Reactive oxygen species and the MEK/ERK pathway are involved in the toxicity of clostridium perfringens-toxin, a prototype bacterial phospholipase C

Journal of Infectious Diseases

Volumn 206, Issue 8, 2012, Pages 1218-1226

  Monturiol Gross, Laura ^a   Flores Díaz, Marietta ^a   Araya Castillo, Cindy ^a   Pineda Padilla, María José ^a   Clark, Graeme C ^c   Titball, Richard W ^c,d   Alape Girón, Alberto ^a,b  

^a UNIVERSIDAD DE COSTA RICA   (Costa Rica)

^b Ctro Invest en Cie e Ing de Mat   (Costa Rica)

^c DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^d UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIUM TOXIN; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; NORPHENAZONE; OXYGEN RADICAL; PHOSPHOLIPASE C; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLOSTRIDIUM PERFRINGENS; CLOSTRIDIUM PERFRINGENS INFECTION; CONTROLLED STUDY; CYTOTOXICITY; GAS GANGRENE; MORTALITY; MOUSE; MUSCLE NECROSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL;

ANIMALS; ANTIPYRINE; BACTERIAL TOXINS; CALCIUM-BINDING PROTEINS; CELL LINE; CLOSTRIDIUM PERFRINGENS; DISEASE MODELS, ANIMAL; FREE RADICAL SCAVENGERS; GAS GANGRENE; MAP KINASE SIGNALING SYSTEM; MICE; MUSCLE, SKELETAL; REACTIVE OXYGEN SPECIES; SURVIVAL ANALYSIS; TREATMENT OUTCOME; TYPE C PHOSPHOLIPASES;

EID: 84866918145     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jis496     Document Type: Article

References (49)

1. Ramrakhiani L, Chand S. Recent progress on phospholipases: different sources, assay methods, industrial potential and pathogenicity. Appl Biochem Biotechnol 2011; 164:991-1022.
2. MacFarlane MG, Knight BCJG. The biochemistry of bacterial toxins. I. Lechitinase activity of Clostridium welchii toxins. Biochem J 1941; 35:884-902.
3. Shimizu T, Ohtani K, Hirakawa H, et al. Complete genome sequence of Clostridium perfringens an anaerobic flesh-eater. Proc Natl Acad Sci USA 2002; 99:996-1001. (Pubitemid 34106624)
4. Petit L, Gilbert M, Popoff MR. Clostridium perfringens: toxinotype and genotype. Trends Microbiol 1999; 7:104-10. (Pubitemid 29271996)
5. Flores-Díaz M, Alape-Girón A. Role of Clostridium perfringens phospholipase C in the pathogenesis of gas gangrene. Toxicon 2003; 42:979-86. (Pubitemid 38201496)
6. Jean D, Briolat V, Reysset G. Oxidative stress response in Clostridium perfringens. Microbiology 2004; 150:1649-59. (Pubitemid 38923664)
7. O'Brien DK, Melville SB. Effects of Clostridium perfringens alphatoxin (PLC) and perfringolysin O (PFO) on cytotoxicity to macrophages, on escape from the phagosomes of macrophages, and on persistence of C. perfringens in host tissues. Infect Immun. 2004; 72:5204-15. (Pubitemid 39223406)
8. Awad MM, Bryant AE, Stevens DL, Rood JI. Virulence studies on chromosomal α-toxin and θ-toxin mutants constructed by allelic exchange provide genetic evidence for the essential role of α-toxin in Clostridium perfringens-mediated gas gangrene. Mol Microbiol 1995; 15:191-202.
9. Alape-Girón A, Flores-Diaz M, Guillouard I, et al. Mapping critical residues for the toxic activities of Clostridium perfringens phospholipase C. Eur J Biochem 2000; 267:5191-7. (Pubitemid 30641316)
10. Stevens DL, Titball RW, Jepson M, Bayer CR, Hayes-Schroer SM, Bryant AE. Immunization with the C-Domain of alpha-Toxin prevents lethal infection, localizes tissue injury, and promotes host response to challenge with Clostridium perfringens. J Infect Dis 2004; 190:767-73. (Pubitemid 39050007)
11. Naylor CE, Eaton JT, Howells A, et al. Structure of the key toxin in gas gangrene. Nat Struct Biol 1998; 5:738-46. (Pubitemid 28359811)
12. Urbina P, Collado MI, Alonso A, et al. Unexpected wide substrate specificity of C. perfringens α-toxin phospholipase C. Biochim Biophys Acta 2011; 1808:2618-27.
13. Bryant AE, Bayer CR, Bayes-Schoer SM, Stevens DL. Activation of platelet gpIIbIIIa by phospholipase C from Clostridium perfringens involves store-operated calcium entry. J Infect Dis 2003; 187:408-17. (Pubitemid 36184581)
14. Ochi S, Oda M, Matsuda H, Ikari S, Sakurai J. Clostridium perfringens alpha-toxin activates the sphingomyelin metabolism system in sheep erythrocytes. J Biol Chem 2004; 279:12181-9. (Pubitemid 38445783)
15. Flores-Díaz M, Thelestam M, Clark GC, Titball RW, Alape-Girón A. Effects of Clostridium perfringens phospholipase C in mammalian cells. Anaerobe 2004; 10:115-23. (Pubitemid 38519812)
16. Gustafson C, Tagesson C. Phospholipase C from Clostridium perfringens stimulates phospholipase A2-mediated arachidonic acid release in cultured intestinal epithelial cells (NT 407). Scand J Gastroenterol 1990; 25:363-71. (Pubitemid 20184826)
17. Oda M, Ikari S, Matsuno T, Morimune Y, Nagahama M, Sakurai J. Signal transduction mechanism involved in Clostridium perfringens alpha-toxin-induced superoxide anion generation in rabbit neutrophils. Infect Immun 2006; 74:2876-86. (Pubitemid 43672998)
18. Flores-Díaz M, Alape-Giron A, Clark G, et al. A cellular deficiency of gangliosides causes hypersensitivity to Clostridium perfringens phospholipase C. J Biol Chem 2005; 280:26680-9. (Pubitemid 41040700)
19. Masini A, et al. Lipid hydroperoxide induced mitochondrial dysfunction following acute ethanol intoxication in rats. The critical role for mitochondrial reduced glutathione. Biochem Pharmacol 1994; 47:217-24.
20. Mayer M, Noble M. N-acetyl-L-cysteine is a pluripotent protector against cell death and enhancer of trophic factor-mediated cell survival in vitro. Proc Natl Acad Sci USA 1994; 91:7496-500.
21. Patel M, Day BJ. Metalloporphyrin class of therapeutic catalytic antioxidants. Trends Pharmacol Sci 1999; 20:359-64. (Pubitemid 29421616)
22. Moreno-Manzano V, Ishikawa Y, Lucio-Cazana J, Kitamura M. Selective involvement of superoxide anion, but not downstream compounds hydrogen peroxide and peroxynitrite, in tumor necrosis factor-alpha-induced apoptosis of rat mesangial cells. J Biol Chem 2000; 275:12684-91. (Pubitemid 30241419)
23. Kono H, et al. Edaravone, a novel free radical scavenger, prevents liver injury and mortality in rats administered endotoxin. J Pharmacol Exp Ther 2003; 307:74-82. (Pubitemid 37151893)
24. Bohler T, et al. TNF-alpha and IL-1alpha induce apoptosis in subconfluent rat mesangial cells. Evidence for the involvement of hydrogen peroxide and lipid peroxidation as second messengers. Cytokine 2000; 12:986-91. (Pubitemid 30479480)
25. Samuni A, et al. Multifunctional antioxidant activity of HBED iron chelator. Free Radic Biol Med 2001; 30:170-7. (Pubitemid 32121794)
26. Antunes F, Cadenas E. Cellular titration of apoptosis with steady state concentrations of H2O2: submicromolar levels of H2O2 induce apoptosis through Fenton chemistry independent of the cellular thiol state. Free Radic Biol Med 2001; 30:1008-18. (Pubitemid 32333031)
27. Li W, et al. Foam cell death induced by 7-beta-hydroxycholesterol is mediated by labile iron-driven oxidative injury: mechanisms underlying induction of ferritin in human atheroma. Free Radic Biol Med 2005; 39:864-75.
28. Garner B, Li W, Roberg K, Brunk UT. On the cytoprotective role of ferritin in macrophages and its ability to enhance lysosomal stability. Free Radic Res 1997; 27:487-500. (Pubitemid 28026532)
29. Alessandrini A, Namura S, Moskowitz MA, Bonventre JV. MEK1 protein kinase inhibition protects against damage resulting from focal cerebral ischemia. Proc Natl Acad Sci USA 1999; 96:12866-9. (Pubitemid 29513594)
30. Wang X, Martindale J, Holbrook N. Requirement for ERK activation in Cisplatin-induced apoptosis. J Biol Chem 2000; 275:39435-43. (Pubitemid 32058968)
31. Malassagne B, et al. The superoxide dismutase mimetic MnTBAP prevents Fas-Induced acute liver failure in the mouse. Gastroenterology 2001; 121:1451-9. (Pubitemid 33140462)
32. Yang Y, Li Q, Shuaib A. Neuroprotection by 2-h postisquemia administration of two free radical scavengers, α-phenyl-n-tert-butyl- nitrone (PBN) and N-tert-butyl-(2-sulfophenyl)-nitrone (S-PBN), in rats subjected to focal embolic cerebral isquemia. Exp Neurol 2000; 163:39-45. (Pubitemid 30314358)
33. Tsuruya K, et al. Antioxidant ameliorates cisplatin-induced renal tubular cell death through inhibition of death receptor-mediated pathways. Am J Physiol Renal Physiol 2003; 285:208-18.
34. Ritter C, et al. Treatment with N-acetylcysteine plus deferoxamine protects rats against oxidative stress and improves survival in sepsis. Crit Care Med 2004; 32:342-9. (Pubitemid 38234109)
35. Rando TA. Oxidative stress and the pathogenesis of muscular dystrophies. Am J Phys Med Rehabil 2002; 81:S175-86. (Pubitemid 35192977)
36. Anaya DA, McMahon K, Nathens AB, Sullivan SR, Foy H, Bulger E. Predictors of mortality and limb loss in necrotizing soft tissue infections. Arch Surg 2005; 140:151-7. (Pubitemid 40229103)
37. Nagahama MM, Michiue K, Mukai M, Ochi S, Sakurai J. Mechanism of membrane damage by Clostridium perfringens alpha-toxin. Microbiol Immunol 1998; 42:533-8. (Pubitemid 28380848)
38. Kruszewski M. Labile iron pool: the main determinant of cellular response to oxidative stress. Mutat Res 2003; 531:81-92. (Pubitemid 37456724)
39. Abe S, Kirima K, Tsuchiya K, et al. The reaction rate of edaravone (3-methyl-1-phenyl-2-pyrazolin-5-one (MCI-186)) with hydroxyl radical. Chem Pharm Bull 2004; 52:186-91. (Pubitemid 41656750)
40. Yoshida H, Yanai H, Namiki Y, Fukatsu-Sasaki K, Furutani N, Tada N. Neuroprotective effects of edaravone: a novel free radical scavenger in cerebrovascular injury. CNS Drug Rev 2006; 12:9-20. (Pubitemid 44133577)
41. Tsujita K, Shimomura H, Kaikita K, et al. Long-term efficacy of edaravone in patients with acute myocardial infarction. Circ J 2006; 70:832-7. (Pubitemid 43979118)
42. Torres M, Forman HJ. Redox signalling and the MAP kinase pathways. Biofactors 2003; 17:287-96. (Pubitemid 37267162)
43. Zhuang S, Schnellmann RG. A death-promoting role for extracellular signal-regulated kinase. J Pharmacol Exp Ther 2007; 292: F440-7.
44. Wang X, Wang H, Xu L, et al. Significant neuroprotection against ischemic brain injury by inhibition of the MEK1 protein kinase in mice: exploration of potential mechanism associated with apoptosis. J Pharmacol Exp Ther 2003; 304:172-8. (Pubitemid 36008925)
45. Clausen F, Lundqvist H, Ekmark S, Lewen A, Ebendal T, Hillered L. Oxygen free radical-dependent activation of extracellular signalregulated kinase mediates apoptosis-like cell death after traumatic Brain Injury. J Neutrotrauma 2004; 21:1168-82. (Pubitemid 39280844)
46. Sabbatini M, Santillo M, Pisani A, et al. Inhibition of Ras/ERK1/2 signalling protects against postischemic renal injury. Am J Physiol Renal Physiol 2006; 290:F1408-15. (Pubitemid 43830766)
47. Chu CT, Levinthal DJ, Kulich SM, Chalovich EM, DeFranco DB. Oxidative neuronal injury: the dark side of ERK1/2. Eur J Biochem 2004; 271:2060-6. (Pubitemid 38747975)
48. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39:44-84. (Pubitemid 44566469)
49. Victor VM, Rocha M, Espulgues JV, De la Fuente M. Role of free radicals in sepsis: antioxidant therapy. Curr Pharm Des 2005; 11:3141-58. (Pubitemid 41149930)