CD38 is expressed as noncovalently associated homodimers on the surface of murine B lymphocytes

European Journal of Biochemistry

Volumn 271, Issue 5, 2004, Pages 1025-1034

  Moreno García, Miguel E ^a   Partida Sánchez, Santiago ^b   Primack, Julie ^b   Sumoza Toledo, Adriana ^a   Muller Steffner, Hélène ^c   Schuber, Francis ^c   Oppenheimer, Norman ^d   Lund, Frances E ^b   Santos Argumedo, Leopoldo ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b TRUDEAU INSTITUTE   (United States)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

B lymphocytes; CD38; Homodimer stability; NAD+ glycohydrolase; Protein structure

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYL CYCLASE; CD38 ANTIGEN; DETERGENT; DIMER; MEMBRANE PROTEIN; MUTANT PROTEIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL MEMBRANE; CELL SURFACE; CYTOPLASM; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

ADP-RIBOSYL CYCLASE; ANIMALS; ANTIGENS, CD; ANTIGENS, CD38; B-LYMPHOCYTES; CELL LINE; CELL MEMBRANE; DETERGENTS; DIMERIZATION; GLYCOSIDE HYDROLASES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SPLEEN;

ANIMALIA; APLYSIA CALIFORNICA; MURINAE;

EID: 1542284573     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.2004.04006.x     Document Type: Article

References (37)

1. Santos-Argumedo, L., Teixeira, C., Preece, G., Kirkham, P.A. & Parkhouse, R.M.E. (1993) A B lymphocyte surface molecule mediating activation and protection from apoptosis via calcium channels. J. Immunol. 15, 3119-3130.
2. Mehta, K., Shahid, U. & Malavasi, F. (1996) Human CD38, a cell-surface protein with multiple function. FASEB J. 10, 1408-1417.
3. Lund, F.E., Cockayne, D.A., Randall, T.D., Solvason, N., Schuber, F. & Howard, M.C. (1998) CD38: a new paradigm in lymphocyte activation and signal transduction. Immunol. Rev. 161, 79-93.
4. Howard, M.C., Grimaldi, J.C., Bazan, J.F., Lund, F.E., Santos-Argumedo, L., Parkhouse, R.M.E., Walseth, T.F. & Lee, H.C. (1993) Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science 262, 1056-1059.
5. +. J. Biol. Chem. 270, 30327-30333.
6. Kirkham, P.A., Santos-Argumedo, L., Harnett, M.M. & Parkhouse, R.M.E. (1994) Murine B-cell activation via CD38 and protein tyrosine phosphorylation. Immunology 83, 513-516.
7. Kitanaka, A., Suzuki, T., Ito, C., Nishigaki, H., Coustain-Smith, E., Tanaka, T., Kubota, Y. & Campana, D. (1999) CD38-mediated signaling events in murine pro-B cells expressing human CD38 with or without its cytoplasmic domain. J. Immunol. 162, 1952-1958.
8. Kumagai, M., Coustan-Smith, E., Murray, D.J., Silvennoinen, O., Murti, K.G., Evans, W.E., Malavasi, F. & Campana, D. (1995) Ligation of CD38 suppresses human B lymphopoiesis. J. Exp. Med. 181, 1101-1110.
9. Zubiar, M., Guirado, M., Terhorst, C., Malavasi, F. & Sancho, J. (1999) The CD3-γδε transducing module mediates CD38-induced protein-tyrosine kinase and mitogen-activated protein kinase activation in Jurkat T cells. J. Biol. Chem. 274, 20633-20642.
10. Yasue, T., Baba, M., Mori, S., Mizoguchi, C., Uehara, S. & Takatsu, K. (1999) IgG1 production by sIgD+ splenic B cells and peritoneal B-1 cells in response to IL-5 and CD38 ligation. Int. Immunol. 11, 915-923.
11. Hellmich, M.R. & Strumwasser, F. (1991) Purification and characterization of a molluscan egg-specific NADase, a second-messenger enzyme. Cell Regul. 2, 193-202.
12. + into a calcium-mobilizing metabolite. Cell Regul. 2, 203-209.
13. + glycohydrolase family. Int. Immunol. 6, 1353-1360.
14. Itoh, M., Ishihara, K., Tomizawa, H., Tanaka, H., Kobune, Y., Ishikawa, J., Kaisho, T. & Hirano, T. (1994) Molecular cloning of murine BST-1 having homology with CD38 and Aplysia ADP-ribosyl cyclase. Biochem. Biophys. Res. Commun. 203, 1309-1317.
15. Yamamoto-Katayama, S., Ariyoshi, M., Ishihara, K., Hirano, T., Jingami, H. & Morikawa, K. (2002) Crystallographic studies on human BST-1/CD157 with ADP-ribosyl cyclase and NAD glycohydrolase activities. J. Mol. Biol. 316, 711-723.
16. Prasad, G.S., McRee, D.E., Stura, E.A., Levitt, D.G., Lee, H.C. & Stout, C.D. (1996) Crystal structure of Aplysia ADP ribosyl cyclase, a homologue of the bifunctional ectozyme CD38. Nat. Struct. Biol. 3, 957-964.
17. Franco, L., Zocchi, E., Calder, L., Guida, L., Benatti, U. & De Flora, A. (1994) Self-aggregation of the transmembrane glycoprotein CD38 purified from human erythrocytes. Biochem. Biophys. Res. Commun. 202, 1710-1715.
18. Bruzzone, S., Guida, L., Franco, L., Zocchi, E., Corte, G. & De Flora, A. (1998) Dimeric and tetrameric forms of catalytically active transmembrane CD38 in transfected HeLa cells. FEBS Lett. 433, 275-278.
19. Harada, N., Santos-Argumedo, L., Chang, R., Grimaldi, J.C., Lund, F.E., Brannan, C.I., Copeland, N.G., Jenkins, N.A., Heath, A.W. & Parkhouse, R.M. (1993) Expression cloning of a cDNA encoding a novel murine B cell activation marker. Homology to human CD38. J. Immunol. 151, 3111-3118.
20. Jackson, D.G. & 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, 2811-2815.
21. Lund, F.E., Yu, N., Kim, K.M., Reth, M. & 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.
22. Han, M.K., Kim, S.J., Park, Y.R., Shin, Y.M., Park, H.J., Park, K.J., Park, K.H., Kim, H.K., Jang, S.I., An, N.H. & Kim, U.H. (2002) Antidiabetic effect of a prodrug of cysteine, L-2-oxothiazolidine-4-carboxylic acid, through CD38 dimerization and internalization. J. Biol. Chem. 277, 5315-5321.
23. Chidambaram, N., Wong, E.T. & Chang, C.F. (1998) Differential oligomerization of membrane-bound CD38/ADP-ribosyl cyclase in porcine heart microsomes. Biochem. Mol. Biol. Int. 44, 1225-1233.
24. Khoo, K.M. & Chang, C.F. (1998) Purification and characterization of CD38/ADP-ribosyl cyclase from rat lung. Biochem. Mol. Biol. Int. 44, 841-850.
25. Khoo, K.M. & Chang, C.F. (2000) Localization of plasma membrane CD38 is domain specific in rat hepatocyte. Arch. Biochem. Biophys. 373, 35-43.
26. Umar, S., Malavasi, F. & 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.
27. Cockayne, D.A., Muchamuel, T., Grimaldi, J.C., Muller-Steffner, H., Randall, T.D., Lund, F.E., Murray, R., Schuber, F. & Howard, M.C. (1998) Mice deficient for the ecto-nicotinamide adenine dinucleotide glycohydrolase CD38 exhibit altered humoral immune responses. Blood 92, 1324-1333.
28. Lund, F.E., Solvason, N.W., Cooke, M.P., Health, A.W., Grimaldi, J.C., Parkhouse, R.M., Goodnow, C.C. & Howard, M.C. (1995) Signaling through murine CD38 is impaired in antigen receptor-unresponsive B cells. Eur. J. Immunol. 25, 1338-1345.
29. O'Farrel, P.H. (1975) High resolution Two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007-4021.
30. Lund, F.E. & Muller-Steffner, H.M., Yu, N., Stout, C.D., Schuber, F. & Howard, M.C. (1999) CD38 signaling in B lymphocytes is controlled by its ectodomain but occurs independently of enzymatically generated ADP-ribose or cyclic ADP-ribose. J. Immunol. 162, 2693-2702.
31. + exchangers NHE1-3: plasma membrane NHE2 has a rapid rate of degradation. Am. J. Physiol. Cell Physiol. 281, C2039-C2048.
32. Hsu, Y.T. & Youle, R.J. (1997) Nonionic detergents induce dimerization among members of the Bcl-2 family. J. Biol. Chem. 272, 13829-13834.
33. Hsu, Y.T. & Youle, R.J. (1998) Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J. Biol. Chem. 273, 10777-10783.
34. Munshi, C., Aarhus, R., Graeff, R., Walseth, T.F., Levitt, D. & Lee, H.C. (2000) Identification of the enzymatic active site of CD38 by site-directed mutagenesis. J. Biol. Chem. 275, 21566-21571.
35. Haardt, M., Benharouga, M., Lechardeur, D., Kartner, N. & Lukacs, G.L. (1999) C-terminal truncations destabilize the cystic fibrosis transmembrane conductance regulator without impairing its biogenesis. A novel class of mutation. J. Biol. Chem. 274, 21873-21877.
36. Fan, H., Meng, W., Kilian, C., Grams, S. & Reutter, W. (1997) Domain-specific N-glycosylation of the membrane glycoprotein dipeptidase IV (CD26) influences its subcellular trafficking, biological stability, enzyme activity and protein folding. Eur. J. Biochem. 246, 243-251.
37. Franco, L., Guida, L., Bruzzone, S., Zocchi, E., Usai, C. & De Flora, A. (1998) The transmembrane glycoprotein CD38 is a catalytically active transporter responsible for generation and influx of the second messenger cyclic ADP-ribose across membranes. FASEB J. 12, 1507-1520.