Molecular biomarkers in chronic lymphocytic leukemia

Advances in Experimental Medicine and Biology

Volumn 792, Issue , 2013, Pages 193-214

  Malek, Sami ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Biomarkers; CLL; Disease progression; Overall survival; Response to therapy

Indexed keywords

BIOLOGICAL MARKER; CD38 ANTIGEN; IMMUNOGLOBULIN HEAVY CHAIN; MESSENGER RNA; PROTEIN KINASE ZAP 70; PROTEIN P53;

ARTICLE; CANCER DIAGNOSIS; CANCER PROGNOSIS; CANCER SURVIVAL; CELL POPULATION; CHRONIC LYMPHATIC LEUKEMIA; DIAGNOSTIC ACCURACY; DISEASE ASSOCIATION; DISEASE MARKER; FLUORESCENCE IN SITU HYBRIDIZATION; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; HUMAN; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; OVERALL SURVIVAL; PATIENT COUNSELING; PATIENT DECISION MAKING; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RELIABILITY; REPRODUCIBILITY; RISK ASSESSMENT; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; TREATMENT RESPONSE; TUMOR SUPPRESSOR GENE; VALIDITY;

EID: 84934443966     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-8051-8_9     Document Type: Article

References (103)

1. Chiorazzi N, Rai KR, Ferrarini M. Chronic lymphocytic leukemia. N Engl J Med. 2005; 352(8):804-15.
2. Hallek M, Cheson BD, Catovsky D, Caligaris-Cappio F, Dighiero G, Dohner H, et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute-Working Group 1996 guidelines. Blood. 2008;111(12):5446-56.
3. Chiorazzi N, Ferrarini M. Cellular origin(s) of chronic lymphocytic leukemia: cautionary notes and additional considerations and possibilities. Blood. 2011;117(6):1781-91.
4. Malek S. Clinical utility of prognostic markers in chronic lymphocytic leukemia [review]. ASCO Educ Book. 2010;2010:263-7.
5. Van Bockstaele F, Verhasselt B, Philippe J. Prognostic markers in chronic lymphocytic leukemia: a comprehensive review. Blood Rev. 2009;23(1):25-47.
6. Rassenti LZ, Huynh L, Toy TL, Chen L, Keating MJ, Gribben JG, et al. ZAP-70 compared with immunoglobulin heavy-chain gene mutation status as a predictor of disease progression in chronic lymphocytic leukemia. N Engl J Med. 2004;351(9):893-901.
7. Brenner H, Gondos A, Pulte D. Trends in long-term survival of patients with chronic lymphocytic leukemia from the 1980s to the early 21st century. Blood. 2008;111(10): 4916-21.
8. Rai KR, Sawitsky A, Cronkite EP, Chanana AD, Levy RN, Pasternack BS. Clinical staging of chronic lymphocytic leukemia. Blood. 1975;46(2):219-34.
9. Landgren O, Albitar M, Ma W, Abbasi F, Hayes RB, Ghia P, et al. B-cell clones as early markers for chronic lymphocytic leukemia. N Engl J Med. 2009;360(7):659-67.
10. Rawstron AC, Bennett FL, O'Connor SJ, Kwok M, Fenton JA, Plummer M, et al. Monoclonal B-cell lymphocytosis and chronic lymphocytic leukemia. N Engl J Med. 2008;359(6): 575-83.
11. Dohner H, Stilgenbauer S, Benner A, Leupolt E, Krober A, Bullinger L, et al. Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med. 2000;343(26): 1910-6.
12. Juliusson G, Oscier DG, Fitchett M, Ross FM, Stockdill G, Mackie MJ, et al. Prognostic subgroups in B-cell chronic lymphocytic leukemia defined by specific chromosomal abnormalities. N Engl J Med. 1990;323(11):720-4.
13. Shanafelt TD, Witzig TE, Fink SR, Jenkins RB, Paternoster SF, Smoley SA, et al. Prospective evaluation of clonal evolution during long-term follow-up of patients with untreated earlystage chronic lymphocytic leukemia. J Clin Oncol. 2006;24(28):4634-41.
14. Malek SN. The biology and clinical significance of acquired genomic copy number aberrations and recurrent gene mutations in chronic lymphocytic leukemia. Oncogene. 2013;32(23):2805-17.
15. Sorror ML, Storer BE, Sandmaier BM, Maris M, Shizuru J, Maziarz R, et al. Five-year follow-up of patients with advanced chronic lymphocytic leukemia treated with allogeneic hematopoietic cell transplantation after nonmyeloablative conditioning. J Clin Oncol. 2008; 26(30):4912-20.
16. Schetelig J, van Biezen A, Brand R, Caballero D, Martino R, Itala M, et al. Allogeneic hematopoietic stem-cell transplantation for chronic lymphocytic leukemia with 17p deletion: a retrospective European Group for Blood and Marrow Transplantation analysis. J Clin Oncol. 2008;26(31):5094-100.
17. Dreger P, Dohner H, Ritgen M, Bottcher S, Busch R, Dietrich S, et al. Allogeneic stem cell transplantation provides durable disease control in poor-risk chronic lymphocytic leukemia: long-term clinical and MRD results of the German CLL Study Group CLL3X trial. Blood. 2010;116(14):2438-47.
18. Wierda W, O'Brien S, Wen S, Faderl S, Garcia-Manero G, Thomas D, et al. Chemoimmunotherapy with fludarabine, cyclophosphamide, and rituximab for relapsed and refractory chronic lymphocytic leukemia. J Clin Oncol. 2005;23(18):4070-8.
19. Keating MJ, O'Brien S, Albitar M, Lerner S, Plunkett W, Giles F, et al. Early results of a chemoimmunotherapy regimen of fludarabine, cyclophosphamide, and rituximab as initial therapy for chronic lymphocytic leukemia. J Clin Oncol. 2005;23(18):4079-88.
20. Hallek M, Fischer K, Fingerle-Rowson G, Fink AM, Busch R, Mayer J, et al. Addition of rituximab to fludarabine and cyclophosphamide in patients with chronic lymphocytic leukaemia: a randomised, open-label, phase 3 trial. Lancet. 2010;376(9747):1164-74.
21. Ouillette P, Collins R, Shakhan S, Li J, Peres E, Kujawski L, et al. Acquired genomic copy number aberrations and survival in chronic lymphocytic leukemia. Blood. 2011;118(11): 3051-61.
22. Shanafelt TD, Hanson C, Dewald GW, Witzig TE, LaPlant B, Abrahamzon J, et al. Karyotype evolution on fluorescent in situ hybridization analysis is associated with short survival in patients with chronic lymphocytic leukemia and is related to CD49d expression. J Clin Oncol. 2008;26(14):e5-6.
23. Stilgenbauer S, Sander S, Bullinger L, Benner A, Leupolt E, Winkler D, et al. Clonal evolution in chronic lymphocytic leukemia: acquisition of high-risk genomic aberrations associated with unmutated VH, resistance to therapy, and short survival. Haematologica. 2007;92(9):1242-5.
24. Delgado J, Espinet B, Oliveira AC, Abrisqueta P, de la Serna J, Collado R, et al. Chronic lymphocytic leukaemia with 17p deletion: a retrospective analysis of prognostic factors and therapy results. Br J Haematol. 2012;157(1):67-74.
25. Tam CS, Shanafelt TD, Wierda WG, Abruzzo LV, Van Dyke DL, O'Brien S, et al. De novo deletion 17p13.1 chronic lymphocytic leukemia shows significant clinical heterogeneity: the M. D. Anderson and Mayo Clinic experience. Blood. 2009;114(5):957-64.
26. Best OG, Gardiner AC, Davis ZA, Tracy I, Ibbotson RE, Majid A, et al. A subset of Binet stage A CLL patients with TP53 abnormalities and mutated IGHV genes have stable disease. Leukemia. 2009;23(1):212-4.
27. Pettitt AR, Jackson R, Carruthers S, Dodd J, Dodd S, Oates M, et al. Alemtuzumab in combination with methylprednisolone is a highly effective induction regimen for patients with chronic lymphocytic leukemia and deletion of TP53: final results of the National Cancer Research Institute CLL206 trial. J Clin Oncol. 2012;30(14):1647-55.
28. Saiya-Cork K, Collins R, Parkin B, Ouillette P, Kuizon E, Kujawski L, et al. A pathobiological role of the insulin receptor in chronic lymphocytic leukemia. Clin Cancer Res. 2011;17(9):2679-92.
29. Herling M, Patel KA, Weit N, Lilienthal N, Hallek M, Keating MJ, et al. High TCL1 levels are a marker of B-cell receptor pathway responsiveness and adverse outcome in chronic lymphocytic leukemia. Blood. 2009;114(21):4675-86.
30. Tsimberidou AM, Tam C, Abruzzo LV, O'Brien S, Wierda WG, Lerner S, et al. Chemoimmunotherapy may overcome the adverse prognostic significance of 11q deletion in previously untreated patients with chronic lymphocytic leukemia. Cancer. 2009;115(2): 373-80.
31. Gunnarsson R, Isaksson A, Mansouri M, Goransson H, Jansson M, Cahill N, et al. Large but not small copy-number alterations correlate to high-risk genomic aberrations and survival in chronic lymphocytic leukemia: a high-resolution genomic screening of newly diagnosed patients. Leukemia. 2010;24(1):211-5.
32. Pfeifer D, Pantic M, Skatulla I, Rawluk J, Kreutz C, Martens UM, et al. Genome-wide analysis of DNA copy number changes and LOH in CLL using high-density SNP arrays. Blood. 2007;109(3):1202-10.
33. Ouillette P, Collins R, Shakhan S, Li J, Li C, Shedden K, et al. The prognostic significance of various 13q14 deletions in chronic lymphocytic leukemia. Clin Cancer Res. 2011;17(21): 6778-90.
34. Ouillette P, Erba H, Kujawski L, Kaminski M, Shedden K, Malek SN. Integrated genomic profiling of chronic lymphocytic leukemia identifies subtypes of deletion 13q14. Cancer Res. 2008;68(4):1012-21.
35. Ouillette P, Fossum S, Parkin B, Ding L, Bockenstedt P, Al-Zoubi A, et al. Aggressive chronic lymphocytic leukemia with elevated genomic complexity is associated with multiple gene defects in the response to DNA double-strand breaks. Clin Cancer Res. 2010;16(3): 835-47.
36. Brown JR, Hanna M, Tesar B, Werner L, Pochet N, Asara JM, et al. Integrative genomic analysis implicates gain of PIK3CA at 3q26 and MYC at 8q24 in chronic lymphocytic leukemia. Clin Cancer Res. 2012;18(14):3791-802.
37. Saddler C, Ouillette P, Kujawski L, Shangary S, Talpaz M, Kaminski M, et al. Comprehensive biomarker and genomic analysis identifies p53 status as the major determinant of response to MDM2 inhibitors in chronic lymphocytic leukemia. Blood. 2008;111(3): 1584-93.
38. Kujawski L, Ouillette P, Erba H, Saddler C, Jakubowiak A, Kaminski M, et al. Genomic complexity identifies patients with aggressive chronic lymphocytic leukemia. Blood. 2008; 112(5):1993-2003.
39. Parker H, Rose-Zerilli MJ, Parker A, Chaplin T, Wade R, Gardiner A, et al. 13q deletion anatomy and disease progression in patients with chronic lymphocytic leukemia. Leukemia. 2011;25(3):489-97.
40. Dal Bo M, Rossi FM, Rossi D, Deambrogi C, Bertoni F, Del Giudice I, et al. 13q14 deletion size and number of deleted cells both influence prognosis in chronic lymphocytic leukemia. Genes Chromosomes Cancer. 2011;50(8):633-43.
41. Mayr C, Speicher MR, Kofler DM, Buhmann R, Strehl J, Busch R, et al. Chromosomal translocations are associated with poor prognosis in chronic lymphocytic leukemia. Blood. 2006;107(2):742-51.
42. Rigolin GM, Cibien F, Martinelli S, Formigaro L, Rizzotto L, Tammiso E, et al. Chromosome aberrations detected by conventional karyotyping using novel mitogens in chronic lymphocytic leukemia with "normal" FISH: correlations with clinicobiologic parameters. Blood. 2012;119(10):2310-3.
43. Muthusamy N, Breidenbach H, Andritsos L, Flynn J, Jones J, Ramanunni A, et al. Enhanced detection of chromosomal abnormalities in chronic lymphocytic leukemia by conventional cytogenetics using CpG oligonucleotide in combination with pokeweed mitogen and phorbol myristate acetate. Cancer Genet. 2011;204(2):77-83.
44. Heerema NA, Byrd JC, Dal Cin PS, Dell' Aquila ML, Koduru PR, Aviram A, et al. Stimulation of chronic lymphocytic leukemia cells with CpG oligodeoxynucleotide gives consistent karyotypic results among laboratories: a CLL Research Consortium (CRC) Study. Cancer Genet Cytogenet. 2010;203(2):134-40.
45. Delgado J, Aventin A, Briones J, Sanchez J, Nomdedeu J, Sierra J. The use of tetradecanoylphorbol acetate-stimulated peripheral blood cells enhances the prognostic value of interphase fluorescence in situ hybridization in patients with chronic lymphocytic leukemia. Genes Chromosomes Cancer. 2010;49(4):327-32.
46. Put N, Konings P, Rack K, Jamar M, Van Roy N, Libouton JM, et al. Improved detection of chromosomal abnormalities in chronic lymphocytic leukemia by conventional cytogenetics using CpG oligonucleotide and interleukin-2 stimulation: a Belgian multicentric study. Genes Chromosomes Cancer. 2009;48(10):843-53.
47. Dicker F, Schnittger S, Haferlach T, Kern W, Schoch C. Immunostimulatory oligonucleotideinduced metaphase cytogenetics detect chromosomal aberrations in 80% of CLL patients: a study of 132 CLL cases with correlation to FISH, IgVH status, and CD38 expression. Blood. 2006;108(9):3152-60.
48. Haferlach C, Dicker F, Schnittger S, Kern W, Haferlach T. Comprehensive genetic characterization of CLL: a study on 506 cases analysed with chromosome banding analysis, interphase FISH, IgV(H) status and immunophenotyping. Leukemia. 2007;21(12):2442-51.
49. Van Den Neste E, Robin V, Francart J, Hagemeijer A, Stul M, Vandenberghe P, et al. Chromosomal translocations independently predict treatment failure, treatment-free survival and overall survival in B-cell chronic lymphocytic leukemia patients treated with cladribine. Leukemia. 2007;21(8):1715-22.
50. Wattel E, Preudhomme C, Hecquet B, Vanrumbeke M, Quesnel B, Dervite I, et al. p53 mutations are associated with resistance to chemotherapy and short survival in hematologic malignancies. Blood. 1994;84(9):3148-57.
51. el Rouby S, Thomas A, Costin D, Rosenberg CR, Potmesil M, Silber R, et al. p53 gene mutation in B-cell chronic lymphocytic leukemia is associated with drug resistance and is independent of MDR1/MDR3 gene expression. Blood. 1993;82(11):3452-9.
52. Gaidano G, Ballerini P, Gong JZ, Inghirami G, Neri A, Newcomb EW, et al. p53 mutations in human lymphoid malignancies: association with Burkitt lymphoma and chronic lymphocytic leukemia. Proc Natl Acad Sci U S A. 1991;88(12):5413-7.
53. Zenz T, Krober A, Scherer K, Habe S, Buhler A, Benner A, et al. Monoallelic TP53 inactivation is associated with poor prognosis in chronic lymphocytic leukemia: results from a detailed genetic characterization with long-term follow-up. Blood. 2008;112(8): 3322-9.
54. Dicker F, Herholz H, Schnittger S, Nakao A, Patten N, Wu L, et al. The detection of TP53 mutations in chronic lymphocytic leukemia independently predicts rapid disease progression and is highly correlated with a complex aberrant karyotype. Leukemia. 2009;23(1):117-24.
55. Rossi D, Cerri M, Deambrogi C, Sozzi E, Cresta S, Rasi S, et al. The prognostic value of TP53 mutations in chronic lymphocytic leukemia is independent of Del17p13: implications for overall survival and chemorefractoriness. Clin Cancer Res. 2009;15(3):995-1004.
56. Malcikova J, Smardova J, Rocnova L, Tichy B, Kuglik P, Vranova V, et al. Monoallelic and biallelic inactivation of TP53 gene in chronic lymphocytic leukemia: selection, impact on survival and response to DNA damage. Blood. 2009;114(26):5307-14.
57. Trbusek M, Smardova J, Malcikova J, Sebejova L, Dobes P, Svitakova M, et al. Missense mutations located in structural p53 DNA-binding motifs are associated with extremely poor survival in chronic lymphocytic leukemia. J Clin Oncol. 2011;29(19):2703-8.
58. Gonzalez D, Martinez P, Wade R, Hockley S, Oscier D, Matutes E, et al. Mutational status of the TP53 gene as a predictor of response and survival in patients with chronic lymphocytic leukemia: results from the LRF CLL4 trial. J Clin Oncol. 2011;29(16):2223-9.
59. Zenz T, Eichhorst B, Busch R, Denzel T, Habe S, Winkler D, et al. TP53 mutation and survival in chronic lymphocytic leukemia. J Clin Oncol. 2010;28(29):4473-9.
60. Castro JE, James DF, Sandoval-Sus JD, Jain S, Bole J, Rassenti L, et al. Rituximab in combination with high-dose methylprednisolone for the treatment of chronic lymphocytic leukemia. Leukemia. 2009;23(10):1779-89.
61. Lin KI, Tam CS, Keating MJ, Wierda WG, O'Brien S, Lerner S, et al. Relevance of the immunoglobulin VH somatic mutation status in patients with chronic lymphocytic leukemia treated with fludarabine, cyclophosphamide, and rituximab (FCR) or related chemoimmunotherapy regimens. Blood. 2009;113(14):3168-71.
62. Tschumper RC, Geyer SM, Campbell ME, Kay NE, Shanafelt TD, Zent CS, et al. Immunoglobulin diversity gene usage predicts unfavorable outcome in a subset of chronic lymphocytic leukemia patients. J Clin Invest. 2008;118(1):306-15.
63. Hamblin TJ, Davis Z, Gardiner A, Oscier DG, Stevenson FK. Unmutated Ig V(H) genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood. 1999; 94(6):1848-54.
64. Damle RN, Wasil T, Fais F, Ghiotto F, Valetto A, Allen SL, et al. Ig V gene mutation status and CD38 expression as novel prognostic indicators in chronic lymphocytic leukemia. Blood. 1999;94(6):1840-7.
65. Fais F, Ghiotto F, Hashimoto S, Sellars B, Valetto A, Allen SL, et al. Chronic lymphocytic leukemia B cells express restricted sets of mutated and unmutated antigen receptors. J Clin Invest. 1998;102(8):1515-25.
66. Langerak AW, Davi F, Ghia P, Hadzidimitriou A, Murray F, Potter KN, et al. Immunoglobulin sequence analysis and prognostication in CLL: guidelines from the ERIC review board for reliable interpretation of problematic cases. Leukemia. 2011;25(6):979-84.
67. Ghia P, Stamatopoulos K, Belessi C, Moreno C, Stilgenbauer S, Stevenson F, et al. ERIC recommendations on IGHV gene mutational status analysis in chronic lymphocytic leukemia. Leukemia. 2007;21(1):1-3.
68. Sahota SS, Babbage G, Zojer N, Ottensmeier CH, Stevenson FK. Determining mutational status of immunoglobulin v genes in chronic lymphocytic leukemia: a useful prognostic indicator. Methods Mol Med. 2005;115:129-44.
69. Matthews C, Catherwood M, Morris TC, Alexander HD. Routine analysis of IgVH mutational status in CLL patients using BIOMED-2 standardized primers and protocols. Leuk Lymphoma. 2004;45(9):1899-904.
70. Deglesne PA, Chevallier N, Letestu R, Baran-Marszak F, Beitar T, Salanoubat C, et al. Survival response to B-cell receptor ligation is restricted to progressive chronic lymphocytic leukemia cells irrespective of Zap70 expression. Cancer Res. 2006;66(14):7158-66.
71. Nedellec S, Renaudineau Y, Bordron A, Berthou C, Porakishvili N, Lydyard PM, et al. B cell response to surface IgM cross-linking identifies different prognostic groups of B-chronic lymphocytic leukemia patients. J Immunol. 2005;174(6):3749-56.
72. Thorselius M, Krober A, Murray F, Thunberg U, Tobin G, Buhler A, et al. Strikingly homologous immunoglobulin gene rearrangements and poor outcome in VH3-21-using chronic lymphocytic leukemia patients independent of geographic origin and mutational status. Blood. 2006;107(7):2889-94.
73. Del Principe MI, Del Poeta G, Buccisano F, Maurillo L, Venditti A, Zucchetto A, et al. Clinical significance of ZAP-70 protein expression in B-cell chronic lymphocytic leukemia. Blood. 2006;108(3):853-61.
74. Orchard JA, Ibbotson RE, Davis Z, Wiestner A, Rosenwald A, Thomas PW, et al. ZAP-70 expression and prognosis in chronic lymphocytic leukaemia. Lancet. 2004;363 (9403):105-11.
75. Crespo M, Bosch F, Villamor N, Bellosillo B, Colomer D, Rozman M, et al. ZAP-70 expression as a surrogate for immunoglobulin-variable-region mutations in chronic lymphocytic leukemia. N Engl J Med. 2003;348(18):1764-75.
76. Deaglio S, Vaisitti T, Aydin S, Bergui L, D'Arena G, Bonello L, et al. CD38 and ZAP-70 are functionally linked and mark CLL cells with high migratory potential. Blood. 2007;110(12): 4012-21.
77. Chen L, Apgar J, Huynh L, Dicker F, Giago-McGahan T, Rassenti L, et al. ZAP-70 directly enhances IgM signaling in chronic lymphocytic leukemia. Blood. 2005;105(5):2036-41.
78. Wiestner A, Rosenwald A, Barry TS, Wright G, Davis RE, Henrickson SE, et al. ZAP-70 expression identifies a chronic lymphocytic leukemia subtype with unmutated immunoglobulin genes, inferior clinical outcome, and distinct gene expression profile. Blood. 2003;101 (12):4944-51.
79. Chen L, Widhopf G, Huynh L, Rassenti L, Rai KR, Weiss A, et al. Expression of ZAP-70 is associated with increased B-cell receptor signaling in chronic lymphocytic leukemia. Blood. 2002;100(13):4609-14.
80. Claus R, Lucas DM, Stilgenbauer S, Ruppert AS, Yu L, Zucknick M, et al. Quantitative DNA methylation analysis identifies a single CpG dinucleotide important for ZAP-70 expression and predictive of prognosis in chronic lymphocytic leukemia. J Clin Oncol. 2012;30(20): 2483-91.
81. Damle RN, Temburni S, Calissano C, Yancopoulos S, Banapour T, Sison C, et al. CD38 expression labels an activated subset within chronic lymphocytic leukemia clones enriched in proliferating B cells. Blood. 2007;110(9):3352-9.
82. Ghia P, Guida G, Stella S, Gottardi D, Geuna M, Strola G, et al. The pattern of CD38 expression defines a distinct subset of chronic lymphocytic leukemia (CLL) patients at risk of disease progression. Blood. 2003;101(4):1262-9.
83. Hamblin TJ, Orchard JA, Ibbotson RE, Davis Z, Thomas PW, Stevenson FK, et al. CD38 expression and immunoglobulin variable region mutations are independent prognostic variables in chronic lymphocytic leukemia, but CD38 expression may vary during the course of the disease. Blood. 2002;99(3):1023-9.
84. Del Poeta G, Maurillo L, Venditti A, Buccisano F, Epiceno AM, Capelli G, et al. Clinical significance of CD38 expression in chronic lymphocytic leukemia. Blood. 2001;98(9): 2633-9.
85. Patten PE, Buggins AG, Richards J, Wotherspoon A, Salisbury J, Mufti GJ, et al. CD38 expression in chronic lymphocytic leukemia is regulated by the tumor microenvironment. Blood. 2008;111(10):5173-81.
86. Ibrahim S, Keating M, Do KA, O'Brien S, Huh YO, Jilani I, et al. CD38 expression as an important prognostic factor in B-cell chronic lymphocytic leukemia. Blood. 2001;98(1): 181-6.
87. Ouillette P, Li J, Shaknovich R, Li Y, Melnick A, Shedden K, Malek SN. Incidence and clinical implications of ATM aberrations in chronic lymphocytic leukemia. Genes Chromosomes Cancer. 2012;51(12):1125-32.
88. Yan XJ, Dozmorov I, Li W, Yancopoulos S, Sison C, Centola M, et al. Identification of outcome-correlated cytokine clusters in chronic lymphocytic leukemia. Blood. 2011;118(19): 5201-10.
89. Tomic J, Lichty B, Spaner DE. Aberrant interferon-signaling is associated with aggressive chronic lymphocytic leukemia. Blood. 2011;117(9):2668-80.
90. Sivina M, Hartmann E, Kipps TJ, Rassenti L, Krupnik D, Lerner S, et al. CCL3 (MIP-1alpha) plasma levels and the risk for disease progression in chronic lymphocytic leukemia. Blood. 2011;117(5):1662-9.
91. Shedden K, Li Y, Ouillette P, Malek SN. Characteristics of chronic lymphocytic leukemia with somatically acquired mutations in NOTCH1 exon 34. Leukemia. 2012;26(5):1108-10.
92. Rossi D, Rasi S, Fabbri G, Spina V, Fangazio M, Forconi F, et al. Mutations of NOTCH1 are an independent predictor of survival in chronic lymphocytic leukemia. Blood. 2012;119(2): 521-9.
93. Gattei V, Bulian P, Del Principe MI, Zucchetto A, Maurillo L, Buccisano F, et al. Relevance of CD49d protein expression as overall survival and progressive disease prognosticator in chronic lymphocytic leukemia. Blood. 2008;111(2):865-73.
94. Austen B, Skowronska A, Baker C, Powell JE, Gardiner A, Oscier D, et al. Mutation status of the residual ATM allele is an important determinant of the cellular response to chemotherapy and survival in patients with chronic lymphocytic leukemia containing an 11q deletion. J Clin Oncol. 2007;25(34):5448-57.
95. Grabowski P, Hultdin M, Karlsson K, Tobin G, Aleskog A, Thunberg U, et al. Telomere length as a prognostic parameter in chronic lymphocytic leukemia with special reference to VH gene mutation status. Blood. 2005;105(12):4807-12.
96. Heintel D, Kienle D, Shehata M, Krober A, Kroemer E, Schwarzinger I, et al. High expression of lipoprotein lipase in poor risk B-cell chronic lymphocytic leukemia. Leukemia. 2005;19(7):1216-23.
97. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, et al. A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005;353(17):1793-801.
98. Wierda WG, O'Brien S, Wang X, Faderl S, Ferrajoli A, Do KA, et al. Multivariable model for time to first treatment in patients with chronic lymphocytic leukemia. J Clin Oncol. 2011; 29(31):4088-95.
99. Bulian P, Tarnani M, Rossi D, Forconi F, Del Poeta G, Bertoni F, et al. Multicentre validation of a prognostic index for overall survival in chronic lymphocytic leukaemia. Hematol Oncol. 2011;29(2):91-9.
100. Letestu R, Levy V, Eclache V, Baran-Marszak F, Vaur D, Naguib D, et al. Prognosis of Binet stage A chronic lymphocytic leukemia patients: the strength of routine parameters. Blood. 2010;116(22):4588-90.
101. Wierda WG, O'Brien S, Wang X, Faderl S, Ferrajoli A, Do KA, et al. Characteristics associated with important clinical end points in patients with chronic lymphocytic leukemia at initial treatment. J Clin Oncol. 2009;27(10):1637-43.
102. Shanafelt TD, Jenkins G, Call TG, Zent CS, Slager S, Bowen DA, et al. Validation of a new prognostic index for patients with chronic lymphocytic leukemia. Cancer. 2009;115(2): 363-72.
103. Rassenti LZ, Jain S, Keating MJ, Wierda WG, Grever MR, Byrd JC, et al. Relative value of ZAP-70, CD38, and immunoglobulin mutation status in predicting aggressive disease in chronic lymphocytic leukemia. Blood. 2008;112(5):1923-30.