Cellular transformation by cigarette smoke extract involves alteration of glycolysis and mitochondrial function in esophageal epithelial cells

International Journal of Cancer

Volumn 127, Issue 2, 2010, Pages 269-281

  Kim, Myoung Sook ^a   Huang, Yiping ^a   Lee, Juna ^a   Zhong, Xiaoli ^a   Jiang, Wei Wen ^a   Ratovitski, Edward A ^a   Sidransky, David ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cigarette smoke extract; Esophageal cancer; Glycolysis

Indexed keywords

ADENOSINE TRIPHOSPHATE; CIGARETTE SMOKE; GLUCOSE; LACTIC ACID; NERVE CELL ADHESION MOLECULE; UVOMORULIN; VIMENTIN; CADHERIN; DEOXYGLUCOSE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL GROWTH; CELL INVASION; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; ESOPHAGUS MUCOSA; GENE EXPRESSION; GLYCOLYSIS; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PRIORITY JOURNAL; CELL CULTURE; DRUG EFFECT; DRUG RESISTANCE; ESOPHAGUS TUMOR; FLOW CYTOMETRY; GENETICS; METABOLISM; OXYGEN CONSUMPTION; PATHOLOGY; RESPIRATORY TRACT MUCOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOKING; SQUAMOUS CELL CARCINOMA; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; BLOTTING, WESTERN; CADHERINS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; DEOXYGLUCOSE; DRUG RESISTANCE, NEOPLASM; ESOPHAGEAL NEOPLASMS; FLOW CYTOMETRY; GLYCOLYSIS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NEOPLASMS, SQUAMOUS CELL; OXYGEN CONSUMPTION; REACTIVE OXYGEN SPECIES; RESPIRATORY MUCOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SMOKING;

EID: 77953706284     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25057     Document Type: Article

References (67)

1. WHO. The World Health Report. Geneva, Switzerland, 1997.
2. Goseki N, Koike M, Yoshida M. Histopathologic characteristics of early stage esophageal carcinoma. A comparative study with gastric carcinoma. Cancer 1992;69:1088-93.
3. Shimada Y, Watanabe G, Kawamura J, Soma T, Okabe M, Ito T, Inoue H, Kondo M, Mori Y, Tanaka E, Imamura M. Clinical significance of osteopontin in esophageal squamous cell carcinoma: comparison with common tumor markers. Oncology 2005;68: 285-92.
4. Brockmann JG, St Nottberg H, Glodny B, Heinecke A, Senninger NJ. CYFRA 21-1 serum analysis in patients with esophageal cancer. Clin Cancer Res 2000;6:4249-52.
5. Stoner GD, Gupta A. Etiology and chemoprevention of esophageal squamous cell carcinoma. Carcinogenesis 2001;22: 1737-46.
6. Husgafvel-Pursiainen K. Genotoxicity of environmental tobacco smoke: a review. Mutat Res 2004;567:427-45.
7. Nishikawa A, Mori Y, Lee IS, Tanaka T, Hirose M. Cigarette smoking, metabolic activation and carcinogenesis. Curr Drug Metab 2004;5:363-73. (Pubitemid 39276601)
8. Smith CJ, Hansch C. The relative toxicity of compounds in mainstream cigarette smoke condensate. Food Chem Toxicol 2000;38:637-46. (Pubitemid 30624144)
9. Hecht SS. Tobacco smoke carcinogens and breast cancer. Environ Mol Mutagen 2002; 39:119-26.
10. Stabbert R, Voncken P, Rustemeier K, Haussmann HJ, Roemer E, Schaffernicht H, Patskan G. Toxicological evaluation of an electrically heated cigarette. II. Chemical composition of mainstream smoke. J Appl Toxicol 2003;23:329-39. (Pubitemid 37185413)
11. DeMarini DM. Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Mutat Res 2004;567:447-74.
12. Narayan S, Jaiswal AS, Kang D, Srivastava P, Das GM, Gairola CG. Cigarette smoke condensate-induced transformation of normal human breast epithelial cells in vitro. Oncogene 2004;23:5880-9. (Pubitemid 39093532)
13. Kundu CN, Balusu R, Jaiswal AS, Gairola CG, Narayan S. Cigarette smoke condensate-induced level of adenomatous polyposis coli blocks long-patch base excision repair in breast epithelial cells. Oncogene 2007;26:1428-38. (Pubitemid 46340812)
14. Jaiswal AS, Aneja R, Connors SK, Joshi HC, Multani AS, Pathak S, Narayan S. 9- bromonoscapine-induced mitotic arrest of cigarette smoke condensate-transformed breast epithelial cells. J Cell Biochem 2009; 106:1146-56.
15. Kaushik G, Kaushik T, Khanduja S, Pathak CM, Khanduja KL. Cigarette smoke condensate promotes cell proliferation through disturbance in cellular redox homeostasis of transformed lung epithelial type-II cells. Cancer Lett 2008;270:120-31.
16. Zhang L, Wu R, Dingle RW, Gairola CG, Valentino J, Swanson HI. Cigarette smoke condensate and dioxin suppress culture shock induced senescence in normal human oral keratinocytes. Oral Oncol 2007; 43:693-700. (Pubitemid 47058371)
17. Ramage L, Jones AC, Whelan CJ. Induction of apoptosis with tobacco smoke and related products in A549 lung epithelial cells in vitro. J Inflamm (Lond) 2006;3:3. (Pubitemid 43759264)
18. Carter CA, Hamm JT. Multiplexed quantitative high content screening reveals that cigarette smoke condensate induces changes in cell structure and function through alterations in cell signaling pathways in human bronchial cells. Toxicology 2009;261:89-102.
19. Warburg O. On the origin of cancer cells. Science 1956;123:309-14.
20. Unwin RD, Craven RA, Harnden P, Hanrahan S, Totty N, Knowles M, Eardley I, Selby PJ, Banks RE. Proteomic changes in renal cancer and co-ordinate demonstration of both the glycolytic and mitochondrial aspects of the Warburg effect. Proteomics 2003;3:1620-32.
21. Tuttle SW, Maity A, Oprysko PR, Kachur AV, Ayene IS, Biaglow JE, Koch CJ. Detection of reactive oxygen species via endogenous oxidative pentose phosphate cycle activity in response to oxygen concentration: implications for the mechanism of HIF-1alpha stabilization under moderate hypoxia. J Biol Chem 2007;282:36790-6.
22. Langbein S, Frederiks WM, zur Hausen A, Popa J, Lehmann J, Weiss C, Alken P, Coy JF. Metastasis is promoted by a bioenergetic switch: new targets for progressive renal cell cancer. Int J Cancer 2008;122:2422-8.
23. Rathmell JC, Fox CJ, Plas DR, Hammerman PS, Cinalli RM, Thompson CB. Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-independent survival. Mol Cell Biol 2003;23: 7315-28.
24. Kaluz S, Kaluzová M, Chrastina A, Olive PL, Pastoreková S, Pastorek J, Lerman MI, Stanbridge EJ. Lowered oxygen tension induces expression of the hypoxia marker MN/carbonic anhydrase IX in the absence of hypoxia-inducible factor 1 alpha stabilization: a role for phosphatidylinositol 30-kinase. Cancer Res 2002;62:4469-77.
25. Isidoro A, Martínez M, Fernández PL, Ortega AD, Santamaría G, Chamorro M, Reed JC, Cuezva JM. Alteration of the bioenergetic phenotype of mitochondria is a hallmark of breast, gastric, lung and oesophageal cancer. Biochem J 2004;378: 17-20.
26. Kulawiec M, Arnouk H, Desouki MM, Kazim L, Still I, Singh KK. Proteomic analysis of mitochondria-to-nucleus retrograde response in human cancer. Cancer Biol Ther 2006;5:967-75.
27. Amuthan G, Biswas G, Ananadatheerthavarada HK, Vijayasarathy C, Shephard HM, Avadhani NG. Mitochondrial stress-induced calcium signaling, phenotypic changes and invasive behavior in human lung carcinoma A549 cells. Oncogene 2002;21:7839-49.
28. Tan D, Goerlitz DS, Dumitrescu RG, Han D, Seillier-Moiseiwitsch F, Spernak SM, Orden RA, Chen J, Goldman R, Shields PG. Associations between cigarette smoking and mitochondrial DNA abnormalities in buccal cells. Carcinogenesis 2008;29:1170-7.
29. Jin Z, Gao F, Flagg T, Deng X. Tobacco-specific nitrosamine 4- (methylnitrosamino)-1-(3-pyridyl)-1-butanone promotes functional cooperation of Bcl2 and c-Myc through phosphorylation in regulating cell survival and proliferation. J Biol Chem 2004;279:40209-19.
30. Palozza P, Sheriff A, Serini S, Boninsegna A, Maggiano N, Ranelletti FO, Calviello G, Cittadini A. Lycopene induces apoptosis in immortalized fibroblasts exposed to tobacco smoke condensate through arresting cell cycle and down-regulating cyclin D1, pAKT and pBad. Apoptosis 2005;10:1445-56.
31. Low B, Liang M, Fu J. p38 mitogen-activated protein kinase mediates sidestream cigarette smoke-induced endothelial permeability. J Pharmacol Sci 2007;104:225-31. (Pubitemid 47122470)
32. Kim MS, Chang X, Yamashita K, Nagpal JK, Baek JH, Wu G, Trink B, Ratovitski EA, Mori M, Sidransky D. Aberrant promoter methylation and tumor suppressive activity of the DFNA5 gene in colorectal carcinoma. Oncogene 2008;27: 3624-34. (Pubitemid 351793800)
33. Lee W, Choi HI, Kim MJ, Park SY. Depletion of mitochondrial DNA upregulates the expression of MDR1 gene via an increase in mRNA stability. Exp Mol Med 2008;40:109-17. (Pubitemid 351346823)
34. Yu M, Zhou Y, Shi Y, Ning L, Yang Y, Wei X, Zhang N, Hao X, Niu R. Reduced mitochondrial DNA copy number is correlated with tumor progression and prognosis in Chinese breast cancer patients. IUBMB Life 2007;59:450-7. (Pubitemid 47124001)
35. Ongwijitwat S, Liang HL, Graboyes EM, Wong-Riley MT. Nuclear respiratory factor 2 senses changing cellular energy demands and its silencing down-regulates cytochrome oxidase and other target gene mRNAs. Gene 2006;374:39-49. (Pubitemid 43737128)
36. Zhang H, Gao P, Fukuda R, Kumar G, Krishnamachary B, Zeller KI, Dang CV, Semenza GL. HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 2007;11: 407-20. (Pubitemid 46670080)
37. Li F, Wang Y, Zeller KI, Potter JJ, Wonsey DR, O'Donnell KA, Kim JW, Yustein JT, Lee LA, Dang CV. Myc stimulates nuclearly encoded mitochondrial genes and mitochondrial biogenesis. Mol Cell Biol 2005;25:6225-34.
38. Zou CP, Youssef EM, Zou CC, Carey TE, Lotan R. Differential effects of chromosome 3p deletion on the expression of the putative tumor suppressor RAR beta and on retinoid resistance in human squamous carcinoma cells. Oncogene 2001; 20:6820-7.
39. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 2006;3:187-97.
40. Elstrom RL, Bauer DE, Buzzai M, Karnauskas R, Harris MH, Plas DR, Zhuang H, Cinalli RM, Alavi A, Rudin CM, Thompson CB. Akt stimulates aerobic glycolysis in cancer cells. Cancer Res 2004; 64:3892-9.
41. Kawauchi K, Araki K, Tobiume K, Tanaka N. p53 regulates glucose metabolism through an IKK-NF-kappaB pathway and inhibits cell transformation. Nat Cell Biol 2008;10:611-18.
42. Cuezva JM, Krajewska M, de Heredia ML, Krajewski S, Santamaría G, Kim H, Zapata JM, Marusawa H, Chamorro M, Reed JC. The bioenergetic signature of cancer: a marker of tumor progression. Cancer Res 2002;62:6674-81.
43. Cuezva JM, Chen G, Alonso AM, Isidoro A, Misek DE, Hanash SM, Beer DG. The bioenergetic signature of lung adenocarcinomas is a molecular marker of cancer diagnosis and prognosis. Carcinogenesis 2004;25:1157-63.
44. Liang J, Slingerland JM. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2003;2: 339-45.
45. Semenza GL. Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit Rev Biochem Mol Biol 2000;35:71-103.
46. Smith TA. Mammalian hexokinases and their abnormal expression in cancer. Br J Biomed Sci 2000;57:170-8.
47. Du XL, Hu H, Lin DC, Xia SH, Shen XM, Zhang Y, Luo ML, Feng YB, Cai Y, Xu X, Han YL, Zhan QM, et al. Proteomic profiling of proteins dysregulted in Chinese esophageal squamous cell carcinoma. J Mol Med 2007;85:863-75.
48. Kordom C, Maritz GS, De Kock M. Maternal nicotine exposure during pregnancy and lactation. I. Effect on glycolysis in the lungs of the offspring. Exp Lung Res 2003;29:79-89.
49. Bridges RB. Protective action of thiols on neutrophil function. Eur J Respir Dis Suppl 1985;139:40-8.
50. Bridges RB, Kraal JH, Huang LJ, Chancellor BM. Effects of tobacco smoke on chemotaxis and glucose metabolism of polymorphonuclear leukocytes. Infect Immun 1977;15:115-23.
51. Kennedy JR, Elliott AM. Cigarette smoke: the effect of residue on mitochondrial structure. Science 1970;168:1097-8.
52. Gairola C, Aleem MI. Cigarette smoke: effect of aqueous and nonaqueous fractions on mitochondrial function. Nature 1973; 241:287-8.
53. Hays LE, Zodrow DM, Yates JE, Deffebach ME, Jacoby DB, Olson SB, Pankow JF, Bagby GC. Cigarette smoke induces genetic instability in airway epithelial cells by suppressing FANCD2 expression. Br J Cancer 2008;98:1653-61.
54. Stern R, Shuster S, Neudecker BA, Formby B. Lactate stimulates fibroblast expression of hyaluronan and CD44: the Warburg effect revisited. Exp Cell Res 2002;276: 24-31.
55. Gatenby RA, Gawlinski ET, Gmitro AF, Kaylor B, Gillies RJ. Acid-mediated tumor invasion: a multidisciplinary study. Cancer Res 2006;66:5216-23.
56. Fischer K, Hoffmann P, Voelkl S, Meidenbauer N, Ammer J, Edinger M, Gottfried E, Schwarz S, Rothe G, Hoves S, Renner K, Timischl B, et al. Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood 2007;109:3812-19.
57. Jiao S, Liu B, Gao A, Ye M, Jia X, Zhang F, Liu H, Shi X, Huang C. Benzo (a) pyrene-caused increased G1-S transition requires the activation of c-Jun through p53-dependent PI-3K/Akt/ERK pathway in human embryo lung fibroblasts. Toxicol Lett 2008;178:167-75
58. Zhang J, Kamdar O, Le W, Rosen GD, Upadhyay D. Nicotine induces resistance to chemotherapy by modulating mitochondrial signaling in lung cancer. Am J Respir Cell Mol Biol 2009;40:135-46.
59. Su F, Overholtzer M, Besser D, Levine AJ. WISP-1 attenuates p53-mediated apoptosis in response to DNA damage through activation of the Akt kinase. Genes Dev 2002;16:46-57.
60. You Z, Saims D, Chen S, Zhang Z, Guttridge DC, Guan KL, MacDougald OA, Brown AM, Evan G, Kitajewski J, Wang CY. Wnt signaling promotes oncogenic transformation by inhibiting c-Myc-induced apoptosis. J Cell Biol 2002;157: 429-40.
61. Kometani T, Yoshino I, Miura N, Okazaki H, Ohba T, Takenaka T, Shoji F, Yano T, Maehara Y. Benzo[a]pyrene promotes proliferation of human lung cancer cells by accelerating the epidermal growth factor receptor signaling pathway. Cancer Lett 2009;278:27-33.
62. Xu J, Huang H, Pan C, Zhang B, Liu X, Zhang L. Nicotine inhibits apoptosis induced by cisplatin in human oral cancer cells. Int J Oral Maxillofac Surg 2007;36: 739-44.
63. Wong LS, Green HM, Feugate JE, Yadav M, Nothnagel EA, Martins-Green M. Effects of "second-hand" smoke on structure and function of fibroblasts, cells that are critical for tissue repair and remodeling. BMC Cell Biol 2004;5:13.
64. Gordon JE, Schoenecker PL, Osland JD, Dobbs MB, Szymanski DA, Luhmann SJ. Smoking and socio-economic status in the etiology and severity of Legg-Calvé-Perthes' disease. J Pediatr Orthop B 2004;13:367-70.
65. Duan L, Wu AH, Sullivan-Halley J, Bernstein L. Passive smoking and risk of oesophageal and gastric adenocarcinomas. Br J Cancer 2009;100:1483-5.
66. He J, Whelton PK. Passive cigarette smoking increases risk of coronary heart disease. Eur Heart J 1999;20:1764-5.
67. Schick S, Glantz S. Philip Morris toxicological experiments with fresh sidestream smoke: more toxic than mainstream smoke. Tob Control 2005;14: 396-404.