MC4R Variants Modulate α-MSH and Setmelanotide Induced Cellular Signaling at Multiple Levels

J Clin Endocrinol Metab. 2024 Sep 16;109(10):2452-2466. doi: 10.1210/clinem/dgae210.

Abstract

Context: The melanocortin-4 receptor (MC4R) plays an important role in body weight regulation. Pathogenic MC4R variants are the most common cause of monogenic obesity.

Objective: We have identified 17 MC4R variants in adult and pediatric patients with obesity. Here we aimed to functionally characterize these variants by analyzing 4 different aspects of MC4R signaling. In addition, we aimed to analyze the effect of setmelanotide, a potent MC4R agonist, on these MC4R variants.

Materials and methods: Cell surface expression and α-melanocyte stimulating hormone (α-MSH)- or setmelanotide-induced cAMP response, β-arrestin-2 recruitment, and ERK activation were measured in cells expressing either wild type or variant MC4R.

Results: We found a large heterogeneity in the function of these variants. We identified variants with a loss of response for all studied MC4R signaling, variants with no cAMP accumulation or ERK activation but normal β-arrestin-2 recruitment, and variants with normal cAMP accumulation and ERK activation but decreased β-arrestin-2 recruitment, indicating disrupted desensitization and signaling mechanisms. Setmelanotide displayed a greater potency and similar efficacy as α-MSH and induced significantly increased maximal cAMP responses of several variants compared to α-MSH. Despite the heterogeneity in functional response, there was no apparent difference in the obesity phenotype in our patients.

Conclusion: We show that these obesity-associated MC4R variants affect MC4R signaling differently yet lead to a comparable clinical phenotype. Our results demonstrate the clinical importance of assessing the effect of MC4R variants on a range of molecular signaling mechanisms to determine their association with obesity, which may aid in improving personalized treatment.

Keywords: G-protein-coupled receptors; genetic variation; melanocortin-4 receptor; obesity; setmelanotide; α-MSH; β-arrestins.

MeSH terms

  • Adult
  • Child
  • Cyclic AMP* / metabolism
  • HEK293 Cells
  • Humans
  • Obesity / genetics
  • Obesity / metabolism
  • Receptor, Melanocortin, Type 4* / agonists
  • Receptor, Melanocortin, Type 4* / genetics
  • Receptor, Melanocortin, Type 4* / metabolism
  • Signal Transduction* / drug effects
  • alpha-MSH* / analogs & derivatives
  • alpha-MSH* / pharmacology

Substances

  • Receptor, Melanocortin, Type 4
  • alpha-MSH
  • MC4R protein, human
  • setmelanotide
  • Cyclic AMP