Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review
  • Published:

DNA adduct burden and tobacco carcinogenesis

Oncogene volume 21, pages 7376–7391 (2002)Cite this article

Abstract

DNA adducts associated with tobacco smoking could provide a marker of biologically effective dose of tobacco carcinogens and improve individual cancer risk prediction. A significant number of clinical and epidemiologic studies have reported associations of increased DNA adduct levels with the occurrence of the prevalent tobacco related cancers including cancer of the lung, head and neck, and bladder. The inducibility of DNA adducts following in vitro treatments using blood lymphocytes also appears to be a risk factor in the development of lung and head and neck cancer. Corroborative evidence pointing to the importance of DNA adducts in tobacco carcinogenesis include numerous studies showing associations of tobacco smoke exposure with the induction of DNA adducts in humans in vivo. Further effort is necessary, however, to more fully characterize the dose–response relationship between smoking and DNA adducts in exposed target and surrogate tissues. The relationship between gene polymorphisms thought to modify tobacco-related cancer risk and DNA adduct levels is complex. Results of some DNA adduct studies (both in vitro and in vivo) appear inconsistent with the epidemiologic findings. This is evident for polymorphisms involving both carcinogen metabolism (e.g. GSTP1) and DNA repair (e.g. XRCC1). Molecular studies of human tumors suggest associations of p53 mutation with DNA adducts and have revealed correlations of DNA adduct levels with somatic alterations (e.g. 3p21 LOH) that are thought to occur at the very earliest stages of tobacco carcinogenesis. More research is needed to assess the relationship between endogenous sources of DNA adducts and tobacco smoke exposure and the relative oncogenic effects of chemically stable versus unstable DNA adducts. Many potentially fruitful new avenues of cancer research are emerging that integrate DNA adduct analyses with assessments of smoking, genetics, diet and ambient air quality. These investigations aim to understand the multifactorial nature of interindividual variability in response to tobacco carcinogens. As these trends continue a variety of innovative study designs and approaches will become important in human populations.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

Abbreviations

GSTM1, GSTT1, GSTP1:

Glutathione S-transferase M1, T1, P1

NAT1, NAT2:

N-acetyltransferase type I and type II

NQQ1 :

NAD(P)H:quinone oxidoreductase type I

BP:

benzo(a)pyrene

BPDE:

7,8-dihydro-7,8-dihydroxybenzo(a)pyrene 9, 10-oxide

MNC:

mononuclear cells

PAH:

polynuclear aromatic hydrocarbons

GSH:

glutathione

HPLC:

high performance liquid chromatography

1-OHPY:

1-hydroxypyrene

WBC:

white blood cells

GS/MS:

gas chromatography-mass spectrometry

eA:

1,N6-ethenodeoxyadenosine

eC:

3,N4-etheneodeoxycytidine

M1G:

3-(2-deoxy-β-D-erythro-pentofuranosyl)pyrimido[1,2-α]purin-10(3H)-one

BP-6 N7Gua:

7-(benzo[a]pyren-6-yl)guanine

ELISA:

enzyme linked immunosorbent assay

8-oxo-dG:

8-hydroxy-2′-deoxyguanosine

PhIP:

2-amino-1-methyl-6-phenylimidazao[4,5-b]pyridine

HPV:

human papilloma virus

EPIC:

European Prospective Investigation into Cancer and Nutrition

References

  • Alexandrov K, Rojas M, Geneste O, Castegnaro M, Camus AM, Petruzzelli S, Giuntini C, Bartsch H . 1992 Cancer Res. 52: 6248–6253

  • Andreassen A, Kure EH, Nielsen PS, Autrup H, Haugen A . 1996 Mutat. Res. 368: 275–282

  • Aoki Y, Sato H, Nishimura N, Takahashi S, Itoh K, Yamamoto M . 2001 Toxicol. Appl. Pharmacol. 173: 154–160

  • Arnould JP, Kubiak R, Belowski J, Belegaud J, Szczeklik J . 2000 Pathol. Bio. (Paris) 48: 548–553

  • Arnould JP, Pfohl-Leszkowicz A, Bach V, Libert JP, Belegaud J . 1999 Hum. Exp. Toxicol. 18: 314–321

  • Banaszewski J, Szmeja Z, Szyfter W, Szyfter K, Baranczewski P, Moller L . 2000 Eur. Arch. Otorhinolaryngol. 257: 149–153

  • Bartsch H, Nair J . 2001 Adv. Exp. Med. Biol. 500: 675–686

  • Bartsch H, Rojas M, Alexandrov K, Risch A . 1998 Recent Results Cancer Res. 154: 86–96

  • Beserati Nia A, Van Straaten HW, Godschalk RW, Van Zandwijk N, Balm AJ, Kleinjans JC, Van Schooten FJ . 2000 Environ. Mol. Mutagen 36: 127–133

  • Binkova B, Topinka J, Mrackova G, Gajdosova D, Vidova P, Stavkova Z, Peterka V, Pilcik T, Rimar V, Dobias L, Farmer PB, Sram RJ . 1998 Muta. Res. 416: 67–84

  • Blair IA . 2001 Exp. Gerontol. 36: 1473–1481

  • Bodell WJ, Devanesan PD, Rogan EG, Cavalieri EL . 1989 Chem. Res. Toxicol. 2: 312–315

  • Bonassi S, Neri M, Puntoni R . 2001 Mutat. Res. 480–481: 349–358

  • Bucci F, Galati R, Zito R, Falasca G, Federico A, Verdina A . 1998 Anticancer Res. 18: 2669–2674

  • Burcham PC . 1998 Mutagenesis 13: 287–305

  • Butkiewicz D, Grzybowska E, Phillips DH, Hemminki K, Chorazy M . 2000 Environ. Mol. Mutagen. 35: 99–105

  • Butkiewicz D, Rusin M, Enewold L, Shields PG, Chorazy M, Harris CC . 2001 Carcinogenesis 22: 593–597

  • Carmichael PL . 1998 Arch. Toxicol. 20: Suppl 199–205

  • Casale GP, Singhal M, Bhattacharya S, RamaNathan R, Roberts KP, Barbacci DC, Zhao J, Jankowiak R, Gross ML, Cavalieri EL, Small GJ, Rennard SI, Mumford JL, Shen M . 2001 Chem. Res. Toxicol. 14: 192–201

  • Chakravarti D, Mailander PC, Li KM, Higginbotham S, Zhang HL, Gross ML, Meza JL, Cavalieri EL, Rogan EG . 2001 Oncogene 20: 7945–7953

  • Chen HJ, Zhang L, Cox J, Cunningham JA, Chung FL . 1998 Chem. Res. Toxicol. 11: 1474–1480

  • Chen L, Devanesan PD, Higginbotham S, Ariese F, Jankowiak R, Small GJ, Rogan EG, Cavalieri EL . 1996 Chem. Res. Toxicol. 9: 897–903

  • Cheng L, Spitz MR, Hong WK, Wei Q . 2000a Carcinogenesis 21: 1527–1530

  • Cheng YW, Chen CY, Lin P, Huang KH, Lin TS, Wu MH, Lee H . 2000b Eur. J. Cancer 36: 1381–1388

  • Cheng YW, Hsieh LL, Lin PP, Chen CP, Chen CY, Lin TS, Su JM, Lee H . 2001 Environ. Mol. Mutagen. 37: 304–310

  • Coles B, Yang M, Lang NP, Kadlubar FF . 2000a Cancer Lett. 156: 167–175

  • Coles BF, Anderson KE, Doerge DR, Churchwell MI, Lang NP, Kadlubar FF . 2000b Cancer Res. 60: 573–579

  • Cuzick J . 1995 J. Natl. Cancer Inst. 87: 861–862

  • David-Beabes GL, London SJ . 2001 Lung Cancer 34: 333–339

  • Devanesan PD, Higginbotham S, Ariese F, Jankowiak R, Suh M, Small GJ, Cavalieri EL, Rogan EG . 1996 Chem. Res. Toxicol. 9: 1113–1116

  • Divine KK, Gilliland FD, Crowell RE, Stidley CA, Bocklage TJ, Cook DL, Belinsky SA . 2001 Mutat. Res. 461: 273–278

  • Duell EJ, Holly EA, Bracci PM, Liu M, Wiencke JK, Kelsey KT . 2002 J. Natl. Cancer Inst. 94: 297–306

  • Duell EJ, Wiencke JK, Cheng TJ, Varkonyi A, Zuo ZF, Ashok TD, Mark EJ, Wain JC, Christiani DC, Kelsey KT . 2000 Carcinogenesis 21: 965–971

  • Endo C, Sato M, Fujimura S, Sakurada A, Aikawa H, Takahashi S, Usuda K, Saito Y, Sagawa M . 2000 Surg. Today 30: 695–699

  • Fennell TR, MacNeela JP, Morris RW, Watson M, Thompson CL, Bell DA . 2000 Cancer Epidemiol. Biomarkers Prev. 9: 705–712

  • Fields WR, Morrow CS, Doss AJ, Sundberg K, Jernstrom B, Townsend AJ . 1998 Mol. Pharmacol. 54: 298–304

  • Franklin WA, Gazdar AF, Haney J, Wistuba II, La Rosa FG, Kennedy T, Ritchey DM, Miller YE . 1997 J. Clin. Invest. 100: 2133–2137

  • Garner RC . 1998 Mutat. Res. 402: 67–75

  • Godschalk RW, Dallinga JW, Wikman H, Risch A, Kleinjans JC, Bartsch H, Van Schooten FJ . 2001 Pharmacogenetics 11: 389–398

  • Godschalk RW, Maas LM, Van Zandwijk N, van't Veer LJ, Breedijk A, Borm PJ, Verhaert J, Kleinjans JC, van Schooten FJ . 1998 Carcinogenesis 19: 819–825

  • Goldman R, Enewold L, Pellizzari E, Beach JB, Bowman ED, Krishnan SS, Shields PG . 2001 Cancer Res. 61: 6367–6371

  • Grant DJ, Bell DA . 2000 Mol. Carcinog. 29: 198–204

  • Grinberg-Funes RA, Singh VN, Perera FP, Bell DA, Young TL, Dickey C, Wang LW, Santella RM . 1994 Carcinogenesis 15: 2449–2454

  • Grzybowska E, Butkiewicz D, Motykiewicz G, Chorazy M . 2000 Mutat. Res. 469: 271–277

  • Grzybowska E, Hemminki K, Szeliga J, Chorazy M . 1993 Carcinogenesis 14: 2523–2526

  • Gupta RC, Arif JM, Gairola CG . 1999 Mutat. Res. 424: 195–205

  • Hardie LJ, Briggs JA, Davidson LA, Allan JM, King RF, Williams GI, Wild CP . 2000 Carcinogenesis 21: 167–172

  • Harries LW, Stubbins MJ, Forman D, Howard GC, Wolf CR . 1997 Carcinogenesis 18: 641–644

  • Hecht SS, McIntee EJ, Wang M . 2001 Toxicology 166: 31–36

  • Hegmann KT, Fraser AM, Keaney RP, Moser SE, Nilasena DS, Sedlars M, Higham-Gren L, Lyon JL . 1993 Epidemiology 4: 444–448

  • Helleberg H, Xu H, Ehrenberg L, Hemminki K, Rannug U, Tornqvist M . 2001 Mutagenesis 16: 333–337

  • Hemminki K, Koskinen M, Rajaniemi H, Zhao C . 2000 Regul. Toxicol. Pharmacol. 32: 264–275

  • Hemminki K, Koskinen M, Zhao C . 2001 Int. J. Cancer 92: 923–926

  • Hirao T, Nelson HH, Ashok TD, Wain JC, Mark EJ, Christiani DC, Wiencke JK, Kelsey KT . 2001 Cancer Res. 61: 612–615

  • Hoque A, Albanes D, Lippman SM, Spitz MR, Taylor PR, Klein EA, Thompson IM, Goodman P, Stanford JL, Crowley JJ, Coltman CA, Santella RM . 2001 Cancer Causes Control 12: 627–633

  • Hou SM, Falt S, Yang K, Nyberg F, Pershagen G, Hemminki K, Lambert B . 2001 Cancer Epidemiol. Biomarkers Prev. 10: 133–140

  • Hu X, Herzog C, Zimniak P, Singh SV . 1999 Cancer Res. 59: 2358–2362

  • Izzotti A, Bagnasco M, D'Agostini F, Cartiglia C, Lubet RA, Kelloff GJ, De Flora S . 1999 Carcinogenesis 20: 1499–1505

  • Jacobson JS, Begg MD, Wang LW, Wang Q, Agarwal M, Norkus E, Singh VN, Young TL, Yang D, Santella RM . 2000 Cancer Epidemiol. Biomarkers Prev. 9: 1303–1311

  • Jaiswal AK, Bell DW, Radjendirane V, Testa JR . 1999 Pharmacogenetics 9: 413–418

  • Josyula S, Schut HA, Diwan BA, Anver MR, Anderson LM . 2000 Int. J. Oncol. 17: 811–818

  • Kadlubar FF, Anderson KE, Haussermann S, Lang NP, Barone GW, Thompson PA, MacLeod SL, Chou MW, Mikhailova M, Plastaras J, Marnett LJ, Nair J, Velic I, Bartsch H . 1998 Mutat. Res. 405: 125–133

  • Kantarci OH, Lesnick TG, Yang P, Meyer RL, Hebrink DD, McMurray CT, Weinshenker BG . 2002 Mayo Clin. Proc. 77: 17–22

  • Kato S, Bowman ED, Harrington AM, Blomeke B, Shields PG . 1995 J. Natl. Cancer Inst. 87: 902–907

  • Kihara M, Noda K . 1999 Cancer Lett. 137: 53–60

  • Kriek E, Rojas M, Alexandrov K, Bartsch H . 1998 Mutat. Res. 400: 215–231

  • Kure EH, Ryberg D, Hewer A, Phillips DH, Skaug V, Baera R, Haugen A . 1996 Carcinogenesis 17: 2201–2215

  • Kyrtopoulos SA, Georgiadis P, Autrup H, Demopoulos N, Farmer P, Haugen A, Katsouyanni K, Lambert B, Ovrebo S, Sram R, Stefanou G, Topinka J . 2001 Mutat. Res. 496: 207–228

  • Le Marchand L, Seifried A, Lum A, Wilkens LR . 2000 Cancer Epidemiol. Biomarkers Prev. 9: 181–184

  • Leuratti C, Singh R, Lagneau C, Farmer PB, Plastaras JP, Marnet LJ, Shuker DE . 1998 Carcinogenesis 19: 1919–1924

  • Li D, Firozi PF, Chang P, Wang LE, Xiong P, Sturgis EM, Eicher SA, Spitz MR, Hong WK, Wei Q . 2001a Int. J. Cancer 93: 436–440

  • Li D, Firozi PF, Wang LE, Bosken CH, Spitz MR, Hong WK, Wei Q . 2001b Cancer Res. 61: 1445–1450

  • Li D, Firozi PF, Zhang W, Shen J, DiGiovanni J, Lau S, Evans D, Friess H, Hassan M, Abbruzzese JL . 2002 Mutat. Res. 513: 37–48

  • Lodovici M, Akpan V, Giovannini L, Migliani F, Dolara P . 1998 Chem. Biol. Interact. 116: 199–212

  • London SJ, Lehman TA, Taylor JA . 1997 Cancer Res. 57: 5001–5003

  • Long 2nd DJ, Jaiswal AK . 2000 Chem. Biol. Interact. 129: 99–112

  • Marcus PM, Vineis P, Rothman N . 2000 Pharmacogenetics 10: 115–122

  • Martone T, Airoldi L, Magagnotti C, Coda R, Randone D, Malaveille C, Avanzi G, Merletti F, Hautefeuille A, Vineis P . 1998 Int. J. Cancer 75: 512–516

  • Marzilli LA, Koertje C, Vouros P . 2001 Methods Mol. Biol. 162: 395–406

  • Matullo G, Guarrera S, Carturan S, Peluso M, Malaveille C, Davico L, Piazza A, Vineis P . 2001a Int. J. Cancer 92: 562–567

  • Matullo G, Palli D, Peluso M, Guarrera S, Carturan S, Celentano E, Krogh V, Munnia A, Tumino R, Polidoro S, Piazza A, Vineis P . 2001b Carcinogenesis 22: 1437–1445

  • Melendez-Colon VJ, Luch A, Seidel A, Baird WM . 1999 Carcinogenesis 20: 1885–1891

  • Melendez-Colon VJ, Smith CA, Seidel A, Luch A, Platt KL, Baird WM . 1997 Proc. Natl. Acad. Sci. USA 94: 13542–13547

  • Melikian AA, Sun P, Prokopczyk B, El-Bayoumy K, Hoffman D, Wang X, Waggoner S . 1999a Cancer Lett. 146: 127–134

  • Melikian AA, Wang X, Waggoner S, Hoffmann D, El-Bayoumy K . 1999b Oncol. Rep. 6: 1371–1376

  • Misra RR, Tangrea JA, Virtamo J, Ratnasinghe D, Andersen MR, Barrett M, Taylor PR, Albanes D . 2001 Cancer Lett. 164: 161–167

  • Mitsudomi T, Oyama T, Nishida K, Ogami A, Osaki T, Sugio K, Yasumoto K, Sugimachi K, Gazdar AF . 1996 Clin. Cancer Res. 2: 1185–1189

  • Moller L, Grzybowska E, Zeisig M, Cimander B, Hemminki K, Chorazy M . 1996 Carcinogenesis 17: 61–66

  • Moller P, Wallin H . 1998 Mutat. Res. 410: 271–290

  • Mollerup S, Ryberg D, Hewer A, Phillips DH, Haugen A . 1999 Cancer Res. 59: 3317–3320

  • Mooney LA, Bell DA, Santella RM, Van Bennekum AM, Ottman R, Paik M, Blaner WS, Lucier GW, Covey L, Young TL, Cooper TB, Glassman AH, Perera FP . 1997 Carcinogenesis 18: 503–509

  • Mooney LA, Santella RM, Covey L, Jeffrey AM, Bigbee W, Randall MC, Cooper TB, Ottman R, Tsai WY, Wazneh L et al . 1995 Cancer Epidemiol. Biomarkers Prev. 4: 627–634

  • Motykiewicz G, Michalska J, Pendzich J, Malusecka E, Strozyk M, Kalinowska E, Butkiewicz D, Mielzynska D, Midro A, Santella RM, Chorazy M . 1998 Toxicol. Lett. 96–97: 195–202

  • Nair J, Gal A, Tamir S, Tannenbaum SR, Wogan GN, Bartsch H . 1998 Carcinogenesis 19: 2081–2084

  • Nath RG, Ocando JE, Guttenplan JB, Chung FL . 1998 Cancer Res. 58: 581–584

  • Nelson HH, Kelsey KT, Mott LA, Karagas MR . 2002 Cancer Res. 62: 152–155

  • Nelson HH, Wiencke JK, Gunn L, Wain JC, Christiani DC, Kelsey KT . 1998 Cancer Res. 58: 1804–1807

  • Ni J, Liu T, Kolbanovskiy A, Krzeminski J, Amin S, Geacintov NE . 1998 Anal. Biochem. 264: 222–229

  • Nia AB, Maas LM, Brouwer EM, Kleinjans JC, Van Schooten FJ . 2000 Carcinogenesis 21: 1335–1340

  • Nowell S, Ambrosone CB, Ozawa S, MacLeod SL, Mrackova G, Williams S, Plaxco J, Kadlubar FF, Lang NP . 2000 Pharmacogenetics 10: 789–797

  • Olshan AF, Watson MA, Weissler MC, Bell DA . 2002 Cancer Lett. 178: 181–186

  • Ozawa S, Schoket B, McDaniel LP, Tang YM, Ambrosone CB, Kostic S, Vincze I, Kadlubar FF . 1999 Carcinogenesis 20: 991–995

  • Palli D, Russo A, Masala G, Saieva C, Guarrera S, Carturan S, Munnia A, Matullo G, Peluso M . 2001 Int. J. Cancer 94: 121–127

  • Palli D, Vineis P, Russo A, Berrino F, Krogh V, Masala G, Munnia A, Panico S, Taioli E, Tumino R, Garte S, Peluso M . 2000 Int. J. Cancer 87: 444–451

  • Pan G, Hanaoka T, Yamano Y, Hara K, Ichiba M, Wang Y, Zhang J, Feng Y, Shujuan Z, Guan D, Gao G, Liu N, Takahashi K . 1998 Carcinogenesis 19: 1963–1968

  • Park IW, Wistuba II, Maitra A, Milchgrub S, Virmani AK, Minna J, Gazdar AF . 1999 J. Natl. Cancer Inst. 91: 1863–1868

  • Park JY, Lee SY, Jeon HS, Bae NC, Chae SC, Joo S, Kim CH, Park JH, Kam S, Kim IS, Jung TH . 2002 Cancer Epidemiol. Biomarkers Prev. 11: 23–27

  • Pavanello S, Clonfero E . 2000 Mutat. Res. 463: 285–308

  • Pavanello S, Favretto D, Brugnone F, Mastrangelo F, Dal Pra G, Clonfero E . 1999 Carcinogenesis 20: 431–435

  • Peluso M, Airoldi L, Armelle M, Martone T, Coda R, Malaveille C, Giacomelli G, Terrone C, Casetta G, Vineis P . 1998 Cancer Epidemiol. Biomarkers Prev. 7: 341–346

  • Peluso M, Airoldi L, Magagnotti C, Fiorini L, Munnia A, Hautefeuille A, Malaveille C, Vineis P . 2000 Carcinogenesis 21: 183–187

  • Peluso M, Castegnaro M, Malaveille C, Friesen M, Garren L, Hautefeuille A, Vineis P, Kadlubar F, Bartsch H . 1991 Carcinogenesis 12: 713–717

  • Perera F, Brenner D, Jeffrey A, Mayer J, Tang D, Warburton D, Young TI, Wazneh L, Latriano L, Motykiewicz G et al . 1992 Environ. Health Perspect. 98: 133–137

  • Perera F, Mayer J, Jaretzki A, Hearne S, Brenner D, Young TL, Fischman HK, Grimes M, Grantham S, Tang MX, Tsai WY, Santella RM . 1989 Cancer Res. 49: 4446–4451

  • Petruska JM, Mosebrook DR, Jakab GJ, Trush MA . 1992 Carcinogenesis 13: 1075–1081

  • Petruzzelli S, Celi A, Pulera N, Baliva F, Viegi G, Carrozzi L, Ciacchini G, Bottai M, Di Pede F, Paoletti P, Giuntini C . 1998 Cancer Res. 58: 4122–4126

  • Phillips DH, Castegnaro M . 1999 Mutagenesis 14: 301–315

  • Phillips DH, Farmer PB, Beland FA, Nath RG, Poirier MC, Reddy MV, Turteltaub KW . 2000 Environ. Mol. Mutagen. 35: 222–233

  • Phillips DH, Hewer A, Martin CN, Garner RC, King MM . 1988 Nature 336: 790–792

  • Piipari R, Savela K, Nurminen T, Hukkanen J, Raunio H, Hakkola J, Mantyla T, Beaune P, Edwards RJ, Boobis AR, Anttila S . 2000 Int. J. Cancer 86: 610–616

  • Povey AC . 2000 Toxicol. Pathol. 28: 405–414

  • Ratnasinghe D, Yao SX, Tangrea JA, Qiao YL, Andersen MR, Barrett MJ, Giffen CA, Erozan Y, Tockman MS, Taylor PR . 2001 Cancer Epidemiol. Biomarkers Prev. 10: 119–123

  • Reddy MV . 2000 Regul. Toxicol. Pharmacol. 32: 256–263

  • Ren Q, Murphy SE, Zheng Z, Lazarus P . 2000 Drug Metab. Dispos. 28: 1352–1360

  • Risch A, Wikman H, Thiel S, Schmezer P, Edler L, Drings P, Dienemann H, Kayser K, Schulz V, Spiegelhalder B, Bartsch H . 2001 Pharmacogenetics 11: 757–764

  • Roberts KP, Lin CH, Singhal M, Casale GP, Small GJ, Jankowiak R . 2000 Electrophoresis 21: 799–806

  • Rojas M, Alexandrov K, Cascorbi I, Brockmoller J, Likhachev A, Pozharisski K, Bouvier G, Auburtin G, Mayer L, Kopp-Schneider A, Roots I, Bartsch H . 1998 Pharmacogenetics 8: 109–118

  • Rojas M, Cascorbi I, Alexandrov K, Kriek E, Auburtin G, Mayer L, Kopp-Schneider A, Roots I, Bartsch H . 2000 Carcinogenesis 21: 35–41

  • Rojas M, Godschalk R, Alexandrov K, Cascorbi I, Kriek E, Ostertag J, Van Schooten FJ, Bartsch H . 2001 Carcinogenesis 22: 1015–1018

  • Romano G, Sgambato A, Boninsegna A, Flamini G, Curigliano G, Yang Q, La Gioia V, Signorelli C, Ferro A, Capelli G, Santella RM, Cittadini A . 1999 Cancer Epidemiol. Biomarkers Prev. 8: 91–96

  • Ryberg D, Hewer A, Phillips DH, Haugen A . 1994 Cancer Res. 54: 5801–5803

  • Ryberg D, Skaug V, Hewer A, Phillips DH, Harries LW, Wolf CR, Ogreid D, Ulvik A, Vu P, Haugen A . 1997 Carcinogenesis 18: 1285–1289

  • Saha BK, Bishayee A, Kanjilal NB, Chatterjee M . 2001 Cell Mol. Life Sci. 58: 1141–1149

  • Savela K, Hemminki K . 1991 Carcinogenesis 12: 503–508

  • Schabath MB, Spitz MR, Zhang X, Declos GL, Wu X . 2000 Carcinogenesis 21: 1163–1166

  • Schoket B, Kostic S, Vincze I . 1993 IARC Sci. Publ. 124: 315–319

  • Schoket B, Papp G, Levay K, Mrackova G, Kadlubar FF, Vincze I . 2001 Mutat. Res. 482: 57–69

  • Schoket B, Phillips DH, Kostic S, Vincze I . 1998 Carcinogenesis 19: 841–846

  • Seto H, Ohkubo T, Kanoh T, Koike M, Nakamura K, Kawahara Y . 1993 Arch. Environ. Contam. Toxicol. 24: 498–503

  • Shields PG, Bowman ED, Harrington AM, Doan VT, Weston A . 1993 Cancer Res. 53: 3486–3492

  • Shinozaki R, Inoue S, Choi KS . 1998 Cytometry 31: 300–306

  • Shinozaki R, Inoue S, Choi KS, Tatsuno T . 1999 Arch. Environ. Health 54: 79–85

  • Soni M, Madurantakan M, Krishnaswamy K . 1998 Toxicology 126: 155–162

  • Stern MC, Umbach DM, van Gils CH, Lunn RM, Taylor JA . 2001 Cancer Epidemiol. Biomarkers Prev. 10: 125–131

  • Sturgis EM, Castillo EJ, Li L, Zheng R, Eicher SA, Clayman GL, Strom SS, Spitz MR, Wei Q . 1999 Carcinogenesis 20: 2125–2129

  • Sugimura H, Kohno T, Wakai K, Nagura K, Genka K, Igarashi H, Morris BJ, Baba S, Ohno Y, Gao C, Li Z, Wang J, Takezaki T, Tajima K, Varga T, Sawaguchi T, Lum JK, Martinson JJ, Tsugane S, Iwamasa T, Shinmura K, Yokota J . 1999 Cancer Epidemiol. Biomarkers Prev. 8: 669–674

  • Sundberg K, Dreij K, Seidel A, Jernstrom B . 2002 Chem. Res. Toxicol. 15: 170–179

  • Szeliga J, Dipple A . 1998 Chem. Res. Toxicol. 11: 1–11

  • Szyfter K, Banaszewski J, Jaolszynski P, Pabiszczak M, Szyfter W, Szmeja Z . 1999a Acta Biochim. Pol. 46: 275–287

  • Szyfter K, Szmeja Z, Szyfter W, Hemminki K, Banaszewski J, Jaskula-Sztul R, Louhelainen J . 1999b Mutat. Res. 445: 259–274

  • Talaska G, al-Juburi AZ, Kadlubar FF . 1991 Proc. Natl. Acad. Sci. USA 88: 5350–5354

  • Talaska G, Schamer M, Casetta G, Tizzani A, Vineis P . 1994 Cancer Lett. 84: 93–97

  • Tan WG, Carnelley TJ, Murphy P, Wang H, Lee J, Barker S, Weinfeld M, Le XC . 2001 J. Chromatogr. A 924: 377–386

  • Tang D, Phillips DH, Stampfer M, Mooney LA, Hsu Y, Cho S, Tsai WY, Ma J, Cole KJ, She MN, Perera FP . 2001 Cancer Res. 61: 6708–6712

  • Tang D, Santella RM, Blackwood AM, Young TL, Mayer J, Jaretzki A, Grantham S, Tsai WY, Perera FP . 1995 Cancer Epidemiol. Biomarkers Prev. 4: 341–346

  • Tang DL, Rundle A, Warburton D, Santella RM, Tsai WY, Chiamprasert S, Hsu YZ, Perera FP . 1998 Carcinogenesis 19: 1949–1953

  • Thier R, Balkenhol H, Lewalter J, Selinski S, Dommermuth A, Bolt HM . 2001 Mutat. Res. 482: 41–46

  • Thurston SW, Wand MP, Wiencke JK . 2000 Biometrics 56: 139–144

  • Timbrell JA . 1998 Toxicology 129: 1–12

  • Topinka J, Schwarz LR, Wiebel FJ, Cerna M, Wolff T . 2000 Mutat. Res. 469: 83–93

  • Turteltaub KW, Dingley KH . 1998 Toxicol. Lett. 102–103: 435–439

  • Uno S, Dalton TP, Shertzer HG, Genter MB, Warshawsky D, Talaska G, Nebert DW . 2001 Biochem. Biophys. Res. Commun. 289: 1049–1056

  • Vainio H . 1998 Toxicol. Lett. 102–103: 581–589

  • van Delft JH, Baan RA, Roza L . 1998a Crit. Rev. Toxicol. 28: 477–510

  • van Delft JHG, Steenwinkel MS, van Asten JG, de Vogel N, Bruijntjes-Rozier TC, Schouten T, Cramer P, Maas L, van Herwijnen MH, van Schooten F, Hopmans PM . 2001 Ann. Occup. Hyg. 45: 395–408

  • van Delft JH, Steenwinkel MJ, van Asten JG, van Es J, Kraak A, Baan RA . 1998b Ann. Occup. Hyg. 42: 105–114

  • van Lieshout EM, Roelofs HM, Dekker S, Mulder CJ, Wobbes T, Jansen JB, Peters WH . 1999 Cancer Res. 59: 586–589

  • Van Schooten FJ, Hirvonen A, Maas LM, De Mol BA, Kleinjans JC, Bell DA, Durrer JD . 1998 FASEB J. 12: 1409–1417

  • Viezzer C, Norppa H, Clonfero E, Gabbani G, Mastrangelo G, Hirvonen A, Celotti L . 1999 Mutat. Res. 431: 259–269

  • Vineis P, Kogevinas M, Simonato L, Brennan P, Boffetta P . 2000 Mutat. Res. 463: 103–110

  • Vineis P, Martone T . 1996 Ann. Ist. Super Sanita 32: 21–27

  • Vineis P, Ronco G . 1992 Environ. Health Perspect. 98: 95–99

  • Vulimiri SV, Wu X, Baer-Dubowska W, de Andrade M, Detry M, Spitz MR, DiGiovanni J . 2000 Mol. Carcinog. 27: 34–46

  • Wang M, Abbruzzese JL, Friess H, Hittelman WN, Evans DB, Abbruzzese MC, Chiao P, Li D . 1998a Cancer Res. 58: 38–41

  • Wang Y, Ichiba M, Iyadomi M, Zhang J, Tomokuni K . 1998b Ind. Health 36: 337–346

  • Watson MA, Stewart RK, Smith GB, Massey TE, Bell DA . 1998 Carcinogenesis 19: 275–280

  • Wei Q, Cheng L, Amos CI, Wang LE, Guo Z, Hong WK, Spitz MR . 2000 J. Natl. Cancer Inst. 92: 1764–1772

  • Whyatt RM, Bell DA, Jedrychowski W, Santella RM, Garte SJ, Cosma G, Manchester DK, Young TL, Cooper TB, Ottman R, Perera FP . 1998 Carcionogenesis 19: 1389–1392

  • Whyatt RM, Perera FP, Jedrychowski W, Santella RM, Garte S, Bell DA . 2000 Cancer Epidemiol. Biomarkers Prev. 9: 207–221

  • Whyatt RM, Jedruchowski W, Hemminki K, Santella RM, Tsai WY, Yang K, Perera FP . 2001 Cancer Epidemiol. Biomarkers Prev. 10: 581–588

  • Wiencke JK, Kelsey KT, Varkonyi A, Semey K, Wain JC, Mark E, Christiani DC . 1995 Cancer Res. 55: 4910–4914

  • Wiencke JK, Nelson H, Wain J, Mark E, Christiani DC, Kelsey KT . 1998 Association of increased PAH DNA adducts and p53 mutations in lung cancer. Proceedings of the 89th Annual Meeting of the American Association for Cancer Research 39: 1998 p 562

  • Wiencke JK, Kelsey KT . 2002 Teen smoking, ‘field cancerization’ and a critical period hypothesis for lung cancer susceptibility Env. Health Perspect, June 2002

  • Wiencke JK, Thurston SW, Kelsey KT, Varkonyi A, Wain JC, Mark EJ, Christiani DC . 1999 J. Natl. Cancer Inst. 91: 614–619

  • Wikman H, Risch A, Klimek F, Schmezer P, Spiegelhalder B, Dienemann H, Kayser K, Schulz V, Drings P, Bartsch H . 2000 Int. J. Cancer 88: 932–937

  • Williams MD, Sandler AB . 2001 Cancer Treat. Res. 105: 31–52

  • Wistuba II, Behrens C, Virmani AK, Mele G, Milchgrub S, Girard L, Fondon 3rd JW, Garner HR, McKay B, Latif F, Lerman MI, Lam S, Gazdar AF, Minna JD . 2000 Cancer Res. 60: 1949–1960

  • Wistuba II, Bryant D, Behrens C, Milchgrub S, Virmani AK, Ashfaq R, Minna JD, Gazdar AF . 1999 Clin. Cancer Res. 5: 991–1000

  • Xing JZ, Carnelley T, Lee J, Watson WP, Booth E, Weinfeld M, Le XC . 2001 Methods Mol. Biol. 162: 419–428

  • Yang SC, Weinfeld M, Jenq SN, Kang ZC, Lee H . 2000 Chem. Res. Toxicol. 13: 1046–1050

  • Yang K, Fang JL, Hemminki K . 1998 Mutat. Res. 422: 285–295

  • Yi P, Sun X, Doerge DR, Fu PP . 1998 Chem. Res. Toxicol. 11: 1032–1041

  • Yueh MF, Nguyen N, Famourzadeh M, Strassburg CP, Oda Y, Guengerich FP, Tukey RH . 2001 Carcinogenesis 22: 943–950

  • Zhang J, Ichiba M, Feng Y, Pan G, Hanaoka T, Yamano Y, Hara K, Takahashi K, Tomokuni K . 2000 Int. Arch. Occup. Environ. Health 73: 127–135

  • Zhou G, Hernandez NS, Randerath E, Randerath K . 2000 Mutat. Res. 447: 137–147

  • Zienolddiny S, Ryberg D, Arab MO, Skaug V, Haugen A . 2001 Br. J. Cancer 84: 226–231

Download references

Acknowledgements

This work was supported by NIH ES06717.

Author information

Authors and Affiliations

  1. Department of Epidemiology and Biostatistics, Laboratory for Molecular Epidemiology, University of California San Francisco, San Francisco, 94143-0560, California, CA, USA

    John K Wiencke

Authors
  1. John K Wiencke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John K Wiencke.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wiencke, J. DNA adduct burden and tobacco carcinogenesis. Oncogene 21, 7376–7391 (2002). https://doi.org/10.1038/sj.onc.1205799

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1205799

Keywords

This article is cited by

Search

Advanced search

Quick links