Stimulation of unprimed macrophages with immune complexes triggers a low output of nitric oxide by calcium-dependent neuronal nitric-oxide synthase

Journal of Biological Chemistry

Volumn 287, Issue 7, 2012, Pages 4492-4502

  Huang, Zhi ^a,b   Hoffmann, FuKun W ^a   Fay, Jeffrey D ^a   Hashimoto, Ann C ^a   Chapagain, Moti L ^a   Kaufusi, Pakieli H ^a   Hoffmann, Peter R ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b JINAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINES; ELEVATED LEVEL; ERK ACTIVATION; IMMUNE COMPLEX; LOW LEVEL; MAP KINASE; NITRIC OXIDE SYNTHASES; NITRIC-OXIDE SYNTHASE; PHAGOCYTIC CAPACITY; SELENOPROTEINS; SIGNALING PATHWAYS;

ANTIGEN-ANTIBODY REACTIONS; CALCIUM; NITRIC OXIDE; PHOSPHORYLATION;

MACROPHAGES;

CALCIUM; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FC RECEPTOR; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PROSTAGLANDIN E2; SELENOPROTEIN; SELENOPROTEIN K; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; INTRACELLULAR SIGNALING; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; ANTIGEN-ANTIBODY COMPLEX; ANTIVIRAL AGENTS; CALCIUM; CELL LINE; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; INTERFERON-GAMMA; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PHAGOCYTOSIS; PHOSPHORYLATION; RECEPTORS, IGG;

EID: 84856865418     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.315598     Document Type: Article

References (43)

1. Daëron, M. (1997) Fc receptor biology. Annu. Rev. Immunol. 15, 203-234
2. Nimmerjahn, F., and Ravetch, J. V. (2007) Fc-receptors as regulators of immunity. Adv. Immunol. 96, 179-204 (Pubitemid 350018720)
3. Nimmerjahn, F., and Ravetch, J. V. (2006) Fcg receptors: old friends and new family members. Immunity 24, 19-28 (Pubitemid 43077197)
4. Nimmerjahn, F., Bruhns, P., Horiuchi, K., and Ravetch, J. V. (2005) FcgRIV: a novel FcR with distinct IgG subclass specificity. Immunity 23, 41-51 (Pubitemid 41019656)
5. Waterman, P. M., and Cambier, J. C. (2010) The conundrum of inhibitory signaling by ITAM-containing immunoreceptors: potential molecular mechanisms. FEBS Lett. 584, 4878-4882
6. Mozaffarian, N., Berman, J. W., and Casadevall, A. (1995) Immune complexes increase nitric oxide production by interferon-g- stimulated murine macrophage-like J774.16 cells. J. Leukoc. Biol. 57, 657-662
7. Chesrown, S. E., Monnier, J., Visner, G., and Nick, H. S. (1994) Regulation of inducible nitric oxide synthase mRNA levels by LPS, INF-g, TGF-β, and IL-10 in murine macrophage cell lines and rat peritoneal macrophages. Biochem. Biophys. Res. Commun. 200, 126-134 (Pubitemid 24183583)
8. Paludan, S. R. (2000) Synergistic action of pro-inflammatory agents: cellular and molecular aspects. J. Leukoc. Biol. 67, 18-25
9. Granger, D. L., Hibbs, J. B., Jr., Perfect, J. R., and Durack, D. T. (1988) Specific amino acid (L-arginine) requirement for the microbiostatic activity of murine macrophages. J. Clin. Invest. 81, 1129-1136
10. MacMicking, J., Xie, Q. W., and Nathan, C. (1997) Nitric oxide and macrophage function. Annu. Rev. Immunol. 15, 323-350 (Pubitemid 27169284)
11. Tripathi, P., Kashyap, L., and Singh, V. (2007) The role of nitric oxide in inflammatory reactions. FEMS Immunol. Med. Microbiol. 51, 443-452 (Pubitemid 350076162)
12. Connelly, L., Jacobs, A. T., Palacios-Callender, M., Moncada, S., and Hobbs, A. J. (2003) Macrophage endothelial nitric-oxide synthase autoregulates cellular activation and pro-inflammatory protein expression. J. Biol. Chem. 278, 26480-26487 (Pubitemid 36876789)
13. Nathan, C. (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J. 6, 3051-3064
14. Kasten, T. P., Collin-Osdoby, P., Patel, N., Osdoby, P., Krukowski, M., Misko, T. P., Settle, S. L., Currie, M. G., and Nickols, G. A. (1994) Potentiation of osteoclast bone-resorption activity by inhibition of nitric oxide synthase. Proc. Natl. Acad. Sci. U.S.A. 91, 3569-3573 (Pubitemid 24139471)
15. Mayer, B., and Hemmens, B. (1997) Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem. Sci. 22, 477-481 (Pubitemid 27515914)
16. Bredt, D. S., Hwang, P. M., and Snyder, S. H. (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347, 768-770
17. Mungrue, I. N., and Bredt, D. S. (2004) nNOS at a glance: implications for brain and brawn. J. Cell Sci. 117, 2627-2629 (Pubitemid 38997246)
18. Shaul, P. W. (2002) Regulation of endothelial nitric oxide synthase: location, location, location. Annu. Rev. Physiol. 64, 749-774
19. Schödel, J., Padmapriya, P., Marx, A., Huang, P. L., Ertl, G., and Kuhlencordt, P. J. (2009) Expression of neuronal nitric oxide synthase splice variants in atherosclerotic plaques of apoE knockout mice. Atherosclerosis 206, 383-389
20. Schmidt, H. H., Warner, T. D., Nakane, M., Förstermann, U., and Murad, F. (1992) Regulation and subcellular location of nitrogen oxide synthases in RAW264.7 macrophages. Mol. Pharmacol. 41, 615-624 (Pubitemid 23021446)
21. Verma, S., Hoffmann, F. W., Kumar, M., Huang, Z., Roe, K., Nguyen-Wu, E., Hashimoto, A. S., and Hoffmann, P. R. (2011) Selenoprotein K knockout mice exhibit deficient calcium flux in immune cells and impaired immune responses. J. Immunol. 186, 2127-2137
22. Huang, Z., Hoffmann, F. W., Norton, R. L., Hashimoto, A. C., and Hoffmann, P. R. (2011) Selenoprotein K is a novel target of m-calpain, and cleavage is regulated by Toll-like receptor-induced calpastatin in macrophages. J. Biol. Chem. 286, 34830-34838
23. Jagnandan, D., Sessa, W. C., and Fulton, D. (2005) Intracellular location regulates calcium-calmodulin-dependent activation of organelle-restricted eNOS. Am. J. Physiol. Cell Physiol. 289, C1024-C1033 (Pubitemid 41430168)
24. Miller, L., Alley, E. W., Murphy, W. J., Russell, S. W., and Hunt, J. S. (1996) Progesterone inhibits inducible nitric oxide synthase gene expression and nitric oxide production in murine macrophages. J. Leukoc. Biol. 59, 442-450 (Pubitemid 26135560)
25. Rose, D. M., Winston, B. W., Chan, E. D., Riches, D. W., Gerwins, P., Johnson, G. L., and Henson, P. M. (1997) Fc g receptor cross-linking activates p42, p38, and JNK/SAPK mitogen-activated protein kinases in murine macrophages. Role for p42MAPK in Fcγ receptor-stimulated TNF-αsynthesis. J. Immunol. 158, 3433-3438 (Pubitemid 127484064)
26. Dong, C., Davis, R. J., and Flavell, R. A. (2002) MAP kinases in the immune response. Annu. Rev. Immunol. 20, 55-72 (Pubitemid 34293420)
27. Fernandez-Boyanapalli, R., McPhillips, K. A., Frasch, S. C., Janssen, W. J., Dinauer, M. C., Riches, D. W., Henson, P. M., Byrne, A., and Bratton, D. L. (2010) Impaired phagocytosis of apoptotic cells by macrophages in chronic granulomatous disease is reversed by IFN-γ in a nitric oxide-dependent manner. J. Immunol. 185, 4030-4041
28. Bogdan, C. (2001) Nitric oxide and the immune response. Nat. Immunol. 2, 907-916
29. Fox, S. W., and Chow, J. W. (1998) Nitric oxide synthase expression in bone cells. Bone 23, 1-6 (Pubitemid 28327494)
30. Schwartz, D., Mendonca, M., Schwartz, I., Xia, Y., Satriano, J., Wilson, C. B., and Blantz, R. C. (1997) Inhibition of constitutive nitric oxide synthase (NOS) by nitric oxide generated by inducible NOS after lipopolysaccharide administration provokes renal dysfunction in rats. J. Clin. Invest. 100, 439-448 (Pubitemid 27349092)
31. Chauhan, S. D., Seggara, G., Vo, P. A., Macallister, R. J., Hobbs, A. J., and Ahluwalia, A. (2003) Protection against lipopolysaccharide-induced endothelial dysfunction in resistance and conduit vasculature of iNOS knockout mice. FASEB J. 17, 773-775
32. Nicolin, V., Ponti, C., Narducci, P., Grill, V., Bortul, R., Zweyer, M., Vaccarezza, M., and Zauli, G. (2005) Different levels of the neuronal nitric oxide synthase isoform modulate the rate of osteoclastic differentiation of TIB-71 and CRL-2278 RAW 264.7 murine cell clones. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 286, 945-954 (Pubitemid 41434218)
33. Hecker, M., Walsh, D. T., and Vane, J. R. (1992) J. Cardiovasc. Pharmacol. 20, Suppl. 12, S139-S141
34. Roman, V., Dugas, N., Abadie, A., Amirand, C., Zhao, H., Dugas, B., and Kolb, J. P. (1997) Characterization of a constitutive type III nitric oxide synthase in human U937 monocytic cells. Stimulation by soluble CD23. Immunology 91, 643-648 (Pubitemid 27312350)
35. Lancaster, J. R., Jr. (1997) A tutorial on the diffusibility and reactivity of free nitric oxide. Nitric Oxide 1, 18-30
36. Vaughn, M. W., Kuo, L., and Liao, J. C. (1998) Estimation of nitric oxide production and reaction rates in tissue by use of a mathematical model. Am. J. Physiol. 274, H2163-H2176
37. Tümer, C., Bilgin, H. M., Obay, B. D., Diken, H., Atmaca, M., and Kelle, M. (2007) Effect of nitric oxide on phagocytic activity of lipopolysaccharide-induced macrophages: possible role of exogenous L-arginine. Cell Biol. Int. 31, 565-569 (Pubitemid 46660643)
38. Kim, J., Park, H., Myung-Hyun, J., Han, S. H., Chung, H., Lee, J. S., Park, J. S., and Yoon, M. Y. (2008) The effects of anthrax lethal factor on the macrophage proteome: potential activity on nitric oxide synthases. Arch. Biochem. Biophys. 472, 58-64
39. Young, J. D., Ko, S. S., and Cohn, Z. A. (1984) The increase in intracellular free calcium associated with IgGγ2b/γ1 Fc receptor-ligand interactions. Role in phagocytosis. Proc. Natl. Acad. Sci. U.S.A. 81, 5430-5434 (Pubitemid 14048761)
40. 2+ flux as an initial event in phagocytosis by rat Kupffer cells. Eur. J. Biochem. 131, 539-543
41. Tejle, K., Magnusson, K. E., and Rasmusson, B. (2002) Phagocytosis and phagosome maturation are regulated by calcium in J774 macrophages interacting with unopsonized prey. Biosci. Rep. 22, 529-540 (Pubitemid 36250192)
42. 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
43. Nunes, P., and Demaurex, N. (2010) The role of calcium signaling in phagocytosis. J. Leukoc. Biol. 88, 57-68