Development and characterization of high affinity leptins and leptin antagonists

J Biol Chem. 2011 Feb 11;286(6):4429-42. doi: 10.1074/jbc.M110.196402. Epub 2010 Nov 30.

Abstract

Leptin is a pleiotropic hormone acting both centrally and peripherally. It participates in a variety of biological processes, including energy metabolism, reproduction, and modulation of the immune response. So far, structural elements affecting leptin binding to its receptor remain unknown. We employed random mutagenesis of leptin, followed by selection of high affinity mutants by yeast surface display and discovered that replacing residue Asp-23 with a non-negatively charged amino acid leads to dramatically enhanced affinity of leptin for its soluble receptor. Rational mutagenesis of Asp-23 revealed the D23L substitution to be most effective. Coupling the Asp-23 mutation with alanine mutagenesis of three amino acids (L39A/D40A/F41A) previously reported to convert leptin into antagonist resulted in potent antagonistic activity. These novel superactive mouse and human leptin antagonists (D23L/L39A/D40A/F41A), termed SMLA and SHLA, respectively, exhibited over 60-fold increased binding to leptin receptor and 14-fold higher antagonistic activity in vitro relative to the L39A/D40A/F41A mutants. To prolong and enhance in vivo activity, SMLA and SHLA were monopegylated mainly at the N terminus. Administration of the pegylated SMLA to mice resulted in a remarkably rapid, significant, and reversible 27-fold more potent increase in body weight (as compared with pegylated mouse leptin antagonist), because of increased food consumption. Thus, recognition and mutagenesis of Asp-23 enabled construction of novel compounds that induce potent and reversible central and peripheral leptin deficiency. In addition to enhancing our understanding of leptin interactions with its receptor, these antagonists enable in vivo study of the role of leptin in metabolic and immune processes and hold potential for future therapeutic use in disease pathologies involving leptin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution*
  • Animals
  • Body Weight / drug effects*
  • Eating / drug effects*
  • HEK293 Cells
  • Humans
  • Leptin / analogs & derivatives*
  • Leptin / antagonists & inhibitors
  • Leptin / chemistry
  • Leptin / genetics
  • Leptin / metabolism
  • Leptin / pharmacology
  • Male
  • Mice
  • Mutagenesis
  • Mutation, Missense*
  • Polyethylene Glycols* / chemistry
  • Polyethylene Glycols* / metabolism
  • Polyethylene Glycols* / pharmacology
  • Protein Binding
  • Receptors, Leptin / genetics
  • Receptors, Leptin / metabolism

Substances

  • Leptin
  • Receptors, Leptin
  • leptin, Ala(39,40,41)-
  • pegylated leptin
  • Polyethylene Glycols