Ribonuclease 7 Shields the Kidney and Bladder from Invasive Uropathogenic Escherichia coli Infection

J Am Soc Nephrol. 2019 Aug;30(8):1385-1397. doi: 10.1681/ASN.2018090929. Epub 2019 Jun 25.

Abstract

Background: Evidence suggests that antimicrobial peptides, components of the innate immune response, protect the kidneys and bladder from bacterial challenge. We previously identified ribonuclease 7 (RNase 7) as a human antimicrobial peptide that has bactericidal activity against uropathogenic Escherichia coli (UPEC). Functional studies assessing RNase 7's contributions to urinary tract defense are limited.

Methods: To investigate RNase 7's role in preventing urinary tract infection (UTI), we quantified urinary RNase 7 concentrations in 29 girls and adolescents with a UTI history and 29 healthy female human controls. To assess RNase 7's antimicrobial activity in vitro in human urothelial cells, we used siRNA to silence urothelial RNase 7 production and retroviral constructs to stably overexpress RNase 7; we then evaluated UPEC's ability to bind and invade these cells. For RNase 7 in vivo studies, we developed humanized RNase 7 transgenic mice, subjected them to experimental UTI, and enumerated UPEC burden in the urine, bladder, and kidneys.

Results: Compared with controls, study participants with a UTI history had 1.5-fold lower urinary RNase 7 concentrations. When RNase 7 was silenced in vitro, the percentage of UPEC binding or invading human urothelial cells increased; when cells overexpressed RNase 7, UPEC attachment and invasion decreased. In the transgenic mice, we detected RNase 7 expression in the kidney's intercalated cells and bladder urothelium. RNase 7 humanized mice exhibited marked protection from UPEC.

Conclusions: These findings provide evidence that RNase 7 has a role in kidney and bladder host defense against UPEC and establish a foundation for investigating RNase 7 as a UTI prognostic marker or nonantibiotic-based therapy.

Keywords: antimicrobial peptides; intercalated cells; ribonuclease 7; urinary tract infection; urothelium.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adolescent
  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Antimicrobial Cationic Peptides / genetics
  • Child
  • Child, Preschool
  • Escherichia coli Infections / enzymology*
  • Female
  • Gene Silencing
  • Humans
  • Immunity, Innate
  • Infant
  • Kidney / enzymology*
  • Kidney / microbiology
  • Male
  • Mice
  • Mice, Transgenic
  • Phenotype
  • Prognosis
  • Ribonucleases / genetics*
  • Urinary Bladder / enzymology*
  • Urinary Bladder / microbiology
  • Urinary Tract Infections / enzymology*
  • Urinary Tract Infections / microbiology*
  • Uropathogenic Escherichia coli*
  • Urothelium / metabolism
  • Urothelium / pathology
  • Young Adult

Substances

  • Anti-Bacterial Agents
  • Antimicrobial Cationic Peptides
  • Ribonucleases
  • Ribonuclease 7