Impairment of the intestinal barrier is evident in untreated but absent in suppressively treated HIV-infected patients

Gut. 2009 Feb;58(2):220-7. doi: 10.1136/gut.2008.150425. Epub 2008 Oct 20.

Abstract

Background and aims: Impairment of the gastrointestinal mucosal barrier contributes to progression of HIV infection. The purpose of this study was to investigate the effect of highly active antiretroviral therapy (HAART) on the HIV-induced intestinal barrier defect and to identify underlying mechanisms.

Methods: Epithelial barrier function was characterised by impedance spectroscopy and [(3)H]mannitol fluxes in duodenal biopsies from 11 untreated and 8 suppressively treated HIV-infected patients, and 9 HIV-seronegative controls. The villus/crypt ratio was determined microscopically. Epithelial apoptoses were analysed by terminal deoxynucleotidyl transferase-mediated deoxyuridine triphosphate nick-end labelling (TUNEL) and caspase-3 staining. Tight junction protein expression was quantified by densitometric analysis of immunoblots. Mucosal cytokine production was determined by cytometric bead array.

Results: Only in untreated but not in treated HIV-infected patients, epithelial resistance was reduced (13 (1) vs 23 (2) ohm cm(2), p<0.01) and mannitol permeability was increased compared with HIV-negative controls (19 (3) vs 9 (1) nm/s, p<0.05). As structural correlates, epithelial apoptoses and expression of the pore-forming claudin-2 were increased while expression of the sealing claudin-1 was reduced in untreated compared with treated patients and HIV-negative controls. Furthermore, villous atrophy was evident and mucosal production of interleukin 2 (IL2), IL4 and tumour necrosis factor alpha (TNFalpha) was increased in untreated but not in treated HIV-infected patients. Incubation with IL2, IL4, TNFalpha and IL13 reduced the transepithelial resistance of rat jejunal mucosa.

Conclusions: Suppressive HAART abrogates HIV-induced intestinal barrier defect and villous atrophy. The HIV-induced barrier defect is due to altered tight junction protein composition and elevated epithelial apoptoses. Mucosal cytokines are mediators of the HIV-induced mucosal barrier defect and villous atrophy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Anti-HIV Agents / therapeutic use
  • Antiretroviral Therapy, Highly Active
  • Apoptosis
  • Blotting, Western / methods
  • Case-Control Studies
  • Cell Membrane Permeability / drug effects
  • Claudin-1
  • Claudin-4
  • Claudins
  • Cytokines / immunology
  • Cytokines / pharmacology
  • Disease Progression
  • Duodenum
  • Electric Impedance
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism*
  • Epithelial Cells / virology
  • Female
  • HIV Infections / drug therapy
  • HIV Infections / metabolism*
  • HIV Infections / virology
  • Humans
  • Interleukin-13 / analysis
  • Intestinal Absorption / drug effects
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / metabolism*
  • Intestinal Mucosa / virology
  • Male
  • Mannitol / metabolism
  • Membrane Proteins / analysis
  • Middle Aged
  • Occludin
  • Rats
  • Rats, Wistar
  • Tight Junctions / drug effects
  • Tight Junctions / metabolism
  • Tight Junctions / virology
  • Virus Replication / drug effects

Substances

  • Anti-HIV Agents
  • CLDN1 protein, human
  • CLDN2 protein, human
  • CLDN4 protein, human
  • Claudin-1
  • Claudin-4
  • Claudins
  • Cldn1 protein, rat
  • Cytokines
  • Interleukin-13
  • Membrane Proteins
  • OCLN protein, human
  • Occludin
  • Ocln protein, rat
  • Mannitol