Helminth-derived molecules inhibit colitis-associated colon cancer development through NF-κB and STAT3 regulation

Int J Cancer. 2019 Dec 1;145(11):3126-3139. doi: 10.1002/ijc.32626. Epub 2019 Aug 30.

Abstract

Inflammation is currently considered a hallmark of cancer and plays a decisive role in different stages of tumorigenesis, including initiation, promotion, progression, metastasis and resistance to antitumor therapies. Colorectal cancer is a disease widely associated with local chronic inflammation. Additionally, extrinsic factors such as infection may beneficially or detrimentally alter cancer progression. Several reports have noted the ability of various parasitic infections to modulate cancer development, favoring tumor progression in many cases and inhibiting tumorigenesis in others. The aim of our study was to determine the effects of excreted/secreted products of the helminth Taenia crassiceps (TcES) as a treatment in a murine model of colitis-associated colon cancer (CAC). Here, we found that after inducing CAC, treatment with TcES was able to reduce inflammatory cytokines such as IL-1β, TNF-α, IL-33 and IL-17 and significantly attenuate colon tumorigenesis. This effect was associated with the inhibition of signal transducer and activator of transcription 3 and nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) phosphorylation. Furthermore, we determined that TcES interfered with LPS-induced NF-κB p65 activation in human colonic epithelial cell lines in a Raf-1 proto-oncogene-dependent manner. Moreover, in three-dimensional cultures, TcES promoted reorganization of the actin cytoskeleton, altering cell morphology and forming colonospheres, features associated with a low grade of aggressiveness. Our study demonstrates a remarkable effect of helminth-derived molecules on suppressing ongoing colorectal cancer by downregulating proinflammatory and protumorigenic signaling pathways.

Keywords: Taenia crassiceps; NF-κB; STAT3; colorectal cancer; inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / administration & dosage*
  • Anti-Inflammatory Agents / pharmacology
  • Azoxymethane / adverse effects*
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Colitis / chemically induced
  • Colitis / complications
  • Colitis / drug therapy*
  • Colonic Neoplasms / drug therapy*
  • Colonic Neoplasms / etiology
  • Disease Models, Animal
  • Female
  • Helminth Proteins / administration & dosage*
  • Helminth Proteins / pharmacology
  • Humans
  • Interleukin-1beta / metabolism
  • Interleukin-33 / metabolism
  • Mice
  • NF-kappa B / metabolism
  • Phosphorylation
  • Proto-Oncogene Mas
  • STAT3 Transcription Factor / metabolism
  • Taenia / metabolism*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Anti-Inflammatory Agents
  • Helminth Proteins
  • IL1B protein, human
  • IL33 protein, human
  • Interleukin-1beta
  • Interleukin-33
  • MAS1 protein, human
  • NF-kappa B
  • Proto-Oncogene Mas
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • TNF protein, human
  • Tumor Necrosis Factor-alpha
  • Azoxymethane