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

Volumn 108, Issue 4, 2006, Pages 1135-1144

  Deaglio, Silvia ^a   Vaisitti, Tiziana ^a   Aydin, Semra ^a   Ferrero, Enza ^a   Malavasi, Fabio ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b Biology and Biochemistry ^*  (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD31 ANTIGEN; CD38 ANTIGEN; CHEMOKINE; MEMBRANE RECEPTOR; PLEXIN; PLEXIN B1; PROTEIN; PROTEIN CD100; PROTEIN KINASE ZAP 70; UNCLASSIFIED DRUG;

B LYMPHOCYTE; CELL PROLIFERATION; CELL SURVIVAL; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL RESEARCH; DISEASE COURSE; GENE MUTATION; GENETIC ANALYSIS; GENETIC POLYMORPHISM; HUMAN; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION;

EID: 33747187494     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-01-013003     Document Type: Review

References (123)

1. Rozman C, Montserrat E. Chronic lymphocytic leukemia. N Engl J Med. 1995;333:1052-1057.
2. Caligaris-Cappio F, Hamblin TJ. B-cell chronic lymphocytic leukemia: a bird of a different feather. J Clin Oncol. 1999;17:399-408.
3. Chiorazzi N, Ferrarini M. B cell chronic lymphocytic leukemia: lessons learned from studies of the B cell antigen receptor. Annu Rev Immunol. 2003;21:841-894.
4. Stevenson FK, Caligaris-Cappio F. Chronic lymphocytic leukemia: revelations from the B-cell receptor. Blood. 2004;103:4389-4395.
5. Shanafelt TD, Geyer SM, Kay NE. Prognosis at diagnosis: integrating molecular biologic insights into clinical practice for patients with CLL. Blood. 2004;103:1202-1210.
6. Rai KR, Sawitsky A, Cronkite EP, Chanana AD, Levy RN, Pasternack BS. Clinical staging of chronic lymphocytic leukemia. Blood. 1975;46:219-234.
7. Binet JL, Auquier A, Dighiero G, et al. A new prognostic classification of chronic lymphocytic leukemia derived from a multivariate survival analysis. Cancer. 1981;48:198-206.
8. Rozman C, Montserrat E, Rodriguez-Fernandez JM, et al. Bone marrow histologic pattern: the best single prognostic parameter in chronic lymphocytic leukemia: a multivariate survival analysis of 329 cases. Blood. 1984;64:642-648.
9. Montserrat E, Sanchez-Bisono J, Vinolas N, Rozman C. Lymphocyte doubling time in chronic lymphocytic leukaemia: analysis of its prognostic significance. Br J Haematol. 1986;62:567-575.
10. 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;94:1848-1854.
11. 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.
12. Hamblin TJ, Orchard JA, Gardiner A, Oscier DG, Davis Z, Stevenson FK. Immunoglobulin V genes and CD38 expression in CLL. Blood. 2000;95:2455-2457.
13. Ibrahim S, Keating M, Do KA, et al. CD38 expression as an important prognostic factor in B-cell chronic lymphocytic leukemia. Blood. 2001;98:181-186.
14. Morabito F, Mangiola M, Oliva B, et al. Peripheral blood CD38 expression predicts survival in B-cell chronic lymphocytic leukemia. Leuk Res. 2001;25:927-932.
15. Del Poeta G, Maurillo L, Venditti A, et al. Clinical significance of CD38 expression in chronic lymphocytic leukemia. Blood. 2001;98:2633-2639.
16. D'Arena G, Musto P, Cascavilla N, et al. CD38 expression correlates with adverse biological features and predicts poor clinical outcome in B-cell chronic lymphocytic leukemia. Leuk Lymphoma. 2001;42:109-114.
17. 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.
18. Heintel D, Schwarzinger I, Chizzali-Bonfadin C, et al. Association of CD38 antigen expression with other prognostic parameters in early stages of chronic lymphocytic leukemia. Leuk Lymphoma. 2001;42:1315-1321.
19. Durig J, Naschar M, Schmucker U, et al. CD38 expression is an important prognostic marker in chronic lymphocytic leukaemia. Leukemia. 2002;16:30-35.
20. Chevallier P, Penther D, Avet-Loiseau H, et al. CD38 expression and secondary 17p deletion are important prognostic factors in chronic lymphocytic leukaemia. Br J Haematol. 2002;116:142-150.
21. 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.
22. Domingo-Domenech E, Domingo-Claros A, Gonzalez-Barca E, et al. CD38 expression in B-chronic lymphocytic leukemia: association with clinical presentation and outcome in 155 patients. Haematologica. 2002;87:1021-1027.
23. Mainou-Fowler T, Dignum H, Taylor PR, et al. Quantification improves the prognostic value of CD38 expression in B-cell chronic lymphocytic leukaemia. Br J Haematol. 2002;118:755-761.
24. Hsi ED, Kopecky KJ, Appelbaum FR, et al. Prognostic significance of CD38 and CD20 expression as assessed by quantitative flow cytometry in chronic lymphocytic leukaemia. Br J Haematol. 2003;120:1017-1025.
25. Manocha S, Matrai Z, Osthoff M, Carter A, Pettitt AR. Correlation between cell size and CD38 expression in chronic lymphocytic leukaemia. Leuk Lymphoma. 2003;44:797-800.
26. Chang CC, Liu CZ, Cleveland RP. Relative importance of CD38 expression over myeloid-associated markers expression in predicting the clinical course of B-CLL patients. Leuk Lymphoma. 2003;44:977-982.
27. Ottaggio L, Viaggi S, Zunino A, et al. Chromosome aberrations evaluated by comparative genomic hybridization in B-cell chronic lymphocytic leukemia: correlation with CD38 expression. Haematologica. 2003;88:769-777.
28. Durig J, Nuckel H, Cremer M, et al. ZAP-70 expression is a prognostic factor in chronic lymphocytic leukemia. Leukemia. 2003;17:2426-2434.
29. 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;19:750-758.
30. Gentile M, Mauro FR, Calabrese E, et al. The prognostic value of CD38 expression in chronic lymphocytic leukaemia patients studied prospectively at diagnosis: a single institute experience. Br J Haematol. 2005;130:549-557.
31. Mayr C, Speicher MR, Kofler DM, et al. Chromosomal translocations are associated with poor prognosis in chronic lymphocytic leukemia. Blood. 2006;107:742-751.
32. 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.
33. Del Giudice I, Morilla A, Osuji N, et al. Zeta-chain associated protein 70 and CD38 combined predict the time to first treatment in patients with chronic lymphocytic leukemia. Cancer. 2005;104:2124-2132.
34. 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.
35. Boonstra JG, von't Veer MB, Gratama JW. The use of CD38 expression by monoclonal B lymphocytes as a prognostic factor in B-cell chronic lymphocytic leukemia. J Biol Regul Homeost Agents. 2004;18:340-346.
36. Matrai Z. CD38 as a prognostic marker in CLL. Hematology. 2005;10:39-46.
37. 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.
38. Ghia P, Guida G, Scielzo C, Geuna M, Caligaris-Cappio F. CD38 modifications in chronic lymphocytic leukemia: are they relevant? Leukemia. 2004;18:1733-1735.
39. Alessio M, Roggero S, Funaro A, et al. CD38 molecule: structural and biochemical analysis on human T lymphocytes, thymocytes, and plasma cells. J Immunol. 1990;145:878-884.
40. Funaro A, Horenstein AL, Calosso L, et al. Identification and characterization of an active soluble form of human CD38 in normal and pathological fluids. Int Immunol. 1996;8:1643-1650.
41. Mallone R, Ferrua S, Morra M, et al. Characterization of a CD38-like 78-kilodalton soluble protein released from B cell lines derived from patients with X-linked agammaglobulinemia. J Clin Invest. 1998;101:2821-2830.
42. Umar S, Malavasi F, Mehta K. Post-translational modification of CD38 protein into a high molecular weight form alters its catalytic properties. J Biol Chem. 1996;271:15922-15927.
43. Mehta K, Shahid U, Malavasi F. Human CD38, a cell-surface protein with multiple functions. FASEB J. 1996;10:1408-1417.
44. Funaro A, De Monte LB, Dianzani U, Forni M, Malavasi F. Human CD38 is associated to distinct molecules which mediate transmembrane signaling in different lineages. Eur J Immunol. 1993;23:2407-2411.
45. Morra M, Zubiaur M, Terhorst C, Sancho J, Malavasi F. CD38 is functionally dependent on the TCR/CD3 complex in human T cells. FASEB J. 1998;12:581-592.
46. Lund FE, Yu N, Kim KM, Reth M, Howard MC. Signaling through CD38 augments B cell antigen receptor (BCR) responses and is dependent on BCR expression. J Immunol. 1996;157:1455-1467.
47. 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.
48. Deaglio S, Zubiaur M, Gregorini A, et al. Human CD38 and CD16 are functionally dependent and physically associated in natural killer cells. Blood. 2002;99:2490-2498.
49. Zilber MT, Gregory S, Mallone R, et al. CD38 expressed on human monocytes: a coaccessory molecule in the superantigen-induced proliferation. Proc Natl Acad Sci U S A. 2000;97:2840-2845.
50. Zilber MT, Setterblad N, Vasselon T, et al. MHC class II/CD38/CD9: a lipid-raft-dependent signaling complex in human monocytes. Blood. 2005;106:3074-3081.
51. 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.
52. Zubiaur M, Fernandez O, Ferrero E, et al. CD38 is associated with lipid rafts and upon receptor stimulation leads to Akt/protein kinase B and Erk activation in the absence of the CD3-zeta immune receptor tyrosine-based activation motifs. J Biol Chem. 2002;277:13-22.
53. Munoz P, Navarro MD, Pavon EJ, et al. CD38 signaling in T cells is initiated within a subset of membrane rafts containing Lck and the CD3-zeta subunit of the T cell antigen receptor. J Biol Chem. 2003;278:50791-50802.
54. Bhan AK, Reinherz EL, Poppema S, McCluskey RT, Schlossman SF. Location of T cell and major histocompatibility complex antigens in the human thymus. J Exp Med. 1980;152:771-782.
55. Terhorst C, van Agthoven A, LeClair K, Snow P, Reinherz E, Schlossman S. Biochemical studies of the human thymocyte cell-surface antigens T6, T9 and T10. Cell. 1981;23:771-780.
56. Deaglio S, Mehta K, Malavasi F. Human CD38: a (r)evolutionary story of enzymes and receptors. Leuk Res. 2001;25:1-12.
57. Howard M, Grimaldi JC, Bazan JF, et al. Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science. 1993;262:1056-1059.
58. Schuber F, Lund FE. Structure and enzymology of ADP-ribosyl cyclases: conserved enzymes that produce multiple calcium mobilizing metabolites. Curr Mol Med. 2004;4:249-261.
59. Lee HC. Physiological functions of cyclic ADP-ribose and NAADP as calcium messengers. Annu Rev Pharmacol Toxicol. 2001;41:317-345.
60. Guse AH. Cyclic ADP-ribose (cADPR) and nicotinic acid adenine dinucleotide phosphate (NAADP): novel regulators of Ca2+-signaling and cell function. Curr Mol Med. 2002;2:273-282.
61. De Flora A, Zocchi E, Guida L, Franco L, Bruzzone S. Autocrine and paracrine calcium signaling by the CD38/NAD+/cyclic ADP-ribose system. Ann N Y Acad Sci. 2004;1028:176-191.
62. Krebs C, Adriouch S, Braasch F, et al. CD38 controls ADP- ribosyltransferase-2-catalyzed ADP-ribosylation of T cell surface proteins. J Immunol. 2005;174:3298-3305.
63. Malavasi F, Funaro A, Roggero S, Horenstein A, Calosso L, Mehta K. Human CD38: a glycoprotein in search of a function. Immunol Today. 1994;15:95-97.
64. Deaglio S, Malavasi F. Human CD38: a receptor, an (ecto)enzyme, a disease marker and lots more. Modern Aspct Immunobiol. 2002;2:121-125.
65. Kitanaka A, Suzuki T, Ito C, et al. CD38-mediated signaling events in murine pro-B cells expressing human CD38 with or without its cytoplasmic domain. J Immunol. 1999;162:1952-1958.
66. Kontani K, Kukimoto I, Nishina H, et al. Tyrosine phosphorylation of the c-cbl proto-oncogene product mediated by cell surface antigen CD38 in HL-60 cells. J Biol Chem. 1996;271:1534-1537.
67. Mallone R, Funaro A, Zubiaur M, et al. Signaling through CD38 induces NK cell activation. Int Immunol. 2001;13:397-409.
68. Zubiaur M, Izquierdo M, Terhorst C, Malavasi F, Sancho J. CD38 ligation results in activation of the Raf-1/mitogen-activated protein kinase and the CD3-zeta/zeta-associated protein-70 signaling pathways in Jurkat T lymphocytes. J Immunol. 1997;159:193-205.
69. Silvennoinen O, Nishigaki H, Kitanaka A, et al. CD38 signal transduction in human B cell precursors: rapid induction of tyrosine phosphorylation, activation of syk tyrosine kinase, and phosphorylation of phospholipase C-gamma and phosphatidylinositol 3-kinase. J Immunol. 1996;156:100-107.
70. Moreno-Garcia ME, Lopez-Bojorques LN, Zentella A, Humphries LA, Rawlings DJ, Santos-Argumedo L. CD38 signaling regulates B lymphocyte activation via a phospholipase C (PLC)-gamma 2-independent, protein kinase C, phosphatidylcholine-PLC, and phospholipase D-dependent signaling cascade. J Immunol. 2005;174:2687-2695.
71. Munshi C, Aarhus R, Graeff R, Walseth TF, Levitt D, Lee HC. Identification of the enzymatic active site of CD38 by site-directed mutagenesis. J Biol Chem. 2000;275:21566-21571.
72. Deaglio S, Dianzani U, Horenstein AL, et al. Human CD38 ligand: a 120-KDA protein predominantly expressed on endothelial cells. J Immunol. 1996;156:727-734.
73. 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.
74. Deaglio S, Mallone R, Baj G, et al. CD38/CD31, a receptor/ligand system ruling adhesion and signaling in human leukocytes. Chem Immunol. 2000;75:99-120.
75. Lund FE, Muller-Steffner HM, Yu N, Stout CD, Schuber F, Howard MC. CD38 signaling in B lymphocytes is controlled by its ectodomain but occurs independently of enzymatically generated ADP-ribose or cyclic ADP-ribose. J Immunol. 1999;162:2693-2702.
76. Cho YS, Han MK, Choi YB, Yun Y, Shin J, Kim UH. Direct interaction of the CD38 cytoplasmic tail and the Lck SH2 domain: Cd38 transduces T cell activation signals through associated Lck. J Biol Chem. 2000;275:1685-1690.
77. Deaglio S, Mallone R, Baj G, et al. Human CD38 and its ligand CD31 define a unique lamina propria T lymphocyte signaling pathway. FASEB J. 2001;15:580-582.
78. Ferrero E, Malavasi F. Human CD38, a leukocyte receptor and ectoenzyme, is a member of a novel eukaryotic gene family of nicotinamide adenine dinucleotide+-converting enzymes: extensive structural homology with the genes for murine bone marrow stromal cell antigen 1 and aplysian ADP-ribosyl cyclase. J Immunol. 1997;159:3858-3865.
79. Ferrero E, Saccucci F, Malavasi F. The human CD38 gene: polymorphism, CpG island, and linkage to the CD157 (BST-1) gene. Immunogenetics. 1999;49:597-604.
80. Ferrero E, Malavasi F. A Natural History of the Human CD38 Gene. London, United Kingdom: Kluwer Academic Publishers; 2002.
81. Deaglio S, Malavasi F. The CD38/CD157 mammalian gene family: an evolutionary paradigm for other leukocyte surface enzymes. Purinergic Signaling. In press.
82. 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.
83. Bohnhorst JO, Bjorgan MB, Thoen JE, Natvig JB, Thompson KM. Bm1-Bm5 classification of peripheral blood B cells reveals circulating germinal center founder cells in healthy individuals and disturbance in the B cell subpopulations in patients with primary Sjogren's syndrome. J Immunol. 2001;167:3610-3618.
84. Tangye SG, Avery DT, Hodgkin PD. A division-linked mechanism for the rapid generation of Ig-secreting cells from human memory B cells. J Immunol. 2003;170:261-269.
85. d'Arbonneau F, Pers JO, Devauchelle V, Pennec Y, Saraux A, Youinou P. BAFF-induced changes in B cell antigen receptor-containing lipid rafts in Sjogren's syndrome. Arthritis Rheum. 2006;54:115-126.
86. Martin F, Kearney JF. Marginal-zone B cells. Nat Rev Immunol. 2002;2:323-335.
87. Dono M, Zupo S, Leanza N, et al. Heterogeneity of tonsillar subepithelial B lymphocytes, the splenic marginal zone equivalents. J Immunol. 2000;164:5596-5604.
88. 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.
89. Kumagai M, Coustan-Smith E, Murray DJ, et al. Ligation of CD38 suppresses human B lymphopoiesis. J Exp Med. 1995;181:1101-1110.
90. Kitanaka A, Ito C, Nishigaki H, Campana D. CD38-mediated growth suppression of B-cell progenitors requires activation of phosphatidylinositol 3-kinase and involves its association with the protein product of the c-cbl proto-oncogene. Blood. 1996;88:590-598.
91. Kitanaka A, Ito C, Coustan-Smith E, Campana D. CD38 ligation in human B cell progenitors triggers tyrosine phosphorylation of CD19 and association of CD19 with lyn and phosphatidylinositol 3-kinase. J Immunol. 1997;159:184-192.
92. Deaglio S, Vaisitti T, Malavasi F. Role of human CD38 in B cell signaling. VIII HLDA Meeting Adelaide, Australia; 2004.
93. Zupo S, Rugari E, Dono M, Taborelli G, Malavasi F, Ferrarini M. CD38 signaling by agonistic monoclonal antibody prevents apoptosis of human germinal center B cells. Eur J Immunol. 1994;24:1218-1222.
94. 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.
95. Chiorazzi N, Rai KR, Ferrarini M. Chronic lymphocytic leukemia. N Engl J Med. 2005;352:804-815.
96. 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.
97. 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.
98. 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.
99. Jaksic O, Paro MM, Kardum Skelin I, Kusec R, Pejsa V, Jaksic B. CD38 on B-cell chronic lymphocytic leukemia cells has higher expression in lymph nodes than in peripheral blood or bone marrow. Blood. 2004;103:1968-1969.
100. 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.
101. 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.
102. Elhabazi A, Marie-Cardine A, Chabbert-de Ponnat I, Bensussan A, Boumsell L. Structure and function of the immune semaphorin CD100/SEMA4D. Crit Rev Immunol. 2003;23:65-81.
103. Kumanogoh A, Kikutani H. Roles of the semaphorin family in immune regulation. Adv Immunol. 2003;81:173-198.
104. Kumanogoh A, Kikutani H. The CD100-CD72 interaction: a novel mechanism of immune regulation. Trends Immunol. 2001;22:670-676.
105. Burger JA, Tsukada N, Burger M, Zvaifler NJ, Dell'Aquila M, Kipps TJ. Blood-derived nurse-like cells protect chronic lymphocytic leukemia B cells from spontaneous apoptosis through stromal cell-derived factor-1. Blood. 2000;96:2655-2663.
106. Tsukada N, Burger JA, Zvaifler NJ, Kipps TJ. Distinctive features of "nurselike" cells that differentiate in the context of chronic lymphocytic leukemia. Blood. 2002;99:1030-1037.
107. Hamblin AD, Hamblin TJ. Functional and prognostic role of ZAP-70 in chronic lymphocytic leukaemia. Expert Opin Ther Targets. 2005;9:1165-1178.
108. Chan AC, van Oers NS, Tran A, et al. Differential expression of ZAP-70 and Syk protein tyrosine kinases, and the role of this family of protein tyrosine kinases in TCR signaling. J Immunol. 1994;152:4758-4766.
109. Kuroyama H, Ikeda T, Kasai M, et al. Identification of a novel isoform of ZAP-70, truncated ZAP kinase. Biochem Biophys Res Commun. 2004;315:935-941.
110. Rao N, Dodge I, Band H. The Cbl family of ubiquitin ligases: critical negative regulators of tyrosine kinase signaling in the immune system. J Leukoc Biol. 2002;71:753-763.
111. Schweighoffer E, Vanes L, Mathiot A, Nakamura T, Tybulewicz VL. Unexpected requirement for ZAP-70 in pre-B cell development and allelic exclusion. Immunity. 2003;18:523-533.
112. 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.
113. Deaglio S, Vaisitti T, Malavasi F. CD38 ligation in B-chronic lymphocytic leukemia cells induces sequential tyrosine phosphorylation of ZAP-70, PLC-g2 and ERK1/2 proteins [abstract]. Blood. 2004;104. Abstract 959.
114. 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.
115. Peacock JW, Jirik FR. TCR activation inhibits chemotaxis toward stromal cell-derived factor-1: evidence for reciprocal regulation between CXCR4 and the TCR. J Immunol. 1999;162:215-223.
116. Ottoson NC, Pribila JT, Chan AS, Shimizu Y. Cutting edge: T cell migration regulated by CXCR4 chemokine receptor signaling to ZAP-70 tyrosine kinase. J Immunol. 2001;167:1857-1861.
117. 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 leukaemia (B-CLL). Blood. 2006;107:3584-3592.
118. Partida-Sanchez S, Iribarren P, Moreno-Garcia ME, et al. Chemotaxis and calcium responses of phagocytes to formyl peptide receptor ligands is differentially regulated by cyclic ADP ribose. J Immunol. 2004;172:1896-1906.
119. Behar E, Chao NJ, Hiraki DD, et al. Polymorphism of adhesion molecule CD31 and its role in acute graft-versus-host disease. N Engl J Med. 1996;334:286-291.
120. Ortolan E, Vacca P, Capobianco A, et al. CD157, the Janus of CD38 but with a unique personality. Cell Biochem Funct. 2002;20:309-322.
121. Shimaoka Y, Attrep JF, Hirano T, et al. Nurse-like cells from bone marrow and synovium of patients with rheumatoid arthritis promote survival and enhance function of human B cells. J Clin Invest. 1998;102:606-618.
122. Podesta M, Benvenuto F, Pitto A, et al. Concentrative uptake of cyclic ADP-ribose generated by BST-1+ stroma stimulates proliferation of human hematopoietic progenitors. J Biol Chem. 2005;280:5343-5349.
123. Malavasi F. Old and new drugs join forces against hematologic malignancies. Blood. 2005;106:1513-1514.