Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Inhibition of Autolysis by Lipase LipA in Streptococcus pneumoniae Sepsis

  • Kim, Gyu-Lee (School of Pharmacy, Sungkyunkwan University) ;
  • Luong, Truc Thanh (School of Pharmacy, Sungkyunkwan University) ;
  • Park, Sang-Sang (Department of Microbiology, University of Alabama at Birmingham) ;
  • Lee, Seungyeop (School of Pharmacy, Sungkyunkwan University) ;
  • Ha, Jung Ah (School of Pharmacy, Sungkyunkwan University) ;
  • Nguyen, Cuong Thach (School of Pharmacy, Sungkyunkwan University) ;
  • Ahn, Ji Hye (School of Pharmacy, Sungkyunkwan University) ;
  • Park, Ki-Tae (School of Pharmacy, Sungkyunkwan University) ;
  • Paik, Man-Jeong (College of Pharmacy, Sunchon National University) ;
  • Pyo, Suhkneung (School of Pharmacy, Sungkyunkwan University) ;
  • Briles, David E. (Department of Microbiology, University of Alabama at Birmingham) ;
  • Rhee, Dong-Kwon (School of Pharmacy, Sungkyunkwan University)
  • Received : 2017.09.09
  • Accepted : 2017.11.21
  • Published : 2017.12.31
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Abstract

More than 50% of sepsis cases are associated with pneumonia. Sepsis is caused by infiltration of bacteria into the blood via inflammation, which is triggered by the release of cell wall components following lysis. However, the regulatory mechanism of lysis during infection is not well defined. Mice were infected with Streptococcus pneumoniae D39 wild-type (WT) and lipase mutant (${\Delta}lipA$) intranasally (pneumonia model) or intraperitoneally (sepsis model), and survival rate and pneumococcal colonization were determined. LipA and autolysin (LytA) levels were determined by qPCR and western blotting. S. pneumoniae Spd_1447 in the D39 (type 2) strain was identified as a lipase (LipA). In the sepsis model, but not in the pneumonia model, mice infected with the ${\Delta}lipA$ displayed higher mortality rates than did the D39 WT-infected mice. Treatment of pneumococci with serum induced LipA expression at both the mRNA and protein levels. In the presence of serum, the ${\Delta}lipA$ displayed faster lysis rates and higher LytA expression than the WT, both in vitro and in vivo. These results indicate that a pneumococcal lipase (LipA) represses autolysis via inhibition of LytA in a sepsis model.

Keywords

References

  1. Berry, A.M., Lock, R.A., Hansman, D., and Paton, J.C. (1989). Contribution of autolysin to virulence of Streptococcus pneumoniae. Infect. Immun. 57, 2324-2330.
  2. Canvin, J.R., Marvin, A.P., Sivakumaran, M., Paton, J.C., Boulnois, G.J., Andrew, P.W., and Mitchell, T.J. (1995). The role of pneumolysin and autolysin in the pathology of pneumonia and septicemia in mice infected with a type 2 pneumococcus. J. Infect. Dis. 172, 119-123. https://doi.org/10.1093/infdis/172.1.119
  3. Chakravortty, D., Koide, N., Kato, Y., Sugiyama, T., Mu, M.M., Yoshida, T., and Yokochi, T. (2000). The inhibitory action of butyrate on lipopolysaccharide-induced nitric oxide production in RAW 264.7 murine macrophage cells. J. Endotoxin. Res. 6, 243-247. https://doi.org/10.1177/09680519000060030501
  4. Gacser, A., Trofa, D., Schafer, W., and Nosanchuk, J.D. (2007). Targeted gene deletion in Candida parapsilosis demonstrates the role of secreted lipase in virulence. J. Clin Invest. 117, 3049-3058. https://doi.org/10.1172/JCI32294
  5. Gill, S.R., Fouts, D.E., Archer, G.L., Mongodin, E.F., DeBoy, R.T., Ravel, J., Paulsen, I.T., Kolonay, J.F., Brinkac, L., Beanan, M., et al. (2005). Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol. 187, 2426-2438. https://doi.org/10.1128/JB.187.7.2426-2438.2005
  6. Hajaj, B., Yesilkaya, H., Benisty, R., David, M., Andrew, P.W., and Porat, N. (2012). Thiol peroxidase is an important component of Streptococcus pneumoniae in oxygenated environments. Infect. Immun. 80, 4333-4343. https://doi.org/10.1128/IAI.00126-12
  7. Hirst, R.A., Gosai, B., Rutman, A., Guerin, C.J., Nicotera, P., Andrew, P.W., and O'Callaghan, C. (2008). Streptococcus pneumoniae deficient in pneumolysin or autolysin has reduced virulence in meningitis. J. Infect Dis. 197, 744-751. https://doi.org/10.1086/527322
  8. Jorgensen, S., Skov, K.W., and Diderichsen, B. (1991). Cloning, sequence, and expression of a lipase gene from Pseudomonas cepacia: lipase production in heterologous hosts requires two Pseudomonas genes. J. Bacteriol. 173, 559-567. https://doi.org/10.1128/jb.173.2.559-567.1991
  9. Jaeger, K.-E., Ransac, S., Dijkstra, B.W., Colson, C., van Heuvel, M., and Misset, O. (1994). Bacterial lipases. FEMS Microbiol. Rev. 15, 29-63. https://doi.org/10.1111/j.1574-6976.1994.tb00121.x
  10. Joseph, B., Ramteke, P.W., and Thomas, G. (2008). Cold active microbial lipases: some hot issues and recent developments. Biotechnol. Adv. 26, 457-470. https://doi.org/10.1016/j.biotechadv.2008.05.003
  11. Kadioglu, A., Weiser, J.N., Paton, J.C., and Andrew, P.W. (2008). The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Micro. 6, 288-301. https://doi.org/10.1038/nrmicro1871
  12. Kang, N.-S., Park, S.-Y., Lee, K.-R., Lee, S.-M., Lee, B.-G., Shin, D.-H., and Pyo, S. (2002). Modulation of macrophage function activity by ethanolic extract of larvae of Holotrichia diomphalia. J. Ethnopharmacol. 79, 89-94. https://doi.org/10.1016/S0378-8741(01)00369-5
  13. Kerttula, Y., and Weber, T. (1987). Serum lipids in pneumonia of different aetiology. Ann. Clin. Res. 20, 184-188.
  14. Kwon, H.-Y., Kim, S.-W., Choi, M.-H., Ogunniyi, A.D., Paton, J.C., Park, S.-H., Pyo, S.-N., and Rhee, D.-K. (2003). Effect of heat shock and mutations in ClpL and ClpP on virulence gene expression in Streptococcus pneumoniae. Infect. Immun. 71, 3757-3765. https://doi.org/10.1128/IAI.71.7.3757-3765.2003
  15. Lanie, J.A., Ng, W.-L., Kazmierczak, K.M., Andrzejewski, T.M., Davidsen, T.M., Wayne, K.J., Tettelin, H., Glass, J.I., and Winkler, M.E. (2007). Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J. Bacteriol. 189, 38-51. https://doi.org/10.1128/JB.01148-06
  16. Liu, L., Johnson, H.L., Cousens, S., Perin, J., Scott, S., Lawn, J.E., Rudan, I., Campbell, H., Cibulskis, R., and Li, M. (2012). Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. The Lancet 379, 2151-2161. https://doi.org/10.1016/S0140-6736(12)60560-1
  17. Lopez, R., and Garcia, E. (2004). Recent trends on the molecular biology of pneumococcal capsules, lytic enzymes, and bacteriophage. FEMS Microbiol. Rev. 28, 553-580. https://doi.org/10.1016/j.femsre.2004.05.002
  18. Luong, T.T., Kim, E.-H., Bak, J.P., Nguyen, C.T., Choi, S., Briles, D.E., Pyo, S., and Rhee, D.-K. (2015). Ethanol-induced alcohol dehydrogenase E (AdhE). potentiates pneumolysin in Streptococcus pneumoniae. Infect. Immun. 83, 108-119. https://doi.org/10.1128/IAI.02434-14
  19. Martin, G.S. (2012). Sepsis, severe sepsis and septic shock: changes in incidence, pathogens and outcomes. Expert Rev. Anti Infect. Ther. 10, 701-706. https://doi.org/10.1586/eri.12.50
  20. Maslowski, K.M., Vieira, A.T., Ng, A., Kranich, J., Sierro, F., Di, Y., Schilter, H.C., Rolph, M.S., Mackay, F., Artis, D., et al. (2009). Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461, 1282-1286. https://doi.org/10.1038/nature08530
  21. Mellroth, P., Daniels, R., Eberhardt, A., Ronnlund, D., Blom, H., Widengren, J., Normark, S., and Henriques-Normark, B. (2012). LytA, major autolysin of Streptococcus pneumoniae, requires access to nascent peptidoglycan. J. Biol. Chem. 287, 11018-11029. https://doi.org/10.1074/jbc.M111.318584
  22. Munford, R., and Suffredini, A. (2009). Sepsis, severe sepsis, and septic shock; in Principles and practice of infectious diseases. 7th ed. (Philadelphia: Churchill Livingstone).
  23. Nawabi, P., Catron, D.M., and Haldar, K. (2008). Esterification of cholesterol by a type III secretion effector during intracellular Salmonella infection. Mol. Microbiol .68, 173-185. https://doi.org/10.1111/j.1365-2958.2008.06142.x
  24. Nguyen, C.T., Kim, E.-H., Luong, T.T., Pyo, S., and Rhee, D.-K. (2014). ATF3 confers resistance to pneumococcal infection through positive regulation of cytokine production. J. Infect. Dis. 210, 1745-1754. https://doi.org/10.1093/infdis/jiu352
  25. Orihuela, C.J., Gao, G., Francis, K.P., Yu, J., and Tuomanen, E.I. (2004). Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J. Infect. Dis. 190, 1661-1669. https://doi.org/10.1086/424596
  26. Park, J.-S., Lee, E.-J., Lee, J.-C., Kim, W.-K., and Kim, H.-S. (2007). Anti-inflammatory effects of short chain fatty acids in IFN-${\gamma}$-stimulated RAW 264.7 murine macrophage cells: Involvement of NF-${\kappa}B$ and ERK signaling pathways. Int. Immunopharmacol. 7, 70-77. https://doi.org/10.1016/j.intimp.2006.08.015
  27. Pemberton, J.M., Kidd, S.P., and Schmidt, R. (1997). Secreted enzymes of Aeromonas. FEMS Microbiol. Lett. 152, 1-10. https://doi.org/10.1111/j.1574-6968.1997.tb10401.x
  28. Pinsirodom, P., and Parkin, K.L. (2001). Lipase Assays; in Current protocols in food analytical chemistry. Unit C3.1.1-C3.1.13 (John Wiley & Sons, Inc.).
  29. Rollof, J., and Normark, S. (1992). In vivo processing of Staphylococcus aureus lipase. J. Bacteriol. 174, 1844-1847. https://doi.org/10.1128/jb.174.6.1844-1847.1992
  30. Rollof, J., HedstrOM, S.A., and Nilsson-Ehle, P. (1987). Lipolytic activity of Staphylococcus aureus strains from disseminated and localized infections. APMIS 95B, 109-113.
  31. Rollof, J., Braconier, J.H., Soderstrom, C., and Nilsson-Ehle, P. (1988). Interference of Staphylococcus aureus lipase with human granulocyte function. Eur. J. Clin. Microbiol. Infect Dis. 7, 505-510. https://doi.org/10.1007/BF01962601
  32. Stehr, F., Felk, A., Gacser, A., Kretschmar, M., Mahn$\ss$, B., Neuber, K., Hube, B., and Schafer, W. (2004). Expression analysis of the Candida albicans lipase gene family during experimental infections and in patient samples1. FEMS Yeast Res. 4, 401-408. https://doi.org/10.1016/S1567-1356(03)00205-8
  33. Stratton, C.W., Evans, M.E., Burch, D.J., Hawley, H.B., Horsman, T.A., Tu, K.K., and Reller, L.B. (1986). Effect of human serum on inhibition of growth of Staphylococcus aureus by antimicrobial agents. Eur. J. Clin. Microbiol. 5, 351-353. https://doi.org/10.1007/BF02017797
  34. Tran, T.D.-H., Kwon, H.-Y., Kim, E.-H., Kim, K.-W., Briles, D.E., Pyo, S., and Rhee, D.-K. (2011). Decrease in penicillin susceptibility due to heat shock protein ClpL in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 55, 2714-2728. https://doi.org/10.1128/AAC.01383-10
  35. Vinolo, M., Rodrigues, H., Hatanaka, E., Hebeda, C., Farsky, S., and Curi, R. (2009). Short-chain fatty acids stimulate the migration of neutrophils to inflammatory sites. Clin. Sci. (Lond). 117, 331-338. https://doi.org/10.1042/CS20080642
  36. Voigt, C., von Scheidt, B., Gacser, A., Kassner, H., Lieberei, R., Schafer, W., and Salomon, S. (2007). Enhanced mycotoxin production of a lipase-deficient Fusarium graminearum mutant correlates to toxinrelated gene expression. Eur. J. Plant Pathol. 117, 1-12. https://doi.org/10.1007/s10658-006-9063-y
  37. Waldecker, M., Kautenburger, T., Daumann, H., Busch, C., and Schrenk, D. (2008). Inhibition of histone-deacetylase activity by shortchain fatty acids and some polyphenol metabolites formed in the colon. J. Nutr. Biochem. 19, 587-593. https://doi.org/10.1016/j.jnutbio.2007.08.002
  38. Yang, G., Hernandez-Rodriguez, C.S., Beeton, M.L., Wilkinson, P., and Waterfield, N.R. (2012). Pdl1 is a putative lipase that enhances Photorhabdus toxin complex secretion. PLoS Pathog. 8, e1002692. https://doi.org/10.1371/journal.ppat.1002692

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