Pharmacological modulation of dual melanocortin-4 receptor signaling by melanocortin receptor accessory proteins in the Xenopus laevis.


Journal

Journal of cellular physiology
ISSN: 1097-4652
Titre abrégé: J Cell Physiol
Pays: United States
ID NLM: 0050222

Informations de publication

Date de publication:
08 2021
Historique:
revised: 29 12 2020
received: 06 10 2020
accepted: 04 01 2021
pubmed: 28 1 2021
medline: 21 10 2021
entrez: 27 1 2021
Statut: ppublish

Résumé

Physiological modulation of melanocortin-4 receptor (MC4R) signaling by MRAP2 proteins plays an indispensable role in appetite control and energy homeostasis in the central nervous system. Great interspecies differences of the interaction and regulation of melanocortin receptors by MRAP protein family have been reported in several diploid vertebrates but never been investigated in the tetrapod amphibian Xenopus laevis. Here, we performed phylogenetic and synteny-based analyses to explore the evolutionary aspects of dual copies of X. laevis MC4R (xlMC4R) and MRAP2 (xlMRAP2) proteins. Our data showed that xlMRAPs directly interacted with xlMC4Rs on the cell surface as a functional antiparallel dimeric topology and pharmacological studies suggested a homology specific regulatory pattern of the melanocortin system in X. laevis.

Identifiants

pubmed: 33501674
doi: 10.1002/jcp.30280
doi:

Substances chimiques

Adaptor Proteins, Signal Transducing 0
Carrier Proteins 0
Melanocortins 0
Receptor, Melanocortin, Type 4 0
Receptors, Melanocortin 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5980-5993

Informations de copyright

© 2021 Wiley Periodicals LLC.

Références

Asai, M., Ramachandrappa, S., Joachim, M., Shen, Y., Zhang, R., Nuthalapati, N., Ramanathan, V., Strochlic, D. E., Ferket, P., Linhart, K., Ho, C., Novoselova, T. V., Garg, S., Ridderstrale, M., Marcus, C., Hirschhorn, J. N., Keogh, J. M., O'Rahilly, S., Chan, L. F., … Majzoub, J. A. (2013). Loss of function of the melanocortin 2 receptor accessory protein 2 is associated with mammalian obesity. Science, 341, 275-278.
Bednarek, M. A., MacNeil, T., Tang, R., Fong, T. M., Angeles Cabello, M., Maroto, M., & Teran, A. (2008). Analogs of α-melanocyte stimulating hormone with high agonist potency and selectivity at human melanocortin receptor 1b: The role of Trp9 in molecular recognition. Biopolymers, 89, 401-408.
Chaly, A. L., Srisai, D., Gardner, E. E., & Sebag, J. A. (2016). The melanocortin receptor accessory proTEIn 2 promotes food intake through inhibition of the prokineticin receptor-1. eLife, 5:e12397.
Chan, L. F., Webb, T. R., Chung, T.-T., Meimaridou, E., Cooray, S. N., Guasti, L., Chapple, J. P., Egertova, M., Elphick, M. R., Cheetham, M. E., Metherell, L. A., & Clark, A. J. L. (2009). MRAP and MRAP2 are bidirectional regulators of the melanocortin receptor family. Proceedings of the National Academy of Sciences, 106, 6146-6151.
Coll, A. P., Farooqi, I. S., Challis, B. G., Yeo, G. S. H., & O′Rahilly, S. (2004). Proopiomelanocortin and energy balance: Insights from human and murine genetics. The Journal of Clinical Endocrinology & Metabolism, 89, 2557-2562.
Cone, R. D. (2005). Anatomy and regulation of the central melanocortin system. Nature Neuroscience, 8, 571-578.
Flier, J. S. (2004). Obesity wars: Molecular progress confronts an expanding epidemic. Cell, 116, 337-350.
Gantz, I., Miwa, H., Konda, Y., Shimoto, Y., Tashiro, T., Watson, S. J., DelValle, J., & Yamada, T. (1993). Molecular cloning, expression, and gene localization of a fourth melanocortin receptor. Journal of Biological Chemistry, 268, 15174-15179.
Huszar, D., Lynch, C. A., Fairchild-Huntress, V., Dunmore, J. H., Fang, Q., Berkemeier, L. R., Gu, W., Kesterson, R. A., Boston, B. A., Cone, R. D., Smith, F. J., Campfield, L. A., Burn, P., & Lee, F. (1997). Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell, 88, 131-141.
Jiannan, Z., Xin, L., Yawei, Z., Lin, C., Jing, L., Chenlei, W., Yiping, W., Juan, L., & Yajun, W. (2017). The interaction of MC3R and MC4R with MRAP2, ACTH, α-MSH and AgRP in chickens. Journal of Endocrinology, 234, 155-174.
Larsen, L. H., Echwald, S. M., Sørensen, T. I. A., Andersen, T., Wulff, B. S., & Pedersen, O. (2005). Prevalence of mutations and functional analyses of melanocortin 4 receptor variants identified among 750 men with juvenile-onset obesity. The Journal of Clinical Endocrinology & Metabolism, 90, 219-224.
Liang, J., Li, L., Jin, X., Xu, B., Pi, L., Liu, S., Zhu, W., Zhang, C., Luan, B., Gong, L., & Zhang, C. (2018). Pharmacological effect of human melanocortin-2 receptor accessory protein 2 variants on hypothalamic melanocortin receptors. Endocrine, 61, 94-104.
Metherell, L. A., Chan, L. F., & Clark, A. J. L. (2006). The genetics of ACTH resistance syndromes. Best Practice & Research Clinical Endocrinology & Metabolism, 20, 547-560.
Metherell, L. A., Chapple, J. P., Cooray, S., David, A., Becker, C., Rüschendorf, F., Naville, D., Begeot, M., Khoo, B., Nürnberg, P., Huebner, A., Cheetham, M. E., & Clark, A. J. L. (2005). Mutations in MRAP, encoding a new interacting partner of the ACTH receptor, cause familial glucocorticoid deficiency type 2. Nature Genetics, 37, 166-170.
Mosialou, I., Shikhel, S., Liu, J.-M., Maurizi, A., Luo, N., He, Z., Huang, Y., Zong, H., Friedman, R. A., Barasch, J., Lanzano, P., Deng, L., Leibel, R. L., Rubin, M., Nickolas, T., Chung, W., Zeltser, L. M., Williams, K. W., Pessin, J. E., & Kousteni, S. (2017). MC4R-dependent suppression of appetite by bone-derived lipocalin 2. Nature, 543, 385-390.
Novoselova, T. V., Hussain, M., King, P. J., Guasti, L., Metherell, L. A., Charalambous, M., Clark, A. J. L., & Chan, L. F. (2018). MRAP deficiency impairs adrenal progenitor cell differentiation and gland zonation. The FASEB Journal, 32, 6186-6196.
Ollmann, M. M., Wilson, B. D., Yang, Y.-K., Kerns, J. A., Chen, Y., Gantz, I., & Barsh, G. S. (1997). Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related. Protein Science, 278, 135.
Sebag, J. A., & Hinkle, P. M. (2007). Melanocortin-2 receptor accessory protein MRAP forms antiparallel homodimers. Proceedings of the National Academy of Sciences, 104, 20244-20249.
Sebag, J. A., & Hinkle, P. M. (2009). Regions of melanocortin 2 (MC2) receptor accessory protein necessary for dual topology and MC2 receptor trafficking and signaling. Journal of Biological Chemistry, 284, 610-618.
Sebag, J. A., & Hinkle, P. M. (2010). Regulation of G protein-coupled receptor signaling: Specific dominant-negative effects of melanocortin 2 receptor accessory protein 2. Science Signaling, 3, ra28.
Sebag, J. A., Zhang, C., Hinkle, P. M., Bradshaw, A. M., & Cone, R. D. (2013). Developmental control of the melanocortin-4 receptor by MRAP2 proteins in zebrafish. Science, 341, 278-281.
Shutter, J. R., Graham, M., Kinsey, A. C., Scully, S., Lüthy, R., & Stark, K. L. (1997). Hypothalamic expression of ART, a novel gene related to agouti, is up-regulated in obese and diabetic mutant mice. Genes & Development, 11, 593-602.
Wang, M., Chen, Y., Zhu, M., Xu, B., Guo, W., Lyu, Y., & Zhang, C. (2019). Pharmacological modulation of melanocortin-4 receptor by melanocortin receptor accessory protein 2 in Nile tilapia. General and Comparative Endocrinology, 282, 113219.
Xu, A., Choi, K.-L., Wang, Y., Permana, P. A., Yi Xu, L., Bogardus, C., & Cooper, G. J. S. (2002). Identification of novel putative membrane proteins selectively expressed during adipose conversion of 3T3-L1 cells. Biochemical and Biophysical Research Communications, 293, 1161-1167.
Zhang, J., Li, J., Wu, C., Hu, Z., An, L., Wan, Y., Fang, C., Zhang, X., Li, J., & Wang, Y. (2020). The Asp298Asn polymorphism of melanocortin-4 receptor (MC4R) in pigs: Evidence for its potential effects on MC4R constitutive activity and cell surface expression. Animal Genetics, 51, 694-706.
Zhang, M., Chen, Y., Xu, H., Yang, L., Yuan, F., Li, L., Xu, Y., Chen, Y., Zhang, C., & Lin, G. (2018). Melanocortin receptor 4 signaling regulates vertebrate limb regeneration. Developmental Cell, 46, 397-409.e395
Zhu, M., Xu, B., Wang, M., Liu, S., Zhang, Y., & Zhang, C. (2019). Pharmacological modulation of MRAP2 protein on melanocortin receptors in the sea lamprey. Endocrine Connections, 8, 378-388.

Auteurs

Lei Li (L)

Translational Medical Center for Stem Cell Therapy and Institute for Regenerative Medicine, Shanghai East Hospital, Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University, Shanghai, China.

Ying Xu (Y)

Translational Medical Center for Stem Cell Therapy and Institute for Regenerative Medicine, Shanghai East Hospital, Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University, Shanghai, China.

Jihong Zheng (J)

Translational Medical Center for Stem Cell Therapy and Institute for Regenerative Medicine, Shanghai East Hospital, Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University, Shanghai, China.

Zhe Kuang (Z)

Translational Medical Center for Stem Cell Therapy and Institute for Regenerative Medicine, Shanghai East Hospital, Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University, Shanghai, China.

Cong Zhang (C)

Translational Medical Center for Stem Cell Therapy and Institute for Regenerative Medicine, Shanghai East Hospital, Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University, Shanghai, China.

Na Li (N)

Yantai Derui Bio-Tech Co., Ltd., Yantai, Shandong, China.

Gufa Lin (G)

Key Laboratory of Spine and Spinal Cord Injury Repair and Regeneration of Ministry of Education, Orthopaedic Department of Tongji Hospital, School of Life Sciences and Technology, Tongji University, Shanghai, China.

Chao Zhang (C)

Translational Medical Center for Stem Cell Therapy and Institute for Regenerative Medicine, Shanghai East Hospital, Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University, Shanghai, China.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH