Glutathione supplementation attenuates lipopolysaccharide-induced mitochondrial dysfunction and apoptosis in a mouse model of acute lung injury

Frontiers in Physiology

Volumn 3 MAY, Issue , 2012, Pages

  Aggarwal, Saurabh ^a   Dimitropoulou, Christiana ^a   Lu, Qing ^a   Black, Stephen M ^a   Sharma, Shruti ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Acute lung injury; Apoptosis; Glutathione ethyl ester; Lipopolysaccharide; Mitochondrial dysfunction

Indexed keywords

EID: 84866412824     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00161     Document Type: Article

References (53)

1. Behr, J., Maier, K., Degenkolb, B., Krombach, F., and Vogelmeier, C. (1997). Antioxidative and clinical effects of high-dose N-acetylcysteine in fibrosing alveolitis. Adjunctive therapy to maintenance immuno-suppression. Am. J. Respir. Crit. Care Med. 156, 1897-1901.
2. Chatterjee, A., Snead, C., Yetik-Anacak, G., Antonova, G., Zeng, J., and Catravas, J. D. (2008). Heat shock protein 90 inhibitors attenuate LPS-induced endothelial hyperperme-ability. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L755-L763.
3. Chuang, C. Y., Chen, T. L., Cherng, Y. G., Tai, Y. T., Chen, T. G., and Chen, R. M. (2011). Lipopolysac-charide induces apoptotic insults to human alveolar epithelial A549 cells through reactive oxygen species-mediated activation of an intrinsic mitochondrion-dependent pathway. Arch. Toxicol. 85, 209-218.
4. Costantini, P., Chernyak, B. V., Petron-illi, V., and Bernardi, P. (1996). Mod-ulation of the mitochondrial perme-ability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. J. Biol. Chem. 271, 6746-6751.
5. DeLeve, L. D., and Kaplowitz, N. (1990). Importance and regulation of hepatic glutathione. Semin. Liver Dis. 10, 251-266.
6. Drahota, Z., Krivakova, P., Cervinkova, Z., Kmonickova, E., Lotkova, H., Kucera, O., and Houstek, J. (2005). Tert-butyl hydroperoxide selectively inhibits mitochondrial respiratory-chain enzymes in isolated rat hepatocytes. Physiol. Res. 54, 67-72.
7. El-Sayed, N. S., Mahran, L. G., and Khattab, M. M. (2011). Tem-pol, a membrane-permeable radical scavenger, ameliorates lipopolysaccharide-induced acute lung injury in mice: a key role for superoxide anion. Eur. J. Pharmacol. 663, 68-73.
8. Erickson, S. E., Martin, G. S., Davis, J. L., Matthay, M. A., and Eisner, M. D. (2009). Recent trends in acute lung injury mortality: 1996-2005. Crit. Care Med. 37, 1574-1579.
9. Foxton, R. H., Land, J. M., and Heales, S. J. (2007). Tetrahydro-biopterin availability in Parkin-son's and Alzheimer's disease; poten-tial pathogenic mechanisms. Neu-rochem. Res. 32, 751-756.
10. Grandjean, E. M., Berthet, P., Ruff-mann, R., and Leuenberger, P. (2000). Efficacy of oral long-term N-acetylcysteine in chronic bron-chopulmonary disease: a meta-analysis of published double-blind, placebo-controlled clinical trials. Clin. Ther. 22, 209-221.
11. Griffith, O. W. (1980). Determination of glutathione and glutathione disul-fide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 106, 207-212.
12. Haddad, J. J., Safieh-Garabedian, B., Saade, N. E., and Land, S. C. (2001). Thiol regulation of pro-inflammatory cytokines reveals a novel immunopharmacological potential of glutathione in the alveolar epithelium. J. Pharmacol. Exp. Ther. 296, 996-1005.
13. Jaeschke, H., and Bajt, M. L. (2006). Intracellular signaling mecha-nisms of acetaminophen-induced liver cell death. Toxicol. Sci. 89, 31-41.
14. Kasielski, M., and Nowak, D. (2001). Long-term administration of N-acetylcysteine decreases hydrogen peroxide exhalation in subjects with chronic obstructive pul-monary disease. Respir. Med. 95, 448-456.
15. Kawasaki, M., Kuwano, K., Hagi-moto, N., Matsuba, T., Kunitake, R., Tanaka, T., Maeyama, T., and Hara, N. (2000). Protection from lethal apoptosis in lipopolysaccharide-induced acute lung injury in mice by a caspase inhibitor. Am. J. Pathol. 157, 597-603.
16. Kitamura, Y., Hashimoto, S., Mizuta, N., Kobayashi, A., Kooguchi, K., Fujiwara, I., and Nakajima, H. (2001). Fas/FasL-dependent apoptosis of alveolar cells after lipopolysaccharide-induced lung injury in mice. Am. J. Respir. Crit. Care Med. 163, 762-769.
17. Kuwabara, T., and Imajoh-Ohmi, S. (2004). LPS-induced apoptosis is dependent upon mitochondrial dys-function. Apoptosis 9, 467-474.
18. Lang, J. D., McArdle, P. J., O'reilly, P. J., and Matalon, S. (2002). Oxidant-antioxidant balance in acute lung injury. Chest 122, 314S-320S.
19. Lee, T. D., Sadda, M. R., Mendler, M. H., Bottiglieri, T., Kanel, G., Mato, J. M., and Lu, S. C. (2004). Abnormal hepatic methionine and glutathione metabolism in patients with alcoholic hepatitis. Alcohol. Clin. Exp. Res. 28, 173-181.
20. Lee, W. M., Hynan, L. S., Rossaro, L., Fontana, R. J., Stravitz, R. T., Lar-son, A. M., Davern, T. J. II, Mur-ray, N. G., McCashland, T., Reisch, J. S., and Robuck, P. R. (2009). Intra-venous N-acetylcysteine improves transplant-free survival in early stage non-acetaminophen acute liver fail-ure. Gastroenterology 137, 856.e1- 864.e1.
21. Li, M., Chiu, J. F., Mossman, B. T., and Fukagawa, N. K. (2006). Down-regulation of manganese-superoxide dismutase through phos-phorylation of FOXO3a by Akt in explanted vascular smooth muscle cells from old rats. J. Biol. Chem. 281, 40429-40439.
22. Li, X. Y., Donaldson, K., Rahman, I., and MacNee, W. (1994). An inves-tigation of the role of glutathione in increased epithelial permeability induced by cigarette smoke in vivo and in vitro. Am. J. Respir. Crit. Care Med. 149, 1518-1525.
23. Luppi, F., Aarbiou, J., Van Wetering, S., Rahman, I., De Boer, W. I., Rabe, K. F., and Hiemstra, P. S. (2005). Effects of cigarette smoke condensate on proliferation and wound closure of bronchial epithelial cells in vitro: role of glutathione. Respir. Res. 6, 140.
24. Ma, X., Xu, D., Ai, Y., Ming, G., and Zhao, S. (2010). Fas inhibi-tion attenuates lipopolysaccharide-induced apoptosis and cytokine release of rat type II alveolar epithelial cells. Mol. Biol. Rep. 37, 3051-3056.
25. Martinez, O., Nin, N., and Esteban, A. (2009). Prone position for the treatment of acute respiratory dis-tress syndrome: a review of current literature. Arch. Bronconeumol. 45, 291-296.
26. Messana, J. M., Cieslinski, D. A., O'connor, R. P., and Humes, H. D. (1988). Glutathione protects against exogenous oxidant injury to rab-bit renal proximal tubules. Am. J. Physiol. 255, F874-F884.
27. Mishra, D. P., and Dhali, A. (2007). Endotoxin induces luteal cell apop-tosis through the mitochondrial pathway. Prostaglandins Other Lipid Mediat. 83, 75-88.
28. Monick, M. M., Carter, A. B., Rob-eff, P. K., Flaherty, D. M., Peterson, M. W., and Hunninghake, G. W. (2001). Lipopolysaccharide activates Akt in human alveolar macrophages resulting in nuclear accumula-tion and transcriptional activity of beta-catenin. J. Immunol. 166, 4713-4720.
29. Nagase, T., Uozumi, N., Aoki-Nagase, T., Terawaki, K., Ishii, S., Tomita, T., Yamamoto, H., Hashizume, K., Ouchi, Y., and Shimizu, T. (2003). A potent inhibitor of cytosolic phos-pholipase A2, arachidonyl trifluo-romethyl ketone, attenuates LPS-induced lung injury in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 284, L720-L726.
30. Nunes, C., Barbosa, R. M., Almeida, L., and Laranjinha, J. (2011). Nitric oxide and DOPAC-induced cell death: from GSH depletion to mito-chondrial energy crisis. Mol. Cell. Neurosci. 48, 94-103.
31. Pacht, E. R., Timerman, A. P., Lykens, M. G., and Merola, A. J. (1991 Deficiency of alveolar fluid glutathione in patients with sepsis and the adult respiratory distress syndrome. Chest 100, 1397-1403.
32. Pocernich, C. B., Cardin, A. L., Racine, C. L., Lauderback, C. M., and But-terfield, D. A. (2001). Glutathione elevation and its protective role in acrolein-induced protein damage in synaptosomal membranes: rele-vance to brain lipid peroxidation in neurodegenerative disease. Neu-rochem. Int. 39, 141-149.
33. Poole, P. J., and Black, P. N. (2001). Oral mucolytic drugs for exacerbations of chronic obstructive pulmonary dis-ease: systematic review. BMJ 322, 1271-1274.
34. Quinlan, G. J., Evans, T. W., and Gut-teridge, J. M. (1994). Oxidative dam-age to plasma proteins in adult respi-ratory distress syndrome. Free Radic. Res. 20, 289-298.
35. Quinlan, G. J., Lamb, N. J., Tilley, R., Evans, T. W., and Gutteridge, J. M. (1997). Plasma hypoxanthine levels in ARDS: implications for oxida-tive stress, morbidity, and mortality. Am. J. Respir. Crit. Care Med. 155, 479-484.
36. Rahman, I., and MacNee, W. (2000a). Oxidative stress and regulation of glutathione in lung inflammation. Eur. Respir. J. 16, 534-554.
37. Rahman, I., and MacNee, W. (2000b). Regulation of redox glutathione levels and gene transcription in lung inflammation: therapeutic approaches. Free Radic. Biol. Med. 28, 1405-1420.
38. Rubenfeld, G. D., Caldwell, E., Peabody, E., Weaver, J., Martin, D. P., Neff, M., Stern, E. J., and Hudson, L. D. (2005). Incidence and outcomes of acute lung injury. N. Engl. J. Med. 353, 1685-1693.
39. Sarkar, F. H., Rahman, K. M., and Li, Y. (2003). Bax translocation to mito-chondria is an important event in inducing apoptotic cell death by indole-3-carbinol (I3C) treatment of breast cancer cells. J. Nutr. 133, 2434S-2439S.
40. Sharma, S., Sud, N., Wiseman, D. A., Carter, A. L., Kumar, S., Hou, Y., Rau, T., Wilham, J., Harmon, C., Oishi, P., Fineman, J. R., and Black, S. M. (2008). Altered carnitine home-ostasis is associated with decreased mitochondrial function and altered nitric oxide signaling in lambs with pulmonary hypertension. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L46-L56.
41. Shinde, S., Golam, K., Kumar, P., Patil, N., and Sadacharan, K. (2005). Peri-operative blood lactate levels, pyru-vate levels,and lactate-pyruvate ratio in children undergoing cardiopul-monary bypass for congenital heart disease. Indian J. Crit. Care Med. 9, 145-150.
42. Singhal, R. K., and Jain, A. (2000). Glu-tathione ethyl ester supplementation prevents mortality in newborn rats exposed to hyperoxia. Biol. Neonate 77, 261-266.
43. Sommer, S. P., Sommer, S., Sinha, B., Walter, D., Aleksic, I., Gohrbandt, B., Otto, C., and Leyh, R. G. (2012). Glutathione preconditioning ame-liorates mitochondria dysfunction during warm pulmonary ischemia-reperfusion injury. Eur. J. Cardiotho-rac. Surg. 41, 140-148.
44. Song, M., Kellum, J. A., Kaldas, H., and Fink, M. P. (2004). Evidence that glutathione depletion is a mech-anism responsible for the anti-inflammatory effects of ethyl pyru-vate in cultured lipopolysaccharide-stimulated RAW 264.7 cells. J. Phar-macol. Exp. Ther. 308, 307-316.
45. Takahashi, M., Sato, T., Shinohara, F., Echigo, S., and Rikiishi, H. (2005). Possible role of glutathione in mito-chondrial apoptosis of human oral squamous cell carcinoma caused by inorganic selenium compounds. Int. J. Oncol. 27, 489-495.
46. Tasaka,S.,Amaya,F., Hashimoto, S., and Ishizaka,A. (2008). Roles of oxidants and redox signaling in the pathogen-esis of acute respiratory distress syn-drome. Antioxid. Redox Signal. 10, 739-753.
47. van Klaveren, R. J., Demedts, M., and Nemery, B. (1997). Cellular glu-tathione turnover in vitro, with emphasis on type II pneumocytes. Eur. Respir. J. 10, 1392-1400.
48. Vargas, M. R., Johnson, D. A., and Johnson, J. A. (2011). Decreased glutathione accelerates neuro-logical deficit and mitochondrial pathology in familial ALS-linked hSOD1(G93A) mice model. Neurobiol. Dis. 43, 543-551.
49. Villa, P., Saccani,A., Sica, A., and Ghezzi, P. (2002). Glutathione protects mice from lethal sepsis by limiting inflammation and potentiating host defense. J. Infect. Dis. 185, 1115-1120.
50. Wang, X., McCullough, K. D., Franke, T. F., and Holbrook, N. J. (2000). Epidermal growth factor receptor-dependent Akt activation by oxida-tive stress enhances cell survival. J. Biol. Chem. 275, 14624-14631.
51. Wiseman, D. A., Sharma, S., and Black, S. M. (2010). Elevated zinc induces endothelial apoptosis via disruption of glutathione metabolism: role of the ADP translocator. Biometals 23, 19-30.
52. Z'Graggen, B. R., Tornic, J., Muller-Edenborn, B.,Reyes,L., Booy, C., and Beck-Schimmer, B. (2010). Acute lung injury: apoptosis in effector and target cells of the upper and lower airway compartment. Clin. Exp. Immunol. 161, 324-331.
53. Zhang, F., Wang, X., Wang, W., Li, N., and Li, J. (2008). Glu-tamine reduces TNF-alpha by enhancing glutathione synthesis in lipopolysaccharide-stimulated alveolar epithelial cells of rats. Inflammation 31, 344-350.