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.

Genetic susceptibility to tobacco-related cancer

Abstract

Although cigarette smoking is the dominant risk factor for several epithelial cancers, only a small fraction of individuals with tobacco exposure develop cancer. The underlying hypothesis is that genetic factors may render certain smokers more susceptible to cancer than others. Genetic alterations in critical regulatory pathways may predispose cells to carcinogenesis. These pathways include regulation of xenobiotic metabolism; control of genomic stability, including DNA repair mechanisms, cell-cycle checkpoints, apoptosis and telomere length; and control of microenvironmental factors, such as matrix metalloproteinases, inflammation and growth factors. In addition, epigenetic events, such as promoter hypermethylation and loss of imprinting, are also involved in carcinogenesis. In this review, we will summarize recent advances in genetic susceptibility to tobacco-related cancer. Emphasizing on risk assessment, we will describe how genetic variations in the above-mentioned genetic pathways modify the tobacco-related cancer risk. In addition, we will discuss how genetic variations may assist in predicting clinical outcome, such as the natural history of cancer and treatment response. The measurements of genetic susceptibility by both genotypic and phenotypic assays are covered in the text. Finally, we present a number of current concerns that need to be addressed as the exciting field of molecular cancer epidemiology advances rapidly.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Similar content being viewed by others

References

  • Aaronson S . (1991). Science, 254, 1146–1153.

  • Abdel-Rahman SZ, Anwar WA, Abdel-Ala WE, Mostafa HM and Au WW . (1998). Cancer Detect. Prev., 22, 129–138.

  • Alexandrie AK, Sundberg MI, Seidegard J, Tornling G and Rannug A . (1994). Carcinogenesis, 15, 1785–1790.

  • Altshuler D, Hirschhorn JN, Klannemark M, Lindgren CM, Vohl MC, Nemesh J, Lane CR, Schaffner SF, Bolk S, Brewer C, Tuomi T, Gaudet D, Hudson TJ, Daly M, Groop L and Lander ES . (2000). Nat. Genet., 26, 76–80.

  • Anttila S, Hirvonen A, Husgafvel-Pursiainen K, Karjalainen A, Nurminen T and Vainio H . (1994). Carcinogenesis, 15, 1133–1335.

  • Anwar WA, Abdel-Rahman SZ, El Zein RA, Mostafa HM and Au WW . (1996). Carcinogenesis, 17, 1923–1929.

  • Austin GE, Lam L, Zaki SR, Chan WC, Hodge T, Hou J, Swan D, Zhang W, Racine M, Whitsett C and Brown T . (1993). Leukemia, 7, 1445–1450.

  • Badawi AF, Mostafa MH, Probert A and O'Connor PJ . (1995). Eur. J. Cancer Prev., 4, 45–59.

  • Ballaz S and Mulshine JL . (2003). Clin. Lung Cancer, 5, 46–62.

  • Bartsch H, Nair U, Risch A, Rojas M, Wikman H and Alexandrov K . (2000). Cancer Epidemiol. Biomarkers Prev., 9, 3–28.

  • Benhamou S, Lee WJ, Alexandrie AK, Boffetta P, Bouchardy C, Butkiewicz D, Brockmoller J, Clapper ML, Daly A, Dolzan V, Ford J, Gaspari L, Haugen A, Hirvonen A, Husgafvel-Pursiainen K, Ingelman-Sundberg M, Kalina I, Kihara M, Kremers P, Le Marchand L, London SJ, Nazar-Stewart V, Onon-Kihara M, Rannug A, Romkes M, Ryberg D, Seidegard J, Shields P, Strange RC, Stucker I, To-Figueras J, Brennan P and Taioli E . (2002). Carcinogenesis, 23, 1343–1350.

  • Benhamou S, Reinikainen M, Bouchardy C, Dayer P and Hirvonen A . (1998). Cancer Res., 58, 5291–5293.

  • Bergamaschi D, Gasco M, Hiller L, Sullivan A, Syed N, Trigiante G, Yulug I, Merlano M, Numico G, Comino A, Attard M, Reelfs O, Gusterson B, Bell AK, Heath V, Tavassoli M, Farrell PJ, Smith P, Lu X and Crook T . (2003). Cancer Cell, 3, 387–402.

  • Betticher DC, Thatcher N, Altermatt HJ, Hoban P, Ryder WD and Heighway J . (1995). Oncogene, 11, 1005–1011.

  • Biros E, Kohut A, Biros I, Kalina I, Bogyiova E and Stubna J . (2002). Lung Cancer, 35, 231–235.

  • Blackburn EH . (2001). Cell, 106, 661–673.

  • Bonassi S, Abbondandolo A, Camurri L, Dal Pra L, De Ferrari M, Degrassi F, Forni A, Lamberti L, Lando C, Padovani P, Sbrana I, Vecchio D and Puntoni R . (1995). Cancer Genet. Cytogenet., 79, 133–135.

  • Bosken CH, Wei Q, Amos CI and Spitz MR . (2002). J. Natl. Cancer Inst., 94, 1091–1099.

  • Bouchardy C, Mitrunen K, Wikman H, Husgafvel-Pursiainen K, Dayer P, Benhamou S and Hirvonen A . (1998). Pharmacogenetics, 8, 291–298.

  • Brockmöller J, Cascorbi I, Kerb R and Roots I . (1996). Cancer Res., 56, 3915–3925.

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

  • Cajas-Salazar N, Au WW, Zwischenberger JB, Sierra-Torres CH, Salama SA, Alpard SK and Tyring SK . (2003). Cancer Genet. Cytogenet., 145, 97–102.

  • Camps C, Sarries C, Roig B, Sanchez JJ, Queralt C, Sancho E, Martinez N, Taron M and Rosell R . (2003). Clin. Lung Cancer, 4, 237–241.

  • Cascorbi I, Brockmoller J, Mrozikiewicz PM, Bauer S, Loddenkemper R and Roots I . (1996). Cancer Res., 56, 3961–3966.

  • Cascorbi I, Henning S, Brockmoller J, Gephart J, Meisel C, Muller JM, Loddenkemper R and Roots I . (2000). Cancer Res., 60, 644–649.

  • Chan SW and Blackburn EH . (2003). Mol. Cell, 11, 1379–1387.

  • Chen H, Lum A, Seifried A, Wilkens LR and Le Marchand L . (1999). Cancer Res., 59, 3045–3058.

  • Chen WC, Wu HC, Hsu CD, Chen HY and Tsai FJ . (2002). Urol. Oncol., 7, 63–66.

  • Chin L, Artandi SE, Shen Q, Tam A, Lee SL, Gottlieb GJ, Greider CW and DePinho RA . (1999). Cell, 97, 527–538.

  • Choi JY, Lee KM, Cho SH, Kim SW, Choi HY, Lee SY, Im HJ, Yoon KJ, Choi H, Choi I, Hirvonen A, Hayes RB and Kang D . (2003). Pharmacogenetics, 13, 349–355.

  • Christmann M, Tomicic MT, Roos WP and Kaina B . (2003). Toxicology, 193, 3–34.

  • Cortessis VK, Siegmund K, Xue S, Ross RK and Yu MC . (2003). Carcinogenesis, 24, 1645–1650.

  • Cui H, Cruz-Correa M, Giardiello FM, Hutcheon DF, Kafonek DR, Brandenburg S, Wu Y, He X, Powe NR and Feinberg AP . (2003). Science, 299, 1753–1755.

  • Cui H, Horon IL, Ohlsson R, Hamilton SR and Feinberg AP . (1998). Nat. Med., 4, 1276–1280.

  • Curigliano G, Zhang YJ, Wang LY, Flamini G, Alcini A, Ratto C, Giustacchini M, Alcini E, Cittadini A and Santella RM . (1996). Carcinogenesis, 17, 911–916.

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

  • David-Beabes G, Lunn RM and London S . (2001). Cancer Epidemiol. Biomarkers Prev., 10, 911–912.

  • Deal C, Ma J, Wilkin F, Paquette J, Rozen F, Ge B, Hudson T, Stampfer M and Pollak M . (2001). J. Clin. Endocrinol. Metab., 86, 1274–1280.

  • Debatin KM . (2004). Cancer Immunol. Immunother., 53, 153–159.

  • de Laat WL, Jaspers NG and Hoeijmakers JH . (1999). Genes Dev., 3, 768–785.

  • de Lange T . (2002). Oncogene, 21, 532–540.

  • De Mellow JS and Baxter RC . (1988). Biochem. Biophys. Res. Commun., 156, 199–204.

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

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

  • Dunn BP, Vedal S, San RH, Kwan WF, Nelems B, Enarson DA and Stich HF . (1991). Int. J. Cancer, 48, 485–492.

  • Dunn SE, Hardman RA, Kari FW and Barrett JC . (1997). Cancer Res., 57, 2687–2693.

  • d’Errico A, Taioli E, Chen X and Vineis P . (1996). Biomarkers, 1, 149–173.

  • Engel LS, Taioli E, Pfeiffer R, Garcia-Closas M, Marcus PM, Lan Q, Boffetta P, Vineis P, Autrup H, Bell DA, Branch RA, Brockmoller J, Daly AK, Heckbert SR, Kalina I, Kang D, Katoh T, Lafuente A, Lin HJ, Romkes M, Taylor JA and Rothman N . (2002). Am. J. Epidemiol., 156, 95–109.

  • Fajas L, Auboeuf D, Raspe E, Schoonjans K, Lefebvre AM and Saladin R . (1997). J. Biol. Chem., 272, 18779–18789.

  • Farker K, Lehmann MH, Oelschlagel B, Haerting J, Hoffmann A, Janitzky V and Schubert J . (1998). Exp. Toxicol. Pathol., 50, 425–431.

  • Feinberg AP, Cui H and Ohlsson R . (2002). Semin. Cancer Biol., 12, 389–398.

  • Ferguson-Smith AC and Surani MA . (2001). Science, 293, 1086–1089.

  • Fisher MJ, Virmani AK, Wu L, Aplenc R, Harper JC, Powell SM, Rebbeck TR, Sidransky D, Gazdar AF and El-Deiry WS . (2001). Clin. Cancer Res., 7, 1688–1697.

  • Fishman D, Faulds G, Jeffery R, Mohamed-Ali V, Yudkin JS, Humphries S and Woo P . (1998). J. Clin. Invest., 102, 1369–1376.

  • Gao CM, Takezaki T, Wu JZ, Li ZY, Liu YT, Li SP, Ding JH, Su P, Hu X, Xu TL, Sugimura H and Tajima K . (2002). Cancer Lett., 188, 95–102.

  • Garcia-Closas M, Kelsey KT, Wiencke JK, Xu X, Wain JC and Christiani DC . (1997). Cancer Causes Control, 8, 544–553.

  • Geisler SA and Olshan AF . (2001). Am. J. Epidemiol., 154, 95–105.

  • Ghilardi G, Biondi ML, Caputo M, Leviti S, DeMonti M, Guagnellini E and Scorza R . (2002). Clin. Cancer Res., 8, 3820–3823.

  • Gisselsson D, Jonson T, Petersen A, Strombeck B, Dal Cin P, Hoglund M, Mitelman F, Mertens F and Mandahl N . (2001). Proc. Natl. Acad. Sci. USA, 98, 12683–12688.

  • Goode EL, Ulrich CM and Potter JD . (2002). Cancer Epidemiol. Biomarkers Prev., 11, 1513–1530.

  • Goto I, Yoneda S, Yamamoto M and Kawajiri K . (1996). Cancer Res., 56, 3725–3730.

  • Grady WM, Willis J, Guilford PJ, Dunbier AK, Toro TT, Lynch H, Wiesner G, Ferguson K, Eng C, Park JG, Kim SJ and Markowitz S . (2000). Nat. Genet., 26, 16–17.

  • Haber JE . (1999). Cell, 97, 829–832.

  • Hackett JA, Feldser DM and Greider CW . (2001). Cell, 106, 275–286.

  • Hagmar L, Brogger A, Hansteen I, Heim S, Hogstedt B, Knudsen L, Lambert B, Linnainmaa K, Mitelman F, Nordenson I, Reuterwall C, Salomaa S, Skerfving S and Sorsa M . (1994). Cancer Res., 54, 2919–2922.

  • Hamada GS, Sugimura H, Suzuki I, Nagura K, Kiyokawa E, Iwase T, Tanaka M, Takahashi T, Watanabe S, Kino I and Tsugane S . (1995). Cancer Epidemiol. Biomarkers Prev., 4, 63–67.

  • Harrela M, Koistinen H, Kaprio J, Lehtovirta M, Tuomilehto J, Eriksson J, Toivanen L, Koskenvuo M, Leinonen P, Koistinen R and Seppala M . (1996). J. Clin. Invest., 98, 2612–2615.

  • Harris CC . (1993). Science, 262, 1980–1981.

  • Harris MJ, Coggan M, Langton L, Wilson SR and Board PG . (1998). Pharmacogenetics, 8, 27–31.

  • Hassett C, Aicher L, Sidhu JS and Omiecinski CJ . (1994). Hum. Mol. Genet., 3, 421–428.

  • Hayashi S, Watanabe J, Nakachi K and Kawajiri K . (1991). J. Biochem., 110, 407–411.

  • Hayashi SI, Watanabe J and Kawajiri K . (1992). Jpn. J. Cancer Res., 83, 866–870.

  • Hayes JD and Pulford DJ . (1995). Crit. Rev. Biochem. Mol. Biol., 30, 445–600.

  • Hazra A, Chamberlain RM, Grossman HB, Zhu Y, Spitz MR and Wu X . (2003). Cancer Res., 63, 1157–1159.

  • Hecht SS . (1999). J. Natl. Cancer Inst., 91, 1194–1210.

  • Herman JG . (1999). Semin. Cancer Biol., 9, 359–367.

  • Herman JG and Baylin SB . (2003). N. Engl. J. Med., 349, 2042–2054.

  • Hinoda Y, Okayama N, Takano N, Fujimura K, Suehiro Y, Hamanaka Y, Hazama S, Kitamura Y, Kamatani N and Oka M . (2002). Int. J. Cancer, 102, 526–529.

  • Hirata H, Naito K, Yoshihiro S, Matsuyama H, Suehiro Y and Hinoda Y . (2003). Int. J. Cancer, 106, 372–374.

  • Hirvonen A, Husgafvel-Pursiainen K, Anttila S and Vainio H . (1993). Carcinogenesis, 14, 1479–1481.

  • Hirvonen A, Husgafvel-Pursiainen K, Karjalainen A, Anttila S and Vainio H . (1992). Cancer Epidemiol. Biomarkers Prev., 1, 485–489.

  • Hoffmann D, Hoffmann I and El-Bayoumy K . (2001). Chem. Res. Toxicol., 14, 767–790.

  • Hojilla CV, Mohammed FF and Khokha R . (2003). Br. J. Cancer, 89, 1817–1821.

  • Holley SL, Parkes G, Matthias C, Bockmuhl U, Jahnke V, Leder K, Strange RC, Fryer AA and Hoban PR . (2001). Am. J. Pathol., 159, 1917–1924.

  • Hong Y, Pedersen N, Brismar K, Hall K and de Faire U . (1996). J. Clin. Endocrinol. Metab., 81, 1791–1797.

  • Houlston RS . (2000). Pharmacogenetics, 10, 105–114.

  • Hsu TC . (1987). In vitro Cell Dev. Biol., 23, 591–603.

  • Hsu TC, Johnston DA, Cherry LM, Ramkissoon D, Schantz SP, Jessup JM, Winn RJ, Shirley L and Furlong C . (1989). Int. J. Cancer, 43, 403–409.

  • Hu JJ, Roush GC, Berwick M, Dubin N, Mahabir S, Chandiramani M and Boorstein R . (1996). Cancer Epidemiol. Biomarkers Prev., 5, 263–270.

  • Huang QR, Morris D and Manolios N . (1997). Mol. Immunol., 34, 577–582.

  • Hung HC, Chuang J, Chien YC, Chern HD, Chiang CP, Kuo YS, Hildesheim A and Chen CJ . (1997). Cancer Epidemiol. Biomarkers Prev., 6, 901–905.

  • Hung RJ, Boffetta P, Brockmoller J, Butkiewicz D, Cascorbi I, Clapper ML, Garte S, Haugen A, Hirvonen A, Anttila S, Kalina I, Le Marchand L, London SJ, Rannug A, Romkes M, Salagovic J, Schoket B, Gaspari L and Taioli E . (2003). Carcinogenesis, 24, 875–882.

  • Inatomi H, Katoh T, Kawamoto T and Matsumoto T . (1999). Int. J. Urol., 6, 446–454.

  • Ishibe N, Wiencke JK, Zuo ZF, McMillan A, Spitz M and Kelsey KT . (1997). Cancer Epidemiol. Biomarkers Prev., 6, 1075–1080.

  • Jeng YL, Wu MH, Huang HB, Lin WY, You SL, Chu TY, Chen CJ and Sun CA . (2003). Anticancer Res., 23, 5149–5152.

  • Jensen RA and Page DL . (1993). Hum. Pathol., 24, 455–456.

  • Jeon HS, Kim KM, Park SH, Lee SY, Choi JE, Lee GY, Kam S, Park RW, Kim IS, Kim CH, Jung TH and Park JY . (2003). Carcinogenesis, 24, 1677–1681.

  • Jernstrom H, Chu W, Vesprini D, Tao Y, Majeed N, Deal C, Pollak M and Narod SA . (2001). Mol. Genet. Metab., 72, 144–154.

  • Johns LE and Houlston RS . (2000). Environ. Mol. Mutagen., 36, 221–227.

  • Jones PA and Baylin SB . (2002). Nat. Rev. Genet., 3, 415–428.

  • Jones PA and Laird PW . (1999). Nat. Genet., 21, 163–167.

  • Joos L, He JQ, Shepherdson MB, Connett JE, Anthonisen NR, Pare PD and Sandford AJ . (2002). Hum. Mol. Genet., 11, 569–576.

  • Joseph P and Jaiswal AK . (1994). Proc. Natl. Acad. Sci. USA, 91, 8413–8417.

  • Kalow W, Tang BK and Endrenyi I . (1998). Pharmacogenetics, 8, 283–289.

  • Kanayama H, Yokota K, Kurokawa Y, Murakami Y, Nishitani M and Kagawa S . (1998). Cancer, 82, 1359–1366.

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

  • Katoh T, Inatomi H, Nagaoka A and Sugita A . (1995). Carcinogenesis, 16, 655–657.

  • Katoh T, Kaneko S, Takasawa S, Nagata N, Inatomi H, Ikemura K, Itoh H, Matsumoto T, Kawamoto T and Bell DA . (1999). Pharmacogenetics, 9, 165–169.

  • Kawajiri K, Nakachi K, Imai K, Yoshii A, Shinoda N and Watanabe J . (1990). FEBS Lett., 263, 131–133.

  • Kiemeney LA and Schoenberg M . (1996). J. Urol., 156, 867–872.

  • Kihara M, Kihara M and Noda K . (1994). Carcinogenesis, 16, 2331–2336.

  • Kihara M, Kihara M, Noda K and Okamoto N . (1993). Cancer Lett., 71, 151–155.

  • Kihara M and Noda K . (1999). Cancer Lett., 137, 53–60.

  • Knight JC, Keating BJ, Rockett KA and Kwiatkowski DP . (2003). Nat. Genet., 33, 469–475.

  • Laiho M and Latonen L . (2003). Ann. Med., 35, 391–397.

  • Landi S, Moreno V, Gioia-Patricola L, Guino E, Navarro M, de Oca J, Capella G, Canzian F and Bellvitge Colorectal Cancer Study Group. (2003). Cancer Res., 63, 3560–3566.

  • Le Marchand L, Donlon T, Lum-Jones A, Seifried A and Wilkens LR . (2002). Cancer Epidemiol. Biomarkers Prev., 11, 409–412.

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

  • Le Marchand L, Sivaraman L, Pierce L, Seifried A, Lum A, Wilkens LR and Lau AF . (1998). Cancer Res., 58, 4858–4863.

  • LeRoith D, Werner H, Beitner-Johnson D and Roberts Jr. CT . (1995). Endocr. Rev., 16, 143–163.

  • Lewis SJ, Cherry NM, Niven RM, Barber PV and Povey AC . (2001). Lung Cancer, 34, 177–183.

  • Lin DX, Tang YM, Peng Q, Lu SX, Ambrosone CB and Kadlubar FF . (1998). Cancer Epidemiol. Biomarkers Prev., 7, 1013–1018.

  • Lin P, Wang HJ, Lee H, Lee HS, Wang SL, Hsueh YM, Tsai KJ and Chen CY . (1999). J. Toxicol. Environ. Health A, 58, 187–197.

  • Lin P, Wang SL, Wang HJ, Chen KW, Lee HS, Tsai KJ, Chen CY and Lee H . (2000). Br. J. Cancer, 82, 852–857.

  • London SJ, Daly AK, Cooper J, Navidi WC, Carpenter CL and Idle JR . (1995). J. Natl. Cancer Inst., 87, 1246–1253.

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

  • Lunn RM, Helzlsouer KJ, Parshad R, Umbach DM, Harris EL, Sanford KK and Bell DA . (2000). Carcinogenesis, 21, 551–555.

  • Mabrouk I, Baccouche S, El-Abed R, Mokdad-Gargouri R, Mosbah A, Said S, Daoud J, Frikha M, Jlidi R and Gargouri A . (2003). Ann. NY Acad. Sci., 1010, 764–770.

  • Malats N, Camus-Radon AM, Nyberg F, Ahrens W, Constantinescu V, Mukeria A, Benhamou S, Batura-Gabryel H, Bruske-Hohlfeld I, Simonato L, Menezes A, Lea S, Lang M and Boffetta P . (2000). Cancer Epidemiol. Biomarkers Prev., 9, 827–833.

  • Malkinson AM, Bauer A, Meyer A, Dwyer-Nield L, Koski K, Keith R, Geraci M and Miller Y . (2000). Chest, 117, 228S.

  • Manning CB, Vallyathan V and Mossman BT . (2002). Int. Immunopharmacol., 2, 191–200.

  • Marcus PM, Hayes RB, Vineis P, Garcia-Closas M, Caporaso NE, Autrup H, Branch RA, Brockmoller J, Ishizaki T, Karakaya AE, Ladero JM, Mommsen S, Okkels H, Romkes M, Roots I and Rothman N . (2000a). Cancer Epidemiol. Biomarkers Prev., 9, 461–467.

  • Marcus PM, Vineis P and Rothman N . (2000b). Pharmacogenetics, 10, 115–122.

  • Marsh HP, Haldar NA, Bunce M, Marshall SE, le Monier K, Winsey SL, Christodoulos K, Cranston D, Welsh KI and Harris AL . (2003). Br. J. Cancer, 89, 1096–1101.

  • Martin SG, Laroche T, Suka N, Grunstein M and Gasser SM . (1999). Cell, 97, 621–633.

  • Martinez C, Agundez JA, Olivera M, Martin R, Ladero JM and Benitez J . (1995). Pharmacogenetics, 5, 207–214.

  • Matakidou A, Eisen T and Houlston RS . (2003). Mutagenesis, 18, 377–385.

  • Matthias C, Branigan K, Jahnke V, Leder K, Haas J, Heighway J, Jones PW, Strange RC, Fryer AA and Hoban PR . (1998). Clin. Cancer Res., 4, 2411–2418.

  • Matthias C, Jahnke V, Jones PW, Hoban PR, Alldersea JE, Worrall SF, Fryer AA and Strange RC . (1999). Cancer Epidemiol. Biomarkers Prev., 8, 815–823.

  • Matullo G, Guarrera S, Carturan S, Peluso M, Malaveille C, Davico L, Piazza A and 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 and Vineis P . (2001b). Carcinogenesis, 22, 1437–1445.

  • Mayne ST, Buenconsejo J and Anderich DT . (1999). Am. J. Epidemiol., 149, 13–20.

  • McCann J . (1999). J. Natl. Cancer Inst., 91, 497–498.

  • McEachern MJ and Iyer S . (2001). Mol. Cell, 7, 695–704.

  • McEachern MJ, Krauskopf A and Blackburn EH . (2000). Annu. Rev. Genet., 34, 331–358.

  • McWilliams JE, Sanderson BJ, Harris EL, Richert-Boe KE and Henner WD . (1995). Cancer Epidemiol. Biomarkers Prev., 4, 589–594.

  • Miao X, Yu C, Tan W, Xiong P, Liang G, Lu W and Lin D . (2003). Cancer Res., 63, 3987–3990.

  • Miller DG, Tiwari R, Pathak S, Hopwood VL, Gilbert F and Hsu TC . (1998). Cancer Epidemiol. Biomarkers Prev., 7, 321–327.

  • Miller DP, De Vivo I, Neuberg D, Wain JC, Lynch TJ, Su L and Christiani DC . (2003a). Int. J. Cancer, 104, 758–763.

  • Miller DP, Liu G, De Vivo I, Lynch TJ, Wain JC, Su L and Christiani DC . (2002). Cancer Res., 62, 2819–2823.

  • Miller DP, Neuberg D, de Vivo I, Wain JC, Lynch TJ, Su L and Christiani DC . (2003b). Epidemiology, 14, 545–551.

  • Minematsu N, Nakamura H, Tateno H, Nakajima T and Yamaguchi K . (2001). Biochem. Biophys. Res. Commun., 289, 116–119.

  • Morita S, Yano M, Tsujinaka T, Akiyama Y, Taniguchi M, Kaneko K, Miki H, Fujii T, Yoshino K, Kusuoka H and Monden M . (1999). Int. J. Cancer, 80, 685–688.

  • Murray GI, Duncan ME, O'Neil P, McKay JA, Melvin WT and Fothergill JE . (1998). J. Pathol., 185, 256–261.

  • Murray GI, Duncan ME, O'Neil P, Melvin WT and Fothergill JE . (1996). Nat. Med., 2, 461–462.

  • Myohanen SK, Baylin SB and Herman JG . (1998). Cancer Res., 58, 591–593.

  • Nakachi K, Imai K, Hayashi S, Watanabe J and Kawajiri K . (1991). Cancer Res., 51, 5177–5180.

  • Nakachi K, Imai K, Hayashi SI and Kawajiri K . (1993). Cancer Res., 53, 2994–2999.

  • Nazar-Stewart V, Vaughan TL, Stapleton P, Van Loo J, Nicol-Blades B and Eaton DL . (2003). Lung Cancer, 40, 247–258.

  • Nia A, Maas LM, Brouwer EM, Kleinjans JC and Van Schooten FJ . (2000). Carcinogenesis (Lond.), 21, 1335–1340.

  • Nickerson T, Huynh H and Pollack M . (1997). Biochem. Biophys. Res. Commun., 237, 690–693.

  • Nimura Y, Yokoyama S, Fujimori M, Aoki T, Adachi W, Nasu T, He M, Ping YM and Iida F . (1997). Cancer (Phila.), 80, 852–857.

  • Okada T, Kawashima K, Fukushi S, Minakuchi T and Nishimura S . (1994). Pharmacogenetics, 4, 333–340.

  • Oyama T, Kawamoto T, Mizoue T, Yasumoto K, Kodama Y and Mitsudomi T . (1997). Anticancer Res., 17, 577–582.

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

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

  • Park JY, Muscat JE, Ren Q, Schantz SP, Harwick RD, Stern JC, Pike V, Richie Jr JP and Lazarus P . (1997). Cancer Epidemiol. Biomarkers Prev., 6, 791–797.

  • Park JY, Park SH, Choi JE, Lee SY, Jeon HS, Cha SI, Kim CH, Park JH, Kam S, Park RW, Kim IS and Jung TH . (2002b). Cancer Epidemiol. Biomarkers Prev., 11, 993–997.

  • Park SJ, Zhao H, Spitz MR, Grossman HB and Wu X . (2003). Mutat. Res., 536, 131–137.

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

  • Perera FP, Mooney LA, Stampfer M, Phillips DH, Bell DA, Rundle A, Cho S, Tsai WY, Ma J, Blackwood A, Tang D and Physicians’ Health Cohort Study. (2002). Carcinogenesis, 23, 1641–1646.

  • Peto R, Darby S, Deo H, Silcocks P, Whitley E and Doll R . (2000). BMJ, 321, 323–329.

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

  • Pfeifer K . (2000). Am. J. Hum. Genet., 67, 777–787.

  • Philip PA, Fitzgerald DL, Cartwright RA, Peake MD and Rogers HJ . (1988). Carcinogenesis, 9, 491–493.

  • Phillips DH . (2002). Carcinogenesis, 23, 1979–2004.

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

  • Phillips DH, Schoket B, Hewer A, Bailey E, Kostic S and Vincze I . (1990). Int. J. Cancer, 46, 569–575.

  • Pinabasi H, Silig Y, Cetinkaya O, Seyfikli Z and Pinabasi E . (2003). Cancer Genet. Cytogenet., 146, 125–129.

  • Qiao Y, Spitz MR, Shen H, Guo Z, Shete S, Hedayati M, Grossman L, Mohrenweiser H and Wei Q . (2002). Carcinogenesis, 23, 295–299.

  • Qiuling S, Yuxin Z, Suhua Z, Cheng X, Shuguang L and Fengsheng H . (2003). Carcinogenesis, 24, 1499–1503.

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

  • Rebbeck TR . (1997). Cancer Epidemiol. Biomarkers Prev., 6, 733–743.

  • Reik W and Walter J . (2001). Nat. Rev. Genet., 2, 21–32.

  • Rojas E, Lopez MC and Valverde M . (1999). J. Chromatogr. B Biomed. Sci. Appl., 722, 225–254.

  • Rosell R, Taron M, Alberola V, Massuti B and Felip E . (2003). Lung Cancer, 1, S97–102.

  • Rosen CJ, Kurland ES, Vereault D, Adler RA, Rackoff PJ, Craig WY, Witte S, Rogers J and Bilezikian JP . (1998). J. Clin. Endocrinol. Metab., 83, 2286–2290.

  • Ross D, Traver RD, Siegel D, Kuehl BL, Misra V and Rauth AM . (1996). Br. J. Cancer, 74, 995–996.

  • Rosvold EA, McGlynn KA, Lustbader ED and Buetow KH . (1995). Pharmacogenetics, 5, 199–206.

  • Rotwein P, Pollock KM, Didier DK and Krivi GG . (1986). J. Biol. Chem., 261, 4828–4832.

  • Roy B, Beamon J, Balint E and Reisman D . (1994). Mol. Cell. Biol., 14, 7805–7815.

  • Ruano-Ravina A, Figueiras A, Loidi L and Barros-Dios JM . (2003). Anticancer Res., 23, 4333–4337.

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

  • Saarikoski ST, Reinikainen M, Anttila S, Karjalainen A, Vainio H, Husgafvel-Pursiainen K and Hirvonen A . (2000). Pharmacogenetics, 10, 183–185.

  • Santella RM . (1999). Cancer Epidemiol. Biomarkers Prev., 8, 733–739.

  • Sanyal S, Festa F, Sakano S, Zhang Z, Steineck G, Norming U, Wijkstrom H, Larsson P, Kumar R and Hemminki K . (2004). Carcinogenesis, 25, 729–734.

  • Schabath MB, Spitz MR, Grossman HB, Zhang K, Dinney CP, Zheng PJ and Wu X . (2003). J. Natl. Cancer Inst., 95, 540–547.

  • Schabath MB, Spitz MR, Hong WK, Delclos GL, Reynolds WF, Gunn GB, Whitehead LW and Wu X . (2002). Lung Cancer, 37, 35–40.

  • Schabath MB, Spitz MR, Zhang X, Delclos GL and Wu X . (2000). Carcinogenesis, 21, 1163–1166.

  • Seidegard J, Vorachek WR, Pero RW and Pearson WR . (1988). Proc. Natl. Acad. Sci. USA, 85, 7293–7297.

  • Sellers TA, Chen PL, Potter JD, Bailey-Wilson JE, Rothschild H and Elston RC . (1994). Am. J. Med. Genet., 52, 308–314.

  • Seow A, Zhao B, Poh WT, Teh M, Eng P, Wang YT, Tan WC, Lee EJ and Lee HP . (1999). Carcinogenesis, 20, 1877–1881.

  • Shen H, Spitz MR, Wang LE, Hong WK and Wei Q . (2001a). Cancer Epidemiol. Biomarkers Prev., 10, 397–401.

  • Shen H, Sturgis EM, Khan SG, Qiao Y, Shahlavi T, Eicher SA, Xu Y, Wang X, Strom SS, Spitz MR, Kraemer KH and Wei Q . (2001b). Cancer Res., 61, 3321–3325.

  • Shen H, Wang L, Spitz MR, Hong WK, Mao L and Wei Q . (2002). Cancer Res., 62, 4992–4995.

  • Shields PG and Harris CC . (2000). J. Clin. Oncol., 8, 2309–2315.

  • Shih CM, Lin PT, Wang HC, Huang WC and Wang YC . (2000). Jpn. J. Cancer Res., 91, 9–15.

  • Shima I, Sasaguri Y, Kusukawa J, Yamana H, Fujita H, Kakegawa T and Morimatsu M . (1992). Cancer, 70, 2747–2753.

  • Shopland DR, Eyre HJ and Pechacek TF . (1991). J. Natl. Cancer Inst., 83, 1142–1148.

  • Siegel D, McGuinness SM, Winski SL and Ross D . (1999). Pharmacogenetics, 9, 113–121.

  • Sjalander A, Birgander R, Rannug A, Alexandrie AK, Tornling G and Beckman G . (1996). Hum. Hered., 46, 221–225.

  • Smith WM, Zhou XP, Kurose K, Gao X, Latif F, Kroll T, Sugano K, Cannistra SA, Clinton SK, Maher ER, Prior TW and Eng C . (2001). Hum. Genet., 109, 146–151.

  • Smogorzewska A, Karlseder J, Holtgreve-Grez H, Jauch A and de Lange T . (2002). Curr. Biol., 12, 1635–1644.

  • Song C, Xing D, Tan W, Wei Q and Lin D . (2001). Cancer Res., 61, 3272–3275.

  • Spitz MR, Wei Q, Dong Q, Amos CI and Wu X . (2003). Cancer Epidemiol. Biomarkers Prev., 12, 689–698.

  • Spitz MR, Wu X, Wang Y, Wang LE, Shete S, Amos CI, Guo Z, Lei L, Mohrenweiser H and Wei Q . (2001). Cancer Res., 61, 1354–1357.

  • Stolzenberg-Solomon RZ, Qiao YL, Abnet CC, Ratnasinghe DL, Dawsey SM, Dong ZW, Taylor PR and Mark SD . (2003). Cancer Epidemiol. Biomarkers Prev., 12, 1222–1226.

  • Stucker I, Hirvonen A, de Waziers I, Cabelguenne A, Mitrunen K, Cenee S, Koum-Besson E, Hemon D, Beaune P and Loriot MA . (2002). Carcinogenesis, 23, 1475–1481.

  • Su L, Liu G, Zhou W, Xu LL, Miller DP, Park S, Lynch TJ, Wain JC and Christiani DC . (2003). Cancer Epidemiol. Biomarkers Prev., 12, 174–175.

  • Su T, Bao Z, Zhang QY, Smith TJ, Hong JY and Ding X . (2000). Cancer Res., 60, 5074–5079.

  • 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 and Yokota J . (1999). Cancer Epidemiol. Biomarkers Prev., 8, 669–674.

  • Sweeney C, Nazar-Stewart V, Stapleton PL, Eaton DL and Vaughan TL . (2003). Cancer Epidemiol. Biomarkers Prev., 12, 527–533.

  • Tefre T, Ryberg D, Haugen A, Nebert DW, Skaug V, Brogger A and Borresen AL . (1991). Pharmacogenetics, 1, 20–25.

  • Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC and Sasaki YF . (2000). Environ. Mol. Mutagen., 35, 206–221.

  • To-Figueras J, Gene M, Gomez-Catalan J, Galan MC, Fuentes M, Ramon JM, Rodamilans M, Huguet E and Corbella J . (1997). Carcinogenesis, 18, 1529–1533.

  • To-Figueras J, Gene M, Gomez-Catalan J, Pique E, Borrego N, Carrasco JL, Ramon J and Corbella J . (1999). Cancer Causes Control, 10, 65–70.

  • Tsai FJ, Lu HF, Yeh LS, Hsu CD and Chen WC . (2001). Urol. Res., 29, 412–416.

  • Vaessen N, Heutink P, Janssen JA, Witteman JC, Testers L, Hofman A, Lamberts SW, Oostra BA, Pols HA and van Duijn CM . (2001). Diabetes, 50, 637–642.

  • Veglia F, Matullo G and Vineis P . (2003). Cancer Epidemiol. Biomarkers Prev., 12, 157–160.

  • Vineis P, Veglia F, Benhamou S, Butkiewicz D, Cascorbi I, Clapper ML, Dolzan V, Haugen A, Hirvonen A, Ingelman-Sundberg M, Kihara M, Kiyohara C, Kremers P, Le Marchand L, Ohshima S, Pastorelli R, Rannug A, Romkes M, Schoket B, Shields P, Strange RC, Stucker I, Sugimura H, Garte S, Gaspari L and Taioli E . (2003). Int. J. Cancer, 104, 650–657.

  • Vogelstein B and Kinzler KW . (1992). Cell, 70, 523–526.

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

  • Wang AH, Sun CS, Li LS, Huang JY, Chen QS and Xu DZ . (2004). World J. Gastroenterol., 10, 940–944.

  • Wang H, Tan W, Hao B, Miao X, Zhou G, He F and Lin D . (2003a). Cancer Res., 63, 8057–8061.

  • Wang J, Deng Y, Cheng J, Ding J and Tokudome S . (2003b). Cancer Lett., 201, 185–193.

  • Wang L, Habuchi T, Takahashi T, Mitsumori K, Kamoto T, Kakehi Y, Kakinuma H, Sato K, Nakamura A, Ogawa O and Kato T . (2002a). Carcinogenesis, 23, 257–264.

  • Wang LE, Cheng L, Spitz MR and Wei Q . (2003c). Lung Cancer, 42, 1–8.

  • Wang LI, Miller DP, Sai Y, Liu G, Su L, Wain JC, Lynch TJ and Christiani DC . (2001). J. Natl. Cancer Inst., 93, 1818–1821.

  • Wang Y, Liang D, Spitz MR, Zhang K, Dong Q, Amos CI and Wu X . (2003d). Cancer, 98, 1701–1706.

  • Wang Y, Spitz MR, Tsou AM, Zhang K, Makan N and Wu X . (2002b). Lung Cancer, 35, 137–142.

  • Wang Y, Spitz MR, Zhu Y, Dong Q, Shete S and Wu X . (2003e). DNA Repair (Amst.), 2, 901–908.

  • Wang YC, Lee HS, Chen SK, Chang YY and Chen CY . (1999). Eur. J. Cancer, 35, 226–230.

  • Warren AJ and Shields PG . (1997). Proc. Soc. Exp. Biol. Med., 216, 172–180.

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

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

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

  • Williams JA, Stone EM, Millar BC, Gusterson BA, Grover PL and Phillips DH . (1998). Pharmacogenetics, 8, 519–528.

  • Williams MP and Pounder RE . (1999). Am. J. Gastroenterol., 94, S11–S16.

  • Wong KK, Chang S, Weiler SR, Ganesan S, Chaudhuri J, Zhu C, Artandi SE, Rudolph KL, Gottlieb GJ, Chin L, Alt FW and DePinho RA . (2000). Nat. Genet., 26, 85–88.

  • Wood RD, Mitchell M, Sgouros J and Lindahl T . (2001). Science, 291, 1284–1289.

  • Woodson K, Flood A, Green L, Tangrea JA, Hanson J, Cash B, Schatzkin A and Schoenfeld P . (2004). J. Natl. Cancer Inst., 96, 407–410.

  • Wu X, Amos CI, Kemp BL, Shi H, Jiang H, Wan Y and Spitz MR . (1998a). Cancer Epidemiol. Biomarkers Prev., 7, 13–18.

  • Wu X, Amos CI, Zhu Y, Zhao H, Grossman BH, Shay JW, Luo S, Hong WK and Spitz MR . (2003a). J. Natl. Cancer Inst., 95, 1211–1218.

  • Wu X, Gu J, Amos CI, Jiang H, Hong WK and Spitz MR . (1998b). Cancer, 83, 1118–1127.

  • Wu X, Gu J, Hong WK, Lee JJ, Amos CI, Jiang H, Winn RJ, Fu KK, Cooper J and Spitz MR . (1998c). J. Natl. Cancer Inst., 90, 1393–1399.

  • Wu X, Gwyn K, Amos CI, Makan N, Hong WK and Spitz MR . (2001). Carcinogenesis, 22, 923–928.

  • Wu X, Shi H, Jiang H, Kemp B, Hong WK, Delclos GL and Spitz MR . (1997). Carcinogenesis, 18, 967–973.

  • Wu X, Zhao H, Amos CI, Shete S, Makan N, Hong WK, Kadlubar FF and Spitz MR . (2002). J. Natl. Cancer Inst., 94, 681–690.

  • Wu X, Zhao H, Wei Q, Amos CI, Zhang K, Guo Z, Qiao Y, Hong WK and Spitz MR . (2003b). Carcinogenesis, 24, 505–509.

  • Xing DY, Tan W, Song N and Lin DX . (2001). Int. J. Cancer, 95, 140–143.

  • Xu LL, Wain JC, Miller DP, Thurston SW, Su L, Lynch TJ and Christiani DC . (2001). Cancer Epidemiol. Biomarkers Prev., 10, 303–309.

  • Yu C, Lu W, Tan W, Xing D, Liang G, Miao X and Lin D . (2003). Cancer Epidemiol. Biomarkers Prev., 12, 176.

  • Yu C, Pan K, Xing D, Liang G, Tan W, Zhang L and Lin D . (2002). Cancer Res., 62, 6430–6433.

  • Zambon CF, Basso D, Navaglia F, Falda A, Belluco C, Fogar P, Greco E, Gallo N, Farinati F, Cardin R, Rugge M, Di Mario F and Plebani M . (2004). Gastroenterology, 126, 382–384.

  • Zhang X, Su T, Zhang QY, Gu J, Caggana M, Li H and Ding X . (2002). J. Pharmacol. Exp. Ther., 302, 416–423.

  • Zhao H, Spitz MR, Gwyn KM and Wu X . (2002). Mol. Carcinogen., 33, 99–104.

  • Zhao H, Spitz MR, Tomlinson GE, Zhang H, Minna JD and Wu X . (2001). Cancer Res., 61, 7819–7824.

  • Zheng Y, Shen H, Sturgis EM, Wang LE, Eicher SA, Strom SS, Frazier ML, Spitz MR and Wei Q . (2001). Carcinogenesis, 22, 1195–1199.

  • Zhong S, Howie AF, Ketterer B, Taylor J, Hayes JD, Beckett GJ, Wathen CG, Wolf CR and Spurr NK . (1991). Carcinogenesis, 12, 1533–1537.

  • Zhou W, Liu G, Miller DP, Thurston SW, Xu LL, Wain JC, Lynch TJ, Su L and Christiani DC . (2002a). Cancer Res., 62, 1377–1381.

  • Zhou W, Liu G, Miller DP, Thurston SW, Xu LL, Wain JC, Lynch TJ, Su L and Christiani DC . (2003). Cancer Epidemiol. Biomarkers Prev., 12, 359–365.

  • Zhou W, Liu G, Thurston SW, Xu LL, Miller DP, Wain JC, Lynch TJ, Su L and Christiani DC . (2002b). Cancer Epidemiol. Biomarkers Prev., 11, 15–21.

  • Zhou W, Thurston SW, Liu G, Xu LL, Miller DP, Wain JC, Lynch TJ, Su L and Christiani DC . (2001). Cancer Epidemiol. Biomarkers Prev., 10, 461–466.

  • Zhu Y, Spitz MR, Amos CI, Lin J, Schabath MB and Wu X . (2004). Cancer Res., 64, 2251–2257.

  • Zhu Y, Spitz MR, Lei L, Mills GB and Wu X . (2001). Cancer Res., 61, 7825–7829.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xifeng Wu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wu, X., Zhao, H., Suk, R. et al. Genetic susceptibility to tobacco-related cancer. Oncogene 23, 6500–6523 (2004). https://doi.org/10.1038/sj.onc.1207811

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1207811

Keywords

This article is cited by

Search

Quick links