Skip to main content
SpringerLink
Log in

The Ca2+-Mobilizing Second Messenger Cyclic ADP-Ribose

  • Chapter
Calcium: The Molecular Basis of Calcium Action in Biology and Medicine

Abstract

Signal transduction via elevation of the intracellular free Ca2+-concentration ([Ca2+] i ) is one of the fundamental events observed in cell regulation. Cellular systems as diverse as oocytes, muscle cells, neurons and cells of the immune system, but also plant cells and protozoa utilize Ca2+-signaling to fulfill their diverse physiological functions. This fundamental importance implies that the principle of Ca2+-signaling — an elevation of the concentration of free Ca2+-ions in the cytosol, the nucleus and perhaps also inside specific organelles — has been conserved during evolution. On the other hand, research in the field of Ca2+-signaling during the last years has shown that multiple cellular mechanisms with a multitude of molecular players are involved in the regulation of [Ca2+] i . The main cellular mechanisms that directly increase [Ca2+] i are Ca2+-release from intracellular Ca2+-stores and Ca2+-entry across the plasma membrane. Re-uptake into Ca2+-stores, active transport of Ca2+-ions from the cytosol into the extracellular space and buffering by Ca2+-binding proteins are the mechanisms to decrease [Ca2+] i .

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ashamu, G.A., Sethi, J.K., Galione, A. and Potter, B.V.L., 1997, Roles for adenosine ribose hydroxyl groups in cyclic adenosine 5′-diphsophate ribose-mediated Ca2+-release, Biochemistry 36, 9509–9517.

    Article  PubMed  CAS  Google Scholar 

  • Ashcroft, KM. and Ashcroft, S.J.H., 1992, Mechanism of insulin secretion, in Insulin — Molecular Biology to Pathology, KM. Ashcroft and S.J.H. Ashcroft (eds.), Oxford University Press, Oxford, pp. 97–150.

    Google Scholar 

  • Bailey, V.C., Fortt, S.M., Summerhill, R.J., Galione, A. and Potter, B.V.L., 1996, Cyclic aristeromycin diphosphate ribose: A potent and poorly hydrolysable Ca2+-mobilising mimic of cyclic adenosine diphosphate ribose, FEBS Lett. 379, 227–230.

    Article  PubMed  CAS  Google Scholar 

  • Bailey, V.C., Sethi, J.K., Fortt, S.M., Galione, A. and Potter, B.V.L., 1997, 7-Deaza cyclic adenosine 5′-diphosphate ribose: First example of a Ca2+-mobilizing partial agonist related to cyclic adenosine 5′-diphosphate ribose, Chem. Biol. 4, 51–61.

    Article  PubMed  CAS  Google Scholar 

  • Berridge, M.J., 1993, Inositol trisphosphate and calcium signaling, Nature 361, 315–325.

    Article  PubMed  CAS  Google Scholar 

  • Cancela, J.M. and Petersen, O.H., 1998, The cyclic ADP-ribose antagonist 8-NH2-cADP-ribose blocks cholecystokinin-evoked cytosolic Ca2+ spiking in pancreatic acinar cells, Pflügers Arch. Eur. J. Physiol. 435, 746–748.

    Article  CAS  Google Scholar 

  • Cancela, J.M., Churchill, G.C. and Galione, A., 1999, Coordination of agonist-induced Ca2+-signaling patterns by NAADP in pancreatic acinar cells, Nature 398, 74–76.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Clementi, E., Riccio, M., Sciorati, C., Nistico, G. and Meldolesi, J., 1996, The type 2 ryanodine receptor of neurosecretory PC 12 cells is activated by cyclic ADP-ribose, J. Biol. Chem. 271, 17739–17745.

    Article  PubMed  CAS  Google Scholar 

  • Cui, Y., Galione, A. and Terrar, D.A., 1999, Effects of photoreleased cADP-ribose on calcium transients and calcium sparks in myocytes isolated from guinea-pig and rat ventricles, Biochem. J. 342, 269–273.

    Article  PubMed  CAS  Google Scholar 

  • da Silva, C, Heyer, P., Schweitzer, K., Malavasi, F., Mayr, G.W. and Guse, A.H., 1998a, Ectocellular CD38-catalyzed synthesis and intracellular Ca2+-signaling activity of cyclic ADP-ribose in T-lymphocytes are not functionally related, FEBS Lett. 439, 291–296.

    Article  PubMed  Google Scholar 

  • da Silva, CP, Potter, B.V.L., Mayr, G.W. and Guse, A.H., 1998b, Quantification of intracellular levels of cyclic ADP-ribose by high-performance liquid chromatography, J. Chromatogr. B 707, 43–50.

    Article  Google Scholar 

  • Dousa, T.P., Chini, E.N. and Beers, K.W., 1996, Adenine nucleotide diphosphates: Emerging second messengers acting via intracellular Ca2+ release, Am. J. Physiol. 271 (Cell Physiol. 40), C1007–C1024.

    PubMed  CAS  Google Scholar 

  • Ebihara, S., Sasaki, T., Hida, W., Kikuchi, Y., Oshiro, T., Shimura, S., Takasawa, T., Okamoto, H., Nishiyama, A., Akaike, N. and Shirato, K., 1997, Role of cyclic ADP-ribose in ATP-activated potassium currents in alveolar macrophages, J. Biol. Chem. 272, 16023–16029.

    Article  PubMed  CAS  Google Scholar 

  • Favre, C.J., Nüsse, O., Lew, D.P. and Krause, K.-H., 1996, Store-operated Ca2+ influx: What is the message from the stores to the membrane?, J. Lab. Clin. Med. 128, 1–9.

    Article  Google Scholar 

  • Franco, L., Guida, L., Bruzzone, S., Zocchi, E., Usai, C. and de Flora, A., 1998, The transmembrane glycoprotein CD38 is a catalytically active transporter responsible for generation and influx of the second messenger cADPR across membranes, FASEB J. 12, 1507–1520.

    PubMed  CAS  Google Scholar 

  • Galione, A., Lee, H.C. and Busa W.B.,1991, Ca2+-induced Ca2+-release in sea urchin egg homogenates: Modulation by cyclic ADP-ribose, Science 253, 1143–1146.

    Article  PubMed  CAS  Google Scholar 

  • Galione, A., White, A., Willmott, N., Turner, M., Potter, B.V.L. and Watson, S.P., 1993, cGMP mobilizes intracellular Ca2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis, Nature 365, 456–459.

    Article  PubMed  CAS  Google Scholar 

  • Graeff, R.M., Franco, L., De Flora, 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.

    Article  PubMed  CAS  Google Scholar 

  • Guse, A.H., da Silva, CP, Emmrich, F., Ashamu, G.A., Potter, B.V.L. and Mayr, G.W, 1995, Characterization of cyclic adenosine diphosphate-ribose-induced Ca2+-release in T-lymphocyte cell lines, J. Immunol. 155, 3353–3359.

    PubMed  CAS  Google Scholar 

  • Guse, A.H., da Silva, C.P., Weber, K., Ashamu, G.A., Potter, B.V.L. and Mayr, G.W, 1996, Regulation of cyclic ADP-ribose-induced Ca2+-release by Mg2+ and inorganic phosphate, J. Biol. Chem. 271, 23946–23954.

    Article  PubMed  CAS  Google Scholar 

  • Guse, A.H., da Silva, C.P., Weber, K., Armah, C., Schulze, C., Potter, B.V.L., Mayr, G.W. and Hilz, H., 1997a, 1-(5-Phospho-β-D-ribosyl)2′-phosphoadenosine 5′-phosphate cyclic anhydride-induced Ca2+-release in human T cell lines, Eur. J. Biochem. 245, 411–417.

    Article  PubMed  CAS  Google Scholar 

  • Guse, A.H., Berg, I., da Silva, C.P., Potter, B.V.L. and Mayr, G.W, 1997b, Ca2+-entry induced by cyclic ADP-ribose in intact T-lymphocytes, J. Biol. Chem. 272, 8546–8550.

    Article  PubMed  CAS  Google Scholar 

  • Guse, A.H., 1998, Ca2+-signaling in T-lymphocytes, Crit. Rev. Immunol 18, 419–448.

    Article  PubMed  CAS  Google Scholar 

  • Guse, A.H., 1999, Cyclic ADP-ribose: A novel Ca2+-mobilising second messenger, Cell. Signal. 5, 309–316.

    Article  Google Scholar 

  • Guse, A.H., da Silva, C.P., Berg, I., Weber, K., Heyer, R., Hohenegger, M., Ashamu, G.A., Skapenko, A.L., Schulze-Koops, H., Potter, B.V.L. and Mayr, G.W., 1999, Regulation of Ca2+-signaling in T-lymphocytes by the second messenger cyclic ADP-ribose, Nature 398, 70–73.

    Article  PubMed  CAS  Google Scholar 

  • Hellmich, M.R. and Strumwasser, F., 1991, Purification and characterization of a molluscan egg-specific NADase, a second messenger enzyme, Cell Reg. 2, 193–202.

    CAS  Google Scholar 

  • Higashida, H., Yokoyama, S., Hashii, M., Taketo, M., Higashida, M., Takayasu, T., Ohshima, T., Takasawa, S., Okamoto, H. and Noda, M., 1997, Muscarinic receptor-mediated dual regulation of ADP-ribosyl cyclase in NG108-15 neuronal cell membranes, J. Biol. Chem. 272,31272–31277.

    Article  PubMed  CAS  Google Scholar 

  • Higashida, H., Egorova, A., Higashida, C., Zhong, Z.G., Yokohama, S., Noda, M. and Zhang, J.S., 1999, Sympathetic potentiation of cyclic ADP-ribose formation in rat cardiac myocytes, J. Biol. Chem. 274, 33348–33354.

    Article  PubMed  CAS  Google Scholar 

  • Hirata, Y., Kimuram, 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.

    Article  PubMed  CAS  Google Scholar 

  • Howard, M., Grimaldi, J.C., Bazan, J.F., Lund, F., Santos-Argumedo, L., Parkhouse, R.M.E., Walseth, T.F. and Lee, H.C., 1993, Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38, Science 262, 1056–1059.

    Article  PubMed  CAS  Google Scholar 

  • Ikehata, F., Satoh, J., Nata, K., Tohgo, A., Nakazawa, T., Kato, I., Kobayashi, I., Akiyama, T., Takasawa, S., Toyota, T. and Okamoto, H., 1998, Autoantibodies against CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase) that impair glucose-induced insulin secretion in noninsulin-dependent diabetes patients, J. Clin. Invest. 102, 395–401.

    Article  PubMed  CAS  Google Scholar 

  • 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 β cells, J. Biol. Chem. 270, 30045–30050.

    Article  PubMed  CAS  Google Scholar 

  • Kim, H., Jacobson, E.L. and Jacobson, M.K., 1993, Synthesis and degradation of cyclic ADP-ribose by NAD glycohydrolases, Science 261, 1330–1333.

    Article  PubMed  CAS  Google Scholar 

  • Kuemmerle, J.F. and Makhlouf, G.M., 1995, Agonist-stimulated cyclic ADP-ribose, J. Biol. Chem. 270, 25488–25494.

    Article  PubMed  CAS  Google Scholar 

  • Lee, H.C., Walseth, T.F., Bratt, G.T., Hayes, R.N. and Clapper, D.L., 1989. Structural determination of a cyclic metabolite of NAD+ with intracellular Ca2+-mobilizing activity, J. Biol. Chem. 264, 1608–1615.

    PubMed  CAS  Google Scholar 

  • Lee, H.C., 1993, Potentiation of calcium-and caffeine-induced calcium release by cADPR, J. Biol. Chem. 268, 293–299.

    PubMed  CAS  Google Scholar 

  • Lee, H.C., Aarhus, R. and Walseth, T.F., 1993, Calcium mobilization by dual receptors during fertilization of sea urchin eggs, Science 1993, 352–355.

    Google Scholar 

  • Lee, H.C., 1994, The crystal structure of cyclic ADP-ribose, Nature Struct. Biol. 1, 143–144.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Lee, H.C., 1997, Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP, Physiol. Rev. 77, 1133–1164.

    PubMed  CAS  Google Scholar 

  • Lee, H.C., 1999, A unified mechanism of enzymatic synthesis of two calcium messengers: cADPR and NAADP, Biol. Chem. 380, 785–793.

    Article  PubMed  CAS  Google Scholar 

  • Masuda, W., Takenaka, S., Tsuyama, S., Tokunaga, M., Yamaji, R., Inui, H., Miyatake, K. and Nakano, Y, 1997, Inositol 1,4,5-trisphosphate and cyclic ADP-ribose mobilize Ca2+ in a protist, Euglena gracilis, Comp. Biochem. Physiol. 118, 279–283.

    CAS  Google Scholar 

  • Matsumura, N. and Tanuma, S., 1998, Involvement of cytosolic NAD+ glycohydrolase in cADPR metabolism, Biochem. Biophys. Res. Commun. 253, 246–252.

    Article  PubMed  CAS  Google Scholar 

  • Meszaros, L.G., Bak, J. and Chu, A., 1993, Cyclic ADP-ribose as an endogenous activator of the non-skeletal type ryanodine receptor Ca2+ channel, Nature 364, 76–79.

    Article  PubMed  CAS  Google Scholar 

  • Migaud, M.E., Pederick, R.L., Bailey, V.C. and Potter, B.V.L., 1999, Probing Aplysia californica adenosine 5′-diphosphate-ribosyl cyclase for substrate binding requirements: Design of potent inhibitors, Biochemistry 38, 9195–9214.

    Article  Google Scholar 

  • Morita, K., Kitayama, S. and Dohi, T., 1997, Stimulation of cyclic ADP-ribose synthesis by acetylcholine and ist role in catecholamine release in bovine adrenal chromaffin cells, J. Biol. Chem. 272, 21002–21009.

    Article  PubMed  CAS  Google Scholar 

  • Munshi, C., Fryxell, K.B., Lee, H.C. and Branton, W.B., 1997, Large-scale production of human CD38 in yeast fermentation, Meth. Enzymol. 280, 318–330.

    Article  PubMed  CAS  Google Scholar 

  • Munshi, C., Thiel, D.J., Mathews, I.I., Aarhus, R., Walseth, T.F. and Lee, H.C., 1999, Characterization of the active site of ADP-ribosyl cyclase, J. Biol. Chem. 274, 30770–30777.

    Article  PubMed  CAS  Google Scholar 

  • Ng, J., Gustavsson, J., Jondal, M. and Andersson, T., 1990, Regulation of calcium influx across the plasma membrane of the human T-leukemic cell line, JURKAT: Dependence on a rise in cytosolic free calcium can be dissociated from formation of inositol phosphates, Biochim. Biophys. Acta 1053, 97–105.

    Article  PubMed  CAS  Google Scholar 

  • Prakash, Y.S., Kannan, M.S., Walseth, T.F. and Sieck, G.C., 1998, Role of cyclic ADP-ribose in the regulation of [Ca2+]i in porcine tracheal smooth muscle, Am. J. Physiol. 274 (Cell Physiol. 43), C1653–C1660.

    PubMed  CAS  Google Scholar 

  • Prasad, G.S., McRee, D.E., Stura, E.A., Levitt, D.G., Lee, H.C. and Stout, CD., 1996, Crystal structure of Aplysia ADP ribosyl cyclase, a homologue of the bifunctional ectoenzyme CD38, Nature Struct. Biol. 3, 957–964.

    Article  PubMed  CAS  Google Scholar 

  • Putney, J.W., Jr., 1986, A model for receptor-regulated calcium entry, Cell Calcium 7, 1–12.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Rakovic, S., Ciu, Y., Iino, S., Galione, A., Ashamu, G.A., Potter, B.V.L. and Terrar, D.A., 1999, An antagonist of cADP-ribose inhibits arrythmogenic oscillations of intracellular Ca2+ in heart cells, J. Biol. Chem. 274, 17820–17827.

    Article  PubMed  CAS  Google Scholar 

  • Reyes-Harde, M., Empson, R., Potter, B.V.L., Galione, A. and Stanton, P.K., 1999, Evidence of a role for cyclic ADP-ribose in long-term synaptoc depression in hippocampus, Proc. Natl. Acad. Sci. USA 96, 4061–4066.

    Article  PubMed  CAS  Google Scholar 

  • Schulz, I., Krause, E., Gonzalez, A., Göbel, A., Sternfeld, L. and Schmid, A., 1999, Agonist-stimulated pathways of calcium signaling in pancreatic acinar cells, Biol. Chem. 380, 903–908.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sitsapesan, R. and Williams, A.J., 1995, Cyclic ADP-ribose and related compounds activate sheep skeletal sarcoplasmic reticulum Ca2+ release channel, Am. J. Physiol. 268 (Cell Physiol. 37), C1235–C1240.

    PubMed  CAS  Google Scholar 

  • Sonnleitner, A., Conti, A., Bertocchini, F., Schindler, H.G. and Sorrentino, V, 1998, Functional properties of the ryanodine receptor type 3 (RyR3) Ca2+ release channel, EMBO J. 17, 2790–2798.

    Article  PubMed  CAS  Google Scholar 

  • Takasawa, S., Tohgo, A., Noguchi, N., Koguma, T., Nata, K., Sugimoto, T., Yonekura, H. and Okamoto, H., 1993a, 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.

    PubMed  CAS  Google Scholar 

  • Takasawa, S., Nata, K., Yonekura, H. and Okamoto, H., 1993b, Cyclic ADP-ribose in insulin secretion from pancreatic β cells, Science 259, 370–373.

    Article  PubMed  CAS  Google Scholar 

  • Takasawa, S., Akiyama, T., Nata, K., Kuroki, M., Tohgo, A., Noguchi, N., Kobayashi, S., Kato, I., Katada, T. and Okamoto, H., 1998, Cyclic ADP-ribose and inositol 1,4,5-trsiphosphate as alternate second messengers for intracellular Ca2+ mobilization in normal and diabetic β-cells, J. Biol. Chem. 273, 2497–2500.

    Article  PubMed  CAS  Google Scholar 

  • Thorn, P., Gerasimenko, O. and Petersen O.H., 1994, Cyclic ADP-ribose regulation of ryanodine receptors involved in agonist evoked cytosolic Ca2+-oscillations in pancreatic acinar cells, EMBO J. 13, 2038–2043.

    PubMed  CAS  Google Scholar 

  • Vu, C.Q., Lu, P.-J., Chen, CS. and Jacobson, M.K., 1996, 2′-Phospho-cyclic ADP-ribose, a calcium-mobilizing agent derived from NADP, J. Biol Chem. 271, 4747–4754.

    Article  PubMed  Google Scholar 

  • 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, 26686–26691.

    PubMed  CAS  Google Scholar 

  • Walseth, T.F. and Lee, H.C, 1993, Synthesis and characterization of antagonists of cyclic-ADP-ribose-induced Ca2+-release, Biochim. Biophys. Acta 1178, 235–242.

    Article  PubMed  CAS  Google Scholar 

  • Willmott, N., Sethi, J., 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. 27l, 3699–3705.

    Google Scholar 

  • Wong, L., Aarhus, R., Lee, H.C. and Walseth, T.F., 1999, Cyclic 3-deaza-adenosine diphosphoribose: A potent and stable analog of cyclic ADP-ribose, Biochim. Biophys. Acta 1472, 555–564.

    Article  PubMed  CAS  Google Scholar 

  • Wu, Y., Kuzma, J., Marechal, E., Graeff, R., Lee, H.C., Foster, R. and Chuah, N.H., 1997, Abscisic acid signaling through cyclic ADP-ribose in plants, Science, 278, 2126–2130.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, F.-J., Gu, Q.-M., Jing, P. and Sih, C.J., 1995, Enzymatic cyclization of nicotinamide adenine dinucleotide phosphate (NADP), Bioorg. Med. Chem. Lett. 19, 2267–2272.

    Article  Google Scholar 

  • Zhang, F.-J., Yamada, S., Gu, Q.-M. and Sih, C.J., 1996, Synthesis and characterization of cyclic ATP-ribose: A potent mediator of calcium release, J. Bioorg. Med. Chem. Lett. 6, 1203–1208.

    Article  CAS  Google Scholar 

  • Zhang, F.-J., Gu, Q.-M. and Sih, C.J., 1999, Bioorganic chemistry of cyclic ADP-ribose (cADPR), Bioorg. Med. Chem. 1, 653–664.

    Article  Google Scholar 

  • Zocchi, E., Daga, A., Usai, C., Franco, L., Guida, L., Bruzzone, S., Costa, A., Marchetti, C. and De Flora, A., 1998, Expression of CD38 increases intracellular calcium concentration and reduces doubling time in HeLa and 3T3 cells, J. Biol Chem. 273, 8017–8024.

    Article  PubMed  CAS  Google Scholar 

  • Zocchi, E., Usai, C., Guida, L., Franco, L., Bruzzone, S., Passalacqua, M. and de Flora, A., 1999, Ligand-induced internalization of CD38 results in intracellular Ca2+ mobilization: Role of NAD transport across cell membranes, FASEB J. 13, 273–283.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Cellular Signal Transduction, Institute for Medical Biochemistry and Molecular Biology, University Hospital Eppendorf, University of Hamburg, Hamburg, Germany

    Andreas H. Guse

Authors
  1. Andreas H. Guse
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Université Libre de Bruxelles, Belgium

    Roland Pochet

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer Science+Business Media New York

About this chapter

Cite this chapter

Guse, A.H. (2000). The Ca2+-Mobilizing Second Messenger Cyclic ADP-Ribose. In: Pochet, R., Donato, R., Haiech, J., Heizmann, C., Gerke, V. (eds) Calcium: The Molecular Basis of Calcium Action in Biology and Medicine. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0688-0_7

Download citation

  • DOI: https://doi.org/10.1007/978-94-010-0688-0_7

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-0-7923-6422-1

  • Online ISBN: 978-94-010-0688-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation