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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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Self-citationAgRP(83-132) Acts as an Inverse Agonist on the Human-Melanocortin-4 Receptor
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Whole-brain mapping of the direct inputs and axonal projections of POMC and AgRP neurons
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“Axonal Projection Patterns of POMC Neurons and AgRP Neurons Previous anterograde tracing and immunocytochemistry labeling have revealed that POMC neurons project to the paraventricular thalamic nucleus (PVT) and several hypothalamic nuclei (Fodor et al., 1998; Bagnol et al., 1999; Cowley et al., 2001).”
BackgroundPro-opiomelanocortin processing in the hypothalamus: impact on melanocortin signalling and obesity
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“Anatomical evidence for this is supplied by the observation that AGRP and POMC neurons project to identical brain areas (Bagnol et al. 1999).”
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“that project to identical areas of the brain (Bagnol et al., 1999), the brainstem has few, if any, AgRP-immunoreactive cell bodies and receives limited terminals from the ARC.”
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“The impetus for focusing on the PVH included the following: (i) MC4R expression is dense in the PVH (10–12), (ii) it receives strong input from AgRP and POMC neurons (13, 14), (iii) injection of MC3/4R ligands into the PVH affects feeding (14–16), (iv) PVH-directed lesions cause obesity (17, 18), and most importantly,…”
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Fenselau, H., Campbell, J. N., Verstegen, A. M. J., Madara, J. C., Xu, J., Shah, B. P., Resch, J. M., Yang, Z., Mandelblat-Cerf, Y., Livneh, Y., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4442 · Cited by 233
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“In fact, both ARC neurons and their projection targets in the PVN express MC4 receptors (Bagnol et al., 1999; Kishi et al., 2003) and are activated shortly after MBH leucine administration, as evidenced by c-Fos expression and Erk1/2 phosphorylation.”
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“The redundant wiring and differential regulation of Pomc and MC4R neurons provide another safeguarding mechanism to ensure sufficient inhibition of anorexigenic drive.”
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“are generally believed to originate exclusively from NPY containing neurons in the ARH (24, 25).”
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“ARC neurons are the only neurons producing agoutirelated peptide (AgRP) in mice brain (Bangol et al. 1999) thus providing an excellent deterministic clue of the ARC.”
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“Such a mechanism has been recently postulated for the melanocortin-3 receptor effect on the melanocortin feeding system (23).”
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60 YEARS OF POMC: Regulation of feeding and energy homeostasis by α-MSH
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“nucleus/area (Bagnol et al. 1999).”
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“AgRP is a peptide synthesized in the arcuate nucleus and projects to other key feeding hypothalamic nuclei and sites throughout the brain (2, 19, 26).”
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“Anatomical studies demonstrate that -MSH and AgRP neurons innervate a variety of brain regions that have been well characterized in stress reactions (4).”
BackgroundMethodInfluentialSelf-citationRole of FoxO transcription factors in aging and age-related metabolic and neurodegenerative diseases
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Autoantibodies against α-MSH, ACTH, and LHRH in anorexia and bulimia nervosa patients
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“The role of melanocortins in body weight regulation: opportunities for the treatment of obesity”
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CART in the regulation of appetite and energy homeostasis
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“POMC/CART neurons express the melanocortin 3-receptor (MC3-R) which is specific for melanocortin peptides derived from the posttranslational cleavage of POMC (Bagnol et al., 1999), such as the anorectic α-MSH (Fan et al., 1997; Huszar, 1997; Kim et al., 2000; Zheng et al., 2005).”
BackgroundResultInfluentialZheng, H., Corkern, M., Stoyanova, I., Patterson, L. M., Tian, R., & Berthoud, H.-R. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00781.2002 · Cited by 135
“hypothalamic and many extrahypothalamic areas (1,33,34), Both α-MSH and CART-peptide have been”
BackgroundInfluentialRole of central melanocortin pathways in energy homeostasis
Garfield, A. S., Lam, D. D., Marston, O. J., Przydzial, M. J., & Heisler, L. K. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.02.002 · Cited by 139
Differential Role of Melanocortin Receptor Subtypes in Cachexia
Marks, D. L., Butler, A. A., Turner, R. J., Brookhart, G., & Cone, R. D. (2003) · Endocrinology · doi:10.1210/en.2002-221099 · Cited by 134
Neural melanocortin receptors in obesity and related metabolic disorders
Girardet, C., & Butler, A. A. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.05.004 · Cited by 128
“The largest population is located in the hypothalamus, and more specifically in the lateral part of the ARC.”
InfluentialInvestigation of the melanocyte stimulating hormones on food intake
Abbott, C. R., Rossi, M., Kim, M.-S., AlAhmed, S. H., Taylor, G. M., Ghatei, M. A., Smith, D. M., & Bloom, S. R. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02386-6 · Cited by 127
The Melanocortin-3 Receptor Is Required for Entrainment to Meal Intake
Sutton, G. M., Pérez–Tilve, D., Nogueiras, R., Fang, J., Kim, J. K., Cone, R. D., Gimble, J. M., Tschöp, M. H., & Butler, A. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3615-08.2008 · Cited by 132
“Pomc and AgRP neurons innervate hypothalamic areas involved in entrainment of anticipatory behaviors to feeding (Bagnol et al., 1999; Haskell-Luevano et al., 1999; Singru et al., 2007).”
BackgroundKishi, T., Aschkenasi, C. J., Choi, B. J., Lopez, M. E., Lee, C. E., Liu, H., Hollenberg, A. N., Friedman, J. M., & Elmquist, J. K. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20432 · Cited by 119
“The PVH receives dense -MSH and AgRP inputs from the Arc in the rat (Jacobowitz and O’donohue, 1978; Bagnol et al., 1999; Haskell-Luevano et al., 1999) and mouse (Broberger et al., 1998b).”
BackgroundInputs to the ventrolateral bed nucleus of the stria terminalis
Shin, J., Geerling, J. C., & Loewy, A. D. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21870 · Cited by 115
“…AgRP immunoreactivity was also found in neuronal somata only within the medial subregion of the arcuate hypothalamic nucleus, again consistent with previous in situ hybridization and immunohistochemical findings (Broberger et al., 1998; Elias et al., 1998b; Hahn et al., 1998; Bagnol et al., 1999).”
ResultThe regulation of food intake by selective stimulation of the type 3 melanocortin receptor (MC3R)
Marks, D. L., Hruby, V. J., Brookhart, G., & Cone, R. D. (2005) · Peptides · doi:10.1016/j.peptides.2005.01.025 · Cited by 116
“Several lines of evidence suggest that γ-MSH acts on the MC3R within the hypothalamic arcuate nucleus to dampen the activity of arcuate POMC neurons via direct and indirect neural mechanisms [1,10,29,31].”
BackgroundInvolvement of melanocortin-4 receptor in anxiety and depression
Chaki, S., & Okuyama, S. (2005) · Peptides · doi:10.1016/j.peptides.2004.11.029 · Cited by 114
Wirth, M. M., Olszewski, P. K., Yu, C., Levine, A. S., & Giraudo, S. Q. (2001) · Peptides · doi:10.1016/s0196-9781(00)00367-3 · Cited by 115
Distribution and Function of Melanocortin Receptors within the Brain
Mountjoy, K. G. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-6354-3_3 · Cited by 113
Creemers, J. W. M., Pritchard, L. E., Gyte, A., Rouzic, P. L., Meulemans, S. M. P., Wardlaw, S. L., Zhu, X., Steiner, D. F., Davies, N., Armstrong, D., et al. (2005) · Endocrinology · doi:10.1210/en.2005-1373 · Cited by 112
Functions for pro-opiomelanocortin-derived peptides in obesity and diabetes
Mountjoy, K. G. (2010) · Biochemical Journal · doi:10.1042/bj20091957 · Cited by 110
Cognitive and autonomic determinants of energy homeostasis in obesity
Richard, D. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.103 · Cited by 113
Cerdá‐Reverter, J. M., Agulleiro, M. J., Guillot, R., Sánchez, E., Ceinos, R. M., & Rotllant, J. (2011) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2010.10.108 · Cited by 105
“In rodents, two discrete groups of neurons in the hypothalamus (arcuate nucleus) and the medulla (nucleus of the tractus solitarius) also produce POMC (Bangol et al., 1999).”
BackgroundSleep Deprivation and Central Appetite Regulation
Liu, S., Wang, X., Zheng, Q., Gao, L., & Sun, Q. (2022) · Nutrients · doi:10.3390/nu14245196 · Cited by 117
“This loop is composed of appetite-suppressing POMC neurons in the hypothalamic arcuate nucleus, appetite-promoting AgRP neurons, melanocortin receptor-4 (MC4R)-positive neurons in the paraventricular nucleus, and the neural projections between them [46].”
BackgroundWilliams, D. L., Bowers, R. R., Bartness, T. J., Kaplan, J. M., & Grill, H. J. (2003) · Endocrinology · doi:10.1210/en.2003-0440 · Cited by 102
Melanocortin‐3 Receptor mRNA Expression in Pro‐Opiomelanocortin Neurones of the Rat Arcuate Nucleus
Jégou, S., Boutelet, I., & Vaudry, H. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00477.x · Cited by 101
Wang, C., Bomberg, E. M., Levine, A. S., Billington, C. J., & Kotz, C. M. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00125.2007 · Cited by 99
“6, A and B), indicating that BDNF in the VMH reduces feeding and body weight gain via its receptor TrkB. ARC NPY neurons project to other areas of the hypothalamus, including the PVN and VMH. NPY has been reported to increase feeding not only after administration into the PVN but also after VMH injection (5, 9, 24, 31…”
BackgroundPathophysiology and treatment of inflammatory anorexia in chronic disease
Braun, T. P., & Marks, D. L. (2010) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1007/s13539-010-0015-1 · Cited by 108
“Importantly, α-MSH and AgRP immunoreactive fibers project to many of the same locations across the CNS, although AgRP projections are less dense [81–83].”
BackgroundBrain effects of melanocortins☆
BERTOLINI, A., Tacchi, R., & Vergoni, A. V. (2008) · Pharmacological Research · doi:10.1016/j.phrs.2008.10.005 · Cited by 100
Watts, A. G. (2000) · Hormones and Behavior · doi:10.1006/hbeh.2000.1581 · Cited by 98
Fekete, C., Singru, P. S., Sanchez, E., Sarkar, S., Christoffolete, M. A., Riberio, R. S., Rand, W. M., Emerson, C. H., Bianco, A. C., & Lechan, R. M. (2006) · Endocrinology · doi:10.1210/en.2005-0956 · Cited by 97
Adan, R. A. H., & Kas, M. J. (2003) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(03)00130-5 · Cited by 97
Chisada, S., Kurokawa, T., Murashita, K., Rønnestad, I., Taniguchi, Y., Toyoda, A., Sakaki, Y., Takeda, S., & Yoshiura, Y. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.10.008 · Cited by 95
Fang, X., Jiang, S., Wang, J., Bai, Y., Kim, C. S., Blake, D., Weintraub, N. L., Lei, Y., & Lu, X.-Y. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-01004-x · Cited by 95
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Central and peripheral control of food intake
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The Central Nervous System Sites Mediating the Orexigenic Actions of Ghrelin
Mason, B. L., Wang, Q., & Zigman, J. M. (2013) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021113-170310 · Cited by 89
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Hypothalamic Melanocortin System Regulates Sympathetic Nerve Activity in Brown Adipose Tissue
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Responsiveness to Peripherally Administered Melanocortins in Lean and Obese Mice
Blüher, S., Ziotopoulou, M., Bullen, J. W., Moschos, S. J., Ungsunan, L., Kokkotou, E. G., Maratos–Flier, E., & Mantzoros, C. S. (2004) · Diabetes · doi:10.2337/diabetes.53.1.82 · Cited by 89
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“Hypothalamic POMC neurons project to a wide variety of brain regions (Bagnol et al., 1999; Haskell-Luevano et al., 1999), and it has been suggested that subpopulations of POMC neurons innervate distinct target sites (King and Hentges, 2011).”
Background
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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