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References

  1. Chen Y, Lu Y, Lu C, Zhang I. 2009. Beclin-1 expression is a predictor of clinical outcome in patients with esophageal squamous cell carcinoma and correlated to hypoxia-inducible factor (HIF)-1 alpha expression. Pathol. Oncol. Res. 15: 487-493.
    Pubmed PMC CrossRef
  2. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK. 2009. Phosphorylation-driven assembly of RIP1RIP3 complex regulates programmed necrosis and virusinduced inflammation. Cell 137: 1112-1123.
    Pubmed PMC CrossRef
  3. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, et al. 2005. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1: 112-119.
    Pubmed CrossRef
  4. Goldstein P, Kroemer G. 2007. Cell death by necrosis:towards a molecular definition. Trends Biochem. Sci. 32: 37-43.
    Pubmed CrossRef
  5. Hitomi J, Christofferson DE, Ng A, Yao J, Degterev A, Xavier RJ, Yuan J. 2008. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135: 1311-1323.
    Pubmed PMC CrossRef
  6. Jeong KC, Jeong HS, Rhee JH, Lee SE, Chung SS, Starks AM, et al. 2000. Construction and phenotypic evaluation of a Vibrio vulnificus vvpE mutant for elastolytic protease. Infect. Immun. 68: 5096-5106.
    Pubmed PMC CrossRef
  7. Kabeya Y, Mizishima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19: 5720-5728.
    Pubmed PMC CrossRef
  8. Kim WH, Goo SY, Lee K-H, Park S-J. 2009. Vibrio vulnificusinduced cell death of human mononuclear cells requires ROS-dependent activation of p38 and ERK 1/2 MAPKs. Immunol. Invest. 38: 31-48.
    Pubmed CrossRef
  9. Kim WH, Goo SY, Shin MH, Chun S-J, Lee H, Lee K-H, Park S-J. 2008. Vibrio vulnificus-induced death of Jurkat Tcells requires activation of p38 mitogen-activated protein kinase by NADPH oxidase-derived reactive oxygen species. Cell. Immunol. 253: 81-91.
    Pubmed CrossRef
  10. Kroemer G, El-Deiry WW, Golstein P, Peter ME, Vaux D, Vandenabeele P, et al. 2005. Classification of cell death:recommendations of the nomenclature committee on cell death. Cell Death Differ. 12: 1463-1467.
    Pubmed CrossRef
  11. Lee H-J, Kim J-A, Lee M-A, Park S-J, Lee K-H. 2013. Regulation of haemolysin (VvhA) production by ferric uptake regulator (Fur) in Vibrio vulnificus: repression of vvhA transcription by Fur and proteolysis of VvhA by Furrepressive exoproteases. Mol. Microbiol. 88: 813-826.
    Pubmed CrossRef
  12. Lee M-A, Kim J-A, Yang YJ, Shin MY, Park S-J, Lee K-H. 2014. VvpM, an extracellular metalloprotease of Vibrio vulnificus, induces apoptotic death of human cells. J. Microbiol. 52:1036-1043.
    Pubmed CrossRef
  13. Levine B, Kroemer G. 2008. Autophagy in the pathogenesis of disease. Cell 132: 27-42.
    Pubmed PMC CrossRef
  14. Mizushima N, Yoshimori T, Levine B. 2010. Methods in mammalian autophagy research. Cell 140: 313-326.
    Pubmed PMC CrossRef
  15. Modtowy S. 2013. Autophagy and bacterial clearance: a not so clear picture. Cell. Microbiol. 15: 395-402.
    Pubmed PMC CrossRef
  16. Sivridis E, Koukourakis MI, Zois CE, Ledaki I, Ferguson DJ, Harris AL, et al. 2010. LC3A-positive light microscopy detected patterns of autophagy and prognosis in operable breast carcinomas. Am. J. Pathol. 176: 2477-2489.
    Pubmed PMC CrossRef
  17. Sm aili SS, P ereira G J, C osta MM, R ocha KK, R odrigues L , do Carmo LG, et al. 2013. The role of calcium stores in apoptosis and autophagy. Curr. Mol. Med. 13: 252-265.
  18. Strom MS, Paranjpye RN. 2000. Epidemiology and pathogenesis of Vibrio vulnificus. Microbes Infect. 2: 177-188.
    CrossRef
  19. Tanida I, Minematsu-Ikeguchi N, Ueno T, Kominami E. 2005. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1: 84-91.
    Pubmed CrossRef
  20. 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
  21. Wang J. 2008. Beclin 1 bridges autophagy, apoptosis, and differentiation. Autophagy 4: 947-948.
    Pubmed CrossRef
  22. Yoshioka A, Miyata H, Doki Y, Yamasaki M, Sohma I, Gotoh K, et al. 2008. LC3, an autophagosome marker, is highly expressed in gastrointestinal cancers. Int. J. Oncol. 33:461-468.
    Pubmed
  23. Young MM, Kester M, Wang HG. 2013. Sphingolipids:regulators of crosstalk between apoptosis and autophagy. J. Lipid Res. 54: 5-19.
    Pubmed PMC CrossRef
  24. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, et al. 2009. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325: 332-336.
    Pubmed CrossRef

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Article

Note

J. Microbiol. Biotechnol. 2015; 25(2): 302-306

Published online February 28, 2015 https://doi.org/10.4014/jmb.1501.01007

Copyright © The Korean Society for Microbiology and Biotechnology.

VvpM Induces Human Cell Death via Multifarious Modes Including Necroptosis and Autophagy

Mi-Ae Lee 1, Jeong-A Kim 1, Mee-Young Shin 2, Jeong K. Lee 1, Soon-Jung Park 2 and Kyu-Ho Lee 1*

1Department of Life Science, Sogang University, Seoul 121-742, Republic of Korea, 2Department of Environmental Medical Biology, Brain Korea 21 PLUS Project for Medical Science, Yonsei University College of Medicine, Seoul 120-752, Republic of Korea

Received: January 6, 2015; Accepted: January 14, 2015

Abstract

VvpM, one of the extracellular metalloproteases produced by Vibrio vulnificus, induces
apoptotic cell death via a pathway consisting of ERK activation, cytochrome c release, and
activation of caspases-9 and -3. VvpM-treated cells also showed necrotic cell death as stained
by propidium iodide (PI). The percentage of PI-stained cells was decreased by pretreatment
with Necrostatin-1, indicating that VvpM-mediated cell death occurs through necroptosis. The
appearance of autophagic vesicles and lipidated form of light-chain-3B in rVvpM-treated cells
suggests an involvement of autophagy in this process. Therefore, the multifarious action of
VvpM might be one of the factors responsible for V. vulnificus pathogenesis.

Keywords: Vibrio vulnificus, Metalloprotease VvpM, Necroptosis, Autophagy

References

  1. Chen Y, Lu Y, Lu C, Zhang I. 2009. Beclin-1 expression is a predictor of clinical outcome in patients with esophageal squamous cell carcinoma and correlated to hypoxia-inducible factor (HIF)-1 alpha expression. Pathol. Oncol. Res. 15: 487-493.
    Pubmed KoreaMed CrossRef
  2. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK. 2009. Phosphorylation-driven assembly of RIP1RIP3 complex regulates programmed necrosis and virusinduced inflammation. Cell 137: 1112-1123.
    Pubmed KoreaMed CrossRef
  3. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, et al. 2005. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1: 112-119.
    Pubmed CrossRef
  4. Goldstein P, Kroemer G. 2007. Cell death by necrosis:towards a molecular definition. Trends Biochem. Sci. 32: 37-43.
    Pubmed CrossRef
  5. Hitomi J, Christofferson DE, Ng A, Yao J, Degterev A, Xavier RJ, Yuan J. 2008. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135: 1311-1323.
    Pubmed KoreaMed CrossRef
  6. Jeong KC, Jeong HS, Rhee JH, Lee SE, Chung SS, Starks AM, et al. 2000. Construction and phenotypic evaluation of a Vibrio vulnificus vvpE mutant for elastolytic protease. Infect. Immun. 68: 5096-5106.
    Pubmed KoreaMed CrossRef
  7. Kabeya Y, Mizishima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19: 5720-5728.
    Pubmed KoreaMed CrossRef
  8. Kim WH, Goo SY, Lee K-H, Park S-J. 2009. Vibrio vulnificusinduced cell death of human mononuclear cells requires ROS-dependent activation of p38 and ERK 1/2 MAPKs. Immunol. Invest. 38: 31-48.
    Pubmed CrossRef
  9. Kim WH, Goo SY, Shin MH, Chun S-J, Lee H, Lee K-H, Park S-J. 2008. Vibrio vulnificus-induced death of Jurkat Tcells requires activation of p38 mitogen-activated protein kinase by NADPH oxidase-derived reactive oxygen species. Cell. Immunol. 253: 81-91.
    Pubmed CrossRef
  10. Kroemer G, El-Deiry WW, Golstein P, Peter ME, Vaux D, Vandenabeele P, et al. 2005. Classification of cell death:recommendations of the nomenclature committee on cell death. Cell Death Differ. 12: 1463-1467.
    Pubmed CrossRef
  11. Lee H-J, Kim J-A, Lee M-A, Park S-J, Lee K-H. 2013. Regulation of haemolysin (VvhA) production by ferric uptake regulator (Fur) in Vibrio vulnificus: repression of vvhA transcription by Fur and proteolysis of VvhA by Furrepressive exoproteases. Mol. Microbiol. 88: 813-826.
    Pubmed CrossRef
  12. Lee M-A, Kim J-A, Yang YJ, Shin MY, Park S-J, Lee K-H. 2014. VvpM, an extracellular metalloprotease of Vibrio vulnificus, induces apoptotic death of human cells. J. Microbiol. 52:1036-1043.
    Pubmed CrossRef
  13. Levine B, Kroemer G. 2008. Autophagy in the pathogenesis of disease. Cell 132: 27-42.
    Pubmed KoreaMed CrossRef
  14. Mizushima N, Yoshimori T, Levine B. 2010. Methods in mammalian autophagy research. Cell 140: 313-326.
    Pubmed KoreaMed CrossRef
  15. Modtowy S. 2013. Autophagy and bacterial clearance: a not so clear picture. Cell. Microbiol. 15: 395-402.
    Pubmed KoreaMed CrossRef
  16. Sivridis E, Koukourakis MI, Zois CE, Ledaki I, Ferguson DJ, Harris AL, et al. 2010. LC3A-positive light microscopy detected patterns of autophagy and prognosis in operable breast carcinomas. Am. J. Pathol. 176: 2477-2489.
    Pubmed KoreaMed CrossRef
  17. Sm aili SS, P ereira G J, C osta MM, R ocha KK, R odrigues L , do Carmo LG, et al. 2013. The role of calcium stores in apoptosis and autophagy. Curr. Mol. Med. 13: 252-265.
  18. Strom MS, Paranjpye RN. 2000. Epidemiology and pathogenesis of Vibrio vulnificus. Microbes Infect. 2: 177-188.
    CrossRef
  19. Tanida I, Minematsu-Ikeguchi N, Ueno T, Kominami E. 2005. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1: 84-91.
    Pubmed CrossRef
  20. 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
  21. Wang J. 2008. Beclin 1 bridges autophagy, apoptosis, and differentiation. Autophagy 4: 947-948.
    Pubmed CrossRef
  22. Yoshioka A, Miyata H, Doki Y, Yamasaki M, Sohma I, Gotoh K, et al. 2008. LC3, an autophagosome marker, is highly expressed in gastrointestinal cancers. Int. J. Oncol. 33:461-468.
    Pubmed
  23. Young MM, Kester M, Wang HG. 2013. Sphingolipids:regulators of crosstalk between apoptosis and autophagy. J. Lipid Res. 54: 5-19.
    Pubmed KoreaMed CrossRef
  24. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, et al. 2009. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325: 332-336.
    Pubmed CrossRef