A bacterial RTX toxin causes programmed necrotic cell death through calcium-mediated mitochondrial dysfunction

Journal of Infectious Diseases

Volumn 207, Issue 9, 2013, Pages 1406-1415

  Kim, Young Ran ^a,f   Lee, Shee Eun ^a,c,d   Kang, In Chol ^e   Nam, Kwang Il ^a   Choy, Hyon E ^a,c   Rhee, Joon Haeng ^a,b,c  

^a Chonnam National University Medical School   (South Korea)

^b National Research Laboratory of Molecular Microbial Pathogenesis   (South Korea)

^c Genome Research Center for Enteropathogenic Bacteria   (South Korea)

^d Seoul National University   (South Korea)

^e Chonnam National University   (South Korea)

^f Dongshin University   (South Korea)

Author keywords

calcium; JNK; mitochondria; programmed necrotic cell death; RTX toxin

Indexed keywords

ADENOSINE DEAMINASE; BACTERIAL TOXIN; MITOGEN ACTIVATED PROTEIN KINASE P38; RTXA1 TOXIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL VIABILITY; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY TEST; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HELA CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VIBRIO VULNIFICUS;

ADENOSINE TRIPHOSPHATE; APOPTOSIS; BACTERIAL TOXINS; CALCIUM; CYTOTOXINS; EPITHELIAL CELLS; HELA CELLS; HUMANS; IMMUNOBLOTTING; MICROSCOPY, CONFOCAL; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PROTEIN TRANSPORT; VIBRIO VULNIFICUS;

EID: 84875998824     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jis746     Document Type: Article

References (28)

1. Burns DL, Barbieri JT, Iglewski BH, Rappuoli R. Bacterial protein toxins. Washington, DC: ASM Press, 2003.
2. Welch RA. RTX toxin structure and function: a story of numerous anomalies and few analogies in toxin biology. Curr Top Microbiol Immunol 2001; 257:85-111. (Pubitemid 32230026)
3. Lin W, Fullner KJ, Clayton R, et al. Identification of a Vibrio cholerae RTX toxin gene cluster that is tightly linked to the cholera toxin prophage. Proc Natl Acad Sci USA 1999; 96:1071-6. (Pubitemid 29072185)
4. Kim YR, Lee SE, Kook H, et al. Vibrio vulnificus RTX toxin kills host cells only after contact of the bacteria with host cells. Cell Microbiol 2008; 10:848-62. (Pubitemid 351386941)
5. Lupardus PJ, Shen A, Bogyo M, Garcia KC. Small molecule-induced allosteric activation of the Vibrio cholerae RTX cysteine protease domain. Science 2008; 322:265-8.
6. Prochazkova K, Satchell KJ. Structure-function analysis of inositol hexakisphosphate-induced autoprocessing of the Vibrio cholerae multifunctional autoprocessing RTX toxin. J Biol Chem 2008; 283:23656-64.
7. Egerer M, Satchell KJ. Inositol hexakisphosphate-induced autoprocessing of large bacterial protein toxins. PLoS Pathog 2010; 6:e1000942.
8. Satchell KJ. MARTX, multifunctional autoprocessing repeats-in-toxin toxins. Infect Immun 2007; 75:5079-84. (Pubitemid 350033594)
9. Kudryashov DS, Cordero CL, Reisler E, Satchell KJ. Characterization of the enzymatic activity of the actin cross-linking domain from the Vibrio cholerae MARTX Vc toxin. J Biol Chem 2008; 283:445-52.
10. Lee S, Kim YR, Lee JY, Rhee JH, Park CS, Kim DY. Dynamic analysis of pathogen-infected host cells using quantitative phase microscopy. J Biomed Opt 2011; 16:036004.
11. Lo HR, Lin JH, Chen YH, et al. RTX toxin enhances the survival of Vibrio vulnificus during infection by protecting the organism from phagocytosis. J Infect Dis 2011; 203:1866-74.
12. Jeong HG, Satchell KJ. Additive function of Vibrio vulnificus MARTX (Vv) and VvhA cytolysins promotes rapid growth and epithelial tissue necrosis during intestinal infection. PLoS Pathog 2012; 8:e1002581.
13. Lee BC, Choi SH, Kim TS. Vibrio vulnificus RTX toxin plays an important role in the apoptotic death of human intestinal epithelial cells exposed to Vibrio vulnificus. Microbes Infect 2008; 10:1504-13.
14. Xing JZ, Zhu L, Jackson JA, et al. Dynamic monitoring of cytotoxicity on microelectronic sensors. Chem Res Toxicol 2005; 18:154-61. (Pubitemid 40256233)
15. Dhakal BK, Lee W, Kim YR, Choy HE, Ahnn J, Rhee JH. Caenorhabditis elegans as a simple model host for Vibrio vulnificus infection. Biochem Biophys Res Commun 2006; 346:751-7. (Pubitemid 43949256)
16. Kim YR, Kim BU, Kim SY, et al. Outer membrane vesicles of Vibrio vulnificus deliver cytolysin-hemolysin VvhA into epithelial cells to induce cytotoxicity. Biochem Biophys Res Commun 2010; 399:607-12.
17. Kim YR, Lee SE, Kim CM, et al. Characterization and pathogenic significance of Vibrio vulnificus antigens preferentially expressed in septicemic patients. Infect Immun 2003; 71:5461-71. (Pubitemid 37205596)
18. Osicka R, Prochazkova K, Sulc M, Linhartova I, Havlicek V, Sebo P. A novel "clip-and-link" activity of repeat in toxin (RTX) proteins from gram-negative pathogens. Covalent protein cross-linking by an Asp-Lys isopeptide bond upon calcium-dependent processing at an Asp-Pro bond. J Biol Chem 2004; 279:24944-56. (Pubitemid 38756742)
19. Kim WH, Goo SY, Lee KH, Park SJ. Vibrio vulnificus-induced cell death of human mononuclear cells requires ROS-dependent activation of p38 and ERK 1/2 MAPKs. Immunol Invest 2009; 38:31-48.
20. Korzeniewski C, Callewaert DM. An enzyme-release assay for natural cytotoxicity. J Immunol Methods 1983; 64:313-20. (Pubitemid 14243095)
21. Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 2005; 73:1907-16. (Pubitemid 40470787)
22. Festjens N, Vanden Berghe T, Vandenabeele P. Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta 2006; 1757:1371-87. (Pubitemid 44472550)
23. Golstein P, Kroemer G. Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 2007; 32:37-43. (Pubitemid 46043552)
24. Kennedy CL, Smith DJ, Lyras D, Chakravorty A, Rood JI. Programmed cellular necrosis mediated by the pore-forming alpha-toxin from Clostridium septicum. PLoS Pathog 2009; 5:e1000516.
25. Chung KJ, Cho EJ, Kim MK, et al. RtxA1-induced expression of the small GTPase Rac2 plays a key role in the pathogenicity of Vibrio vulnificus. J Infect Dis 2010; 201:97-105.
26. Patel VJ, Gardner E, Burton CS. Vibrio vulnificus septicemia and leg ulcer. J Am Acad Dermatol 2002; 46:S144-5.
27. Park SD, Shon HS, Joh NJ. Vibrio vulnificus septicemia in Korea: clinical and epidemiologic findings in seventy patients. J Am Acad Dermatol 1991; 24:397-403.
28. Tsai YH, Huang TJ, Hsu RW, et al. Necrotizing soft-tissue infections and primary sepsis caused by Vibrio vulnificus and Vibrio cholerae non-O1. J Trauma 2009; 66:899-905.