Calcium Signaling by Cyclic ADP-Ribose and NAADP: A Decade of Exploration

Cell Biochemistry and Biophysics

Volumn 28, Issue 1, 1998, Pages 1-17

  Lee, Hon Cheung ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

ADP ribosyl cyclase; Ca+2 signaling; CD38; Cyclic ADP ribose (cADPR); NAADP

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; CALCIUM; CYCLIC ADENOSINE DIPHOSPHATE RIBOSE; DRUG DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINIC ACID ADENINE DINUCLEOTIDE;

ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

ADENOSINE DIPHOSPHATE RIBOSE; ANIMALS; CALCIUM; CYCLIC ADP-RIBOSE; HUMANS; MODELS, MOLECULAR; NAD; SIGNAL TRANSDUCTION;

EID: 0031972642     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02738306     Document Type: Review

References (76)

1. Berridge, M. (1993) Inositol trisphosphate and calcium signalling. Nature 361, 315-325.
2. Lee, H. C. (1996) Cyclic ADP-ribose and calcium signaling in eggs. Biol. Signals 5, 101-110.
3. 2+ release channels and their regulation by endogenous effectors. Annu. Rev. Physiol. 56, 485-508.
4. Clementi, E., Riccio, M., Sciorati, C., Nistico, G., and Meldolesi, J. (1996) The type 2 ryanodine receptor of neurosecretory PC12 cells is activated by cyclic ADP-ribose. Role of the nitric oxide/cGMP pathway. J. Biol. Chem. 271, 17,739-17,745.
5. Willmott, N., Sethi, J. K., Walseth, T. F., Lee, H. C., White, A. M., and Galione, A. (1996) Nitric oxide-induced mobilization of intracellular calcium via the cyclic ADP-ribose signaling pathway. J. Biol. Chem. 271, 3699-3705.
6. Johnson, C. H., Knight, M. R., Kondo, T., Masson, P., Sedbrook, J., Haley, A., and Trewavas, A. (1995) Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 269, 1863-1865.
7. 2+-mobilizing activity. J. Biol. Chem. 264, 1608-1615.
8. 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.
9. Ghosh, T. K., Bian, J., and Gill, D. L. (1990) Intracellular calcium release mediated by sphingosine derivatives generated in cells. Science 248, 1653-1656.
10. 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.
11. 2+-release from non-mitochondrial stores in sea urchin egg homogenates. J. Biol. Chem. 260, 13,947-13,954.
12. Lee, H. C., Aarhus, R., Graeff, R., Gumack, M. E., and Walseth, T. F. (1994) Cyclic ADP ribose activation of the ryanodine receptor is mediated by calmodulin. Nature 370, 307-309.
13. Lee, H. C., Aarhus, R., and Graeff, R. M. (1995) Sensitization of calcium-induced calcium release by cyclic ADP-ribose and calmodulin. J. Biol. Chem. 270, 9060-9066.
14. 2+ channel triggered by cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA 92, 3244-3248.
15. Lee, H. C. and Aarhus, R. (1991) ADP-ribosyl cyclase: an enzyme that cyclizes NAD+ into a calcium-mobilizing metabolite. Cell Regul. 2, 203-209.
16. Yamada, S., Gu, Q. M., and Sih, C. J. (1994) Cyclic ADP-ribose via stereoselective cyclization β-NAD. J. Am. Chem. Soc. 116, 10,787, 10,788.
17. Lee, H. C., Aarhus, R., and Levitt, D. (1994) The crystal structure of cyclic ADP-ribose. Nature Struct. Biol. 1, 143,144.
18. 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.
19. 2+ mobilizing activities of cyclic ADP-ribose and inositol trisphosphate. Cell Regul. 1, 279-290.
20. 2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253, 1143-1146.
21. Lee, H. C. (1993) Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose. J. Biol. Chem. 268, 293-299.
22. Lee, H. C. (1996) Modulator and messenger functions of cyclic ADP-ribose in calcium signaling. Recent Prog. Horm. Res. 51, 355-388.
23. 2+ release by cyclic ADP-ribose. Trends Cell Biol. 4, 431-436.
24. Walseth, T. F., Aarhus, R., Zeleznikar, R. J., Jr., and Lee, H. C. (1991) Determination of endogenous levels of cyclic ADP-ribose in rat tissues. Biochim. Biophys. Acta 1094, 113-120.
25. 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.
26. Graeff, R. M., Walseth, T. F., and Lee, H. C. (1997) A radio-immunoassay for measuring endogenous levels of cyclic ADP-ribose in tissues. Meth. Enzymol. 280, 230-241.
27. 2+-mobilizing activity. J. Biol. Chem. 264, 11,725-11,731.
28. 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.
29. Lee, H. C., Galione, A., and Walseth, T. F. (1994) Cyclic ADP-ribose: metabolism and calcium mobilizing function. Vit. Horm. 48, 199-257.
30. 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.
31. Prasad, G. S., Levitt, D. G., Lee, H. C., and Stout, C. D. (1996) Crystallization of ADP-ribosyl cyclase from Aplysia californica. Proteins 24, 138-140.
32. Koshiyama, H., Lee, H. C., and Tashjian, A. H., Jr. (1991) Novel mechanism of intracellular calcium release in pituitary cells. J. Biol. Chem. 266, 16,985-16,988.
33. 2+ release. Biochim. Biophys. Acta 1178, 235-242.
34. Walseth, T. F., Aarhus, R., Kerr, J. A., and Lee, H. C. (1993) Identification of cyclic ADP-ribose-binding proteins by photoaffinity labeling. J. Biol. Chem. 268, 26,686-26,691.
35. Lee, H. C., Aarhus, R., and Walseth, T. F. (1993) Calcium mobilization by dual receptors during fertilization of sea urchin eggs. Science 261, 352-355.
36. 2+ release in T lymphocyte cell lines. J. Immunol. 155, 3353-3359.
37. 2+ release in intestinal longitudinal muscle. J. Biol. Chem. 270, 25,488-25,494.
38. Rakovic, S., Galione, A., Ashamu, G. A., Potter, B. V. L., and Terrar, D. A. (1996) A specific cyclic ADP-ribose antagonist inhibits cardiac excitation-contraction coupling. Curr. Biol. 6, 989-996.
39. Galione, A., Mcdougall, A., Busa, W. B., Willmott, N., Gillot, I., and Whitaker, M. (1993) Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs. Science 261, 348-352.
40. 2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature 365, 456-459.
41. 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.
42. 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.
43. 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, 26,052-26,054.
44. Kim, H., Jacobson, E. L., and Jacobson, M. K. (1993) Synthesis and degradation of cyclic ADP-ribose by NAD glycohydrolases. Science 261, 1330-1333.
45. + glycohydrolase, ADP-ribosyl cyclase and cyclic ADP-ribose hydrolase activities at the outer surface of human erythrocytes. Biochem. Biophys. Res. Comm. 196, 1459-1465.
46. Mehta, K., Shahid, U., and Malavasi, F. (1996) Human CD38, a cell-surface protein with multiple functions. FASEB J. 10, 1408-1417.
47. 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.
48. 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.
49. 2+ from a thapsigargin-insensitive pool. Biochem. J. 315, 721-725.
50. +. J. Biol. Chem. 271, 8513-8516.
51. Lee, H. C., Aarhus, R., Gee, K. R., and Kestner, T. (1997) Caged nicotinic acid adenine dinucleotide phosphate - synthesis and use. J. Biol. Chem. 272, 4172-4178.
52. 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, 30,327-30,333.
53. Lee, H. C., Graeff, R. M., Munshi, C. B., Walseth, T. F., and Aarhus, R. (1997) Large scale purification of Aplysia ADP-ribosyl cyclase and measurement of its activity by a fluorimetric assay. Meth. Enzymol. 280, 331-340.
54. Tohgo, A., Takasawa, S., Noguchi, N., Koguma, T., Nata, K., Sugimoto, T., Furuya, Y., Yonekura, H., and Okamoto, H. (1994) Essential cysteine residues for cyclic ADP-ribose synthesis and hydrolysis by CD38. J. Biol. Chem. 269, 28,555-28,557.
55. Berridge, M. J. (1993) A tale of two messengers. Nature 365, 388,389.
56. 2+ from islet microsomes. J. Biol. Chem. 272, 3133-3136.
57. Ayabe, T., Kopf, G. S., and Schultz, R. M. (1995) Regulation of mouse egg activation: presence of ryanodine receptors and effects of microinjected ryanodine and cyclic ADP ribose on uninseminated and inseminated eggs. Develop. 121, 2233-2244.
58. Yue, C., White, K. L., Reed, W. A., and Bunch, T. D. (1995) The existence of inositol 1,4,5-trisphosphate and ryanodine receptors in mature bovine oocytes. Develop. 121, 2645-2654.
59. 2+ channel. Nature 364, 76-79.
60. 2+ release channel. Am. J. Physiol. 268, C1235-1240.
61. Kannan, M. S., Fenton, A. M., Prakash, Y. S., and Sieck, G. C. (1996) Cyclic ADP-ribose stimulates sarcoplasmic reticulum calcium release in porcine coronary artery smooth muscle. Am. J. Physiol. 39, H801-H806.
62. Takasawa, S., Nata, K., Yonekura, H., and Okannoto, H. (1993) Cyclic ADP-ribose in insulin secretion from pancreatic beta cells. Science 259, 370-373.
63. 2+ oscillations in pancreatic acinar cells. EMBO J. 13, 2038-2043.
64. 2+ from single isolated pancreatic zymogen granules. Cell 84,473-480.
65. 2+ entry in bullfrog sympathetic neurons. Neuron 12, 1073-1079.
66. 2+-dependent currents in cultured rat dorsal root ganglion neurons by a sperm factor and cyclic ADP-ribose. Mol. Biol. Cell 3, 1415-1425.
67. 2+ release from rat brain microsomes. FEBS Lett. 318, 259-263.
68. Higashida, H., Robbins, J., Egorova, A., Noda, M., Taketo, M., Ishizaka, N., Takasawa, S., Okamoto, H., and Brown, D. A. (1995) Nicotinamide adenine dinucleotide regulates muscarinic receptor-coupled K+ (M) channels in rodent NG108-15 Cells. J. Physiol. 482, 317-323.
69. Linden, D. J., Dawson, T. M., and Dawson, V. L. (1995) An evaluation of the nitric oxide/cGMP/cGMP-dependent protein kinase cascade in the induction of cerebellar long-term depression in culture. J. Neurosci. 15, 5098-5105.
70. Deflora, A., Guida, L., Franco, L., Zocchi, E., Pestarino, M., Usai, C., Marchetti, C., Fedele, E., Fontana, G., and Raiteri, M. (1996) Ecto-cellular in vitro and in vivo metabolism of cADP-ribose in cerebellum. Biochem. J. 320, 665-671.
71. 2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose. Science 268, 735-737.
72. 2+ from the nuclear envelope. Cell 80, 439-444.
73. 2+ release in mouse T-lymphoma cells. J. Biol. Chem. 270, 17,917-17,922.
74. 2+ from, distinct intracellular pools in permeabilized lacrimal acinar cells. FEBS Lett. 360, 303-306.
75. 2+ and inorganic phosphate. J. Biol. Chem. 271, 23,946-23,953.
76. 2+ in isolated rat osteoclasts. Am. J. Physiol. 39, F469-F475.