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Original Article

Gene Expression Profiling of B Cell Chronic Lymphocytic Leukemia Reveals a Homogeneous Phenotype Related to Memory B Cells

¹ Institute for Cancer Genetics, Departments of Pathology and Genetics & Development, Columbia University, New York, NY 10032
² IBM T.J. Watson Research Center, Yorktown Heights, New York, NY 10598
³ Department of Adult Oncology Dana-Farber Cancer Institute, Department of Medicine, Harvard Medical School, Boston, MA 02115
⁴ Department of Pathology, New York University Medical Center, New York, NY 10016
⁵ Ematologia 1, Department of Hematology, Ospedale Maggiore, I.R.C.C.S., Milan 20122, Italy
⁶ First Genetic Trust, Inc., Lyndhurst, NJ 07071

Address correspondence to Riccardo Dalla-Favera, Institute for Cancer Genetics, Columbia University, 1150 St. Nicholas Ave., New York, NY 10032. Phone: 212-304-7381; Fax: 212-304-5537; E-mail: rd10{at}columbia.edu

B cell–derived chronic lymphocytic leukemia (B-CLL) represents a common malignancy whose cell derivation and pathogenesis are unknown. Recent studies have shown that >50% of CLLs display hypermutated immunoglobulin variable region (IgV) sequences and a more favorable prognosis, suggesting that they may represent a distinct subset of CLLs which have transited through germinal centers (GCs), the physiologic site of IgV hypermutation. To further investigate the phenotype of CLLs, their cellular derivation and their relationship to normal B cells, we have analyzed their gene expression profiles using oligonucleotide-based DNA chip microarrays representative of 12,000 genes. The results show that CLLs display a common and characteristic gene expression profile that is largely independent of their IgV genotype. Nevertheless, a restricted number of genes (<30) have been identified whose differential expression can distinguish IgV mutated versus unmutated cases and identify them in independent panels of cases. Comparison of CLL profiles with those of purified normal B cell subpopulations indicates that the common CLL profile is more related to memory B cells than to those derived from naive B cells, CD5⁺ B cells, and GC centroblasts and centrocytes. Finally, this analysis has identified a subset of genes specifically expressed by CLL cells of potential pathogenetic and clinical relevance.

Key Words: somatic hypermutation • germinal center • CD5 • DNA microarray • cluster analysis

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• Pasqualucci, L., Guglielmino, R., Houldsworth, J., Mohr, J., Aoufouchi, S., Polakiewicz, R., Chaganti, R. S. K., Dalla-Favera, R. (2004). Expression of the AID protein in normal and neoplastic B cells. Blood 104: 3318-3325 [Abstract] [Full Text]  
• Shen, Y., Iqbal, J., Huang, J. Z., Zhou, G., Chan, W. C. (2004). BCL2 protein expression parallels its mRNA level in normal and malignant B cells. Blood 104: 2936-2939 [Abstract] [Full Text]  
• Rodriguez, A., Martinez, N., Camacho, F. I., Ruiz-Ballesteros, E., Algara, P., Garcia, J.-F., Menarguez, J., Alvaro, T., Fresno, M. F., Solano, F., Mollejo, M., Martin, C., Piris, M. A. (2004). Variability in the Degree of Expression of Phosphorylated I{kappa}B{alpha} in Chronic Lymphocytic Leukemia Cases With Nodal Involvement. Clin. Cancer Res. 10: 6796-6806 [Abstract] [Full Text]  
• Widhopf, G. F. II, Rassenti, L. Z., Toy, T. L., Gribben, J. G., Wierda, W. G., Kipps, T. J. (2004). Chronic lymphocytic leukemia B cells of more than 1% of patients express virtually identical immunoglobulins. Blood 104: 2499-2504 [Abstract] [Full Text]  
• Haslinger, C., Schweifer, N., Stilgenbauer, S., Dohner, H., Lichter, P., Kraut, N., Stratowa, C., Abseher, R. (2004). Microarray Gene Expression Profiling of B-Cell Chronic Lymphocytic Leukemia Subgroups Defined by Genomic Aberrations and VH Mutation Status. JCO 22: 3937-3949 [Abstract] [Full Text]  
• Rassenti, L. Z., Huynh, L., Toy, T. L., Chen, L., Keating, M. J., Gribben, J. G., Neuberg, D. S., Flinn, I. W., Rai, K. R., Byrd, J. C., Kay, N. E., Greaves, A., Weiss, A., Kipps, T. J. (2004). ZAP-70 Compared with Immunoglobulin Heavy-Chain Gene Mutation Status as a Predictor of Disease Progression in Chronic Lymphocytic Leukemia. NEJM 351: 893-901 [Abstract] [Full Text]  
• Lopez-Giral, S., Quintana, N. E., Cabrerizo, M., Alfonso-Perez, M., Sala-Valdes, M., de Soria, V. G. G., Fernandez-Ranada, J. M., Fernandez-Ruiz, E., Munoz, C. (2004). Chemokine receptors that mediate B cell homing to secondary lymphoid tissues are highly expressed in B cell chronic lymphocytic leukemia and non-Hodgkin lymphomas with widespread nodular dissemination. J. Leukoc. Biol. 76: 462-471 [Abstract] [Full Text]  
• Stevenson, F. K., Caligaris-Cappio, F. (2004). Chronic lymphocytic leukemia: revelations from the B-cell receptor. Blood 103: 4389-4395 [Abstract] [Full Text]  
• Messmer, B. T., Albesiano, E., Messmer, D., Chiorazzi, N. (2004). The pattern and distribution of immunoglobulin VH gene mutations in chronic lymphocytic leukemia B cells are consistent with the canonical somatic hypermutation process. Blood 103: 3490-3495 [Abstract] [Full Text]  
• Tiwari, S., Felekkis, K., Moon, E.-Y., Flies, A., Sherr, D. H., Lerner, A. (2004). Among circulating hematopoietic cells, B-CLL uniquely expresses functional EPAC1, but EPAC1-mediated Rap1 activation does not account for PDE4 inhibitor-induced apoptosis. Blood 103: 2661-2667 [Abstract] [Full Text]  
• Thieblemont, C., Nasser, V., Felman, P., Leroy, K., Gazzo, S., Callet-Bauchu, E., Loriod, B., Granjeaud, S., Gaulard, P., Haioun, C., Traverse-Glehen, A., Baseggio, L., Bertucci, F., Birnbaum, D., Magrangeas, F., Minvielle, S., Avet-Loiseau, H., Salles, G., Coiffier, B., Berger, F., Houlgatte, R. (2004). Small lymphocytic lymphoma, marginal zone B-cell lymphoma, and mantle cell lymphoma exhibit distinct gene-expression profiles allowing molecular diagnosis. Blood 103: 2727-2737 [Abstract] [Full Text]  
• Chiaretti, S., Li, X., Gentleman, R., Vitale, A., Vignetti, M., Mandelli, F., Ritz, J., Foa, R. (2004). Gene expression profile of adult T-cell acute lymphocytic leukemia identifies distinct subsets of patients with different response to therapy and survival. Blood 103: 2771-2778 [Abstract] [Full Text]  
• Ghia, P., Prato, G., Scielzo, C., Stella, S., Geuna, M., Guida, G., Caligaris-Cappio, F. (2004). Monoclonal CD5+ and CD5- B-lymphocyte expansions are frequent in the peripheral blood of the elderly. Blood 103: 2337-2342 [Abstract] [Full Text]  
• Hoyer, K. K., Pang, M., Gui, D., Shintaku, I. P., Kuwabara, I., Liu, F.-T., Said, J. W., Baum, L. G., Teitell, M. A. (2004). An Anti-Apoptotic Role for Galectin-3 in Diffuse Large B-Cell Lymphomas. Am. J. Pathol. 164: 893-902 [Abstract] [Full Text]  
• He, B., Chadburn, A., Jou, E., Schattner, E. J., Knowles, D. M., Cerutti, A. (2004). Lymphoma B Cells Evade Apoptosis through the TNF Family Members BAFF/BLyS and APRIL. J. Immunol. 172: 3268-3279 [Abstract] [Full Text]  
• Shanafelt, T. D., Call, T. G. (2004). Current Approach to Diagnosis and Management of Chronic Lymphocytic Leukemia. Mayo Clin Proc. 79: 388-398 [Abstract]  
• Parrado, A., Robledo, M., Moya-Quiles, M. R., Marin, L. A., Chomienne, C., Padua, R. A., Alvarez-Lopez, M. R. (2004). The promyelocytic leukemia zinc finger protein down-regulates apoptosis and expression of the proapoptotic BID protein in lymphocytes. Proc. Natl. Acad. Sci. USA 101: 1898-1903 [Abstract] [Full Text]  
• Shanafelt, T. D., Geyer, S. M., Kay, N. E. (2004). Prognosis at diagnosis: integrating molecular biologic insights into clinical practice for patients with CLL. Blood 103: 1202-1210 [Abstract] [Full Text]  
• Damle, R. N., Batliwalla, F. M., Ghiotto, F., Valetto, A., Albesiano, E., Sison, C., Allen, S. L., Kolitz, J., Vinciguerra, V. P., Kudalkar, P., Wasil, T., Rai, K. R., Ferrarini, M., Gregersen, P. K., Chiorazzi, N. (2004). Telomere length and telomerase activity delineate distinctive replicative features of the B-CLL subgroups defined by immunoglobulin V gene mutations. Blood 103: 375-382 [Abstract] [Full Text]  
• Kern, C., Cornuel, J.-F., Billard, C., Tang, R., Rouillard, D., Stenou, V., Defrance, T., Ajchenbaum-Cymbalista, F., Simonin, P.-Y., Feldblum, S., Kolb, J.-P. (2004). Involvement of BAFF and APRIL in the resistance to apoptosis of B-CLL through an autocrine pathway. Blood 103: 679-688 [Abstract] [Full Text]  
• Basso, K., Liso, A., Tiacci, E., Benedetti, R., Pulsoni, A., Foa, R., Di Raimondo, F., Ambrosetti, A., Califano, A., Klein, U., Favera, R. D., Falini, B. (2004). Gene Expression Profiling of Hairy Cell Leukemia Reveals a Phenotype Related to Memory B Cells with Altered Expression of Chemokine and Adhesion Receptors. JEM 199: 59-68 [Abstract] [Full Text]  
• Politi, K., Szabolcs, M., Fisher, P., Kljuic, A., Ludwig, T., Efstratiadis, A. (2004). A Mouse Model of Uterine Leiomyosarcoma. Am. J. Pathol. 164: 325-336 [Abstract] [Full Text]  
• Byrd, J. C., Stilgenbauer, S., Flinn, I. W. (2004). Chronic Lymphocytic Leukemia. ASH Education Book 2004: 163-183 [Abstract] [Full Text]  
• Stankovic, T., Hubank, M., Cronin, D., Stewart, G. S., Fletcher, D., Bignell, C. R., Alvi, A. J., Austen, B., Weston, V. J., Fegan, C., Byrd, P. J., Moss, P. A. H., Taylor, A. M. R. (2004). Microarray analysis reveals that TP53- and ATM-mutant B-CLLs share a defect in activating proapoptotic responses after DNA damage but are distinguished by major differences in activating prosurvival responses. Blood 103: 291-300 [Abstract] [Full Text]  
• Cochran, D. A. E., Evans, C. A., Blinco, D., Burthem, J., Stevenson, F. K., Gaskell, S. J., Whetton, A. D. (2003). Proteomic Analysis of Chronic Lymphocytic Leukemia Subtypes with Mutated or Unmutated Ig VH Genes. Mol. Cell. Proteomics 2: 1331-1341 [Abstract] [Full Text]  
• Capello, D., Cerri, M., Muti, G., Berra, E., Oreste, P., Deambrogi, C., Rossi, D., Dotti, G., Conconi, A., Vigano, M., Magrini, U., Ippoliti, G., Morra, E., Gloghini, A., Rambaldi, A., Paulli, M., Carbone, A., Gaidano, G. (2003). Molecular histogenesis of posttransplantation lymphoproliferative disorders. Blood 102: 3775-3785 [Abstract] [Full Text]  
• Kienle, D., Krober, A., Katzenberger, T., Ott, G., Leupolt, E., Barth, T. F. E., Moller, P., Benner, A., Habermann, A., Muller-Hermelink, H. K., Bentz, M., Lichter, P., Dohner, H., Stilgenbauer, S. (2003). VH mutation status and VDJ rearrangement structure in mantle cell lymphoma: correlation with genomic aberrations, clinical characteristics, and outcome. Blood 102: 3003-3009 [Abstract] [Full Text]  

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