Cancer-associated fibroblasts barrier breaking via TGF-β blockade paved way for docetaxel micelles delivery to treat pancreatic cancer

Int J Pharm. 2024 Nov 15:665:124706. doi: 10.1016/j.ijpharm.2024.124706. Epub 2024 Sep 12.

Abstract

TGF-β is a crucial regulator in tumor microenvironment (TME), especially for myofibroblastic cancer-associated fibroblasts (myCAFs). The myCAFs can be motivated by TGF-β signaling to erect pro-tumor TME, meanwhile, myCAFs overexpress TGF-β to mediate the crosstalk between tumor and stromal cells. The blockade of TGF-β can break cancer-associated fibroblasts barrier, consequently opening the access for drugs into tumor. The TGF-β is a promising target in anti-tumor therapy. Herein, we introduced a two-stage combination therapy (TC-Therapy), including TGF-β receptor I inhibitor SB525334 (SB) and cytotoxicity agent docetaxel micelle (DTX-M). We found that SB and DTX-M synergistically inhibited myCAFs proliferation and elevated p53 protein expression in BxPC-3/3T3 mixed cells. Gene and protein tests demonstrated that SB cut off TGF-β signaling via receptor blockade and it did not arouse TGF-β legend compensated internal autocrine. On the contrary, two agents combined decreased TGF-β secretion and inhibited myCAFs viability marked by α-SMA and FAPα. TC-Therapy was applied in BxPc-3/3T3 mixed tumor-bearing mice model. After TC-Therapy, the α-SMA+/ FAPα+ myCAFs faded increasingly and collagenous fibers mainly secreted by myCAFs decreased dramatically as well. More than that, the myCAFs barrier breaking helped to normalize micro-vessels and paved way for micelle penetration. The TGF-β protein level of TC-Therapy in TME was much lower than that of simplex DTX-M, which might account for TME restoration. In conclusion, TGF-β inhibitor acted as the pioneer before nano chemotherapeutic agents. The TC-Therapy of TGF-β signaling inhibition and anti-tumor agent DTX-M is a promising regimen without arising metastasis risk to treat pancreatic cancer. The therapeutic regimen focused on TGF-β related myCAFs reminds clinicians to have a comprehensive understanding of pancreatic cancer.

Keywords: Cancer-associated fibroblasts; Combination therapy; Docetaxel micelle; TGF-β signalling; Tumor microenvironment.

MeSH terms

  • 3T3 Cells
  • Animals
  • Antineoplastic Agents* / administration & dosage
  • Antineoplastic Agents* / pharmacology
  • Cancer-Associated Fibroblasts* / drug effects
  • Cancer-Associated Fibroblasts* / metabolism
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Docetaxel* / administration & dosage
  • Docetaxel* / pharmacology
  • Drug Delivery Systems / methods
  • Humans
  • Imidazoles
  • Mice
  • Mice, Inbred BALB C
  • Micelles*
  • Pancreatic Neoplasms* / drug therapy
  • Pancreatic Neoplasms* / pathology
  • Quinoxalines
  • Receptor, Transforming Growth Factor-beta Type I / antagonists & inhibitors
  • Receptor, Transforming Growth Factor-beta Type I / metabolism
  • Signal Transduction / drug effects
  • Transforming Growth Factor beta* / antagonists & inhibitors
  • Transforming Growth Factor beta* / metabolism
  • Tumor Microenvironment / drug effects

Substances

  • Docetaxel
  • Micelles
  • Transforming Growth Factor beta
  • Antineoplastic Agents
  • 6-(2-tert-butyl-5-(6-methylpyridin-2-yl)-1H-imidazol-4-yl)quinoxaline
  • Receptor, Transforming Growth Factor-beta Type I
  • Imidazoles
  • Quinoxalines