The role of CD38 in Fcγ receptor (FcγR)-mediated phagocytosis in murine macrophages

Journal of Biological Chemistry

Volumn 287, Issue 18, 2012, Pages 14502-14514

  Kang, John ^a   Park, Kwang Hyun ^a,c   Kim, Jwa Jin ^b   Jo, Eun Kyeong ^b   Han, Myung Kwan ^a   Kim, Uh Hyun ^a  

^a Chonbuk National University Medical School   (South Korea)

^b Chungnam National University   (South Korea)

^c Nambu University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BLEBBISTATIN; CYCLASES; EX-VIVO; EXTRACELLULAR; IMMUNE SYSTEMS; IN-VIVO; INTRACELLULAR CA; LONG LASTING; MURINE MACROPHAGES; MYCOBACTERIUM BOVIS; PHAGOSOMES; PRE-TREATMENT; RYANODINE; SECOND MESSENGER;

ANTIGEN-ANTIBODY REACTIONS; ENZYME ACTIVITY; MACROPHAGES; MAMMALS;

CALCIUM;

BLEBBISTATIN; CALCIUM ION; CD38 ANTIGEN; CYCLIC ADENOSINE DIPHOSPHATE RIBOSE; FC RECEPTOR; IMMUNOGLOBULIN G; NICOTINIC ACID ADENINE DINUCLEOTIDE PHOSPHATE; RYANODINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EX VIVO STUDY; EXTRACELLULAR CALCIUM; HOST RESISTANCE; IN VIVO STUDY; INTERNALIZATION; MACROPHAGE; MOUSE; MYCOBACTERIUM BOVIS; NONHUMAN; OPSONIZATION; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, CD38; CALCIUM; CALCIUM SIGNALING; CELL LINE; CYCLIC ADP-RIBOSE; MACROPHAGES, PERITONEAL; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MYCOBACTERIUM BOVIS; PHAGOCYTOSIS; RECEPTORS, IGG;

MURINAE; MUS; MYCOBACTERIUM BOVIS BCG;

EID: 84860364617     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.329003     Document Type: Article

References (88)

1. 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 (Pubitemid 24035045)
2. Lund, F., Solvason, N., Grimaldi, J. C., Parkhouse, R. M., and Howard, M. (1995) Murine CD38. An immunoregulatory ectoenzyme. Immunol. Today 16, 469-473
3. 2+-mobilizing activity. J. Biol. Chem. 264, 1608-1615
4. + into a calcium-mobilizing metabolite. Cell Regul. 2, 203-209
5. 2+ release in sea urchin egg homogenates. Modulation by cyclic ADP-ribose. Science 253, 1143-1146
6. 2+ influx. Arterioscler. Thromb. Vasc. Biol. 30, 575-581
7. Zabrenetzky, V., and Gallin, E. K. (1988) Inositol 1,4,5-trisphosphate concentrations increase after adherence in the macrophage-like cell line J774.1. Biochem. J. 255, 1037-1043 (Pubitemid 18263969)
8. Milara, J., Mata, M., Mauricio, M. D., Donet, E., Morcillo, E. J., and Cortijo, J. (2009) Sphingosine 1-phosphate increases human alveolar epithelial IL-8 secretion, proliferation, and neutrophil chemotaxis. Eur. J. Pharmacol. 609, 132-139
9. 2+ signaling in interleukin-8-treated lymphokine- activated killer cells. J. Biol. Chem. 285, 21877-21887
10. 2+ trigger. Sci. Signal. 1, re10
11. 2+ from a thapsigargin-insensitive pool. Biochem. J. 315, 721-725
12. Calcraft, P. J., Ruas, M., Pan, Z., Cheng, X., Arredouani, A., Hao, X., Tang, J., Rietdorf, K., Teboul, L., Chuang, K. T., Lin, P., Xiao, R., Wang, C., Zhu, Y., Lin, Y., Wyatt, C. N., Parrington, J., Ma, J., Evans, A. M., Galione, A., and Zhu, M. X. (2009) NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459, 596-600
13. 2+ mobilization from acidic organelles triggered by NAADP. FEBS Lett. 584, 1966-1974
14. 2+ from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell 111, 703-708
15. 2+ from acidic stores. Biochem. Soc. Trans. 34, 922-926
16. 2+ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci. Signal. 4, ra31
17. De Flora, A., Franco, L., Guida, L., Bruzzone, S., Usai, C., and Zocchi, E. (2000) Topology of CD38. Chem. Immunol. 75, 79-98 (Pubitemid 30088770)
18. +/cyclic ADP-ribose transport. J. Biol. Chem. 286, 44480-44490
19. Orciani, M., Cavaletti, G., Fino, V., Mattioli-Belmonte, M., Tredici, G., Bruni, P., and Di Primio, R. (2008) Exploiting CD38-mediated endocytosis for immunoliposome internalization. Anticancer Drugs. 19, 599-605
20. Trubiani, O., Guarnieri, S., Orciani, M., Salvolini, E., and Di Primio, R. (2004) Sphingolipid microdomains mediate CD38 internalization. Topography of the endocytosis. Int. J. Immunopathol. Pharmacol. 17, 293-300 (Pubitemid 39481672)
21. Funaro, A., Reinis, M., Trubiani, O., Santi, S., Di Primio, R., and Malavasi, F. (1998) CD38 functions are regulated through an internalization step. J. Immunol. 160, 2238-2247 (Pubitemid 28119904)
22. + transport across cellmembranes. FASEB J. 13, 273-283
23. +-dependent internalization of the transmembrane glycoprotein CD38 in human Namalwa B cells. FEBS Lett. 396, 327-332
24. Rah, S. Y., Park, K. H., Nam, T. S., Kim, S. J., Kim, H., Im, M. J., and Kim, U. H. (2007) Association of CD38 with nonmuscle myosin heavy chain IIA and Lck is essential for the internalization and activation of CD38. J. Biol. Chem. 282, 5653-5660 (Pubitemid 47093780)
25. Niedergang, F., and Chavrier, P. (2004) Signaling and membrane dynamics during phagocytosis. Many roads lead to the phagos(R)ome. Curr. Op. Cell Biol. 16, 422-428 (Pubitemid 38903149)
26. Song, E. K., Lee, Y. R., Yu, H. N., Kim, U. H., Rah, S. Y., Park, K. H., Shim, I. K., Lee, S. J., Park, Y. M., Chung, W. G., Kim, J. S., and Han, M. K. (2008) Extracellular NAD is a regulator for FcγR-mediated phagocytosis in murine macrophages. Biochem. Biophys. Res. Commun. 367, 156-161
27. Goldstein, I. M., Horn, J. K., Kaplan, H. B., and Weissmann, G. (1974) Calcium-induced lysozyme secretion from human polymorphonuclear leukocytes. Biochem. Biophys. Res. Commun. 60, 807-812
28. Lew, P. D., Monod, A., Waldvogel, F. A., Dewald, B., Baggiolini, M., and Pozzan, T. (1986) Quantitative analysis of the cytosolic free calcium dependency of exocytosis from three subcellular compartments in intact human neutrophils. J. Cell Biol. 102, 2197-2204 (Pubitemid 16052159)
29. Valerius, N. H., Stendahl, O., Hartwig, J. H., and Stossel, T. P. (1981) Distribution of actin-binding protein and myosin in polymorphonuclear leukocytes during locomotion and phagocytosis. Cell 24, 195-202 (Pubitemid 11157144)
30. 2+-dependent regulatory protein of actin gel-sol transformation, and its intracellular distribution in a variety of cells and tissues. J. Cell Biol. 91, 901-906
31. Bengtsson, T., Jaconi, M. E., Gustafson, M., Magnusson, K. E., Theler, J. M., Lew, D. P., and Stendahl, O. (1993) Actin dynamics in human neutrophils during adhesion and phagocytosis is controlled by changes in intracellular free calcium. Eur. J. Cell Biol. 62, 49-58 (Pubitemid 23324678)
32. Jaconi, M. E., Lew, D. P., Carpentier, J. L., Magnusson, K. E., Sjögren, M., and Stendahl, O. (1990) Cytosolic free calcium elevation mediates the phagosome-lysosome fusion during phagocytosis in human neutrophils. J. Cell Biol. 110, 1555-1564 (Pubitemid 20169492)
33. Albert, R. K., Embree, L. J., McFeely, J. E., and Hickstein, D. D. (1992) Expression and function of β2 integrins on alveolar macrophages from human and nonhuman primates. Am. J. Respir. Cell Mol. Biol. 7, 182-189
34. Hirsch, C. S., Ellner, J. J., Russell, D. G., and Rich, E. A. (1994) Complement receptor-mediated uptake and tumor necrosis factor-α-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages. J. Immunol. 152, 743-753 (Pubitemid 24072978)
35. Taylor, M. E., and Drickamer, K. (1993) Structural requirements for high affinity binding of complex ligands by the macrophage mannose receptor. J. Biol. Chem. 268, 399-404 (Pubitemid 23021335)
36. Ezekowitz, R. A., Sastry, K., Bailly, P., and Warner, A. (1990) Molecular characterization of the human macrophage mannose receptor. Demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. J. Exp. Med. 172, 1785-1794
37. Downing, J. F., Pasula, R., Wright, J. R., Twigg, H. L., 3rd, and Martin, W. J., 2nd (1995) Surfactant protein a promotes attachment of Mycobacterium tuberculosis to alveolar macrophages during infection with human immunodeficiency virus. Proc. Natl. Acad. Sci. 92, 4848-4852
38. Dunne, D. W., Resnick, D., Greenberg, J., Krieger, M., and Joiner, K. A. (1994) The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid. Proc. Natl, Acad. Sci. U.S.A. 91, 1863-1867 (Pubitemid 24080306)
39. Ravetch, J. V., and Bolland, S. (2001) IgG Fc receptors. Annu. Rev. Immunol. 19, 275-290 (Pubitemid 32368037)
40. 2+ flux as an initial event in phagocytosis by rat Kupffer cells. Eur. J. Biochem. 131, 539-543
41. Young, J. D., Ko, S. S., and Cohn, Z. A. (1984) The increase in intracellular free calcium associated with IgG γ2b/γ1 Fc receptor-ligand interactions. Role in phagocytosis. Proc. Natl. Acad. Sci. 81, 5430-5434 (Pubitemid 14048761)
42. 2+-independent phagocytosis in human neutrophils. Nature 315, 509-511
43. Sawyer, D. W., Sullivan, J. A., and Mandell, G. L. (1985) Intracellular free calcium localization in neutrophils during phagocytosis. Science 230, 663-666 (Pubitemid 16190958)
44. Kusner, D. J., Hall, C. F., and Jackson, S. (1999) Fcγ receptor-mediated activation of phospholipase D regulates macrophage phagocytosis of IgG-opsonized particles. J. Immunol. 162, 2266-2274 (Pubitemid 29288850)
45. Nimmerjahn, F., Bruhns, P., Horiuchi, K., and Ravetch, J. V. (2005) FcγRIV. A novel FcR with distinct IgG subclass specificity. Immunity 23, 41-51 (Pubitemid 41019656)
46. Cooney, D. S., Phee, H., Jacob, A., and Coggeshall, K. M. (2001) Signal transduction by human-restricted Fc γ RIIa involves three distinct cytoplasmic kinase families leading to phagocytosis. J. Immunol. 167, 844-854 (Pubitemid 32660840)
47. Strzelecka-Kiliszek, A., Kwiatkowska, K., and Sobota, A. (2002) Lyn and Syk kinases are sequentially engaged in phagocytosis mediated by FcγR. J. Immunol. 169, 6787-6794 (Pubitemid 36899263)
48. Kiener, P. A., Rankin, B. M., Burkhardt, A. L., Schieven, G. L., Gilliland, L. K., Rowley, R. B., Bolen, J. B., and Ledbetter, J. A. (1993) Cross-linking of Fc γ receptor I (FcγRI) and receptor II (FcγRII) on monocytic cells activates a signal transduction pathway common to both Fc receptors that involves the stimulation of p72 Syk protein-tyrosine kinase. J. Biol. Chem. 268, 24442-24448 (Pubitemid 23335439)
49. Berridge, M. J. (1993) Inositol trisphosphate and calcium signaling. Nature 361, 315-325
50. Graeff, R. M., Walseth, T. F., Fryxell, K., and Branton, W. D., Lee, H. C. (1994) Enzymatic synthesis and characterizations of cyclic GDP-ribose. A procedure for distinguishing enzymes with ADP-ribosyl cyclase activity. J. Biol. Chem. 269, 30260-30267
51. 2+ and membrane potential in lymphocytes. Nature 295, 68-71
52. Desjardins M., Celis J. E., van Meer G., Dieplinger H., Jahraus A., Griffiths G., and Huber L. A. (1994) Molecular characterization of phagosomes. J. Biol. Chem. 269, 32194-32200
53. Shui W., Sheu L., Liu J., Smart B., Petzold C. J., Hsieh T. Y., Pitcher A., Keasling J. D., and Bertozzi C. R. (2008) Membrane proteomics of phagosomes suggests a connection to autophagy. Proc. Natl. Acad. Sci. U.S.A. 105, 16952-16957
54. Graeff, R., and Lee, H. C. (2002) A novel cycling assay for cellular cADP-ribose with nanomolar sensitivity. Biochem. J. 361, 379-384 (Pubitemid 34174505)
55. Graeff, R. M., and Lee, H. C. (2003) High throughput fluorescence-based assays for cyclic ADP-ribose, NAADP, and their metabolic enzymes. Comb. Chem. High Throughput Screen. 6, 367-379 (Pubitemid 36612356)
56. Koval, M., Preiter, K., Adles, C., Stahl, P. D., and Steinberg, T. H. (1998) Size of IgG-opsonized particles determines macrophage response during internalization. Exp. Cell Res. 242, 265-273 (Pubitemid 28366542)
57. 3 receptor, attenuates the positive inotropic effect of α-adrenergic stimulation in guinea pig papillary muscle. Br. J. Pharmacol. 130, 650-654
58. 2+ in heart cells. J. Biol. Chem. 274, 17820-17827
59. 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 (Pubitemid 24250128)
60. 2+ by caffeine and ryanodine induces apoptosis of Chinese hamster ovary cells transfected with ryanodine receptor. J. Biol. Chem. 275, 19978-19984
61. Bowman, E. J., Siebers, A., and Altendorf, K. (1988) Bafilomycins.Aclass of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. 85, 7972-7976
62. Kovács, M., Tóth, J., Hetényi, C., Málnási-Csizmadia A, and Sellers, J. R. (2004) Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 279, 35557-35563 (Pubitemid 39100557)
63. Braun, A., Gessner, J. E., Varga-Szabo, D., Syed, S. N., Konrad, S., Stegner, D., Vögtle, T., Schmidt, R. E., and Nieswandt, B. (2009) STIM1 is essential for Fcγ receptor activation and autoimmune inflammation. Blood 113, 1097-1104
64. Lieberman, L. A., and Higgins, D. E. (2009) A small-molecule screen identifies the antipsychotic drug pimozide as an inhibitor of Listeria monocytogenes infection. Antimicrob. Agents Chemother. 53, 756-764
65. Cuttell, L., Vaughan, A., Silva, E., Escaron, C. J., Lavine, M., Van Goethem, E., Eid, J. P., Quirin, M., and Franc, N. C. (2008) Undertaker, a Drosophila Junctophilin, links Draper-mediated phagocytosis and calcium homeostasis. Cell 135, 524-534
66. Link, T. M., Park, U., Vonakis, B. M., Raben, D. M., Soloski, M. J., and Caterina, M. J. (2010) TRPV2 has a pivotal role in macrophage particle binding and phagocytosis. Nat. Immunol. 11, 232-239
67. Lytton, J., Westlin, M., and Hanley, M. R. (1991) Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J. Biol. Chem. 266, 17067-17071 (Pubitemid 21907906)
68. Blitzer, R. D., Gil, O., Omri, G., and Landau, E. M. (1991) Nifedipine blocks calcium-dependent cholinergic depolarization in the guinea pig hippocampus. Brain Res. 542, 293-299
69. Merritt, J. E., Armstrong, W. P., Benham, C. D., Hallam, T. J., Jacob, R., Jaxa-Chamiec, A., Leigh, B. K., McCarthy, S. A., Moores, K. E., and Rink, T. J. (1990) SK&F 96365, a novel inhibitor of receptor-mediated calcium entry. Biochem. J. 271, 515-522 (Pubitemid 20344770)
70. Churamani, D., Carrey, E. A., Dickinson, G. D., and Patel, S. (2004) Determination of cellular nicotinic acid-adenine dinucleotide phosphate (NAADP) levels. Biochem. J. 380, 449-454 (Pubitemid 38788117)
71. Marks, P. W., and Maxfield, F. R. (1990) Local and global changes in cytosolic-free calcium in neutrophils during chemotaxis and phagocytosis. Cell Calcium. 11, 181-190 (Pubitemid 20095541)
72. Partida-Sánchez, S., Cockayne, D. A., Monard, S., Jacobson, E. L., Oppenheimer, N., Garvy, B., Kusser, K., Goodrich, S., Howard, M., Harmsen, A., Randall, T. D., and Lund, F. E. (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. Nat. Med. 7, 1209-1216 (Pubitemid 33063776)
73. 2+ stores during phagocytosis in human neutrophils. Science 265, 1439-1441
74. Serrander, L., Skarman, P., Rasmussen, B., Witke, W., Lew, D. P., Krause, K. H., Stendahl, O., and Nüsse, O. (2000) Selective inhibition of IgG-mediated phagocytosis in gelsolin-deficient murine neutrophils. J. Immunol. 165, 2451-3457
75. Arora, P. D., Chan, M. W., Anderson, R. A., Janmey, P. A., and McCulloch, C. A. (2005) Separate functions of gelsolin mediate sequential steps of collagen phagocytosis. Mol. Biol. Cell. 16, 5175-5190 (Pubitemid 41566830)
76. Kim, E., Enelow, R. I., Sullivan, G. W., and Mandell, G. L. (1992) Regional and generalized changes in cytosolic-free calcium in monocytes during phagocytosis. Infect. Immun. 60, 1244-1248
77. Elferink, J. G. (1982) Interference of the calcium antagonists verapamil and nifedipine with lysosomal enzyme release from rabbit polymorphonuclear leukocytes. Arzneimittelforschung 32, 1417-1420
78. Dieter, P., Fitzke, E., and Duyster, J. (1993) BAPTA induces a decrease of intracellular-free calcium and a translocation and inactivation of protein kinase C in macrophages. Biol. Chem. Hoppe Seyler 374, 171-174
79. Wilsson, A., Lundqvist, H., Gustafsson, M., and Stendahl, O. (1996) Killing of phagocytosed Staphylococcus aureus by human neutrophils requires intracellular free calcium. J. Leukoc. Biol. 59, 902-907 (Pubitemid 26238487)
80. Matsumura, K., Orita, K., Wakamoto, Y., and Yasuda, K. (2006) Phagocytic response to fully controlled plural stimulation of antigens on macrophage using on-chip microcultivation system. J. Nanobiotechnology 4, 7
81. Muñoz, P., Mittelbrunn, M., de la Fuente, H., Pérez- Martínez, M., García-Pérez, A., Ariza-Veguillas A, Malavasi, F., Zubiaur, M., Sánchez-Madrid, F., and Sancho, J. (2008) Antigen-induced clustering of surface CD38 and recruitment of intracellular CD38 to the immunologic synapse. Blood. 111, 3653-3664
82. Wadsworth, S. J., and Goldfine, H. (1999) Listeria monocytogenes phospholipase C-dependent calcium signaling modulates bacterial entry into J774 macrophage-like cells. Infect. Immun. 67, 1770-1778 (Pubitemid 29144396)
83. Schaff, U. Y., Dixit, N., Procyk, E., Yamayoshi, I., Tse, T., and Simon, S. I. (2010) Orai1 regulates intracellular calcium, arrest, and shape polarization during neutrophil recruitment in shear flow. Blood 115, 657-666
84. McLeish, K. R., Dean, W. L., Wellhausen, S. R., and Stelzer, G. T. (1989) Role of intracellular calcium in priming of human peripheral blood monocytes by bacterial lipopolysaccharide. Inflammation 13, 681-692 (Pubitemid 19283599)
85. Klein, J. B., Payne, V., Schepers, T. M., and McLeish, K. R. (1990) Bacterial lipopolysaccharide enhances polymorphonuclear leukocyte function independent of changes in intracellular calcium. Inflammation 14, 599-611 (Pubitemid 20350859)
86. Rosales, C., and Brown, E. J. (1991) Two mechanisms for IgG Fc receptor-mediated phagocytosis by human neutrophils. J. Immunol. 146, 3937-3944
87. Ichinose, M., Asai, M., and Sawada, M. (1995) β-Endorphin enhances phagocytosis of latex particles in mouse peritoneal macrophages. Scand. J. Immunol. 42, 311-316
88. Ichinose, M., Asai, M., and Sawada, M. (1995) Enhancement of phagocytosis by dynorphinAin mouse peritoneal macrophages. J. Neuroimmunol. 60, 37-43