Smart pH-Sensitive Nanogels for Enhancing Synergistic Anticancer Effects of Integrin αvβ3 Specific Apoptotic Peptide and Therapeutic Nitric Oxide

ACS Appl Mater Interfaces. 2019 Sep 25;11(38):34663-34675. doi: 10.1021/acsami.9b10830. Epub 2019 Sep 16.

Abstract

Apoptotic peptide (kla), which can trigger the mitochondria-mediated apoptotic programmed cell death, has been widely recognized as a potential anticancer agent. However, its therapeutic potential has been significantly impaired by its poor biostability, lack of tumor specificity, and particularly low cellular uptake. Herein, a linear peptide Arg-Trp-d-Arg-Asn-Arg (RWrNR) was identified as an integrin αvβ3 specific ligand with a nanomolar dissociation constant (Kd = 0.95 nM), which can greatly improve kla antitumor activity (IC50 = 8.81 μM) by improving its cellular uptake, compared to the classic integrin-recognition motif c-RGDyK (IC50 = 37.96 μM). Particularly, the RWrNR-kla conjugate can be entrapped in acidic sensitive nanogels (RK/Parg/CMCS-NGs), composed of poly-l-arginine (Parg) and carboxymethyl chitosan (CMCS, pI = 6.8), which can not only carry out controlled release of RWrNR-kla in response to the tumor acidic microenvironment, and consequently enhance its tumor specificity and cell internalization, but also trigger tumor-associated macrophages to generate nitric oxide, leading to enhanced synergistic anticancer efficacy. Importantly, RK/Parg/CMCS-NGs have been proven to effectively activate the apoptosis signaling pathway in vivo and significantly inhibit tumor growth with minimal adverse effects. To summarize, RK/Parg/CMCS-NGs are a promising apoptotic peptide-based therapeutics with enhanced tumor accumulation, cytosolic delivery, and synergistic anticancer effects, thereby holding great potential for the treatment of malignant tumors.

Keywords: acid-responsive; apoptotic peptide; integrin αvβ3 agonist; nanogels; synergistic anticancer.

MeSH terms

  • Animals
  • Antineoplastic Agents* / chemistry
  • Antineoplastic Agents* / pharmacokinetics
  • Antineoplastic Agents* / pharmacology
  • Apoptosis / drug effects*
  • Drug Delivery Systems*
  • Humans
  • Integrin alphaVbeta3 / metabolism*
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Nanogels
  • Neoplasm Proteins
  • Neoplasms, Experimental* / drug therapy
  • Neoplasms, Experimental* / metabolism
  • Neoplasms, Experimental* / pathology
  • Nitric Oxide* / chemistry
  • Nitric Oxide* / pharmacokinetics
  • Nitric Oxide* / pharmacology
  • Peptides* / chemistry
  • Peptides* / pharmacokinetics
  • Peptides* / pharmacology
  • RAW 264.7 Cells
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • Integrin alphaVbeta3
  • Nanogels
  • Neoplasm Proteins
  • Peptides
  • Nitric Oxide