Genome-wide DNA profiling better defines the prognosis of chronic lymphocytic leukaemia
Andrea Rinaldi
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
These authors contributed equally to this study.
Search for more papers by this authorMichael Mian
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Division of Haematology, Azienda Ospedaliera S. Maurizio, Bolzano/Bozen, Italy
These authors contributed equally to this study.
Search for more papers by this authorIvo Kwee
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Dalle Molle Institute for Artificial Intelligence (IDSIA), Manno, Switzerland
These authors contributed equally to this study.
Search for more papers by this authorDavide Rossi
Division of Haematology, Department of Clinical and Experimental Medicine and IRCAD, Amedeo Avogadro University of Eastern Piedmont, Novara
Search for more papers by this authorClara Deambrogi
Division of Haematology, Department of Clinical and Experimental Medicine and IRCAD, Amedeo Avogadro University of Eastern Piedmont, Novara
Search for more papers by this authorAfua A. Mensah
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Search for more papers by this authorFrancesco Forconi
Division of Haematology, Department of Clinical Medicine and Immunological Sciences, University of Siena and AOUS, Siena
Search for more papers by this authorValeria Spina
Division of Haematology, Department of Clinical and Experimental Medicine and IRCAD, Amedeo Avogadro University of Eastern Piedmont, Novara
Search for more papers by this authorEmanuele Cencini
Division of Haematology, Department of Clinical Medicine and Immunological Sciences, University of Siena and AOUS, Siena
Search for more papers by this authorRita Santachiara
Division of Haematology, Department of Oncology and Haematology, University of Modena and Reggio Emilia, Modena
Search for more papers by this authorRoberto Marasca
Division of Haematology, Department of Oncology and Haematology, University of Modena and Reggio Emilia, Modena
Search for more papers by this authorValter Gattei
Clinical and Experimental Onco-Haematology Unit, Centro di Riferimento Oncologico, I.R.C.C.S., Aviano (PN), Italy
Search for more papers by this authorFranco Cavalli
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Search for more papers by this authorEmanuele Zucca
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Search for more papers by this authorGianluca Gaidano
Division of Haematology, Department of Clinical and Experimental Medicine and IRCAD, Amedeo Avogadro University of Eastern Piedmont, Novara
Search for more papers by this authorFrancesco Bertoni
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Search for more papers by this authorAndrea Rinaldi
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
These authors contributed equally to this study.
Search for more papers by this authorMichael Mian
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Division of Haematology, Azienda Ospedaliera S. Maurizio, Bolzano/Bozen, Italy
These authors contributed equally to this study.
Search for more papers by this authorIvo Kwee
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Dalle Molle Institute for Artificial Intelligence (IDSIA), Manno, Switzerland
These authors contributed equally to this study.
Search for more papers by this authorDavide Rossi
Division of Haematology, Department of Clinical and Experimental Medicine and IRCAD, Amedeo Avogadro University of Eastern Piedmont, Novara
Search for more papers by this authorClara Deambrogi
Division of Haematology, Department of Clinical and Experimental Medicine and IRCAD, Amedeo Avogadro University of Eastern Piedmont, Novara
Search for more papers by this authorAfua A. Mensah
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Search for more papers by this authorFrancesco Forconi
Division of Haematology, Department of Clinical Medicine and Immunological Sciences, University of Siena and AOUS, Siena
Search for more papers by this authorValeria Spina
Division of Haematology, Department of Clinical and Experimental Medicine and IRCAD, Amedeo Avogadro University of Eastern Piedmont, Novara
Search for more papers by this authorEmanuele Cencini
Division of Haematology, Department of Clinical Medicine and Immunological Sciences, University of Siena and AOUS, Siena
Search for more papers by this authorRita Santachiara
Division of Haematology, Department of Oncology and Haematology, University of Modena and Reggio Emilia, Modena
Search for more papers by this authorRoberto Marasca
Division of Haematology, Department of Oncology and Haematology, University of Modena and Reggio Emilia, Modena
Search for more papers by this authorValter Gattei
Clinical and Experimental Onco-Haematology Unit, Centro di Riferimento Oncologico, I.R.C.C.S., Aviano (PN), Italy
Search for more papers by this authorFranco Cavalli
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Search for more papers by this authorEmanuele Zucca
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Search for more papers by this authorGianluca Gaidano
Division of Haematology, Department of Clinical and Experimental Medicine and IRCAD, Amedeo Avogadro University of Eastern Piedmont, Novara
Search for more papers by this authorFrancesco Bertoni
Oncology Institute of Southern Switzerland (IOSI), Bellinzona, Switzerland
Search for more papers by this authorSummary
The integration of molecular and clinical information to tailor treatments remains an important research challenge in chronic lymphocytic leukaemia (CLL). This study aimed to identify genomic lesions associated with a poor outcome and a higher risk of histological transformation. A mono-institutional cohort of 147 cases was used as the test series, and a multi-institutional cohort of 176 cases as a validation series. Genomic profiles were obtained using Affymetrix SNP 6.0. The impact of the recurrent minimal common regions (MCRs) on overall survival was evaluated by univariate analysis followed by multiple-test correction. The independent prognostic significance was assessed by multivariate analysis. Eight MCRs showed a prognostic impact: gains at 2p25.3-p22.3 (MYCN), 2p22.3, 2p16.2-p14 (REL), 8q23.3-q24.3 (MYC), losses at 8p23.1-p21.2, 8p21.2, and of the TP53 locus. Gains at 2p and 8q and TP53 inactivation maintained prognostic significance in multivariate analysis and a hierarchical model confirmed their relevance. Gains at 2p also determined a higher risk of Richter syndrome transformation. The prediction of outcome for CLL patients might be improved by evaluating the presence of gains at 2p and 8q as novel genomic regions besides those included in the ‘standard’ fluorescence in situ hybridization panel.
Supporting Information
Fig S1. Diagram showing the study design and the workflow of samples.
Fig S2. Ideogram showing distribution of DNA gains and losses in 158 CLL patients.
Fig S3. The demonstration of deletions at 8p23·1-p21·2 better defines CLL prognostic groups.
Fig S4. The demonstration of gains at 8q23·3-q24·3 better defines CLL prognostic groups.
Fig S5. The demonstration of gains at 2p16·2-p14 better defines CLL prognostic groups.
Table SI. Minimal common regions (MCR) identified in the test series of 148 CLL patients and their impact on OS by univariate analysis.
Table SII. Cox regression analysis to classify patients in a hierarchical
model for OS.
| Filename | Description |
|---|---|
| BJH_8789_sm_FigS1.tiff2.4 MB | Supporting info item |
| BJH_8789_sm_FigS2.tiff2.3 MB | Supporting info item |
| BJH_8789_sm_FigS3.tiff1.3 MB | Supporting info item |
| BJH_8789_sm_FigS4.tiff1.3 MB | Supporting info item |
| BJH_8789_sm_FigS5.tiff1.4 MB | Supporting info item |
| BJH_8789_sm_TableS1.pdf65.5 KB | Supporting info item |
| BJH_8789_sm_TableS2.doc33 KB | Supporting info item |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Bea, S., Lopez-Guillermo, A., Ribas, M., Puig, X., Pinyol, M., Carrio, A., Zamora, L., Soler, F., Bosch, F., Stilgenbauer, S., Colomer, D., Miro, R., Montserrat, E. & Campo, E. (2002) Genetic imbalances in progressed B-cell chronic lymphocytic leukemia and transformed large-cell lymphoma (Richter’s syndrome). American Journal of Pathology, 161, 957–968.
- Chapiro, E., Leporrier, N., Radford-Weiss, I., Bastard, C., Mossafa, H., Leroux, D., Tigaud, I., De Braekeleer, M., Terre, C., Brizard, F., Callet-Bauchu, E., Struski, S., Veronese, L., Fert-Ferrer, S., Taviaux, S., Lesty, C., Davi, F., Merle-Beral, H., Bernard, O.A., Sutton, L., Raynaud, S.D. & Nguyen-Khac, F. (2010) Gain of the short arm of chromosome 2 (2p) is a frequent recurring chromosome aberration in untreated chronic lymphocytic leukemia (CLL) at advanced stages. Leukemia Research, 34, 63–68.
- Chiorazzi, N. & Ferrarini, M. (2011) Cellular origin(s) of chronic lymphocytic leukemia: cautionary notes and additional considerations and possibilities. Blood, 117, 1781–1791.
- Dal-Bo, M., Bertoni, F., Forconi, F., Zucchetto, A., Bomben, R., Marasca, R., Deaglio, S., Laurenti, L., Efremov, D.G., Gaidano, G., Del Poeta, G. & Gattei, V. (2009) Intrinsic and extrinsic factors influencing the clinical course of B-cell chronic lymphocytic leukemia: prognostic markers with pathogenetic relevance. Journal of Translational Medicine, 7, 76.
- Deambrogi, C., De Paoli, L., Fangazio, M., Cresta, S., Rasi, S., Spina, V., Gattei, V., Gaidano, G. & Rossi, D. (2010) Analysis of the REL, BCL11A, and MYCN proto-oncogenes belonging to the 2p amplicon in chronic lymphocytic leukemia. American Journal of Hematology, 85, 541–544.
- Dighiero, G. & Hamblin, T.J. (2008) Chronic lymphocytic leukaemia. Lancet, 371, 1017–1029.
- Dohner, H., Stilgenbauer, S., Benner, A., Leupolt, E., Krober, A., Bullinger, L., Dohner, K., Bentz, M. & Lichter, P. (2000) Genomic aberrations and survival in chronic lymphocytic leukemia. New England Journal of Medicine, 343, 1910–1916.
- Fabris, S., Mosca, L., Todoerti, K., Cutrona, G., Lionetti, M., Intini, D., Matis, S., Colombo, M., Agnelli, L., Gentile, M., Spriano, M., Callea, V., Festini, G., Molica, S., Lambertenghi Deliliers, G., Morabito, F., Ferrarini, M. & Neri, A. (2008) Molecular and transcriptional characterization of 17p loss in B-cell chronic lymphocytic leukemia. Genes Chromosomes Cancer, 47, 781–793.
- Forconi, F., Rinaldi, A., Kwee, I., Sozzi, E., Raspadori, D., Rancoita, P.M.V., Scandurra, M., Rossi, D., Deambrogi, C., Capello, D., Zucca, E., Marconi, D., Bomben, R., Gattei, V., Lauria, F., Gaidano, G. & Bertoni, F. (2008) Genome-wide DNA profiling identifies an unstable profile with recurrent imbalances predicting outcome in chronic lymphocytic leukemia with 17p deletion. British Journal of Haematology, 143, 532–536.
- Hallek, M. (2008) Prognostic factors in chronic lymphocytic leukemia. Annals of Oncology, 19(Suppl. 4), iv51–53.
-
Hallek, M. (2009) State-of-the-art treatment of chronic lymphocytic leukemia.
Hematology American Society Hematology Education Program, 440–449.
10.1182/asheducation-2009.1.440 Google Scholar
- Hallek, M., Cheson, B.D., Catovsky, D., Caligaris-Cappio, F., Dighiero, G., Dohner, H., Hillmen, P., Keating, M.J., Montserrat, E., Rai, K.R. & Kipps, T.J. (2008) Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia (IWCLL) updating the National Cancer Institute-Working Group (NCI-WG) 1996 guidelines. Blood, 111, 5446–5456.
- Hartmann, E., Fernandez, V., Moreno, V., Valls, J., Hernandez, L., Bosch, F., Abrisqueta, P., Klapper, W., Dreyling, M., Hoster, E., Muller-Hermelink, H.K., Ott, G., Rosenwald, A. & Campo, E. (2008) Five-gene model to predict survival in mantle-cell lymphoma using frozen or formalin-fixed, paraffin-embedded tissue. Journal of Clinical Oncology, 26, 4966–4972.
- Hartmann, E.M., Campo, E., Wright, G., Lenz, G., Salaverria, I., Jares, P., Xiao, W., Braziel, R.M., Rimsza, L.M., Chan, W.C., Weisenburger, D.D., Delabie, J., Jaffe, E.S., Gascoyne, R.D., Dave, S.S., Mueller-Hermelink, H.K., Staudt, L.M., Ott, G., Bea, S. & Rosenwald, A. (2010) Pathway discovery in mantle cell lymphoma by integrated analysis of high-resolution gene expression and copy number profiling. Blood, 116, 953–961.
- Herishanu, Y., Perez-Galan, P., Liu, D., Biancotto, A., Pittaluga, S., Vire, B., Gibellini, F., Njuguna, N., Lee, E., Stennett, L., Raghavachari, N., Liu, P., McCoy, J.P., Raffeld, M., Stetler-Stevenson, M., Yuan, C., Sherry, R., Arthur, D.C., Maric, I., White, T., Marti, G.E., Munson, P., Wilson, W.H. & Wiestner, A. (2010) The lymph node microenvironment promotes B-cell receptor signaling, NF-{kappa}B activation, and tumor proliferation in chronic lymphocytic leukemia. Blood, 117, 563–574.
- Hewamana, S., Alghazal, S., Lin, T.T., Clement, M., Jenkins, C., Guzman, M.L., Jordan, C.T., Neelakantan, S., Crooks, P.A., Burnett, A.K., Pratt, G., Fegan, C., Rowntree, C., Brennan, P. & Pepper, C. (2008) The NF-kappaB subunit Rel A is associated with in vitro survival and clinical disease progression in chronic lymphocytic leukemia and represents a promising therapeutic target. Blood, 111, 4681–4689.
- Janoueix-Lerosey, I., Schleiermacher, G., Michels, E., Mosseri, V., Ribeiro, A., Lequin, D., Vermeulen, J., Couturier, J., Peuchmaur, M., Valent, A., Plantaz, D., Rubie, H., Valteau-Couanet, D., Thomas, C., Combaret, V., Rousseau, R., Eggert, A., Michon, J., Speleman, F. & Delattre, O. (2009) Overall genomic pattern is a predictor of outcome in neuroblastoma. Journal of Clinical Oncology, 27, 1026–1033.
- Kienle, D.L., Korz, C., Hosch, B., Benner, A., Mertens, D., Habermann, A., Krober, A., Jager, U., Lichter, P., Dohner, H. & Stilgenbauer, S. (2005) Evidence for distinct pathomechanisms in genetic subgroups of chronic lymphocytic leukemia revealed by quantitative expression analysis of cell cycle, activation, and apoptosis-associated genes. Journal of Clinical Oncology, 23, 3780–3792.
- Klapproth, K. & Wirth, T. (2010) Advances in the understanding of MYC-induced lymphomagenesis. British Journal of Haematology, 149, 484–497.
- Krober, A., Seiler, T., Benner, A., Bullinger, L., Bruckle, E., Lichter, P., Dohner, H. & Stilgenbauer, S. (2002) V(H) mutation status, CD38 expression level, genomic aberrations, and survival in chronic lymphocytic leukemia. Blood, 100, 1410–1416.
- Krober, A., Bloehdorn, J., Hafner, S., Buhler, A., Seiler, T., Kienle, D., Winkler, D., Bangerter, M., Schlenk, R.F., Benner, A., Lichter, P., Dohner, H. & Stilgenbauer, S. (2006) Additional genetic high-risk features such as 11q deletion, 17p deletion, and V3-21 usage characterize discordance of ZAP-70 and VH mutation status in chronic lymphocytic leukemia. Journal of Clinical Oncology, 24, 969–975.
- Lenz, G., Wright, G.W., Emre, N.C., Kohlhammer, H., Dave, S.S., Davis, R.E., Carty, S., Lam, L.T., Shaffer, A.L., Xiao, W., Powell, J., Rosenwald, A., Ott, G., Muller-Hermelink, H.K., Gascoyne, R.D., Connors, J.M., Campo, E., Jaffe, E.S., Delabie, J., Smeland, E.B., Rimsza, L.M., Fisher, R.I., Weisenburger, D.D., Chan, W.C. & Staudt, L.M. (2008) Molecular subtypes of diffuse large B-cell lymphoma arise by distinct genetic pathways. Proceedings of the National Academy of Sciences of the United States of America, 105, 13520–13525.
- Lerner, M., Harada, M., Loven, J., Castro, J., Davis, Z., Oscier, D., Henriksson, M., Sangfelt, O., Grander, D. & Corcoran, M.M. (2009) DLEU2, frequently deleted in malignancy, functions as a critical host gene of the cell cycle inhibitory microRNAs miR-15a and miR-16-1. Experimental Cell Research, 315, 2941–2952.
- Malcikova, J., Smardova, J., Rocnova, L., Tichy, B., Kuglik, P., Vranova, V., Cejkova, S., Svitakova, M., Skuhrova Francova, H., Brychtova, Y., Doubek, M., Brejcha, M., Klabusay, M., Mayer, J., Pospisilova, S. & Trbusek, M. (2009) Monoallelic and biallelic inactivation of TP53 gene in chronic lymphocytic leukemia: selection, impact on survival, and response to DNA damage. Blood, 114, 5307–5314.
- Mian, M., Rinaldi, A., Mensah, A.A., Rossi, D., Ladetto, M., Forconi, F., Marasca, R., Gattei, V., Zucca, E., Cavalli, F., Gaidano, G., Kwee, I. & Bertoni, F. (2011) Del(13q14.3) length matters: an integrated analysis of genomic, FISH and clinical data in 169 chronic lymphocytic leukemia patients with 13q deletion alone or normal karyotype Hematological Oncology, doi: 10.1002/hon.997. in press.
- Moussay, E., Palissot, V., Vallar, L., Poirel, H.A., Wenner, T., El Khoury, V., Aouali, N., Van Moer, K., Leners, B., Bernardin, F., Muller, A., Cornillet-Lefebvre, P., Delmer, A., Duhem, C., Ries, F., van Dyck, E. & Berchem, G. (2010) Determination of genes and microRNAs involved in the resistance to fludarabine in vivo in chronic lymphocytic leukemia. Molecular Cancer, 9, 115.
- Olshen, A.B., Venkatraman, E.S., Lucito, R. & Wigler, M. (2004) Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics, 5, 557–572.
- R Development Core Team (2009) R: A Language and Environment For Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
- Refaeli, Y., Young, R.M., Turner, B.C., Duda, J., Field, K.A. & Bishop, J.M. (2008) The B cell antigen receptor and overexpression of MYC can cooperate in the genesis of B cell lymphomas. PLoS Biology, 6, e152.
- Rinaldi, A., Mian, M., Chigrinova, E., Arcaini, L., Bhagat, G., Novak, U., Rancoita, P.M.V., De Campos, C., Forconi, F., Gascoyne, R., Facchetti, F., Ponzoni, M., Govi, S., Ferreri, A.J., Mollejo, M., Piris, M.A., Baldini, L., Soulier, J., Thieblemont, C., Canzonieri, V., Gattei, V., Marasca, R., Franceschetti, S., Gaidano, G., Tucci, A., Uccella, S., Tibiletti, M.G., Dirnhofer, S., Tripodo, C., Doglioni, C., Dalla-Favera, R., Cavalli, F., Zucca, E., Kwee, I. & Bertoni, F. (2011) Genome wide DNA-profiling of marginal zone lymphomas identifies subtype-specific lesions with an impact on the clinical outcome. Blood, 117, 1595–1604.
- Rossi, D., Cerri, M., Deambrogi, C., Sozzi, E., Cresta, S., Rasi, S., De Paoli, L., Spina, V., Gattei, V., Capello, D., Forconi, F., Lauria, F. & Gaidano, G. (2009a) The prognostic value of TP53 mutations in chronic lymphocytic leukemia is independent of Del17p13: implications for overall survival and chemorefractoriness. Clinical Cancer Research, 15, 995–1004.
- Rossi, D., Lobetti Bodoni, C., Genuardi, E., Monitillo, L., Drandi, D., Cerri, M., Deambrogi, C., Ricca, I., Rocci, A., Ferrero, S., Bernocco, E., Capello, D., De Paoli, L., Bergui, L., Boi, M., Omede, P., Massaia, M., Tarella, C., Passera, R., Boccadoro, M., Gaidano, G. & Ladetto, M. (2009b) Telomere length is an independent predictor of survival, treatment requirement and Richter’s syndrome transformation in chronic lymphocytic leukemia. Leukemia, 23, 1062–1072.
- Rubio-Moscardo, F., Blesa, D., Mestre, C., Siebert, R., Balasas, T., Benito, A., Rosenwald, A., Climent, J., Martinez, J.I., Schilhabel, M., Karran, E.L., Gesk, S., Esteller, M., Deleeuw, R., Staudt, L.M., Fernandez-Luna, J.L., Pinkel, D., Dyer, M.J. & Martinez-Climent, J.A. (2005) Characterization of 8p21.3 chromosomal deletions in B-cell lymphoma: TRAIL-R1 and TRAIL-R2 as candidate dosage-dependent tumor suppressor genes. Blood, 106, 3214–3222.
- Salaverria, I., Zettl, A., Bea, S., Moreno, V., Valls, J., Hartmann, E., Ott, G., Wright, G., Lopez-Guillermo, A., Chan, W.C., Weisenburger, D.D., Gascoyne, R.D., Grogan, T.M., Delabie, J., Jaffe, E.S., Montserrat, E., Muller-Hermelink, H.K., Staudt, L.M., Rosenwald, A. & Campo, E. (2007) Specific secondary genetic alterations in mantle cell lymphoma provide prognostic information independent of the gene expression-based proliferation signature. Journal of Clinical Oncology, 25, 1216–1222.
- Scandurra, M., Mian, M., Greiner, T.C., Rancoita, P.M.V., de Campos, C.P., Chan, W.C., Vose, J.M., Chigrinova, E., Inghirami, G., Chiappella, A., Baldini, L., Ponzoni, M., Ferreri, A.J.M., Franceschetti, S., Gaidano, G., Moreno, S.M., Piris, M.A., Facchetti, F., Tucci, A., Nomdedeu, J.F., Lazure, T., Lambotte, O., Uccella, S., Pinotti, G., Pruneri, G., Martinelli, G., Young, K.H., Tibiletti, M.G., Rinaldi, A., Zucca, E., Kwee, I. & Bertoni, F. (2010a) Genomic lesions associated with a different clinical outcome in diffuse large B-cell lymphoma treated with R-CHOP. British Journal of Haematology, 151, 221–231.
- Scandurra, M., Rossi, D., Deambrogi, C., Rancoita, P.M.V., Chigrinova, E., Mian, M., Cerri, M., Rasi, S., Sozzi, E., Forconi, F., Ponzoni, M., Montes-Moreno, S., Piris, M.A., Inghirami, G., Zucca, E., Gattei, V., Rinaldi, A., Kwee, I., Gaidano, G. & Bertoni, F. (2010b) Genomic profiling of Richter’s syndrome: recurrent lesions and differences with de novo diffuse large B-cell lymphomas. Hematological Oncology, 28, 62–67.
- Stevenson, F.K. & Caligaris-Cappio, F. (2004) Chronic lymphocytic leukemia: revelations from the B-cell receptor. Blood, 103, 4389–4395.
- Testoni, M., Kwee, I., Greiner, T.C., Montes-Moreno, S., Vose, J., Chan, W.C., Chiappella, A., Baldini, L., Ferreri, A.J.M., Gaidano, G., Mian, M., Zucca, E. & Bertoni, F.(2011) Gains of MYC locus and outcome in patients with diffuse large B-cell lymphoma treated with R-CHOP British Journal of Haematology, doi: 10.1111/j.1365-2141.2011.08675.x. in press.
- Vallat, L., Magdelenat, H., Merle-Beral, H., Masdehors, P., Potocki De Montalk, G., Davi, F., Kruhoffer, M., Sabatier, L., Orntoft, T.F. & Delic, J. (2003) The resistance of B-CLL cells to DNA damage-induced apoptosis defined by DNA microarrays. Blood, 101, 4598–4606.
- Zenz, T., Eichhorst, B., Busch, R., Denzel, T., Habe, S., Winkler, D., Buhler, A., Edelmann, J., Bergmann, M., Hopfinger, G., Hensel, M., Hallek, M., Dohner, H. & Stilgenbauer, S. (2010) TP53 mutation and survival in chronic lymphocytic leukemia. Journal of Clinical Oncology, 28, 4473–4479.
- Zhang, W., Kater, A.P., Widhopf Ii, G.F., Chuang, H.Y., Enzler, T., James, D.F., Poustovoitov, M., Tseng, P.H., Janz, S., Hoh, C., Herschman, H., Karin, M. & Kipps, T.J. (2010) B-cell activating factor and v-Myc myelocytomatosis viral oncogene homolog (c-Myc) influence progression of chronic lymphocytic leukemia. Proceedings of the National Academy of Sciences of the United States of America, 107, 18956–18960.
- Zhao, X., Li, C., Paez, J.G., Chin, K., Janne, P.A., Chen, T.H., Girard, L., Minna, J., Christiani, D., Leo, C., Gray, J.W., Sellers, W.R. & Meyerson, M. (2004) An integrated view of copy number and allelic alterations in the cancer genome using single nucleotide polymorphism arrays. Cancer Research, 64, 3060–3071.
Citing Literature
