Effects of Amylin Against Amyloid-β-Induced Tauopathy and Synapse Loss in Primary Neurons

J Alzheimers Dis. 2019;70(4):1025-1040. doi: 10.3233/JAD-190161.

Abstract

Recent studies demonstrate that peripheral amylin treatment reduces pathology in mouse models of Alzheimer's disease (AD). However, soluble and aggregated amylin are distinct species; while amylin is a physiological neuropeptide, amylin aggregation is a pathological factor for diabetes. We thus hypothesized that because of their similarity in secondary structures, amylin antagonizes amyloid-β peptide (Aβ)-induced AD pathology in neurons with a dose-dependent pattern. To test the hypothesis, we conducted both in vitro and in vivo experiments with different doses of amylin and with its analog, pramlintide. Here we report that a high concentration of either Aβ or amylin alone induced tau phosphorylation (pTau) in primary neurons. Interestingly, with a low concentration, amylin had direct effects to reverse the Aβ-induced pTau, as well as damaged neuronal synapses and neurite disorganization. However, when the concentration was high (10.24 μM), amylin lost the effects against the Aβ-induced cellular AD pathology and, together with Aβ, worsened tauopathy in neurons. In the 5XFAD AD mouse model, daily peripheral amylin treatment with a low dose (200 μg/kg) more effectively reduced amyloid burden, and increased synapse, but with a high dose (800 μg/kg), it more effectively reduced tauopathy. Correspondingly, amylin treatment improved learning and memory in these mice. It demonstrates that amylin has a dose-dependent U-shape effect against AD pathogenesis. Within a physiological range, amylin is a neuroprotective hormone against AD in neurons; but when both Aβ and amylin concentrations are elevated, imbalance of Aβ and amylin may contribute to brain AD pathogenesis.

Keywords: Alzheimer’s disease; U-shape; amylin; amyloid-β peptide; pramlintide; synapse; tauopathy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amyloid beta-Peptides / toxicity*
  • Animals
  • Animals, Newborn
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Female
  • Humans
  • Islet Amyloid Polypeptide / pharmacology*
  • Islet Amyloid Polypeptide / therapeutic use
  • Mice
  • Mice, Transgenic
  • Neurons / drug effects*
  • Neurons / pathology
  • Peptide Fragments / toxicity*
  • Pregnancy
  • Rats
  • Rats, Wistar
  • Synapses / drug effects*
  • Synapses / pathology
  • Tauopathies / chemically induced*
  • Tauopathies / drug therapy*
  • Tauopathies / pathology

Substances

  • Amyloid beta-Peptides
  • Islet Amyloid Polypeptide
  • Peptide Fragments
  • amyloid beta-protein (1-42)