
Hillebrand, J. J., Kas, M. J., & Adan, R. A. H. (2005) · Peptides · doi:10.1016/j.peptides.2004.11.027 · Cited by 41
Melanocortin-3 Receptors and Metabolic Homeostasis
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“In the rat brain, POMC is also expressed in two discrete neuronal groups, the arcuate nucleus (Ac) of the hypothalamus, and the caudal region of the nucleus of the tractus solitarius (NTS) of the medulla (Bangol et al., 1999).”
Gene expression profiling of melanocortin system in neuropathic rats supports a role in nociception
Beltramo, M., Campanella, M., Tarozzo, G., Fredduzzi, S., Corradini, L., Forlani, A., Bertorelli, R., & Reggiani, A. M. (2003) · Molecular Brain Research · doi:10.1016/j.molbrainres.2003.08.001 · Cited by 40
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“POMC and AgRP neurons in the ARC exhibit similar projection patterns throughout the brain [6, 14], innervating brain regions involved in neuroendocrine control and adaptive behaviors related to stress, such as the paraventricular nucleus of the hypothalamus (PVN), bed nucleus of the stria terminalis, and amygdala [14].”
BackgroundSelf-citationSerotonergic pathways converge upon central melanocortin systems to regulate energy balance
Zhou, L., Williams, T. B., Lachey, J. L., Kishi, T., Cowley, M. A., & Heisler, L. K. (2005) · Peptides · doi:10.1016/j.peptides.2004.12.028 · Cited by 39
Leptin and melanocortin signaling in the hypothalamus
Bjørbæk, C., & Hollenberg, A. N. (2002) · Vitamins and hormones · doi:10.1016/s0083-6729(02)65068-x · Cited by 40
Metadata
- Authors
- Bagnol, D., Lu, X.-Y., Kaelin, C. B., Day, H. E. W., Ollmann, M., Gantz, I., Akil, H., Barsh, G. S., & Watson, S. J.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Mental Health Research Institute (AU)
- Howard Hughes Medical Institute (US)
- University of Michigan (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1999-09-15
- Volume
- 19
- Issue
- 18
- Pages
- RC26-RC26
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6782481
- OpenAlex
- W1572502886
- Cited by
- 425
- References
- 29
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 15 · 2023: 11 · 2022: 11 · 2021: 12 · 2020: 10 · 2019: 11 · 2018: 14 · 2017: 12 · 2016: 14 · 2015: 20 · 2014: 9 · 2013: 16 · 2012: 18
- FWCI
- 6.81
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (P01 MH 42251, P01MH042251)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK-54032-01, R01DK054032, DK 28506)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Keywords
- agouti-related protein, proopiomelanocortin, melanocortin 3 receptor, melanocortin-4 receptor, melanocortin signaling, orexigenic peptides, product inhibition, neuroanatomy, feeding behavior
- MeSH terms
- Animals, Autoradiography, Brain, Immunohistochemistry, Male, Nerve Fibers, Pro-Opiomelanocortin, Proteins, Rats, Sprague-Dawley, In Situ Hybridization, Receptors, Corticotropin, Intercellular Signaling Peptides and Proteins, Receptor, Melanocortin, Type 3, Receptor, Melanocortin, Type 4, Rats, Agouti-Related Protein
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