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Centromeric chromosomal translocations show tissue-specific differences between squamous cell carcinomas and adenocarcinomas

Oncogene volume 24, pages 1571–1579 (2005)Cite this article

Abstract

Structural chromosomal aberrations are common in epithelial tumors. Here, we compared the location of centromeric breaks associated with whole arm translocations in seven adenocarcinoma cell lines and nine squamous cell carcinoma cell lines using SKY, microarray-based comparative genomic hybridization (array CGH) and fluorescence in situ hybridization (FISH). Whole arm translocations were more frequent in squamous cell carcinomas (112 in nine cell lines and nine in one short-term culture) than in adenocarcinomas (13 in seven cases) and most often resulted in copy number alterations. Array CGH analysis demonstrated that in all squamous cell carcinomas and in most adenocarcinomas, the breakpoints of unbalanced whole arm translocations occurred between the two clones on the array flanking the centromeres. However, FISH with centromeric probes revealed that in squamous cell carcinomas, the marker chromosomes with whole arm translocations contained centromeres comprised of material from both participating chromosomes, while in adenocarcinomas centromeric material from only one of the chromosomes was present. These observations suggest that different mechanisms of centromeric instability underlie the formation of chromosomal aberrations in adenocarcinomas and squamous cell carcinomas.

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References

  • Albertson DG, Collins C, McCormick F and Gray JW . (2003). Nat. Genet., 34, 369–376.

  • Bakshi RP, Galande S and Muniyappa K . (2001). Crit. Rev. Biochem. Mol. Biol., 36, 1–37.

  • Chen TR, Drabkowski D, Hay RJ, Macy M and Peterson Jr W . (1987). Cancer Genet. Cytogenet., 27, 125–134.

  • Eshelman JR, Casey G, Kochera ME, Sedwick WD, Swinler SE, Veigl ML, Willson JKV, Schwartz S and Markowitz SD . (1998). Oncogene, 17, 719–725.

  • Floridia G, Zatterale A, Zuffardi O and Tyler-Smith C . (2000). EMBO Rep., 1, 489–493.

  • van Grieken NC, Weiss MM, Meijer GA, Hermsen MA, Scholte GH, Lindeman J, Craanen ME, Bloemena E, Meuwissen SG, Baak JP and Kuipers EJ . (2000). J. Pathol., 192, 301–306.

  • Hermsen MAJA, Baak JPA, Weiss J, Meijer GA, Weiss JM, Walboomers JJM, Snijders PJF and van Diest PJ . (1998). J. Pathol., 186, 356–362.

  • Hermsen MAJA, Guervós MA, Meijer GA, Baak JPA, lvarez-Marcos C, Salas A, Sampedro A and van Diest PJ . (2001). J. Pathol., 194, 177–182.

  • Hermsen MAJA, Joenje H, Arwert F, Welters MJP, Braakhuis BJM, Bagnay M, Westerveld A and Slater R . (1996). Genes Chromosomes Cancer, 15, 1–9.

  • Hermsen MAJA, Postma C, Baak JPA, Weiss MM, Rapallo A, Sciutto A, Roemen G, Arends J-W, Richard W, Giaretti W, De Goeij A and Meijer GA . (2002). Gastroenterology, 123, 1109–1119.

  • Hermsen MAJA, Xie Y, Rooimans MA, Meijer GA, Baak JPA, Plukker JTM, Arwert F and Joenje H . (2001). Fam. Cancer, 1, 39–43.

  • Israeli O, Gotlieb WH, Friedman E, Goldman B, Ben-Baruch G, Aviram-Goldring A and Rienstein S . (2003). Gynecol. Oncol., 90, 629–636.

  • Jain AN, Tokuyasu TA, Snijders AM, Segraves R, Albertson DG and Pinkel D . (2002). Genome Res., 12, 325–332.

  • Jin C, Jin Y, Wennerberg J, Dictor M and Mertens F . (2000). Genes Chromosomes Cancer, 28, 66–76.

  • Jin Y, Jin C, Salemark L, Martins C, Wennerberg J and Mertens F . (2000). Chromosoma, 109, 476–481.

  • Joenje H and Patel KJ . (2001). Nat. Rev. Genet., 2, 446–457.

  • Luk C, Tsao MS, Bayani J, Shepherd F and Squire JA . (2001). Cancer Genet. Cytogenet., 125, 87–99.

  • Martins C, Jin Y, Jin C, Wennerberg J, Hoglund M and Mertens F . (1999). Eur. J. Cancer, 35, 498–501.

  • Meijer GA, Hermsen MA, Baak JP, van Diest PJ, Meuwissen SG, Belien JA, Hoovers JM, Joenje H, Snijders PJ and Walboomers JM . (1998). J. Clin. Pathol., 51, 901–909.

  • Nakao K, Mehta KR, Fridlyand J, Moore DH, Jain AN, Lafuente A, Wiencke JW, Terdiman JP and Waldman FM . (2004). Carcinogenesis Mar 4 [Epub ahead of print].

  • NCI and NCBI's SKY/M-FISH and CGH Database (2001). http://www.ncbi.nlm.nih.gov/sky/skyweb.cgi.

  • Pei J, Balsara BR, Li W, Litwin S, Gabrielson E, Feder M, Jen J and Testa JR . (2001). Genes Chromosomes Cancer, 31, 282–287.

  • Petersen I, Langreck H, Wolf G, Schwendel A, Psille R, Vogt P, Reichel MB, Ried T and Dietel M . (1997). Br. J. Cancer, 75, 79–86.

  • Pinkel D, Segraves R, Sudar D, Clark S, Poole I, Kowbel D, Collins C, Kuo W-L, Chen C, Zhai Y, Dairkee SH, Ljung B-M, Gray JW and Albertson DG . (1998). Nat. Genet., 20, 207–211.

  • Rattner JB, Hendzel MJ, Furbee CS, Muller MT and Bazett-Jones DP . (1996). J. Cell Biol., 134, 1097–1107.

  • Schlegel J, Stumm G, Scherthan H, Bocker T, Zirngibl HR, Rüschoff J and Hofstädter F . (1995). Cancer Res., 55, 6002–6005.

  • Schrock E, Garini Y, Köhler M and Ried T . (1999). Diagnostic Cytogenetics Wegner R (ed). Springer Verlag: Berlin, pp. 416–438.

    Book  Google Scholar 

  • Schrock E, Weaver Z and Albertson D . (2001). Current Protocols in Cytometry Tanke H (ed). John Wiley and Sons: New York, pp. 8.12.1–8.12.21.

    Google Scholar 

  • Snijders AM, Nowak N, Segraves R, Blackwood S, Brown N, Conroy J, Hamilton G, Hindle AK, Huey B, Kimura K, Law S, Myambo K, Palmer J, Ylstra B, Yue JP, Gray JW, Jain AN, Pinkel D and Albertson DG . (2001). Nat. Genet., 29, 263–264.

  • Snijders AM, Fridlyand J, Mans DA, Segraves R, Jain AN, Pinkel D and Albertson DG . (2003). Oncogene, 22, 4370–4379.

  • Soulie P, Fourme E, Hamelin R, Asselain B, Salmon R-J, Dutrillaux B and Muleris M . (1999). Cancer Genet. Cytogenet., 115, 118–122.

  • Sumner AT, Mitchell AR and Ellis PM . (1998). J. Med. Genet., 35, 833–835.

  • Telenius H, Pelmear AH, Tunnacliffe A, Carter NP, Behmel A, Ferguson-Smith MA, Nordenskjold M, Pfragner R and Ponder BA . (1992). Genes Chromosomes Cancer, 4, 257–263.

  • Tirkkonen M, Johannsson O, Agnarsson BA, Olsson H, Ingvarsson S, Karhu R, Tanner M, Isola J, Barkardottir RB, Borg A and Kallioniemi OP . (1997). Cancer Res., 57, 1222–1227.

  • Van Triest B, Pinedo HM, van Hensbergen Y, Smid K, Telleman F, Schoenmakers PS, van der Wilt CL, van Laar JA, Noordhuis P, Jansen G and Peters GJ . (1999). Clin. Cancer Res., 5, 643–654.

  • Varis A, Puolakkainen P, Savolainen H, Kokkola A, Salo J, Nieminen O, Nordling S and Knuutila S . (2001). Cancer Genet. Cytogenet., 127, 53–58.

  • Warburton PE and Earnshaw WC . (1997). Bioessays, 19, 97–99.

  • Weiss MM, Kuipers EJ, Hermsen MA, van Grieken NC, Offerhaus J, Baak JP, Meuwissen SG and Meijer GA . (2003). J. Pathol., 199, 157–165.

  • Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N, Bugge M, Hulten M, Qu X, Russo JJ and Viegas-Pequignot E . (1999). Nature, 402, 187–191.

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Acknowledgements

The work in this paper was supported by the Dutch Cancer Society, KWF Grant VU97-1455 and the Sacha Swarttouw-Hijmans foundation, by the German Federal Ministry of Education and Research, BioFuture Grant 0311875, and United States Public Health Service Grant CA94407.

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Author notes

  1. Mario Hermsen

    Present address: Department of Otolaryngology, Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Hospital Central de Asturias, Oviedo, Spain

  2. Evelin Schrock

    Present address: Institute of Clinical Genetics, Medical Faculty Carl Gustav Carus, University of Technology, Dresden, Germany

Authors and Affiliations

  1. Department of Pathology, VU University Medical Center, Amsterdam, The Netherlands

    Mario Hermsen, Marta Alonso Guervós, Jan Baak, Paul van Diest & Gerrit Meijer

  2. UCSF Comprehensive Cancer Center, San Francisco, USA

    Antoine Snijders, Daniel Pinkel & Donna Albertson

  3. Institute of Molecular Biotechnology, Friedrich-Schiller-University, Jena, Germany

    Simone Tænzer, Ulrike Koerner & Evelin Schrock

  4. Department of Pathology, SiR Hospital, Stavanger, Norway

    Jan Baak

  5. Institute of Medical Genetics, Humboldt University, Berlin, Germany

    Evelin Schrock

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  1. Mario Hermsen
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Correspondence to Mario Hermsen.

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Hermsen, M., Snijders, A., Guervós, M. et al. Centromeric chromosomal translocations show tissue-specific differences between squamous cell carcinomas and adenocarcinomas. Oncogene 24, 1571–1579 (2005). https://doi.org/10.1038/sj.onc.1208294

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