Capsule type defines the capability of Klebsiella pneumoniae in evading Kupffer cell capture in the liver

PLoS Pathog. 2022 Aug 1;18(8):e1010693. doi: 10.1371/journal.ppat.1010693. eCollection 2022 Aug.

Abstract

Polysaccharide capsule is the main virulence factor of K. pneumoniae, a major pathogen of bloodstream infections in humans. While more than 80 capsular serotypes have been identified in K. pneumoniae, only several serotypes are frequently identified in invasive infections. It is documented that the capsule enhances bacterial resistance to phagocytosis, antimicrobial peptides and complement deposition under in vitro conditions. However, the precise role of the capsule in the process of K. pneumoniae bloodstream infections remains to be elucidated. Here we show that the capsule promotes K. pneumoniae survival in the bloodstream by protecting bacteria from being captured by liver resident macrophage Kupffer cells (KCs). Our real-time in vivo imaging revealed that blood-borne acapsular K. pneumoniae mutant is rapidly captured and killed by KCs in the liver sinusoids of mice, whereas, to various extents, encapsulated strains bypass the anti-bacterial machinery in a serotype-dependent manner. Using capsule switched strains, we show that certain high-virulence (HV) capsular serotypes completely block KC's capture, whereas the low-virulence (LV) counterparts confer partial protection against KC's capture. Moreover, KC's capture of the LV K. pneumoniae could be in vivo neutralized by free capsular polysaccharides of homologous but not heterologous serotypes, indicating that KCs specifically recognize the LV capsules. Finally, immunization with inactivated K. pneumoniae enables KCs to capture the HV K. pneumoniae. Together, our findings have uncovered that KCs are the major target cells of K. pneumoniae capsule to promote bacterial survival and virulence, which can be reversed by vaccination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Capsules
  • Humans
  • Klebsiella Infections* / microbiology
  • Klebsiella pneumoniae
  • Kupffer Cells
  • Liver
  • Mice
  • Polysaccharides
  • Sepsis*

Substances

  • Polysaccharides

Grants and funding

This work was supported by grants from National Natural Science Foundation of China 31820103001, 31530082, 81671972, 31728002 (J.-R.Z.) and 3210010245 (J.W.), Tsinghua University Spring Breeze Fund 20201080767 (J.-R.Z.), the China Postdoctoral Science Foundation 2020M680518 (J.W.), the Tsinghua-Peking Joint Center for Life Sciences Postdoctoral Foundation (X.H., J.W.), and grant from Boehringer Ingelheim (J.-R.Z.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.