Chlorinated benzenes cause concomitantly oxidative stress and induction of apoptotic markers in lung epithelial cells (A549) at nonacute toxic concentrations

Journal of Proteome Research

Volumn 10, Issue 2, 2011, Pages 363-378

  Mörbt, Nora ^a   Tomm, Janina ^a   Feltens, Ralph ^a   Mögel, Iljana ^a   Kalkhof, Stefan ^a   Murugesan, Kalaimathi ^a   Wirth, Henry ^a,b   Vogt, Carsten ^a   Binder, Hans ^b   Lehmann, Irina ^a   Von Bergen, Martin ^a  

^a HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

1,2 dichlorobenzene; Apoptosis; Chlorobenzene; Lung epithelial cells; VOC

Indexed keywords

1,2 DICHLOROBENZENE; BENZENE DERIVATIVE; CASPASE 3; CHLOROBENZENE; CYCLINE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN BETA 1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C2; NUCLEOPHOSMIN; PDCD6IP PROTEIN; PROHIBITIN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEOME; REACTIVE OXYGEN METABOLITE; SERINE THREONINE RECEPTOR ASSOCIATED PROTEIN; SERINE TRANSFER RNA LIGASE; STYRENE; TRANSALDOLASE; TRANSALDOLASE 1; UNCLASSIFIED DRUG; VOLATILE ORGANIC COMPOUND; VOLTAGE DEPENDENT ANION CHANNEL 2;

APOPTOSIS; ARTICLE; CELL DEATH; CELLULAR STRESS RESPONSE; CHLORINATION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; GEL ELECTROPHORESIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; INDOOR AIR POLLUTION; INDUSTRIALIZATION; INTRACELLULAR SIGNALING; LUNG ALVEOLUS EPITHELIUM; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; OCCUPATIONAL EXPOSURE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN QUALITY; PROTEOMICS; QUALITY CONTROL; TWO DIMENSIONAL GEL ELECTROPHORESIS; VALIDATION STUDY;

APOPTOSIS; BIOLOGICAL MARKERS; CASPASE 3; CELL LINE, TUMOR; CELL SURVIVAL; CHLOROBENZENES; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FLOW CYTOMETRY; HUMANS; LUNG; OCCUPATIONAL EXPOSURE; OXIDATIVE STRESS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOME; REACTIVE OXYGEN SPECIES; RESPIRATORY MUCOSA; TOXICITY TESTS; VOLATILE ORGANIC COMPOUNDS;

EID: 79955414547     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr1005718     Document Type: Article

References (106)

1. Hodgson, M.; Levin, H.; Wolkoff, P. Volatile organic compounds and indoor air. J. Allergy Clin. Immunol. 1994, 94 (2 Pt 2), 296-303.
2. Molhave, L. Indoor climate, air pollution, and human comfort. J. Expo. Anal. Environ. Epidemiol. 1991, 1 (1), 63-81.
3. Rehwagen, M.; Schlink, U.; Herbarth, O. Seasonal cycle of VOCs in apartments. Indoor Air 2003, 13 (3), 283-91. (Pubitemid 37465476)
4. Willhite, C. C.; Book, S. A. Toxicology update. J. Appl. Toxicol. 1990, 10 (4), 307-10.
5. Heinisch, R. J.; Kettrup, A.; Bergheim, W.; Martens, D.; Wenzel, S. Persistent chlorinated hydrocarbons (PCHC), source-orientated monitoring in aquatic media. 4. The Chlorobenzenes. Freesenius Environ. Bull. 2006, 15 (3)
6. Boethling, R.; Fenner, K.; Howard, P.; Klecka, G.; Madsen, T.; Snape, J. R.; Whelan, M. J. Environmental persistence of organic pollutants: guidance for development and review of POP risk profiles. Integr. Environ. Assess Manas. 2009, 5 (4), 539-56.
7. CDC, NIOH and NIOSH basis for an occupational health standard: chlorobenzene MMWR Morb Mortal Wkly Rep 1994, 4, (43, 148-149).
8. ATDSDR, Toxicological profile for chlorobenzene. Agency for Toxic Substances and Disease Registry (ATDSR), 1990.
9. ATSDR, Toxicological profile for chlorobenzene. Agency for Toxic Substances and Disease Registry (ATDSR), 1990.
10. ATSDR, Toxicological profile for Dichlorobenzene. Agency for Toxic Substances and Disease Registry (ATDSR), 2006.
11. Howard, P. Large Production and Priority Pollutants. Handbook of Environmental Fate and Exposure Data for Organic Chemicals, Lewis Publishers: 1989.
12. Hissing, A. M.; Van Ommen, B.; Van Bladeren, P. J. Dose dependent kinetics and metabolism of 1,2-dichlorobenzene in rat; effect of pretreatment with phenobarbital. Xenobiotica 1996, 26 (1), 89-105. (Pubitemid 26108103)
13. Kusters, E.; Lauwerys, R. Biological monitoring of exposure to monochlorobenzene. Int. Arch. Occup. Environ. Health 1990, 62 (4), 329-31. (Pubitemid 20195522)
14. von Burg, R. Toxicology updates. Monochlorobenzene. J. Appl. Physiol. 1981, 95 (6), 2444-52.
15. Diez, U.; Kroessner, T.; Rehwagen, M.; Richter, M.; Wetzig, H.; Schulz, R.; Borte, M.; Metzner, G.; Krumbiegel, P.; Herbarth, O. Effects of indoor painting and smoking on airway symptoms in atopy risk children in the irst year of life results of the LARS-study. Leipzig Allergy High-Risk Children Study. Int. J. Hyg. Environ. Health 2000, 203 (1), 23-8. (Pubitemid 30305937)
16. Hippelein, M. Background concentrations of individual and total volatile organic compounds in residential indoor air of Schleswig-Holstein, Germany. J. Environ. Monit. 2004, 6 (9), 745-52. (Pubitemid 39312409)
17. BUA, BUA-Report: Chlorobenzene CAS-No. 108-90-7. Advisory Committee on Existing Chemicals of Environmental Relevance (BUA); Hirzel Verlag, S., Ed.; German Chemical Society, Gesellschaft Deutscher Chemiker: Stuttgart, 1993.
18. Diez, U.; Rehwagen, M.; Rolle-Kampczyk, U.; Wetzig, H.; Schulz, R.; Richter, M.; Lehmann, I.; Borte, M.; Herbarth, O. Redecoration of apartments promotes obstructive bronchitis in atopy risk infants-results of the LARS Study. Int. J. Hyg. Environ. Health 2003, 206 (3), 173-9. (Pubitemid 36807092)
19. Lehmann, I.; Thoelke, A.; Weiss, M.; Schlink, U.; Schulz, R.; Diez, U.; Sierig, G.; Emmrich, F.; Jacob, B.; Belcredi, P.; Bolte, G.; Heinrich, J.; Herbarth, O.; Wichmann, H. E.; Borte, M. T cell reactivity in neonates from an East and a West German city-results of the LISA study. Allergy 2002, 57 (2), 129-36. (Pubitemid 34538891)
20. Lehmann, I.; Rehwagen, M.; Diez, U.; Seiffart, A.; Rolle-Kampczyk, U.; Richter, M.; Wetzig, H.; Borte, M.; Herbarth, O. Enhanced in vivo IgE production and T cell polarization toward the type 2 phenotype in association with indoor exposure to VOC: results of the LARS study. Int. J. Hyg. Environ. Health 2001, 204 (4), 211-21. (Pubitemid 34087352)
21. Fischader, G.; Roder-Stolinski, C.; Wichmann, G.; Nieber, K.; Lehmann, I. Release of MCP-1 and IL-8 from lung epithelial cells exposed to volatile organic compounds. Toxicol. In Vitro 2008, 22 (2), 359-66. (Pubitemid 351163541)
22. Sheets, P. L.; Yost, G. S.; Carlson, G. P. Benzene metabolism in human lung cell lines BEAS-2B and A549 and cells overexpressing CYP2F1. J. Biochem. Mol. Toxicol. 2004, 18 (2), 92-9. (Pubitemid 38607681)
23. Chuang, C. Y.; Chen, T. L.; Chen, R. M. Molecular mechanisms of lipopolysaccharide-caused induction of surfactant protein-A gene expression in human alveolar epithelial A549 cells. Toxicol. Lett. 2009, 191 (2 -3), 132-9.
24. Roder-Stolinski, C.; Fischader, G.; Oostingh, G. J.; Eder, K.; Duschl, A. ; Lehmann, I. Chlorobenzene induces the NF-kappa B and p38 MAP kinase pathways in lung epithelial cells. Inhal. Toxicol. 2008, 20 (9), 813-20. (Pubitemid 352032214)
25. den Besten, C.; Vet, J. J.; Besselink, H. T.; Kiel, G. S.; van Berkel, B. J.; Beems, R.; van Bladeren, P. J. The liver, kidney, and thyroid toxicity of chlorinated benzenes. Toxicol. Appl. Pharmacol. 1991, 111 (1), 69-81.
26. Feltens, R.; Mogel, I.; Roder-Stolinski, C.; Simon, J. C.; Herberth, G.; Lehmann, I. Chlorobenzene induces oxidative stress in human lung epithelial cells in vitro. Toxicol. Appl. Pharmacol. 2009.
27. Wichmann, G.; Muhlenberg, J.; Fischader, G.; Kulla, C.; Rehwagen, M.; Herbarth, O.; Lehmann, I. An experimental model for the determination of immunomodulating effects by volatile compounds. Toxicol. In Vitro 2005, 19 (5), 685-93. (Pubitemid 40719543)
28. Roder-Stolinski, C.; Fischader, G.; Oostingh, G. J.; Feltens, R.; Kohse, F.; von Bergen, M.; Morbt, N.; Eder, K.; Duschl, A.; Lehmann, I. Styrene induces an inflammatory response in human lung epithelial cells via oxidative stress and NF-kappaB activation. Toxicol. Appl. Pharmacol. 2008, 231 (2), 241-7.
29. Kroger, M.; Hellmann, J.; Toldo, L.; Gluckmann, M.; von Eiff, B.; Fella, K.; Kramer, P. J. Toxicoproteomics: irst experiences in a BMBF-study. Altex 2004, 21 (3), 28-40.
30. Wetmore, B. A.; Merrick, B. A. Toxicoproteomics: proteomics applied to toxicology and pathology. Toxicol. Pathol. 2004, 32 (6), 619-42. (Pubitemid 39491933)
31. Marouga, R.; David, S.; Hawkins, E. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 2005, 382 (3), 669-78. (Pubitemid 40890994)
32. Jungblut, P. R.; Holzhutter, H. G.; Apweiler, R.; Schluter, H. The speciation of the proteome. Chem. Cent. J. 2008, 2, 16.
33. Morbt, N.; Mogel, I.; Kalkhof, S.; Feltens, R.; Roder-Stolinski, C.; Zheng, J.; Vogt, C.; Lehmann, I.; von Bergen, M. Proteome changes in human bronchoalveolar cells following styrene exposure indicate involvement of oxidative stress in the molecular-response mechanism. Proteomics 2009, 9 (21), 4920-33.
34. Harvilchuck, J. A.; Pu, X.; Klaunig, J. E.; Carlson, G. P. Indicators of oxidative stress and apoptosis in mouse whole lung and Clara cells following exposure to styrene and its metabolites. Toxicology 2009, 264 (3), 171-8.
35. Nedelcheva, V.; Gut, I.; Soucek, P.; Frantik, E. Cytochrome P450 catalyzed oxidation of monochlorobenzene, 1,2- and 1,4-dichlorobenzene in rat, mouse, and human liver microsomes. Chem. Biol. Interact. 1998, 115 (1), 53-70. (Pubitemid 28375748)
36. den Besten, C.; Ellenbroek, M.; van der Ree, M. A.; Rietjens, I. M.; van Bladeren, P. J. The involvement of primary and secondary metabolism in the covalent binding of 1,2- and 1,4-dichloroben- zenes. Chem. Biol. Interact. 1992, 84 (3), 259-75.
37. Kumagai, S.; Matsunaga, I. Identiication of urinary metabolites of human subjects exposed to o-dichlorobenzene. Int. Arch. Occup. Environ. Health 1995, 67 (3), 207-9.
38. Kumagai, S.; Matsunaga, I. Concentrations of urinary metabolites in workers exposed to monochlorobenzene and variation in the concentration during a workshift. Occup. Environ. Med. 1994, 51 (2), 120-4. (Pubitemid 24117923)
39. Mangal, D.; Vudathala, D.; Park, J. H.; Lee, S. H.; Penning, T. M.; Blair, I. A. Analysis of 7,8-dihydro-8-oxo-2'-deoxyguanosine in cellular DNA during oxidative stress. Chem. Res. Toxicol. 2009, 22 (5), 788-97.
40. Georgieva, D.; Risch, M.; Kardas, A.; Buck, F.; von Bergen, M.; Betzel, C. Comparative analysis of the venom proteomes of Vipera ammodytes ammodytes and Vipera ammodytes meridionalis. J Proteome Res. 2008, 7 (3), 866-86.
41. Neuhoff, V.; Arold, N.; Taube, D.; Ehrhardt, W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 1988, 9 (6), 255-62.
42. Berth, M.; Moser, F. M.; Kolbe, M.; Bernhardt, J. The state ofthe art in the analysis of two-dimensional gel electrophoresis images. Appl. Microbiol. Biotechnol. 2007, 76 (6), 1223-43. (Pubitemid 47459790)
43. Strimmer, K. A unified approach to false discovery rate estimation. BMC Bioinform. 2008, 9, 303.
44. Strimmer, K. fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 2008, 24 (12), 1461-2. (Pubitemid 351851002)
45. Jehmlich, N.; Schmidt, F.; Taubert, M.; Seifert, J.; von Bergen, M.; Richnow, H. H.; Vogt, C. Comparison of methods for simultaneous identiication of bacterial species and determination of metabolic activity by protein-based stable isotope probing (Protein-SIP) experiments. Rapid Commun. Mass Spectrom. 2009, 23 (12), 1871-8.
46. Müller, S.; Kohajda, T.; Findeiss, S.; Stadler, P.; Washietl, S.; Kellis, M.; von Bergen, M.; Kalkhof, S. Optimization of parameters for coverage of low molecular weight proteins. Anal. Bioanal. Chem. , 1-15.
47. Santos, P. M.; Roma, V.; Benndorf, D.; von Bergen, M.; Harms, H.; Sa-Correia, I. Mechanistic insights into the global response to phenol in the phenol-biodegrading strain Pseudomonas sp. M1 revealed by quantitative proteomics. Omics 2007, 11 (3), 233-51. (Pubitemid 47463367)
48. Benndorf, D.; Muller, A.; Bock, K.; Manuwald, O.; Herbarth, O.; von Bergen, M. Identification of spore allergens from the indoor mould Aspergillus versicolor. Allergy 2008, 63 (4), 454-60. (Pubitemid 351341819)
49. Hammer, O.; Harper, D. A. T.; Ryan, P. D. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 2001 4, (1), 9.
50. Joachimiak, M. P.; Weisman, J. L.; May, B. JColorGrid: software for the visualization of biological measurements. BMC Bioinform. 2006, 7, 225.
51. Lehmann, I.; Roder-Stolinski, C.; Nieber, K.; Fischader, G. In vitro models for the assessment of inflammatory and immunomodulatory effects of the volatile organic compound chlorobenzene. Exp. Toxicol. Pathol. 2008, 60 (2-3), 185-93.
52. Gargas, M. L.; Burgess, R. J.; Voisard, D. E.; Cason, G. H.; Andersen, M. E. Partition coeficients of low-molecular-weight volatile chemicals in various liquids and tissues. Toxicol. Appl. Pharmacol. 1989, 98 (1), 87-99. (Pubitemid 19094137)
53. Croute, F.; Poinsot, J.; Gaubin, Y.; Beau, B.; Simon, V.; Murat, J. C.; Soleilhavoup, J. P. Volatile organic compounds cytotoxicity and expression of HSP72, HSP90 and GRP78 stress proteins in cultured human cells. Biochim. Biophys. Acta 2002, 1591 (1-3), 147-55. (Pubitemid 35238022)
54. Duan, X.; Kelsen, S. G.; Clarkson, A. B., Jr.; Ji, R.; Merali, S. SILAC analysis of oxidative stress-mediated proteins in human pneumocytes: new role for treacle. Proteomics.
55. Martin, H. J.; Breyer-Pfaff, U.; Wsol, V.; Venz, S.; Block, S.; Maser, E. Purification and characterization of akr1b10 from human liver: role in carbonyl reduction of xenobiotics. Drug Metab. Dispos. 2006, 34 (3), 464-70. (Pubitemid 43290905)
56. Burczynski, M. E.; Lin, H. K.; Penning, T. M. Isoform-specific induction of a human aldo-keto reductase by polycyclic aromatic hydrocarbons (PAHs), electrophiles, and oxidative stress: implications for the alternative pathway of PAH activation catalyzed by human dihydrodiol dehydrogenase. Cancer Res. 1999, 59 (3), 607-14. (Pubitemid 29076058)
57. Penning, T. M.; Drury, J. E. Human aldo-keto reductases: Function, gene regulation, and single nucleotide polymorphisms. Arch. Biochem. Biophys. 2007, 464 (2), 241-50. (Pubitemid 47214569)
58. Takahashi, O.; Oishi, S.; Yoneyama, M.; Ogata, A.; Kamimura, H. Antiestrogenic effect of paradichlorobenzene in immature mice and rats. Arch. Toxicol. 2007, 81 (7), 505-17. (Pubitemid 47012466)
59. Ross, D. Metabolic basis of benzene toxicity. Eur. J. Haematol. Suppl. 1996, 60, 111-8.
60. Rietjens, I. M.; den Besten, C.; Hanzlik, R. P.; van Bladeren, P. J. Cytochrome P450-catalyzed oxidation of halobenzene derivatives. Chem. Res. Toxicol. 1997, 10 (6), 629-35. (Pubitemid 27263780)
61. Croute, F.; Beau, B.; Arrabit, C.; Gaubin, Y.; Delmas, F.; Murat, J. C.; Soleilhavoup, J. P. Pattern of stress protein expression in human lung cell-line A549 after short- or long-term exposure to cadmium. Environ. Health Perspect. 2000, 108 (1), 55-60. (Pubitemid 30064095)
62. Slebos, D. J.; Ryter, S. W.; Choi, A. M. Heme oxygenase-1 and carbon monoxide in pulmonary medicine. Respir Res. 2003, 4, 7.
63. Slebos, D. J.; Ryter, S. W.; van der Toorn, M.; Liu, F.; Guo, F.; Baty, C. J.; Karlsson, J. M.; Watkins, S. C.; Kim, H. P.; Wang, X.; Lee, J. S.; Postma, D. S.; Kauffman, H. F.; Choi, A. M. Mitochondrial localization and function of heme oxygenase-1 in cigarette smoke-induced cell death. Am. J. Respir. Cell Mol. Biol. 2007, 36 (4), 409-17. (Pubitemid 46622998)
64. Singh, H.; Ashley, R. H. Redox regulation of CLIC1 by cysteine residues associated with the putative channel pore. Biophys. J. 2006, 90 (5), 1628-38.
65. Banki, K.; Hutter, E.; Colombo, E.; Gonchoroff, N. J.; Perl, A. Glutathione levels and sensitivity to apoptosis are regulated by changes in transaldolase expression. J. Biol. Chem. 1996, 271 (51), 32994-3001. (Pubitemid 27008736)
66. Rho, H. K.; Park, J.; Suh, J. H.; Kim, J. B. Transcriptional regulation of mouse 6-phosphogluconate dehydrogenase by ADD1/SREBP1c. Biochem. Biophys. Res. Commun. 2005, 332 (1), 288-96. (Pubitemid 40719485)
67. Kozar, R. A.; Weibel, C. J.; Cipolla, J.; Klein, A. J.; Haber, M. M.; Abedin, M. Z.; Trooskin, S. Z. Antioxidant enzymes are induced during recovery from acute lung injury. Crit. Care Med. 2000, 28 (7), 2486-91. (Pubitemid 30604458)
68. Kubo, E.; Hasanova, N.; Tanaka, Y.; Fatma, N.; Takamura, Y.; Singh, D. P.; Akagi, Y. Protein expression profiling of lens epithelial cells from Prdx6-depleted mice and their vulnerability to UV radiation exposure. Am. J. Physiol. Cell Physiol. , 298 (2), C342-54.
69. Holcik, M.; Gordon, B. W.; Korneluk, R. G. The internal ribosome entry site-mediated translation of antiapoptotic protein XIAP is modulated by the heterogeneous nuclear ribonucleoproteins C1 and C2. Mol. Cell. Biol. 2003, 23 (1), 280-8. (Pubitemid 36008520)
70. Cheng, E. H.; Sheiko, T. V.; Fisher, J. K.; Craigen, W. J.; Korsmeyer, S. J. VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 2003, 301 (5632), 513-7. (Pubitemid 36900308)
71. Kile, B. T.; Panopoulos, A. D.; Stirzaker, R. A.; Hacking, D. F.; Tahtamouni, L. H.; Willson, T. A.; Mielke, L. A.; Henley, K. J.; Zhang, J. G.; Wicks, I. P.; Stevenson, W. S.; Nurden, P.; Watowich, S. S.; Justice, M. J. Mutations in the cofilin partner Aip1/Wdr1 cause autoinflammatory disease and macrothrombocytopenia. Blood 2007, 110 (7), 2371-80. (Pubitemid 47523157)
72. White, S. R.; Williams, P.; Wojcik, K. R.; Sun, S.; Hiemstra, P. S.; Rabe, K. F.; Dorscheid, D. R. Initiation of apoptosis by actin cytoskeletal derangement in human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 2001, 24 (3), 282-94. (Pubitemid 32228376)
73. Gourlay, C. W.; Ayscough, K. R. The actin cytoskeleton: a key regulator of apoptosis and ageing. Nat. Rev. Mol. Cell Biol. 2005, 6 (7), 583-9. (Pubitemid 40943049)
74. Phillips, A. C.; Vousden, K. H. E2F-1 induced apoptosis. Apoptosis 2001, 6 (3), 173-82. (Pubitemid 32423726)
75. Wang, S.; Nath, N.; Fusaro, G.; Chellappan, S. Rb and prohibitin target distinct regions of E2F1 for repression and respond to different upstream signals. Mol. Cell. Biol. 1999, 19 (11), 7447-60. (Pubitemid 29493408)
76. Fusaro, G.; Wang, S.; Chellappan, S. Differential regulation of Rb family proteins and prohibitin during camptothecin-induced apoptosis. Oncogene 2002, 21 (29), 4539-48. (Pubitemid 34785730)
77. Grisendi, S.; Mecucci, C.; Falini, B.; Pandolfi, P. P. Nucleophosmin and cancer. Nat. Rev. Cancer 2006, 6 (7), 493-505. (Pubitemid 43980539)
78. Lee, H. Z.; Wu, C. H.; Chang, S. P. Release of nucleophosmin from the nucleus: Involvement in aloe-emodin-induced human lung non small carcinoma cell apoptosis. Int. J. Cancer 2005, 113 (6), 971-6.
79. Mehlen, P.; Coronas, V.; Ljubic-Thibal, V.; Ducasse, C.; Granger, L.; Jourdan, F.; Arrigo, A. P. Small stress protein Hsp27 accumulation during dopamine-mediated differentiation of rat olfactory neurons counteracts apoptosis. Cell Death Differ. 1999, 6 (3), 227-33. (Pubitemid 29145826)
80. Pandey, P.; Saleh, A.; Nakazawa, A.; Kumar, S.; Srinivasula, S. M.; Kumar, V.; Weichselbaum, R.; Nalin, C.; Alnemri, E. S.; Kufe, D.; Kharbanda, S. Negative regulation of cytochrome c-mediated oligomerization of Apaf-1 and activation of procaspase-9 by heat shock protein 90. EMBO J. 2000, 19 (16), 4310-22. (Pubitemid 30623742)
81. Sur, R.; Lyte, P. A.; Southall, M. D. Hsp27 regulates pro- inflammatory mediator release in keratinocytes by modulating NF-kappaB signaling. J. Invest. Dermatol. 2008, 128 (5), 1116-22. (Pubitemid 351543202)
82. Park, K. J.; Gaynor, R. B.; Kwak, Y. T. Heat shock protein 27 association with the I kappa B kinase complex regulates tumor necrosis factor alpha-induced NF-kappa B activation. J. Biol. Chem. 2003, 278 (37), 35272-8.
83. Bialik, S.; Berissi, H.; Kimchi, A. A high throughput proteomics screen identifies novel substrates of death-associated protein kinase. Mol. Cell. Proteomics 2008, 7 (6), 1089-98. (Pubitemid 351943956)
84. Casas, C.; Ribera, J.; Esquerda, J. E. Antibodies against c-Jun N-terminal peptide cross-react with neo-epitopes emerging after caspase-mediated proteolysis during apoptosis. J. Neurochem. 2001 , 77 (3), 904-15. (Pubitemid 32466787)
85. Mourtada-Maarabouni, M.; Kirkham, L.; Farzaneh, F.; Williams, G. T. Functional expression cloning reveals a central role for the receptor for activated protein kinase C 1 (RACK1) in T cell apoptosis. J. Leukoc. Biol. 2005, 78 (2), 503-14. (Pubitemid 41061322)
86. Bardales, R. H.; Xie, S. S.; Schaefer, R. F.; Hsu, S. M. Apoptosis is a major pathway responsible for the resolution of type II pneumocytes in acute lung injury. Am. J. Pathol. 1996, 149 (3), 845-52. (Pubitemid 26334168)
87. Debret, R.; El Btaouri, H.; Duca, L.; Rahman, I.; Radke, S.; Haye, B.; Sallenave, J. M.; Antonicelli, F. Annexin A1 processing is associated with caspase-dependent apoptosis in BZR cells. FEBS Lett. 2003, 546 (2-3), 195-202. (Pubitemid 36782410)
88. Rhee, H. J.; Kim, G. Y.; Huh, J. W.; Kim, S. W.; Na, D. S. Annexin I is a stress protein induced by heat, oxidative stress and a sulfhydryl-reactive agent. Eur. J. Biochem. 2000, 267 (11), 3220-5. (Pubitemid 30341148)
89. Kondoh, H.; Lleonart, M. E.; Bernard, D.; Gil, J. Protection from oxidative stress by enhanced glycolysis; a possible mechanism of cellular immortalization. Histol. Histopathol. 2007, 22 (1), 85-90. (Pubitemid 46117093)
90. Lelli, S. M.; San Martin de Viale, L. C.; Mazzetti, M. B. Response of glucose metabolism enzymes in an acute porphyria model. Role of reactive oxygen species. Toxicology 2005, 216 (1), 49-58. (Pubitemid 41531258)
91. Wang, M.; Xiao, G. G.; Li, N.; Xie, Y.; Loo, J. A.; Nel, A. E. Use of a fluorescent phosphoprotein dye to characterize oxidative stress- induced signaling pathway components in macrophage and epithelial cultures exposed to diesel exhaust particle chemicals. Electrophoresis 2005, 26 (11), 2092-108. (Pubitemid 40852641)
92. Orsatti, L.; Forte, E.; Tomei, L.; Caterino, M.; Pessi, A.; Talamo, F. 2-D Difference in gel electrophoresis combined with Pro-Q Diamond staining: a successful approach for the identification of kinase/phosphatase targets. Electrophoresis 2009, 30 (14), 2469-76.
93. Banki, K.; Hutter, E.; Gonchoroff, N. J.; Perl, A. Molecular ordering in HIV-induced apoptosis. Oxidative stress, activation of caspases, and cell survival are regulated by transaldolase. J. Biol. Chem. 1998, 273 (19), 11944-53. (Pubitemid 28272104)
94. Lachaise, F.; Martin, G.; Drougard, C.; Perl, A.; Vuillaume, M.; Wegnez, M.; Sarasin, A.; Daya-Grosjean, L. Relationship between posttranslational modification of transaldolase and catalase deficiency in UV-sensitive repair-deficient xeroderma pigmentosum fibroblasts and SV40-transformed human cells. Free Radic. Biol. Med. 2001, 30 (12), 1365-73. (Pubitemid 32522951)
95. Shetty, S. Regulation of urokinase receptor mRNA stability by hnRNP C in lung epithelial cells. Mol. Cell. Biochem. 2005, 272 (1-2), 107-18. (Pubitemid 40867371)
96. Velusamy, T.; Shetty, P.; Bhandary, Y. P.; Liu, M. C.; Shetty, S.; Posttranscriptional regulation of urokinase receptor expression by heterogeneous nuclear ribonuclear protein, C. Biochemistry 2008, 47 (24), 6508-17. (Pubitemid 351874242)
97. Jin, X.; Wang, L. S.; Xia, L.; Zheng, Y.; Meng, C.; Yu, Y.; Chen, G. Q.; Fang, N. Y. Hyper-phosphorylation of alpha-enolase in hypertrophied left ventricle of spontaneously hypertensive rat. Biochem. Biophys. Res. Commun. 2008, 371 (4), 804-9.
98. Jung, H.; Seong, H. A.; Manoharan, R.; Ha, H. Serine-threonine kinase receptor-associated protein inhibits apoptosis signal- regulating kinase 1 function through direct interaction. J. Biol. Chem. , 285 (1), 54-70.
99. Christian, K. J.; Lang, M. A.; Raffalli-Mathieu, F. Interaction of heterogeneous nuclear ribonucleoprotein C1/C2 with a novel cisregulatory element within p53 mRNA as a response to cytostatic drug treatment. Mol. Pharmacol. 2008, 73 (5), 1558-67. (Pubitemid 351574845)
100. Stone, J. R.; Maki, J. L.; Collins, T. Basal and hydrogen peroxide stimulated sites of phosphorylation in heterogeneous nuclear ribonucleoprotein C1/C2. Biochemistry 2003, 42 (5), 1301-8. (Pubitemid 36184071)
101. Rossner, P., Jr.; Svecova, V.; Milcova, A.; Lnenickova, Z.; Solansky, I.; Sram, R. J. Seasonal variability of oxidative stress markers in city bus drivers Part II. Oxidative damage to lipids and proteins. Mutat. Res. 2008, 642 (1-2), 21-7.
102. Adams, J. M. Ways of dying: multiple pathways to apoptosis. Genes Dev. 2003, 17 (20), 2481-95. (Pubitemid 37271417)
103. Xiao, G. G.; Wang, M.; Li, N.; Loo, J. A.; Nel, A. E. Use of proteomics to demonstrate a hierarchical oxidative stress response to diesel exhaust particle chemicals in a macrophage cell line. J. Biol. Chem. 2003, 278 (50), 50781-90. (Pubitemid 37548927)
104. Liu, M. J.; Takahashi, Y.; Wada, T.; He, J.; Gao, J.; Tian, Y.; Li, S.; Xie, W. The aldo-keto reductase Akr1b7 gene is a common transcriptional target ofxenobiotic receptors pregnane Xreceptor and constitutive androstane receptor. Mol. Pharmacol. 2009, 76 (3), 604-11.
105. Stoilov, I.; Jansson, I.; Sarfarazi, M.; Schenkman, J. B. Roles of cytochrome p450 in development. Drug Metabol. Drug Interact. 2001, 18 (1), 33-55. (Pubitemid 32291033)
106. Sladek, N. E. Transient induction of increased aldehyde dehy- drogenase 3A1 levels in cultured human breast (adeno)carcinoma cell lines via 5'-upstream xenobiotic, and electrophile, responsive elements is, respectively, estrogen receptor-dependent and -independent. Chem. Biol. Interact. 2003, 143 (144), 63-74. (Pubitemid 36253579)