Chromosome-associated protein D3 promotes bacterial clearance in human intestinal epithelial cells by repressing expression of amino acid transporters

Gastroenterology. 2015 Jun;148(7):1405-1416.e3. doi: 10.1053/j.gastro.2015.02.013. Epub 2015 Feb 18.

Abstract

Background & aims: Defects in colonic epithelial barrier defenses are associated with ulcerative colitis (UC). The proteins that regulate bacterial clearance in the colonic epithelium have not been completely identified. The Drosophila chromosome-associated protein D3 (dCAP-D3) regulates responses to bacterial infection. We examined whether CAP-D3 promotes bacterial clearance in human colonic epithelium.

Methods: Clearance of Salmonella or adherent-invasive Escherichia coli LF82 was assessed by gentamycin protection assays in HT-29 and Caco-2 cells expressing small hairpin RNAs against CAP-D3. We used immunoblot assays to measure levels of CAP-D3 in colonic epithelial cells from patients with UC and healthy individuals (controls). RNA sequencing identified genes activated by CAP-D3. We analyzed the roles of CAP-D3 target genes in bacterial clearance using gentamycin protection and immunofluorescence assays and studies with pharmacologic inhibitors.

Results: CAP-D3 expression was reduced in colonic epithelial cells from patients with active UC. Reduced CAP-D3 expression decreased autophagy and impaired intracellular bacterial clearance by HT-29 and Caco-2 colonic epithelial cells. Lower levels of CAP-D3 increased transcription of genes encoding SLC7A5 and SLC3A2, the products of which heterodimerize to form an amino acid transporter in HT-29 cells after bacterial infection; levels of SLC7A5-SLC3A2 were increased in tissues from patients with UC compared with controls. Reduced CAP-D3 in HT-29 cells resulted in earlier recruitment of SLC7A5 to Salmonella-containing vacuoles, increased activity of mTORC1, and increased survival of bacteria. Inhibition of SLC7A5-SLC3A2 or mTORC1 activity rescued the bacterial clearance defects of CAP-D3-deficient cells.

Conclusions: CAP-D3 down-regulates transcription of genes that encode amino acid transporters (SLC7A5 and SLC3A2) to promote bacterial autophagy by colon epithelial cells. Levels of CAP-D3 protein are reduced in patients with active UC; strategies to increase its levels might restore mucosal homeostasis to patients with active UC.

Keywords: Condensin; Dysbiosis; Inflammatory Bowel Disease; Innate Immunity.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adenosine Triphosphatases
  • Autophagy
  • Caco-2 Cells
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Colitis, Ulcerative / immunology
  • Colitis, Ulcerative / metabolism
  • Colitis, Ulcerative / microbiology
  • Crohn Disease / immunology
  • Crohn Disease / metabolism
  • Crohn Disease / microbiology
  • Drosophila Proteins
  • Epithelial Cells / immunology
  • Epithelial Cells / metabolism*
  • Epithelial Cells / microbiology*
  • Escherichia coli / immunology
  • Escherichia coli / physiology*
  • Fusion Regulatory Protein 1, Heavy Chain / genetics
  • Fusion Regulatory Protein 1, Heavy Chain / metabolism*
  • Gene Expression Regulation
  • HT29 Cells
  • Humans
  • Immunity, Innate
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / metabolism*
  • Intestinal Mucosa / microbiology*
  • Large Neutral Amino Acid-Transporter 1 / genetics
  • Large Neutral Amino Acid-Transporter 1 / metabolism*
  • Mechanistic Target of Rapamycin Complex 1
  • Microbial Viability
  • Multiprotein Complexes / metabolism
  • RNA Interference
  • Salmonella / immunology
  • Salmonella / physiology*
  • Signal Transduction
  • TOR Serine-Threonine Kinases / metabolism
  • Time Factors
  • Transcription, Genetic
  • Transfection

Substances

  • Cell Cycle Proteins
  • Drosophila Proteins
  • Fusion Regulatory Protein 1, Heavy Chain
  • Large Neutral Amino Acid-Transporter 1
  • Multiprotein Complexes
  • NCAPD3 protein, human
  • SLC3A2 protein, human
  • Mechanistic Target of Rapamycin Complex 1
  • TOR Serine-Threonine Kinases
  • Adenosine Triphosphatases
  • CAP-D3 protein, Drosophila

Associated data

  • GEO/GSE62520