Suppression of leptin-AI/AII transcripts by insulin in goldfish liver: A fish specific response of leptin under food deprivation

Gen Comp Endocrinol. 2019 Nov 1:283:113240. doi: 10.1016/j.ygcen.2019.113240. Epub 2019 Aug 5.

Abstract

Leptin is primarily considered a peripheral satiety hormone and is also found to perform important roles in energy homeostasis in vertebrates ranging from fish to mammals. The liver is a major source of leptin production in teleost fish. Using goldfish as a model, a previous report by our group illustrated the positive regulation of leptin mRNA levels by treatment with the hyperglycemic hormone glucagon, and our present study provided evidence for the negative regulation of hepatic leptin-AI and leptin-AII transcripts through the administration of the hypoglycemic hormone insulin. This study is the first to demonstrate changes in the hepatopancreatic insulin, glucagon, leptin-AI and leptin-AII mRNA levels in goldfish during fasting and refeeding. Insulin was found to be effective in suppressing leptin-AI and leptin-AII transcript levels in goldfish liver via both in vivo intraperitoneal injection and in vitro cell incubation approaches. Only the insulin receptor, not the IGF-I receptor, was involved in insulin-inhibited leptin mRNA level. The suppression of leptin levels by insulin was caused by the activation of MKK3/6/p38MAPK and MEK1/2/Erk1/2 cascades. Insulin treatment could eliminate the stimulation of glucagon on leptin mRNA level. Our study describes the regulation and signal transduction mechanism of insulin on leptin mRNA levels in the goldfish liver, suggesting that the leptin function in fish is speculated to be not only an anorexigenic factor but also a metabolic mediator. This also supports the hypothesis that the poikilothermal fish use a passive survival strategy during the periods of food deprivation, which is mediated by the fish-specifically high leptin levels induced by the cooperation of insulin and glucagon.

Keywords: Fasting; Glucagon; Goldfish; Insulin; Leptin; Regulation; Signal transduction; mRNA level.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Colforsin / pharmacology
  • Fasting
  • Feeding Behavior / drug effects
  • Food Deprivation / physiology*
  • Glucagon / pharmacology
  • Goldfish / genetics*
  • Hepatopancreas / drug effects
  • Hepatopancreas / metabolism
  • Humans
  • Injections, Intraperitoneal
  • Insulin / administration & dosage
  • Insulin / pharmacology*
  • Insulin-Like Growth Factor I / pharmacology
  • Insulin-Like Growth Factor II / pharmacology
  • Leptin / genetics*
  • Leptin / metabolism
  • Liver / drug effects
  • Liver / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, Leptin / metabolism
  • Signal Transduction / drug effects

Substances

  • Insulin
  • Leptin
  • RNA, Messenger
  • Receptors, Leptin
  • Colforsin
  • Insulin-Like Growth Factor I
  • Insulin-Like Growth Factor II
  • Glucagon