Protein kinase F regulates the virulence of Mycobacterium tuberculosis

蛋白激酶F调节结核分枝杆菌的毒力

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Abstract

The serine/threonine protein kinase F (PknF) of Mycobacterium tuberculosis (Mtb) has poorly defined targets and functions but is involved in limiting NLRP3 inflammasome activation in murine macrophages and dendritic cells in vitro . The importance of PknF for the virulence of Mtb in vivo is not known. Here, we demonstrate that the Mtb CDC1551 deletion mutant of pknF ( Δ pknF ) expresses significantly increased levels of the lipid pthiocerol dimycoserosate (PDIM), a polyketide lipid with pro-virulence properties. The Δ pknF mutant strain, when compared to the Mtb and complemented strains, had a 100-fold increase in growth at day 28 and about a 10-fold increase in growth at days 90-98 in the lungs of mice. The increase in pulmonary bacterial loads after infection with Δ pknF strain was conserved even in Nlrp3 -deficient mice, arguing that PknF modulates Mtb virulence independently of NLRP3-inflammasome activation in mice. Staining of lung sections revealed increased inflammation in the lungs of Δ pknF strain-infected mice when compared to Mtb and the complemented mutant strain. Highly susceptible B6.Sst1 (S) mice displayed decreased host resistance with significantly decreased survival when infected with the Δ pknF strain compared to the complemented strain or Mtb. In conclusion, our data suggest that expression of PknF, as a modulator of multiple downstream effector proteins, restricts the virulence of Mtb in the lungs of mice through an NLRP3 inflammasome-independent mechanism but potentially via suppressing expression of the virulence lipid, PDIM. AUTHOR SUMMARY: The human pathogen Mycobacterium tuberculosis (Mtb) encodes 11 serine/threonine protein kinases (Pkn A-I,K and L). In vitro , PknF inhibits activation of innate immune responses in macrophages and dendritic cells. The importance of that protein for the virulence of the bacteria in the context of a live animal infection is unknown. We used a hypersusceptible mouse strain to analyze the impact of deleting the pknF gene on the virulence of the bacteria by monitoring the survival of the mice. We show that the Δ pknF deletion mutant kills mice faster than wild-type bacteria or Δ pknF mutant bacteria expressing a wild-type copy of the pknF gene (Δ pknF -C). Next, we analyzed the growth of the different bacterial strains in the infected mice and demonstrated that at day 28 and day 90-98 timepoints the Δ pknF mutant bacterial strains showed a significant increase in bacterial burden in the lungs, bronchoalveolar lavage fluid and the spleen. An analysis of the total lipids of the bacterial stocks showed that the Δ pknF Mtb bacteria increased expression of the virulence lipid, pthiocerol dimycoserosate (PDIM), suggesting a negative regulation of this lipid by PknF likely affecting bacterial virulence in the lungs of mice.

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