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Article

Role of poly(ADP-ribosyl)ation in a ‘two-hit’ model of hypoxia and oxidative stress in human A549 epithelial cells in vitro

  • Authors:
    • Katalin Erdélyi
    • Pál Pacher
    • László Virág
    • Csaba Szabó
  • View Affiliations / Copyright

    Affiliations: Department of Anesthesiology, The University of Texas Medical Branch, Galveston, TX 77555-1102, USA
  • Pages: 339-346
    |
    Published online on: May 29, 2013
       https://doi.org/10.3892/ijmm.2013.1397
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Abstract

A preceding hypoxic insult can sensitize the cells or the organism to a subsequent, second insult. The aim of the present study was to investigate the molecular mechanism of this phenomenon (often termed ‘two-hit’ injury paradigm), in an in vitro model of hypoxia/oxidative stress injury in A549 epithelial cells, with special emphasis on the role of the nuclear enzyme poly(ADP-ribose) polymerase-1 (PARP-1) in the process. Pre-exposure of the cells to 24 h hypoxia significantly reduced intracellular glutathione (GSH) levels, reduced mitochondrial activity and adenosine triphosphate (ATP) levels. However pre-exposure to hypoxia failed to induce any change in PARP-1 expression and activation, DNA single‑strand breaks or plasma membrane integrity. Pre-exposure to hypoxia markedly increased the sensitivity of the cells to subsequent oxidative stress-induced DNA damage. Hydrogen peroxide (H2O2) induced a concentration-dependent increase in DNA breakage, PARP activation, depletion of intracellular ATP, inhibition of mitochondrial activity and two distinct parameters that quantify the breakdown of plasma membrane integrity (propidium iodide uptake or lactate dehydrogenase release). PARP-1 activation played a significant role in the H2O2-induced cell death response because PARP activation, depletion of intracellular ATP, inhibition of mitochondrial activity, and the breakdown of plasma membrane integrity were attenuated in cells with permanently silenced PARP-1. Based on measurement of the endogenous antioxidant GSH, we hypothesized that the mechanism of hypoxia-mediated enhancement of H2O2 involves depletion of the GSH during the hypoxic period, which renders the cells more sensitive to a subsequent DNA single‑strand break elicited by H2O2. DNA strand breakage then activates PARP-1, leading to the inhibition of mitochondrial function, depletion of ATP and cell necrosis. PARP-1 deficiency protects against the cytotoxicity, to a lesser degree, by protecting against GSH depletion during the hypoxic period, and, to a larger degree, by maintaining mitochondrial function and preserving intracellular ATP levels during the subsequent oxidative stress period.
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View References

1 

Saadia R and Schein M: Multiple organ failure. How valid is the ‘two hit’ model? J Accid Emerg Med. 16:163–166. 1999.

2 

Rotstein OD: Modeling the two-hit hypothesis for evaluating strategies to prevent organ injury after shock/resuscitation. J Trauma. 54:S203–S206. 2003.PubMed/NCBI

3 

West MA, Li MH, Seatter SC and Bubrick MP: Pre-exposure to hypoxia or septic stimuli differentially regulates endotoxin release of tumor necrosis factor, interleukin-6, interleukin-1, prostaglandin E2, nitric oxide, and superoxide by macrophages. J Trauma. 37:82–89. 1994. View Article : Google Scholar

4 

Kim SY, Choi YJ, Joung SM, Lee BH, Jung YS and Lee JY: Hypoxic stress up-regulates the expression of Toll-like receptor 4 in macrophages via hypoxia-inducible factor. Immunology. 129:516–524. 2010. View Article : Google Scholar : PubMed/NCBI

5 

Brehmer F, Bendix I, Prager S, van de Looij Y, Reinboth BS, Zimmermanns J, Schlager GW, Brait D, Sifringer M, Endesfelder S, Sizonenko S, Mallard C, Bührer C, Felderhoff-Mueser U and Gerstner B: Interaction of inflammation and hyperoxia in a rat model of neonatal white matter damage. PLoS One. 7:e490232012. View Article : Google Scholar : PubMed/NCBI

6 

Cheng XQ, Song LJ, Li H, Di H, Zhang YY and Chen DF: Beneficial effect of the polysaccharides from Bupleurum smithii var. parvifolium on ‘two-hit’ acute lung injury in rats. Inflammation. 35:1715–1722. 2012.

7 

Kox M, Vaneker M, van der Hoeven JG, Scheffer GJ, Hoedemaekers CW and Pickkers P: Effects of vagus nerve stimulation and vagotomy on systemic and pulmonary inflammation in a two-hit model in rats. PLoS One. 7:e344312012. View Article : Google Scholar : PubMed/NCBI

8 

Szabo C: Role of poly(ADP-ribose) synthetase in inflammation. Eur J Pharmacol. 350:1–19. 1998. View Article : Google Scholar : PubMed/NCBI

9 

Pacher P and Szabo C: Role of poly(ADP-ribose) polymerase 1 (PARP-1) in cardiovascular diseases: the therapeutic potential of PARP inhibitors. Cardiovasc Drug Rev. 25:235–260. 2007. View Article : Google Scholar : PubMed/NCBI

10 

Graziani G and Szabo C: Clinical perspectives of PARP inhibitors. Pharmacol Res. 52:109–118. 2005. View Article : Google Scholar : PubMed/NCBI

11 

Erdélyi K, Bai P, Kovács I, Szabó E, Mocsár G, Kakuk A, Szabo C, Gergely P and Virág L: Dual role of poly(ADP-ribose) glycohydrolase in the regulation of cell death in oxidatively stressed A549 cells. FASEB J. 23:3553–3563. 2009.PubMed/NCBI

12 

Salzman A, Denenberg AG, Ueta I, O’Connor M, Linn SC and Szabo C: Induction and activity of nitric oxide synthase in cultured human intestinal epithelial monolayers. Am J Physiol. 270:G565–G573. 1996.PubMed/NCBI

13 

Jakovljevic B, Novakov-Mikic A, Brkic S, Bogavac MA, Tomic S and Miler V: Lipid peroxidation in the first trimester of pregnancy. J Matern Fetal Neonatal Med. 25:1316–1318. 2012. View Article : Google Scholar : PubMed/NCBI

14 

Suzuki K, Olah G, Modis K, Coletta C, Kulp G, Gerö D, Szoleczky P, Chang T, Zhou Z, Wu L, Wang R, Papapetropoulos A and Szabo C: Hydrogen sulfide replacement therapy protects the vascular endothelium in hyperglycemia by preserving mitochondrial function. Proc Natl Acad Sci USA. 108:13829–13834. 2011. View Article : Google Scholar : PubMed/NCBI

15 

Módis K, Gero D, Erdélyi K, Szoleczky P, DeWitt D and Szabo C: Cellular bioenergetics is regulated by PARP1 under resting conditions and during oxidative stress. Biochem Pharmacol. 83:633–643. 2012.PubMed/NCBI

16 

Southan GJ, Zingarelli B, O’Connor M, Salzman AL and Szabo C: Spontaneous rearrangement of aminoalkylisothioureas into mercaptoalkylguanidines, a novel class of nitric oxide synthase inhibitors with selectivity towards the inducible isoform. Br J Pharmacol. 117:619–632. 1996. View Article : Google Scholar

17 

Gerö D, Módis K, Nagy N, Szoleczky P, Tóth ZD, Dormán G and Szabo C: Oxidant-induced cardiomyocyte injury: identification of the cytoprotective effect of a dopamine 1 receptor agonist using a cell-based high-throughput assay. Int J Mol Med. 20:749–761. 2007.PubMed/NCBI

18 

Virág L and Szabo C: Purines inhibit poly(ADP-ribose) polymerase activation and modulate oxidant-induced cell death. FASEB J. 15:99–107. 2011.PubMed/NCBI

19 

Virág L, Scott GS, Cuzzocrea S, Marmer D, Salzman AL and Szabo C: Peroxynitrite-induced thymocyte apoptosis: the role of caspases and poly(ADP-ribose) synthetase (PARS) activation. Immunology. 94:345–355. 1998.PubMed/NCBI

20 

Virág L, Salzman AL and Szabo C: Poly(ADP-ribose) synthetase activation mediates mitochondrial injury during oxidant-induced cell death. J Immunol. 161:3753–3759. 1998.PubMed/NCBI

21 

Ha HC and Snyder SH: Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci USA. 96:13978–13982. 1999. View Article : Google Scholar : PubMed/NCBI

22 

Szoleczky P, Módis K, Nagy N, Dóri Tóth Z, DeWitt D, Szabo C and Gero D: Identification of agents that reduce renal hypoxia-reoxygenation injury using cell-based screening: purine nucleosides are alternative energy sources in LLC-PK1 cells during hypoxia. Arch Biochem Biophys. 517:53–70. 2012.

23 

Szabo C, Saunders C, O’Connor M and Salzman AL: Peroxynitrite causes energy depletion and increases permeability via activation of poly(ADP-ribose) synthetase in pulmonary epithelial cells. Am J Respir Cell Mol Biol. 16:105–109. 1997. View Article : Google Scholar : PubMed/NCBI

24 

Kennedy M, Denenberg AG, Szabo C and Salzman AL: Poly(ADP-ribose) synthetase activation mediates increased permeability induced by peroxynitrite in Caco-2BBe cells. Gastroenterology. 114:510–518. 1998. View Article : Google Scholar : PubMed/NCBI

25 

Liaudet L, Szabó A, Soriano FG, Zingarelli B, Szabo C and Salzman AL: Poly(ADP-ribose) synthetase mediates intestinal mucosal barrier dysfunction after mesenteric ischemia. Shock. 14:134–141. 2000. View Article : Google Scholar : PubMed/NCBI

26 

Shimoda K, Murakami K, Enkhbaatar P, Traber LD, Cox RA, Hawkins HK, Schmalstieg FC, Komjati K, Mabley JG, Szabo C, Salzman AL and Traber DL: Effect of poly(ADP ribose) synthetase inhibition on burn and smoke inhalation injury in sheep. Am J Physiol Lung Cell Mol Physiol. 285:L240–L249. 2003. View Article : Google Scholar : PubMed/NCBI

27 

Szabo C, Lim LH, Cuzzocrea S, Getting SJ, Zingarelli B, Flower RJ, Salzman AL and Perretti M: Inhibition of poly(ADP-ribose) synthetase attenuates neutrophil recruitment and exerts antiinflammatory effects. J Exp Med. 186:1041–1049. 1997. View Article : Google Scholar : PubMed/NCBI

28 

Cuzzocrea S, Zingarelli B, Gilad E, Hake P, Salzman AL and Szabo C: Protective effects of 3-aminobenzamide, an inhibitor of poly(ADP-ribose) synthase in a carrageenan-induced model of local inflammation. Eur J Pharmacol. 342:67–76. 1998. View Article : Google Scholar : PubMed/NCBI

29 

Veres B, Gallyas F Jr, Varbiro G, Berente Z, Osz E, Szekeres G, Szabo C and Sumegi B: Decrease of the inflammatory response and induction of the Akt/protein kinase B pathway by poly(ADP-ribose) polymerase 1 inhibitor in endotoxin-induced septic shock. Biochem Pharmacol. 65:1373–1382. 2003. View Article : Google Scholar : PubMed/NCBI

30 

Goldfarb RD, Marton A, Szabó E, Virág L, Salzman AL, Glock D, Akhter I, McCarthy R, Parrillo JE and Szabo C: Protective effect of a novel, potent inhibitor of poly(adenosine 5′-diphosphate-ribose) synthetase in a porcine model of severe bacterial sepsis. Crit Care Med. 30:974–980. 2002.

31 

Soriano FG, Liaudet L, Szabó E, Virág L, Mabley JG, Pacher P and Szabo C: Resistance to acute septic peritonitis in poly(ADP-ribose) polymerase-1-deficient mice. Shock. 17:286–292. 2002. View Article : Google Scholar : PubMed/NCBI

32 

Bai P and Virág L: Role of poly(ADP-ribose) polymerases in the regulation of inflammatory processes. FEBS Lett. 586:3771–3777. 2012. View Article : Google Scholar : PubMed/NCBI

33 

Cantoni O and Guidarelli A: Peroxynitrite damages U937 cell DNA via the intermediate formation of mitochondrial oxidants. IUBMB Life. 60:753–756. 2008. View Article : Google Scholar : PubMed/NCBI

34 

Jean JC, Liu Y and Joyce-Brady M: The importance of gamma-glutamyl transferase in lung glutathione homeostasis and antioxidant defense. Biofactors. 17:161–173. 2003. View Article : Google Scholar : PubMed/NCBI

35 

Cuzzocrea S, Zingarelli B, O’Connor M, Salzman AL and Szabo C: Effect of L-buthionine-(S,R)-sulphoximine, an inhibitor of gamma-glutamylcysteine synthetase on peroxynitrite- and endotoxic shock-induced vascular failure. Br J Pharmacol. 123:525–537. 1998. View Article : Google Scholar : PubMed/NCBI

36 

Kiss L, Chen M, Gero D, Módis K, Lacza Z and Szabo C: Effects of 7-ketocholesterol on the activity of endothelial poly(ADP-ribose) polymerase and on endothelium-dependent relaxant function. Int J Mol Med. 18:1113–1117. 2006.PubMed/NCBI

37 

Mizumoto K, Glascott PA Jr and Farber JL: Roles for oxidative stress and poly(ADP-ribosyl)ation in the killing of cultured hepatocytes by methyl methanesulfonate. Biochem Pharmacol. 46:1811–1818. 1993. View Article : Google Scholar : PubMed/NCBI

38 

Bump EA and Brown JM: Role of glutathione in the radiation response of mammalian cells in vitro and in vivo. Pharmacol Ther. 47:117–136. 1990. View Article : Google Scholar : PubMed/NCBI

39 

Zucker B, Hanusch J and Bauer G: Glutathione depletion in fibroblasts is the basis for apoptosis-induction by endogenous reactive oxygen species. Cell Death Differ. 4:388–395. 1997. View Article : Google Scholar : PubMed/NCBI

40 

Puhakka A, Ollikainen T, Soini Y, Kahlos K, Säily M, Koistinen P, Pääkkö P, Linnainmaa K and Kinnula VL: Modulation of DNA single-strand breaks by intracellular glutathione in human lung cells exposed to asbestos fibers. Mutat Res. 514:7–17. 2002. View Article : Google Scholar : PubMed/NCBI

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Spandidos Publications style
Erdélyi K, Pacher P, Virág L and Szabó C: Role of poly(ADP-ribosyl)ation in a ‘two-hit’ model of hypoxia and oxidative stress in human A549 epithelial cells in vitro. Int J Mol Med 32: 339-346, 2013.
APA
Erdélyi, K., Pacher, P., Virág, L., & Szabó, C. (2013). Role of poly(ADP-ribosyl)ation in a ‘two-hit’ model of hypoxia and oxidative stress in human A549 epithelial cells in vitro. International Journal of Molecular Medicine, 32, 339-346. https://doi.org/10.3892/ijmm.2013.1397
MLA
Erdélyi, K., Pacher, P., Virág, L., Szabó, C."Role of poly(ADP-ribosyl)ation in a ‘two-hit’ model of hypoxia and oxidative stress in human A549 epithelial cells in vitro". International Journal of Molecular Medicine 32.2 (2013): 339-346.
Chicago
Erdélyi, K., Pacher, P., Virág, L., Szabó, C."Role of poly(ADP-ribosyl)ation in a ‘two-hit’ model of hypoxia and oxidative stress in human A549 epithelial cells in vitro". International Journal of Molecular Medicine 32, no. 2 (2013): 339-346. https://doi.org/10.3892/ijmm.2013.1397
Copy and paste a formatted citation
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Spandidos Publications style
Erdélyi K, Pacher P, Virág L and Szabó C: Role of poly(ADP-ribosyl)ation in a ‘two-hit’ model of hypoxia and oxidative stress in human A549 epithelial cells in vitro. Int J Mol Med 32: 339-346, 2013.
APA
Erdélyi, K., Pacher, P., Virág, L., & Szabó, C. (2013). Role of poly(ADP-ribosyl)ation in a ‘two-hit’ model of hypoxia and oxidative stress in human A549 epithelial cells in vitro. International Journal of Molecular Medicine, 32, 339-346. https://doi.org/10.3892/ijmm.2013.1397
MLA
Erdélyi, K., Pacher, P., Virág, L., Szabó, C."Role of poly(ADP-ribosyl)ation in a ‘two-hit’ model of hypoxia and oxidative stress in human A549 epithelial cells in vitro". International Journal of Molecular Medicine 32.2 (2013): 339-346.
Chicago
Erdélyi, K., Pacher, P., Virág, L., Szabó, C."Role of poly(ADP-ribosyl)ation in a ‘two-hit’ model of hypoxia and oxidative stress in human A549 epithelial cells in vitro". International Journal of Molecular Medicine 32, no. 2 (2013): 339-346. https://doi.org/10.3892/ijmm.2013.1397
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