Chaperone-Derived Copper(I)-Binding Peptide Nanofibers Disrupt Copper Homeostasis in Cancer Cells

Angew Chem Int Ed Engl. 2024 Dec 16;63(51):e202412477. doi: 10.1002/anie.202412477. Epub 2024 Nov 18.

Abstract

Copper (Cu) is a transition metal that plays crucial roles in cellular metabolism. Cu+ homeostasis is upregulated in many cancers and contributes to tumorigenesis. However, therapeutic strategies to target Cu+ homeostasis in cancer cells are rarely explored because small molecule Cu+ chelators have poor binding affinity in comparison to the intracellular Cu+ chaperones, enzymes, or ligands. To address this challenge, we introduce a Cu+ chaperone-inspired supramolecular approach to disrupt Cu+ homeostasis in cancer cells that induces programmed cell death. The Nap-FFMTCGGCR peptide self-assembles into nanofibers inside cancer cells with high binding affinity and selectivity for Cu+ due to the presence of the unique MTCGGC motif, which is conserved in intracellular Cu+ chaperones. Nap-FFMTCGGCR exhibits cytotoxicity towards triple negative breast cancer cells (MDA-MB-231), impairs the activity of Cu+ dependent co-chaperone super oxide dismutase1 (SOD1), and induces oxidative stress. In contrast, Nap-FFMTCGGCR has minimal impact on normal HEK 293T cells. Control peptides show that the self-assembly and Cu+ binding must work in synergy to successfully disrupt Cu+ homeostasis. We show that assembly-enhanced affinity for metal ions opens new therapeutic strategies to address disease-relevant metal ion homeostasis.

Keywords: Cancer therapeutics; Cu+ homeostasis interruption; Intracellular self-assembly; Oxidative stress.

MeSH terms

  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology
  • Cell Line, Tumor
  • Copper* / chemistry
  • Copper* / metabolism
  • Homeostasis* / drug effects
  • Humans
  • Molecular Chaperones* / chemistry
  • Molecular Chaperones* / metabolism
  • Nanofibers* / chemistry
  • Peptides* / chemistry
  • Peptides* / metabolism
  • Peptides* / pharmacology

Substances

  • Copper
  • Peptides
  • Molecular Chaperones
  • Antineoplastic Agents