CD38 expression labels an activated subset within chronic lymphocytic leukemia clones enriched in proliferating B cells

Blood

Volumn 110, Issue 9, 2007, Pages 3352-3359

  Damle, Rajendra N ^a,b   Temburni, Sonal ^a   Calissano, Carlo ^a   Yancopoulos, Sophia ^a   Banapour, Taraneh ^a   Sison, Cristina ^a   Allen, Steven L ^c,d   Rai, Kanti R ^d,e   Chiorazzi, Nicholas ^a,d  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c North Shore Long Island Center for Advanced Medicine   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e Feinstein Institute for Medical Research ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; CD38 ANTIGEN; CD69 ANTIGEN; KI 67 ANTIGEN; L SELECTIN; PROTEIN BCL 2; PROTEIN KINASE ZAP 70; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE;

ADULT; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL CYCLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL PROTECTION; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME RELEASE; FEMALE; HUMAN; HUMAN CELL; LEUKEMIA CELL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MAJOR CLINICAL STUDY; MALE; MOLECULAR CLONING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 36148992239     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-04-083832     Document Type: Article

References (70)

1. Fais F, Ghiotto F, Hashimoto S, et al. Chronic lymphocytic leukemia B cells express restricted sets of mutated and unmutated antigen receptors. J Clin Invest. 1998;102:1515-1525.
2. Damle RN, Wasil T, Fais F, et al. Ig V gene mutation status and CD38 expression as novel prognostic indicators in chronic lymphocytic leukemia. Blood. 1999;94:1840-1847.
3. Rosenwald A, Alizadeh AA, Widhopf G, et al. Relation of gene expression phenotype to immunoglobulin mutation genotype in B cell chronic lymphocytic leukemia. J Exp Med. 2001;194:1639-1647.
4. Wiestner A, Rosenwald A, Barry TS, 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;101:4944-4951.
5. Dohner H, Stilgenbauer S, Benner A, et al. Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med. 2000;343:1910-1916.
6. Pettitt AR, Sherrington PD, Stewart G, Cawley JC, Taylor AM, Stankovic T. p53 dysfunction in B-cell chronic lymphocytic leukemia: inactivation of ATM as an alternative to TP53 mutation. Blood. 2001;98:814-822.
7. Hamblin TJ, Davis Z, Gardiner A, Oscier DG, Stevenson FK. Unmutated Ig VH genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood. 1999;94:1848-1854.
8. Jelinek DF, Tschumper RC, Geyer SM, et al. Analysis of clonal B-cell CD38 and immunoglobulin variable region sequence status in relation to clinical outcome for B-chronic lymphocytic leukaemia. Br J Haematol. 2001;115:854-861.
9. Del Poeta G, Maurillo L, Venditti A, et al. Clinical significance of CD38 expression in chronic lymphocytic leukemia. Blood. 2001;98:2633-2639.
10. Marasca R, Maffei R, Morselli M, et al. Immunoglobulin mutational status detected through single-round amplification of partial V(H) region represents a good prognostic marker for clinical outcome in chronic lymphocytic leukemia. J Mol Diagn. 2005;7:566-574.
11. Crespo M, Bosch F, Villamor N, et al. ZAP-70 expression as a surrogate for immunoglobulin-variable-region mutations in chronic lymphocytic leukemia. N Engl J Med. 2003;348:1764-1775.
12. Durig J, Nuckel H, Cremer M, et al. ZAP-70 expression is a prognostic factor in chronic lymphocytic leukemia. Leukemia. 2003;17:2426-2434.
13. Rassenti LZ, Hunynh L, Toy TL, 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;351:893-901.
14. Schroers R, Griesinger F, Trumper L, et al. Combined analysis of ZAP-70 and CD38 expression as a predictor of disease progression in B-cell chronic lymphocytic leukemia. Leukemia. 2005.
15. Krober A, Seiler T, Benner A, et al. V(H) mutation status, CD38 expression level, genomic aberrations, and survival in chronic lymphocytic leukemia. Blood. 2002;100:1410-1416.
16. Stilgenbauer S, Bullinger L, Lichter P, Dohner H. Genetics of chronic lymphocytic leukemia: genomic aberrations and V(H) gene mutation status in pathogenesis and clinical course. Leukemia. 2002;16:993-1007.
17. Deaglio S, Capobianco A, Bergui L, et al. CD38 is a signaling molecule in B-cell chronic lymphocytic leukemia cells. Blood. 2003;102:2146-2155.
18. Deaglio S, Vaisitti T, Aydin S, Ferrero E, Malavasi F. In-tandem insight from basic science combined with clinical research: CD38 as both marker and key component of the pathogenetic network underlying chronic lymphocytic leukemia. Blood. 2006;108:1135-1144.
19. Deaglio S, Morra M, Mallone R, et al. Human CD38 (ADP-ribosyl cyclase) is a counter-receptor of CD31, an Ig superfamily member. J Immunol. 1998;160:395-402.
20. Deaglio S, Vaisitti T, Bergui L, et al. CD38 and CD100 lead a network of surface receptors relaying positive signals for B-CLL growth and survival. Blood. 2005;105:3042-3050.
21. Deaglio S, Vaisitti T, Billington R, et al. CD38/CD19: a lipid raft-dependent signaling complex in human B cells. Blood. 2007;109:5390-5398.
22. Funaro A, Morra M, Calosso L, Zini MG, Ausiello CM, Malavasi F. Role of the human CD38 molecule in B cell activation and proliferation. Tissue Antigens. 1997;49:7-15.
23. Frasca L, Fedele G, Deaglio S, et al. CD38 orchestrates migration, survival, and Th1 immune response of human mature dendritic cells. Blood. 2006;107:2392-2399.
24. Klein U, Tu Y, Stolovitzky GA, et al. Gene expression profiling of B cell chronic lymphocytic leukemia reveals a homogeneous phenotype related to memory B cells. J Exp Med. 2001;194:1625-1638.
25. Huttmann A, Klein-Hitpass L, Thomale J, et al. Gene expression signatures separate B-cell chronic lymphocytic leukaemia prognostic subgroups defined by ZAP-70 and CD38 expression status. Leukemia. 2006;20:1774-1782.
26. Sembries S, Pahl H, Stilgenbauer S, Dohner H, Schriever F. Reduced expression of adhesion molecules and cell signaling receptors by chronic lymphocytic leukemia cells with 11q deletion. Blood. 1999;93:624-631.
27. Damle RN, Ghiotto F, Valetto A, et al. B-cell chronic lymphocytic leukemia cells express a surface membrane phenotype of activated, antigen-experienced B lymphocytes. Blood. 2002;99:4087-4093.
28. Trentin L, Zambello R, Sancetta R, et al. B lymphocytes from patients with chronic lymphoproliferative disorders are equipped with different co stimulatory molecules. Cancer Res. 1997;57:4940-4947.
29. Delmer A, Ajchenbaum-Cymbalista F, Tang R, et al. Overexpression of cyclin D2 in chronic B-cell malignancies. Blood. 1995;85:2870-2876.
30. Vrhovac R, Delmer A, Tang R, Marie JP, Zittoun R, Ajchenbaum-Cymbalista F. Prognostic significance of the cell cycle inhibitor p27Kip1 in chronic B-cell lymphocytic leukemia. Blood. 1998;91:4694-4700.
31. Wolowiec D, Ciszak L, Kosmaczewska A, et al. Cell cycle regulatory proteins and apoptosis in B-cell chronic lymphocytic leukemia. Haematologica. 2001;86:1296-1304.
32. Jaroslav P, Martina H, Jiri S, et al. Expression of cyclins D1, D2, and D3 and Ki-67 in leukemia. Leuk Lymphoma. 2005;46:1605-1612.
33. Messmer BT, Messmer D, Allen SL, et al. In vivo measurements document the dynamic cellular kinetics of chronic lymphocytic leukemia B cells. J Clin Invest. 2005;115:755-764.
34. Obermann EC, Went P, Tzankov A, et al. Cell cycle phase distribution analysis in chronic lymphocytic leukaemia: a significant number of cells reside in early G1-phase. J Clin Pathol. 2006;60:794-797.
35. Pepper C, Ward R, Lin TT, et al. Highly purified CD38(+) and CD38(-) sub-clones derived from the same chronic lymphocytic leukemia patient have distinct gene expression signatures despite their monoclonal origin. Leukemia. 2007;21:687-696.
36. Rufer N, Dragowska W, Thornbury G, Roosnek E, Lansdorp PM. Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry. Nat Biotechnol. 1998;16:743-747.
37. Damle RN, Batliwalla FM, Ghiotto F, et al. Telomere length and telomerase activity delineate distinctive replicative features of the B-CLL subgroups defined by immunoglobulin V gene mutations. Blood. 2004;103:375-382.
38. Kim NW, Piatyszek MA, Prowse KR, et al. Specific association of human telomerase activity with immortal cells and cancer. Science. 1994;266:2011-2015.
39. Pascual V, Liu YJ, Magalski A, de Bouteiller O, Banchereau J, Capra JD. Analysis of somatic mutation in five B cell subsets of human tonsil. J Exp Med. 1994;180:329-339.
40. Cutrona G, Colombo M, Matis S, et al. Clonal heterogeneity in CLL cells: response to surface IgM crosslinking is more efficient in CD38, ZAP-70 positive cells. Haematologica. 2007: In press.
41. Hulkkonen J, Vilpo L, Hurme M, Vilpo J. Surface antigen expression in chronic lymphocytic leukemia: clustering analysis, interrelationships and effects of chromosomal abnormalities. Leukemia. 2002;16:178-185.
42. Vilpo J, Tobin G, Hulkkonen J, et al. Mitogen induced activation, proliferation and surface antigen expression patterns in unmutated and hypermutated chronic lymphocytic leukemia cells. Eur J Haematol. 2005;75:34-40.
43. Simms PE, Ellis TM. Utility of flow cytometric detection of CD69 expression as a rapid method for determining poly- and oligoclonal lymphocyte activation. Clin Diagn Lab Immunol. 1996;3:301-304.
44. Shiow LR, Rosen DB, Brdickova N, et al. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature. 2006;440:540-544.
45. Kishimoto TK, Jutila MA, Butcher EC. Identification of a human peripheral lymph node homing receptor: a rapidly down-regulated adhesion molecule. Proc Natl Acad Sci U S A. 1990;87:2244-2248.
46. Shi Y, Agematsu K, Ochs HD, Sugane K. Functional analysis of human memory B-cell subpopulations: IgD+CD27+ B cells are crucial in secondary immune response by producing high affinity IgM. Clin Immunol. 2003;108:128-137.
47. Borst J, Hendriks J, Xiao Y. CD27 and CD70 in T cell and B cell activation. Curr Opin Immunol. 2005;17:275-281.
48. Nolz JC, Tschumper RC, Pittner BT, Darce JR, Kay NE, Jelinek DF. ZAP-70 is expressed by a subset of normal human B-lymphocytes displaying an activated phenotype. Leukemia. 2005;19:1018-1024.
49. Cutrona G, Colombo M, Matis S, et al. B lymphocytes in humans express ZAP-70 when activated in vivo. Eur J Immunol. 2006;36:558-569.
50. Scielzo C, Camporeale A, Geuna M, et al. ZAP-70 is expressed by normal and malignant human B-cell subsets of different maturational stage. Leukemia. 2006;20:689-695.
51. Chen L, Widhopf G, Huynh L, et al. Expression of ZAP-70 is associated with increased B-cell receptor signaling in chronic lymphocytic leukemia. Blood. 2002;100:4609-4614.
52. Chen L, Apgar J, Huynh L, et al. ZAP-70 directly enhances IgM signaling in chronic lymphocytic leukemia. Blood. 2005;105:2036-2041.
53. Richardson SJ, Matthews C, Catherwood MA, et al. ZAP-70 expression is associated with enhanced ability to respond to migratory and survival signals in B-cell chronic lymphocytic leukemia (B-CLL). Blood. 2006;107:3584-3592.
54. Gobessi S, Laurenti L, Longo PG, Sica S, Leone G, Efremov DG. ZAP-70 enhances B-cell-receptor signaling despite absent or inefficient tyrosine kinase activation in chronic lymphocytic leukemia and lymphoma B cells. Blood. 2007;109:2032-2039.
55. Weng NP, Palmer LD, Levine BL, Lane HC, June CH, Hodes RJ. Tales of tails: regulation of telomere length and telomerase activity during lymphocyte development, differentiation, activation, and aging. Immunol Rev. 1997;160:43-54.
56. Igarashi H, Sakaguchi N. Telomerase activity is induced in human peripheral B lymphocytes by the stimulation to antigen receptor. Blood. 1997;89:1299-1307.
57. Blackburn EH. The end of the (DNA) line. Nat Struct Biol. 2000;7:847-850.
58. Porakishvili N, Kulikova N, Jewell AP, et al. Differential expression of CD180 and IgM by B-cell chronic lymphocytic leukaemia cells using mutated and unmutated immunoglobulin VH genes. Br J Haematol. 2005;131:313-319.
59. Zucchetto A, Bomben R, Dal Bo M, et al. A scoring system based on the expression of six surface molecules allows the identification of three prognostic risk groups in B-cell chronic lymphocytic leukemia. J Cell Physiol. 2006;207:354-363.
60. Hultdin M, Rosenquist R, Thunberg U, et al. Association between telomere length and V(H) gene mutation status in chronic lymphocytic leukaemia: clinical and biological implications. Br J Cancer. 2003;88:593-598.
61. Grabowski P, Hultdin M, Karlsson K, et al. Telomere length as a prognostic parameter in chronic lymphocytic leukemia with special reference to VH gene mutation status. Blood. 2005;105:4807-4812.
62. Ricca I, Rocci A, Drandi D, et al. Telomere length identifies two different prognostic subgroups among VH-unmutated B-cell chronic lymphocytic leukemia patients. Leukemia. 2007;21:697-705.
63. Ghia P, Guida G, Stella S, et al. The pattern of CD38 expression defines a distinct subset of chronic lymphocytic leukemia (CLL) patients at risk of disease progression. Blood. 2003;101:1262-1269.
64. Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol. 2000;182:311-322.
65. Pittner BT, Shanafelt TD, Kay NE, Jelinek DF. CD38 expression levels in chronic lymphocytic leukemia B cells are associated with activation marker expression and differential responses to interferon stimulation. Leukemia. 2005;19:2264-2272.
66. Calissano C, Damle R, Banapour T, et al. In vivo labeling of newly synthesized DNA suggests that the CD38+ fraction is enriched in proliferating cells within a clone of chronic lymphocytic leukemia B cells [abstract]. Blood. 2006;108:12a-13a.
67. Kitada S, Andersen J, Akar S, et al. Expression of apoptosis-regulating proteins in chronic lymphocytic leukemia: correlations with in vitro and in vivo chemoresponses. Blood. 1998;91:3379-3389.
68. Granziero L, Ghia P, Circosta P, et al. Survivin is expressed on CD40 stimulation and interfaces proliferation and apoptosis in B-cell chronic lymphocytic leukemia. Blood. 2001;97:2777-2783.
69. Pepper C, Brennan P, Alghazal S, et al. CD38+ chronic lymphocytic leukaemia cells co-express high levels of ZAP-70 and are functionally distinct from their CD38- counter-parts. Leukemia. 2006;20:743-744.
70. Chiorazzi N, Rai KR, Ferrarini M. Chronic lymphocytic leukemia. N Engl J Med. 2005;352:804-815.