The CD38 lymphocyte differentiation marker: New insight into its ectoenzymatic activity and its role as a signal transducer

Immunity

Volumn 7, Issue 3, 1997, Pages 315-324

  Shubinsky, George ^a   Schlesinger, Michael ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CD38 ANTIGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

B LYMPHOCYTE; ENZYME ACTIVITY; GROWTH REGULATION; HUMAN; LYMPHOCYTE DIFFERENTIATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

EID: 0030820079     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80353-2     Document Type: Review

References (99)

1. Aarhus, R., Graeff, R.M., Dickey, D.M., Walseth, T.F., and Lee, H.C. (1995). ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium-mobilizing metabolite from NADP. J. Biol. Chem. 270, 30327-30333.
2. Aiken, C., Konner, J., Landau, N.R., Lenburg, M.E., and Trono, D. (1994). Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 76, 853-864.
3. Alessio, M., Roggero, S., Funaro, A., De Monte, L.B., Peruzzi, L., Geuna, M., and Malavasi, F. (1990). CD38 molecule: structural and biochemical analysis on human T lymphocytes, thymocytes, and plasma cells. J. Immunol. 145, 878-886.
4. Ausiello, C.M., Urbani, F., la Sala, A., Funaro, A., and Malavasi, F. (1995). CD38 ligation induces discrete cytokine mRNA expression in human cultured lymphocytes. Eur. J. Immunol. 25, 1477-1480.
5. Banchereau, J., and Rousset, F. (1992). Human B lymphocytes: phenotype, proliferation and differentiation. Adv. Immunol. 52, 125-262.
6. +CD4-CD8-thymocytes. Int. Immunol. 7, 213-221.
7. Beers, K.W., Chini, E.N., and Dousa, T.P. (1995). All-trans-retinoic acid stimulates synthesis of cyclic ADP-ribose in renal LLC-PK1 cells. J. Clin. Invest. 95, 2385-2390.
8. + thymocytes, and B cell maturation. J. Exp. Med. 183, 1707-1717.
9. Chan, A.C., Desai, D.M., and Weiss, A. (1994). The role of protein tyrosine kinases and protein tyrosinephosphatasesin T cell antigen receptor signal transduction. Annu. Rev. Immunol. 12, 555-592.
10. Deaglio, S., Dianzani, U., Horenstein, A.L., Fernandez, J.E., van Kooten, C., Bragardo, M., Funaro, A., Garbarino, G., Di Virgilio, F., Banchereau, J., et al. (1996). Human CD38 ligand: a 120-KDA protein predominantly expressed on endothelial cells. J. Immunol. 156, 727-734.
11. Debili, N., Coulombel, L., Croisille, L., Katz, A., Guichard, J., Breton-Gorius, J., and Vainchenker, W. (1996). Characterization of a bipotent erythro-megakaryocytic progenitor in human bone marrow. Blood 88, 1284-1296.
12. de Cremoux, P., Zimber, A., Calvo, F., Lanotte, M., Mercken, L., and Abita, J.P. (1991). Gs alpha availability to cholera toxin-catalysed ADP-ribosylation is decreased in membranes of retinoic acid-treated leukemic cell lines HL-60 and THP-1: a posttranslational effect. Biochem. Pharmacol. 42, 2141-2146.
13. Deterre, P., Gelman, L., Gary-Gouy, H., Arrieumerlou, C., Berthelier, V., Tixier, J.-M., Ktorza, S., Goding, J., Schmitt, C., and Bismuth, G. (1996). Coordinated regulation in human T cells of nucleotide-hydrolyzing ecto-enzymatic activities, including CD38 and PC-1: possible role in the recycling of nicotinamide adenine dinucleotide metabolites. J. Immunol. 157, 1381-1388.
14. Dianzani, U., and Malavasi, F. (1995). Lymphocyte adhesion to endothelium. Crit. Rev. Immunol. 15, 167-176.
15. Drach, J., McQueen, T., Engel, H., Andreeff, M., Robertson, K.A., Collins, S.J., Malavasi, F., and Mehta, K. (1994). Retinoic acid-induced expression of CD38 antigen in myeloid cells is mediated through retinoic acid receptor-alpha. Cancer Res. 54, 1746-1752.
16. Englund, P.T. (1993). The structure and biosynthesis of glycosyl phosphatidylinositol protein anchors. Annu. Rev. Biochem. 62, 121-138.
17. Funaro, A., De Monte, L.B., Dianzani, U., Forni, M., and Malavasi, F. (1993). Human CD38 is associated to distinct molecules which mediate transmembrane signaling in different lineages. Eur. J. Immunol. 23, 2407-2411.
18. Furuya, Y., Takasawa, S., Yonekura, H., Tanaka, T., Takahara, J., and Okamoto, H. (1995). Cloning of a cDNA encoding rat bone marrow stromal cell antigen 1 (BST-1) from the islets of Langerhans. Gene 165, 329-335.
19. Galibert, L., Burdin, N., de Saint-Vis, B., Garrone, P., Van-Kooten, C., Banchereau, J., and Rousset, F. (1996). CD40 and B cell antigen receptor dual triggering of resting B lymphocytes turns on a partial germinal center phenotype. J. Exp. Med. 183, 77-85.
20. Grimaldi, J.C., Balasubramanian, S., Kabra, N.H., Shanafelt, A., Bazan, J.F., Zurawski, G., and Howard, M.C. (1995). CD38-mediated ribosylation of proteins. J. Immunol. 155, 811-817.
21. Guida, L., Franco, I., Zocchi, E., and De Flora, A. (1995). Structural role of disulfide bridges in the cyclic ADP-ribose related bifunctional ectoenzyme CD38. FEBS Lett. 368, 481-484.
22. Hercend, T., Ritz, J., Schlossman, S.F., and Reinherz, E.L. (1981). Comparative expression of T9, T10, and Ia antigens on activated human T cell subsets. Hum. Immunol. 3, 247-259.
23. Hirata, Y., Kimura, N., Sato, K., Ohsugi, Y., Takasawa, S., Okamoto, H., Ishikawa, J., Kaisho, T., Ishihara, K., and Hirano, T. (1994). ADP ribosyl cyclase activity of a novel bone marrow stromal cell surface molecule, BST-1. FEBS Lett. 356, 244-248.
24. Ho, J.L., Zhu, B., He, S., Du, B., and Rothman, R. (1994). Interleukin 4 receptor signaling in human monocytes and U937 cells involves the activation of a phosphatidylcholine-specific phospholipase C: a comparison with chemotactic peptide, FMLP, phospholipase D, and sphingomyelinase. J. Exp. Med. 180, 1457-1466.
25. + glycohydrolase to a functional domain in the carboxyl terminus. J. Immunol. 158, 741-747.
26. Howard, M., Grimaldi, J.C., Bazan, J.F., Lund, F.E., Santos Argumedo, L., Parkhouse, R.M., Walseth, T.F., and Lee, H.C. (1993). Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science 262, 1056-1059.
27. Ikizawa, K., Kajiwara, K., Bazaki, Y., Koshio, T., and Yanagihara, Y. (1996). Evidence for a role of phosphatidylinositol 3-kinase in IL4-induced germline C epsilon transcription. Cell, Immunol. 170, 130-140.
28. Itoh, M., Ishihara, K., Tomizawa, H., Tanaka, H., Kobune, Y., Ishikawa, J., Kaisho, T., and Hirano, T. (1994). Molecular cloning of murine BST-1 having homology with CD38and Aplysia ADP-ribosyl cyclase. Biochem. Biophys. Res. Commun. 203, 1309-1317.
29. Jackson, D.G., and Bell, J.I. (1990). Isolation of a cDNA encoding the human CD38 (T10) molecule, a cell surface glycoprotein with an unusual discontinuous pattern of expression during lymphocyte differentiation. J. Immunol. 144, 2811-2817.
30. Johnston, J.A., Wang, L.M., Hanson, E.O., Sun, X.J., White, M.F., Oakes, S.A., Pierce, J.H., and O'Shea, J.J. (1995). Interleukins 2, 4, 7, and 15 stimulate tyrosine phosphorylation of insulin receptor substrates 1 and 2 in T cells: potential role of JAK kinases. J. Biol. Chem. 270, 28527-28530.
31. Kahn, R.A., and Gilman, A.G. (1984). Purification of a protein cofactor required for ADP-ribosylation of the stimulatory regulatory component of adenylate cyclase by cholera toxin. J. Biol. Chem. 259, 6228-6234.
32. Kato, I., Takasawa, S., Akabane, A., Tanaka, O., Abe, H., Takamura, T., Suzuki, Y., Nata, K., Yonekura, H., Yoshimoto, T., and Okamoto, H. (1995). Regulatory role of CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase) in insulin secretion by glucose in pancreatic beta cells: enhanced insulin secretion in CD38-expressing transgenic mice. J. Biol. Chem. 270, 30045-30050.
33. Kikuchi, Y., Yasue, T., Miyake, K., Kimoto, M., and Takatsu, K. (1995). CD38 ligation induces tyrosine phosphorylation of Bruton tyrosine kinase and enhanced expression of interleukin 5-receptor alpha chain: synergistic effects with interleukin 5. Proc. Natl. Acad. Sci. USA 92, 11814-11818.
34. Kim, K.M., Alber, G., Weiser, P., and Reth, M. (1993a). Signalling function of the B-cell antigen receptors, Immunol. Rev. 132, 125-146.
35. Kim, U.-H., Han, M.-K., Park, B.-H., Kim, H.-R., and An, N.-H. (1993b). Function of NAD glycohydrolase in ADP-ribose uptake from NAD by human erythrocytes. Biochim. Biophys. Acta 1178, 121-126.
36. Kirkham, P.A., Santos-Argumedo, L., Harnett, M.M., and Parkhouse, R.M.E. (1994). Murine B-cell activation via CD38 and protein tyrosine phosphorylation. Immunology 83, 513-516.
37. Kitanaka, A., Ito, C., Nishigaki, H., and Campana, D. (1996). 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 88, 590-598.
38. Koch-Nolte, F., Klein, J., Hollmann, C., Kuhl, M., Haag, F., Gaskins, H.R., Leiter, E., and Thiele, H.G. (1995). Defects in the structure and expression of the genes for the T cell marker Rt6 in NZW and (NZB X NZW)F1 mice. Int. Immunol. 7, 883-890.
39. Koch-Nolte, F., Petersen, D., Balasubramanian, S., Haag, F., Kahlke, D., Willer, T., Kastelein, R., Bazan, F., and Thiele, H.G. (1996). Mouse T cell membrane proteins Rt6-1 and Rt6-2 are arginine/protein mono(ADPribosyl)transferases and share secondary structure motifs with ADP-ribosylating bacterial toxins. J. Biol. Chem. 271, 7686-7693.
40. Koguma, T., Takasawa, S., Tohgo, A., Karasawa, T., Furuya, Y., Yonekura, H., and Okamoto, H. (1994). Cloning and characterization of cDNA encoding rat ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase (homologue to human CD38) from islets of Langerhans. Biochim. Biophys. Acta 1223, 160-162.
41. Kontani, K., Kukimonto, I., Kanda, Y., Inoue, S., Kishimoto, H., Hoshino, S., Katada, T. (1996a). Induction of CD38/NADase and its monoclonal antibody-induced tyrosine phosphorylation in human leukemia cell lines. Biochem. Biophys. Res. Commun. 222, 466-471.
42. Kontani, K., Kukimoto, I., Nishina, H., Hoshino, S., Hazeki, O., Kanaho, Y., and Katada, T. (1996b). Tyrosine phosphorylation of the c-cbl proto-oncogene product mediated by cell surface antigen CD38 in HL-60 cells. J. Biol. Chem. 271, 1534-1537.
43. Kramer, G., Steiner, G., Fodinger, D., Fiebiger, E., Rappersberger, C., Binder, S., Hofbauer, J., and Marberger, M. (1995). High expression of a CD38-like molecule in normal prostatic epithelium and its differential loss in benign and malignant disease. J. Urol. 154, 1636-1641.
44. + glycohydrolase activity. Eur. J. Biochem. 239, 177-183.
45. Kumagai, N., Morii, N., Fujisawa, K., Nemoto, Y., and Narumiya, S. (1993). ADP-ribosylation of rho p21 inhibits lysophosphatidic acid-induced protein tyrosine phosphorylation and phosphatidylinositol 3-kinase activation in cultured Swiss 3T3 cells. J. Biol. Chem. 268, 24535-24538.
46. Kumagai, M., Coustan-Smith, E., Murray, D.J., Silvennoinen, O., Gopal Murti, K., Evans, W.E., Malavasi, F., and Campana, D. (1995). Ligation of CD38 suppresses human B lymphopoiesis. J. Exp. Med. 181, 1101-1110.
47. Kumar, R., Shoemaker, A.R., and Verma, A.K. (1994). Retinoic acid nuclear receptors and tumor promotion: decreased expression of retinoic acid nuclear receptors by the tumor promoter 12-O-tetradecanoylphorbol-13-acetate. Carcinogenesis 15, 701-705.
48. Lagresle, C., Bella, C., and Defrance, T. (1993). Phenotypic and functional heterogeneity of the IgD-B cell compartment: identification of two major tonsillar B cell subsets. Int. Immunol. 5, 1259-1269.
49. Lagresle, C., Bella, C., Daniel, P.T., Krammer, P.H., and Defrance, T. (1995). Regulation of germinal center B cell differentiation. Role of the human APO-1/Fas (CD95) molecule. J. Immunol. 154, 5746-5756.
50. Langhans-Rajasekaran, S.A., Wan, Y., and Huang, X.Y. (1995). Activation of Tsk and Btk tyrosine kinases by G protein beta gamma subunits. Proc. Natl. Acad. Sci. USA 92, 8601-8605.
51. Lee, H.C., Aarhus, R., Graeff, R., Gurnack, M.E., and Walseth, T.F. (1994). Cyclic ADP ribose activation of the ryanodine receptor is mediated by calmodulin. Nature 370, 307-309.
52. Liew, F.M., and Yamanishi, K. (1992). Regulation of transglutaminase 1 gene expression by 12-O-tetradecanoylphorbol-13-acetate, dexamethasone, and retinoic acid in cultured human keratinocytes. Exp. Cell Res. 202, 310-315.
53. Liu, Y.J., Malisan, F., de Bouteiller, O., Guret, C., Lebecque, S., Banchereau, J., Mills, F.C., Max, E.E., and Martinez-Valdez, H. (1996). Within germinal centers, isotype switching of immunoglobulin genes occurs after the onset of somatic mutation. Immunity 4, 241-250.
54. Lund, F.E., Solvason, N.W., Cooke, M.P., Health, A.W., Grimaldi, J.C., Parkhouse, R.M.E., Goodnow, C.C., and Howard, M.C. (1995a). Signaling through murine CD38 is impaired in antigen receptor-unresponsive B cells. Eur. J. Immunol. 25, 1338-1345.
55. Lund, F., Solvason, N., Grimaldi, J.C., Parkhouse, R.M.E., and Howard, M. (1995b). Murine CD38: an immunoregulatory ectoenzyme. Immunol. Today 16, 469-473.
56. Lund, F.E., Yu, N., Kim, K.M., Reth, M., and Howard, M.C. (1996). Signaling through CD38 augments B cell antigen receptor (BCR) responses and is dependent on BCR expression. J. Immunol. 157, 1455-1467.
57. MacLennan, I.C.M. (1994). Germinal centers. Annu. Rev. Immunol. 12, 117-139.
58. Malavasi, F., Funaro, A., Roggero, S., Horenstein, A., Calosso, L., and Mehta, K. (1994). Human CD38: a glycoprotein in search of a function, Immunol. Today 15, 95-97.
59. Mehta, K., Shahid, U., and Malavasi, F. (1996). Human CD38, a cell-surface protein with multiple functions. FASEB J. 10, 1408-1417.
60. Mizuguchi, M., Otsuka, N., Sato, M., Ishii, Y., Kon, S., Yamada, M., Nishina, H., Katada, T., and Ikeda, K. (1995). Neuronal localization of CD38 antigen in the human brain. Brain Res. 697, 235-240.
61. Muszynski, K.W., Ruscetti, F.W., Heidecker, G., Rapp, U., Troppmair, J., Gooya, J.M., and Keller, J.R. (1995). Raf-1 protein is required for growth factor-induced proliferation of hematopoietic cells. J. Exp. Med. 181, 2189-2199.
62. Nakagawara, K., Mori, M., Takasawa, S., Nata, K., Takamura, T., Berlova, A., Tohgo, A., Karasawa, T., Yonekura, H., Takeuchi, T., and Okamoto, H. (1995). Assignment of CD38, the gene encoding human leukocyte antigen CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase), to chromosome 4p15. Cytogenet. Cell Genet. 69, 38-39.
63. Nishina, H., Inageda, K., Takahashi, K., Hoshino, S., Ikeda, K., and Katada, T. (1994). Cell surface antigen CD38 identified as ectoenzyme of NAD glycohydrolase has hyaluronate-binding activity. Biochem. Biophys. Res. Commun. 203, 1318-1323.
64. Oertel, J., Oertel, B., Schleicher, J., and Huhn, D. (1996). Immunotyping of blasts in human bone marrow. Ann. Hematol. 72, 125-129.
65. Okazaki, I.J., and Moss, J. (1996). Structure and function of eukaryotic mono-ADP-ribosyltransferases. Rev. Physiol. Biochem. Pharmacol. 129, 51-104.
66. Oliver, A.L., Martin, F., and Kearney, J.F. (1997). Mouse CD38 is down-regulated on germinal center B cells and mature plasma cells. J. Immunol. 158, 1108-1115.
67. Panchamoorthy, G., Fukazawa, T., Miyake, S., Soltoff, S., Reedquist, K., Druker, B., Shoelson, S., Cantley, L., and Band, H. (1996). p120cbl is a major substrate of tyrosine phosphorylation upon B cell antigen receptor stimulation and interacts in vivo with Fyn and Syk tyrosine kinases, Grb2 and She adaptors, and the p85 subunit of phosphatidylinositol 3-kinase. J. Biol. Chem. 271, 3187-3194.
68. Pascual, V., Liu, Y.-J., Magalski, A., de Bouteiller, O., Banchereau, J., and Capra, J.D. (1994). Analysis of somatic mutation in five B cell subsets of human tonsil. J. Exp. Med. 180, 329-339.
69. Pernis, A., Witthuhn, B., Keegan, A.D., Nelms, K., Garfein, E., Ihle, J.M., Paul, W.E., Pierce, J.H., and Rothman, P. (1995). Interleukin 4 signals through two related pathways. Proc. Natl. Acad. Sci. USA 92, 7971-7975.
70. Post, G.R., and Brown, J.H. (1996). G protein-coupled receptors and signaling pathways regulating growth responses. FASEB J. 10, 741-749.
71. Prince, H.E., York, J., and Jensen, E.R. (1992). Phenotypic comparison of the three populations of human lymphocytes defined by CD45RO and CD45RA expression. Cell, Immunol. 145, 254-262.
72. Ramaschi, G., Torti, M., Tolnai Festetics, E., Sinigaglia, F., Malavasi, F., and Balduini, C. (1996). Expression of cyclic ADP-ribose-synthetizing CD38 molecule on human platelet membrane. Blood 87, 2308-2313.
73. Reinherz, E.L., Kung, PC., Goldstein, G., Levey, R.H., and Schlossman, S.F. (1980). Discrete stages of human intrathymic differentiation: analysis of normal thymocytes and leukemic lymphoblasts of T-cell lineage. Proc. Natl. Acad. Sci. USA 77, 1588-1592.
74. Santos-Argumedo, L., Teixeira, C., Preece, G., Kirkham, P.A., and Parkhouse, R.M.E. (1993). A B lymphocyte surface molecule mediating activation and protection from apoptosis via calcium channels. J. Immunol. 151, 3119-3130.
75. Santos-Argumedo, L., Lund, F.E., Heath, A.W., Solvason, N., Wu, W.W., Grimaldi, J.C., Parkhouse, R.M.E., and Howard, M. (1995). CD38 unresponsiveness of xid B cells implicates Bruton's tyrosine kinase (btk) as a regulator of CD38 induced signal transduction. Int. Immunol. 7, 163-169.
76. Satterthwaite, A., and Witte, O. (1996). Genetic analysis of tyrosine kinase function in B cell development. Annu. Rev. Immunol. 14, 131-154.
77. Shipp, M.A., and Look, AT. (1993). Hematopoietic differentiation antigens that are membrane-associated enzymes: cutting is the key! Blood 82, 1052-1070.
78. Shubinsky, G., and Schlesinger, M. (1994). The effect of interleukin 4 on the cell cycle of a human B-cell lymphoma line. Cell Prolif. 27, 489-499.
79. Shubinsky, G., and Schlesinger, M. (1997). The mechanism of interleukin-4-induced down-regulation of CD38 on human B cells. Cell, Immunol. 173, 87-95.
80. Silvennoinen, O., Nishigaki, H., Kitanaka, A., Kumagai, M., Ito, C., Malavasi, F., Lin, Q., Conley, M.E., and Campana, D. (1996). 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. 156, 100-107.
81. Stashenko, P., Nadler, L.M., Hardy, R., and Schlossman, S.F. (1981). Expression of cell surface markers after human B lymphocyte activation. Proc. Natl. Acad. Sci. USA 78, 3848-3852.
82. Tahayato, A., Lefebvre, P., Formstecher, P., and Dautrevaux, M. (1993). A protein kinase C-dependent activity modulates retinoic acid-induced transcription. Mol. Endocrinol. 7, 1642-1653.
83. Takahashi, K., Kukimoto, I., Tokita, K., Inageda, K., Inoue, S., Kontani, K., Hoshino, S., Nishina, H., Kanaho, Y., and Katada, T. (1995). Accumulation of cyclic ADP-ribose measured by a specific radioimmunoassay in differentiated human leukemic HL-60 cells with all-trans retinoic acid. FEBS Lett. 371, 204-208.
84. Takasawa, S., Tohgo, A., Noguchi, N., Koguma, T., Nata, K., Sugimoto, T., Yonekura, H., and Okamoto, H. (1993). Synthesis and hydrolysis of cyclic ADP-ribose by human leukocyte antigen CD38 and inhibition of the hydrolysis by ATP. J. Biol. Chem. 268, 26052-26054.
85. - progenitor cells. Blood 77, 1218-1227.
86. Tohgo, A., Takasawa, S., Noguchi, N., Koguma, T., Nata, K., Sugimoto, T., Furuya, Y., Yonekura, H., and Okamoto, H. (1994). Essential cysteine residues forcyclic ADP-ribose synthesis and hydrolysis by CD38. J. Biol. Chem. 269, 28555-28557.
87. Umar, S., Malavasi, F., and Mehta, K. (1996). Post-translational modification of CD38 protein into a high molecular weight form alters its catalytic properties. J. Biol. Chem. 271, 15922-15927.
88. Vicari, A.P., Bean, A.G.D., and Zlotnik, A. (1996). A role for BP-3/ BST-1 antigen in early Tcell development. Int. Immunol. 8, 183-191.
89. von Boehmer, H. (1992). Thymic selection: a matter of life and death, Immunol. Today 13, 454-458.
90. + cells in the rat. Am. J. Pathol. 148, 2043-2056.
91. Wan, Y., Kurosaki, T., and Huang, X.-Y. (1996). Tyrosine kinases in activation of the MAP kinase cascade by G-protein-coupled receptors. Nature 380, 541-544.
92. lck-associated protein. J. Immunol. 156, 2819-2827.
93. Weiss, A., and Littman, D.R. (1994). Signal transduction by lymphocyte antigen receptors. Cell 76, 263-274.
94. Yamashita, Y., Miyake, K., Kikuchi, Y., Takatsu, K., Noda, S., Kosugi, A., and Kimoto, M. (1995). A monoclonal antibody against a murine CD38 homologue delivers a signal to B cells for prolongation of survival and protection against apoptosisin vitro: unresponsiveness of X-linked immunodeficient B cells. Immunology 85, 248-255.
95. + glycohydrolaseand ADP-ribosyl cyclase activities of leukocyte cell surface antigen CD38 by gangliosides. J. Biol. Chem. 271, 12951-12957.
96. Zhang, L.X., Mills, K.J., Dawson, M.I., Collins, S.J., and Jetten, A.M. (1995). Evidence for the involvement of retinoic acid receptor RAR alpha-dependent signaling pathway in the induction of tissue transglutaminase and apoptosis by retinoids. J. Biol. Chem. 270, 6022-6029.
97. Zocchi, E., Franco, L., Guida, L., Calder, L., and De Flora, A. (1995). Self-aggregation of purified and membrane-bound erythrocyte CD38 induces extensive decrease of its ADP-ribosyl cyclase activity. FEBS Lett. 359, 35-40.
98. Zupo, S., Dono, M., Massara, R., Taborelli, G., Chiorazzi, N., and Ferrarini, M. (1994a). Expression of CD5 and CD38 by human CD5-B cells: requirement for special stimuli. Eur. J. Immunol. 24, 1426-1433.
99. Zupo, S., Rugari, E., Dono, M., Taborelli, G., Malavasi, F., and Ferrarini, M. (1994b). CD38 signaling by agonistic monoclonal antibody prevents apoptosis of human germinal center B cells. Eur. J. Immunol. 24, 1218-1222.