Synbindin deficiency inhibits colon carcinogenesis by attenuating Wnt cascade and balancing gut microbiome

Int J Cancer. 2019 Jul 1;145(1):206-220. doi: 10.1002/ijc.32074. Epub 2019 Jan 10.

Abstract

The molecular mechanisms that control the development of colorectal cancer (CRC) remain poorly defined. Here we show Synbindin promoted CRC oncogenesis by activating Wnt signaling and altering gut microbiome. Synbindin upregulation in human CRCs was associated with poor patient prognosis. Intestine-specific disruption of Synbindin balanced the disturbed gut microbiota and protected mice against tumor formation in the colitis-associated cancer (CAC) model. The protective role was compromised after gut microbiota depletion. In host, increased goblet cells and mucin2 expression, together with increased intestinal epithelial cells (IECs) apoptosis and decreased epithelial proliferation were observed. Further transcriptomic sequencing identified Wnt signaling a major regulatory node downstream of Synbindin. Combined molecular and cellular characterizations revealed that Synbindin confers Disheveled-3 (DVL3)-based signalosome assembly and acts as a modular scaffold for DVL3 and Axin2 complex, orchestrating the intensity of Wnt signaling. These findings identify a critical role of Synbindin in gut microbiome composition and Wnt signaling activation in colorectal carcinogenesis, and highlight Synbindin as an adaptor protein with multifaceted roles.

Keywords: CRC; DVL3; Synbindin; Wnt signaling; gut microbiome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axin Protein / metabolism
  • Carcinogenesis
  • Colitis / chemically induced
  • Colitis / metabolism
  • Colitis / microbiology
  • Colitis / pathology
  • Colorectal Neoplasms / metabolism*
  • Colorectal Neoplasms / microbiology*
  • Colorectal Neoplasms / pathology
  • Dextran Sulfate
  • Dishevelled Proteins / metabolism
  • Gastrointestinal Microbiome / physiology*
  • HCT116 Cells
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microbiota / physiology
  • Mucin-2 / metabolism
  • Nerve Tissue Proteins / deficiency*
  • Nerve Tissue Proteins / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Vesicular Transport Proteins / deficiency*
  • Vesicular Transport Proteins / metabolism
  • Wnt Signaling Pathway*

Substances

  • AXIN2 protein, human
  • Axin Protein
  • Axin2 protein, mouse
  • DVL3 protein, human
  • Dishevelled Proteins
  • Dvl3 protein, mouse
  • Mucin-2
  • Nerve Tissue Proteins
  • RNA, Messenger
  • TRAPPC4 protein, human
  • Trappc4 protein, mouse
  • Vesicular Transport Proteins
  • Dextran Sulfate