A unified mechanism of enzymatic synthesis of two calcium messengers: Cyclic ADP-ribose and NAADP

Biological Chemistry

Volumn 380, Issue 7-8, 1999, Pages 785-793

  Lee, Hon Cheung ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

ADP ribosyl cyclase; Calcium signaling; CD38; Cyclic ADP ribose; NAADP; X ray crystallography

Indexed keywords

ADENINE DERIVATIVE; ADENOSINE DIPHOSPHATE RIBOSE; CALCIUM ION; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NICOTINIC ACID DERIVATIVE; PHOSPHATE;

CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CATALYSIS; ENZYME SYNTHESIS; EUKARYOTE; HUMAN; INVERTEBRATE; MAMMAL; NONHUMAN; PLANT; PRIORITY JOURNAL; PROTOZOON; REVIEW; SECOND MESSENGER;

ADENOSINE DIPHOSPHATE RIBOSE; ADP-RIBOSYL CYCLASE; ANIMALS; ANTIGENS, CD; ANTIGENS, CD38; ANTIGENS, DIFFERENTIATION; CALCIUM; CATALYSIS; CYCLIC ADP-RIBOSE; HUMANS; MEMBRANE GLYCOPROTEINS; MOLECULAR STRUCTURE; NAD+ NUCLEOSIDASE; NADP;

EUKARYOTA; INVERTEBRATA; MAMMALIA; PROTOZOA;

EID: 0032830476     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/BC.1999.098     Document Type: Review

References (80)

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 NADR J. Biol. Chem. 270, 30327-30333.
2. +. J. Biol. Chem. 271, 8513-8516.
3. 2+ release channels, ryanodine receptor and inositol 1,4,5-trisphosphate receptor, play different roles during fertilization in Ascidians. Dev. Biol. 189, 174-185.
4. Albrieux, M., Lee, H.C., and Villaz, M. (1998). Calcium signaling by cyclic ADP-ribose, NAADP, and inositol trisphosphate are involved in distinct functions in Ascidian oocytes. J. Biol. Chem. 273, 14566-14574.
5. 2+ from individual plant vacuoles by both lnsP3 and cyclic ADP-ribose. Science 268, 735-737.
6. Barth, H., Preiss, J.C., Hofmann, F., and Aktories, K. (1998). Characterization of the catalytic site of the ADP-ribsoyltransferase Clostridium botulinum C2 toxin by site-directed mutagenesis. J. Biol. Chem. 273, 29506-29511.
7. Bell, C.E., and Eisenberg, D. (1996). Crystal structure of diphtheria toxin bound to nicotinamide adenine dinucleotide. Biochemistry 35, 1137-1149.
8. Berridge, M.J. (1993). Inositol trisphosphate and calcium signalling. Nature 361, 315-325.
9. 2+ spiking. Curr. Biol. 8, 865-868.
10. 2+-signalling patterns by NAADP in pancreatic acinarcells. Nature 398, 74-76.
11. +-dependent internalization of recombinant CD38 in CHO cells. Arch. Biochem. Biophys. 363, 267-272.
12. Chini, E.N., Beers, K.W., and Dousa, T.P. (1995). Nicotinate adenine dinucleotide phosphate (NAADP) triggers a specific calcium release system in sea urchin eggs. J. Biol. Chem. 270, 3216-3223.
13. Clapper, D.L., Walseth, T.F., Dargie, P.J., and Lee, H.C. (1987). Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J. Biol. Chem. 262, 9561-9568.
14. 2+ mobilizing activities of cyclic ADP-ribose and inositol trisphosphate. Cell Regul. 1, 279-290.
15. Dong, C., Willerford, D., Alt, F.W., and Cooper, M.D. (1996). Genomic organization and chromosomal localization of the mouse BP3 gene, a member of the CD38/ADP-ribosyl cyclase family. Immunogenetics 45, 35-43.
16. Franco, L., Guida, L., Bruzzone, S., Zocchi, E., Usai, C., and Flora, A.D. (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.
17. 2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253, 1143-1146.
18. 2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature 365, 456-459.
19. 2+ from a thapsigargin-insensitive pool. Biochem. J. 315, 721-725.
20. 2+ release. J. Biol. Chem. 271, 11599-11602.
21. Graeff, R.M., Mehta, K., and Lee, H.C. (1994a). GDP-ribosyl cyclase activity as a measure of CD38 induction by retinoic acid in HL-60 cells. Biochem. Biophys. Res. Commun. 205, 722-727.
22. Graeff, R.M., Walseth, T.F., Fryxell, K., Branton, W.D., and Lee, H.C. (1994b). Enzymatic synthesis and characterizations of cyclic GDP-ribose. A procedure for distinguishing enzymes with ADP-ribosyl cyclase activity. J. Biol. Chem. 269, 30260-30267.
23. Graeff, R.M., Walseth, T.F., Hill, H.K., and Lee, H.C. (1996). Fluorescent analogs of cyclic ADP-ribose: synthesis, spectral characterization, and use. Biochemistry 35, 379-386.
24. Graeff, R.M., Franco, L., Deflora, A., and Lee, H.C. (1998). Cyclic GMP-dependent and-independent effects on the synthesis of the calcium messengers cyclic ADP-ribose and nicotinic acid adenine dinucleotide phosphate. J. Biol. Chem. 273, 118-125.
25. 2+ release in T lymphocyte cell lines. J. Immunol. 155, 3353-3359.
26. 2+ and inorganic phosphate. J. Biol. Chem. 271, 23946-23953.
27. 2+ entry induced by cyclic ADP-ribose in intact T-lymphocytes. J. Biol. Chem. 272, 8546-8550.
28. Guse, A.H., da Silva, C.P., Berg, I., Skapenko, A.L., Weber, K., Heyer, P., Hohenegger, M., Ashamu, G.A., Schulze-Koops, H., Potter, B.V.L., and Mayr, G.W. (1999). Regulation of calcium signalling in T lymphocytes by the second messenger cyclic ADP-ribose. Nature 398, 70-73.
29. Hellmich, M.R., and Strumwasser, F. (1991). Purification and characterization of a molluscan egg-specific NADase, a second-messenger enzyme. Cell Regul. 2, 193-202.
30. 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.
31. Huang, M.S., Adebanjo, O., Moonga, B.S., Goldstein, S., Lai, F.A., Lipschitz, D.A., and Zaidi, M. (1998). Upregulation of functional ryanodine receptors during in vitro aging of human diploid fibroblasts, Biochem. Biophys. Res. Commun. 245, 50-52.
32. 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 CD38 and Aplysia ADP-ribosyl cyclase. Biochem. Biophys. Res. Commun. 203, 1309-1317.
33. 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 patem of expression during lymphocyte differentiation. J. Immunol. 144, 2811-2815.
34. Kim, H., Jacobson, E.L., and Jacobson, M.K. (1993). Synthesis and degradation of cyclic ADP-ribose by NAD glycohydrolases. Science 261, 1330-1333.
35. Koradi, R., Billeter, M., and Wuthrich, K. (1996). MOLMOL: aprogram for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55.
36. Leckie, C.P., McAinsh, M.R., Allen, G.J., Sanders, D., and Hetherington, A.M. (1998). Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA 95, 15837-15842.
37. Lee, H.C. (1993). Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose. J. Biol. Chem. 268, 293-299.
38. Lee, H.C. (1995). Cyclic ADP-ribose: A mediator of a calcium signaling pathway. In: 'Ryanodine Receptors', V. Sorrentino, ed., (Boca Raton, Fl., USA: CRC Press).
39. Lee, H.C. (1996). Modulator and messenger functions of cyclic ADP-ribose in calcium signaling. Re. Prog. Horm. Res. 51, 355-388.
40. Lee, H.C. (1997). Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP. Physiol. Rev. 77, 1133-1164.
41. + into a calcium-mobilizing metabolite. Cell Regul. 2, 203-209.
42. Lee, H.C., and Aarhus, R. (1993). Wide distribution of an enzyme that catalyzes the hydrolysis of cyclic ADP-ribose. Biochim. Biophys. Acta 1164, 68-74.
43. Lee, H.C., and Aarhus, R. (1995). A derivative of NADP mobilizes calcium stores insensitive to inositol trisphosphate and cyclic ADP-ribose. J. Biol. Chem. 270, 2152-2157.
44. Lee, H.C., and Aarhus, R. (1997). Structural determinants of nicotinic acid adenine dinucleotide phosphate important for its calcium-mobilizing activity. J. Biol. Chem. 272, 20378-20383.
45. Lee, H.C., and Aarhus, R. (1998). Fluorescent analogs of NAADP with calcium mobilizing activity. Biochim. Biophys. Acta 1425, 263-271.
46. 2+-mobilizing activity. J. Biol. Chem. 264, 1608-1615.
47. Lee, H.C., Zocchi, E., Guida, L., Franco, L., Benatti, U., and De Flora, A. (1993). Production and hydrolysis of cyclic ADP-ribose at the outer surface of human erythrocytes. Biochem. Biophys. Res. Commun. 191, 639-645.
48. Lee, H.C., Aarhus, R., Graeff, R., Gurnack, M.E., and Walseth, T.F. (1994a). Cyclic ADP ribose activation of the ryanodine receptor is mediated by calmodulin. Nature 370, 307-309.
49. Lee, H.C., Aarhus, R., and Levitt, D. (1994b). The crystal structure of cyclic ADP-ribose. Nature Struct. Biol. 1, 143-144.
50. Lee, H.C., Galione, A., and Walseth, T.F. (1994c). Cyclic ADP-ribose: metabolism and calcium mobilizing function. Vit. Horm. 48, 199-257.
51. Lee, H.C., Aarhus, R., and Graeff, R.M. (1995a). Sensitization of calcium-induced calcium release by cyclic ADP-ribose and calmodulin. J. Biol. Chem. 270, 9060-9066.
52. Lee, H.C., Graeff, R., and Walseth, T.F. (1995b). Cyclic ADP-ribose and its metabolic enzymes. Biochimie 77, 345-355.
53. 2+ signaling. Adv. Exper. Med. Biol. 419, 411-419.
54. Lee, H.C., Munshi, C., and Graeff, R. (1999). Structures and activities of cyclic ADP-ribose, NAADP and their metabolic enzymes. Mol. Cell. Biochem. 193, 89-98.
55. Lee, S.-J., Madden, P.J., and Shen, S.S. (1998). U73122 blocked the cGMP-induced calcium release in sea urchin eggs. Exp. Cell Res. 242, 328-340.
56. Masuda, W., Takenaka, S., Inageda, K., Nishina, H., Takahashi, K., Katada, T., Tsuyama, S., Inui, H., Miyatake, K., and Nakano, Y. (1997a). Oscillation of ADP-ribosyl cyclase activity during the cell cycle and function of cyclic ADP-ribose in a unicellular organism, Euglena Gracilis. FEBS Lett. 405, 104-106.
57. 2+ in a protist, Euglena Gracilis. Comp. Biochem. Physiol. 118, 279-283.
58. Mothet, J.P., Fossier, P., Meunier, F.M., Stinnakre, J., Taue, L., and Baux, G. (1998). Cyclic ADP-ribose and calcium-induced calcium release regulate neurotransmitter release at a cholinergic synapse of Aplysia. J. Physiol. 507.2, 405-414.
59. + glycohydrolase. J. Biol. Chem. 271, 23967-23972.
60. Munshi, C., Baumann, C., Levitt, D., Bloomfield, V.A., and Lee, H.C. (1998). The homo-dimeric form of ADP-ribosyl cyclase in solution. Biochim. Biophys. Acta 1388, 428-436.
61. Prasad, G.S., McRee, D.E., Stura, E.A., Levitt, D.G., Lee, H.C., and Stout, C.D. (1996). Crystal structure of Aplysia ADP ribosyl cyclase, a homologue of the bifunctional ectozyme CD38. Nature Struct. Biol. 3, 957-964.
62. 2+-mobilizing activity. J. Biol. Chem. 264, 11725-11731.
63. Santella, L., and Kyozuka, K. (1997). Association of calmodulin with nuclear structures in starfish oocytes and its role in the resumption of meiosis. Eur. J. Biochem. 246, 602-610.
64. Sauve, A.A., Munshi, C., Lee, H.C., and Schramm, V.L. (1998).The reaction mechanism for CD38. A single intermediate is responsible for cyclization, hydrolysis, and base-exchange chemistries. Biochemistry 37, 13239-13249.
65. Sethi, J.K., Empson, R.M., Bailey, V.C., Potter, B.V.L., and Galione, A. (1997). 7-Deaza-8-bromo-cyclic ADP-ribose, the first membrane-permeant, hydrolysis-resistant cyclic ADP-ribose antagonist. J. Biol. Chem. 272, 16358-16363.
66. 2+ release channel. EMBO J. 17, 2790-2798.
67. Sorrentino, V., and Volpe, P (1993). Ryanodine receptors: how many, where and why? Trends Pharmacol. Sci. 14, 98-103.
68. States, D.J., Walseth, T.F., and Lee, H.C. (1992). Similarities in amino acid sequences of Aplysia ADP-ribosyl cyclase and human lymphocyte antigen CD38. Trends Biochem. Sci. 17, 495.
69. Staxen, I., Pical, C., Montgomery, L.T., Gray, J.E., Hetherington, A.M., and McAinsh, M.R. (1999). Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. Proc. Natl. Acad. Sci. USA 96, 1779-1784.
70. Takasawa, S., Nata, K., Yonekura, H., and Okamoto, H. (1993a). Cyclic ADP-ribose in insulin secretion from pancreatic beta cells. Science 259, 370-373.
71. Takasawa, S., Tohgo, A., Noguchi, N., Koguma, T., Nata, K., Sugimoto, T., Yonekura, H., and Okamoto, H. (1993b). 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.
72. 2+ mobilization in normal and diabetic beta-cells. J. Biol. Chem. 273, 2497-2500.
73. Tao, W., Grubmeyer, C., and Blanchard, J.S. (1996). Transition state structure of Salmonella typhimurium orotate phosphoribosyltransferase. Biochemistry 35, 14-21.
74. 2+ oscillations in pancreatic acinar cells. EMBO J. 13, 2038-2043.
75. 2+ release. Biochim. Biophys. Acta 1178, 235-242.
76. Wilson, H.L., and Galione, A. (1998). Differential regulation of nicotinic acid adenine dinucleotide phosphate and cADP-ribose production by cAMP and cGMR Biochem. J. 331, 837-843.
77. Wu, Y., Kuzma, J., Marechal, E., Graeff, R., Lee, H.C., Foster, R., and Chua, N.H. (1997). Abscisic acid signaling through cyclic ADP-ribose in plants. Science 278, 2126-2130.
78. +-dependent internalization of the transmembrane glycoprotein CD38 in human Namalwa β cells. FEBS Lett. 396, 32-332.
79. Zocchi, E., Daga, A., Usai, C., Franco, L., Guida, L., Bruzzone, S., Costa, A., Marchetti, C., and Deflora, A. (1998). Expression of CD38 increases intracellular calcium concentration and reduces doubling time in HeLa and 3T3 cells. J. Biol. Chem. 273, 8017-8024.
80. + transport across cell membranes. FASEB J. 13, 273-283.