Short-term cigarette smoke exposure induces reversible changes in energy metabolism and cellular redox status independent of inflammatory responses in mouse lungs

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 303, Issue 10, 2012, Pages

  Agarwal, Amit R ^a   Zhao, Liqin ^a   Sancheti, Harsh ^a   Sundar, Isaac K ^b   Rahman, Irfan ^b   Cadenas, Enrique ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Chronic obstructive pulmonary disease; Glutathione; Glycolysis; Mitochondria; NAD(P)H; Pentose phosphate pathway

Indexed keywords

CIGARETTE SMOKE; CYTOCHROME C OXIDASE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE; PYRIDINE NUCLEOTIDE; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

A J MOUSE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ELECTRON TRANSPORT; ENERGY METABOLISM; GENE EXPRESSION; GLUCOSE METABOLISM; GLYCOLYSIS; INFLAMMATION; MALE; MOUSE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; SMOKING;

ANIMALS; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GLUCOSE; GLUCOSEPHOSPHATE DEHYDROGENASE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE (NADP+)(PHOSPHORYLATING); LUNG; MALE; MICE; MITOCHONDRIA; OXIDATION-REDUCTION; PNEUMONIA; PROTON PUMPS; SMOKING; TIME FACTORS; TOBACCO SMOKE POLLUTION;

EID: 84869164924     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00219.2012     Document Type: Article

References (51)

1. Barbini L, Rodríguez J, Dominguez F, Vega F. Glyceraldehyde-3-phosphate dehydrogenase exerts different biologic activities in apoptotic and proliferating hepatocytes according to its subcellular localization. Mol Cell Biochem 300: 19-28, 2007.
2. Bolanos JP, Almeida A. The pentose-phosphate pathway in neuronal survival against nitrosative stress. IUBMB Life 62: 14-18, 2010.
3. Bolanos JP, Delgado-Esteban M, Herrero-Mendez A, Fernandez-Fernandez S, Almeida A. Regulation of glycolysis and pentose-phosphate pathway by nitric oxide: impact on neuronal survival. Biochim Biophys Acta 1777: 789-793, 2008.
4. Cantin AM, North SL, Hubbard RC, Crystal RG. Normal alveolar epithelial lining fluid contains high levels of glutathione. J Appl Physiol 63: 152-157, 1987.
5. Chung S, Sundar IK, Yao H, Ho YS, Rahman I. Glutaredoxin 1 regulates cigarette smoke-mediated lung inflammation through differential modulation of IκB kinases in mice: impact on histone acetylation. Am J Physiol Lung Cell Mol Physiol 299: L192-L203, 2010.
6. Edirisinghe I, Yang SR, Yao H, Rajendrasozhan S, Caito S, Adenuga D, Wong C, Rahman A, Phipps RP, Jin ZG, Rahman I. VEGFR-2 inhibition augments cigarette smoke-induced oxidative stress and inflammatory responses leading to endothelial dysfunction. FASEB J 22: 2297-2310, 2008.
7. Fischer A. Intermediary metabolism of the lung. Environ Health Perspect 55: 149-158, 1984.
8. Freeman H, Shimomura K, Horner E, Cox RD, Ashcroft FM. Nicotinamide nucleotide transhydrogenase: a key role in insulin secretion. Cell Metab 3: 35-45, 2006.
9. Garcia-Nogales P, Almeida A, Fernandez E, Medina JM, Bolanos JP. Induction of glucose-6-phosphate dehydrogenase by lipopolysaccharide contributes to preventing nitric oxide-mediated glutathione depletion in cultured rat astrocytes. J Neurochem 72: 1750-1758, 1999.
10. Ghezzi P, Romines B, Fratelli M, Eberini I, Gianazza E, Casagrande S, Laragione T, Mengozzi M, Herzenberg LA. Protein glutathionylation: coupling and uncoupling of glutathione to protein thiol groups in lymphocytes under oxidative stress and HIV infection. Mol Immunol 38: 773-780, 2002.
11. Glaser PE, Gross RW. Rapid plasmenylethanolamine-selective fusion of membrane bilayers catalyzed by an isoform of glyceraldehyde-3-phosphate dehydrogenase: discrimination between glycolytic and fusogenic roles of individual isoforms. Biochemistry 34: 12193-12203, 1995.
12. Griffith OW, Bridges RJ, Meister A. Transport of γ-glutamyl amino acids: role of glutathione and γ-glutamyl transpeptidase. Proc Natl Acad Sci USA 76: 6319-6322, 1979.
13. Griffith OW, Mulcahy RT. The enzymes of glutathione synthesis: γ-glutamylcysteine synthetase. Adv Enzymol Relat Areas Mol Biol 73: 209-267, 1999.
14. Hara MR, Agrawal N, Kim SF, Cascio MB, Fujimuro M, Ozeki Y, Takahashi M, Cheah JH, Tankou SK, Hester LD, Ferris CD, Hayward SD, Snyder SH, Sawa A. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 7: 665-674, 2005.
15. Hwang JW, Rajendrasozhan S, Yao H, Chung S, Sundar IK, Huyck HL, Pryhuber GS, Kinnula VL, Rahman I. FOXO3 deficiency leads to increased susceptibility to cigarette smoke-induced inflammation, airspace enlargement, and chronic obstructive pulmonary disease. J Immunol 187: 987-998, 2011.
16. Ishitani R, Chuang DM. Glyceraldehyde-3-phosphate dehydrogenase antisense oligodeoxynucleotides protect against cytosine arabinonucleoside-induced apoptosis in cultured cerebellar neurons. Proc Natl Acad Sci USA 93: 9937-9941, 1996.
17. Klaidman LK, Leung AC, Adams JD Jr. High-performance liquid chromatography analysis of oxidized and reduced pyridine dinucleotides in specific brain regions. Anal Biochem 228: 312-317, 1995.
18. Klatt P, Lamas S. Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 267: 4928-4944, 2000.
19. Ludwig PW. Cigarette smoking causes accumulation of polymorphonuclear leukocytes in alveolar septum. Am Rev Respir Dis 131: 828-830, 1985
20. Meister A. Glutathione-ascorbic acid antioxidant system in animals. J Biol Chem 269: 9397-9400, 1994.
21. Meyer-Siegler K, Mauro DJ, Seal G, Wurzer J, deRiel JK, Sirover MA. A human nuclear uracil DNA glycosylase is the 37-kDa subunit of glyceraldehyde-3-phosphate dehydrogenase. Proc Natl Acad Sci USA 88: 8460-8464, 1991.
22. Mohr S, Hallak H, de Boitte A, Lapetina EG, Brüne B. Nitric oxideinduced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 274: 9427-9430, 1999.
23. Moodie FM, Marwick JA, Anderson CS, Szulakowski P, Biswas SK, Bauter MR, Kilty I, Rahman I. Oxidative stress and cigarette smoke alter chromatin remodeling but differentially regulate NF-κB activation and proinflammatory cytokine release in alveolar epithelial cells. FASEB J 18: 1897-1899, 2004.
24. Pauwels RA, Buist AS, Calverley PM, Jenkins CR, Hurd SS. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease. NHLBI/WHO Global Initiative for Chronic Obstructive Lung Disease (GOLD) Workshop Summary. Am J Respir Crit Care Med 163: 1256-1276, 2001.
25. Pedersen A, Karlsson GB, Rydstrom J. Proton-translocating transhydrogenase: an update of unsolved and controversial issues. J Bioenerg Biomembr 40: 463-473, 2008.
26. Pullman ME, Penefsky HS, Datta A, Racker E. Partial resolution of the enzymes catalyzing oxidative phosphorylation. I. Purification and properties of soluble dinitrophenol-stimulated adenosine triphosphatase. J Biol Chem 235: 3322-3329, 1960.
27. Rahman I. Inflammation and the regulation of glutathione level in lung epithelial cells. Antioxid Redox Signal 1: 425-447, 1999.
28. Rahman I, Li XY, Donaldson K, Harrison DJ, MacNee W. Glutathione homeostasis in alveolar epithelial cells in vitro and lung in vivo under oxidative stress. Am J Physiol Lung Cell Mol Physiol 269: L285-L292, 1995
29. Rahman I, Li XY, Donaldson K, MacNee W. Cigarette smoke, glutathione metabolism and epithelial permeability in rat lungs. Biochem Soc Trans 23: 235S, 1995.
30. Rahman I, MacNee W. Lung glutathione and oxidative stress: implications in cigarette smoke-induced airway disease. Am J Physiol Lung Cell Mol Physiol 277: L1067-L1088, 1999.
31. Rajendrasozhan S, Chung S, Sundar IK, Yao H, Rahman I. Targeted disruption of NF-κB1 (p50) augments cigarette smoke-induced lung inflammation and emphysema in mice: a critical role of p50 in chromatin remodeling. Am J Physiol Lung Cell Mol Physiol 298: L197-L209, 2010.
32. Ralser M, Wamelink M, Kowald A, Gerisch B, Heeren G, Struys E, Klipp E, Jakobs C, Breitenbach M, Lehrach H, Krobitsch S. Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J Biol 6: 10, 2007.
33. Ralser M, Wamelink MMC, Latkolik S, Jansen EEW, Lehrach H, Jakobs C. Metabolic reconfiguration precedes transcriptional regulation in the antioxidant response. Nat Biotechnol 27: 604-605, 2009.
34. Rangasamy T, Cho CY, Thimmulappa RK, Zhen L, Srisuma SS, Kensler TW, Yamamoto M, Petrache I, Tuder RM, Biswal S. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 114: 1248-1259, 2004.
35. Rangasamy T, Misra V, Zhen L, Tankersley CG, Tuder RM, Biswal S. Cigarette smoke-induced emphysema in A/J mice is associated with pulmonary oxidative stress, apoptosis of lung cells, and global alterations in gene expression. Am J Physiol Lung Cell Mol Physiol 296: L888-L900, 2009
36. Sarir H, Mortaz E, Karimi K, Kraneveld AD, Rahman I, Caldenhoven E, Nijkamp FP, Folkerts G. Cigarette smoke regulates the expression of TLR4 and IL-8 production by human macrophages. J Inflamm 6: 12, 2009.
37. Sawa A, Khan AA, Hester LD, Snyder SH. Glyceraldehyde-3-phosphate dehydrogenase: nuclear translocation participates in neuronal and nonneuronal cell death. Proc Natl Acad Sci USA 94: 11669-11674, 1997.
38. Schafer FQ, Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30: 1191-1212, 2001.
39. Seelig GF, Simondsen RP, Meister A. Reversible dissociation of γ-glutamylcysteine synthetase into two subunits. J Biol Chem 259: 9345-9347, 1984
40. Shenton D, Grant C. Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochem J 374: 513-519, 2003.
41. Singh R, Green MR. Sequence-specific binding of transfer RNA by glyceraldehyde-3-phosphate dehydrogenase. Science 259: 365-368, 1993.
42. Sundar IK, Chung S, Hwang JW, Arunachalam G, Cook S, Yao H, Mazur W, Kinnula VL, Fisher AB, Rahman I. Peroxiredoxin 6 differentially regulates acute and chronic cigarette smoke mediated lung inflammatory response and injury. Exp Lung Res 36: 451-462, 2010.
43. Tristan C, Shahani N, Sedlak TW, Sawa A. The diverse functions of GAPDH: views from different subcellular compartments. Cell Signal 23: 317-323, 2011.
44. Velsor LW, Kariya C, Kachadourian R, Day BJ. Mitochondrial oxidative stress in the lungs of cystic fibrosis transmembrane conductance regulator protein mutant mice. Am J Respir Cell Mol Biol 35: 579-586, 2006
45. Yao H, Arunachalam G, Hwang JW, Chung S, Sundar IK, Kinnula VL, Crapo JD, Rahman I. Extracellular superoxide dismutase protects against pulmonary emphysema by attenuating oxidative fragmentation of ECM. Proc Natl Acad Sci USA 107: 15571-15576, 2010.
46. Yao H, Chung S, Hwang JW, Rajendrasozhan S, Sundar IK, Dean DA, McBurney MW, Guarente L, Gu W, Rönty M, Kinnula VL, Rahman I. SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice. J Clin Invest 122: 2032-2045, 2012
47. Yao H, Edirisinghe I, Rajendrasozhan S, Yang SR, Caito S, Adenuga D, Rahman I. Cigarette smoke-mediated inflammatory and oxidative responses are strain-dependent in mice. Am J Physiol Lung Cell Mol Physiol 294: L1174-L1186, 2008.
48. Yao H, Rahman I. Current concepts on oxidative/carbonyl stress, inflammation and epigenetics in pathogenesis of chronic obstructive pulmonary disease. Toxicol Appl Pharmacol 254: 72-85, 2011.
49. Yap LP, Sancheti H, Ybanez MD, Garcia J, Cadenas E, Han D. Determination of GSH, GSSG, and GSNO using HPLC with electrochemical detection. Methods Enzymol 473: 137-147, 2010.
50. Yin F, Sancheti H, Cadenas E. Silencing of nicotinamide nucleotide transhydrogenase impairs cellular redox homeostasis and energy metabolism in PC12 cells. Biochim Biophys Acta 1817: 401-409, 2012.
51. Yoshida T, Tuder RM. Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Physiol Rev 87: 1047-1082, 2007.