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ABSTRACT

Background The survival of patients with diffuse large-B-cell lymphoma after chemotherapy is influenced by molecular features of the tumors. We used the gene-expression profiles of these lymphomas to develop a molecular predictor of survival.

Methods Biopsy samples of diffuse large-B-cell lymphoma from 240 patients were examined for gene expression with the use of DNA microarrays and analyzed for genomic abnormalities. Subgroups with distinctive gene-expression profiles were defined on the basis of hierarchical clustering. A molecular predictor of risk was constructed with the use of genes with expression patterns that were associated with survival in a preliminary group of 160 patients and was then tested in a validation group of 80 patients. The accuracy of this predictor was compared with that of the international prognostic index.

Results Three gene-expression subgroups — germinal-center B-cell–like, activated B-cell–like, and type 3 diffuse large-B-cell lymphoma — were identified. Two common oncogenic events in diffuse large-B-cell lymphoma, bcl-2 translocation and c-rel amplification, were detected only in the germinal-center B-cell–like subgroup. Patients in this subgroup had the highest five-year survival rate. To identify other molecular determinants of outcome, we searched for individual genes with expression patterns that correlated with survival in the preliminary group of patients. Most of these genes fell within four gene-expression signatures characteristic of germinal-center B cells, proliferating cells, reactive stromal and immune cells in the lymph node, or major-histocompatibility-complex class II complex. We used 17 genes to construct a predictor of overall survival after chemotherapy. This gene-based predictor and the international prognostic index were independent prognostic indicators.

Conclusions DNA microarrays can be used to formulate a molecular predictor of survival after chemotherapy for diffuse large-B-cell lymphoma.

Source Information

From the Metabolism Branch, Center for Cancer Research (A.R., L.M.S.), and the Biometric Research Branch, Division of Cancer Treatment and Diagnosis (G.W.), National Cancer Institute, National Institutes of Health, Bethesda, Md.; the Department of Pathology and Microbiology, University of Nebraska Medical Center, Omaha (W.C.C.); British Columbia Cancer Center, Vancouver, B.C., Canada (J.M.C., R.D.G.); Hospital Clinic, University of Barcelona, Barcelona, Spain (E.C.); Southwest Oncology Group and James P. Wilmot Cancer Center, University of Rochester School of Medicine, Rochester, N.Y. (R.I.F.); the Department of Pathology, University of Würzburg, Würzburg, Germany (H.K.M.-H.); and the Department of Immunology, Norwegian Radium Hospital, Oslo, Norway (E.B.S.).

Other authors were Jena M. Giltnane, B.S., Elaine M. Hurt, Ph.D., Hong Zhao, M.S., Lauren Averett, B.A., Liming Yang, Ph.D., Wyndham H. Wilson, M.D., Ph.D., Elaine S. Jaffe, M.D., Richard Simon, D.Sc., and Richard D. Klausner, M.D., National Cancer Institute, National Institutes of Health (NIH), Bethesda, Md.; John Powell, M.S., Center for Information Technology, NIH, Bethesda, Md.; Patricia L. Duffey, R.N., and Dan L. Longo, M.D., National Institute on Aging, NIH Gerontology Research Center, Baltimore; Timothy C. Greiner, M.D., Dennis D. Weisenburger, M.D., Warren G. Sanger, Ph.D., Bhavana J. Dave, Ph.D., James C. Lynch, Ph.D., Julie Vose, M.D., and James O. Armitage, M.D., University of Nebraska Medical Center, Omaha; Emilio Montserrat, M.D., and Armando López-Guillermo, M.D., Hospital Clinic, University of Barcelona, Barcelona, Spain; Thomas M. Grogan, M.D., and Thomas P. Miller, M.D., Southwest Oncology Group and University of Arizona Cancer Center, Tucson; Michel LeBlanc, Ph.D., Southwest Oncology Group and Fred Hutchinson Cancer Research Center, Seattle; German Ott, M.D., University of Würzburg, Würzburg, Germany; and Stein Kvaloy, M.D., Ph.D., Jan Delabie, M.D., Ph.D., Harald Holte, M.D., Ph.D., Peter Krajci, M.D., Ph.D., and Trond Stokke, Ph.D., Norwegian Radium Hospital, Oslo, Norway.

Address reprint requests to Dr. Staudt at the Metabolism Branch, Center for Cancer Research, National Cancer Institute, Bldg. 10, Rm. 4N114, National Institutes of Health, Bethesda, MD 20892, or at lstaudt{at}mail.nih.gov.

Full Text of this Article

Related Letters:

Molecular Profiling of Lymphoma
Akhtar S., Copur M. S., Ledakis P., Bolton M., Staudt L. M., the Lymphoma/Leukemia Molecular Profiling Project
Extract | Full Text | PDF  
N Engl J Med 2002; 347:1376-1377, Oct 24, 2002. Correspondence

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• Montes-Moreno, S., Roncador, G., Maestre, L., Martinez, N., Sanchez-Verde, L., Camacho, F. I., Cannata, J., Martinez-Torrecuadrada, J. L., Shen, Y., Chan, W. C., Piris, M. A. (2008). Gcet1 (centerin), a highly restricted marker for a subset of germinal center-derived lymphomas. Blood 111: 351-358 [Abstract] [Full Text]  
• Belguise, K., Guo, S., Yang, S., Rogers, A. E., Seldin, D. C., Sherr, D. H., Sonenshein, G. E. (2007). Green Tea Polyphenols Reverse Cooperation between c-Rel and CK2 that Induces the Aryl Hydrocarbon Receptor, Slug, and an Invasive Phenotype. Cancer Res. 67: 11742-11750 [Abstract] [Full Text]  
• Young, K. H., Weisenburger, D. D., Dave, B. J., Smith, L., Sanger, W., Iqbal, J., Campo, E., Delabie, J., Gascoyne, R. D., Ott, G., Rimsza, L., Muller-Hermelink, H. K., Jaffe, E. S., Rosenwald, A., Staudt, L. M., Chan, W. C., Greiner, T. C. (2007). Mutations in the DNA-binding codons of TP53, which are associated with decreased expression of TRAILreceptor-2, predict for poor survival in diffuse large B-cell lymphoma. Blood 110: 4396-4405 [Abstract] [Full Text]  
• Grogg, K L, Miller, R F, Dogan, A (2007). HIV infection and lymphoma. J. Clin. Pathol. 60: 1365-1372 [Abstract] [Full Text]  
• Cillessen, S. A.G.M., Hess, C. J., Hooijberg, E., Castricum, K. C.M., Kortman, P., Denkers, F., Vos, W., van de Wiel, M. A., Schuurhuis, G. J., Ossenkoppele, G. J., Meijer, C. J.L.M., Oudejans, J. J. (2007). Inhibition of the Intrinsic Apoptosis Pathway Downstream of Caspase-9 Activation Causes Chemotherapy Resistance in Diffuse Large B-Cell Lymphoma. Clin. Cancer Res. 13: 7012-7021 [Abstract] [Full Text]  
• Lofstrom, B, Backlin, C, Sundstrom, C, Ekbom, A, Lundberg, I E (2007). A closer look at non-Hodgkin's lymphoma cases in a national Swedish systemic lupus erythematosus cohort: a nested case-control study. Ann Rheum Dis 66: 1627-1632 [Abstract] [Full Text]  
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• Pitini, V., Arrigo, C., Altavilla, G. (2007). Gene Expression Profiling Does Not Identify Molecular Subgroup Among Nodal Peripheral T-Cell Lymphomas. JCO 25: 4851-4851 [Full Text]  
• Cuadros, M., Honrado, E., Zajac, M., Benitez, J., Martinez-Delgado, B., Dave, S. S., Staudt, L. M., Jaffe, E. S., Milne, R., Alves, J., Rodriguez, J. (2007). In Reply. JCO 25: 4851-4852 [Full Text]  
• Minna, J. D., Girard, L., Xie, Y. (2007). Tumor mRNA Expression Profiles Predict Responses to Chemotherapy. JCO 25: 4329-4336 [Full Text]  
• Hsu, D. S., Balakumaran, B. S., Acharya, C. R., Vlahovic, V., Walters, K. S., Garman, K., Anders, C., Riedel, R. F., Lancaster, J., Harpole, D., Dressman, H. K., Nevins, J. R., Febbo, P. G., Potti, A. (2007). Pharmacogenomic Strategies Provide a Rational Approach to the Treatment of Cisplatin-Resistant Patients With Advanced Cancer. JCO 25: 4350-4357 [Abstract] [Full Text]  
• Le Gouill, S., Talmant, P., Touzeau, C., Moreau, A., Garand, R., Juge-Morineau, N., Gaillard, F., Gastinne, T., Milpied, N., Moreau, P., Harousseau, J. L., Avet-Loiseau, H. (2007). The clinical presentation and prognosis of diffuse large B-cell lymphoma with t(14;18) and 8q24/c-MYC rearrangement. haematol 92: 1335-1342 [Abstract] [Full Text]  
• Prakash, S., Swerdlow, S. H (2007). Nodal aggressive B-cell lymphomas: a diagnostic approach. J. Clin. Pathol. 60: 1076-1085 [Abstract] [Full Text]  
• Parekh, S., Polo, J. M., Shaknovich, R., Juszczynski, P., Lev, P., Ranuncolo, S. M., Yin, Y., Klein, U., Cattoretti, G., Favera, R. D., Shipp, M. A., Melnick, A. (2007). BCL6 programs lymphoma cells for survival and differentiation through distinct biochemical mechanisms. Blood 110: 2067-2074 [Abstract] [Full Text]  
• Mueller, C. G., Boix, C., Kwan, W.-H., Daussy, C., Fournier, E., Fridman, W. H., Molina, T. J. (2007). Critical role of monocytes to support normal B cell and diffuse large B cell lymphoma survival and proliferation. J. Leukoc. Biol. 82: 567-575 [Abstract] [Full Text]  
• Nakamura, T., Kuwai, T., Kitadai, Y., Sasaki, T., Fan, D., Coombes, K. R., Kim, S.-J., Fidler, I. J. (2007). Zonal Heterogeneity for Gene Expression in Human Pancreatic Carcinoma. Cancer Res. 67: 7597-7604 [Abstract] [Full Text]  
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• Chung, R., Lai, R., Wei, P., Lee, J., Hanson, J., Belch, A. R., Turner, A. R., Reiman, T. (2007). Concordant but not discordant bone marrow involvement in diffuse large B-cell lymphoma predicts a poor clinical outcome independent of the International Prognostic Index. Blood 110: 1278-1282 [Abstract] [Full Text]  
• Klapper, W., Hoster, E., Rolver, L., Schrader, C., Janssen, D., Tiemann, M., Bernd, H.-W., Determann, O., Hansmann, M.-L., Moller, P., Feller, A., Stein, H., Wacker, H.-H., Dreyling, M., Unterhalt, M., Hiddemann, W., Ott, G. (2007). Tumor Sclerosis but Not Cell Proliferation or Malignancy Grade Is a Prognostic Marker in Advanced-Stage Follicular Lymphoma: The German Low Grade Lymphoma Study Group. JCO 25: 3330-3336 [Abstract] [Full Text]  
• Cuadros, M., Dave, S. S., Jaffe, E. S., Honrado, E., Milne, R., Alves, J., Rodriguez, J., Zajac, M., Benitez, J., Staudt, L. M., Martinez-Delgado, B. (2007). Identification of a Proliferation Signature Related to Survival in Nodal Peripheral T-Cell Lymphomas. JCO 25: 3321-3329 [Abstract] [Full Text]  
• Park, S., Lee, J., Ko, Y. H., Han, A., Jun, H. J., Lee, S. C., Hwang, I. G., Park, Y. H., Ahn, J. S., Jung, C. W., Kim, K., Ahn, Y. C., Kang, W. K., Park, K., Kim, W. S. (2007). The impact of Epstein-Barr virus status on clinical outcome in diffuse large B-cell lymphoma. Blood 110: 972-978 [Abstract] [Full Text]  
• Wong, H. R., Shanley, T. P., Sakthivel, B., Cvijanovich, N., Lin, R., Allen, G. L., Thomas, N. J., Doctor, A., Kalyanaraman, M., Tofil, N. M., Penfil, S., Monaco, M., Tagavilla, M. A., Odoms, K., Dunsmore, K., Barnes, M., Aronow, B. J., for the Genomics of Pediatric SIRS/Septic Shock In, (2007). Genome-level expression profiles in pediatric septic shock indicate a role for altered zinc homeostasis in poor outcome. Physiol. Genomics 30: 146-155 [Abstract] [Full Text]  
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• Morton, L. M., Turner, J. J., Cerhan, J. R., Linet, M. S., Treseler, P. A., Clarke, C. A., Jack, A., Cozen, W., Maynadie, M., Spinelli, J. J., Costantini, A. S., Rudiger, T., Scarpa, A., Zheng, T., Weisenburger, D. D. (2007). Proposed classification of lymphoid neoplasms for epidemiologic research from the Pathology Working Group of the International Lymphoma Epidemiology Consortium (InterLymph). Blood 110: 695-708 [Abstract] [Full Text]  
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• Plonquet, A, Haioun, C, Jais, J-P, Debard, A-L, Salles, G, Bene, M-C, Feugier, P, Rabian, C, Casasnovas, O, Labalette, M, Kuhlein, E, Farcet, J-P, Emile, J-F, Gisselbrecht, C, Delfau-Larue, M-H, On behalf of GELA (Groupe d'etude des lymphomes de, (2007). Peripheral blood natural killer cell count is associated with clinical outcome in patients with aaIPI 2 3 diffuse large B-cell lymphoma. Ann Oncol 18: 1209-1215 [Abstract] [Full Text]  
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