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Tumor suppressor genes on chromosome 3p involved in the pathogenesis of lung and other cancers

Abstract

Loss of heterozygosity (LOH) involving several chromosome 3p regions accompanied by chromosome 3p deletions are detected in almost 100% of small (SCLCs) and more than 90% of non-small (NSCLCs) cell lung cancers. In addition, these changes appear early in the pathogenesis of lung cancer and are found as clonal lesions in the smoking damaged respiratory epithelium including histologically normal epithelium as well as in epithelium showing histologic changes of preneoplasia. These 3p genetic alterations lead to the conclusion that the short arm of human chromosome 3 contains several tumor suppressor gene(s) (TSG(s)). Although the first data suggesting that 3p alterations were involved in lung carcinogenesis were published more than 10 years ago, only recently has significant progress been achieved in identifying the candidate TSGs and beginning to demonstrate their functional role in tumor pathogenesis. Some of the striking results of these findings has been the discovery of multiple 3p TSGs and the importance of tumor acquired promoter DNA methylation as an epigenetic mechanism for inactivating the expression of these genes in lung cancer. This progress, combined with the well known role of smoking as an environmental causative risk factor in lung cancer pathogenesis, is leading to the development of new diagnostic and therapeutic strategies which can be translated into the clinic to combat and prevent the lung cancer epidemic. It is clear now that genetic and epigenetic abnormalities of several genes residing in chromosome region 3p are important for the development of lung cancers but it is still obscure how many of them exist and which of the numerous candidate TSGs are the key players in lung cancer pathogenesis. We review herein our current knowledge and describe the most credible candidate genes.

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Abbreviations

AI:

allelic imbalance

aa:

amino acid

BPDE:

benzo[a]pyrene diol epoxide

CC-RCC:

clear cell renal cell carcinomas

CER1:

common eliminated region

FAR:

frequently affected with rearrangements region

LOH:

loss of heterozygosity

NSCLC:

non-small cell lung cancer

RA:

retinoic acid

SCLC:

small cell lung cancer

TSA:

trichostatin-A

TSG:

tumor suppressor gene

AZA:

5-aza-2′-deoxycytidine

CGH:

comparative genome hybridization

SNP:

single nucleotide polymorphism

FISH:

fluorescent in situ hybridization

References

  • Acevedo CM, Henríquez M, Emmert-Buck MR, Chuaqui RF . 2002 Cancer 94: 793–802

  • Adorjan P, Distler J, Lipscher E, Model F, Muller J, Pelet C, Braun A, Florl AR, Gutig D, Grabs G, Howe A, Kursar M, Lesche R, Leu E, Lewin A, Maier S, Muller V, Otto T, Scholz C, Schulz WA, Seifert HH, Schwope I, Ziebarth H, Berlin K, Piepenbrock C, Olek A . 2002 Nucleic Acids Res. 30: 1–9

  • Agathanggelou A, Honorio S, Macartney DP, Martinez A, Dallol A, Rader J, Fullwood P, Chauhan A, Walker R, Shaw JA, Hosoe S, Lerman MI, Minna JD, Maher ER, Latif F . 2001 Oncogene 20: 1509–1518

  • Agathanggelou A, Dallol A, Zochbauer-Müller S, Hesson L, Honorio S, Minna JD, Maher ER, Latif F . 2002 Proc. AACR 42: 614

  • Alimov A, Kost-Alimova M, Liu J, Li C, Bergerheim U, Imreh S, Klein G, Zabarovsky ER . 2000 Oncogene 19: 1392–1399

  • Angelborg G, Kundu A, Borgstrom P, Frost GI . 2002 Proc. AACR 42: (abstract 5519)

  • Angeloni D, Lerman MI . 2001 Human Lung cancer: Cancer-Causing Genes and Environmental Factors. Sourcebook on Asbestos Diseases Vol 23: Peters GA and Peters BJ (eds) Philadelphia: LexisNexis Press pp. 169–209

    Google Scholar 

  • Astuti D, Agathanggelou A, Honorio S, Dallol A, Martinsson T, Kogner P, Cummins C, Neumann HP, Voutilainen R, Dahia P, Eng C, Maher ER, Latif F . 2001 Oncogene 20: 7573–7577

  • Banham AH, Beasley N, Campo E, Fernandez PL, Fidler C, Gatter K, Jones M, Mason DY, Prime JE, Trougouboff P, Wood K, Cordell JL . 2001 Cancer Res. 61: 8820–8829

  • Bateman A, Birney E, Durbin R, Eddy SR, Finn RD, Sonnhammer EL . 1999 Nucleic. Acids. Res. 27: 260–262

  • Berard J, Laboune F, Mukuna M, Masse S, Kothary R, Bradley WE . 1996 FASEB J. 10: 1091–1097

  • Blaker H, Hofmann WJ, Rieker RJ, Penzel R, Graf M, Otto HF . 1999 Genes Chrom. Cancer 25: 399–402

  • Boldog F, Gemmill RM, West J, Robinson M, Robinson L, Li E, Roche J, Todd S, Waggoner B, Lundstrom R, Jacobson J, Mullokandov MR, Klinger H, Drabkin HA . 1997 Hum. Mol. Genet. 6: 193–203

  • Braga E, Pugacheva E, Basov I, Ermilova V, Kazubskaya T, Mazurenko N, Kisseljov F, Liu J, Garkavtseva R, Debabov V, Zabarovsky E, Kisselev L . 1999 FEBS letters 454: 215–219

  • Braga E, Sentchenko V, Bazov I, Loginov W, Liu J, Debabov V, Ermilova V, Kazubskaya T, Garkavtseva R, Mazurenko N, Kisseljov F, Lerman MI, Kisselev L, Zabarovsky E . 2002 Int. J. Cancer 100: 534–541

  • Brambilla E, Constantin B, Drabkin H, Roche J . 2000 Am. J. Pathol. 156: 939–950

  • Buchhagen DL, Qiu L, Etkind P . 1994 Int. J. Cancer 57: 473–479

  • Burbee DG, Forgacs E, Zochbauer-Muller S, Shivakumar L, Fong K, Gao B, Randle D, Kondo M, Virmani A, Bader S, Sekido Y, Latif F, Milchgrub S, Toyooka S, Gazdar AF, Lerman MI, Zabarovsky E, White M, Minna JD . 2001 J. Natl. Cancer Inst. 93: 691–699

  • Caballero OL, Cohen D, Liu Q, Esteller M, Bonacum J, White P, Engles J, Yochem R, Herman JG, Westra WH, Lengauer C, Sidransky D, Jen J . 2001 Genes Chrom. Cancer 32: 119–125

  • Chen LC, Matsumura K, Deng G, Kurisu W, Ljung BM, Lerman MI, Waldman FM, Smith HS . 1994 Cancer Res. 54: 3021–3024

  • Cheng Y, Poulos NE, Lung ML, Hampton G, Ou B, Lerman MI, Stanbridge EJ . 1998 Proc. Natl. Acad. Sci. USA 95: 3042–3047

  • Croce CM, Sozzi G, Huebner K . 1999 J. Clin. Oncol. 17: 1618–1624

  • Csoka AB, Frost GI, Stern R . 2001 Matrix Biol. 20: 499–508

  • Dahiya R, McCarville J, Hu W, Lee C, Chui RM, Kaur G, Deng G . 1997 Int. J. Cancer 71: 20–25

  • Daigo Y, Nishiwaki T, Kawasoe T, Tamari M, Tsuchiya E, Nakamura Y . 1999a Cancer Res. 59: 1966–1972

  • Daigo Y, Isomura M, Nishiwaki T, Tamari M, Ishikawa S, Kai M, Murata Y, Takeuchi K, Yamane Y, Hayashi R, Minami M, Fujino MA, Hojo Y, Uchiyama I, Takagi T, Nakamura Y . 1999b DNA Res. 6: 37–44

  • Dallol A, Forgacs E, Martinez A, Sekido Y, Walker R, Kishida T, Rabbitts P, Maher E, Minna J, Latif F . 2002 Oncogene 21: 3020–3028

  • Dalmau J, Graus F, Rosenblum MK, Posner JB . 1992 Medicine (Baltimore) 71: 59–72

  • Daly MC, Douglas JB, Bleehen NM, Hastleton P, Twentyman PR, Sundaresan V, Carritt B, Bergh J, Rabbitts PH . 1991 Genomics 9: 113–119

  • Daly MC, Xiang RH, Buchhagen D, Hensel CH, Garcia DK, Killary AM, Minna JD, Naylor SL . 1993 Oncogene 8: 1721–1729

  • Dammann R, Li C, Yoon JH, Chin PL, Bates S, Pfeifer GP . 2000 Nat. Genet. 25: 315–319

  • Dammann R, Yang G, Pfeifer GP . 2001 Cancer Res. 61: 3105–3109

  • De las Heras M, Barsky SH, Hasleton P, Wagner M, Larson E, Egan J, Ortin A, Gimenez-Mas JA, Palmarini M, Sharp JM . 2000 Eur. Respir. J. 16: 330–332

  • Drabkin HA, Mendez MJ, Rabbitts PH, Varkony T, Bergh J, Schlessinger J, Erickson P, Gemmill RM . 1992 Genes Chrom. Cancer 5: 67–74

  • Drabkin HA, West JD, Hotfilder M, Heng YM, Erickson P, Calvo R, Dalmau J, Gemmill RM, Sablitzky F . 1999 Oncogene 18: 2589–2597

  • Dreijerink K, Braga E, Kuzmin I, Geil L, Duh FM, Angeloni D, Zbar B, Lerman MI, Stanbridge EJ, Minna JD, Protopopov A, Li J, Kashuba V, Klein G, Zabarovsky ER . 2001 Proc. Natl. Acad. Sci. USA 98: 7504–7509

  • Drumheller T, McGillivray BC, Behrner D, MacLeod P, McFadden DE, Roberson J, Venditti C, Chorney K, Chorney M, Smith DI . 1996 J. Med. Genet. 33: 842–847

  • Dumon KR, Ishii H, Vecchione A, Trapasso F, Baldassarre G, Chakrani F, Druck T, Rosato EF, Williams NN, Baffa R, During MJ, Huebner K, Croce CM . 2001a Cancer Res. 61: 4827–4836

  • Dumon KR, Ishii H, Fong LY, Zanesi N, Fidanza V, Mancini R, Vecchione A, Baffa R, Trapasso F, During MJ, Huebner K, Croce CM . 2001b Proc. Natl. Acad. Sci. USA 98: 3346–3351

  • Edamatsu H, Kaziro Y, Itoh H . 2000 Genes Cells 5: 849–858

  • Esteller M, Sanchez-Cespedes M, Rosell R, Sidransky D, Baylin SB, Herman JG . 1999 Cancer Res. 59: 67–70

  • Esteller M, Corn PG, Baylin SB, Herman JG . 2001 Cancer Res. 61: 3225–3229

  • Fan X, Paetau A, Aalto Y, Valimaki M, Sane T, Poranen A, Castresana JS, Knuutila S . 2001 Cancer Genet. Cytogenet 128: 97–103

  • Fong KM, Biesterveld EJ, Virmani A, Wistuba I, Sekido Y, Bader SA, Ahmadian M, Ong ST, Rassool FV, Zimmerman PV, Giaccone G, Gazdar AF, Minna JD . 1997 Cancer Res. 57: 2256–2267

  • Fong LY, Fidanza V, Zanesi N, Lock LF, Siracusa LD, Mancini R, Siprashvili Z, Ottey M, Martin SE, Druck T, McCue PA, Croce CM, Huebner K . 2000 Proc. Natl. Acad. Sci. USA 97: 4742–4747

  • Frost GI, Mohapatra G, Wong TM, Csoka AB, Gray JW, Stern R . 2000 Oncogene 19: 870–877

  • Fujisawa H, Kitsukawa T . 1998 Curr. Opin. Neurobiol. 8: 587–592

  • Fullwood P, Marchini S, Rader JS, Martinez A, Macartney D, Broggini M, Morelli C, Barbanti-Brodano G, Maher ER, Latif F . 1999 Cancer Res. 59: 4662–4667

  • Ganly PS, Jarad N, Rudd RM, Rabbitts PH . 1992 Genomics 12: 221–228

  • Gao B, Sekido Y, Maximov A, Saad M, Forgacs E, Latif F, Wei MH, Lerman M, Lee JH, Perez-Reyes E, Bezprozvanny I, Minna JD . 2000 J. Biol. Chem. 275: 12237–12242

  • Garcia-Rostan G, Camp RL, Herrero A, Carcangiu ML, Rimm DL, Tallini G . 2001 Am. J. Pathol. 158: 987–996

  • Gemmill RM, West JD, Boldog F, Tanaka N, Robinson LJ, Smith DI, Li F, Drabkin HA . 1998 Proc. Natl. Acad. Sci. USA 95: 9572–9577

  • Geradts J, Chen JY, Russell EK, Yankaskas JR, Nieves L, Minna JD . 1993 Cell. Growth. Differ. 4: 799–809

  • Geradts J, Fong KM, Zimmerman PV, Maynard R, Minna JD . 1999 Clin. Cancer Res. 5: 791–800

  • Geradts J, Fong KM, Zimmerman PV, Minna JD . 2000 Br. J. Cancer 82: 1191–1197

  • Geurts JM, Schoenmakers EF, Roijer E, Stenman G, Van de Ven WJ . 1997 Cancer Res. 57: 13–17

  • Girard L, Zöchbauer-Muller S, Virmani AK, Gazdar AF, Minna JD . 2000 Cancer Res. 60: 4894–4906

  • Gnarra JR, Ward JM, Porter FD, Wagner JR, Devor DE, Grinberg A, Emmert-Buck MR, Westphal H, Klausner RD, Linehan WM . 1997 Proc. Natl. Acad. Sci. USA 9: 9102–9107

  • Graham S . 1984 J. Natl. Cancer Inst. 73: 1423–1428

  • Greenspan DL, Connolly DC, Wu R, Lei RY, Vogelstein JT, Kim YT, Mok JE, Munoz N, Bosch FX, Shah K, Cho KR . 1997 Cancer Res. 57: 4692–4698

  • Guo Z, Hu X, Afink G, Ponten F, Wilander E, Ponten J . 2000 Int. J. Cancer 86: 518–523

  • Gure AO, Altorki NK, Stockert E, Scanlan MJ, Old LJ, Chen YT . 1998 Cancer Res. 58: 1034–1041

  • Helland A, Kraggerud SM, Kristensen GB, Holm R, Abeler VM, Huebner K, Borresen-Dale AL, Lothe RA . 2000 Int. J. Cancer 88: 217–222

  • Heppell-Parton AC, Nacheva E, Carter NP, Bergh J, Ogilvie D, Rabbitts PH . 1999 Cancer Genet. Cytogenet 111: 105–110

  • Hirano A, Emi M, Tsuneizumi M, Utada Y, Yoshimoto M, Kasumi F, Akiyama F, Sakamoto G, Haga S, Kajiwara T, Nakamura Y . 2001 Clin. Cancer Res. 7: 876–882

  • Houle B, Rochette-Egly C, Bradley WE . 1993 Proc. Natl. Acad. Sci. USA 90: 985–989

  • Hu L-F, Eiriksdottir G, Lebedeva T, Kholodnyuk I, Alimov A, Chen F, Luo Y, Zabarovsky ER, Ingvarsson S, Klein G, Ernberg I . 1996 Genes Chrom. and Cancer 17: 118–126

  • Huebner K, Croce CM . 2001 Nature Rev. Cancer 1: 214–221

  • Ikeda T, Yoshinaga K, Semba S, Kondo E, Ohmori H, Horii A . 2000 Oncol. Rep. 7: 323–326

  • Imreh S, Kholodnyuk I, Allikmets R, Stanbridge EJ, Zabarovsky ER, Klein G . 1994 Genes Chrom. Cancer 11: 237–245

  • Ishii H, Dumon KR, Vecchione A, Trapasso F, Mimori K, Alder H, Mori M, Sozzi G, Baffa R, Huebner K, Croce CM . 2001 Cancer Res. 61: 1578–1584

  • Ishikawa S, Kai M, Tamari M, Takei Y, Takeuchi K, Bandou H, Yamane Y, Ogawa M, Nakamura Y . 1997 DNA Res. 4: 35–43

  • Ivanov S, Liao SY, Ivanova A, Danilkovitch-Miagkova A, Tarasova N, Weirich G, Merrill MJ, Proescholdt MA, Oldfield EH, Lee J, Zavada J, Waheed A, Sly W, Lerman MI, Stanbridge EJ . 2001 Am. J. Pathol. 158: 905–919

  • Jensen DE, Proctor M, Marquis ST, Gardner HP, Ha SI, Chodosh LA, Ishov AM, Tommerup N, Vissing H, Sekido Y, Minna J, Borodovsky A, Schultz DC, Wilkinson KD, Maul GG, Barlev N, Berger SL, Prendergast GC, Rauscher FJ . 1998 Oncogene 16: 1097–1112

  • Ji L, Fang B, Yen N, Fong K, Minna JD, Roth JA . 1999 Cancer Res. 59: 3333–3339

  • Ji L, Nishizaki M, Gao B, Burbee D, Kondo M, Kamibayashi C, Xu K, Atkinson EN, Fang B, Lerman MI, Roth JA, Minna JD . 2002 Cancer Res. 62: 2715–2720

  • Julicher K, Marquitan G, Werner N, Bardenheuer W, Vieten L, Brocker F, Topal H, Seeber S, Opalka B, Schutte J . 1999 J. Natl. Cancer Inst. 91: 1563–1568

  • Kashuba VI, Szeles A, Allikmets R, Bergerheim U, Modi W, Grafodatsky A, Dean M, Stanbridge EJ, Winberg G, Klein G, Zabarovsky ER . 1995 Cancer Genetics Cytogenet. 81: 144–150

  • Keith RL, Miller YE, Gemmill RM, Drabkin HA, Dempsey EC, Kennedy TC, Prindiville S, Franklin WA . 2000 Clin. Cancer Res. 6: 1616–1625

  • Kholodnyuk ID, Kost-Alimova M, Kashuba VI, Gizatullin RZ, Stanbridge E, Szeles A, Zabarovsky ER, Klein G, Imreh S . 1997 Genes Chrom. Cancer 18: 200–211

  • Kidd T, Brose K, Mitchell KJ, Fetter RD, Tessier-Lavigne M, Goodman CS, Tear G . 1998 Cell 92: 205–215

  • Killary AM, Wolf ME, Giambernardi TA, Naylor SL . 1992 Proc. Natl. Acad. Sci USA 89: 10877–10881

  • Kim ST, Lim DS, Canman CE, Kastan MB . 1999 J. Biol. Chem. 274: 37538–37543

  • Kiss H, Yang Y, Kiss C, Andersson K, Klein G, Imreh S, Dumanski JP . 2002 Eur. J. Hum. Genet. 10: 52–61

  • Knudson AG . 1995 Adv. Cancer Res. 67: 1–23

  • Kok K, Naylor SL, Buys CH . 1997 Adv. Cancer Res. 71: 27–92

  • Kondo M, Ji L, Kamibayashi C, Tomizawa Y, Randle D, Sekido Y, Yokota J, Kashuba V, Zabarovsky E, Kuzmin I, Lerman M, Roth J, Minna JD . 2001 Oncogene 20: 6258–6262

  • Kosaki R, Watanabe K, Yamaguchi Y . 1999 Cancer Res. 59: 1141–1145

  • Kuzmin I, Gillespie JW, Protopopov A, Geil L, Dreijerink K, Yang Y, Vocke CD, Duh F-M, Zabarovsky E, Rhim JS, Emmert-Buck MR, Linehan WM, Minna JD, Lerman ML . 2002 Cancer Res. 62: 3498–3502

  • Latif F, Tory K, Modi WS, Graziano SL, Gamble G, Douglas J, Heppell-Parton AC, Rabbitts PH, Zbar B, Lerman MI . 1992 Genes Chrom. Cancer 5: 119–127

  • Latif F, Tory K, Gnarra J, Yao M, Duh F-M, Orcutt ML, Stackhouse T, Kuzmin I, Modi W, Geil L, Schmidt L, Zhou F, Li H, Wei MH, Chen F, Glenn G, Choyke P, Walther MM, Weng Y, Duan D-SR, Dean M, Glavac D, Richards FM, Crossey PA, Ferguson-Smith MA, Le Paslier D, Chumakov I, Cohen D, Chinault AC, Maher ER, Linehan WM, Zbar B, Lerman ML . 1993 Science 260: 1317–1320

  • Le Beau MM, Drabkin H, Glover TW, Gemmill R, Rassool FV, McKeithan TW, Smith DI . 1998 Genes Chrom. Cancer 21: 281–289

  • Lee MG, Kim HY, Byun DS, Lee SJ, Lee CH, Kim JI, Chang SG, Chi SG . 2001 Cancer Res. 61: 6688–6692

  • Lepperdinger G, Strobl B, Kreil G . 1998 J. Biol. Chem. 273: 22466–22470

  • Lerman MI, Minna JD . The International Lung Cancer Chromosome 3p21.3 Tumor Suppressor Gene Consortium 2000 Cancer Res. 60: 6116–6133

    CAS  PubMed  Google Scholar 

  • Li J, Protopopov A, Wang F, Sentchenko V, Petushkov V, Vorontsova O, Petrenko L, Zabarovska V, Muravenko O, Braga E, Kisselev L, Lerman MI, Kashuba V, Klein G, Ernberg I, Wahlestedt C, Zabarovsky ER . 2002 Proc. Natl. Acad. Sci. USA 9: 10724–10729

  • Lindblad-Toh K, Tanenbaum DM, Daly MJ, Winchester E, Lui WO, Villapakkam A, Stanton SE, Larsson C, Hudson TJ, Johnson BE, Lander ES, Meyerson M . 2000 Nat. Biotechnol. 18: 1001–1005

  • Liu J, Zabarovska V, Braga E, Alimov A, Klein G, Zabarovsky ER . 1999 FEBS Letters 462: 121–128

  • Liu N, Gao F, Han Z, Xu X, Underhill CB, Zhang L . 2001 Cancer Res. 61: 5207–5214

  • Lo KW, Kwong J, Hui AB, Chan SY, To KF, Chan AS, Chow LS, Teo PM, Johnson PJ, Huang DP . 2001 Cancer Res. 61: 3877–3881

  • Lotan R . 1980 Biochim. Biophys. Acta. 605: 33–91

  • Lott ST, Lovell M, Naylor SL, Killary AM . 1998 Cancer Res. 58: 3533–3537

  • Lounis H, Mes-Masson AM, Dion F, Bradley WE, Seymour RJ, Provencher D, Tonin PN . 1998 Oncogene 17: 2359–2365

  • Lovell M, Lott ST, Wong P, El-Naggar A, Tucker S, Killary AM . 1999 Cancer Res. 59: 2182–2189

  • Maitra A, Wistuba II, Washington C, Virmani AK, Ashfaq R, Milchgrub S, Gazdar AF, Minna JD . 2001 Am. J. Pathol. 159: 119–130

  • Manning AP, Mes-Masson AM, Seymour RJ, Tetrault M, Provencher DM, Tonin PN . 1999 Mol. Carcinog. 24: 218–225

  • Maruyama R, Toyooka S, Toyooka KO, Harada K, Virmani AK, Zochbauer-Muller S, Farinas AJ, Vakar-Lopez F, Minna JD, Sagalowsky A, Czerniak B, Gazdar AF . 2001 Cancer Res. 61: 8659–8663

  • Maruyama R, Toyooka S, Toyooka KO, Virmani AK, Zochbauer-Muller S, Farinas AJ, Minna JD, McConnell J, Frenkel EP, Gazdar AF . 2002 Clin. Cancer Res. 8: 514–519

  • Matsumoto S, Kasumi F, Sakamoto G, Onda M, Nakamura Y, Emi M . 1997 Genes Chrom. Cancer 20: 268–274

  • Matsumoto S, Minobe K, Utada Y, Furukawa K, Onda M, Sakamoto G, Kasumi F, Nakamura Y, Emi M . 2000 Cancer Lett. 152: 63–69

  • Mirabelli-Primdahl L, Gryfe R, Kim H, Millar A, Luceri C, Dale D, Holowaty E, Bapat B, Gallinger S, Redston M . 1999 Cancer Res. 59: 3346–3351

  • Morrissey C, Martinez A, Zatyka M, Agathanggelou A, Honorio S, Astuti D, Morgan NV, Moch H, Richards FM, Kishida T, Yao M, Schraml P, Latif F, Maher ER . 2001 Cancer Res. 61: 7277–7281

  • Muller CY, O'Boyle JD, Fong KM, Wistuba II, Biesterveld E, Ahmadian M, Miller DS, Gazdar AF, Minna JD . 1998 J. Natl. Cancer Inst. 90: 433–439

  • Murata Y, Tamari M, Takahashi T, Horio Y, Hibi K, Yokoyama S, Inazawa J, Yamakawa K, Ogawa A, Takahashi T, Nakamura Y . 1994 Hum. Mol. Genet. 3: 1341–1344

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

  • Orikasa K, Orikasa S, Horii A . 1998 Cancer Genet. Cytogenet. 104: 104–110

  • Ortiz-Vega S, Khokhlatchev A, Nedwidek M, Zhang Xf X, Dammann R, Pfeifer GP, Avruch J . 2002 Oncogene 21: 1381–1390

  • Otterson GA, Xiao GH, Geradts J, Jin F, Chen WD, Niklinska W, Kaye FJ, Yeung RS . 1998 J. Natl. Cancer Inst. 90: 426–432

  • Palmarini M, Sharp JM, de las Heras M, Fan H . 1999 J. Virol. 73: 6964–6972

  • Palmisano WA, Divine KK, Saccomanno G, Gilliland FD, Baylin SB, Herman JG, Belinsky SA . 2000 Cancer Res. 60: 5954–5958

  • Pandis N, Jin Y, Limon J, Bardi G, Idvall I, Mandahl N, Mitelman F, Heim S . 1993 Genes Chrom. Cancer 6: 151–155

  • Pifarre A, Rosell R, Monzo M, De Anta JM, Moreno I, Sanchez JJ, Ariza A, Mate JL, Martinez E, Sanchez M . 1997 Br. J. Cancer 75: 184–189

  • Pinkel D, Segraves R, Sudar D, Clark S, Poole I, Kowbel D, Collins C, Kuo WL, Chen C, Zhai Y, Dairkee SH, Ljung BM, Gray JW, Albertson DG . 1998 Nat. Genet. 20: 207–211

  • Protopopov AI, Li J, Winberg G, Gizatullin RZ, Kashuba VI, Klein G, Zabarovsky ER . 2002 J. Gene Medicine 4: 397–406

  • Rabbitts P, Bergh J, Douglas J, Collins F, Waters J . 1990 Genes Chrom. Cancer 2: 231–238

  • Rai SK, Duh FM, Vigdorovich V, Danilkovitch-Miagkova A, Lerman MI, Miller AD . 2001 Proc. Natl. Acad. Sci. USA 98: 4443–4448

  • Rimessi P, Gualandi F, Morelli C, Trabanelli C, Wu Q, Possati L, Montesi M, Barrett JC, Barbanti-Brodano G . 1994 Oncogene 9: 3467–3474

  • Roche J, Boldog F, Robinson M, Robinson L, Varella-Garcia M, Swanton M, Waggoner B, Fishel R, Franklin W, Gemmill R, Drabkin H . 1996 Oncogene 12: 1289–1297

  • Roche J, Nasarre P, Rouhaud L, Castellani V, Raymond G, Drabkin H, Constantin B . 2002 Proc. AACR 43: (abstract 115)

  • Roz L, Gramegna M, Ishii H, Croce CM, Sozzi G . 2002 Proc. Natl. Acad. Sci. USA 99: 3615–3620

  • Sanchez Y, el-Naggar A, Pathak S, Killary AM . 1994 Proc. Natl. Acad. Sci. USA 91: 3383–3387

  • Sard L, Accornero P, Tornielli S, Delia D, Bunone G, Campiglio M, Colombo MP, Gramegna M, Croce CM, Pierotti MA, Sozzi G . 1999 Proc. Natl. Acad. Sci. USA 96: 8489–8492

  • Sato M, Sakurada A, Sagawa M, Endo C, Tanita T, Kondo T, Tsuchiya E, Fujimura S, Horii A . 1998 Genes Chrom. Cancer 23: 367–370

  • Schlosshauer PW, Pirog EC, Levine RL, Ellenson LH . 2000 Mod. Pathol. 13: 1066–1071

  • Sekido Y, Bader S, Latif F, Gnarra JR, Gazdar AF, Linehan WM, Zbar B, Lerman MI, Minna JD . 1994 Oncogene 9: 1599–1604

  • Sekido Y, Bader S, Latif F, Chen JY, Duh FM, Wei MH, Albanesi JP, Lee CC, Lerman MI, Minna JD . 1996 Proc. Natl. Acad. Sci. USA 93: 4120–4125

  • Sekido Y, Ahmadian M, Wistuba II, Latif F, Bader S, Wei MH, Duh FM, Gazdar AF, Lerman MI, Minna JD . 1998 Oncogene 16: 3151–3157

  • Semenza GL . 2002 Trends. Mol. Med. 8: Suppl S62–S67

  • Shigemitsu K, Sekido Y, Usami N, Mori S, Sato M, Horio Y, Hasegawa Y, Bader SA, Gazdar AF, Minna JD, Hida T, Yoshioka H, Imaizumi M, Ueda Y, Takahashi M, Shimokata K . 2001 Oncogene 20: 4249–4257

  • Shivakumar L, Minna JD, Sakamaki T, Pestell RG, White MA . 2002 Mol. Cell. Biol. 22: 4309–4318

  • Shridhar R, Shridhar V, Rivard S, Siegfried JM, Pietraszkiewicz H, Ensley J, Pauley R, Grignon D, Sakr W, Miller OJ, Smith DI . 1996a Cancer Res. 56: 5576–5578

  • Shridhar V, Rivard S, Shridhar R, Mullins C, Bostick L, Sakr W, Grignon D, Miller OJ, Smith DI . 1996b Oncogene 12: 1931–1939

  • Shridhar V, Rivard S, Wang X, Shridhar R, Paisley C, Mullins C, Beirnat L, Dugan M, Sarkar F, Miller OJ, Vaitkevicius VK, Smith DI . 1997 Oncogene 14: 2213–2216

  • Siprashvili Z, Sozzi G, Barnes LD, McCue P, Robinson AK, Eryomin V, Sard L, Tagliabue E, Greco A, Fusetti L, Schwartz G, Pierotti MA, Croce CM, Huebner K . 1997 Proc. Natl. Acad. Sci. USA 94: 13771–13776

  • Sozzi G, Veronese ML, Negrini M, Baffa R, Cotticelli MG, Inoue H, Tornielli S, Pilotti S, DeGregorio L, Pastorino U, Pierotti MA, Ohta M, Huebner K, Croce CM . 1996 Cell 85: 17–26

  • Sozzi G, Tornielli S, Tagliabue E, Sard L, Pezzella F, Pastorino U, Minoletti F, Pilotti S, Ratcliffe C, Veronese ML, Goldstraw P, Huebner K, Croce CM, Pierotti MA . 1997 Cancer Res. 57: 5207–5212

  • Sozzi G, Pastorino U, Moiraghi L, Tagliabue E, Pezzella F, Ghirelli C, Tornielli S, Sard L, Huebner K, Pierotti MA, Croce CM, Pilotti S . 1998 Cancer Res. 58: 5032–5037

  • Su TH, Chang JG, Perng LI, Chang CP, Wei HJ, Wang NM, Tsai CH . 2000 Gynecol. Oncol. 76: 193–199

  • Sundaresan V, Heppell-Parton A, Coleman N, Miozzo M, Sozzi G, Ball R, Cary N, Hasleton P, Fowler W, Rabbitts P . 1995 Ann. Oncol. 6: Suppl 1 S27–S31

  • Sundaresan V, Chung G, Heppell-Parton A, Xiong J, Grundy C, Roberts I, James L, Cahn A, Bench A, Douglas J, Minna J, Sekido Y, Lerman M, Latif F, Bergh J, Li H, Lowe N, Ogilvie D, Rabbitts P . 1998a Oncogene 17: 1723–1729

  • Sundaresan V, Roberts I, Bateman A, Bankier A, Sheppard M, Hobbs C, Xiong J, Minna J, Latif F, Lerman M, Rabbitts P . 1998b Mol. Cell. Neurosci. 11: 29–35

  • Sutherland LC, Edwards SE, Cable HC, Poirier GG, Miller BA, Cooper CS, Williams GT . 2000 Oncogene 19: 3774–3781

  • Sutherland LC, Lerman M, Williams GT, Miller BA . 2001 Oncogene 20: 2713–2719

  • Szeles A, Yang Y, Sandlund A, Kholodnyuk I, Kiss H, Kost-Alimova M, Zabarovsky ER, Stanbridge E, Klein G, Imreh S . 1997 Genes Chromos. Cancer 20: 329–336

  • Tanaka H, Shimada Y, Harada H, Shinoda M, Hatooka S, Imamura M, Ishizaki K . 1998 Cancer Res. 58: 3429–3434

  • Thiagalingam S, Lisitsyn NA, Hamaguchi M, Wigler MH, Willson JK, Markowitz SD, Leach FS, Kinzler KW, Vogelstein B . 1996 Cancer Res. 56: 2936–2939

  • Timmer T, Terpstra P, van den Berg A, Veldhuis PM, Ter Elst A, Voutsinas G, Hulsbeek MM, Draaijers TG, Looman MW, Kok K, Naylor SL, Buys CH . 1999 Eur. J. Hum. Genet. 7: 478–486

  • Todd S, Franklin WA, Varella-Garcia M, Kennedy T, Hilliker Jr CE, Hahner L, Anderson M, Wiest JS, Drabkin HA, Gemmill RM . 1997 Cancer Res. 57: 1344–1352

  • Todd MC, Xiang RH, Garcia DK, Kerbacher KE, Moore SL, Hensel CH, Liu P, Siciliano MJ, Kok K, van den Berg A, Veldhuis P, Buys CH, Killary AM, Naylor SL . 1996 Oncogene 13: 2387–2396

  • Tomizawa Y, Sekido Y, Kondo M, Gao B, Yokota J, Roche J, Drabkin H, Lerman MI, Gazdar AF, Minna JD . 2001 Proc. Natl. Acad. Sci. USA 98: 13954–13959

  • Toulouse A, Morin J, Dion PA, Houle B, Bradley WE . 2000 Lung Cancer 28: 127–137

  • Toyooka S, Ouchida M, Jitsumori Y, Tsukuda K, Sakai A, Nakamura A, Shimizu N, Shimizu K . 2000 Biochem. Biophys. Res. Commun. 278: 671–678

  • Toyooka KO, Toyooka S, Virmani AK, Sathyanarayana UG, Euhus DM, Gilcrease M, Minna JD, Gazdar AF . 2001 Cancer Res. 61: 4556–4560

  • Triggs-Raine B, Salo TJ, Zhang H, Wicklow BA, Natowicz MR . 1999 Proc. Natl. Acad. Sci. USA 96: 6296–6300

  • Trusolino L, Comoglio PM . 2002 Nature Rev. Cancer 2: 289–300

  • Tse C, Xiang RH, Bracht T, Naylor SL . 2002 Cancer Res. 62: 542–546

  • Tseng JE, Kemp BL, Khuri FR, Kurie JM, Lee JS, Zhou X, Liu D, Hong WK, Mao L . 1999 Cancer Res. 59: 4798–4803

  • Tschentscher F, Prescher G, Horsman DE, White VA, Rieder H, Anastassiou G, Schilling H, Bornfeld N, Bartz-Schmidt KU, Horsthemke B, Lohmann DR, Zeschnigk M . 2001 Cancer Res. 61: 3439–3442

  • Uzawa N, Yoshida MA, Hosoe S, Oshimura M, Amagasa T, Ikeuchi T . 1998 Cancer Genet. Cytogenet. 107: 125–131

  • van den Berg A, Draaijers TG, Kok K, Timmer T, Van der Veen AY, Veldhuis PM, de Leij L, Gerhartz CD, Naylor SL, Smith DI, Buys CH . 1997 Genes Chrom. Cancer 19: 220–227

  • Vavvas D, Li X, Avruch J, Zhang XF . 1998 J. Biol. Chem. 273: 5439–5442

  • Vieten L, Belair CD, Savelieva L, Julicher K, Brocker F, Bardenheuer W, Schutte J, Opalka B, Reznikoff CA . 1998 Genes. Chrom. Cancer 21: 39–48

  • Virmani AK, Rathi A, Zochbauer-Muller S, Sacchi N, Fukuyama Y, Bryant D, Maitra A, Heda S, Fong KM, Thunnissen F, Minna JD, Gazdar AF . 2000 J. Natl. Cancer Inst. 92: 1303–1307

  • Virmani AK, Muller C, Rathi A, Zoechbauer-Mueller S, Mathis M, Gazdar AF . 2001 Clin. Cancer Res. 7: 584–589

  • Virmani AK, Tsou JA, Siegmund KD, Shen LY, Long TI, Laird PW, Gazdar AF, Laird-Offringa IA . 2002 Cancer Epidemiol. Biomarkers Prev. 11: 291–297

  • Vos MD, Ellis CA, Bell A, Birrer MJ, Clark GJ . 2000 J. Biol. Chem. 275: 35669–35672

  • Waber PG, Lee NK, Nisen PD . 1996 Oncogene 12: 365–369

  • Wang L, Darling J, Zhang JS, Qian CP, Hartmann L, Conover C, Jenkins R, Smith DI . 1998 Oncogene 16: 635–642

  • Wang L, Darling J, Zhang JS, Liu W, Qian J, Bostwick D, Hartmann L, Jenkins R, Bardenhauer W, Schutte J, Opalka B, Smith DI . 2000 Genes Chrom. Cancer 27: 1–10

  • Wei M-H, Latif F, Bader F, Kashuba V, Chen J-J, Duh F-M, Sekido Y, Lee C-C, Geil L, Kuzmin I, Zabarovsky E, Klein G, Zbar B, Minna JD, Lerman MI . 1996 Cancer Res. 56: 1487–1492

  • Werner NS, Siprashvili Z, Fong LY, Marquitan G, Schroder JK, Bardenheuer W, Seeber S, Huebner K, Schutte J, Opalka B . 2000 Cancer Res. 60: 2780–2785

  • Wistuba II, Montellano FD, Milchgrub S, Virmani AK, Behrens C, Chen H, Ahmadian M, Nowak JA, Muller C, Minna JD, Gazdar AF . 1997 Cancer Res. 57: 3154–3158

  • 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, Gazdar AF, Minna JD . 2001 Semin. Oncol. 28: 3–13

  • Wu X, Zhao Y, Honn SE, Tomlinson GE, Minna JD, Hong WK, Spitz MR . 1998 Cancer Res. 58: 1605–1608

  • Wu R, Connolly DC, Dunn RL, Cho KR . 2000 J. Natl. Cancer Inst. 92: 338–344

  • Xian J, Clark KJ, Fordham R, Pannell R, Rabbitts TH, Rabbitts PH . 2001 Proc. Natl. Acad. Sci. USA 98: 15062–15066

  • Xiang RH, Hensel CH, Garcia DK, Carlson HC, Kok K, Daly MC, Kerbacher K, van den Berg A, Veldhuis P, Buys CH, Naylor SL . 1996 Genomics 32: 39–48

  • Xiang R, Davalos AR, Hensel CH, Zhou XJ, Tse C, Naylor SL . 2002 Cancer Res. 62: 2637–2643

  • Yamato T, Orikasa K, Fukushige S, Orikasa S, Horii A . 1999 Cytogenet. Cell Genet. 87: 291–295

  • Yang Y, Kost-Alimova M, Ingvarsson S, Qianhui Q, Kiss H, Szeles A, Kholodnyuk I, Cuthbert A, Klein G, Imreh S . 2001a Proc. Natl. Acad. Sci. USA 98: 1136–1141

  • Yang Q, Mori I, Shan L, Nakamura M, Nakamura Y, Utsunomiya H, Yoshimura G, Suzuma T, Tamaki T, Umemura T, Sakurai T, Kakudo K . 2001b Am. J. Pathol. 158: 299–303

  • Yang Q, Sakurai T, Yoshimura G, Mori I, Nakamura M, Nakamura Y, Suzuma T, Tamaki T, Umemura T, Kakudo K . 2001c Anticancer Res. 21: 1829–1833

  • Zanesi N, Fidanza V, Fong LY, Mancini R, Druck T, Valtieri M, Rudiger T, McCue PA, Croce CM, Huebner K . 2001 Proc. Natl. Acad. Sci. USA 98: 10250–10255

  • Zhang L, Underhill CB, Chen L . 1995 Cancer Res. 55: 428–433

  • Zochbauer-Muller S, Fong KM, Virmani AK, Geradts J, Gazdar AF, Minna JD . 2001a Cancer Res. 61: 249–255

  • Zochbauer-Muller S, Fong KM, Maitra A, Lam S, Geradts J, Ashfaq R, Virmani AK, Milchgrub S, Gazdar AF, Minna JD . 2001b Cancer Res.

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Acknowledgements

We thank the many collaborators that made up the 3p lung cancer tumor suppressor gene consortium, particularly Yoshitaka Sekido and Farida Latif for all of their hard work in the initial identification of the 3p21.3 genes. The membership of the consortium includes: University of Texas Southwestern Medical Center at Dallas, and MD Anderson Cancer Center, Houston, USA Group: Yoshitaka Sekido, Scott Bader, David Burbee, Kwun Fong, Eva Forgacs, Boning Gao, Harold Garner, Adi F Gazdar, Luc Girard, Craig Kamibayashi, Masashi Kondo, Ashwini Pande, Vivek Ramalingam, Dwight Randle, Yoshio Tomizawa, Arvind Virmani, Ivan Wistuba and John D Minna (Dallas), and Lin Ji, Bingling Fang, Neely Atkinson, and Jack A Roth (Houston). University of Birmingham, UK Group: Donia Macartney, Sofia Honorio, Eamonn Maher and Farida Latif. The Karolinska Institute, Sweden, Group: Eleonora Braga, Vladimir Kashuba, Alexei Protopopov, Vera Senchenko, Jingfeng Li, Fuli Wang, Veronika Zabarovska, George Klein, and Eugene R Zabarovsky. NCI, USA Group: (1) Fuh-Mei Duh, Ming-Hui Wei, Laura Geil, Igor Kuzmin, Sergei Ivanov, Intramural Research Support Program, SAIC Frederick, and Laboratory of Immunobiology, National Cancer Institute, Frederick Cancer Research and Development Center, Frederick, MD 21702; (2) Debora Angeloni, Alla Ivanova, Bert Zbar, Michael I Lerman, Laboratory of Immunobiology, National Cancer Institute, Frederick Cancer Research and Development Center, Frederick, MD 21702; (3): Bruce E Johnson, Medicine Branch at the National Naval Medical Center, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892. ER Zabarovsky was supported by research grants from the Swedish Cancer Society, the Swedish Research Council, STINT, Pharmacia Corporation and Karolinska Institute. JD Minna was supported by Lung Cancer SPORE P50 CA70907, and CA71618.

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Zabarovsky, E., Lerman, M. & Minna, J. Tumor suppressor genes on chromosome 3p involved in the pathogenesis of lung and other cancers. Oncogene 21, 6915–6935 (2002). https://doi.org/10.1038/sj.onc.1205835

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