Calcitonin native prefibrillar oligomers but not monomers induce membrane damage that triggers NMDA-mediated Ca2+-influx, LTP impairment and neurotoxicity

Sci Rep. 2019 Mar 26;9(1):5144. doi: 10.1038/s41598-019-41462-0.

Abstract

Amyloid protein misfolding results in a self-assembling aggregation process, characterized by the formation of typical aggregates. The attention is focused on pre-fibrillar oligomers (PFOs), formed in the early stages and supposed to be neurotoxic. PFOs structure may change due to their instability and different experimental protocols. Consequently, it is difficult to ascertain which aggregation species are actually neurotoxic. We used salmon Calcitonin (sCT) as an amyloid model whose slow aggregation rate allowed to prepare stable samples without photochemical cross-linking. Intracellular Ca2+ rise plays a fundamental role in amyloid protein-induced neurodegerations. Two paradigms have been explored: (i) the "membrane permeabilization" due to the formation of amyloid pores or other types of membrane damage; (ii) "receptor-mediated" modulation of Ca2+ channels. In the present paper, we tested the effects of native sCT PFOs- with respect to Monomer-enriched solutions in neurons characterized by an increasing degree of differentiation, in terms of -Ca2+-influx, cellular viability, -Long-Term Potentiation impairment, Post-Synaptic Densities and synaptophysin expression. Results indicated that PFOs-, but not Monomer-enriched solutions, induced abnormal -Ca2+-influx, which could only in part be ascribed to NMDAR activation. Thus, we propose an innovative neurotoxicity mechanism for amyloid proteins where "membrane permeabilization" and "receptor-mediated" paradigms coexist.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyloid / chemistry
  • Amyloid / toxicity*
  • Animals
  • Calcitonin / chemistry
  • Calcitonin / toxicity*
  • Calcium / metabolism
  • Calcium Signaling / drug effects*
  • Cell Line
  • Cell Membrane / metabolism*
  • Cell Membrane / pathology
  • Fish Proteins / chemistry
  • Fish Proteins / toxicity*
  • Long-Term Potentiation / drug effects*
  • Mice
  • N-Methylaspartate / metabolism*
  • Neurons / metabolism*
  • Neurons / pathology
  • Neurotoxicity Syndromes / metabolism*
  • Neurotoxicity Syndromes / pathology
  • Protein Multimerization*
  • Salmon*

Substances

  • Amyloid
  • Fish Proteins
  • N-Methylaspartate
  • Calcitonin
  • Calcium