Complementary role of peripheral and central autonomic nervous system on insulin-like growth factor-1 activation to prevent fatty liver disease

Hepatol Int. 2024 Feb;18(1):155-167. doi: 10.1007/s12072-023-10601-1. Epub 2023 Oct 21.

Abstract

Background: Insulin-like growth factor-1 (IGF-1) is involved in the pathology of non-alcoholic fatty liver disease (NAFLD) and ameliorates fatty infiltration in the liver. It is activated by growth hormone (GH); however, the role of GH-IGF-1 axis in NAFLD developmental phase has not been well identified. Therefore, in this study, we focused on the effect of IGF-1 in NAFLD pathology and GH excretion activation from the pituitary gland by peripheral autonomic neural pathways relaying liver-brain-gut pathway and by central neuropeptides.

Methods: GH and IGF-1 levels were assessed in wild-type and melanocortin-4 receptor knockout mice upon the development of diet-induced NAFLD. The contribution of the peripheral autonomic nervous system connecting the liver-brain-gut axis was assessed by its blockade using capsaicin and that of the central nervous system was assessed by the expression of hypothalamic brain-derived neurotrophic factor (BDNF) and corticotropin-releasing factor (CRH), which activates GH release from the pituitary gland.

Results: In the NAFLD mouse models, the levels of GH and IGF-1 increased (p < .05). Further, hepatic fatty infiltration was suppressed even under peripheral autonomic nervous system blockade (p < .001), which inhibited gastric ghrelin expression. In mice with peripheral autonomic nervous blockade, hypothalamic BDNF and CRH were inhibited (p < .05), resulting in GH and IGF-1 excretion, whereas other neuropeptides of somatostatin and cortistatin showed no changes. These complementary effects were canceled in melanocortin-4 receptor knockout mice, which diminished BDNF and CRH release control.

Conclusions: Our study demonstrates that the release of IGF-1 by the nervous system is a key factor in maintaining the pathological homeostasis of NAFLD, suggesting its therapeutic potential.

Keywords: Autonomic neuron; BDNF; Brain; CRH; GH; Gastrointestinal hormone; Ghrelin; IGF-1; Inter-organ communication; NAFLD; Peptide.

MeSH terms

  • Animals
  • Brain-Derived Neurotrophic Factor
  • Growth Hormone / metabolism
  • Insulin-Like Growth Factor I / metabolism
  • Insulin-Like Peptides
  • Mice
  • Mice, Knockout
  • Neuropeptides* / metabolism
  • Non-alcoholic Fatty Liver Disease* / prevention & control
  • Receptor, Melanocortin, Type 4

Substances

  • Brain-Derived Neurotrophic Factor
  • Insulin-Like Peptides
  • Receptor, Melanocortin, Type 4
  • Insulin-Like Growth Factor I
  • Neuropeptides
  • Growth Hormone