Role of Hypoxia Inducible Factor-1α (HIF-1α) in Innate Defense against Uropathogenic Escherichia coli Infection

PLoS Pathog. 2015 Apr 30;11(4):e1004818. doi: 10.1371/journal.ppat.1004818. eCollection 2015 Apr.

Abstract

Uropathogenic E. coli (UPEC) is the primary cause of urinary tract infections (UTI) affecting approximately 150 million people worldwide. Here, we revealed the importance of transcriptional regulator hypoxia-inducible factor-1 α subunit (HIF-1α) in innate defense against UPEC-mediated UTI. The effects of AKB-4924, a HIF-1α stabilizing agent, were studied using human uroepithelial cells (5637) and a murine UTI model. UPEC adherence and invasion were significantly reduced in 5637 cells when HIF-1α protein was allowed to accumulate. Uroepithelial cells treated with AKB-4924 also experienced reduced cell death and exfoliation upon UPEC challenge. In vivo, fewer UPEC were recovered from the urine, bladders and kidneys of mice treated transurethrally with AKB-4924, whereas increased bacteria were recovered from bladders of mice with a HIF-1α deletion. Bladders and kidneys of AKB-4924 treated mice developed less inflammation as evidenced by decreased pro-inflammatory cytokine release and neutrophil activity. AKB-4924 impairs infection in uroepithelial cells and bladders, and could be correlated with enhanced production of nitric oxide and antimicrobial peptides cathelicidin and β-defensin-2. We conclude that HIF-1α transcriptional regulation plays a key role in defense of the urinary tract against UPEC infection, and that pharmacological HIF-1α boosting could be explored further as an adjunctive therapy strategy for serious or recurrent UTI.

Publication types

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

MeSH terms

  • Administration, Intravesical
  • Animals
  • Anti-Bacterial Agents / administration & dosage
  • Anti-Bacterial Agents / pharmacology
  • Anti-Bacterial Agents / therapeutic use
  • Antimicrobial Cationic Peptides / agonists
  • Antimicrobial Cationic Peptides / metabolism
  • Bacterial Adhesion / drug effects
  • Cell Line
  • Escherichia coli Infections / immunology
  • Escherichia coli Infections / metabolism*
  • Escherichia coli Infections / microbiology
  • Escherichia coli Infections / prevention & control
  • Female
  • Host-Pathogen Interactions / drug effects
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / agonists
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Immunity, Innate* / drug effects
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nitric Oxide / agonists
  • Nitric Oxide / metabolism
  • Piperazines / administration & dosage
  • Piperazines / pharmacology
  • Piperazines / therapeutic use
  • Protein Stability / drug effects
  • Pyridones / administration & dosage
  • Pyridones / pharmacology
  • Pyridones / therapeutic use
  • RNA, Messenger / metabolism
  • Urinary Tract Infections / immunology
  • Urinary Tract Infections / metabolism*
  • Urinary Tract Infections / microbiology
  • Urinary Tract Infections / prevention & control
  • Uropathogenic Escherichia coli / drug effects
  • Uropathogenic Escherichia coli / immunology*
  • Urothelium / drug effects
  • Urothelium / immunology
  • Urothelium / metabolism*
  • Urothelium / microbiology

Substances

  • AKB-4924
  • Anti-Bacterial Agents
  • Antimicrobial Cationic Peptides
  • HIF1A protein, human
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Piperazines
  • Pyridones
  • RNA, Messenger
  • Nitric Oxide