Cytogenetic features of de novo CD5-positive diffuse large B-cell lymphoma: Chromosome aberrations affecting 8p21 and 11q13 constitute major subgroups with different overall survival
Tomoko Yoshioka
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Search for more papers by this authorCorresponding Author
Ikuo Miura
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Third Department of Internal Medicine, Akita University School of Medicine, 1-1-1, Hondo, Akita 010-8543, JapanSearch for more papers by this authorMasaaki Kume
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Search for more papers by this authorNaoto Takahashi
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Search for more papers by this authorMasataka Okamoto
Department of Internal Medicine, Fujita Health University School of Medicine, Toyoake, Japan
Search for more papers by this authorRyo Ichinohasama
Department of Oral Pathology, Tohoku University School of Medicine, Sendai, Japan
Search for more papers by this authorTadashi Yoshino
Department of Pathology, Okayama University School of Medicine, Okayama, Japan
Search for more papers by this authorMotoko Yamaguchi
Second Department of Internal Medicine, Mie University School of Medicine, Tsu, Japan
Search for more papers by this authorMakoto Hirokawa
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Search for more papers by this authorKen-ichi Sawada
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Search for more papers by this authorShigeo Nakamura
Department of Pathology and Molecular Diagnostics, Aichi Cancer Center, Nagoya, Japan
Search for more papers by this authorTomoko Yoshioka
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Search for more papers by this authorCorresponding Author
Ikuo Miura
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Third Department of Internal Medicine, Akita University School of Medicine, 1-1-1, Hondo, Akita 010-8543, JapanSearch for more papers by this authorMasaaki Kume
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Search for more papers by this authorNaoto Takahashi
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Search for more papers by this authorMasataka Okamoto
Department of Internal Medicine, Fujita Health University School of Medicine, Toyoake, Japan
Search for more papers by this authorRyo Ichinohasama
Department of Oral Pathology, Tohoku University School of Medicine, Sendai, Japan
Search for more papers by this authorTadashi Yoshino
Department of Pathology, Okayama University School of Medicine, Okayama, Japan
Search for more papers by this authorMotoko Yamaguchi
Second Department of Internal Medicine, Mie University School of Medicine, Tsu, Japan
Search for more papers by this authorMakoto Hirokawa
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Search for more papers by this authorKen-ichi Sawada
Third Department of Internal Medicine, Akita University School of Medicine, Akita, Japan
Search for more papers by this authorShigeo Nakamura
Department of Pathology and Molecular Diagnostics, Aichi Cancer Center, Nagoya, Japan
Search for more papers by this authorAbstract
De novo CD5-positive diffuse large B-cell lymphoma (CD5+DLBCL) is regarded as a different clinicopathological entity from CD5-negative DLBCL (CD5−DLBCL) and mantle cell lymphoma (MCL). Because only a few published cytogenetic studies of de novo CD5+DLBCL are available, we investigated chromosomal changes in 23 Japanese patients who had de novo CD5+DLBCL. A characteristic of cytogenetic abnormalities in de novo CD5+DLBCL was a high incidence of chromosomal aberrations affecting 8p21 and 11q13. Major chromosomal breakpoints were concentrated at 8p21, 11q13, and 3q27. Patients with 8p21 aberrations showed aggressive clinical features, including advanced stage of disease, elevated serum LDH level, poor performance status, and an inferior survival curve compared with patients who had 11q13 changes (P = .043). Chromosomal abnormalities of both 8p21 and 11q13 were not observed in the same patient, and each abnormality showed different chromosomal gains and losses. These results indicate that de novo CD5+DLBCL may occur in previously unidentified subgroups that differ in their chromosomal abnormalities. The conflicting results of previous studies on prognosis may thus be explained in part by the differences in chromosomal changes. © 2004 Wiley-Liss, Inc.
REFERENCES
- Bastard C, Deweindt C, Kerckaert JP, Lenormand B, Rossi A, Pezzella F, Fruchart C, Duval C, Monconduit M, Tilly H. 1994. LAZ3 rearrangements in non-Hodgkin's lymphoma: correlation with histology, immunophenotype, karyotype, and clinical outcome in 217 patients. Blood 83: 2423–2427.
-
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
- Colomo L, Lopez-Guillermo A, Perales M, Rives S, Martinez A, Bosch F, Colomer D, Falini B, Montserrat E, Campo E. 2003. Clinical impact of the differentiation profile assessed by immunophenotyping in patients with diffuse large B-cell lymphoma. Blood 101: 78–84.
- Gascoyne RD, Dave S, Zettle A, Bea S, Chan WC, Rosenwald A, Jaffe ES, Campo E, Delabie J, Weisenburger D, Greiner TC, Ott G, Muller-Hermelink K, Rimsza L, Hans C, Connors JM, Wright G, Staudt LM. 2003. Gene expression microarray analysis of de novo CD5+ diffuse large B-cell lymphoma (LLMPP Study): a distinct entity? [abstract]. Blood 102: 178a.
- Harada S, Suzuki R, Uehira K, Yatabe Y, Kagami Y, Ogura M, Suzuki H, Oyama A, Kodera Y, Ueda R, Morishima Y, Nakamura S, Seto M. 1999. Molecular and immunological dissection of diffuse large B cell lymphoma: CD5+, and CD5− with CD10+ groups may constitute clinically relevant subtypes. Leukemia 13: 1441–1447.
- Hashimoto K, Miura I, Chyubachi A, Saito M, Miura AB. 1995. Correlations of chromosome abnormalities with histologic and immunologic characteristics in 49 patients from Akita, Japan with non-Hodgkin lymphoma. Cancer Genet Cytogenet 81: 56–65.
- Ichikawa A, Kinoshita T, Watanabe T, Kato H, Nagai H., Tsushita K, Saito H, Hotta, T. 1997. Mutations of the p53 gene as a prognostic factor in aggressive B-cell lymphoma. N Engl J Med 337: 529–534.
- Inaba T, Shimazaki C, Sumikuma T, Okano A, Hatsuse M, Okamoto A, Takahashi R, Ashihara E, Hibi S, Sudo Y, Yamagata N, Murakami S, Rin K, Fujita N, Yoshimura M, Nakagawa M. 2000. Expression of T-cell-associated antigens in B-cell non-Hodgkin's lymphoma. Br J Haematol 109: 592–599.
- The International Non-Hodgkin's Lymphoma Prognostic Factors Project. 1993. A predictive model for aggressive non-Hodgkin's lymphoma. N Engl J Med 329: 987–994.
- ISCN. 1995. An international system for human cytogenetic nomenclature. F Mitelman, editor. Basel, Switzerland: Karger.
- ES Jaffe, NL Harris, H Stein, JW Vardiman, editors. 2001. World Health Organization classification of tumours. Pathology and genetics. Tumours of haematopoietic and lymphoid tissues. Lyon, France: IARC Press.
- Karnan S, Tagawa H, Suzuki R, Suguro M, Yamaguchi M, Okamoto M, Morishima Y, Nakamura S, Seto M. 2004. Analysis of chromosomal imbalances in de novo CD5-positive diffuse large-B-cell lymphoma detected by comparative genomic hybridization. Genes Chromosomes Cancer 39: 77–81.
- Katzenberger T, Lohr A, Schwarz S, Dreyling M, Schoof J, Nickenig C, Stilgenbauer S, Kalla J, Ott MM, Muller-Hermelink HK, Ott G. 2003. Genetic analysis of de novo CD5+ diffuse large B-cell lymphomas suggests an origin from a somatically mutated CD5+ progenitor B cell. Blood 101: 699–702.
- Kobayashi T, Yamaguchi M, Kim S, Morikawa J, Ogawa S, Ueno S, Suh E, Dougherty E, Shmulevich I, Shiku H, Zhang W. 2003. Microarray reveals differences in both tumors and vascular specific gene expression in de novo CD5+ and CD5− diffuse large B-cell lymphomas. Cancer Res 63: 60–66.
- Kroft SH, Howard MS, Picker LJ, Ansari MQ, Aquino DB, McKenna RW. 2000. De novo CD5+ diffuse large B-cell lymphomas. A heterogeneous group containing an unusual form of splenic lymphoma. Am J Clin Pathol 114: 523–533.
- Kume M, Suzuki R, Yatabe Y, Kagami Y, Miura I, Miura AB, Morishima Y, Nakamura S, Seto M. 1997. Somatic hypermutations in the VH segment of immunoglobulin genes of CD5-positive diffuse large B-cell lymphomas. Jpn J Cancer Res 88: 1087–1093.
- Linderoth J, Jerkeman M, Cavallin-Stahl E, Kvaloy S, Torlakovic E. 2003. Immunohistochemical expression of CD23 and CD40 may identify prognostically favorable subgroups of diffuse large B-cell lymphoma: a Nordic Lymphoma Group Study. Clin Cancer Res 9: 722–728.
- Martinez-Climent JA, Vizcarra E, Sanchez D, Blesa D, Marugan I, Benet I, Sole F, Rubio-Moscardo F, Terol MJ, Climent J, Sarsotti E, Tomo M, Andreu E, Salido M, Ruiz M, Prosper F, Siebert R, Dyer MJS, Garcia-Conde J. 2001. Loss of a novel tumor suppressor gene locus at chromosome 8p is associated with leukemia mantle cell lymphoma. Blood 98: 3479–3482.
- Matolcsy A, Chadburn A, Knowles DM. 1995. De novo CD5-positive and Richter's syndrome-associated diffuse large B cell lymphomas are genotypically distinct. Am J Pathol 147: 207–216.
- Murase T, Nakamura S, Kawauchi K, Matsuzaki H, Sakai C, Inaba T, Nasu K, Tashiro K, Suchi T, Saito H. 2000. An Asian variant of intravascular large B-cell lymphoma: clinical, pathological and cytogenetic approaches to diffuse large B-cell lymphoma associated with haemophagocytic syndrome. Br J Haematol 111: 826–834.
- Nakamura N, Kuze T, Hashimoto Y, Hara Y, Hoshi S, Sasaki Y, Shirakawa A, Sato M, Abe M. 2001. Analysis of the immunoglobulin heavy chain gene variable region of CD5-positive and -negative diffuse large B cell lymphoma. Leukemia 15: 452–457.
- Nanjangud G, Rao PH, Hegde A, Teruya-Feldstein J, Donnelly G, Qin J, Jhanwar SC, Zelenetz AD, Chaganti RSK. 2002. Spectral karyotyping identifies new rearrangements, translocations, and clinical associations in diffuse large B-cell lymphoma. Blood 99: 2554–2561.
- Niitsu N, Okabe-Kado J, Okamoto M, Takagi T, Yoshida T, Aoki S, Hirano M, Honma Y. 2001. Serum nm23–H1 protein as a prognostic factor in aggressive non-Hodgkin lymphoma. Blood 97: 1202–1210.
- Offit K, Lo Coco F, Louie DC, Parsa NZ, Leung D, Portlock C, Ye BH, Lista F, Filippa DA, Rosenbaum A, Ladanyi M, Jhanwar S, Dalla-Favera R, Chaganti RSK. 1994. Rearrangement of the bcl-6 gene as a prognostic marker in diffuse large-cell lymphoma. N Engl J Med 331: 74–80.
- Ohno H, Fukuhara S. 1997. Significance of rearrangement of the BCL6 gene in B-cell lymphoid neoplasms. Leuk Lymphoma 27: 53–63.
- Rosenwald A, Wright G, Chan WC, Connors JM, Campo E, Fisher RI, Gascoyne RD, Muller-Hermelink HK, Smeland EB, Giltnane JM, Hurt EM, Zhao H, Averett L, Yang L, Wilson WH, Jaffe ES, Simon R, Klausner RD, Powell J, Duffey PL, Longo DL, Greiner TC, Weisenburger DD, Sanger WG, Dave BJ, Lynch JC, Vose J, Armitage JO, Montserrat E, Lopez-Guillermo A, Grogan TM, Miller TP, LeBlanc M, Ott G, Kvaloy S, Delabie J, Holte H, Krajci P, Stokke T, Staudt LM. 2002. The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N Engl J Med 346: 1937–1947.
- Shimazaki C, Inaba T, Shimura K, Okamoto A, Takahashi R, Hirai H, Sudo Y, Ashihara E, Adachi Y, Murakami S, Saigo K, Fujita N, Nakagawa M. 1999. B-cell lymphoma associated with haemophagocytic syndrome: a clinical, immunological and cytogenetic study. Br J Haematol 104: 672–679.
- Shipp MA, Ross KN, Tamayo P, Weng A.P, Kutok JL, Aguiar RCT, Gaasenbeek M, Angelo M, Reich M, Pinkus GS, Ray TS, Koval MA, Last KW, Norton A, Lister TA, Mesirov J, Neuberg DS, Lander ES, Aster JC, Golub TR. 2002. Diffuse large B-cell lymphoma outcome prediction by gene-expression profiling and supervised machine learning. Nat Med 8: 68–74.
- Takahashi N, Chubachi A, Kume M, Hatano Y, Komatsuda A, Kawabata Y, Yanagiya N, Ichikawa Y, Miura AB, Miura I. 2001a. A clinical analysis of 52 adult patients with hemophagocytic syndrome: the prognostic significance of the underlying diseases. Int J Hematol 74: 209–213.
- Takahashi N, Miura I, Chubachi A, Miura AB, Nakamura S. 2001b. A clinicopathological study of 20 patients with T/natural killer (NK)-cell lymphoma-associated hemophagocytic syndrome with special reference to nasal and nasal-type NK/T-cell lymphoma. Int J Hematol 74: 303–308.
- Taniguchi M, Oka K, Hiasa A, Yamaguchi M, Ohno T, Kita K, Shiku H. 1998. De novo CD5+ diffuse large B-cell lymphomas express VH genes with somatic mutation. Blood 91: 1145–1151.
- Yamaguchi M, Ohno T, Oka K, Taniguchi M, Ito M, Kita K, Shiku H. 1999. De novo CD5-positive diffuse large B-cell lymphoma: clinical characteristics and therapeutic outcome. Br J Haematol 105: 1133–1139.
- Yamaguchi M., Seto M, Okamoto M, Ichinohasama R, Nakamura N, Yoshino T, Suzumiya J, Murase T, Miura I, Akasaka T, Tamaru J, Suzuki R, Kagami Y, Hirano M, Morishima Y, Ueda R, Shiku H, Nakamura S. 2002. De novo CD5+ diffuse large B-cell lymphoma: a clinicopathologic study of 109 patients. Blood 99: 815–821.
- Yatabe Y, Nakamura S, Seto M, Kuroda H, Kagami Y, Suzuki R, Ogura M, Kojima M, Koshikawa T, Ueda R, Suchi T. 1996. Clinicopathologic study of PRAD1/cyclin D1 overexpressing lymphoma with special reference to mantle cell lymphoma. A distinct molecular pathologic entity. Am J Surg Pathol 20: 1110–1122.
- Yatabe Y, Suzuki R, Tobinai K, Matsuno Y, Ichinohasama R, Okamoto M, Yamaguchi M, Tamaru J, Uike N, Hashimoto Y, Morishima Y, Suchi T, Seto M, Nakamura S. 2000. Significance of cyclin D1 overexpression for the diagnosis of mantle cell lymphoma: a clinicopathologic comparison of cyclin D1-positive MCL and cyclin D1-negative MCL-like B-cell lymphoma. Blood 95: 2253–2261.
- Zhang A, Ohshima K, Sato K, Kanda M, Suzumiya J, Shimazaki K, Kawasaki C, Kikuchi M. 1999. Prognostic clinicopathologic factors, including immunologic expression in diffuse large B-cell lymphomas. Pathol Int 49: 1043–1052.