Localisation of a novel region of recurrent amplification in follicular lymphoma to an ∼6.8 Mb region of 13q32-33
Corresponding Author
Michael J. Neat
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London EC1M 6BQ, England, UK.Search for more papers by this authorNicola Foot
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorMichael Jenner
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorLindsey Goff
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorKevin Ashcroft
The Sanger Centre, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, UK
Search for more papers by this authorDeborah Burford
The Sanger Centre, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, UK
Search for more papers by this authorAndy Dunham
The Sanger Centre, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, UK
Search for more papers by this authorAndrew Norton
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorT. Andrew Lister
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorJude Fitzgibbon
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorCorresponding Author
Michael J. Neat
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London EC1M 6BQ, England, UK.Search for more papers by this authorNicola Foot
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorMichael Jenner
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorLindsey Goff
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorKevin Ashcroft
The Sanger Centre, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, UK
Search for more papers by this authorDeborah Burford
The Sanger Centre, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, UK
Search for more papers by this authorAndy Dunham
The Sanger Centre, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, UK
Search for more papers by this authorAndrew Norton
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorT. Andrew Lister
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorJude Fitzgibbon
ICRF Medical Oncology Unit, St. Bartholomew's Hospital, Charterhouse Square, London, UK
Search for more papers by this authorAbstract
Follicular lymphoma (FL) is characterised by the presence of the t(14;18)(q32;q21) and represents ∼25% of new cases of non-Hodgkin's lymphoma. While the t(14;18) is a well-documented rearrangement, the role of secondary cytogenetic abnormalities in the development and progression of these tumours remains unclear. Comparative genomic hybridisation was used to characterise changes in DNA copy number in tumour DNA from patients with this malignancy. The mean numbers of deletion and amplification events found in each of the 45 samples studied were 1.8 and 2.3, respectively. Regions of recurrent (>10% tumour samples) gain involved chromosomes 2p13-16 (16%), 7 (20%), 12 (16%), 13q21-33 (18%), 18 (27%), and X (36%) and frequent losses localised to 6q (29%) and 17p (20%). Amplification of chromosome 13 represents a novel finding in FL. The minimal amplified region was refined to a 6.8-Mb interval of 13q32-33 between the BAC clones 88K16 and 44H20 by fluorescence in situ hybridisation studies using metaphase chromosomes derived from tumour material. There are a number of reports in the literature suggesting that amplification of chromosome 13 also occurs in other human cancers. The location of the putative oncogene on 13q described here in follicular and transformed lymphoma may also be important in the evolution of many other malignancies. © 2001 Wiley-Liss, Inc.
REFERENCES
- Armitage JO, Weisenburger DD. 1998. New approach to classifying non-Hodgkin's lymphomas: clinical features of the major histologic subtypes. Non-Hodgkin's Lymphoma Classification Project. J Clin Oncol 16: 2780–2795.
- Autio K, Aalto Y, Franssila K, Elonen E, Joensuu H, Knuutila S. 1998. Low number of DNA copy number changes in small lymphocytic lymphoma. Haematologica 83: 690–692.
- Avet-Loiseau H, Vigier M, Moreau A, Mellerin MP, Gaillard F, Harousseau JL, Bataille R, Milpied N. 1997. Comparative genomic hybridization detects genomic abnormalities in 80% of follicular lymphomas. Br J Haematol 97: 119–122.
- Bastion Y, Sebban C, Berger F, Felman P, Salles G, Dumontet C, Bryon PA, Coiffier B. 1997. Incidence, predictive factors, and outcome of lymphoma transformation in follicular lymphoma patients. J Clin Oncol 15: 1587–1594.
- Bea S, Ribas M, Hernandez JM, Bosch F, Pinyol M, Hernandez L, Garcia JL, Flores T, Gonzalez M, Lopez-Guillermo A, Piris MA, Cardesa A, Montserrat E, Miro R, Campo E. 1999. Increased number of chromosomal imbalances and high-level DNA amplifications in mantle cell lymphoma are associated with blastoid variants. Blood 93: 4365–4374.
- Beckwith M, Longo DL, O'Connell CD, Moratz CM, Urba WJ. 1990. Phorbol ester-induced, cell-cycle-specific, growth inhibition of human B-lymphoma cell lines. J Natl Cancer Inst 82: 501–509.
- Bentz M, Werner CA, Dohner H, Joos S, Barth TF, Siebert R, Schroder M, Stilgenbauer S, Fischer K, Moller P, Lichter P. 1996. High incidence of chromosomal imbalances and gene amplifications in the classical follicular variant of follicle center lymphoma. Blood 88: 1437–1444.
-
Cigudosa JC,
Parsa NZ,
Louie DC,
Filippa DA,
Jhanwar SC,
Johansson B,
Mitelman F,
Chaganti RSK.
1999.
Cytogenetic analysis of 363 consecutively ascertained diffuse large B-cell lymphomas.
Genes Chromosomes Cancer
25:
123–133.
10.1002/(SICI)1098-2264(199906)25:2<123::AID-GCC8>3.0.CO;2-4 CAS PubMed Web of Science® Google Scholar
-
Cullen MH,
Lister TA,
Brearley RI,
Shand WS,
Stansfeld AG.
1979.
Histological transformation of non-Hodgkin's lymphoma: a prospective study.
Cancer
44:
645–651.
10.1002/1097-0142(197908)44:2<645::AID-CNCR2820440234>3.0.CO;2-Y CAS PubMed Web of Science® Google Scholar
-
Dierlamm J,
Wlodarska I,
Michaux L,
Vermeesch JR,
Meeus P,
Stul M,
Criel A,
Verhoef G,
Thomas J,
Delannoy A,
Louwagie A,
Cassiman JJ,
Mecucci C,
Hagemeijer A,
Van den Berghe H.
1997.
FISH identifies different types of duplications with 12q13-15 as the commonly involved segment in B-cell lymphoproliferative malignancies characterized by partial trisomy 12.
Genes Chromosomes Cancer
20:
155–166.
10.1002/(SICI)1098-2264(199710)20:2<155::AID-GCC6>3.0.CO;2-2 CAS PubMed Web of Science® Google Scholar
- du Manoir S, Schrock E, Bentz M, Speicher MR, Joos S, Ried T, Lichter P, Cremer T. 1995. Quantitative analysis of comparative genomic hybridization. Cytometry 19: 27–41.
- Gaidano G, Hauptschein RS, Parsa NZ, Offit K, Rao PH, Lenoir G, Knowles DM, Chaganti RS, Dalla-Favera R. 1992. Deletions involving two distinct regions of 6q in B-cell non-Hodgkin lymphoma. Blood 80: 1781–1787.
- Goff LK, Neat MJ, Crawley CR, Jones L, Jones E, Lister TA, Gupta RK. 2000. The use of real-time quantitative polymerase chain reaction and comparative genomic hybridization to identify amplification of the REL gene in follicular lymphoma. Br J Haematol 111: 618–625.
- Hauptschein RS, Gamberi B, Rao PH, Frigeri F, Scotto L, Venkatraj VS, Gaidano G, Rutner T, Edwards YH, Chaganti RS, Dalla-Favera R. 1998. Cloning and mapping of human chromosome 6q26-q27 deleted in B-cell non-Hodgkin lymphoma and multiple tumor types. Genomics 50: 170–186.
- Houldsworth J, Mathew S, Rao PH, Dyomina K, Louie DC, Parsa N, Offit K, Chaganti RS. 1996. REL proto-oncogene is frequently amplified in extranodal diffuse large cell lymphoma. Blood 87: 25–29.
- Joos S, Otano-Joos MI, Ziegler S, Bruderlein S, du Manoir S, Bentz M, Moller P, Lichter P. 1996. Primary mediastinal (thymic) B-cell lymphoma is characterized by gains of chromosomal material including 9p and amplification of the REL gene. Blood 87: 1571–1578.
- Kallioniemi A, Kallioniemi OP, Sudar D, Rutovitz D, Gray JW, Waldman F, Pinkel D. 1992. Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors. Science 258: 818–821.
- Kallioniemi OP, Kallioniemi A, Piper J, Isola J, Waldman FM, Gray JW, Pinkel D. 1994. Optimizing comparative genomic hybridization for analysis of DNA sequence copy number changes in solid tumors. Genes Chromosomes Cancer 10: 231–243.
- Kamesaki H, Fukuhara S, Tatsumi E, Uchino H, Yamabe H, Miwa H, Shirakawa S, Hatanaka M, Honjo T. 1986. Cytochemical, immunologic, chromosomal, and molecular genetic analysis of a novel cell line derived from Hodgkin's disease. Blood 68: 285–292.
-
Kirchhoff M,
Gerdes T,
Maahr J,
Rose H,
Bentz M,
Dohner H,
Lundsteen C.
1999.
Deletions below 10 megabasepairs are detected in comparative genomic hybridization by standard reference intervals.
Genes Chromosomes Cancer
25:
410–413.
10.1002/(SICI)1098-2264(199908)25:4<410::AID-GCC17>3.0.CO;2-J CAS PubMed Web of Science® Google Scholar
- Kluin-Nelemans HC, Limpens J, Meerabux J, Beverstock GC, Jansen JH, de Jong D, Kluin PM. 1991. A new non-Hodgkin's B-cell line (DoHH2) with a chromosomal translocation t(14;18)(q32;q21). Leukemia 5: 221–224.
- Knuutila S, Bjorkqvist AM, Autio K, Tarkkanen M, Wolf M, Monni O, Szymanska J, Larramendy ML, Tapper J, Pere H, El-Rifai W, Hemmer S, Wasenius VM, Vidgren V, Zhu Y. 1998. DNA copy number amplifications in human neoplasms: review of comparative genomic hybridization studies. Am J Pathol 152: 1107–1123.
- Knuutila S, Aalto Y, Autio K, Bjorkqvist AM, El-Rifai W, Hemmer S, Huhta T, Kettunen E, Kiuru-Kuhlefelt S, Larramendy ML, Lushnikova T, Monni O, Pere H, Tapper J, Tarkkanen M, Varis A, Wasenius VM, Wolf M, Zhu Y. 1999. DNA copy number losses in human neoplasms. Am J Pathol 155: 683–694.
- Lengauer C, Kinzler KW, Vogelstein B. 1998. Genetic instabilities in human cancers. Nature 396: 643–649.
- McDonnell TJ, Deane N, Platt FM, Nunez G, Jaeger U, McKearn JP, Korsmeyer SJ. 1989. bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell 57: 79–88.
- Monni O, Joensuu H, Franssila K, Knuutila S. 1996. DNA copy number changes in diffuse large B-cell lymphoma—comparative genomic hybridization study. Blood 87: 5269–5278.
- Monni O, Joensuu H, Franssila K, Klefstrom J, Alitalo K, Knuutila S. 1997. BCL2 overexpression associated with chromosomal amplification in diffuse large B-cell lymphoma. Blood 90: 1168–1174.
- Offit K, Parsa NZ, Gaidano G, Filippa DA, Louie D, Pan D, Jhanwar SC, Dalla-Favera R, Chaganti RSK. 1993. 6q deletions define distinct clinico-pathologic subsets of non-Hodgkin's lymphoma. Blood 82: 2157–2162.
- Rao PH, Houldsworth J, Dyomina K, Parsa NZ, Cigudosa JC, Louie DC, Popplewell L, Offit K, Jhanwar SC, Chaganti RSK. 1998. Chromosomal and gene amplification in diffuse large B-cell lymphoma. Blood 92: 234–240.
- Tilly H, Rossi A, Stamatoullas A, Lenormand B, Bigorgne C, Kunlin A, Monconduit M, Bastard C. 1994. Prognostic value of chromosomal abnormalities in follicular lymphoma. Blood 84: 1043–1049.
- Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM. 1984. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 226: 1097–1099.
- Werner CA, Dohner H, Joos S, Trumper LH, Baudis M, Barth TF, Ott G, Moller P, Lichter P, Bentz M. 1997. High-level DNA amplifications are common genetic aberrations in B-cell neoplasms. Am J Pathol 151: 335–342.
- Yuen AR, Kamel OW, Halpern J, Horning SJ. 1995. Long-term survival after histologic transformation of low-grade follicular lymphoma. J Clin Oncol 13: 1726–1733.
- Yunis JJ, Frizzera G, Oken MM, McKenna J, Theologides A, Arnesen M. 1987. Multiple recurrent genomic defects in follicular lymphoma. A possible model for cancer. N Engl J Med 316: 79–84.
-
Zhang Y,
Weber-Matthiesen K,
Siebert R,
Matthiesen P,
Schlegelberger B.
1997.
Frequent deletions of 6q23-24 in B-cell non-Hodgkin's lymphomas detected by fluorescence in situ hybridization.
Genes Chromosomes Cancer
18:
310–313.
10.1002/(SICI)1098-2264(199704)18:4<310::AID-GCC10>3.0.CO;2-K CAS PubMed Web of Science® Google Scholar
-
Zhang Y,
Matthiesen P,
Harder S,
Siebert R,
Castoldi G,
Calasanz MJ,
Wong KF,
Rosenwald A,
Ott G,
Atkin NB,
Schlegelberger B.
2000.
A 3-cM commonly deleted region in 6q21 in leukemias and lymphomas delineated by fluorescence in situ hybridization.
Genes Chromosomes Cancer
27:
52–58.
10.1002/(SICI)1098-2264(200001)27:1<52::AID-GCC7>3.0.CO;2-X CAS PubMed Web of Science® Google Scholar