Glucagon receptor antagonist upregulates circulating GLP-1 level by promoting intestinal L-cell proliferation and GLP-1 production in type 2 diabetes

BMJ Open Diabetes Res Care. 2020 Mar;8(1):e001025. doi: 10.1136/bmjdrc-2019-001025.

Abstract

Objective: Glucagon receptor (GCGR) blockage improves glycemic control and increases circulating glucagon-like peptide-1 (GLP-1) level in diabetic animals and humans. The elevated GLP-1 has been reported to be involved in the hypoglycemic effect of GCGR blockage. However, the source of this elevation remains to be clarified.

Research design and methods: REMD 2.59, a human GCGR monoclonal antibody (mAb), was administrated for 12 weeks in db/db mice and high-fat diet+streptozotocin (HFD/STZ)-induced type 2 diabetic (T2D) mice. Blood glucose, glucose tolerance and plasma GLP-1 were evaluated during the treatment. The gut length, epithelial area, and L-cell number and proliferation were detected after the mice were sacrificed. Cell proliferation and GLP-1 production were measured in mouse L-cell line GLUTag cells, and primary mouse and human enterocytes. Moreover, GLP-1 receptor (GLP-1R) antagonist or protein kinase A (PKA) inhibitor was used in GLUTag cells to determine the involved signaling pathways.

Results: Treatment with the GCGR mAb lowered blood glucose level, improved glucose tolerance and elevated plasma GLP-1 level in both db/db and HFD/STZ-induced T2D mice. Besides, the treatment promoted L-cell proliferation and LK-cell expansion, and increased the gut length, epithelial area and L-cell number in these two T2D mice. Similarly, our in vitro study showed that the GCGR mAb promoted L-cell proliferation and increased GLP-1 production in GLUTag cells, and primary mouse and human enterocytes. Furthermore, either GLP-1R antagonist or PKA inhibitor diminished the effects of GCGR mAb on L-cell proliferation and GLP-1 production.

Conclusions: The elevated circulating GLP-1 level by GCGR mAb is mainly due to intestinal L-cell proliferation and GLP-1 production, which may be mediated via GLP-1R/PKA signaling pathways. Therefore, GCGR mAb represents a promising strategy to improve glycemic control and restore the impaired GLP-1 production in T2D.

Keywords: glucagon receptor; glucagon-like peptide-1 (GLP-1); intestinal hormones; type 2 diabetes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / administration & dosage
  • Cell Proliferation / drug effects
  • Diabetes Mellitus, Experimental / blood
  • Diabetes Mellitus, Type 2 / blood*
  • Glucagon-Like Peptide 1 / blood*
  • Ileum / drug effects
  • Ileum / metabolism*
  • L Cells
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Proglucagon / metabolism
  • Receptors, Glucagon / antagonists & inhibitors
  • Receptors, Glucagon / immunology
  • Receptors, Glucagon / metabolism*
  • Signal Transduction

Substances

  • Antibodies, Monoclonal
  • Receptors, Glucagon
  • Proglucagon
  • Glucagon-Like Peptide 1