Streptococcus pneumoniae-induced oxidative stress in lung epithelial cells depends on pneumococcal autolysis and is reversible by resveratrol

Journal of Infectious Diseases

Volumn 211, Issue 11, 2015, Pages 1822-1830

  Zahlten, Janine ^a   Kim, Ye Ji ^a   Doehn, Jan Moritz ^a   Pribyl, Thomas ^b   Hocke, Andreas C ^a   García, Pedro ^c,d   Hammerschmidt, Sven ^b   Suttorp, Norbert ^a   Hippenstiel, Stefan ^a   Hübner, Ralf Harto ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY OF GREIFSWALD   (Germany)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

autolysin; glutathione; hydrogen peroxide; lung epithelial cells; Nuclear factor erythroid 2 related factor 2; pneumolysin; Streptococcus pneumoniae

Indexed keywords

AUTOLYSIN; CATALASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; PNEUMOLYSIN; PROTEIN LYTA; RESVERATROL; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ANTIOXIDANT; BACTERIAL PROTEIN; HYDROGEN PEROXIDE; INTERLEUKIN 8; PLY PROTEIN, STREPTOCOCCUS PNEUMONIAE; STILBENE DERIVATIVE; STREPTOLYSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOLYSIS; BACTERIAL STRAIN; CELL DEATH; CELL STRESS; CELL VIABILITY; CONTROLLED STUDY; DRUG MECHANISM; EX VIVO STUDY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LUNG ALVEOLUS EPITHELIUM CELL; LUNG PARENCHYMA; MOUSE; NONHUMAN; OXIDATIVE STRESS; PNEUMOCOCCAL INFECTION; PRIMARY BRONCHOEPITHELIAL CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION INITIATION; UPREGULATION; ANIMAL; CELL LINE; CELL SURVIVAL; DRUG EFFECTS; EPITHELIUM CELL; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; STREPTOCOCCUS PNEUMONIA;

ANIMALS; ANTIOXIDANTS; AUTOLYSIS; BACTERIAL PROTEINS; CELL LINE; CELL SURVIVAL; EPITHELIAL CELLS; GLUTATHIONE; GLUTATHIONE DISULFIDE; HUMANS; HYDROGEN PEROXIDE; INTERLEUKIN-8; LUNG; MICE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PNEUMONIA, PNEUMOCOCCAL; STILBENES; STREPTOCOCCUS PNEUMONIAE; STREPTOLYSINS;

EID: 84930445680     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu806     Document Type: Article

References (32)

1. van der Poll T, Opal SM. Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet 2009; 374:1543-56.
2. Kalin M, Ortqvist A, Almela M, et al. Prospective study of prognostic factors in community-acquired bacteremic pneumococcal disease in 5 countries. J Infect Dis 2000; 182:840-7.
3. Pericone CD, Park S, Imlay JA, Weiser JN. Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the Fenton reaction. J Bacteriol 2003; 185:6815-25.
4. Biswas SK, Rahman I. Environmental toxicity, redox signaling and lung inflammation: The role of glutathione. Mol Aspects Med 2009; 30:60-76.
5. Igarashi K, Kataoka K, Itoh K, Hayashi N, Nishizawa M, Yamamoto M. Regulation of transcription by dimerization of erythroid factor Nf-E2 p45 with small Maf proteins. Nature 1994; 367:568-72.
6. Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamato M, Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res 2002; 62:5196-203.
7. Cho HY, Reddy SP, Kleeberger SR. Nrf2 defends the lung from oxidative stress. Antioxid Redox Signal 2006; 8:76-87.
8. Hubner RH, Schwartz JD, De BP, et al. Coordinate control of expression of Nrf2-modulated genes in the human small airway epithelium is highly responsive to cigarette smoking. Mol Med 2009; 15:203-19.
9. Rahman I, Kode A, Biswas SK. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 2006; 1:3159-65.
10. Schmeck B, Zahlten J, Moog K, et al. Streptococcus pneumoniae-induced p38 MAPK-dependent phosphorylation of RelA at the interleukin-8 promotor. J Biol Chem 2004; 279:53241-7.
11. Martner A, Dahlgren C, Paton JC, Wold AE. Pneumolysin released during Streptococcus pneumoniae autolysis is a potent activator of intracellular oxygen radical production in neutrophils. Infect Immun 2008; 76:4079-87.
12. Moscoso M, Claverys JP. Release of DNA into the medium by competent Streptococcus pneumoniae: kinetics, mechanism and stability of the liberated DNA. Mol Microbiol 2004; 54:783-94.
13. Malley R, Henneke P, Morse SC, et al. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc Natl Acad Sci U S A 2003; 100:1966-71.
14. Comhair SAA, Erzurum SC. Antioxidant responses to oxidantmediated lung diseases. Am J Physiol Lung Cell Mol Physiol 2002; 283:L246-55.
15. Duane PG, Rubins JB, Weisel HR, Janoff EN. Identification of hydrogen- peroxide as a Streptococcus pneumoniae toxin for rat alveolar epithelial cells. Infect Immun 1993; 61:4392-7.
16. Park HS, Kim SR, Lee YC. Impact of oxidative stress on lung diseases. Respirology 2009; 14:27-38.
17. Cemek M, Caksen H, Bayiroglu F, Cemek F, Dede S. Oxidative stress and enzymic-non-enzymic antioxidant responses in children with acute pneumonia. Cell Biochem Funct 2006; 24:269-73.
18. Hoetzenecker W, Echtenacher B, Guenova E, et al. ROS-induced ATF3 causes susceptibility to secondary infections during sepsis-associated immunosuppression. Nat Med 2012; 18:128-34.
19. Mehta AJ, Joshi PC, Fan X, et al. Zinc supplementation restores PU.1 and Nrf2 nuclear binding in alveolar macrophages and improves redox balance and bacterial clearance in the lungs of alcohol-fed rats. Alcohol Clin Exp Res 2011; 35:1519-28.
20. Lugade AA, Vethanayagam RR, Nasirikenari M, Bogner PN, Segal BH, Thanavala Y. Nrf2 regulates chronic lung inflammation and B-cell responses to nontypeable Haemophilus influenzae. Am J Respir Cell Mol Biol 2011; 45:557-65.
21. Athale J, Ulrich A, MacGarvey NC, et al. Nrf2 promotes alveolar mitochondrial biogenesis and resolution of lung injury in Staphylococcus aureus pneumonia in mice. Free Radic Biol Med 2012; 53:1584-94.
22. MacGarvey NC, Suliman HB, Bartz RR, et al. Activation of mitochondrial biogenesis by heme oxygenase-1-mediated NF-E2-related factor-2 induction rescues mice from lethal Staphylococcus aureus sepsis. Am J Respir Crit Care Med 2012; 185:851-61.
23. Thimmulappa RK, Scollick C, Traore K, et al. Nrf2-dependent protection from LPS induced inflammatory response and mortality by CDDO-imidazolide. Biochem Biophys Res Commun 2006; 351:883-9.
24. Bolm M, Jansen WTM, Schnabel R, Chhatwal GS. Hydrogen peroxidemediated killing of Caenorhabditis elegans: a common feature of different streptococcal species. Infect Immun 2004; 72:1192-4.
25. Yesilkaya H, Andisi VF, Andrew PW, Bijlsma JJE. Streptococcus pneumoniae and reactive oxygen species: an unusual approach to living with radicals. Trends Microbiol 2013; 21:187-95.
26. Kode A, Rajendrasozhan S, Caito S, Yang SR, Megson IL, Rahman I. Resveratrol induces glutathione synthesis by activation of Nrf2 and protects against cigarette smoke-mediated oxidative stress in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2008; 294:L478-88.
27. Kobayashi A, Kang MI, Watai Y, et al. Oxidative and electophilic stresses activate Nrf2 through inhibition of ubiquitination activity if Keap1. Mol Cell Biol 2006; 26:221-9.
28. Li HG, Xia N, Forstermann U. Cardiovascular effects and molecular targets of resveratrol. Nitric Oxide 2012; 26:102-10.
29. Mullin GE. Red wine, grapes, and better health-resveratrol. Nutr Clin Pract 2011; 26:722-3.
30. Lee IT, Wang SW, Lee CW, et al. Lipoteichoic acid induces HO-1 expression via the TLR2/MyD88/c-Src/NADPH oxidase pathway and Nrf2 in human tracheal smooth muscle cells. J Immunol 2008; 181:5098-110.
31. Rushworth SA, Chen XL, Mackman N, Ogborne RM, O'Connell MA. Lipopolysaccharide-induced heme oxygenase-1 expression in human monocytic cells is mediated via Nrf2 and protein kinase C. J Immunol 2005; 175:4408-15.
32. Marriott HM, Mitchell TJ, Dockrell DH. Pneumolysin: A double-edged sword during the host-pathogen interaction. Curr Mol Med 2008; 8:497-509.