Best Practice & Research Clinical Haematology
Volume 20, Issue 3 , Pages 385-397 , September 2007

The normal counterpart to the chronic lymphocytic leukemia B cell

  • Federico Caligaris-Cappio, MD (Professor of Internal Medicine, Director of the Department of Oncology)

      Affiliations

    • Corresponding Author InformationCorresponding author. Tel.: +39 02 2643 2390; Fax: +39 02 2643 4723.
  • ,
  • Paolo Ghia, MD, PhD (Assistant Professor of Intenal Medicine, Scientific coordinator of the Lymphoma Unit)

References 

  1. Ghia P, Caligaris-Cappio F. The origin of B-cell chronic lymphocytic leukemia. Seminars in Oncology. 2006;33:150–156
  2. Caligaris-Cappio F, Gobbi M, Bofill M, et al. Infrequent normal B lymphocytes express features of B-chronic lymphocytic leukemia. The Journal of Experimental Medicine. 1982;155:623–628
  3. Montecino-Rodriguez E, Leathers H, Dorshkind K. Identification of a B-1 B cell-specified progenitor. Nature Immunology. 2006;7:293–301
  4. Kantor A. A new nomenclature for B cells. Immunology Today. 1991;12:388
  5. Montecino-Rodriguez E, Dorshkind K. New perspectives in B-1 B cell development and function. Trends in Immunology. 2006;27:428–433
  6. Stall AM, Farinas MC, Tarlinton DM, et al. Ly-1 B-cell clones similar to human chronic lymphocytic leukemias routinely develop in older normal mice and young autoimmune (New Zealand Black-related) animals. Proceedings of the National Academy of Sciences of the United States of America. 1988;85:7312–7316
  7. Chiorazzi N, Ferrarini M. B cell chronic lymphocytic leukemia: lessons learned from studies of the B cell antigen receptor. Annual Review of Immunology. 2003;21:841–894
  8. Morikawa K, Oseko F, Morikawa S. Induction of CD5 antigen on human CD5- B cells by stimulation with Staphylococcus aureus Cowan strain I. International Immunology. 1993;5:809–816
  9. Caligaris-Cappio F, Hamblin TJ. B-cell chronic lymphocytic leukemia: a bird of a different feather. Journal of Clinical Oncology. 1999;17:399–408
  10. Rickinson AB, Finerty S, Epstein MA. Interaction of Epstein–Barr virus with leukaemic B cells in vitro. I. Abortive infection and rare cell line establishment from chronic lymphocytic leukaemic cells. Clinical and Experimental Immunology. 1982;50:347–354
  11. Caligaris-Cappio F, Ghia P. The nature and origin of the B-chronic lymphocytic leukemia cell: a tentative model. Hematology/Oncology Clinics of North America. 2004;18:849–862viii
  12. Brossard C, Semichon M, Trautmann A, et al. CD5 inhibits signaling at the immunological synapse without impairing its formation. Journal of Immunology (Baltimore, Md.). 2003;170:4623–4629
  13. Kipps TJ, Carson DA. Autoantibodies in chronic lymphocytic leukemia and related systemic autoimmune diseases. Blood. 1993;81:2475–2487
  14. Youinou P, Pers JO, Jamin C, et al. CD5-positive B cells at the crossroads of B cell malignancy and nonorgan-specific autoimmunity. Pathologie-biologie. 2000;48:574–576
  15. Casali P, Burastero SE, Nakamura M, et al. Human lymphocytes making rheumatoid factor and antibody to ssDNA belong to Leu-1+ B-cell subset. Science. 1987;236:77–81
  16. Caligaris-Cappio F, Riva M, Tesio L, et al. Human normal CD5+ B lymphocytes can be induced to differentiate to CD5- B lymphocytes with germinal center cell features. Blood. 1989;73:1259–1263
  17. Stevenson FK, Caligaris-Cappio F. Chronic lymphocytic leukemia: revelations from the B-cell receptor. Blood. 2004;103:4389–4395
  18. Vuillier F, Dumas G, Magnac C, et al. Lower levels of surface B-cell-receptor expression in chronic lymphocytic leukemia are associated with glycosylation and folding defects of the mu and CD79a chains. Blood. 2005;105:2933–2940
  19. Alfarano A, Indraccolo S, Circosta P, et al. An alternatively spliced form of CD79b gene may account for altered B- cell receptor expression in B-chronic lymphocytic leukemia. Blood. 1999;93:2327–2335
  20. Kurosaki T. Regulation of B cell fates by BCR signaling components. Current Opinion in Immunology. 2002;14:341–347
  21. 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
  22. Lanham S, Hamblin T, Oscier D, et al. Differential signaling via surface IgM is associated with VH gene mutational status and CD38 expression in chronic lymphocytic leukemia. Blood. 2003;101:1087–1093
  23. Moreau EJ, Matutes E, A'Hern RP, et al. Improvement of the chronic lymphocytic leukemia scoring system with the monoclonal antibody SN8 (CD79b). American Journal of Clinical Pathology. 1997;108:378–382
  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. The Journal of Experimental Medicine. 2001;194:1625–1638
  25. Hamblin T. Is chronic lymphocytic leukemia one disease?. Haematologica. 2002;87:1235–1238
  26. Hamblin TJ, Davis Z, Gardiner A, et al. Unmutated Ig V(H) genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood. 1999;94:1848–1854
  27. 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
  28. Crespo M, Bosch F, Villamor N, et al. ZAP-70 expression as a surrogate for immunoglobulin-variable-region mutations in chronic lymphocytic leukemia. The New England Journal of Medicine. 2003;348:1764–1775
  29. 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
  30. Law CL, Sidorenko SP, Chandran KA, et al. Molecular cloning of human Syk. A B cell protein-tyrosine kinase associated with the surface immunoglobulin M-B cell receptor complex. The Journal of Biological Chemistry. 1994;269:12310–12319
  31. Zupo S, Massara R, Dono M, et al. Apoptosis or plasma cell differentiation of CD38-positive B-chronic lymphocytic leukemia cells induced by cross-linking of surface IgM or IgD. Blood. 2000;95:1199–1206
  32. Zupo S, Isnardi L, Megna M, et al. CD38 expression distinguishes two groups of B-cell chronic lymphocytic leukemias with different responses to anti-IgM antibodies and propensity to apoptosis. Blood. 1996;88:1365–1374
  33. Lankester AC, van Schijndel GM, van der Schoot CE, et al. Antigen receptor nonresponsiveness in chronic lymphocytic leukemia B cells. Blood. 1995;86:1090–1097
  34. Pers JO, Berthou C, Porakishvili N, et al. CD5-induced apoptosis of B cells in some patients with chronic lymphocytic leukemia. Leukemia. 2002;16:44–52
  35. Ghia P, Transidico P, Veiga JP, et al. Chemoattractants MDC and TARC are secreted by malignant B-cell precursors following CD40 ligation and support the migration of leukemia-specific T cells. Blood. 2001;98:533–540
  36. 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
  37. 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
  38. Neuland CY, Blattner WA, Mann DL, et al. Familial chronic lymphocytic leukemia. Journal of the National Cancer Institute. 1983;71:1143–1150
  39. Yuille MR, Matutes E, Marossy A, et al. Familial chronic lymphocytic leukaemia: a survey and review of published studies. British Journal of Haematology. 2000;109:794–799
  40. Rawstron AC, Kennedy B, Evans PA, et al. Quantitation of minimal disease levels in chronic lymphocytic leukemia using a sensitive flow cytometric assay improves the prediction of outcome and can be used to optimize therapy. Blood. 2001;98:29–35
  41. Rawstron AC, Green MJ, Kuzmicki A, et al. Monoclonal B lymphocytes with the characteristics of ‘indolent’ chronic lymphocytic leukemia are present in 3.5% of adults with normal blood counts. Blood. 2002;100:635–639
  42. Ghia P, Prato G, Scielzo C, et al. Monoclonal CD5+ and CD5- B-lymphocyte expansions are frequent in the peripheral blood of the elderly. Blood. 2004;103:2337–2342
  43. Marti GE, Rawstron AC, Ghia P, et al. Diagnostic criteria for monoclonal B-cell lymphocytosis. British Journal of Haematology. 2005;130:325–332
  44. Rawstron AC, Yuille MR, Fuller J, et al. Inherited predisposition to CLL is detectable as subclinical monoclonal B-lymphocyte expansion. Blood. 2002;100:2289–2290
  45. Ji W, Qu GZ, Ye P, et al. Frequent detection of bcl-2/JH translocations in human blood and organ samples by a quantitative polymerase chain reaction assay. Cancer Research. 1995;55:2876–2882
  46. Kyle RA, Therneau TM, Rajkumar SV, et al. A long-term study of prognosis in monoclonal gammopathy of undetermined significance. The New England Journal of Medicine. 2002;346:564–569
  47. Ryan CJ, Small EJ. Prostate cancer update: 2005. Current Opinion in Oncology. 2006;18:284–288
  48. Ghia P, Granziero L, Chilosi M, et al. Chronic B cell malignancies and bone marrow microenvironment. Seminars in Cancer Biology. 2002;12:149–155
  49. Liu YJ, Joshua DE, Williams GT, et al. Mechanism of antigen-driven selection in germinal centres. Nature. 1989;342:929–931
  50. Mackay IR, Rose NR. Autoimmunity and lymphoma: tribulations of B cells. Nature Immunology. 2001;2:793–795
  51. Suarez F, Lortholary O, Hermine O, et al. Infection-associated lymphomas derived from marginal zone B cells: a model of antigen-driven lymphoproliferation. Blood. 2006;107:3034–3044
  52. Wotherspoon AC, Doglioni C, Diss TC, et al. Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet. 1993;342:575–577
  53. Jelic S, Filipovic-Ljeskovic I. Positive serology for Lyme disease borrelias in primary cutaneous B-cell lymphoma: a study in 22 patients; is it a fortuitous finding?. Hematological Oncology. 1999;17:107–116
  54. Ferreri AJ, Guidoboni M, Ponzoni M, et al. Evidence for an association between Chlamydia psittaci and ocular adnexal lymphomas. Journal of the National Cancer Institute. 2004;96:586–594
  55. Silvestri F, Pipan C, Barillari G, et al. Prevalence of hepatitis C virus infection in patients with lymphoproliferative disorders. Blood. 1996;87:4296–4301
  56. Kassan SS, Thomas TL, Moutsopoulos HM, et al. Increased risk of lymphoma in sicca syndrome. Annals of Internal Medicine. 1978;89:888–892
  57. Lindsay S, Dailey ME. Malignant lymphoma of the thyroid gland and its relation to Hashimoto disease: a clinical and pathologic study of 8 patients. The Journal of Clinical Endocrinology and Metabolism. 1955;15:1332–1353
  58. Fais F, Ghiotto F, Hashimoto S, et al. Chronic lymphocytic leukemia B cells express restricted sets of mutated and unmutated antigen receptors. The Journal of Clinical Investigation. 1998;102:1515–1525
  59. Kuppers R. Somatic hypermutation and B cell receptor selection in normal and transformed human B cells. Annals of the New York Academy of Sciences. 2003;987:173–179
  60. Wabl M, Cascalho M, Steinberg C. Hypermutation in antibody affinity maturation. Current Opinion in Immunology. 1999;11:186–189
  61. Berek C, Berger A, Apel M. Maturation of the immune response in germinal centers. Cell. 1991;67:1121–1129
  62. MacLennan IC. Germinal centers. Annual Review of Immunology. 1994;12:117–139
  63. William J, Euler C, Christensen S, et al. Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science. 2002;297:2066–2070
  64. Belessi CJ, Davi FB, Stamatopoulos KE, et al. IGHV gene insertions and deletions in chronic lymphocytic leukemia: ‘CLL-biased’ deletions in a subset of cases with stereotyped receptors. European Journal of Immunology. 2006;36:1963–1974
  65. Tobin G, Thunberg U, Johnson A, et al. Chronic lymphocytic leukemias utilizing the VH3-21 gene display highly restricted Vlambda2-14 gene use and homologous CDR3s: implicating recognition of a common antigen epitope. Blood. 2003;101:4952–4957
  66. Kipps TJ, Tomhave E, Pratt LF, et al. Developmentally restricted immunoglobulin heavy chain variable region gene expressed at high frequency in chronic lymphocytic leukemia. Proceedings of the National Academy of Sciences of the United States of America. 1989;86:5913–5917
  67. Kipps TJ. Immunoglobulin genes in chronic lymphocytic leukemia. Blood Cells. 1993;19:615–625
  68. Johnson TA, Rassenti LZ, Kipps TJ. Ig VH1 genes expressed in B cell chronic lymphocytic leukemia exhibit distinctive molecular features. Journal of Immunology (Baltimore, Md.). 1997;158:235–246
  69. Widhopf GF, Rassenti LZ, Toy TL, et al. Chronic lymphocytic leukemia B cells of more than 1% of patients express virtually identical immunoglobulins. Blood. 2004;104:2499–2504
  70. Tobin G, Thunberg U, Karlsson K, et al. Subsets with restricted immunoglobulin gene rearrangement features indicate a role for antigen selection in the development of chronic lymphocytic leukemia. Blood. 2004;104:2879–2885
  71. Ghiotto F, Fais F, Valetto A, et al. Remarkably similar antigen receptors among a subset of patients with chronic lymphocytic leukemia. The Journal of Clinical Investigation. 2004;113:1008–1016
  72. Messmer BT, Albesiano E, Efremov DG, et al. Multiple distinct sets of stereotyped antigen receptors indicate a role for antigen in promoting chronic lymphocytic leukemia. The Journal of Experimental Medicine. 2004;200:519–525
  73. Ghia P, Stamatopoulos K, Belessi C, et al. Geographic patterns and pathogenetic implications of IGHV gene usage in chronic lymphocytic leukemia: the lesson of the IGHV3-21 gene. Blood. 2005;105:1678–1685
  74. Stamatopoulos K, Belessi C, Moreno C, et al. Over 20% of patients with chronic lymphocytic leukemia carry stereotyped receptors: pathogenetic implications and clinical correlations. Blood. 2007;109:259–270
  75. De Re V, De Vita S, Marzotto A, et al. Sequence analysis of the immunoglobulin antigen receptor of hepatitis C virus-associated non-Hodgkin lymphomas suggests that the malignant cells are derived from the rheumatoid factor-producing cells that occur mainly in type II cryoglobulinemia. Blood. 2000;96:3578–3584
  76. Pritsch O, Magnac C, Dumas G, et al. V gene usage by seven hybrids derived from CD5+ B-cell chronic lymphocytic leukemia and displaying autoantibody activity. Blood. 1993;82:3103–3112
  77. Martin T, Duffy SF, Carson DA, Kipps TJ. Evidence for somatic selection of natural autoantibodies. The Journal of Experimental Medicine. 1992;175:983–991
  78. Martin T, Crouzier R, Weber JC, et al. Structure-function studies on a polyreactive (natural) autoantibody. Polyreactivity is dependent on somatically generated sequences in the third complementarity-determining region of the antibody heavy chain. Journal of Immunology (Baltimore, Md.). 1994;152:5988–5996
  79. Herve M, Xu K, Ng YS, et al. Unmutated and mutated chronic lymphocytic leukemias derive from self-reactive B cell precursors despite expressing different antibody reactivity. The Journal of Clinical Investigation. 2005;115:1636–1643
  80. Hillson JL, Karr NS, Oppliger IR, et al. The structural basis of germline-encoded VH3 immunoglobulin binding to staphylococcal protein A. The Journal of Experimental Medicine. 1993;178:331–336
  81. 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
  82. Casola S, Otipoby KL, Alimzhanov M, et al. B cell receptor signal strength determines B cell fate. Nature Immunology. 2004;5:317–327
  83. Melchers F, Rolink AR. B cell tolerance–how to make it and how to break it. Current Topics in Microbiology and Immunology. 2006;305:1–23
  84. Chan AC, Iwashima M, Turck CW, et al. ZAP-70: a 70 kd protein-tyrosine kinase that associates with the TCR zeta chain. Cell. 1992;71:649–662
  85. Rosenwald A, Alizadeh AA, Widhopf G, et al. Relation of gene expression phenotype to immunoglobulin mutation genotype in B cell chronic lymphocytic leukemia. The Journal of Experimental Medicine. 2001;194:1639–1647
  86. 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
  87. Nolz JC, Tschumper RC, Pittner BT, et al. ZAP-70 is expressed by a subset of normal human B-lymphocytes displaying an activated phenotype. Leukemia. 2005;19:1018–1024
  88. Cutrona G, Colombo M, Matis S, et al. B lymphocytes in humans express ZAP-70 when activated in vivo. European Journal of Immunology. 2006;36:558–569
  89. Yamanashi Y, Okada M, Semba T, et al. Identification of HS1 protein as a major substrate of protein-tyrosine kinase(s) upon B-cell antigen receptor-mediated signaling. Proceedings of the National Academy of Sciences of the United States of America. 1993;90:3631–3635
  90. Scielzo C, Ghia P, Conti A, et al. HS1 protein is differentially expressed in chronic lymphocytic leukemia patient subsets with good or poor prognoses. The Journal of Clinical Investigation. 2005;115:1644–1650
  91. 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
  92. Messmer BT, Messmer D, Allen SL, et al. In vivo measurements document the dynamic cellular kinetics of chronic lymphocytic leukemia B cells. The Journal of Clinical Investigation. 2005;115:755–764
  93. Corcione A, Aloisi F, Serafini B, et al. B-cell differentiation in the CNS of patients with multiple sclerosis. Autoimmunity Reviews. 2005;4:549–554
  94. Pizzolo G, Chilosi M, Ambrosetti A, et al. Immunohistologic study of bone marrow involvement in B-chronic lymphocytic leukemia. Blood. 1983;62:1289–1296
  95. Buske C, Gogowski G, Schreiber K, et al. Stimulation of B-chronic lymphocytic leukemia cells by murine fibroblasts, IL-4, anti-CD40 antibodies, and the soluble CD40 ligand. Experimental Hematology. 1997;25:329–337
  96. Fluckiger AC, Rossi JF, Bussel A, et al. Responsiveness of chronic lymphocytic leukemia B cells activated via surface Igs or CD40 to B-cell tropic factors. Blood. 1992;80:3173–3181
  97. Kitada S, Zapata JM, Andreeff M, et al. Bryostatin and CD40-ligand enhance apoptosis resistance and induce expression of cell survival genes in B-cell chronic lymphocytic leukaemia. British Journal of Haematology. 1999;106:995–1004

PII: S1521-6926(07)00021-7

doi: 10.1016/j.beha.2007.02.005

Best Practice & Research Clinical Haematology
Volume 20, Issue 3 , Pages 385-397 , September 2007