Characterization of a CD38-like 78-kilodalton soluble protein released from B cell lines derived from patients with X-linked agammaglobulinemia

Journal of Clinical Investigation

Volumn 101, Issue 12, 1998, Pages 2821-2830

  Mallone, Roberto ^a   Ferrua, Stefania ^a   Morra, Massimo ^a   Zocchi, Elena ^b   Mehta, Kapil ^c   Notarangelo, Luigi D ^d   Malavasi, Fabio ^a,e,f  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF TEXAS   (United States)

^d UNIVERSITY OF BRESCIA   (Italy)

^e UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^f Dipto di Genet Biologia/Biochim   (Italy)

Author keywords

ADP ribosyl cyclase; CD38; Ectoenzyme; Immunodeficiency; Soluble receptor

Indexed keywords

CD38 ANTIGEN; EPITOPE; PROTEIN TYROSINE KINASE;

ARTICLE; B LYMPHOCYTE; CELL IMMORTALIZATION; CELL SURFACE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTERNALIZATION; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; X LINKED AGAMMAGLOBULINEMIA; X RAY CRYSTALLOGRAPHY;

EID: 0032525851     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1068     Document Type: Article

References (61)

1. Malavasi, F., A. Funaro, S. Roggero, A. Horenstein, L. Calosso, and K. Mehta. 1994. Human CD38: a glycoprotein in search of a function. Immunol. Today. 15:95-97.
2. Funaro, A., G.C. Spagnoli, C.M. Ausiello, M. Alessio, S. Roggero, D. Delia, M. Zaccolo, and F. Malavasi. 1990. Involvement of the multilineage CD38 molecule in a unique pathway of cell activation and proliferation. J. Immunol. 145:2390-2396.
3. + lymphocytes: role of the human CD38 molecule. J Immunol. 154:952-959.
4. Deaglio, S., U. Dianzani, A.L. Horenstein, J.E. Fernandez, C. van Kooten, M. Bragardo, A. Funaro, G. Garbarino, F.D. Virgilio, J. Banchereau, and F. Malavasi. 1996. Human CD38 ligand: a 120-kDa protein predominantly expressed on endothelial cells. J. Immunol. 156:727-734.
5. Deaglio, S., M. Morra, R. Mallone, C.M. Ausiello, E. Prager, G. Garbarino, U. Dianzani, H. Stockinger, and F. Malavasi. 1998. Human CD38 (ADP-ribosyl cyclase) is a counter-receptor of CD31, an Ig superfamily member. J. Immunol. 160:395-402.
6. Howard, M., J.C. Grimaldi, J.F. Bazan, F.E. Lund, L. Santos-Argumedo, R.M.E. Parkhouse, T.F. Walseth, and H.C. Lee. 1993. Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science. 262: 1056-1059.
7. Galione, A. 1993. Cyclic ADP-ribose: a new way to control calcium. Science. 259:325-326.
8. Funaro, A., A.L. Horenstein, L. Calosso, M. Morra, R.P. Tarocco, L. Franco, A. De Flora, and F. Malavasi. 1996. Identification and characterization of an active soluble form of human CD38 in normal and pathological fluids. Int. Immunol. 8:1643-1650.
9. Berthelier, V., F. Malavasi, G. Bismuth, C. Schmitt, and P. Deterre. 1996. Report on the 2nd international CD38 workshop. Res. Immunol. 147:407-411.
10. Umar, S., F. Malavasi, and K. Mehta. 1996. Post-translational modification of CD38 protein into a high molecular weight form alters its catalytic properties. J Biol. Chem. 271:15922-15927.
11. Drach, J., S. Zhao, F. Malavasi, and K. Mehta. 1993. Rapid induction of CD38 antigen on myeloid leukemia cells by all trans-retinoic acid. Biochem. Biophys. Res. Commun. 195:545-550.
12. Zocchi, E., L. Franco, L. Guida, L. Calder, and A. De Flora. 1995. Self-aggregation of purified and membrane-bound erythrocyte CD38 induces extensive decrease of its ADP-ribosyl cyclase activity. FEBS (Fed. Eur. Biochem. Soc.) Lett. 359:35-40.
13. Mehta, K., U. Shahid, and F. Malavasi. 1996. Human CD38, a cell surface molecule with multiple functions. FASEB (Fed. Am. Soc. Exp. Biol.) J. 10: 1408-1417.
14. Thomas, J.D., P. Sideras, C.I.E. Smith, I. Vorechovsky, V. Chapman, and W.E. Paul. 1993. Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes. Science. 261:355-358.
15. Santos-Argumedo, L., F.E. Lund, A.W. Heath, N. Solvason, W.W. Wu, J.C. Grimaldi, R.M. Parkhouse, and M. Howard. 1995. CD38 unresponsiveness of xid B cells implicates Bruton's tyrosine kinase (btk) as a regular of CD38-induced signal transduction. Int. Immunol. 7:163-170.
16. Kikuchi, Y., T. Yasue, K. Miyake, M. Kimoto, and K. Takatsu. 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.
17. Yasue, T., H. Nishizumi, S. Aizawa, T. Yamamoto, K. Miyake, C. Mizoguchi, S. Uehara, Y. Kikuchi, and K. Takatsu. 1997. A critical role of Lyn and Fyn for B cell responses to CD38 ligation and interleukin 5. Proc. Natl. Acad. Sci. USA. 94:10307-10312.
18. Hoffman, T., R.J. Winchester, M. Schulkind, J.L. Frias, E.M. Ayoub, and R.A. Good. 1977. Hypoimmunoglobulinemia with normal T cell function in female siblings. Clin. Immunol. Immunopathol. 7:364-371.
19. Conley, M.E., and S.K. Sweinberg. 1992. Females with a disorder phenotypically identical to X-linked agammaglobulinemia. J. Clin. Immunol. 12: 139-143.
20. Malavasi, F., C. Milanese, M. Fabbi, P. Richiardi, F. Caligaris-Cappio, E. Ferrero, S. Roggero, P. Dellabona, and R. Ceppellini. 1984. Generation and characterization of murine monoclonal antibodies against HLA Class II molecules. Diagn. Immunol. 2:53-62.
21. Malavasi, F., F. Caligaris-Cappio, P. Dellabona, P. Richiardi, and A.O. Carbonara. 1984. Characterization of a murine monoclonal antibody specific for human early lymphohemopoietic cells. Hum. Immunol. 9:9-20.
22. Funaro, A., A.L. Horenstein, and F. Malavasi. 1995. Human CD38: a versatile leukocyte molecule with emerging clinical prospectives. Fund. Clin. Immunol. 3:101-114.
23. 2 microglobulin monoclonal antibodies on alloantigen and microbial antigen-induced immune responses "in vitro". Scand. J. Immunol. 25:555-565.
24. Peruzzi, L., G. Melioli, L.B. De Monte, M. Alessio, M. Zaccolo, S. Roggero, G. Bellone, A. Funaro, and F. Malavasi. 1989. Microplate selection technique (MPST): a new method for selecting mouse transfectants expressing human gene products. J Immunol. Methods. 123:113-121.
25. lck, increased association with clathrin-coated pits, and altered endosomal sorting. J. Exp. Med. 178:1209-1222.
26. 131I-labeled human growth hormone of high specific radioactivity. Biochem. J. 89:114-123.
27. Hager, D.A., and R.R. Burgess. 1980. Elution of proteins from sodium dodecyl sulfate-polyacrylamide gels, removal of sodium dodecyl sulfate, and renaturation of enzymatic activity: results with sigma subunit of Escherichia coli RNA polymerase, wheat germ DNA topoisomerase, and other enzymes. Anal. Biochem. 109:76-86.
28. Harlow, E., and D. Lane. 1988. Antibodies. A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 641-642.
29. Guida, L., L. Franco, E. Zocchi, and A. De Flora. 1995. Structural role of disulfide bridges in the cyclic ADP-ribose related bifunctional ectoenzyme CD38. FEBS (Fed. Eur. Biol. Soc.) Lett. 368:481-484.
30. Graeff, R.M., T.F. Walseth, K. Fryxell, W.D. Branton, and H.C. Lee. 1994. Enzymatic synthesis and characterizations of cyclic GDP-ribose: a procedure for distinguishing enzymes with ADP-ribosyl cyclase activity. J. Biol. Chem. 269:30260-30267.
31. Funaro, A., L.B. De Monte, U. Dianzani, M. Forni, and F. Malavasi. 1993. Human CD38 is associated to distinct molecules which mediate transmembrane signaling in different lineages. Eur. J. Immunol. 23:2407-2411.
32. Funaro, A., M. Reinis, O. Trubiani, S. Santi, R. Di Primio, and F. Malavasi. 1998. CD38 functions are regulated through an internalization step. J. Immunol. 160:2238-2247.
33. Hoshino, S., I. Kukimoto, K. Kontani, S. Inoue, Y. Kanda, F. Malavasi, and T. Katada. 1997. Mapping of the catalytic and epitopic sites of human CD38/NADase to a functional domain in the carboxy terminus. J. Immunol. 158:741-747.
34. Kansas, G.S., G.S. Wood, and T.F. Tedder. 1991. Expression, distribution, and biochemistry of human CD39. J. Immunol. 146:2235-2244.
35. Di Rosa, G., M.J. Feito, M. Bragardo, G. Aversa, U. Dianzani, and F. Malavasi. 1997. CD39 and CD26 are associated with CD38 in human NK cells. J. Biol. Regul. Homeost. Agents. 11:12a. (Abstr.)
36. Deterre, P., L. Gelman, H. Gary-Gouy, C. Arrieumerlou, V. Berthelier, J.M. Tixier, S. Ktorza, J. Goding, C. Schmitt, and G. Bismuth. 1996. Coordinated regulation in human T cells of nucleotide-hydrolyzing ecto-enzymatic activities, including CD38 and PC-1. J. Immunol. 157:1381-1388.
37. 2+)-apyrase. J. Biol. Chem. 271:9898-9901.
38. Hurwitz, R., J. Hozier, T. LeBien, J. Minowada, K. Gajl-Peczalska, I. Kubonishi, and J. Kersey. 1979. Characterisation of a leukemic cell line of the pre-B phenotype. Int. J. Cancer. 23:174-180.
39. Pegoraro, L., L. Matera, J. Ritz, A. Levis, A. Palumbo, and G. Biagini. 1983. Establishment of a Ph1-positive human cell line (BV173). J. Natl. Cancer Inst. 70:447-453.
40. Alessio, M., S. Roggero, A. Funaro, L.B. De Monte, L. Peruzzi, M. Geuna, and F. Malavasi. 1990. CD38 molecule: structural and biochemical analysis on human T lymphocytes, thymocytes, and plasma cells. J. Immunol. 145:878-884.
41. Lee, H.C., E. Zocchi, L. Guida, L. Franco, U. Benatti, and A. De Flora. 1993. Production and hydrolysis of cyclic ADP-ribose at the outer surface of human erythrocytes. Biochim. Biophys. Res. Commun. 191:639-645.
42. Lund, F., N. Solvason, J.C. Grimaldi, R.M.H. Parkhouse, and M. Howard. 1995. Murine CD38: an immunoregulatory ectoenzyme. Immunol. Today. 16:469-473.
43. Oliver, A.M., F. Martin, and J.F. Kearney. 1947. Mouse CD38 is down-regulated on germinal center B cells and mature plasma cells. J. Immunol. 158: 1108-1115.
44. Kinnon, C., S. Hinshelwood, R.J. Levinsky, and R.C. Lovering. 1993. X-linked agammaglobulinemia - gene clonine and future prospects. Immunol. Today. 14:554-558.
45. Conley, M.E., O. Parolini, J. Rohrer, and D. Campana. 1994. X-linked agammaglobulinemia: new approaches to old questions based on the identification of the defective gene. Immunol. Rev. 138:5-21.
46. Conley, M.E. 1985. B cells in patients with X-linked agammaglobulinemia. J. Immunol. 134:3070-3074.
47. Conley, M.E., M.E. Fitch-Hilgenberg, J.L. Cleveland, O. Parolini, and J. Rohrer. 1994. Screening of genomic DNA to identify mutations in the gene for Bruton's tyrosine kinase. Hum. Mol. Genet. 3:1751-1756.
48. Yel, L., Y. Minegishi, E. Coustan-Smith, R.H. Buckley, H. Trubel, L.M. Pachman, G.R. Kitchingman, D. Campana, J. Rohrer, and M.E. Conley. 1996. Mutations in the μ heavy-chain gene in patients with agammaglobulinemia. N. Engl. J. Med. 335:1486-1493.
49. Nata, K., T. Takamura, T. Karasawa, T. Kumagai, W. Hashioka, A. Tohgo, H. Yonekura, S. Takasawa, S. Nakamura, and H. Okamoto. 1997. Human gene encoding CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase): organization, nucleotide sequence, and alternative splicing. Gene. 186:285-292.
50. +-converting enzymes. J. Immunol. 159:3858-3865.
51. Prasad, G.S., D.E. McRee, E.A. Stura, D.G. Levitt, H.C. Lee, and C.D. Stout. 1996. Crystal structure of Aplysia ADP ribosyl cyclase, a homologue of the bifunctional ectoenzyme CO38. Nat. Struct. Biol. 3:1-8.
52. States, D.J., T.F. Walseth, and H.C. Lee. 1992. Similarities in amino acid sequences of Aplysia ADP-ribosyl cyclase and human lymphocyte antigen CD38. Trends Biochem. Sci. 17:495.
53. Munshi, C.B., K.B. Fryxell, H.C. Lee, and W.D. Branton. 1997. Large-scale production of human CD38 in yeast by fermentation. Methods Enzymol. 280:318-330.
54. Gearing, A.J.H., and W. Newman. 1993. Circulating adhesion molecules in disease. Immunol. Today. 14:506-512.
55. Morra, M., M. Zubiaur, C. Terhorst, J. Sancho, and F. Malavasi. 1998. CD38 is functionally dependent on TCR/CD3 complex in human T cells. FASEB (Fed. Am. Soc. Exp. Biol.) J. 12:581-592.
56. Zupo, S., E. Rugari, M. Dono, G. Taborelli, F. Malavasi, and M. Ferrarini. 1994. CD38 signaling by agonistic monoclonal antibody prevents apoptosis of human germinal center B cells. Eur. J. Immunol. 24:1218-1222.
57. Kumagai, M., E. Coustan-Smith, D.J. Murray, O. Silvennoinen, K.G. Murti, W.E. Evans, F. Malavasi, and D. Campana. 1995. Ligation of CD38 suppresses human B lymphopoiesis. J. Exp. Med. 181:1101-1110.
58. Cesano, A., S. Visonneau, S. Deaglio, F. Malavasi, and D. Santoli. 1998. Role of CD38 and its ligand in the regulation of MHC non-restricted cytotoxic T cells. J. Immunol. 160:1106-1115.
59. Yamashita, Y., K. Miyake, Y. Kikuchi, K. Takatsu, S. Noda, A. Kosugi, and M. Kimoto. 1995. A monoclonal antibody against a murine CD38 homologue delivers a signal to B cells for prolongation of survival and protection against apoptosis in vitro: unresponsiveness of X-linked immunodeficient B cells. Immunology. 85:248-255.
60. Vorechovsky, I., J.N. Zhou, L. Hammarstrom, C.I. Smith, J.D. Thomas, W.E. Paul, L.D. Notarangelo, and E. Bernatowska-Matuszkiewicz. 1993. Absence of xid mutation in X-linked agammaglobulinaemia. Lancet. 342:552.
61. Stashenko, P., L.M. Nadler, R. Hardy, and S.F. Schlossman. 1981. Expression of cell surface markers after human B lymphocyte activation. Proc. Natl. Acad. Sci. USA. 78:3848-3852.