Intracellular network of phosphatidylinositol 3-kinase, mammalian target of the rapamycin/70 kDa ribosomal S6 kinase 1, and mitogen-activated protein kinases pathways for regulating mycobacteria-induced IL-23 expression in human macrophages

Cellular Microbiology

Volumn 8, Issue 7, 2006, Pages 1158-1171

  Yang, Chul Su ^a   Song, Chang Hwa ^a   Lee, Ji Sook ^b   Jung, Saet Byel ^a   Oh, Jae Hee ^a   Park, Jongsun ^a   Kim, Hwa Jung ^a   Park, Jeong Kyu ^a   Paik, Tae Hyun ^b   Jo, Eun Kyeong ^a  

^a Chungnam National University   (South Korea)

^b Konyang University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12; INTERLEUKIN 23; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P19; PROTEIN P40; RAPAMYCIN; S6 KINASE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2;

APOPTOSIS; ARTICLE; BACTERIAL INFECTION; CELL CULTURE; CELL ISOLATION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPOSURE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-10; INTERLEUKIN-12; INTERLEUKIN-12 SUBUNIT P40; INTERLEUKIN-23; INTERLEUKIN-23 SUBUNIT P19; INTERLEUKINS; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; MYCOBACTERIUM TUBERCULOSIS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN SUBUNITS; PROTO-ONCOGENE PROTEINS C-AKT; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

CORYNEBACTERINEAE; MAMMALIA; MYCOBACTERIUM TUBERCULOSIS;

EID: 33745013651     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00699.x     Document Type: Article

References (45)

1. Abeliovich, H., Dunn, W. A., Jr, Kim, J., and Klionsky, D. J. (2000) Dissection of autophagosome biogenesis into distinct nucleation and expansion steps. J Cell Biol 151: 1025-1034.
2. Abraham, R. T., and Wiederrecht, G. J. (1996) Immunopharmacology of rapamycin. Annu Rev Immunol 14: 483-510.
3. Agrawal, S., Agrawal, A., Doughty, B., Gerwitz, A., Blenis, J., Van Dyke, T., et al. (2003) Cutting edge: Different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos. J Immunol 171: 4984-4989.
4. Aste-Amezaga, M., Ma, X., Sartori, A., and Trinchieri, G. (1998) Molecular mechanisms of the induction of IL-12 and its inhibition by IL-10. J Immunol 160: 5936-5944.
5. Atkins, M. B., Hidalgo, M., Stadler, W. M., Logan, T. F., Dutcher, J. P., Hudes, G. R., et al. (2004) Randomized phase II study of multiple dose levels of CCI-779, a novel mammalian target of rapamycin kinase inhibitor, in patients with advanced refractory renal cell carcinoma. J Clin Oncol 22: 909-918.
6. Bulut, Y., Michelsen, K. S., Hayrapetian, L., Naiki, Y., Spallek, R., Singh, M., et al. (2005) Mycobacterium tuberculosis heat shock proteins use diverse Toll-like receptor pathways to activate pro-inflammatory signals. J Biol Chem 280: 20961-20967.
7. Burnett, P. E., Barrow, R. K., Cohen, N., Snyder, S. H., and Sabatini, D. M. (1998) RAFT1 phosphorylation of the translational regulators p70, S6 kinase and 4E-BP1. Proc Natl Acad Sci USA 95: 1432 -1437.
8. Chan, E. D., Morris, K. R., Belisle, J. T., Hill, P., Remigio, L. K., Brennan, P. J., et al. (2001) Induction of inducible nitric oxide synthase-NO* by lipoarabinomannan of Mycobacterium tuberculosis is mediated by MEK1-ERK, MKK7-JNK, and NF-kappaB signaling pathways. Infect Immun 69: 2001-2010.
9. Cooper, A. M., Kipnis, A., Turner, J., Magram, J., Ferrante, J., and Orme, I. M. (2002) Mice lacking bioactive IL-12 can generate protective, antigen-specific cellular responses to mycobacterial infection only if the IL-12 p40 subunit is present. J Immunol 168: 1322-1327.
10. Fukao, T., and Koyasu, S. (2003) PI3K and negative regulation of TLR signaling. Trends Immunol 24: 358-363.
11. Fukao, T., Tanabe, M., Terauchi, Y., Ota, T., Matsuda, S., Asano, T., et al. (2002) PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat Immunol 3: 875-881.
12. Goodridge, H. S., Harnett, W., Liew, F. Y., and Harnett, M. M. (2003) Differential regulation of interleukin-12 p40 and p35 induction via Erk mitogen-activated protein kinase-dependent and -independent mechanisms and the implications for bioactive IL-12 and IL-23 responses. Immunology 109: 415-425.
13. Gutierrez, M. G., Master, S. S., Singh, S. B., Taylor, G. A., Colombo, M. I., and Deretic, V. (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119: 753-766.
14. Hickman, S. P., Chan, J., and Salgame, P. (2002) Mycobacterium tuberculosis induces differential cytokine production from dendritic cells and macrophages with divergent effects on naive T cell polarization. J Immunol 168: 4636-4642.
15. Huang, S., and Houghton, P. J. (2003) Targeting mTOR signaling for cancer therapy. Curr Opin Pharmacol 3: 371-317.
16. Into, T., and Shibata, K. (2005) Apoptosis signal-regulating kinase 1-mediated sustained p38 mitogen-activated protein kinase activation regulates mycoplasmal lipoprotein- and staphylococcal peptidoglycan-triggered Toll-like receptor 2 signalling pathways. Cell Microbiol 7: 1305 -1317.
17. Jones, B. W., Means, T. K., Heldwein, K. A., Keen, M. A., Hill, P. J., Belisle, J. T., et al. (2001) Different Toll-like receptor agonists induce distinct macrophage responses. J Leukoc Biol 69: 1036-1044.
18. Jung, S. B., Song, C. H., Yang, C. S., Kim, S. Y., Lee, K. S., Shin, A. R., et al. (2005) Role of the phosphatidylinositol 3-kinase and mitogen-activated protein kinase pathways in the secretion of tumor necrosis factor-alpha and interleukin-10 by the PPD antigen of Mycobacterium tuberculosis. J Clin Immunol 25: 482-490.
19. Kalamidas, S. A., Kondomerkos, D. J., Kotoulas, O. B., and Hann, A. C. (2004) Electron microscopic and biochemical study of the effects of rapamycin on glycogen autophagy in the newborn rat liver. Microsc Res Tech 63: 215-219.
20. Kanazawa, T., Taneike, I., Akaishi, R., Yoshizawa, F., Furuya, N., Fujimura, S., et al. (2004) Amino acids and insulin control autophagic proteolysis through different signaling pathways in relation to mTOR in isolated rat hepatocytes. J Biol Chem 279: 8452-8459.
21. Kim, A. H., Khursigara, G., Sun, X., Franke, T. F., and Chao, M. V. (2001) Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Mol Cell Biol 21: 893-901.
22. Krishnegowda, G., Hajjar, A. M., Zhu, J., Douglass, E. J., Uematsu, S., Akira, S., et al. (2005) Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: Cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J Biol Chem 280: 8606-8616.
23. Kusaba, H., Ghosh, P., Derin, R., Buchholz, M., Sasaki, C., Madara, K., et al. (2005) Interleukin-12-induced interferon-gamma production by human peripheral blood T cells is regulated by mammalian target of rapamycin (mTOR). J Biol Chem 280: 1037-1043.
24. Langrish, C. L., McKenzie, B. S., Wilson, N. J., de Waal Malefyt, R., Kastelein, R. A., and Cua, D. J. (2004) IL-12 and IL-23: Master regulators of innate and adaptive immunity. Immunol Rev 202: 96 -105.
25. Lu, H. T., Yang, D. D., Wysk, M., Gatti, E., Mellman, I., Davis, R. J., et al. (1999) Defective IL-12 production in mitogen-activated protein (MAP) kinase kinase 3 (Mkk3)-deficient mice. EMBO J 18: 1845-1857.
26. Ma, X., and Trinchieri, G. (2001) Regulation of interleukin-12 production in antigen-presenting cells. Adv Immunol 79: 55-92.
27. Maiti, D., Bhattacharyya, A., and Basu, J. (2001) Lipoarabinomannan from Mycobacterium tuberculosis promotes macrophage survival by phosphorylating Bad through a phosphatidylinositol 3-kinase/Akt pathway. J Biol Chem 276: 329-333.
28. Martin, M., Schifferle, R. E., Cuesta, N., Vogel, S. N., Katz, J., and Michalek, S. M. (2003) Role of the phosphatidylinositol 3 kinase-Akt pathway in the regulation of IL-10 and IL-12 by Porphyromonas gingivalis lipopolysaccharide. J Immunol 171: 717-725.
29. Means, T., Wang, S., Lien, E., Yoshimura, A., Golenbock, D., and Fenton, M. (1999) Human toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J Immunol 163: 3920-3927.
30. Monti, P., Mercalli, A., Leone, B. E., Valerio, D. C., Allavena, P., and Piemonti, L. (2003) Rapamycin impairs antigen uptake of human dendritic cells. Transplantation 75: 137-145.
31. Napolitani, G., Rinaldi, A., Bertoni, F., Sallusto, F., and Lanzavecchia, A. (2005) Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat Immunol 6: 769-776.
32. Noda, T., and Ohsumi, Y. (1998) Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 273: 3963-3966.
33. Oppmann, B., Lesley, R., Blom, B., Timans, J. C., Xu, Y., Hunte, B., et al. (2000) Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13: 715-725.
34. Ottenhoff, T. H., Verreck, F. A., Lichtenauer-Kaligis, E. G., Hoeve, M. A., Sanal, O., and van Dissel, J. T. (2002) Genetics, cytokines and human infectious disease: Lessons from weakly pathogenic mycobacteria and salmonellae. Nat Genet 32: 97-105.
35. Ottenhoff, T. H., Verreck, F. A., Hoeve, M. A., and van de Vosse, E. (2005) Control of human host immunity to mycobacteria. Tuberculosis (Edinb) 85: 53-64.
36. Pullen, N., Dennis, P. B., Andjelkovic, M., Dufner, A., Kozma, S. C., Hemmings, B. A., et al. (1998) Phosphorylation and activation of p70s6k by PDK1. Science 279: 707-710.
37. Snijders, A., Hilkens, C. M., van der Pouw Kraan, T. C., Engel, M., Aarden, L. A., and Kapsenberg, M. L. (1996) Regulation of bioactive IL-12 production in lipopolysaccharide-stimulated human monocytes is determined by the expression of the p35 subunit. J Immunol 156: 1207-1212.
38. Song, C. H., Kim, H. J., Park, J. K., Lim, J. H., Kim, U. O., Kim, J. S., et al. (2000) Depressed interleukin-12 (IL-12), but not IL-18, production in response to a 30- or 32-kilodalton mycobacterial antigen in patients with active pulmonary tuberculosis. Infect Immun 68: 4477-4484.
39. Song, C. H., Lee, J. S., Lee, S. H., Lim, K., Kim, H. J., Park, J. K., et al. (2003) Role of mitogen-activated protein kinase pathways in the production of tumor necrosis factor-alpha, interleukin-10, and monocyte chemotactic protein-1 by Mycobacterium tuberculosis H37Rv-infected human monocytes. J Clin Immunol 23: 194-201.
40. Toker, A., and Cantley, L. C. (1997) Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 387: 673 -676.
41. Trinchieri, G. (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3: 133-146.
42. Uthaisangsook, S., Day, N. K., Hitchcock, R., Lerner, A., James-Yarish, M., Good, R. A., et al. (2003) Negative regulation of interleukin-12 production by a rapamycin-sensitive signaling pathway: A brief communication. Exp Biol Med (Maywood) 228: 1023-1027.
43. Verreck, F. A., de Boer, T., Langenberg, D. M., Hoeve, M. A., Kramer, M., Vaisberg, E., et al. (2004) IL-23 producing type-1 macrophages promote whereas IL-10 producing type-2 human macrophages subvert immunity to (myco) bacteria. Proc Natl Acad Sci USA 101: 4560-4565.
44. Wasowska, B. A., Zheng, X. X., Strom, T. B., and Kupieck-Weglinski, J. W. (2001) Adjunctive rapamycin and CsA treatment inhibits monocyte/ macrophage associated cytokines/chemokines in sensitized cardiac graft recipients. Transplantation 71: 1179 -1183.
45. Yang, C. S., Lee, J. S., Jung, S. B., Oh, J. H., Song, C. H., Kim, H. J., et al. (2006) Differential regulation of interleukin-12 and tumor necrosis factor-α by phosphatidylinositol 3-kinase and ERK 1/2 pathways during Mycobacterium tuberculosis Infection. Clin Exp Immunol 143: 150-160.