Functional restoration of CD56bright NK cells facilitates immune control via IL-15 and NKG2D in patients under antiviral treatment for chronic hepatitis B

Hepatol Int. 2017 Sep;11(5):419-428. doi: 10.1007/s12072-017-9803-4. Epub 2017 Jun 20.

Abstract

Background and aims: Hepatitis B virus (HBV) is intrinsically immunogenic, with long-lasting immune control in many patients. However, the mechanisms and key cell types underlying effective immune control are incompletely understood.

Methods: We studied the restoration of natural killer (NK) cell numbers and function post antiviral treatment in 52 hepatitis B e antigen (HBeAg)-positive chronic hepatitis B (CHB) patients who received telbivudine (LdT) for 48 weeks. Blood samples were collected at week 0, 12, 24, 36, and 48 and tested for HBV DNA, hepatitis B surface antigen (HBsAg), HBeAg, liver enzymes, and NK cell parameters.

Results: Compared with baseline, the number of peripheral CD3-CD56bright NK cells increased significantly from week 24 to 48, especially in patients with baseline alanine transaminase (ALT) two- to fivefold the upper line of normal (ULN) or HBV DNA <9 log10 copies/ml. Expression (number and density) of activating receptors NKG2D and NKp46 on CD3-CD56bright NK cells was enhanced, while inhibitory receptor NKG2A decreased. Notably, numbers of CD3-CD56bright or NKG2D+CD3-CD56bright NK cells were significantly better restored in patients with HBeAg seroconversion. NK cell activating serum interleukin 15 (IL-15) was significantly increased during LdT treatment, especially in HBeAg seroconverters. LdT significantly enhanced expression of NKG2D and IL-15 in cultures of purified peripheral NK cells from treatment-naïve HBeAg-positive CHB patients.

Conclusions: Functional restoration of CD56bright NK cells via upregulation of IL-15 and NKG2D is a novel activity of LdT and likely other antivirals, independent of its effect on HBV replication. This also demonstrates the importance of host immune restoration in controlling chronic HBV infection.

Keywords: Chronic hepatitis B; IL-15; NKG2D; Natural killer cells; Telbivudine.

MeSH terms

  • Adolescent
  • Adult
  • Alanine Transaminase / blood
  • Antiviral Agents / therapeutic use*
  • DNA, Viral / analysis
  • Female
  • Hepatitis B e Antigens / blood
  • Hepatitis B virus / immunology
  • Hepatitis B, Chronic / blood
  • Hepatitis B, Chronic / drug therapy*
  • Hepatitis B, Chronic / immunology
  • Humans
  • Interleukin-15 / immunology*
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / physiology
  • Male
  • Middle Aged
  • Telbivudine
  • Thymidine / analogs & derivatives*
  • Thymidine / therapeutic use
  • Young Adult

Substances

  • Antiviral Agents
  • DNA, Viral
  • Hepatitis B e Antigens
  • Interleukin-15
  • Telbivudine
  • Alanine Transaminase
  • Thymidine