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References

  1. Abdul-Sater AA, Saïd-Sadier N, Lam VM, Singh B, Pettengill MA, Soares F, et al. 2010. Enhancement of reactive oxygen species production and chlamydial infection by the mitochondrial Nod-like family member NLRX1. J. Biol. Chem. 285: 41637-41645.
    Pubmed PMC CrossRef
  2. Al-Younes HM, Brinkmann V, Meyer TF. 2004. Interaction of Chlamydia trachomatis serovar L2 with the host autophagic pathway. Infect. Immun. 72: 4751-4762.
    Pubmed PMC CrossRef
  3. Al-Zeer MA, Al-Younes HM, Braun PR, Zerrahn J, Meyer TF. 2009. IFN-gamma-inducible Irga6 mediates host resistance against Chlamydia trachomatis v ia a utophagy . PLoS One 4:e4588.
    Pubmed PMC CrossRef
  4. Beatty WL. 2007. Lysosome repair enables host cell survival and bacterial persistence following Chlamydia trachomatis infection. Cell Microbiol. 9: 2141-2152.
    Pubmed CrossRef
  5. Brojatsch J, Lima H, Kar AK, Jacobson LS, Muehlbauer SM, Chandran K, et al. 2014. A proteolytic cascade controls lysosome rupture and necrotic cell death mediated by lysosome-destabilizing adjuvants. PLoS One 9: e95032.
    Pubmed PMC CrossRef
  6. Byrne GI, Ojcius DM. 2004. Chlamydia and apoptosis: life and death decisions of an intracellular pathogen. Nat. Rev. Microbiol. 2: 802-808.
    Pubmed CrossRef
  7. Chen Y, Azad MB, Gibson SB. 2010. Methods for detecting autophagy and determining autophagy-induced cell death. Can. J. Physiol. Pharmacol. 88: 285-295.
    Pubmed CrossRef
  8. Du K, Cheng XL, Zhou M, Li Q. 2013. Chlamydia inhibit host cell apoptosis by inducing Bag-1 via the MAPK/ERK survival pathway. Apoptosis 18: 1083-1092.
    Pubmed CrossRef
  9. Eno CO, Zhao GP, Venkatanarayan A, Wang B, Flores ER, Li C. 2013. Noxa couples lysosomal membrane permeabilization and apoptosis during oxidative stress. Free Radic. Biol. Med. 65: 26-37.
    Pubmed PMC CrossRef
  10. Fan T , Lu H, Hu H , Shi L, McClarty GA, N ance DM, et al. 1998. Inhibition of apoptosis in Chlamydia-infected cells:blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med. 187: 487-496.
    Pubmed PMC CrossRef
  11. Fischer SF, Schwarz C, Vier J, Hacker G. 2001. Characterization of anti-apoptotic activities of Chlamydia pneumoniae in human cells. Infect. Immun. 69: 7121-7129.
    Pubmed PMC CrossRef
  12. Gao LY, Kwaik YA. 2000. The modulation of host cell apoptosis by intracellular bacterial pathogens. Trends Microbiol. 8: 306-313.
    CrossRef
  13. Han J, Zhong CQ, Zhang DW. 2011. Programmed necrosis:backup to and competitor with apoptosis in the immune system. Nat. Immunol. 12: 1143-1149.
    Pubmed CrossRef
  14. Johansson AC, Appelqvist H, Nilsson C, Kågedal K, Roberg K, Ollinger K. 2010. Regulation of apoptosis-associated lysosomal membrane permeabilization. Apoptosis 15: 527-540.
    Pubmed PMC CrossRef
  15. Jungas T, Verbeke P, Darville T, Ojcius DM. 2004. Cell death, BAX activation, and HMGB1 release during infection with Chlamydia. Microbes Infect. 6: 1145-1155.
    Pubmed CrossRef
  16. Kirkegaard T, Jaattela M. 2009. Lysosomal involvement in cell death and cancer. Biochim. Biophys. Acta 1793: 746-754.
    Pubmed CrossRef
  17. Ling LU, Tan KB, Lin H, Chiu GN. 2011. The role of reactive oxygen species and autophagy in safingol-induced cell death. Cell Death Dis. 2: e129.
    Pubmed PMC CrossRef
  18. Mihalik R, Imre G, Petak I, Szende B, Kopper L. 2004. Cathepsin B-independent abrogation of cell death by CA074-OMe upstream of lysosomal breakdown. Cell Death Differ. 11: 1357-1360.
    Pubmed CrossRef
  19. Morgan MJ, Kim YS, Liu ZG. 2008. TNF alpha and reactive oxygen species in necrotic cell death. Cell Res. 18: 343-349.
    Pubmed CrossRef
  20. Nohl H, Gille L. 2005. Lysosomal ROS formation. Redox Rep. 10:199-205.
    Pubmed CrossRef
  21. Nunes A, Gomes JP. 2014. Evolution, phylogeny, and molecular epidemiology of Chlamydia. Infect. Genet. Evol. 23: 49-64.
    Pubmed CrossRef
  22. Ouellette SP, Dorsey FC, Moshiach S, Cleveland JL, Carabeo RA. 2011. Chlamydia species-dependent differences in the growth requirement for lysosomes. PLoS One 6: e16783.
    Pubmed PMC CrossRef
  23. Pachikara N, Zhang H, Pan Z, Jin S, Fan H. 2009. Productive Chlamydia trachomatis lymphogranuloma venereum 434 infection in cells with augmented or inactivated autophagic activities. FEMS Microbiol. Lett. 292: 240-249.
    Pubmed PMC CrossRef
  24. Sawai H, Domae N. 2011. Discrimination between primary necrosis and apoptosis by necrostatin-1 in Annexin Vpositive/propidium iodide-negative cells. Biochem. Biophys. Res. Commun. 411: 569-573.
    Pubmed CrossRef
  25. Scaffidi P, Misteli T, Bianchi ME. 2002. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195.
    Pubmed CrossRef
  26. Sun HS, Eng EW, Jeganathan S, Sin AT, Patel PC, Gracey E, et al. 2012. Chlamydia trachomatis vacuole maturation in infected macrophages. J. Leukoc. Biol. 92: 815-827.
    Pubmed PMC CrossRef
  27. Tanida I, Ueno T, Kominami E. 2008. LC3 and autophagy. Methods Mol. Biol. 445: 77-88.
    Pubmed CrossRef
  28. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. 2010. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 11: 700-714.
    Pubmed CrossRef
  29. Vanden Berghe T, Vanlangenakker N, Parthoens E, Deckers W, Devos M, Festjens N, et al. 2010. Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ. 17: 922-930.
    Pubmed CrossRef
  30. Verzola D, Ratto E, Villaggio B, Parodi EL, Pontremoli R, Garibotto G, Viazzi F. 2014. Uric acid promotes apoptosis in human proximal tubule cells by oxidative stress and the activation of NADPH oxidase NOX 4. PLoS One 9: e115210.
    Pubmed PMC CrossRef
  31. Wang JS, Wu D, Huang DY, Lin WW. 2015. TAK1 inhibition-induced RIP1-dependent apoptosis in murine macrophages relies on constitutive TNF-α signaling and ROS production. J. Biomed. Sci. 22: 76.
    Pubmed PMC CrossRef
  32. Waring P. 2005. Redox active calcium ion channels and cell death. Arch. Biochem. Biophys. 434: 33-42.
    Pubmed CrossRef
  33. Weinrauch Y, Zychlinsky A. 1999. The induction of apoptosis by bacterial pathogens. Annu. Rev. Microbiol. 53: 155-187.
    Pubmed CrossRef
  34. Wei X, Shao B, He Z, Ye T, Luo M, Sang Y, et al. 2015. Cationic nanocarriers induce cell necrosis through impairment of Na+/K+-ATPase and cause subsequent inflammatory response. Cell Res. 25: 237-253.
    Pubmed PMC CrossRef
  35. Ying S, Pettengill M, Ojcius DM, Häcker G. 2007. Host-cell survival and death during Chlamydia infection. Curr. Immunol. Rev. 3: 31-40.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(4): 790-798

Published online April 28, 2016 https://doi.org/10.4014/jmb.1510.10082

Copyright © The Korean Society for Microbiology and Biotechnology.

Involvement of Lysosome Membrane Permeabilization and Reactive Oxygen Species Production in the Necrosis Induced by Chlamydia muridarum Infection in L929 Cells

Lixiang Chen 1, Cong Wang 1, Shun Li 1, Xin Yu 1, Xue Liu 1, Rongrong Ren 1, Wenwen Liu 2, Xiaojing Zhou 3, Xiaonan Zhang 1 and Xiaohui Zhou 1*

1Shanghai Public Health Clinical Center, Key Laboratory of Medical Molecular Virology, MOE/MOH, Fudan Univeristy, Shanghai 201508, P.R. China, 2Affiliated Hospital of Chifeng University, Chifeng 024000, P.R. China, 3The First Affiliated Hospital of Bengbu Medical College, Bengbu 233004, P.R. China

Received: October 23, 2015; Accepted: January 29, 2016

Abstract

Chlamydiae, obligate intracellular bacteria, are associated with a variety of human diseases.
The chlamydial life cycle undergoes a biphasic development: replicative reticulate bodies
(RBs) phase and infectious elementary bodies (EBs) phase. At the end of the chlamydial
intracellular life cycle, EBs have to be released to the surrounded cells. Therefore, the
interactions between Chlamydiae and cell death pathways could greatly influence the
outcomes of Chlamydia infection. However, the underlying molecular mechanisms remain
elusive. Here, we investigated host cell death after Chlamydia infection in vitro, in L929 cells,
and showed that Chlamydia infection induces cell necrosis, as detected by the propidium
iodide (PI)-Annexin V double-staining flow-cytometric assay and Lactate dehydrogenase
(LDH) release assay. The production of reactive oxygen species (ROS), an important factor in
induction of necrosis, was increased after Chlamydia infection, and inhibition of ROS with
specific pharmacological inhibitors, diphenylene iodonium (DPI) or butylated hydroxyanisole
(BHA), led to significant suppression of necrosis. Interestingly, live-cell imaging revealed that
Chlamydia infection induced lysosome membrane permeabilization (LMP). When an inhibitor
upstream of LMP, CA-074-Me, was added to cells, the production of ROS was reduced with
concomitant inhibition of necrosis. Taken together, our results indicate that Chlamydia
infection elicits the production of ROS, which is dependent on LMP at least partially, followed
by induction of host-cell necrosis. To our best knowledge, this is the first live-cell-imaging
observation of LMP post Chlamydia infection and report on the link of LMP to ROS to necrosis
during Chlamydia infection.

Keywords: Chlamydia, Necrosis, Lysosome Membrane Permeabilization, Reactive Oxygen Species Production

References

  1. Abdul-Sater AA, Saïd-Sadier N, Lam VM, Singh B, Pettengill MA, Soares F, et al. 2010. Enhancement of reactive oxygen species production and chlamydial infection by the mitochondrial Nod-like family member NLRX1. J. Biol. Chem. 285: 41637-41645.
    Pubmed KoreaMed CrossRef
  2. Al-Younes HM, Brinkmann V, Meyer TF. 2004. Interaction of Chlamydia trachomatis serovar L2 with the host autophagic pathway. Infect. Immun. 72: 4751-4762.
    Pubmed KoreaMed CrossRef
  3. Al-Zeer MA, Al-Younes HM, Braun PR, Zerrahn J, Meyer TF. 2009. IFN-gamma-inducible Irga6 mediates host resistance against Chlamydia trachomatis v ia a utophagy . PLoS One 4:e4588.
    Pubmed KoreaMed CrossRef
  4. Beatty WL. 2007. Lysosome repair enables host cell survival and bacterial persistence following Chlamydia trachomatis infection. Cell Microbiol. 9: 2141-2152.
    Pubmed CrossRef
  5. Brojatsch J, Lima H, Kar AK, Jacobson LS, Muehlbauer SM, Chandran K, et al. 2014. A proteolytic cascade controls lysosome rupture and necrotic cell death mediated by lysosome-destabilizing adjuvants. PLoS One 9: e95032.
    Pubmed KoreaMed CrossRef
  6. Byrne GI, Ojcius DM. 2004. Chlamydia and apoptosis: life and death decisions of an intracellular pathogen. Nat. Rev. Microbiol. 2: 802-808.
    Pubmed CrossRef
  7. Chen Y, Azad MB, Gibson SB. 2010. Methods for detecting autophagy and determining autophagy-induced cell death. Can. J. Physiol. Pharmacol. 88: 285-295.
    Pubmed CrossRef
  8. Du K, Cheng XL, Zhou M, Li Q. 2013. Chlamydia inhibit host cell apoptosis by inducing Bag-1 via the MAPK/ERK survival pathway. Apoptosis 18: 1083-1092.
    Pubmed CrossRef
  9. Eno CO, Zhao GP, Venkatanarayan A, Wang B, Flores ER, Li C. 2013. Noxa couples lysosomal membrane permeabilization and apoptosis during oxidative stress. Free Radic. Biol. Med. 65: 26-37.
    Pubmed KoreaMed CrossRef
  10. Fan T , Lu H, Hu H , Shi L, McClarty GA, N ance DM, et al. 1998. Inhibition of apoptosis in Chlamydia-infected cells:blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med. 187: 487-496.
    Pubmed KoreaMed CrossRef
  11. Fischer SF, Schwarz C, Vier J, Hacker G. 2001. Characterization of anti-apoptotic activities of Chlamydia pneumoniae in human cells. Infect. Immun. 69: 7121-7129.
    Pubmed KoreaMed CrossRef
  12. Gao LY, Kwaik YA. 2000. The modulation of host cell apoptosis by intracellular bacterial pathogens. Trends Microbiol. 8: 306-313.
    CrossRef
  13. Han J, Zhong CQ, Zhang DW. 2011. Programmed necrosis:backup to and competitor with apoptosis in the immune system. Nat. Immunol. 12: 1143-1149.
    Pubmed CrossRef
  14. Johansson AC, Appelqvist H, Nilsson C, Kågedal K, Roberg K, Ollinger K. 2010. Regulation of apoptosis-associated lysosomal membrane permeabilization. Apoptosis 15: 527-540.
    Pubmed KoreaMed CrossRef
  15. Jungas T, Verbeke P, Darville T, Ojcius DM. 2004. Cell death, BAX activation, and HMGB1 release during infection with Chlamydia. Microbes Infect. 6: 1145-1155.
    Pubmed CrossRef
  16. Kirkegaard T, Jaattela M. 2009. Lysosomal involvement in cell death and cancer. Biochim. Biophys. Acta 1793: 746-754.
    Pubmed CrossRef
  17. Ling LU, Tan KB, Lin H, Chiu GN. 2011. The role of reactive oxygen species and autophagy in safingol-induced cell death. Cell Death Dis. 2: e129.
    Pubmed KoreaMed CrossRef
  18. Mihalik R, Imre G, Petak I, Szende B, Kopper L. 2004. Cathepsin B-independent abrogation of cell death by CA074-OMe upstream of lysosomal breakdown. Cell Death Differ. 11: 1357-1360.
    Pubmed CrossRef
  19. Morgan MJ, Kim YS, Liu ZG. 2008. TNF alpha and reactive oxygen species in necrotic cell death. Cell Res. 18: 343-349.
    Pubmed CrossRef
  20. Nohl H, Gille L. 2005. Lysosomal ROS formation. Redox Rep. 10:199-205.
    Pubmed CrossRef
  21. Nunes A, Gomes JP. 2014. Evolution, phylogeny, and molecular epidemiology of Chlamydia. Infect. Genet. Evol. 23: 49-64.
    Pubmed CrossRef
  22. Ouellette SP, Dorsey FC, Moshiach S, Cleveland JL, Carabeo RA. 2011. Chlamydia species-dependent differences in the growth requirement for lysosomes. PLoS One 6: e16783.
    Pubmed KoreaMed CrossRef
  23. Pachikara N, Zhang H, Pan Z, Jin S, Fan H. 2009. Productive Chlamydia trachomatis lymphogranuloma venereum 434 infection in cells with augmented or inactivated autophagic activities. FEMS Microbiol. Lett. 292: 240-249.
    Pubmed KoreaMed CrossRef
  24. Sawai H, Domae N. 2011. Discrimination between primary necrosis and apoptosis by necrostatin-1 in Annexin Vpositive/propidium iodide-negative cells. Biochem. Biophys. Res. Commun. 411: 569-573.
    Pubmed CrossRef
  25. Scaffidi P, Misteli T, Bianchi ME. 2002. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195.
    Pubmed CrossRef
  26. Sun HS, Eng EW, Jeganathan S, Sin AT, Patel PC, Gracey E, et al. 2012. Chlamydia trachomatis vacuole maturation in infected macrophages. J. Leukoc. Biol. 92: 815-827.
    Pubmed KoreaMed CrossRef
  27. Tanida I, Ueno T, Kominami E. 2008. LC3 and autophagy. Methods Mol. Biol. 445: 77-88.
    Pubmed CrossRef
  28. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. 2010. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 11: 700-714.
    Pubmed CrossRef
  29. Vanden Berghe T, Vanlangenakker N, Parthoens E, Deckers W, Devos M, Festjens N, et al. 2010. Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ. 17: 922-930.
    Pubmed CrossRef
  30. Verzola D, Ratto E, Villaggio B, Parodi EL, Pontremoli R, Garibotto G, Viazzi F. 2014. Uric acid promotes apoptosis in human proximal tubule cells by oxidative stress and the activation of NADPH oxidase NOX 4. PLoS One 9: e115210.
    Pubmed KoreaMed CrossRef
  31. Wang JS, Wu D, Huang DY, Lin WW. 2015. TAK1 inhibition-induced RIP1-dependent apoptosis in murine macrophages relies on constitutive TNF-α signaling and ROS production. J. Biomed. Sci. 22: 76.
    Pubmed KoreaMed CrossRef
  32. Waring P. 2005. Redox active calcium ion channels and cell death. Arch. Biochem. Biophys. 434: 33-42.
    Pubmed CrossRef
  33. Weinrauch Y, Zychlinsky A. 1999. The induction of apoptosis by bacterial pathogens. Annu. Rev. Microbiol. 53: 155-187.
    Pubmed CrossRef
  34. Wei X, Shao B, He Z, Ye T, Luo M, Sang Y, et al. 2015. Cationic nanocarriers induce cell necrosis through impairment of Na+/K+-ATPase and cause subsequent inflammatory response. Cell Res. 25: 237-253.
    Pubmed KoreaMed CrossRef
  35. Ying S, Pettengill M, Ojcius DM, Häcker G. 2007. Host-cell survival and death during Chlamydia infection. Curr. Immunol. Rev. 3: 31-40.
    Pubmed KoreaMed CrossRef