Biased agonism as a novel strategy to harness the proresolving properties of melanocortin receptors without eliciting melanogenic effects

Journal of Immunology

Volumn 194, Issue 7, 2015, Pages 3381-3388

  Montero Melendez, Trinidad ^a   Gobbetti, Thomas ^a   Cooray, Sadani N ^a   Jonassen, Thomas E N ^b   Perretti, Mauro ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; MELANOCORTIN 1 RECEPTOR; MELANOCORTIN 3 RECEPTOR; MELANOCORTIN RECEPTOR; MELANOCORTIN RECEPTOR AGONIST; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; UNCLASSIFIED DRUG; [3 [1 (2 NITROPHENYL) 1H PYRROL 2 YL]ALLYLIDENAMINO]GUANIDINIUM ACETATE; ANTIINFLAMMATORY AGENT; CALCIUM; GUANIDINE DERIVATIVE; MELANIN; N-(3-(1-(2-NITROPHENYL)-1H-PYRROL-2-YL)ALLYLIDENAMINO)GUANIDINE; PYRROLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTHRITIS; ARTICLE; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG SAFETY; ENZYME PHOSPHORYLATION; HEK293 CELL LINE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; MACROPHAGE; MALE; MELANOCYTE; MELANOGENESIS; MOUSE; NONHUMAN; NORMAL HUMAN; PERITONITIS; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; AGONISTS; ANIMAL; ARTHRITIS, EXPERIMENTAL; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; EXPERIMENTAL MELANOMA; GENE INACTIVATION; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLISM; NEUTROPHIL; PATHOLOGY; PERITONEUM MACROPHAGE; PHAGOCYTOSIS;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ARTHRITIS, EXPERIMENTAL; CALCIUM; DISEASE MODELS, ANIMAL; GENE KNOCKOUT TECHNIQUES; GUANIDINES; HEK293 CELLS; HUMANS; INFLAMMATION; MACROPHAGES, PERITONEAL; MALE; MELANINS; MELANOMA, EXPERIMENTAL; MICE; NEUTROPHILS; PERITONITIS; PHAGOCYTOSIS; PYRROLES; RECEPTOR, MELANOCORTIN, TYPE 1; RECEPTOR, MELANOCORTIN, TYPE 3; RECEPTORS, MELANOCORTIN; SIGNAL TRANSDUCTION;

EID: 84925858431     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402645     Document Type: Article

References (46)

1. Cone, R. D. 2006. Studies on the physiological functions of the melanocortin system. Endocr. Rev. 27: 736-749.
2. Böhm, M., and S. Grässel. 2012. Role of proopiomelanocortin-derived peptides and their receptors in the osteoarticular system: from basic to translational research. Endocr. Rev. 33: 623-651.
3. Catania, A. 2008. Neuroprotective actions of melanocortins: a therapeutic opportunity. Trends Neurosci. 31: 353-360.
4. Getting, S. J. 2006. Targeting melanocortin receptors as potential novel therapeutics. Pharmacol. Ther. 111: 1-15.
5. Catania, A., V. Gerloni, S. Procaccia, L. Airaghi, M. G. Manfredi, C. Lomater, L. Grossi, and J. M. Lipton. 1994. The anticytokine neuropeptide alpha-melanocyte-stimulating hormone in synovial fluid of patients with rheumatic diseases: comparisons with other anticytokine molecules. Neuroimmunomodulation 1: 321-328.
6. Rajora, N., G. Ceriani, A. Catania, R. A. Star, M. T. Murphy, and J. M. Lipton. 1996. alpha-MSH production, receptors, and influence on neopterin in a human monocyte/macrophage cell line. J. Leukoc. Biol. 59: 248-253.
7. Buckley, C. D., D. W. Gilroy, C. N. Serhan, B. Stockinger, and P. P. Tak. 2013. The resolution of inflammation. Nat. Rev. Immunol. 13: 59-66.
8. Wallace, J. L. 2014. Exploiting endogenous anti-inflammatory pathways as a therapeutic approach to multiorgan inflammatory disease. Am. J. Pathol. 184: 2154-2155.
9. Hench, P. S., E. C. Kendall, C. H. Slocumb, and H. F. Polley. 1950. Effects of cortisone acetate and pituitary ACTH on rheumatoid arthritis, rheumatic fever and certain other conditions. Arch. Intern. Med. (Chic). 85: 545-666.
10. Getting, S. J., H. C. Christian, R. J. Flower, and M. Perretti. 2002. Activation of melanocortin type 3 receptor as a molecular mechanism for adrenocorticotropic hormone efficacy in gouty arthritis. Arthritis Rheum. 46: 2765-2775.
11. Montero-Melendez, T., H. B. Patel, and M. Perretti. 2011. Role of melanocortin receptors in the regulation of gouty inflammation. Curr. Rheumatol. Rep. 13: 138-145.
12. Mapa, J. B., and M. H. Pillinger. 2010. New treatments for gout. Curr. Opin. Investig. Drugs 11: 499-506.
13. Wootten, D., A. Christopoulos, and P. M. Sexton. 2013. Emerging paradigms in GPCR allostery: implications for drug discovery. Nat. Rev. Drug Discov. 12: 630-644.
14. Pantel, J., S. Y. Williams, D. Mi, J. Sebag, J. D. Corbin, C. D. Weaver, and R. D. Cone. 2011. Development of a high throughput screen for allosteric modulators of melanocortin-4 receptor signaling using a real time cAMP assay. Eur. J. Pharmacol. 660: 139-147.
15. Kenakin, T., and A. Christopoulos. 2013. Signalling bias in new drug discovery: detection, quantification and therapeutic impact. Nat. Rev. Drug Discov. 12: 205-216.
16. Reiter, E., S. Ahn, A. K. Shukla, and R. J. Lefkowitz. 2012. Molecular mechanism of β-arrestin-biased agonism at seven-transmembrane receptors. Annu. Rev. Pharmacol. Toxicol. 52: 179-197.
17. Mastrofrancesco, A., A. Kokot, A. Eberle, N. C. Gibbons, K. U. Schallreuter, E. Strozyk, M. Picardo, C. C. Zouboulis, T. A. Luger, and M. Böhm. 2010. KdPT, a tripeptide derivative of alpha-melanocyte-stimulating hormone, suppresses IL-1 beta-mediated cytokine expression and signaling in human sebocytes. J. Immunol. 185: 1903-1911.
18. Montero-Melendez, T., H. B. Patel, M. Seed, S. Nielsen, T. E. Jonassen, and M. Perretti. 2011. The melanocortin agonist AP214 exerts anti-inflammatory and proresolving properties. Am. J. Pathol. 179: 259-269.
19. Ortega-Gómez, A., M. Perretti, and O. Soehnlein. 2013. Resolution of inflammation: an integrated view. EMBO Mol. Med. 5: 661-674.
20. Bannenberg, G. L., N. Chiang, A. Ariel, M. Arita, E. Tjonahen, K. H. Gotlinger, S. Hong, and C. N. Serhan. 2005. Molecular circuits of resolution: formation and actions of resolvins and protectins. J. Immunol. 174: 4345-4355.
21. Patel, H. B., M. Bombardieri, A. L. Sampaio, F. D'Acquisto, M. Gray, P. Grieco, S. J. Getting, C. Pitzalis, and M. Perretti. 2010. Anti-inflammatory and anti-osteoclastogenesis properties of endogenous melanocortin receptor type 3 in experimental arthritis. FASEB J. 24: 4835-4843.
22. Daoussis, D., I. Antonopoulos, and A. P. Andonopoulos. 2014. ACTH as a treatment for acute crystal-induced arthritis: update on clinical evidence and mechanisms of action. Semin. Arthritis Rheum. 43: 648-653.
23. Schlesinger, N. 2008. Overview of the management of acute gout and the role of adrenocorticotropic hormone. Drugs 68: 407-415.
24. Groer, C. E., K. Tidgewell, R. A. Moyer, W. W. Harding, R. B. Rothman, T. E. Prisinzano, and L. M. Bohn. 2007. An opioid agonist that does not induce mu-opioid receptor - arrestin interactions or receptor internalization. Mol. Pharmacol. 71: 549-557.
25. Getting, S. J., C. W. Lam, A. S. Chen, P. Grieco, and M. Perretti. 2006. Melanocortin 3 receptors control crystal-induced inflammation. FASEB J. 20: 2234-2241.
26. Hench, P. S. 1950. Introduction: cortisone and ACTH in clinical medicine. Proc. Staff Meet. Mayo Clin. 25: 474-476.
27. Gong, R. 2012. The renaissance of corticotropin therapy in proteinuric nephropathies. Nat. Rev. Nephrol. 8: 122-128.
28. Berkovich, R., and M. A. Agius. 2014. Mechanisms of action of ACTH in the management of relapsing forms of multiple sclerosis. Ther. Adv. Neurol. Disord. 7: 83-96.
29. Leoni, G., M. B. Voisin, K. Carlson, S. Getting, S. Nourshargh, and M. Perretti. 2010. The melanocortin MC(1) receptor agonist BMS-470539 inhibits leucocyte trafficking in the inflamed vasculature. Br. J. Pharmacol. 160: 171-180.
30. Kang, L., K. W. McIntyre, K. M. Gillooly, Y. Yang, J. Haycock, S. Roberts, A. Khanna, T. F. Herpin, G. Yu, X. Wu, et al. 2006. A selective small molecule agonist of the melanocortin-1 receptor inhibits lipopolysaccharide-induced cytokine accumulation and leukocyte infiltration in mice. J. Leukoc. Biol. 80: 897-904.
31. Montero-Melendez, T., M. F. Madeira, L. V. Norling, A. Alsam, M. A. Curtis, T. A. da Silva, and M. Perretti. 2014. Association between periodontal disease and inflammatory arthritis reveals modulatory functions by melanocortin receptor type 3. Am. J. Pathol. 184: 2333-2341.
32. García-Borrón, J. C., B. L. Sánchez-Laorden, and C. Jiménez-Cervantes. 2005. Melanocortin-1 receptor structure and functional regulation. Pigment Cell Res. 18: 393-410.
33. Buscà, R., and R. Ballotti. 2000. Cyclic AMP a key messenger in the regulation of skin pigmentation. Pigment Cell Res. 13: 60-69.
34. Sutton, G. M., B. Duos, L. M. Patterson, and H. R. Berthoud. 2005. Melanocortinergic modulation of cholecystokinin-induced suppression of feeding through extracellular signal-regulated kinase signaling in rat solitary nucleus. Endocrinology 146: 3739-3747.
35. Sarkar, A., Y. Sreenivasan, and S. K. Manna. 2003. alpha-Melanocyte-stimulating hormone induces cell death in mast cells: involvement of NF-kappaB. FEBS Lett. 549: 87-93.
36. Ottani, A., M. Galantucci, E. Ardimento, L. Neri, F. Canalini, A. Calevro, D. Zaffe, E. Novellino, P. Grieco, D. Giuliani, and S. Guarini. 2013. Modulation of the JAK/ERK/STAT signaling in melanocortin-induced inhibition of local and systemic responses to myocardial ischemia/reperfusion. Pharmacol. Res. 72: 1-8.
37. Doyle, J. R., J. P. Fortin, M. Beinborn, and A. S. Kopin. 2012. Selected melanocortin 1 receptor single-nucleotide polymorphisms differentially alter multiple signaling pathways. J. Pharmacol. Exp. Ther. 342: 318-326.
38. Denat, L., A. L. Kadekaro, L. Marrot, S. A. Leachman, and Z. A. Abdel-Malek. 2014. Melanocytes as instigators and victims of oxidative stress. J. Invest. Dermatol. 134: 1512-1518.
39. Perretti, M. 1997. Endogenous mediators that inhibit the leukocyte-endothelium interaction. Trends Pharmacol. Sci. 18: 418-425.
40. Serhan, C. N., S. D. Brain, C. D. Buckley, D. W. Gilroy, C. Haslett, L. A. O'Neill, M. Perretti, A. G. Rossi, and J. L. Wallace. 2007. Resolution of inflammation: state of the art, definitions and terms. FASEB J. 21: 325-332.
41. Ditzel, H. J. 2004. The K/BxN mouse: a model of human inflammatory arthritis. Trends Mol. Med. 10: 40-45.
42. Herraiz, C., C. Jiménez-Cervantes, P. Zanna, and J. C. García-Borrón. 2009. Melanocortin 1 receptor mutations impact differentially on signalling to the cAMP and the ERK mitogen-activated protein kinase pathways. FEBS Lett. 583: 3269-3274.
43. Haslach, E. M., H. Huang, M. Dirain, G. Debevec, P. Geer, R. G. Santos, M. A. Giulianotti, C. Pinilla, J. R. Appel, S. R. Doering, et al. 2014. Identification of tetrapeptides from a mixture based positional scanning library that can restore nM full agonist function of the L106P, I69T, I102S, A219V, C271Y, and C271R human melanocortin-4 polymorphic receptors (hMC4Rs). J. Med. Chem. 57: 4615-4628.
44. Büch, T. R., D. Heling, E. Damm, T. Gudermann, and A. Breit. 2009. Pertussis toxin-sensitive signaling of melanocortin-4 receptors in hypothalamic GT1-7 cells defines agouti-related protein as a biased agonist. J. Biol. Chem. 284: 26411-26420.
45. Breit, A., K. Wolff, H. Kalwa, H. Jarry, T. Büch, and T. Gudermann. 2006. The natural inverse agonist agouti-related protein induces arrestin-mediated endocytosis of melanocortin-3 and -4 receptors. J. Biol. Chem. 281: 37447-37456.
46. Mo, X. L., and Y. X. Tao. 2013. Activation of MAPK by inverse agonists in six naturally occurring constitutively active mutant human melanocortin-4 receptors. Biochim. Biophys. Acta 1832: 1939-1948.