Chromosomal abnormalities and novel disease-related regions in progression from Barrett's esophagus to esophageal adenocarcinoma

International Journal of Cancer

Volumn 125, Issue 10, 2009, Pages 2349-2359

  Akagi, Tadayuki ^a,f   Ito, Tetsuo ^b   Kato, Motohiro ^d   Jin, Zhe ^b   Cheng, Yulan ^b   Kan, Takatsugu ^b   Yamamoto, Go ^d   Olaru, Alexandru ^b   Kawamata, Norihiko ^a   Boult, Jessica ^a   Soukiasian, Harmik J ^e   Miller, Carl W ^a   Ogawa, Seishi ^d   Meltzer, Stephen J ^b,c   Koeffler, H Phillip ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

^e CEDARS SINAI MEDICAL CENTER   (United States)

^f KANAZAWA UNIVERSITY   (Japan)

Author keywords

BNC2; Copy number neutral; Esophageal adenocarcinoma; LOH; SNP chip

Indexed keywords

MESSENGER RNA;

ADULT; AGED; ARTICLE; BARRETT ESOPHAGUS; CANCER GROWTH; CHROMOSOME 9P; CHROMOSOME ABERRATION; CHROMOSOME ANALYSIS; CHROMOSOME DELETION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ESOPHAGEAL ADENOCARCINOMA; FEMALE; GENE AMPLIFICATION; GENE EXPRESSION; GENE NUMBER; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; HUMAN CELL; MALE; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR SUPPRESSOR GENE;

ADENOCARCINOMA; AGED; AGED, 80 AND OVER; BARRETT ESOPHAGUS; BLOTTING, WESTERN; CHROMOSOME ABERRATIONS; DISEASE PROGRESSION; DNA-BINDING PROTEINS; ESOPHAGEAL NEOPLASMS; ESOPHAGUS; FEMALE; GENE DOSAGE; GENE EXPRESSION PROFILING; GENOME, HUMAN; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LOSS OF HETEROZYGOSITY; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR MARKERS, BIOLOGICAL;

EID: 70349864986     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24620     Document Type: Article

References (59)

1. Shaheen N, Ransohoff DF. Gastroesophageal reflux, Barrett's esophagus, and esophageal cancer: scientific review. JAMA 2002; 287:1972-1981
2. Wijnhoven BP, Tilanus HW, Dinjens WN. Molecular biology of Barrett's adenocarcinoma. Ann Surg 2001;233:322-337
3. McManus DT, Olaru A, Meltzer SJ. Biomarkers of esophageal adenocarcinoma and Barrett's esophagus. Cancer Res 2004;64:1561-1569 (Pubitemid 38428671)
4. Moskaluk CA, Hu J, Perlman EJ. Comparative genomic hybridization of esophageal and gastroesophageal adenocarcinomas shows consensus areas of DNA gain and loss. Genes Chromosomes Cancer 1998; 22:305-311 (Pubitemid 28304521)
5. van Dekken H, Geelen E, Dinjens WN, Wijnhoven BP, Tilanus HW, Tanke HJ, Rosenberg C. Comparative genomic hybridization of cancer of the gastroesophageal junction: deletion of 14Q31-32.1 discriminates between esophageal (Barrett's) and gastric cardia adenocarcinomas. Cancer Res 1999;59:748-752 (Pubitemid 29076077)
6. van Dekken H, Vissers CJ, Tilanus HW, Tanke HJ, Rosenberg C. Clonal analysis of a case of multifocal oesophageal (Barrett's) adenocarcinoma by comparative genomic hybridization. J Pathol 1999;188: 263-266 (Pubitemid 29317768)
7. Walch AK, Zitzelsberger HF, Bruch J, Keller G, Angermeier D, Aubele MM, Mueller J, Stein H, Braselmann H, Siewert JR, Höfler H, Werner M. Chromosomal imbalances in Barrett's adenocarcinoma and the metaplasia-dysplasia- carcinoma sequence. Am J Pathol 2000; 156:555-566 (Pubitemid 30643811)
8. Varis A, Puolakkainen P, Savolainen H, Kokkola A, Salo J, Nieminen O, Nordling S, Knuutila S. DNA copy number profiling in esophageal Barrett adenocarcinoma: comparison with gastric adenocarcinoma and esophageal squamous cell carcinoma. Cancer Genet Cytogenet 2001;127:53-58 (Pubitemid 32530094)
9. Riegman PH, Vissers KJ, Alers JC, Geelen E, Hop WC, Tilanus HW, van Dekken H. Genomic alterations in malignant transformation of Barrett's esophagus. Cancer Res 2001;61:3164-3170 (Pubitemid 32691970)
10. Croft J, Parry EM, Jenkins GJ, Doak SH, Baxter JN, Griffiths AP, Brown TH, Parry JM. Analysis of the premalignant stages of Barrett's oesophagus through to adenocarcinoma by comparative genomic hybridization. Eur J Gastroenterol Hepatol 2002;14:1179-1186 (Pubitemid 35471525)
11. Su M, Chin SF, Li XY, Edwards P, Caldas C, Fitzgerald RC. Comparative genomic hybridization of esophageal adenocarcinoma and squamous cell carcinoma cell lines. Dis Esophagus 2006;19:10-14.
12. Nannya Y, Sanada M, Nakazaki K, Hosoya N, Wang L, Hangaishi A, Kurokawa M, Chiba S, Bailey DK, Kennedy GC, Ogawa S. A robust algorithm for copy number detection using high-density oligonucleotide single nucleotide polymorphism genotyping arrays. Cancer Res 2005;65:6071-6079 (Pubitemid 40994391)
13. Engle LJ, Simpson CL, Landers JE. Using high-throughput SNP technologies to study cancer. Oncogene 2006;25:1594-1601
14. Yamamoto G, Nannya Y, Kato M, Sanada M, Levine RL, Kawamata N, Hangaishi A, Kurokawa M, Chiba S, Gilliland DG, Koeffler HP, Ogawa S. Highly sensitive method for genomewide detection of allelic composition in nonpaired, primary tumor specimens by use of affymetrix single-nucleotide-polymorphism genotyping microarrays. Am J Hum Genet 2007;81:114-126 (Pubitemid 47001161)
15. Pfeifer D, Pantic M, Skatulla I, Rawluk J, Kreutz C, Martens UM, Fisch P, Timmer J, Veelken H. Genome-wide analysis of DNA copy number changes and LOH in CLL using high-density SNP arrays. Blood 2007;109:1202-1210 (Pubitemid 46220669)
16. Lehmann S, Ogawa S, Raynaud SD, Sanada M, Nannya Y, Ticchioni M, Bastard C, Kawamata N, Koeffler HP. Molecular allelokaryotyping of early-stage, untreated chronic lymphocytic leukemia. Cancer 2008;112:1296-1305
17. Mullighan CG, Goorha S, Radtke I, Miller CB, Coustan-Smith E, Dalton JD, Girtman K, Mathew S, Ma J, Pounds SB, Su X, Pui CH, et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature 2007;446:758-764 (Pubitemid 46582031)
18. Kawamata N, Ogawa S, Zimmermann M, Kato M, Sanada M, Hemminki K, Yamatomo G, Nannya Y, Koehler R, Flohr T, Miller CW, Harbott J, et al. Molecular allelokaryotyping of pediatric acute lymphoblastic leukemias by high-resolution single nucleotide polymorphism oligonucleotide genomic microarray. Blood 2008;111:776-784
19. Raghavan M, Lillington DM, Skoulakis S, Debernardi S, Chaplin T, Foot NJ, Lister TA, Young BD. Genome-wide single nucleotide polymorphism analysis reveals frequent partial uniparental disomy due to somatic recombination in acute myeloid leukemias. Cancer Res 2005; 65:375-378
20. Fitzgibbon J, Smith LL, Raghavan M, Smith ML, Debernardi S, Skoulakis S, Lillington D, Lister TA, Young BD. Association between acquired uniparental disomy and homozygous gene mutation in acute myeloid leukemias. Cancer Res 2005;65:9152-9154 (Pubitemid 41507976)
21. Tyybäkinoja A, Elonen E, Vauhkonen H, Saarela J, Knuutila S. Single nucleotide polymorphism microarray analysis of karyotypically normal acute myeloid leukemia reveals frequent copy-number-neutral loss of heterozygosity. Haematologica 2008;93:631-632
22. Gorletta TA, Gasparini P, D'Elios MM, Trubia M, Pelicci PG, Di Fiore PP. Frequent loss of heterozygosity without loss of genetic material in acute myeloid leukemia with a normal karyotype. Genes Chromosomes Cancer 2005;44:334-337 (Pubitemid 41397103)
23. Fitzgibbon J, Smith LL, Raghavan M, Smith ML, Debernardi S, Skoulakis S, Lillington D, Lister TA, Young BD. Association between acquired uniparental disomy and homozygous gene mutation in acute myeloid leukemias. Cancer Res 2005;65:9152-9154 (Pubitemid 41507976)
24. Akagi T, Ogawa S, Dugas M, Kawamata N, Yamamoto G, Nannya Y, Sanada M, Miller CW, Yung A, Schnittger S, Haferlach T, Haferlach C, et al. Frequent genomic abnormalities in acute myeloid leukemia/myelodysplastic syndrome with normal karyotype. Haematologica 2009;94:213-223
25. Vanhoutteghem A, Djian P. Basonuclin 2: an extremely conserved homolog of the zinc finger protein basonuclin. Proc Natl Acad Sci USA 2004;101:3468-3473 (Pubitemid 38338218)
26. Romano RA, Li H, Tummala R, Maul R, Sinha S. Identification of Basonuclin2, a DNA-binding zinc-finger protein expressed in germ tissues and skin keratinocytes. Genomics 2004;83:821-833 (Pubitemid 38469924)
27. Vanhoutteghem A, Djian P. Basonuclins 1 and 2, whose genes share a common origin, are proteins with widely different properties and functions. Proc Natl Acad Sci USA 2006;103:12423-12428 (Pubitemid 44267275)
28. Nakamura T, Nekarda H, Hoelscher AH, Bollschweiler E, Harbeck N, Becker K, Siewert JR, Harbeck N. Prognostic value of DNA ploidy and c-erbB-2 oncoprotein overexpression in adenocarcinoma of Barrett's esophagus. Cancer 1994;73:1785-1794 (Pubitemid 24101951)
29. Jankowski J, Hopwood D, Wormsley KG. Expression of epidermal growth factor, transforming growth factor alpha and their receptor in gastro-oesophageal diseases. Dig Dis 1993;11:1-11.
30. Hardwick RH, Barham CP, Ozua P, Newcomb PV, Savage P, Powell R, Rahamin J, Alderson D. Immunohistochemical detection of p53 and c-erbB-2 in oesophageal carcinoma; no correlation with prognosis. Eur J Surg Oncol 1997;23:30-35
31. Hardwick RH, Shepherd NA, Moorghen M, Newcomb PV, Alderson D. c-erbB-2 overexpression in the dysplasia/carcinoma sequence of Barrett's oesophagus. J Clin Pathol 1995;48:129-132
32. Duhaylongsod FG, Gottfried MR, Iglehart JD, Vaughn AL, Wolfe WG. The significance of c-erb B-2 and p53 immunoreactivity in patients with adenocarcinoma of the esophagus. Ann Surg 1995;221: 677-684
33. Fléjou JF, Paraf F, Muzeau F, Fékété F, Hénin D, Jothy S, Potet F. Expression of c-erbB-2 oncogene product in Barrett's adenocarcinoma: pathological and prognostic correlations. J Clin Pathol 1994; 47:23-26 (Pubitemid 24057743)
34. Polkowski W, van Sandick JW, Offerhaus GJ, ten Kate FJ, Mulder J, Obertop H, van Lanschot JJ. Prognostic value of Lauren classification and c-erbB-2 oncogene overexpression in adenocarcinoma of the esophagus and gastroesophageal junction. Ann Surg Oncol 1999;6:290-297
35. Dahlberg PS, Jacobson BA, Dahal G, Fink JM, Kratzke RA, Maddaus MA, Ferrin LJ. ERBB2 amplifications in esophageal adenocarcinoma. Ann Thorac Surg 2004;78:1790-1800
36. Kim R, Ohi Y, Inoue H, Toge T. Expression and relationship between topoisomerase I and II alpha genes in tumor and normal tissues in esophageal, gastric and colon cancers. Anticancer Res 1999;19:5393-5398 (Pubitemid 30103380)
37. Ohashi Y, Sasano H, Yamaki H, Shizawa S, Kikuchi A, Shineha R, Akaishi T, Satomi S, Nagura H. Topoisomerase II alpha expression in esophageal squamous cell carcinoma. Anticancer Res 1999;19:1873-1880 (Pubitemid 29392752)
38. Pritchard KI, Messersmith H, Elavathil L, Trudeau M, O'Malley F, Dhesy-Thind B. HER-2 and topoisomerase II as predictors of response to chemotherapy. J Clin Oncol 2008;26:736-744 (Pubitemid 351264386)
39. Igarashi A, Okochi H, Bradham DM, Grotendorst GR. Regulation of connective tissue growth factor gene expression in human skin fibroblasts and during wound repair. Mol Biol Cell 1993;4:637-645 (Pubitemid 23183611)
40. Deng YZ, Chen PP, Wang Y, Yin D, Koeffler HP, Li B, Tong XJ, Xie D. Connective tissue growth factor is overexpressed in esophageal squamous cell carcinoma and promotes tumorigenicity through beta-catenin-T-cell factor/Lef signaling. J Biol Chem 2007;282: 36571-36581
41. Aebersold DM, Landt O, Berthou S, Gruber G, Beer KT, Greiner RH, Zimmer Y. Prevalence and clinical impact of Met Y1253D-activating point mutation in radiotherapy-treated squamous cell cancer of the oropharynx. Oncogene 2003;22:8519-8523 (Pubitemid 37523903)
42. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, BottomleyW, Davis N, Dicks E, et al. Mutations of the BRAF gene in human cancer. Nature 2002;417:949-954 (Pubitemid 34716871)
43. Sommerer F, Vieth M, Markwarth A, Röhrich K, Vomschloss S, May A, Ell C, Stolte M, Hengge UR, Wittekind C, Tannapfel A. Mutations of BRAF and KRAS2 in the development of Barrett's adenocarcinoma. Oncogene 2004;23:554-558 (Pubitemid 38175010)
44. Esteve A, Martel-Planche G, Sylla BS, Hollstein M, Hainaut P, Montesano R. Low frequency of p16/CDKN2 gene mutations in esophageal carcinomas. Int J Cancer 1996;66:301-304 (Pubitemid 26166190)
45. Muzeau F, Flejou JF, Thomas G, Hamelin R. Loss of heterozygosity on chromosome 9 and p16 (MTS1, CDKN2) gene mutations in esophageal cancers. Int J Cancer 1997;72:27-30. (Pubitemid 27314634)
46. Suzuki H, Zhou X, Yin J, Lei J, Jiang HY, Suzuki Y, Chan T, Hannon GJ, Mergner WJ, Abraham JM, Meltzer SJ. Intragenic mutations of CDKN2B and CDKN2A in primary human esophageal cancers. Hum Mol Genet 1995;4:1883-1887
47. Zhou X, Suzuki H, Shimada Y, Imamura M, Yin J, Jiang HY, Tarmin L, Abraham JM, Meltzer SJ. Genomic DNA and messenger RNA expression alterations of the CDKN2B and CDKN2 genes in esophageal squamous carcinoma cell lines. Genes Chromosomes Cancer 1995;13:285-290
48. Wong DJ, Barrett MT, Stöger R, Emond MJ, Reid BJ. p16INK4a promoter is hypermethylated at a high frequency in esophageal adenocarcinomas. Cancer Res 1997;57:2619-2622 (Pubitemid 27283770)
49. Klump B, Hsieh CJ, Holzmann K, Gregor M, Porschen R. Hypermethylation of the CDKN2/p16 promoter during neoplastic progression in Barrett's esophagus. Gastroenterology 1998;115:1381-1386 (Pubitemid 28545988)
50. Michael D, Beer DG, Wilke CW, Miller DE, Glover TW. Frequent deletions of FHIT and FRA3B in Barrett's metaplasia and esophageal adenocarcinomas. Oncogene 1997;15:1653-1659 (Pubitemid 27466704)
51. Chen YJ, Chen PH, Lee MD, Chang JG. Aberrant FHIT transcripts in cancerous and corresponding non-cancerous lesions of the digestive tract. Int J Cancer 1997;72:955-958
52. Zanesi N, Fidanza V, Fong LY, Mancini R, Druck T, Valtieri M, Rüdiger T, McCue PA, Croce CM, Huebner K. The tumor spectrum in FHIT-deficient mice. Proc Natl Acad Sci USA 2001;98: 10250-10255
53. Fujishita T, Doi Y, Sonoshita M, Hiai H, Oshima M, Huebner K, Croce CM, Taketo MM. Development of spontaneous tumours and intestinal lesions in Fhit gene knockout mice. Br J Cancer 2004;91: 1571-1574 (Pubitemid 39486365)
54. Maley CC, Galipeau PC, Finley JC, Wongsurawat VJ, Li X, Sanchez CA, Paulson TG, Blount PL, Risques RA, Rabinovitch PS, Reid BJ. Genetic clonal diversity predicts progression to esophageal adenocarcinoma. Nat Genet 2006;38:468-473
55. Barrett MT, Sanchez CA, Prevo LJ, Wong DJ, Galipeau PC, Paulson TG, Rabinovitch PS, Reid BJ. Evolution of neoplastic cell lineages in Barrett oesophagus. Nat Genet 1999;22:106-109
56. Wong DJ, Paulson TG, Prevo LJ, Galipeau PC, Longton G, Blount PL, Reid BJ. p16 (INK4a) lesions are common, early abnormalities that undergo clonal expansion in Barrett's metaplastic epithelium. Cancer Res 2001;61:8284-8289 (Pubitemid 33091623)
57. Blount PL, Meltzer SJ, Yin J, Huang Y, Krasna MJ, Reid BJ. Clonal ordering of 17p and 5q allelic losses in Barrett dysplasia and adenocarcinoma. Proc Natl Acad Sci USA 1993;90:3221-3225 (Pubitemid 23111337)
58. Boynton RF, Huang Y, Blount PL, Reid BJ, Raskind WH, Haggitt RC, Newkirk C, Resau JH, Yin J, McDaniel T, Meltzer SJ. Frequent loss of heterozygosity at the retinoblastoma locus in human esophageal cancers. Cancer Res 1991;51:5766-5769
59. Nancarrow DJ, Handoko HY, Smithers BM, Gotley DC, Drew PA, Watson DI, Clouston AD, Hayward NK, Whiteman DC. Genomewide copy number analysis in esophageal adenocarcinoma using high-density single-nucleotide polymorphism arrays. Cancer Res 2008;68:4163-4172