Critical roles of the p110β subtype of phosphoinositide 3-kinase in lipopolysaccharide-induced Akt activation and negative regulation of nitrite production in RAW 264.7 cells

Journal of Immunology

Volumn 180, Issue 4, 2008, Pages 2054-2061

  Tsukamoto, Ken ^a   Hazeki, Kaoru ^a   Hoshi, Megumi ^a   Nigorikawa, Kiyomi ^a   Inoue, Norimitsu ^b   Sasaki, Takehiko ^c   Hazeki, Osamu ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

^c AKITA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C5A; CYCLOOXYGENASE 2; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 12; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; NITRITE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P110; PROTEIN P110 BETA; SHORT HAIRPIN RNA; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; 1 PHOSPHATIDYLINOSITOL 3 KINASE P110 SUBUNIT, MOUSE; 1-PHOSPHATIDYLINOSITOL 3-KINASE P110 SUBUNIT, MOUSE; ISOENZYME;

ANIMAL CELL; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SYNTHESIS; FEMALE; MACROPHAGE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL LINE; DOWN REGULATION; DRUG ANTAGONISM; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PERITONEUM MACROPHAGE; PHYSIOLOGY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL LINE; DOWN-REGULATION; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION; ISOENZYMES; LIPOPOLYSACCHARIDES; MACROPHAGES; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 42149110310     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.4.2054     Document Type: Article

References (46)

1. Akira, S. 2003. Toll-like receptor signaling. J. Biol. Chem. 278: 38105-38108.
2. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4: 499-511.
3. Yamamoto, M., K. Takeda, and S. Akira. 2004. TIR domain-containing adaptors define the specificity of TLR signaling. Mol. Immunol. 40: 861-868.
4. Oshiumi, H., M. Matsumoto, K. Funami, T. Akazawa, and T. Seya. 2003. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-β induction. Nat. Immunol. 4: 161-167.
5. Yamamoto, M., S. Sato, H. Hemmi, S. Uematsu, K. Hoshino, T. Kaisho, O. Takeuchi, K. Takeda, and S. Akira. 2003. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat. Immunol. 4: 1144-1150.
6. Wymann, M. P., and L. Pirola. 1998. Structure and function of phosphoinositide 3-kinases. Biochim. Biophys. Acta 1436: 127-150.
7. Vanhaesebroeck, B., K. Ali, A. Bilancio, B. Geering, and L. C. Foukas. 2005. Signalling by PI3K isoforms: insights from gene-targeted mice. Trends Biochem. Sci. 30: 194-204.
8. Brachmann, S. M., C. M. Yballe, M. Innocenti, J. A. Deane, D. A. Fruman, S. M. Thomas, and L. C. Cantley. 2005. Role of phosphoinositide 3-kinase regulatory isoforms in development and actin rearrangement. Mol. Cell Biol. 25: 2593-2606.
9. Stephens, L. R., A. Eguinoa, H. Erdjument-Bromage, M. Lui, F. Cooke, J. Coadwell, A. S. Smrcka, M. Thelen, K. Cadwallader, P. Tempst, and P. T. Hawkins. 1997. The G βγ sensitivity of a PI3K is dependent upon a tightly associated adaptor, p101. Cell 89: 105-114.
10. Stoyanov, B., S. Volinia, T. Hanck, I. Rubio, M. Loubtchenkov, D. Malek, S. Stoyanova, B. Vanhaesebroeck, R. Dhand, B. Nurnberg, et al. 1995. Cloning and characterization of a G protein-activated human phosphoinositide-3 kinase. Science 269: 690-693.
11. Maier, U., A. Babich, and B. Nurnberg. 1999. Roles of non-catalytic subunits in Gβγ-induced activation of class I phosphoinositide 3-kinase isoforms β and γ. J. Biol. Chem. 274: 29311-29317.
12. 3 and PI3Kγ in chemoattractant-mediated signal transduction. Science 287: 1046-1049.
13. Hirsch, E., V. L. Katanaev, C. Garlanda, O. Azzolino, L. Pirola, L. Silengo, S. Sozzani, A. Mantovani, F. Altruda, and M. P. Wymann. 2000. Central role for G protein-coupled phosphoinositide 3-kinase γ in inflammation. Science 287: 1049-1053.
14. Bondeva, T., L. Pirola, G. Bulgarelli-Leva, I. Rubio, R. Wetzker, and M. P. Wymann. 1998. Bifurcation of lipid and protein kinase signals of PI3Kγ to the protein kinases PKB and MAPK. Science 282: 293-296.
15. Kurosu, H., T. Maehama, T. Okada, T. Yamamoto, S. Hoshino, Y. Fukui, M. Ui, O. Hazeki, and T. Katada. 1997. Heterodimeric phosphoinositide 3-kinase consisting of p85 and p110β is synergistically activated by the βγ subunits of G proteins and phosphotyrosyl peptide. J. Biol. Chem. 272: 24252-24256.
16. Kubo, H., K. Hazeki, S. Takasuga, and O. Hazeki. 2005. Specific role for p85/ p110β in GTP-binding-protein-mediated activation of Akt. Biochem. J. 392: 607-614.
17. Sasaki, T., J. Irie-Sasaki, R. G. Jones, A. J. Oliveira-dos-Santos, W. L. Stanford, B. Bolon, A. Wakeham, A. Itie, D. Bouchard, I. Kozieradzki, et al. 2000. Function of PI3Kγ in thymocyte development, T cell activation, and neutrophil migration. Science 287: 1040-1046.
18. Hazeki, K., K. Nigorikawa, and O. Hazeki. 2007. Role of phosphoinositide 3-kinase in innate immunity. Biol. Pharm. Bull. 30: 1617-1623.
19. Martin, M., K. Rehani, R. S. Jope, and S. M. Michalek. 2005. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6: 777-784.
20. Woodgett, J. R., and P. S. Ohashi. 2005. GSK3: an in-Toll-erant protein kinase? Nat. Immunol. 6: 751-752.
21. Woodgett, J. R. 2005. Recent advances in the protein kinase B signaling pathway. Curr. Opin. Cell Biol. 17: 150-157.
22. Hazeki, K., S. Kinoshita, T. Matsumura, K. Nigorikawa, H. Kubo, and O. Hazeki. 2006. Opposite effects of wortmannin and 2-(4-morpholinyl)-8-phenyl- 1(4H)-benzopyran-4-one hydrochloride on toll-like receptor-mediated nitric oxide production: negative regulation of nuclear factor-κB by phosphoinositide 3-kinase. Mol. Pharmacol. 69: 1717-1724.
23. Nishiguchi, M., M. Matsumoto, T. Takao, M. Hoshino, Y. Shimonishi, S. Tsuji, N. A. Begum, O. Takeuchi, S. Akira, K. Toyoshima, and T. Seya. 2001. Mycoplasma fermentans lipoprotein M161Ag-induced cell activation is mediated by Toll-like receptor 2: role of N-terminal hydrophobic portion in its multiple functions. J. Immunol. 166: 2610-2616.
24. Kubo-Murai, M., K. Hazeki, N. Sukenobu, K. Yoshikawa, K. Nigorikawa, K. Inoue, T. Yamamoto, M. Matsumoto, T. Seya, N. Inoue, and O. Hazeki. 2007. Protein kinase Cδ binds TIRAP/Mal to participate in TLR signaling. Mol. Immunol. 44: 2257-2264.
25. Fukao, T., and S. Koyasu. 2003. PI3K and negative regulation of TLR signaling. Trends Immunol. 24: 358-363.
26. Fields, T. A., and P. J. Casey. 1997. Signalling functions and biochemical properties of pertussis toxin-resistant G-proteins. Biochem. J. 321(Pt. 3): 561-571.
27. Brennan, M. J., J. L. David, J. G. Kenimer, and C. R. Manclark. 1988. Lectin-like binding of pertussis toxin to a 165-kilodalton Chinese hamster ovary cell glycoprotein. J. Biol. Chem. 263: 4895-4899.
28. Matsuo, T., K. Hazeki, O. Hazeki, T. Katada, and M. Ui. 1996. Activation of phosphatidylinositol 3-kinase by concanavalin A through dual signaling pathways, G-protein-coupled and phosphotyrosine-related, and an essential role of the G-protein-coupled signals for the lectin-induced respiratory burst in human monocytic THP-1 cells. Biochem. J. 315(Pt. 2): 505-512.
29. Kuo, C. C., W. T. Lin, C. M. Liang, and S. M. Liang. 2006. Class I and III phosphatidylinositol 3′-kinase play distinct roles in TLR signaling pathway. J. Immunol. 176: 5943-5949.
30. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801.
31. Vieira, O. V., R. J. Botelho, and S. Grinstein. 2002. Phagosome maturation: aging gracefully. Biochem. J. 366: 689-704.
32. Yum, H. K., J. Arcaroli, J. Kupfner, R. Shenkar, J. M. Penninger, T. Sasaki, K. Y. Yang, J. S. Park, and E. Abraham. 2001. Involvement of phosphoinositide 3-kinases in neutrophil activation and the development of acute lung injury. J. Immunol. 167: 6601-6608.
33. Fukao, T., M. Tanabe, Y. Terauchi, T. Ota, S. Matsuda, T. Asano, T. Kadowaki, T. Takeuchi, and S. Koyasu. 2002. PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat. Immunol. 3: 875-881.
34. Engelman, J. A., J. Luo, and L. C. Cantley. 2006. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7: 606-619.
35. Arbibe, L., J. P. Mira, N. Teusch, L. Kline, M. Guha, N. Mackman, P. J. Godowski, R. J. Ulevitch, and U. G. Knaus. 2000. Toll-like receptor 2-mediated NF-κB activation requires a Rac1-dependent pathway. Nat. Immunol. 1: 533-540.
36. Sarkar, S. N., K. L. Peters, C. P. Elco, S. Sakamoto, S. Pal, and G. C. Sen. 2004. Novel roles of TLR3 tyrosine phosphorylation and PI3 kinase in double-stranded RNA signaling. Nat. Struct. Mol. Biol. 11: 1060-1067.
37. Ojaniemi, M., V. Glumoff, K. Harju, M. Liljeroos, K. Vuori, and M. Hallman. 2003. Phosphatidylinositol 3-kinase is involved in Toll-like receptor 4-mediated cytokine expression in mouse macrophages. Eur. J. Immunol. 33: 597-605.
38. Manna, S. K., and B. B. Aggarwal. 2000. Wortmannin inhibits activation of nuclear transcription factors NF-κB and activated protein-1 induced by lipopolysaccharide and phorbol ester. FEBS Lett. 473: 113-118.
39. Ishii, K. J., F. Takeshita, I. Gursel, M. Gursel, J. Conover, A. Nussenzweig, and D. M. Klinman. 2002. Potential role of phosphatidylinositol 3 kinase, rather than DNA-dependent protein kinase, in CpG DNA-induced immune activation. J. Exp. Med. 196: 269-274.
40. Diaz-Guerra, M. J., A. Castrillo, P. Martin-Sanz, and L. Bosca. 1999. Negative regulation by phosphatidylinositol 3-kinase of inducible nitric oxide synthase expression in macrophages. J. Immunol. 162: 6184-6190.
41. Aksoy, E., W. Vanden Berghe, S. Detienne, Z. Amraoui, K. A. Fitzgerald, G. Haegeman, M. Goldman, and F. Willems. 2005. Inhibition of phosphoinositide 3-kinase enhances TRIF-dependent NF-κB activation and IFN-β synthesis downstream of Toll-like receptor 3 and 4. Eur. J. Immunol. 35: 2200-2209.
42. Davies, S. P., H. Reddy, M. Caivano, and P. Cohen. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351: 95-105.
43. Rhee, S. H., H. Kim, M. P. Moyer, and C. Pothoulakis. 2006. Role of MyD88 in phosphatidylinositol 3-kinase activation by flagellin/toll-like receptor 5 engagement in colonic epithelial cells. J. Biol. Chem. 281: 18560-18568.
44. + T cells and enables CpG oligodeoxynucleotide- mediated costimulation. Immunity 25: 783-793.
45. Neumann, D., S. Lienenklaus, O. Rosati, and M. U. Martin. 2002. IL-1β-induced phosphorylation of PKB/Akt depends on the presence of IRAK-1. Eur. J. Immunol. 32: 3689-3698.
46. Foukas, L. C., M. Claret, W. Pearce, K. Okkenhaug, S. Meek, E. Peskett, S. Sancho, A. J. Smith, D. J. Withers, and B. Vanhaesebroeck. 2006. Critical role for the p110α phosphoinositide-3-OH kinase in growth and metabolic regulation. Nature 441: 366-370.