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Japanese Journal of Cancer Research : Gann logoLink to Japanese Journal of Cancer Research : Gann
. 2000 Nov;91(11):1126–1133. doi: 10.1111/j.1349-7006.2000.tb00895.x

Nonrandom Chromosomal Imbalances in Esophageal Squamous Cell Carcinoma Cell Lines: Possible Involvement of the ATF3 and CENPF Genes in the 1q32 Amplicon

Atiphan Pimkhaokham 1,2, Yutaka Shimada 3, Yohji Fukuda 1, Naoki Kurihara 1, Issei Imoto 1, Zeng‐Quan Yang 1, Masayuki Imamura 3, Yusuke Nakamura 4, Teruo Amagasa 2, Johji Inazawa 1,✉
PMCID: PMC5926289  PMID: 11092977

Abstract

Using comparative genomic hybridization (CGH), we investigated copy number aberrations in 29 esophageal squamous cell carcinoma (ESC) cell lines. All lines displayed numerous chromosome imbalances. The most frequent losses were observed on chromosome 18q (65.5%), Xp (48.3%), 3p (44.8%), 4q (44.8%), 8p (41.4%), 11q23–25 (34.5%) and 4p (27.6%), whereas the most common copy number gains were noted at 8q (86.2%), 3q (82.8%), 5p (69%), 7p (69%), 20q (65.5%), 9q (55.2%), 11q (55.2%), 1q (48.3%), Xq (44.8%) and 18p (37.9%). High‐level gains (HLGs) were detected at 3q26 (9 cases), 8q23 (6 cases), 5p14–15 (6 cases), 18p11.2–11.3 (6 cases), 3q27–28 (5 cases), 5p13 (3 cases), 7p14–15 (3 cases), 20q12–13 (3 cases), 11q13 (3 cases), 14q21 (2 cases), 20p11.2 (2 cases), 13q32 (2 case), and 1q32 (1 case). Among them, HLGs of 1q32 have been reported in other types of cancer, including glioblastoma and breast cancers. We successfully narrowed down the smallest common amplicon involving 1q‐gain to the genomic segment between D1S414 and D1S2860 by fluorescence in situ hybridization (FISH). Southern and northern blot analysis clearly demonstrated that ATF3, human activating transcription factor‐3 and CENPF, centromere protein F, mapped within this region, were significantly amplified and over‐expressed in 1q32 amplicon.

Keywords: Esophageal squamous cell carcinoma (ESC), Comparative genomic hybridization (CGH), Amplicon map, Human activating transcription factor 3 (ATF3), Centromere protein F (CENPF)

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REFERENCES

  • 1. ) Pisani , P. , Parkin , D. M. , Bray , F. and Ferlay , J.Estimates of the worldwide mortality from 25 cancers in (1990) . Int. J. Cancer , 83 , 18 – 29 ( 1999. ). [DOI] [PubMed] [Google Scholar]
  • 2. ) Annual Statistical Report of National Health Conditions, Japanese Health and Welfare Statistics Association . J. Health Welfare Stat. , 10 – 15 ( 1999. ).
  • 3. ) Parkin , D. M. , Pisani , P. and Ferlay , J.Estimates of the worldwide incidence of 25 major cancers in (1990) . Int. J. Cancer , 80 , 827 – 841 ( 1999. ). [DOI] [PubMed] [Google Scholar]
  • 4. ) Morita , M. , Kuwano , H. , Ohno , S. , Sugimachi , K. , Seo , Y. , Tomoda , H. , Furusawa , M. and Nakashima , T.Multiple occurrence of carcinoma in the upper aerodigestive tract associated with esophageal cancer: reference to smoking, drinking and family history . Int. J. Cancer , 58 , 207 – 210 ( 1994. ). [DOI] [PubMed] [Google Scholar]
  • 5. ) Ahsan , H. , Neugut , A. I. and Gammon , M. D.Association of adenocarcinoma and squamous cell carcinoma of the esophagus with tobacco‐related and other malignancies . Cancer Epidemiol. Biomarkers Prev. , 6 , 779 – 782 ( 1997. ). [PubMed] [Google Scholar]
  • 6. ) Lengauer , C. , Kinzler , K. W. and Vogelstein , B.Genetic instabilities in human cancers . Nature , 396 , 643 – 649 ( 1998. ). [DOI] [PubMed] [Google Scholar]
  • 7. ) Vogelstein , B. and Kinzler , K. W.The multistep nature of cancer . Trends Genet. , 9 , 138 – 141 ( 1993. ). [DOI] [PubMed] [Google Scholar]
  • 8. ) Rooney , P. H. , Murray , G. I. , Stevenson , D. A. , Haites , N. E. , Cassidy , J. and McLeod , H. L.Comparative genomic hybridization and chromosomal instability in solid tumours . Br. J. Cancer , 80 , 862 – 873 ( 1999. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9. ) Lu , S. H. , Hsieh , L. L. , Luo , F. C. and Weinstein , I. B.Amplification of the EGF receptor and c‐myc genes in human esophageal cancers . Int. J. Cancer , 42 , 502 – 505 ( 1988. ). [DOI] [PubMed] [Google Scholar]
  • 10. ) Jiang , W. , Kahn , S. M. , Tomita , N. , Zhang , Y. J. , Lu , S. H. and Weinstein , I. B.Amplification and expression of the human cyclin D gene in esophageal cancer . Cancer Res. , 52 , 2980 – 2983 ( 1992. ). [PubMed] [Google Scholar]
  • 11. ) Meltzer , S. J.The molecular biology of esophageal carcinoma . Recent Results Cancer Res. , 142 , 1 – 8 ( 1996. ). [DOI] [PubMed] [Google Scholar]
  • 12. ) Montesano , R. , Hollstein , M. and Hainaut , P.Genetic alterations in esophageal cancer and their relevance to etiology and pathogenesis: a review . Int. J. Cancer , 69 , 225 – 235 ( 1996. ). [DOI] [PubMed] [Google Scholar]
  • 13. ) Kallioniemi , A. , Kallioniemi , O. P. , Sudar , D. , Rutovitz , D. , Gray , J. W. , Waldman , F. and Pinkel , D.Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors . Science , 258 , 818 – 821 ( 1992. ). [DOI] [PubMed] [Google Scholar]
  • 14. ) du Manoir , S. , Speicher , M. R. , Joos , S. , Schröck , E. , Popp , S. , Döhner , H. , Kovacs , G. , Robert‐Nicoud , M. , Lichter , P. and Cremer , T.Detection of complete and partial chromosome gains and losses by comparative genomic in situ hybridization . Hum. Genet. , 90 , 590 – 610 ( 1993. ). [DOI] [PubMed] [Google Scholar]
  • 15. ) Joos , S. , Scherthan , H. , Speicher , M. R. , Schlegel , J. , Cremer , T. and Lichter , P.Detection of amplified DNA sequences by reverse chromosome painting using genomic tumor DNA as probe . Hum. Genet. , 90 , 584 – 589 ( 1993. ). [DOI] [PubMed] [Google Scholar]
  • 16. ) Shimada , Y. , Imamura , M. , Wagata , T. , Yamaguchi , N. and Tobe , T.Characterization of 21 newly established esophageal cancer cell lines [published erratum appears in Cancer 1992; 70: 206] . Cancer , 69 , 277 – 284 ( 1992. ). [DOI] [PubMed] [Google Scholar]
  • 17. ) Ariyama , Y. , Sakabe , T. , Shinomiya , T. , Mori , T. , Fukuda , Y. and Inazawa , J.Identification of amplified DNA sequences on double minute chromosomes in a leukemic cell line KY821 by means of spectral karyotyping and comparative genomic hybridization . J. Hum. Genet. , 43 , 187 – 190 ( 1998. ). [DOI] [PubMed] [Google Scholar]
  • 18. ) Shinomiya , T. , Mori , T. , Ariyama , Y. , Sakabe , T. , Fukuda , Y. , Murakami , Y. , Nakamura , Y. and Inazawa , J.Comparative genomic hybridization of squamous cell carcinoma of the esophagus: the possible involvement of the DPI gene in the 13q34 amplicon . Genes Chromosom. Cancer , 24 , 337 – 344 ( 1999. ). [PubMed] [Google Scholar]
  • 19. ) Sakakura , C. , Mori , T. , Sakabe , T. , Ariyama , Y. , Shinomiya , T. , Date , K. , Hagiwara , A. , Yamaguchi , T. , Takahashi , T. , Nakamura , Y. , Abe , T. and Inazawa , J.Gains, losses and amplifications of genomic materials in primary gastric cancers analyzed by comparative genomic hybridization . Genes Chromosom. Cancer , 24 , 299 – 305 ( 1999. ). [DOI] [PubMed] [Google Scholar]
  • 20. ) Almeida , A. , Zhu , X. X. , Vogt , N. , Tyagi , R. , Muleris , M. , Dutrillaux , A. M. , Dutrillaux , B. , Ross , D. , Malfoy , B. and Hanash , S.GAC1, a new member of the leucine‐rich repeat superfamily on chromosome band 1q32.1, is amplified and overexpressed in malignant gliomas . Oncogene , 16 , 2997 – 3002 ( 1998. ). [DOI] [PubMed] [Google Scholar]
  • 21. ) Pack , S. D. , Karkera , J. D. , Zhuang , Z. , Pak , E. D. , Balan , K. V. , Hwu , P. , Park , W. S. , Pham , T. , Ault , D. O. , Glaser , M. , Liotta , L. , Detera‐Wadleigh , S. D. and Wadleigh , R. G.Molecular cytogenetic fingerprinting of esophageal squamous cell carcinoma by comparative genomic hybridization reveals a consistent pattern of chromosomal alterations . Genes Chromosom. Cancer , 25 , 160 – 168 ( 1999. ). [DOI] [PubMed] [Google Scholar]
  • 22. ) Yuan , B. Z. , Miller , M. J. , Keck , C. L. , Zimonjic , D. B. , Thorgeirsson , S. S. and Popescu , N. C.Cloning, characterization and chromosomal localization of a gene frequently deleted in human liver cancer (DLC‐1) homologous to rat RhoGAP . Cancer Res. , 58 , 2196 – 2199 ( 1998. ). [PubMed] [Google Scholar]
  • 23. ) Fujiwara , Y. , Ohata , H. , Kuroki , T. , Koyama , K. , Tsuchiya , E. , Monden , M. and Nakamura , Y.Isolation of a candidate tumor suppressor gene on chromosome 8p21.3–p22 that is homologous to an extracellular domain of the PDGF receptor beta gene . Oncogene , 10 , 891 – 895 ( 1995. ). [PubMed] [Google Scholar]
  • 24. ) Knuutila , S. , Aalto , Y. , Autio , K. , Björkqvist , A. M. , El‐Rifai , W. , Hemmer , S. , Huhta , T. , Kettunen , E. , Kiuru‐Kuhlefelt , S. , Larramendy , M. L. , Lushnikova , T. , Monni , O. , Pere , H. , Tapper , J. , Tarkkanen , M. , Varis , A. , Wasenius , V. M. , Wolf , M. and Zhu , Y.DNA copy number losses in human neoplasms . Am. J. Pathol. , 155 , 683 – 694 ( 1999. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25. ) Lei , J. , Zou , T. T. , Shi , Y. Q. , Zhou , X. , Smolinski , K. N. , Yin , J. , Souza , R. F. , Appel , R. , Wang , S. , Cymes , K. , Chan , O. , Abraham , J. M. , Harpaz , N. and Meltzer , S. J.Infrequent DPC4 gene mutation in esophageal cancer, gastric cancer and ulcerative colitis‐associated neoplasms . Oncogene , 13 , 2459 – 2462 ( 1996. ). [PubMed] [Google Scholar]
  • 26. ) Maesawa , C. , Tamura , G. , Nishizuka , S. , Iwaya , T. , Ogasawara , S. , Ishida , K. , Sakata , K. , Sato , N. , Ikeda , K. , Kimura , Y. , Saito , K. and Satodate , R.MAD‐related genes on 18q21.1, Smad2 and Smad4, are altered infrequently in esophageal squamous cell carcinoma . Jpn. J. Cancer Res. , 88 , 340 – 343 ( 1997. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27. ) Sonoda , G. , Palazzo , J. , du Manoir , S. , Godwin , A. K. , Feder , M. , Yakushiji , M. and Testa , J. R.Comparative genomic hybridization detects frequent overrepresentation of chromosomal material from 3q26, 8q24, and 20q13 in human ovarian carcinomas . Genes Chromosom. Cancer , 20 , 320 – 328 ( 1997. ). [PubMed] [Google Scholar]
  • 28. ) Rácz , A. , Brass , N. , Heckel , D. , Pahl , S. , Remberger , K. and Meese , E.Expression analysis of genes at 3q26–q27 involved in frequent amplification in squamous cell lung carcinoma . Eur. J. Cancer , 35 , 641 – 646 ( 1999. ). [DOI] [PubMed] [Google Scholar]
  • 29. ) Wolff , E. , Girod , S. , Liehr , T. , Vorderwülbecke , U. , Ries , J. , Steininger , H. and Gebhart , E.Oral squamous cell carcinomas are characterized by a rather uniform pattern of genomic imbalances detected by comparative genomic hybridisation . Oral Oncol. , 34 , 186 – 190 ( 1998. ). [DOI] [PubMed] [Google Scholar]
  • 30. ) Hinze , R. , Schagdarsurengin , U. , Taubert , H. , Meye , A. , Würl , P. , Holzhausen , H. J. , Rath , F. W. and Schmidt , H.Assessment of genomic imbalances in malignant fibrous histiocytomas by comparative genomic hybridization . Int. J. Mol. Med. , 3 , 75 – 79 ( 1999. ). [DOI] [PubMed] [Google Scholar]
  • 31. ) Petersen , I. , Bujard , M. , Petersen , S. , Wolf , G. , Goeze , A. , Schwendel , A. , Langreck , H. , Gellert , K. , Reichel , M. , Just , K. , du Manoir , S. , Cremer , T. , Dietel , M. and Ried , T.Patterns of chromosomal imbalances in adenocarcinoma and squamous cell carcinoma of the lung . Cancer Res. , 57 , 2331 – 2335 ( 1997. ). [PubMed] [Google Scholar]
  • 32. ) Ried , T. , Petersen , I. , Holtgreve‐Grez , H. , Speicher , M. R. , Schröck , E. , du Manoir , S. and Cremer , T.Mapping of multiple DNA gains and losses in primary small cell lung carcinomas by comparative genomic hybridization . Cancer Res. , 54 , 1801 – 1806 ( 1994. ). [PubMed] [Google Scholar]
  • 33. ) Björkqvist , A. M. , Husgafvel‐Pursiainen , K. , Anttila , S. , Karjalainen , A. , Tammilehto , L. , Mattson , K. , Vainio , H. and Knuutila , S.DNA gains in 3q occur frequently in squamous cell carcinoma of the lung, but not in adenocarcinoma . Genes Chromosom. Cancer , 22 , 79 – 82 ( 1998. ). [PubMed] [Google Scholar]
  • 34. ) Tapper , J. , Butzow , R. , Wahlstrom , T. , Seppala , M. and Knuutila , S.Evidence for divergence of DNA copy number changes in serous, mucinous and endometrioid ovarian carcinomas . Br. J. Cancer , 75 , 1782 – 1787 ( 1997. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35. ) Weber , R. G. , Sabel , M. , Reifenberger , J. , Sommer , C. , Oberstrass , J. , Reifenberger , G. , Kiessling , M. and Cremer , T.Characterization of genomic alterations associated with glioma progression by comparative genomic hybridization . Oncogene , 13 , 983 – 994 ( 1996. ). [PubMed] [Google Scholar]
  • 36. ) Bieche , I. , Champeme , M. H. and Lidereau , R.Loss and gain of distinct regions of chromosome 1q in primary breast cancer . Clin. Cancer Res. , 1 , 123 – 127 ( 1995. ). [PubMed] [Google Scholar]
  • 37. ) Tirkkonen , M. , Tanner , M. , Karhu , R. , Kallioniemi , A. , Isola , J. and Kallioniemi , O. P.Molecular cytogenetics of primary breast cancer by CGH . Genes Chromosom. Cancer , 21 , 177 – 184 ( 1998. ). [PubMed] [Google Scholar]
  • 38. ) Tarkkanen , M. , Karhu , R. , Kallioniemi , A. , Elomaa , I. , Kivioja , A. H. , Nevalainen , J. , Bohling , T. , Karaharju , E. , Hyytinen , E. and Knuutila , S.Gains and losses of DNA sequences in osteosarcomas by comparative genomic hybridization . Cancer Res. , 55 , 1334 – 1338 ( 1995. ). [PubMed] [Google Scholar]
  • 39. ) Knuutila , S. , Björkqvist , A. M. , Autio , K. , Tarkkanen , M. , Wolf , M. , Monni , O. , Szymanska , J. , Larramendy , M. L. , Tapper , J. , Pere , H. , El‐Rifai , W. , Hemmer , S. , Wasenius , V. M. , Vidgren , V. and Zhu , Y.DNA copy number amplifications in human neoplasms: review of comparative genomic hybridization studies . Am. J. Pathol. , 152 , 1107 – 1123 ( 1998. ). [PMC free article] [PubMed] [Google Scholar]
  • 40. ) Ishiguro , T. , Nakajima , M. , Naito , M. , Muto , T. and Tsuruo , T.Identification of genes differentially expressed in B16 murine melanoma sublines with different metastatic potentials . Cancer Res. , 56 , 875 – 879 ( 1996. ). [PubMed] [Google Scholar]
  • 41. ) Landberg , G. , Erlanson , M. , Roos , G. , Tan , E. M. and Casiano , C. A.Nuclear autoantigen p330d/CENPF: a marker for cell proliferation in human malignancies . Cytometry , 25 , 90 – 98 ( 1996. ). [DOI] [PubMed] [Google Scholar]

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