HIV protease inhibitor ritonavir induces renal fibrosis and dysfunction: role of platelet-derived TGF-β1 and intervention via antioxidant pathways

AIDS. 2020 Jun 1;34(7):989-1000. doi: 10.1097/QAD.0000000000002516.

Abstract

Objective: Chronic kidney disease (CKD) with tubular injury and fibrosis occurs in HIV infection treated with certain protease inhibitor-based antiretroviral therapies. The pathophysiology is unclear.

Design: We hypothesized that fibrosis, mediated by platelet-derived transforming growth factor (TGF)-β1, underlies protease inhibitor-associated CKD. We induced this in mice exposed to the protease inhibitor ritonavir (RTV), and intervened with low-dose inhaled carbon monoxide (CO), activating erythroid 2-related factor (Nrf2)-associated antioxidant pathways.

Methods: Wild-type C57BL/6 mice and mice deficient in platelet TGF-β1, were given RTV (10 mg/kg) or vehicle daily for 8 weeks. Select groups were exposed to CO (250 ppm) for 4 h after RTV or vehicle injection. Renal disorder, fibrosis, and TGF-β1-based and Nrf2-based signaling were examined by histology, immunofluorescence, and flow cytometry. Renal damage and dysfunction were assessed by KIM-1 and cystatin C ELISAs. Clinical correlations were sought among HIV-infected individuals.

Results: RTV-induced glomerular and tubular injury, elevating urinary KIM-1 (P = 0.004). It enhanced TGF-β1-related signaling, accompanied by kidney fibrosis, macrophage polarization to an inflammatory phenotype, and renal dysfunction with cystatin C elevation (P = 0.008). Mice lacking TGF-β1 in platelets were partially protected from these abnormalities. CO inhibited RTV-induced fibrosis and macrophage polarization in association with upregulation of Nrf2 and heme oxygenase-1 (HO-1). Clinically, HIV infection correlated with elevated cystatin C levels in untreated women (n = 17) vs. age-matched controls (n = 19; P = 0.014). RTV-treated HIV+ women had further increases in cystatin C (n = 20; P = 0.05), with parallel elevation of HO-1.

Conclusion: Platelet TGF-β1 contributes to RTV-induced kidney fibrosis and dysfunction, which may be amenable to antioxidant interventions.

Publication types

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

MeSH terms

  • Animals
  • Antioxidants
  • Blood Platelets
  • Fibrosis / chemically induced*
  • HIV Infections / drug therapy*
  • HIV Protease Inhibitors / adverse effects*
  • HIV Protease Inhibitors / therapeutic use
  • Heme Oxygenase-1
  • Kidney Diseases / chemically induced*
  • Mice
  • Mice, Inbred C57BL
  • NF-E2-Related Factor 2
  • Rats
  • Ritonavir / adverse effects*
  • Ritonavir / therapeutic use
  • Tenofovir / adverse effects*
  • Tenofovir / therapeutic use
  • Transforming Growth Factor beta1

Substances

  • Antioxidants
  • HIV Protease Inhibitors
  • NF-E2-Related Factor 2
  • Nfe2l2 protein, mouse
  • Transforming Growth Factor beta1
  • Tenofovir
  • Heme Oxygenase-1
  • Ritonavir