Metformin reduces airway glucose permeability and hyperglycaemia-induced Staphylococcus aureus load independently of effects on blood glucose

Thorax. 2013 Sep;68(9):835-45. doi: 10.1136/thoraxjnl-2012-203178. Epub 2013 May 24.

Abstract

Background: Diabetes is a risk factor for respiratory infection, and hyperglycaemia is associated with increased glucose in airway surface liquid and risk of Staphylococcus aureus infection.

Objectives: To investigate whether elevation of basolateral/blood glucose concentration promotes airway Staphylococcus aureus growth and whether pretreatment with the antidiabetic drug metformin affects this relationship.

Methods: Human airway epithelial cells grown at air-liquid interface (±18 h pre-treatment, 30 μM-1 mM metformin) were inoculated with 5×10(5) colony-forming units (CFU)/cm(2) S aureus 8325-4 or JE2 or Pseudomonas aeruginosa PA01 on the apical surface and incubated for 7 h. Wild-type C57BL/6 or db/db (leptin receptor-deficient) mice, 6-10 weeks old, were treated with intraperitoneal phosphate-buffered saline or 40 mg/kg metformin for 2 days before intranasal inoculation with 1×10(7) CFU S aureus. Mice were culled 24 h after infection and bronchoalveolar lavage fluid collected.

Results: Apical S aureus growth increased with basolateral glucose concentration in an in vitro airway epithelia-bacteria co-culture model. S aureus reduced transepithelial electrical resistance (RT) and increased paracellular glucose flux. Metformin inhibited the glucose-induced growth of S aureus, increased RT and decreased glucose flux. Diabetic (db/db) mice infected with S aureus exhibited a higher bacterial load in their airways than control mice after 2 days and metformin treatment reversed this effect. Metformin did not decrease blood glucose but reduced paracellular flux across ex vivo murine tracheas.

Conclusions: Hyperglycaemia promotes respiratory S aureus infection, and metformin modifies glucose flux across the airway epithelium to limit hyperglycaemia-induced bacterial growth. Metformin might, therefore, be of additional benefit in the prevention and treatment of respiratory infection.

Keywords: Airway Epithelium; Bacterial Infection; COPD Exacerbations; Respiratory Infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Load / drug effects*
  • Blood Glucose / drug effects
  • Blood Glucose / metabolism*
  • Bronchoalveolar Lavage Fluid
  • Cells, Cultured
  • Chemokine CXCL9 / metabolism
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism*
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism
  • Hyperglycemia / blood
  • Hyperglycemia / drug therapy
  • Interleukin-1alpha / metabolism
  • Interleukin-6 / metabolism
  • Metformin / pharmacology*
  • Mice
  • Mice, Inbred C57BL
  • Permeability / drug effects
  • Pseudomonas aeruginosa / drug effects
  • Pseudomonas aeruginosa / growth & development*
  • Receptors, Leptin / deficiency
  • Receptors, Leptin / genetics
  • Respiratory System / metabolism
  • Respiratory System / microbiology
  • Staphylococcus aureus / drug effects
  • Staphylococcus aureus / growth & development*
  • Transforming Growth Factor beta / metabolism

Substances

  • Blood Glucose
  • Chemokine CXCL9
  • Interleukin-1alpha
  • Interleukin-6
  • Receptors, Leptin
  • Transforming Growth Factor beta
  • Granulocyte-Macrophage Colony-Stimulating Factor
  • Metformin