Regulation of Immune Responses by CD38 and cADPR



CD38 was identified more than 20 years ago as a cell surface protein expressed on leukocyte subsets [1, 2]. Over the last decade, antibodies to human CD38 have been used to classify tumors from Multiple Myeloma [3, 4] and Chronic Lymphocytic Leukemia patients [5, 6], to identify which HIV+ patients will develop AIDS [7] and to subset a variety of leukocyte populations including hematopoietic progenitors [8, 9], germinal center B cells [10, 11] and regulatory T cells [12, 13]. However, despite the clear utility of using anti-CD38 antibodies as diagnostic and prognostic tools, it was unclear whether CD38 itself played an important functional role on normal lymphocytes. Since CD38 is expressed on the plasma membrane, it was postulated that CD38 was involved in leukocyte signaling or adhesion [14-16]. Although numerous experiments demonstrated that antibody mediated crosslinking of CD38 activated a variety of different signaling pathways in lymphocytes (reviewed in ref. [17, 18]), it was unclear how CD38 initiated signal transduction since the cytoplasmic tail of CD38 does not contain any known signaling motifs [2, 19].


Hyaluronic Acid Neutrophil Chemotaxis Formylated Peptide Receptor Murine CD38 Nicotinic Acid Adenine Dinucleotide Phosphate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Reinherz EL. Kung PC. Goldstein G. Levey RH and Schlossman SF. 1980. Discrete stages of intrathymic differentiation: analysis of normal thymocytes and leukemic lymphoblasts of the T lineage. Proc. Natl. Acad. Sci. USA. 11: 1588–1592.CrossRefGoogle Scholar
  2. 2.
    Jackson DG and Bell JI. 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.PubMedGoogle Scholar
  3. 3.
    Kawano MM. Mihara K. Tsujimoto T. Huang N and Kuramoto A. 1995. A new phenotypic classification of bone marrow plasmacytosis. Int. J. Hematol. 61: 179–188.PubMedCrossRefGoogle Scholar
  4. 4.
    San Miguel JF. Garcia-Sanz R. Gonzalez M. Moro MJ, Hernandez JM, et al. 1995. A new staging system for multiple myeloma based on the number of S-phase plasma cells. Blood 85: 448–455.PubMedGoogle Scholar
  5. 5.
    Damle RN. Wasil T. Fais F. Ghiotto F. Valetto A, et al. 1999. Ig V gene mutation status and CD38 expression as novel prognostic indicators in chronic lymphocytic leukemia. Blood 94: 1840–1847.PubMedGoogle Scholar
  6. 6.
    Ibrahim S. Keating M. Do KA. O’Brien S, Huh YO, et al. 2001. CD38 expression as an important prognostic factor in B-cell derived lymphocytic leukemia. Blood 98: 181–186.PubMedCrossRefGoogle Scholar
  7. 7.
    Liu Z, Cumberland WG, Hultin LE. Prince HE, Detels R and Giorgi JV. 1997. Elevated CD38 antigen expression on CD8+ T cells is a stronger marker for the risk of chronic HIV disease progression to AIDS and death in the multicenter AIDS cohort study thanCD4+ cell count soluble immune activation markers, or combinations of HLA-DR and CD38 expression. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 16: 83–92.Google Scholar
  8. 8.
    Terstappen LWMM, Huang S. Safford M, Landsorp PM and Loken MR. 1991. Sequential generations of hematopoietic colonies derived from single nonlineage-committed CD34+ CD38+ progenitor cells. Blood 11: 1218–1227.Google Scholar
  9. 9.
    Randall TD, Lund FE, Howard MC and Weissman IL. 1996. Expression of murine CD38 defines a population of long-term reconstituting hematopoietic stem cells. Blood 87: 4057–4067.PubMedGoogle Scholar
  10. 10.
    Liu YJ, Malisan F, de Bouteiller O, Guret C. Lebecque S, et al. 1996. Within germinal centers, isotype switching of immunoglobulin genes occurs after the onset of somatic mutation. Immunity 4: 241–250.PubMedCrossRefGoogle Scholar
  11. 11.
    Oliver AM. Martin F and Kearney JF. 1997. Mouse CD38 is down-regulated on germinal center B cells and mature plasma cells. J. Immunol. 158: 1108–1115.PubMedGoogle Scholar
  12. 12.
    Bean AGD. Godfrey DI, Ferlin WG, Santos-Argumedo L, Parkhouse RME, et al. 1995. CD38 expression on mouse T cells: CD38 defines functionally distinct subsets of ap TCR+CD4CD8+ thymocytes. Int. Immunol. 7: 213–221.PubMedCrossRefGoogle Scholar
  13. 13.
    Read S, Mauze S, Asseman C. Bean A, Coffman R and Powrie F. 1998. CD38+ CD45RBlow CD4+ T cells: a population of T cells with immune regulatory activities in vitro. Eur. J. Immunol. 28: 3435–3447.PubMedCrossRefGoogle Scholar
  14. 14.
    Funaro A, Spagnoli GC, Ausiello CM, Alessio M, Roggero S, et al. 1990. Involvement of the multilineage CD38 molecule in a unique pathway of cell activation and proliferation. J. Immunol. 145:2390–2396.PubMedGoogle Scholar
  15. 15.
    Malavasi F, Funaro A. Alessio M, De Monte LB, Ausiello CM, et al. 1992. CD38: A multi-lineage cell activation molecule with a split personality. Int. J. Clin. Lab. Res. 22: 73–80.PubMedCrossRefGoogle Scholar
  16. 16.
    Malavasi F, Funaro A, Roggero S. Horenstein A, Calosso L and Mehta K. 1994. Human CD38: a glycoprotein in search of a function. Immunol. Today 15: 95–97.PubMedCrossRefGoogle Scholar
  17. 17.
    Mehta K, Shahid U and Malavasi F. 1996. Human CD38, a cell-surface protein with multiple functions. FASEB J. 10: 1408–1417.PubMedGoogle Scholar
  18. 18.
    Lund FE. Cockayne DA. Randall TD, Solvason N, Schuber F and Howard MC. 1998. CD38: A new paradigm in lymphocyte activation and signal transduction. Immunol. Rev. 161:79–93.PubMedCrossRefGoogle Scholar
  19. 19.
    Harada N. Santos-Argumedo L, Chang R, Grimaldi JC, Lund FE, et al. 1993. Expression cloning of a cDNA encoding a novel murine B cell activation marker. J. Immunol. 151: 3111–3118.PubMedGoogle Scholar
  20. 20.
    Howard M, Grimaldi JC, Bazan JF, Lund FE, Santos-Argumedo L, et al. 1993. Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science 262: 1056–1059.PubMedCrossRefGoogle Scholar
  21. 21.
    Takasawa S. Togho A, Noguchi N, Koguma T, Nata K, et al. 1993. Synthesis and hydrolysis of cyclic ADP-ribose by human leukocyte antigen CD38 and inhibition of the hydrolysis by ATP. J. Biol. Chem. 268: 26052–4.PubMedGoogle Scholar
  22. 22.
    Summerhill RJ, Jackson DG and Galione A. 1993. Human lymphocyte antigen CD38 catalyzes the production of cyclic ADP-ribose. FEBS Lett. 335: 231–233.PubMedCrossRefGoogle Scholar
  23. 23.
    Zocchi E. Franco L, Guida L, Benatti U, Bargellesi A, et al. 1993. A single protein immunologically identified as CD38 displays NAD+ glycohydrolase, ADP-ribosyl cyclase and cyclic ADP-ribosyl hydrolase activities at the outer surface of human erythrocytes. Biochem. Biophys. Res. Comm. 196: 1459–1465.PubMedCrossRefGoogle Scholar
  24. 24.
    Aarhus R, Graeff RM, Dickey DM, Walseth TF and Lee HC. 1995. ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium mobilizing metabolite from NADP. J. Biol. Chem. 270: 30327–30333.PubMedCrossRefGoogle Scholar
  25. 25.
    Kumagai M. Coustan-Smith E. Murray DJ, Silvennoinen O, Murti KG, et al. 1995. Ligation of CD38 suppresses human B lymphopoiesis. J. Exp. Med. 181: 1101–1110.PubMedCrossRefGoogle Scholar
  26. 26.
    Lund FE. Muller-Steffner HM. Yu N. Stout CD, Schuber F and Howard M. 1999. CD38 signaling is controlled by its ectodomain but occurs independently of enzymatically generated ADP-ribose or cyclic ADP-ribose. J. Immunol. 162: 2693–2702.PubMedGoogle Scholar
  27. 27.
    Kitanaka A, Suzuki T, Ito C, Nishigaki H. Coustan-Smith E, et al. 1999. CD38-mediated signaling events in murine pro-B cells expressing human CD38 with or without its cytoplasmic domain. J. Immunol. 162: 1952–1958.PubMedGoogle Scholar
  28. 28.
    Partida-Sanchez S, Cockayne DA. Monard S. Jacobson EL, Oppenheimer N, et al. 2001. Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo. Nature Med. 7: 1209–1216.PubMedCrossRefGoogle Scholar
  29. 29.
    Cockayne D, Muchamuel T. Grimaldi JC. Muller-Steffner H, Randall TD. et al. 1998. Mice deficient for the ecto-NAD+ glycohydrolase CD38 exhibit altered humoral immune responses. Blood 92: 1324–1333.PubMedGoogle Scholar
  30. 30.
    Shubinsky G and Schlesinger M. 1997. The CD38 lymphocyte differentiation marker-New insight into its ectoenzymatic activity and its role as a signal transducer. Immunity 7:315–324.PubMedCrossRefGoogle Scholar
  31. 31.
    Santos-Argumedo L. Teixeira C. Preece G. Kirkham PA and Parkhouse RME. 1993. A B lymphocyte surface molecule mediating activation and protection from apoptosis via calcium channels. J. Immunol. 151: 3119–3130.PubMedGoogle Scholar
  32. 32.
    Santos-Argumedo L. Lund FE. Heath AW, Solvason N. Wu WW, et al. 1994. CD38 unresponsiveness of xid B cells implicates Bruton's tyrosine kinase (btk) as a regulator of CD38 induced signal transduction. Int. Immunol. 7: 163–170.CrossRefGoogle Scholar
  33. 33.
    Lund FE. Solvason NW. Cooke MP. Heath AW, Grimaldi JC, et al. 1995. Signaling through murine CD38 is impaired in antigen receptor unresponsive B cells. Eur. J. Immunol. 25: 1338–1345.PubMedCrossRefGoogle Scholar
  34. 34.
    Lund FE. Yu N. Kim K-M, Reth M and Howard MC. 1996. Signaling through CD38 augments B cell antigen receptor (BCR) responses and is dependent on BCR expression. J. Immunol. 157: 1455–1467.PubMedGoogle Scholar
  35. 35.
    Yamashita Y. Miyake K. Kikuchi Y. Takatsu K, Noda S and Kosugi A. 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.PubMedGoogle Scholar
  36. 36.
    Kikuchi Y. Yasue T. Miyake K. Kimoto M and Takatsu K. 1995. CD38 ligation induces tyrosine phosphorylation of Bruton tyrosine kinase and enhanced expression of interleukin 5-receptor a chain: Synergistic effects with interleukin 5. Proc. Natl. Acad. Sci. USA. 92: 11814–11818.PubMedCrossRefGoogle Scholar
  37. 37.
    Yasue T. Nishizumi H. Aizawa S. Yamamoto T, Miyake K, et al. 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.PubMedCrossRefGoogle Scholar
  38. 38.
    Kitanaka A. Ito C. Nishigaki H and Campana D. 1996. CD38 mediated growth suppression of B-cell progenitors requires activation of phosphatidylinositol 3-kinase and involves its association with the protein product of the c-cbl proto-oncogene. Blood 88: 590–598.PubMedGoogle Scholar
  39. 39.
    Silvennoinen O. Nishigaki H. Kitanaka A, Kumagai M, Ito C, et al. 1996. CD38 signal transduction in human B cell precursors. J. Immunol. 156: 100–107.PubMedGoogle Scholar
  40. 40.
    Kitanaka A. Ito C. Coustan-Smith E and Campana D. 1997. CD38 ligation in human B cell progenitors triggers tyrosine phosphorylation of CD 19 and association of CD 19 with Lyn and phosphatidylinositol 3-kinase. J. Immunol. 159: 184–192.PubMedGoogle Scholar
  41. 41.
    Zupo S. Rugari E. Dono M. Taborelli G, Malavasi F and Ferrarini M. 1994. CD38 signaling by agonistic monoclonal antibody prevents apoptosis of human germinal center B cells. Eur. J. Immunol. 24: 1218–1222.PubMedCrossRefGoogle Scholar
  42. 42.
    Funaro A, Morra M, Calosso L, Zini MG, Ausiello CM and Malavasi F. 1997. Role of the human CD38 molecule in B cell activation and proliferation. Tissue Antigens 49: 7–15.PubMedCrossRefGoogle Scholar
  43. 43.
    Ausiello CM, Urbani F. la Sala F, Funaro A and Malavasi F. 1995. CD38 ligation induces discrete cytokine mRNA expression in human cultured lymphocytes. Eur. J. Immunol. 25: 1477–1480.PubMedCrossRefGoogle Scholar
  44. 44.
    Morra M. Zubiaur M, Terhorst C, Sancho J and Malavasi F. 1998. CD38 is functionally dependent on the TCR/CD3 complex in human T cells. FASEB J. 12: 581–592.PubMedGoogle Scholar
  45. 45.
    Zubiaur M. Guirado M. Terhorst C. Malavasi F and Sancho J. 1999. The CD3-gamma delta epsilon transducing module mediates CD38-induced protein-tyrosine kinase and mitogen-activated protein kinase activation in Jurkat T cells. J. Biol. Chem. 274: 20633–20642.PubMedCrossRefGoogle Scholar
  46. 46.
    Konopleva M. Estrov Z. Zhao S. Andreeff M and Mehta K. 1998. Ligation of cell surface CD38 protein with agonistic monoclonal antibody induces a cell growth signal in myeloid leukemia cells. J. Immunol. 161: 4702–4708.PubMedGoogle Scholar
  47. 47.
    Todisco E, Suzuki T, Srivannaboon K. Coustan-Smith E, Raimondi SC, et al. 1999. CD38 ligation inhibits normal and leukemic myelopoiesis. Blood 95: 535–542.Google Scholar
  48. 48.
    Ausiello CM, la Sala A, Ramoni C, Urbani F, Funaro A and Malavasi F. 1996. Secretion of I FN -γ. IL-6, granulocyte-macrophage colony-stimulating factor and IL-10 cytokines after activation of human purified T lymphocytes upon CD38 ligation. Cell. Immunol. 173: 192–197.PubMedCrossRefGoogle Scholar
  49. 49.
    Zubiaur M, Izquierdo M. Terhorst C, Malavasi F and Sancho J. 1997. CD38 ligation results in activation of the Raf-1 /mitogen-activated protein kinase and the CD3-ζ/ζ- sassociated protein-70 signaling pathways in Jurkat T lymphocytes. J. Immunol. 159: 193–205.PubMedGoogle Scholar
  50. 50.
    Zubiaur M, Fernandez O, Ferrero E, Salmeron J, Malissen B, et al. 2002. CD38 is associated with lipid rafts and upon receptor stimulation leads to Akt/Protein Kinase B and erk activation in the absence of the CD3-ζ immune receptor tyrosine-based activation motifs. J. Biol. Chem. 277: 13–22.PubMedCrossRefGoogle Scholar
  51. 51.
    Nishina H, Inageda K, Takahashi K, Hoshino S, Ikeda K and Katada T. 1994. Cell surface antigen CD38 identified as ecto-enzyme of NAD glycohydrolase has hyaluronate-binding activity. Biochem. Biophys. Res. Comm. 203: 1318–1323.PubMedCrossRefGoogle Scholar
  52. 52.
    Deaglio S, Dianzani U, Horenstein AL, Fernandez JE, van Kooten C, et al. 1996. Human CD38 ligand: A 120-KDA protein predominantly expressed on endothelial cells. J. Immunol. 156:727–734.PubMedGoogle Scholar
  53. 53.
    Deaglio S, Morra M, Mallone R, Ausiello CM, Prager E, et al. 1998. Human CD38 (ADP-Ribosyl Cyclase) is a counter-receptor of CD31, an Ig superfamily member. J. Immunol. 160:395–402.PubMedGoogle Scholar
  54. 54.
    Garvy BA and Harmsen AG. 1996. The importance of neutrophils in resistance to pneumococcal pneumonia in adult and neonatal mice. Inflammation 20: 499–512.PubMedCrossRefGoogle Scholar
  55. 55.
    Bergeron Y, Ouellet N, Deslauriers A, Simard M, Olivier M and Bergeron MG. 1998. Cytokine kinetics and other host factors in response to pneumococcal pulmonary infection in mice. Infect. Immun. 66: 912–922.PubMedGoogle Scholar
  56. 56.
    Le Y, Oppenheim J and Wang JM. 2001. Pleiotropic roles of formyl peptide receptors. Cytokine and Growth Factor Rev. 12: 91 –105.CrossRefGoogle Scholar
  57. 57.
    Mukaida N. 2000. Interleukin-8: an expanding universe beyond neutrophil chemotaxis and activation. Int. J. Hematol. 72: 391–398.PubMedGoogle Scholar
  58. 58.
    Zeilhofer HU and Schorr W. 2000. Role of interleukin-8 in neutrophil signaling. Curr. Opin. Hematol. 7: 178–182.PubMedCrossRefGoogle Scholar
  59. 59.
    Mukaida N, Harada A and Matsushima K. 1998. Interleukin-8 (IL-8) and monocyte chemotactic and activating factor (MCAF/MCP-1) chemokines essentially involved in inflammatory and immune reactions. Cytokine Growth Factor. Rev. 9: 9–23.PubMedCrossRefGoogle Scholar
  60. 60.
    Khair OA, Davies RJ and Devalia JL. 1996. Bacterial-induced release of inflammatory mediators by bronchial epithelial cells. Eur. Respir. J. 9: 1913–1922.PubMedCrossRefGoogle Scholar
  61. 61.
    Schiffmann E, Corcoran BA and Wahl SM. 1975. N-formylmethionyl peptides as chemoattractants for leucocytes. Proc. Natl. Acad. Sci. USA. 72: 1059–1062.PubMedCrossRefGoogle Scholar
  62. 62.
    Marasco WA, Phan SH, Krutzsch H, Showell HJ, Feltner DE, et al. 1984. Purification and identification of formyl-methionyl-leucyl-phenylalanine as the major peptide neutrophil chemotactic factor produced by Escherichia coli. J. Biol. Chem. 259: 5430–5409.PubMedGoogle Scholar
  63. 63.
    von Tscharner V, Prod'hom B, Baggiolini M and Reuter H. 1986. Ion channels in human neutrophils activated by a rise in free cytosolic calcium concentration. Nature 324: 369–372.CrossRefGoogle Scholar
  64. 64.
    Demaurex N, Monod A, Lew DP and Krause K-H. 1994. Characterization of receptor-mediated and store-regulated Ca2+ influx human neutrophils. Biochem. J. 297: 595–601.PubMedGoogle Scholar
  65. 65.
    Gao J-L, Lee EJ and Murphy PM. 1999. Impaired antibacterial host defense in mice lacking the N-formylpeptide receptor. J. Exp. Med. 189: 657–662.PubMedCrossRefGoogle Scholar
  66. 66.
    Lee HC. 2001. Physiological functions of cyclic ADP-ribose and NAADP as calcium messengers. Annu. Rev. Pharmacol. Toxicol. 41: 317–345.PubMedCrossRefGoogle Scholar
  67. 67.
    Sethi JK, Empson RM, Bailey VC, Potter BVL 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: 16358–16563.PubMedCrossRefGoogle Scholar
  68. 68.
    Abdallah MA, Biellmann JF, Nordstrom B and Branden CI. 1975. The conformation of adenosine diphosphoribose and 8-bromoadenosine diphosphoribose when bound to liver alcohol dehydrogenase. Euro. J. Biochem. 50: 475–481.CrossRefGoogle Scholar
  69. 69.
    Lentsch AB and Ward PA. 2000. Regulation of inflammatory vascular damage. J. Pathol. 190:343–348.PubMedCrossRefGoogle Scholar
  70. 70.
    Pillinger MH and Abramson SB. 1995. The neutrophil in rheumatoid arthritis. Rheumatoid Arthritis 21: 691 –714.Google Scholar
  71. 71.
    Hanson PR. 1995. Role of neutrophils in myocardial ischemia and reperfusion. Circulation 91: 1872–1885.CrossRefGoogle Scholar
  72. 72.
    McColl SR, Staykova MA, Wozniak A, Fordham S, Bruce J and Willenborg DO. 1998. Treatment with anti-granulocyte antibodies inhibits the effector phase of experimental autoimmune encephalomyelitis. J. Immunol 161:6421–6426.PubMedGoogle Scholar
  73. 73.
    Linden A. 2001. Role of interleukin-17 and the neutrophil in asthma. Int. Arch. Allergy Immunol. 126: 179–184.PubMedCrossRefGoogle Scholar
  74. 74.
    Lee HC and Aarhus R. 1991. ADP-ribosyl cyclase: an enzyme that cyclizes NAD+ into a calcium mobilizing metabolite. Cell Regul. 2: 203–209.PubMedGoogle Scholar
  75. 75.
    Kim U-H, Kim J-S, Han MK, Park B-H and Kim H-R. 1993. Purification and characterization of NAD glycohydrolase from rabbit erythrocytes. Arch. Biochem. Biophys. 305: 147–152.PubMedCrossRefGoogle Scholar
  76. 76.
    Kim H, Jacobson EL and Jacobson MK. 1993. Synthesis and degradation of cyclic ADP-ribose by NAD glycohydrolases. Science 261: 1330–1333.PubMedCrossRefGoogle Scholar
  77. 77.
    Nata K, Takamura T, Karasawa T, Kumagai T, Hashioka W, et al. 1997. Human gene encoding CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase): organization, nucleotide sequence and alternative splicing. Gene 186: 285–292.PubMedCrossRefGoogle Scholar
  78. 78.
    Ferrero E and Malavasi F. 1997. Human CD38, a leukocyte receptor and ectoenzyme, is a member of a novel eukaryotic gene family of nicotinamide adenine dinucleotide+-converting enzymes. J. Immunol. 159: 3858–3865.PubMedGoogle Scholar
  79. 79.
    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 the generation and influx of the second messenger cyclic ADP-ribose across membranes. FASEB J. 12: 1507–1520.PubMedGoogle Scholar
  80. 80.
    Galione A and White A. 1994. Ca2+ release induced by cyclic ADP-ribose. Trends in Cell Biol. 4:431–436.CrossRefGoogle Scholar
  81. 81.
    Prentki M, Wollheim CB and Lew PD. 1984. Ca2+ homeostasis in permeabilized human neutrophilsxharacterization of Ca2+ sequestering pools and the action of inositol 1, 4, 5-trisphosphate. J. Biol. Chem. 259: 13777–13782.PubMedGoogle Scholar
  82. 82.
    Alemany R, Meyer zu Herigndorf D, van Koppen CJ and Jakobs KH. 1999. Formyl peptide receptor signaling in HL-60 cells through sphingosine kinase. J. Biol. Chem. 21 A: 3994–3999.CrossRefGoogle Scholar
  83. 83.
    Meszaros L, Bak J and Chu A. 1993. Cyclic ADP-ribose as an endogenous regulator of the non-skeletal type ryanodine receptor Ca2+ channel. Nature 354: 76–78.CrossRefGoogle Scholar
  84. 84.
    Sitsapesan R, McGarry SJ and Williams AJ. 1995. Cyclic ADP-ribose, the ryanodine receptor and Ca2+ release. Trends Pharmacol. Sci. 16: 386–391.PubMedCrossRefGoogle Scholar
  85. 85.
    Meissner G. 1994. Ryanodine receptor/Ca2+ release channels and their regulation by endogenous effectors. Ann. Rev. Physiol. 56: 485–508.CrossRefGoogle Scholar
  86. 86.
    Lee HC. 1993. Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose. J. Biol. Chem. 268: 293–299.PubMedGoogle Scholar
  87. 87.
    Peterson OH and Cancela JM. 1999. New Ca2+-releasing messengers: are they important in the nervous system? Trends Neurosci. 22: 488–494.CrossRefGoogle Scholar
  88. 88.
    Giannini G, Conti A, Mammarella S, Scrobogna M and Sorrentino V. 1995. The ryanodine receptor/calcium channel genes are widely and differentially expressed in murine brain and peripheral tissues. J. Cell Biol. 128: 893–904.PubMedCrossRefGoogle Scholar
  89. 89.
    Galione A, Lee HC and Busa WB. 1991. Ca2+-induced Ca2+release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253: 1143–6.PubMedCrossRefGoogle Scholar
  90. 90.
    Thomas JM, Masgrau R, Churchill GC and Galione A. 2001. Pharmacological characterization of the putative cADP-ribose receptor. Biochem. J. 359: 451–7.PubMedCrossRefGoogle Scholar
  91. 91.
    Bennett DL, Bootman MD, Berridge MJ and Cheek TR. 1998. Ca2+ entry into PC 12 cells initiated by ryanodine receptors or inositol 1,4,5-trisphosphate receptors. Biochem. J. 329: 349–357.PubMedGoogle Scholar
  92. 92.
    Kiselyov KI, Shin DM, Wang Y, Pessah IN, Allen PD and Muallem S. 2000. Gating of store-operated channels by conformational coupling to ryanodine receptors. Mol. Cell 6: 421–431.PubMedCrossRefGoogle Scholar
  93. 93.
    Kiselyov K, Shin DM, Shcheynikov N, Kurosaki T and Muallem S. 2001. Regulation of Ca2+ -release activated Ca2+ current (Icrac) by ryanodine receptors in inositol 1,4,5-trisphosphate-receptor-deficient DT40 cells. Biochem. J. 360: 17–22.PubMedCrossRefGoogle Scholar
  94. 94.
    Guse AH, da Silva CP, Berg I, Skapenko AL, Weber K, et al. 1999. Regulation of calcium signaling in T lymphocytes by the second messenger cyclic ADP-ribose. Nature 398: 70–73PubMedCrossRefGoogle Scholar
  95. 95.
    Montero M, Garcia-Sancho J and Alvarez J. 1994. Phosphorylation down-regulates the store-operated Ca2+ entry pathway of human neutrophils. J. Biol. Chem. 269: 3963–3967.PubMedGoogle Scholar
  96. 96.
    Hauser CJ, Fekete Z, Adams JM, Garced M, Livingston DH and Deitch EA. 2001. PAF-mediated Ca2+ influx in human neutrophils occurs via store-operated mechanisms. J. Leukoc. Biol. 69: 63–68.PubMedGoogle Scholar
  97. 97.
    Nube O, Serrander L, Foyouzi-Youssefi R, Monod A, Lew DP and Krause K-H. 1997. Store-operated Ca2+ influx and stimulation of exocytosis in HL-60 granulocytes. J. Biol. Chem. 272: 28360–28367.CrossRefGoogle Scholar
  98. 98.
    Khalfi F, Gressier B, Dine T, Brunet C, Luyckx M, et al. 1998. Verapamil inhibits elastase release and superoxide anion production in human neutrophils. Biol. Pharm. Bull. 21. 109–112.PubMedCrossRefGoogle Scholar
  99. 99.
    Krause K-H, Pittet D, Volpe P, Pozzan T, Meldolesi J and Lew DP. 1989. Calciosome, a sarcoplasmic reticulum-like organelle involved in intracellular Ca2+-handling by non-muscle cells: Studies in human neutrophils and HL-60 cells. Cell Calcium 10: 351–361.PubMedCrossRefGoogle Scholar
  100. 100.
    Pettit EJ and Fay FS. 1998. Cytosolic free calcium and the cytoskeleton in the control of leukocyte chemotaxis. Physiol. Rev. 78: 949–967.PubMedGoogle Scholar
  101. 101.
    Perraud AL, Fleig A, Dunn CA, Bagley LA, Launay P, et al. 2001. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 411:595–599.CrossRefGoogle Scholar
  102. 102.
    Sano Y, Inamura K, Miyake A, Mochizuki S, Yokoi H, et al. 2001. Immunocyte Ca2+ influx system mediated by LTRPC2. Science 293: 1327–1330.PubMedCrossRefGoogle Scholar
  103. 103.
    Berg I, Potter BVL, Mayr GW and Guse AH. 2000. Nicotinic acid adenine dinucleotide phosphate (NAADP+) is an essential regulator of T-lymphocyte Ca2+ signaling. J. Cell Biol. 150:581–588.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  1. 1.Trudeau InstituteSaranac LakeUSA

Personalised recommendations