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Impact of Smoking Status on the Biological Behavior of Lung Cancer

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Abstract

Cigarette smoking is the most established risk factor for lung carcinogenesis; however, its effects on the progression of lung cancer are still unclear. We reviewed the clinical investigations on this issue, which imply that smoking status is a treatment predictor and prognostic factor for several subtypes of lung cancer. Moreover, gene alterations and various protein expressions of tumor progression were recognized more frequently in the tumor tissues of smokers than in those of the never smokers. A cellular analysis revealed that tobacco-specific chemical compounds cause genetic or epigenetic alterations, modulate expressions of large numbers of genes that include molecules related to proliferation, invasion and metastasis, and deteriorate anti-tumor immunity. Our findings suggest that smoking promotes the progression of lung cancer, and that elucidating the molecular mechanisms may help to clarify the therapeutic targets.

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References

  1. WA Pryor K Stone (1993) ArticleTitleOxidants in cigarette smoke: radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite Ann N Y Acad Sci 686 12–27 Occurrence Handle8512242 Occurrence Handle10.1111/j.1749-6632.1993.tb39148.x Occurrence Handle1:CAS:528:DyaK3sXkvVygur0%3D

    Article  PubMed  CAS  Google Scholar 

  2. GP Pfeifer MF Denissenko M Olivier N Tretyakova SS Hecht P Hainaut (2002) ArticleTitleTobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers Oncogene 21 7435–51 Occurrence Handle12379884 Occurrence Handle10.1038/sj.onc.1205803 Occurrence Handle1:CAS:528:DC%2BD38XnvVelu7s%3D

    Article  PubMed  CAS  Google Scholar 

  3. PA Wingo T Tong S Bolden (1995) ArticleTitleCancer statistics, 1995 CA Cancer J Clin 45 8–30 Occurrence Handle7528632 Occurrence Handle1:STN:280:DyaK2M7gtlektA%3D%3D Occurrence Handle10.3322/canjclin.45.1.8

    Article  PubMed  CAS  Google Scholar 

  4. AJ Farkas EA Gilpin JM Distefan JP Pierce (1999) ArticleTitleThe effect of household and workplace smoking restrictions on quitting behaviours Tobacco Control 8 261–5 Occurrence Handle10599569 Occurrence Handle1:STN:280:DC%2BD3c%2Fms1GmsA%3D%3D

    PubMed  CAS  Google Scholar 

  5. Food and Agriculture Organization of the United States (FAO). FaoStat Statistical databases. http://www.apps.fao.org/

  6. MS Jaakkola JJ Jaakkola (1997) ArticleTitleAssessment of exposure to environmental tobacco smoke Eur Respir J 10 2384–97 Occurrence Handle9387970 Occurrence Handle10.1183/09031936.97.10102384 Occurrence Handle1:CAS:528:DyaK2sXnt1Ortr4%3D

    Article  PubMed  CAS  Google Scholar 

  7. A Johnson-Early MH Cohen JD Minna LM Paxton BE Fossieck SuffixJr DC Ihde et al. (1980) ArticleTitleSmoking abstinence and small cell lung cancer survival: an association JAMA 244 2175–9 Occurrence Handle10.1001/jama.244.19.2175

    Article  Google Scholar 

  8. GMM Videtic LW Stitt R Dar WI Kocha AT Tomiak PT Truong et al. (2003) ArticleTitleContinued cigarette smoking by patients receiving concurrent chemoradiotherapy for limited-stage small-cell lung cancer is associated with decreased survival J Clin Oncol 21 1544–9 Occurrence Handle12697879 Occurrence Handle10.1200/JCO.2003.10.089

    Article  PubMed  Google Scholar 

  9. CM Tammemagi C Neslund-Dudas M Simoff P Kvale (2004) ArticleTitleSmoking and lung cancer survival: the role of comorbidity and treatment Chest 125 27–37 Occurrence Handle14718417 Occurrence Handle10.1378/chest.125.1.27

    Article  PubMed  Google Scholar 

  10. C-K Toh E-H Wong W-T Lim S-S Leong K-W Fong J Wee et al. (2004) ArticleTitleThe impact of smoking status on the behavior and survival outcome of patients with advanced non-small cell lung cancer. A retrospective analysis Chest 126 1750–6 Occurrence Handle15596669 Occurrence Handle10.1378/chest.126.6.1750

    Article  PubMed  Google Scholar 

  11. I Yoshino H Baba F Fukuyama T Kameyama Y Shikada M Tomiyasu et al. (2002) ArticleTitleA time trend of profile and surgical results in 1123 patients with non-small cell lung cancer Surgery 131 S226–31 Occurrence Handle10.1067/msy.2002.119796

    Article  Google Scholar 

  12. AS Tsao D Liu JJ Lee M Spitz WK Hong (2006) ArticleTitleSmoking affects treatment outcome in patients with advanced nonsmall cell lung cancer Cancer 106 2428–36 Occurrence Handle16634096 Occurrence Handle10.1002/cncr.21884

    Article  PubMed  Google Scholar 

  13. LT Nordquist GR Simon A Canter M Alberts G Bepler (2004) ArticleTitleImproved survival in never-smokers vs current smokers with primary adenocarcinoma of the lung Chest 126 347–51 Occurrence Handle15302716 Occurrence Handle10.1378/chest.126.2.347

    Article  PubMed  Google Scholar 

  14. D Rice HW Kim A Sabichi S Lippman JJ Lee B Williams et al. (2003) ArticleTitleThe risk of second primary lung tumors after resection of stage I nonsmall cell lung cancer Ann Thorac Surg 76 1001–7 Occurrence Handle14529975 Occurrence Handle10.1016/S0003-4975(03)00821-X

    Article  PubMed  Google Scholar 

  15. Y-C Wu C-F J Lin W-H Hsu B-S Huang M-H Huang L-S Wang (2003) ArticleTitleLong-term results of pathological stage I non-small cell lung cancer: validation of using the number of totally removed lymph nodes as a staging control Eur J Cardiothorac Surg 24 994–1001 Occurrence Handle14643819 Occurrence Handle10.1016/S1010-7940(03)00567-0

    Article  PubMed  Google Scholar 

  16. I Yoshino D Kawano T Oba K Yamazaki T Kometani et al. (2006) ArticleTitleSmoking status as a prognostic factor in patients with stage I pulmonary adenocarcinoma Ann Thorac Surg 81 1189–93 Occurrence Handle16564239 Occurrence Handle10.1016/j.athoracsur.2005.09.028

    Article  PubMed  Google Scholar 

  17. I Yoshino A Osoegawa T Yohena T Kameyama E Oki S Oda et al. (2005) ArticleTitleLoss of heterozygosity in non-small cell lung cancer: difference between adenocarcinoma and squamous cell carcinoma Resp Med 99 308–12 Occurrence Handle10.1016/j.rmed.2004.08.008

    Article  Google Scholar 

  18. I Yoshino S Fukuyama T Kameyama H Baba Y Shikada R Suemitsu et al. (2003) ArticleTitleDetection of loss of heterozygosity by high-resolution fluorescent system in non-small cell lung cancer: association of loss of heterozygosity with smoking and tumor progression Chest 123 545–50 Occurrence Handle12576379 Occurrence Handle10.1378/chest.123.2.545 Occurrence Handle1:CAS:528:DC%2BD3sXhslKmt7Y%3D

    Article  PubMed  CAS  Google Scholar 

  19. L Mao JS Lee JM Kurie YH Fan SM Lippman JJ Lee et al. (1997) ArticleTitleClonal genetic alterations in the lungs of current and former smokers J Natl Cancer Inst 89 857–62 Occurrence Handle9196251 Occurrence Handle10.1093/jnci/89.12.857 Occurrence Handle1:CAS:528:DyaK2sXlsFensbw%3D

    Article  PubMed  CAS  Google Scholar 

  20. G Sozzi L Sard L De Gregorio A Marchetti K Musso F Buttitta et al. (1997) ArticleTitleAssociation between cigarette smoking and FHIT gene alterations in lung cancer Cancer Res 57 2121–3 Occurrence Handle9187107 Occurrence Handle1:CAS:528:DyaK2sXjslGju7o%3D

    PubMed  CAS  Google Scholar 

  21. JS Kim H Kim YM Shim J Han J Park DH Kim (2004) ArticleTitleAberrant methylation of the FHIT gene in chronic smokers with early stage squamous cell carcinoma of the lung Carcinogenesis 25 2165–71 Occurrence Handle15231689 Occurrence Handle10.1093/carcin/bgh217 Occurrence Handle1:CAS:528:DC%2BD2cXhtVWgs73N

    Article  PubMed  CAS  Google Scholar 

  22. R Maruyama K Sugio I Yoshino Y Maehara AF Gazdar (2004) ArticleTitleHypermethylation of the FHIT as a prognostic marker in nonsmall cell lung cancer Cancer 100 1472–7 Occurrence Handle15042681 Occurrence Handle10.1002/cncr.20144 Occurrence Handle1:CAS:528:DC%2BD2cXjt1Sru7o%3D

    Article  PubMed  CAS  Google Scholar 

  23. Y Daigaku K Endo E Watanabe T Ono K Yamamoto (2004) ArticleTitleLoss of heterozygosity and DNA damage repair in Saccharomyces cervisiae Mutat Res 22 183–91

    Google Scholar 

  24. IYS Tam LP Chung WS Suen E Wang MCM Wong KK Ho et al. (2006) ArticleTitleDistinct epidermal growth factor receptor and KRAS mutation patterns in non-small cell lung cancer patients with different tobacco exposure and clinicopathologic features Clin Cancer Res 12 1647–53 Occurrence Handle16533793 Occurrence Handle10.1158/1078-0432.CCR-05-1981 Occurrence Handle1:CAS:528:DC%2BD28XitVGmsb8%3D

    Article  PubMed  CAS  Google Scholar 

  25. GP Pfifer P Hainaut (2003) ArticleTitleOn the origin of G → T transversions in lung cancer Mutat Res 526 39–43

    Google Scholar 

  26. Y Fukuyama T Mitsudomi K Sugio T Ishida K Akazawa K Sugimachi (1997) ArticleTitleK-ras and p53 mutations are an independent unfavorable prognostic indicators in patients with non-small cell lung cancer Br J Cancer 78 1125–30

    Google Scholar 

  27. N Hagiwara LE Mechanic GE Trivers HL Cawley M Taga ED Bowman et al. (2006) ArticleTitleQuantitative detection of p53 mutations in plasma DNA from tobacco smokers Cancer Res 66 8309–17 Occurrence Handle16912213 Occurrence Handle10.1158/0008-5472.CAN-06-0991 Occurrence Handle1:CAS:528:DC%2BD28XotFWqu78%3D

    Article  PubMed  CAS  Google Scholar 

  28. T Winton R Livingston D Johnson J Rigas M Johnston C Butts et al. (2005) ArticleTitleNational Cancer Institute of Canada Clinical Trials Group; National Cancer Institute of the United States Intergroup JBR.10 Trial Investigators. Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer N Engl J Med 352 2589–97 Occurrence Handle15972865 Occurrence Handle10.1056/NEJMoa043623 Occurrence Handle1:CAS:528:DC%2BD2MXls1Wqurg%3D

    Article  PubMed  CAS  Google Scholar 

  29. F Le Calvez A Mukeria JD Hunt O Kelm RJ Hung P Taniere et al. (2005) ArticleTitleTP53 and KRAS mutation load and types in lung cancers in relation to tobacco smoke: distinct patterns in never, former, and current smokers Cancer Res 65 5076–83 Occurrence Handle15958551 Occurrence Handle10.1158/0008-5472.CAN-05-0551 Occurrence Handle1:CAS:528:DC%2BD2MXltFemtbo%3D

    Article  PubMed  CAS  Google Scholar 

  30. TM Greatens GA Niehans JB Rubins J Jessurun RA Kratzke MA Maddaus et al. (1998) ArticleTitleDo molecular markers predict survival in non-small-cell lung cancer? Am J Resp Crit Med 157 1093–7 Occurrence Handle1:STN:280:DyaK1c3itlaisQ%3D%3D

    CAS  Google Scholar 

  31. R Ahuja SB Weibel FT Leone (2003) ArticleTitleLung cancer: the oncologist's role in smoking cessation Sem Oncol 30 94–103 Occurrence Handle10.1053/sonc.2003.50000

    Article  Google Scholar 

  32. MT Halpen BW Gillespi KE Warner (1993) ArticleTitlePatterns of absolute risk of lung cancer mortality in former smokers J Natl Cancer Inst 85 457–64 Occurrence Handle10.1093/jnci/85.6.457

    Article  Google Scholar 

  33. Z Zhang J Ma N Sun C Wang (2006) ArticleTitleExpression of nuclear factor-kappa V and its clinical significance in nonsmall-cell lung cancer Ann Thorac Surg 82 243–8 Occurrence Handle16798222 Occurrence Handle10.1016/j.athoracsur.2006.01.049

    Article  PubMed  Google Scholar 

  34. M Pagano S Tam A Theodoras P Beer-Romero G Del Sal V Chau et al. (1995) ArticleTitleRole of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27 Science 269 682–5 Occurrence Handle7624798 Occurrence Handle10.1126/science.7624798 Occurrence Handle1:CAS:528:DyaK2MXntlCltrc%3D

    Article  PubMed  CAS  Google Scholar 

  35. M Gstaiger R Jordan M Lim C Catzavelos J Mestan J Slingerland et al. (2001) ArticleTitleSkp2 is oncogenic and overexpressed in human cancers Proc Natl Acad Sci USA 98 5043–8 Occurrence Handle11309491 Occurrence Handle10.1073/pnas.081474898 Occurrence Handle1:CAS:528:DC%2BD3MXjt1Ogu7c%3D

    Article  PubMed  CAS  Google Scholar 

  36. A Osoegawa I Yoshino S Tanaka K Sugio T Kameyama M Yamaguchi et al. (2004) ArticleTitleRegulation of p27 by S-phase kinase-associated protein 2 is associated with aggressiveness in non-small cell lung cancer J Clin Oncol 22 4165–73 Occurrence Handle15483027 Occurrence Handle10.1200/JCO.2004.01.035 Occurrence Handle1:CAS:528:DC%2BD2cXpslOrsL0%3D

    Article  PubMed  CAS  Google Scholar 

  37. Y Shinohara J Ichihara H Terada (1991) ArticleTitleRemarkablyenhanced expression of the type II hexokinase in rat hepatoma cell line AH130 FEBS Lett 291 55–7 Occurrence Handle1936251 Occurrence Handle10.1016/0014-5793(91)81102-E Occurrence Handle1:CAS:528:DyaK3MXmt12nsLc%3D

    Article  PubMed  CAS  Google Scholar 

  38. I Yoshino T Kameyama Y Shikada T Kometani D Kawano A Osoegawa et al. (2005) ArticleTitleGlycolytic phenotype of non-small cell lung cancer: implication of anaerobic glycolysis on malignant potential J Clin Oncol 24s 9634

    Google Scholar 

  39. J Bernhagen T Calandra RA Mitchell SB Martin KJ Tracey W Voelter et al. (1993) ArticleTitleMIF is a pituitary-derived cytokine that potentiates lethal endotoxemia Nature 365 756–9 Occurrence Handle8413654 Occurrence Handle10.1038/365756a0 Occurrence Handle1:CAS:528:DyaK2cXivVClsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  40. T Calandra J Bernhagen RA Mitchell R Bucala (1994) ArticleTitleThe macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor J Exp Med 179 1895–902 Occurrence Handle8195715 Occurrence Handle10.1084/jem.179.6.1895 Occurrence Handle1:CAS:528:DyaK2cXis1Ortrg%3D

    Article  PubMed  CAS  Google Scholar 

  41. M Tomiyasu I Yoshino R Suemitsu T Okamoto K Sugimachi (2002) ArticleTitleQuantification of MIF mRNA expression in non small cell lung cancer tissues and its clinical significance Clin Cancer Res 8 3755–60 Occurrence Handle12473586 Occurrence Handle1:CAS:528:DC%2BD38XpslCjt70%3D

    PubMed  CAS  Google Scholar 

  42. Y Nakanishi XH Pei K Takayama F Bai M Izumi K Kimotsuki et al. (2000) ArticleTitlePolycyclic aromatic hydrocarbon carcinogens increase ubiquitination of p21 protein after the stabilization of p53 and the expression of p21 Am J Respir Cell Mol Biol 22 747–54 Occurrence Handle10837373 Occurrence Handle1:CAS:528:DC%2BD3cXksVKgsbw%3D

    PubMed  CAS  Google Scholar 

  43. XH Pei Y Nakanishi H Inoue K Takayama F Bai N Hara (2002) ArticleTitlePolycyclic aromatic hydrocarbons induce IL-8 expression through nuclear factor κB activation in A549 cell line Cytokine 19 236–41 Occurrence Handle12393170 Occurrence Handle10.1016/S1043-4666(02)91967-8 Occurrence Handle1:CAS:528:DC%2BD38XnvVentbw%3D

    Article  PubMed  CAS  Google Scholar 

  44. DR Smith PJ Polverini SL Kunkel MB Orringer RI Whyte MD Burdick et al. (1994) ArticleTitleInhibition of interleukin 8 attenuates angiogenesis in bronchogenic carcinoma J Exp Med 179 1409–15 Occurrence Handle7513008 Occurrence Handle10.1084/jem.179.5.1409 Occurrence Handle1:CAS:528:DyaK2cXisVahtLg%3D

    Article  PubMed  CAS  Google Scholar 

  45. MDF Askari MS Tsao HM Schuller (2005) ArticleTitleThe tobacco-specific carcinogen, 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone stimulates proliferation of immortalized human pancreatic duct epithelia through β-adrenergic transactivation of EGF receptors J Cancer Res Clin Oncol 131 639–48 Occurrence Handle16091975 Occurrence Handle10.1007/s00432-005-0002-7 Occurrence Handle1:CAS:528:DC%2BD2MXhtFartL%2FN

    Article  PubMed  CAS  Google Scholar 

  46. H Lemjabbar D Li M Gallup S Sidhu E Drori C Basbaum (2003) ArticleTitleTobacco smoke-induced lung cell proliferation mediated by tumor necrosis factor α-converting enzyme and amphiregulin J Biol Chem 278 26202–7 Occurrence Handle12711607 Occurrence Handle10.1074/jbc.M207018200 Occurrence Handle1:CAS:528:DC%2BD3sXlt1CltLc%3D

    Article  PubMed  CAS  Google Scholar 

  47. EK Chu JS Foley J Cheng AS Patel JM Drazen DJ Tschumperlin (2005) ArticleTitleBronchial epithelial compression regulates epidermal growth factor receptor family ligand expression in an autocrine manner Am J Respr Cell Mole Biol 32 373–80 Occurrence Handle10.1165/rcmb.2004-0266OC Occurrence Handle1:CAS:528:DC%2BD2MXktVCgtbo%3D

    Article  CAS  Google Scholar 

  48. C Mascaux B Martin M Paesmans T Berghmans M Dusart A Haller et al. (2006) ArticleTitleHas Cox-2 a prognostic factor in non-small-cell lung cancer? A systematic review of the literature with meta-analysis of the survival results Br J Cancer 95 139–45 Occurrence Handle16786043 Occurrence Handle10.1038/sj.bjc.6603226 Occurrence Handle1:CAS:528:DC%2BD28XmvFajs70%3D

    Article  PubMed  CAS  Google Scholar 

  49. D Moraitis B Du MS De Lorenzo JO Boyle BB Weksler EG Cohen et al. (2005) ArticleTitleLevels of cyclooxigenase-2 are increased in the oral mucosa of smokers: evidence for the role of epidermal growth factor receptor and its ligands Cancer Res 65 654–70

    Google Scholar 

  50. CA Martey SJ Pollock CK Turner KMA O'Reilly CJ Banglole RP Phipps et al. (2004) ArticleTitleCigarette smoke induce cycooxigenase-2 and microsomal prostaglandine E2 synthase in human lung fibroblasts: implications for lung inflammation and cancer Am J Physiol Lung Cell Mol Physiol 287 L981–91 Occurrence Handle15234907 Occurrence Handle10.1152/ajplung.00239.2003 Occurrence Handle1:CAS:528:DC%2BD2cXhtVaqsLrO

    Article  PubMed  CAS  Google Scholar 

  51. M Nagayama A Sato H Hayakawa T Urano Y Takada A Takada (1994) ArticleTitlePlasminogen activators and their inhibitors in non-small cell lung cancer Cancer 73 1398–405 Occurrence Handle8111706 Occurrence Handle10.1002/1097-0142(19940301)73:5<1398::AID-CNCR2820730514>3.0.CO;2-9 Occurrence Handle1:STN:280:DyaK2c7lsFWiuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  52. H Pederses N Brunner D Francis K ÖSterlind E Rønne HH Hansen et al. (1994) ArticleTitlePrognostic impact of urokinase, urokinase receptor and type 1 plasminogen activator inhibitor in squamous and large cell lung cancer tissue Cancer Res 54 4671–5

    Google Scholar 

  53. H Rapport N Brunner (1995) ArticleTitleThe plasminogen activation system and its role in lung cancer: a review Lung Cancer 12 1–12 Occurrence Handle10.1016/0169-5002(94)00408-F

    Article  Google Scholar 

  54. H Pederses J Grøndahl-Hansen D Francis K ÖSterlind HH Hansen E Rønne et al. (1994) ArticleTitleUrokinase and plasminogen activator inhibitor type 1 in pulmonary adenocarcinoma Cancer Res 54 120–2

    Google Scholar 

  55. M Kodate T Kasai H Hashimoto K Yasumoto Y Iwata H Manabe (1997) ArticleTitleExpression of matrix metalloproteinase (gelatinase) in T1 adenocarcinoma of the lung Pathol International 47 461–9 Occurrence Handle1:CAS:528:DyaK2sXlt1Smsbg%3D Occurrence Handle10.1111/j.1440-1827.1997.tb04525.x

    Article  CAS  Google Scholar 

  56. X-H Pei Y Nakanishi K Takayama F Bai H Hara (1999) ArticleTitleBenzo[a]pyrene activates the human p53 gene through induction of nuclear factor κB Activity J Biol Chem 274 35240–6 Occurrence Handle10575010 Occurrence Handle10.1074/jbc.274.49.35240 Occurrence Handle1:CAS:528:DyaK1MXnvFyrurc%3D

    Article  PubMed  CAS  Google Scholar 

  57. PG Holt D Keast (1977) ArticleTitleEnvironmentally induced changes in immunological function: acute and chronic effects of inhalation of tobacco smoke and other atmospheric contaminants in man and experimental animals Bacterial Rev 41 205–16 Occurrence Handle1:CAS:528:DyaE2sXktVSksbw%3D

    CAS  Google Scholar 

  58. P Anderson OF Pederson B Bach GJ Bonde (1982) ArticleTitleSerum antibodies and immunoglobulins in smokers and nonsmokers Clin Exp Immunol 47 467–73

    Google Scholar 

  59. SM Savage LA Donaldson S Cherian R Chilukuri VA White ML Sopori (1991) ArticleTitleEffect of cigarette smoke on the immune response: II. Chronic exposure to cigarette smoke inhibits surface immunoglobulin-mediated responses in B cells Toxicol Appl Pharmacol 111 523–9 Occurrence Handle1746027 Occurrence Handle10.1016/0041-008X(91)90256-E Occurrence Handle1:CAS:528:DyaK38XnvVentQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  60. AA Frazer-Abel S Baksh SP Fosmire D Willis AM Pierce H Meylemans et al. (2004) ArticleTitleNicotine activates nuclear factor of activated T cells c2 (NFATc2) and prevents cell cycle entry in T cells J Pharmacol Exp Ther 311 758–69 Occurrence Handle15231866 Occurrence Handle10.1124/jpet.104.070060 Occurrence Handle1:CAS:528:DC%2BD2cXptVKru7s%3D

    Article  PubMed  CAS  Google Scholar 

  61. M Stolina S Sharma Y Lin M Dohadwala B Gardner J Luo et al. (2000) ArticleTitleSpecific inhibition of cyclooxigenase 2 restores antitumor reactivity by altering the balance of IL-10 and IL-12 synthesis J Immunol 164 361–70 Occurrence Handle10605031 Occurrence Handle1:CAS:528:DC%2BD3cXisFSr

    PubMed  CAS  Google Scholar 

  62. S Sharma SC Yang L Zhu K Reckamp B Gardner F Baratelli et al. (2005) ArticleTitleTumor cyclooxigenase-2/prostaglandin E2-dependent promotion of FOXP3 expression and CD4 + CD25 + T regulatory cell activities in lung cancer Cancer Res 65 5211–20 Occurrence Handle15958566 Occurrence Handle10.1158/0008-5472.CAN-05-0141 Occurrence Handle1:CAS:528:DC%2BD2MXltFemurc%3D

    Article  PubMed  CAS  Google Scholar 

  63. I Yoshino T Yano M Murata T Ishida K Sugimachi G Kimura et al. (1992) ArticleTitleTumor-reactive T cells accumulate in lung cancer tissues but fail to respond due to tumor cell -derived factor Cancer Res 52 775–81 Occurrence Handle1737336 Occurrence Handle1:STN:280:DyaK387ksFKitw%3D%3D

    PubMed  CAS  Google Scholar 

  64. R Kalra SP Singh SM Savage GL Finci ML Sopori (2000) ArticleTitleEffects of cigarette smoke on immune response: chronic exposure to cigarette smoke impairs antigen-mediated signaling in T cells and depletes IP3-sensitive Ca2+ stores J Pharmacol Exp Ther 293 166–71 Occurrence Handle10734166 Occurrence Handle1:CAS:528:DC%2BD3cXkvFGhtb4%3D

    PubMed  CAS  Google Scholar 

  65. CS Robbins DE Dawe SI Goncharova MA Pouladi AG Drannik FK Swirski et al. (2004) ArticleTitleCigarette smoke decrease pulmonary dendritic cells and impacts antiviral immune responsiveness Am J Resp Cell Mol Biol 30 202–11 Occurrence Handle10.1165/rcmb.2003-0259OC Occurrence Handle1:CAS:528:DC%2BD2cXht1Cisbg%3D

    Article  CAS  Google Scholar 

  66. S Sharma M Stolina SC yang F Baratelli JF Lin K Atianzar et al. (2003) ArticleTitleTumor cyclooxigenase 2-dependent suppression of dendritic cell function Clin Cancer Res 9 961–8 Occurrence Handle12631593 Occurrence Handle1:CAS:528:DC%2BD3sXhvFKiurY%3D

    PubMed  CAS  Google Scholar 

  67. M Takenoyama I Yoshino R Eifuku S Imahayashi M Sugaya M Yasuda et al. (2001) ArticleTitleSuccessful induction of tumor-specific cytotoxic T lymphocytes from patients with non-small cell lung cancer using CD80-transfected autologous tumor cells Jpn J Cancer Res 92 309–15 Occurrence Handle11267941 Occurrence Handle1:CAS:528:DC%2BD3MXjs1Oltrw%3D

    PubMed  CAS  Google Scholar 

  68. LE Raez PA Cassileth JJ Schlesselman K Sridhar S Padmanavhan EZ Fisher et al. (2004) ArticleTitleAllogeneic vaccination with a B7.1 HLA-A gene-modified adenocarcinoma cell line in patients with advanced non-small cell lung cancer J Clin Oncol 22 2800–7 Occurrence Handle15254047 Occurrence Handle10.1200/JCO.2004.10.197 Occurrence Handle1:CAS:528:DC%2BD2cXpsVWkt7s%3D

    Article  PubMed  CAS  Google Scholar 

  69. D O'Mahony S Kummar ME Gutierrez (2005) ArticleTitleNon-small-cell lung cancer vaccine therapy: a concise review J Clin Oncol 23 9022–8 Occurrence Handle16219932 Occurrence Handle10.1200/JCO.2005.02.3101 Occurrence Handle1:CAS:528:DC%2BD28XktVCntw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  70. Song N, Tan W, Xing D, Lin D. CYP1A1 polymorphism and risk of lung cancer in relation to tobacco smoking: a case-control study in China. Carcinogenesis 1001;22:11–6

  71. H Bartsch U Nair A Risch M Rojas H Wikman K Alexandrov (2000) ArticleTitleGenetic polymorphism of CYP genes, alone and combination, as a risk modifier of tobacco-related cancers Cancer Epidemiol Biomarkers Prev 9 3–28 Occurrence Handle10667460 Occurrence Handle1:CAS:528:DC%2BD3cXptVOmtw%3D%3D

    PubMed  CAS  Google Scholar 

  72. PG Shields ED Bowman AM Harrington VT Doan A Weston (1993) ArticleTitlePolycyclic aromatic hydrocarbon-DNA adducts in human lung and cancer susceptibility genes Cancer Res 53 1381–8

    Google Scholar 

  73. K Alexandrov I Cascorbi M Rojas G Bouvier E Kriek H Bartsch (2002) ArticleTitleCYP1A1 and GSTM1 genotypes affect benzo[a]pyrene DNA adducts in smokers' lung: comparison with aromatic/hydrophobic adduct formation Carcinogenesis 23 1969–77 Occurrence Handle12507920 Occurrence Handle10.1093/carcin/23.12.1969 Occurrence Handle1:CAS:528:DC%2BD3sXhtVyqu7c%3D

    Article  PubMed  CAS  Google Scholar 

  74. JP Radicella C Dherin C Desmaze MS Fox S Boiteux (1997) ArticleTitleCloning and characterization of hOGG1, a human homolog of OGG1 gene of Saccharomyces cerevisiae Proc Natl Acad Sci USA 94 8010–5 Occurrence Handle9223305 Occurrence Handle10.1073/pnas.94.15.8010 Occurrence Handle1:CAS:528:DyaK2sXksl2ms7k%3D

    Article  PubMed  CAS  Google Scholar 

  75. T Kohno K Shinmura M Tosaka M Tani SR Kim H Sugimura et al. (1998) ArticleTitleGenetic polymorphisms and alterative splicing of hOGG1, that is involved in the repair of 8-hydroxyguanine in damaged DNA Oncogene 16 3219–25 Occurrence Handle9681819 Occurrence Handle10.1038/sj.onc.1201872 Occurrence Handle1:CAS:528:DyaK1cXksFSls7s%3D

    Article  PubMed  CAS  Google Scholar 

  76. E Evans JG Moggs JR Hwang JM Egly RD Wood (1997) ArticleTitleMechanism of open complex and dual incision formation by human nucleotide excision repair factors EMBO J 16 6559–73 Occurrence Handle9351836 Occurrence Handle10.1093/emboj/16.21.6559 Occurrence Handle1:CAS:528:DyaK2sXnslWkt7Y%3D

    Article  PubMed  CAS  Google Scholar 

  77. SM Hou S Falt S Angelini K Yang F Nyberg B Lambert et al. (2002) ArticleTitleThe XPD variant alleles are associated with increased aromatic DNA adduct level and lung cancer risk Carcinogenesis 23 599–633 Occurrence Handle11960912 Occurrence Handle10.1093/carcin/23.4.599 Occurrence Handle1:CAS:528:DC%2BD38XjvVGrtbw%3D

    Article  PubMed  CAS  Google Scholar 

  78. K Hemminki M Koskinen H Rajaniemi C Zhao (2000) ArticleTitleDNA adducts, mutations, and cancer Regul Toxicol Pharmacol 32 264–75 Occurrence Handle11162720 Occurrence Handle10.1006/rtph.2000.1431 Occurrence Handle1:CAS:528:DC%2BD3MXptlGisQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  79. K Yang L Airoldi R Pastorelli J Restano M Guanci K Hemminiki (1996) ArticleTitleAromatic DNA adducts in lymphocytes of humans working at high and low traffic density areas Chemi Biol Interact 101 127–36 Occurrence Handle10.1016/0009-2797(96)03720-9 Occurrence Handle1:CAS:528:DyaK28XksF2gsLg%3D

    Article  CAS  Google Scholar 

  80. G Boysen SS Hecht (2003) ArticleTitleAnalysis of DNA and protein adducts of benzo[a]pyrene in human tissues using structure-specific methods Mutat Res 543 17–30 Occurrence Handle12510015 Occurrence Handle10.1016/S1383-5742(02)00068-6 Occurrence Handle1:CAS:528:DC%2BD38XpvVahsL0%3D

    Article  PubMed  CAS  Google Scholar 

  81. JM Arif C Dresler ML Clapper G Gairola C Srinivason RA Lubet et al. (2006) ArticleTitleLung DNA adducts detected in human smokers are unrelated to typical polyaromatic carcinogens Chem Res Toxicol 19 295–9 Occurrence Handle16485906 Occurrence Handle10.1021/tx0502443 Occurrence Handle1:CAS:528:DC%2BD28XmvVantg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  82. InstitutionalAuthorNameThe Alpha-Tocopherol Beta-carotens Cancer Prevention Study Group (1994) ArticleTitleThe effect of vitamin E and beta-carotene on the incidence of lung cancer and other cancers in male smokers N Engl J Med 330 1029–35 Occurrence Handle10.1056/NEJM199404143301501

    Article  Google Scholar 

  83. GS Omenn GE Goodman MD Thronquist J Balmes MR Cullen A Glass et al. (1996) ArticleTitleEffects of a combination of beta-carotene and vitamin A on lung cancer and cardiovascular disease N Engl J Med 334 1150–5 Occurrence Handle8602180 Occurrence Handle10.1056/NEJM199605023341802 Occurrence Handle1:CAS:528:DyaK28XjtVyqsLs%3D

    Article  PubMed  CAS  Google Scholar 

  84. SM Lippman JJ Lee DD Karp EE Vokes SE Benner GE Goodman et al. (2001) ArticleTitleRandomized phase III intergroup trial of isotretinoin to prevent second primary tumors in stage I non-small-cell lung cancer J Natl Cancer Inst 93 605–18 Occurrence Handle11309437 Occurrence Handle10.1093/jnci/93.8.605 Occurrence Handle1:CAS:528:DC%2BD3MXjsV2rurs%3D

    Article  PubMed  CAS  Google Scholar 

  85. MA Pereira Y Li F Al-Yazoub PM Kramer F Al-Yaqoub RA Lubet et al. (2002) ArticleTitlePrevention of mouse lung tumors by budesonide and its modulation of biomarkers Carcinogenesis 23 1185–92 Occurrence Handle12117777 Occurrence Handle10.1093/carcin/23.7.1185 Occurrence Handle1:CAS:528:DC%2BD38XlsFKltb8%3D

    Article  PubMed  CAS  Google Scholar 

  86. RL Keith YE Miller TM Hudish CE Girod CE Girod S Sotto-Santiago et al. (2004) ArticleTitlePulmonary prostacyclin synthase overexpression chemoprevents tobacco smoke lung carcinogenesis in mice Cancer Res 64 5897–904 Occurrence Handle15313935 Occurrence Handle10.1158/0008-5472.CAN-04-1070 Occurrence Handle1:CAS:528:DC%2BD2cXmslaksL4%3D

    Article  PubMed  CAS  Google Scholar 

  87. S Shishodia BB Aggarwal (2004) ArticleTitleCyclooxigenase (COX)-2 inhibitor Celecoxib abrogates activation of cigarette smoke-induced nuclear factor (NF)-kB by suppressing activation of IkBa kinase in human non-small cell lung carcinoma: Correlation with suppression of cyclin D1, COX-2, and matrix metalloproteinase-9 Cancer Res 64 5004–12 Occurrence Handle15256475 Occurrence Handle10.1158/0008-5472.CAN-04-0206 Occurrence Handle1:CAS:528:DC%2BD2cXls1Omt7Y%3D

    Article  PubMed  CAS  Google Scholar 

  88. LC Clark GF Coombs SuffixJr BW Turnbull EH Slate DK Chalker J Chow et al. (1996) ArticleTitleEffects of selenium supplementation for cancer prevention in patients with carcinoma of skin JAMA 276 1957–63 Occurrence Handle8971064 Occurrence Handle10.1001/jama.276.24.1957 Occurrence Handle1:CAS:528:DyaK2sXks1eksg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  89. FO Ranelletti S Maggiano FG Serra R Ricci LM Larocca P Lanza et al. (2000) ArticleTitleQuercetin inhibits p21-RAS expression in humancolon cancer cell lines and in primary colorectal tumors Int J Cancer 85 438–45 Occurrence Handle10652438 Occurrence Handle10.1002/(SICI)1097-0215(20000201)85:3<438::AID-IJC22>3.0.CO;2-F Occurrence Handle1:CAS:528:DC%2BD3cXmsVCnsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  90. NZ Jin YP Zhu JW Zhou L Mao RC Zhao TH Fang et al. (2006) ArticleTitlePreventive effects of quercetin against benzo[a]pyrene induced DNA damages and pulmonary precancerous pathologic changes in mice Basic Clin Pharmacol Toxicol 98 593–8 Occurrence Handle16700823 Occurrence Handle10.1111/j.1742-7843.2006.pto_382.x Occurrence Handle1:CAS:528:DC%2BD28Xls1Siur4%3D

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Surgery and Science, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Fukuoka, 812-8582, Japan

    Ichiro Yoshino & Yoshihiko Maehara

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  1. Ichiro Yoshino
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Yoshino, I., Maehara, Y. Impact of Smoking Status on the Biological Behavior of Lung Cancer. Surg Today 37, 725–734 (2007). https://doi.org/10.1007/s00595-007-3516-6

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