Activation of PI3K/Akt signaling has a dominant negative effect on IL-12 production by macrophages infected with Leishmania amazonensis promastigotes

Experimental Parasitology

Volumn 122, Issue 1, 2009, Pages 28-36

  Ruhland, Aaron ^a   Kima, Peter E ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Akt; Cytokines; IL 12; Intracellular parasitism; Leishmania; Parasitic protozoan; PI3K; Protein kinases; Signal transduction

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; GUANINE NUCLEOTIDE BINDING PROTEIN; INTERLEUKIN 12; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PERTUSSIS TOXIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P40; PROTEIN P70; STRESS ACTIVATED PROTEIN KINASE; WORTMANNIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG INHIBITION; ENZYME ACTIVATION; ENZYME INHIBITION; GENE REPRESSION; LEISHMANIA; LEISHMANIASIS; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMASTIGOTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; DENSITOMETRY; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; INTERLEUKIN-12; LEISHMANIA MEXICANA; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPECIFIC PATHOGEN-FREE ORGANISMS;

LEISHMANIA AMAZONENSIS; PROTOZOA;

EID: 64449084586     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2008.12.010     Document Type: Article

References (43)

1. Buxbaum L.U., Uzonna J.E., Goldschmidt M.H., and Scott P. Control of New World cutaneous leishmaniasis is interleukin-12 independent but STAT4 dependent. European Journal of Immunology 32 (2002) 3206-3215
2. Belkaid Y.B., Butcher B., and Sacks D.L. Analysis of cytokine production by inflammatory mouse macrophages at the single-cell level: selective impairment of IL-12 induction in Leishmania-infected cells. European Journal of Immunology 28 (1998) 1389-1400
3. Bennett C.L., Misslitz A., Colledge L., Aebischer T., and Blackburn C. Silent infection of bone marrow-derived dendritic cells by Leishmania mexicana amastigotes. European Journal of Immunology 31 (2001) 876-883
4. Bokoch G.M., and Gilman A.G. Inhibition of receptor-mediated release of arachidonic acid by pertussis toxin. Cell 39 (1984) 301-308
5. Bustin S.A., Benes V., Nolan T., and Pfaffl M.W. Quantitative real-time RT-PCR-a perspective. Journal of Molecular Endocrinology 34 (2005) 597-601
6. Brazil D.P., Yang Z.Z., and Hemmings B.A. Advances in protein kinase B signaling: AKTion on multiple front. Trends in Biochemical Science 29 (2004) 233-242
7. Braun M.C., and Kelsall B.L. Regulation of interleukin-12 production by G-protein-coupled receptors. Microbes and Infection 3 (2001) 99-107
8. Cameron P., McGachy A., Anderson M., Paul A., Coombs G.H., Mottram J.C., Alexander J., and Plevin R. Inhibition of lipopolysaccharide-induced macrophage IL-12 production by Leishmania mexicana amastigotes: the role of cysteine peptidases and the NF-kappaB signaling pathway. Journal of Immunology 173 (2004) 3297-3304
9. Carrera L., Gazzinelli R.T., Badolato R., Hieny S., Muller W., Kuhn R., and Sacks D.L. Leishmania promastigotes selectively inhibit interleukin 12 induction in bone marrow-derived macrophages from susceptible and resistant mice. Journal of Experimental Medicine 183 (1996) 515-526
10. Chen Y.L., Law P.Y., and Loh H.H. Inhibition of PI3K/Akt signaling: an emerging paradigm for targeted cancer therapy. Current Medicinal Chemistry, Anticancer Agents 5 (2005) 575-589
11. Constant S.L., Dong C., Yang D.D., Wysk M., Davis R.J., and Flavell R.A. JNK1 is required for T cell-mediated immunity against Leishmania major infection. Journal of Immunology 165 (2000) 2671-2676
12. D'Andrea A., Aste-Amezaga M., Valiante N.M., Ma X., Kubin M., and Trinchieri G. Interleukin 10 (IL-10) inhibits human lymphocyte interferon γ-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. Journal of Experimental Medicine 178 (1993) 1041-1048
13. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., and Greenberg M.E. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91 (1997) 231-241
14. Deane J.A., and Fruman D.A. Phosphoinositide 3-kinase: diverse roles in immune cell activation. Annual Review of Immunology 22 (2004) 563-598
15. Feng G.J., Goodridge H.S., Harnett M.M., Wei X.Q., Nikolaev A.V., Higson A.P., and Liew F.Y. Extracellular signal-related kinase (ERK) and p38 mitogen-activated protein (MAP) kinases differentially regulate the lipopolysaccharide-mediated induction of inducible nitric oxide synthase and IL-12 in macrophages: Leishmania phosphoglycans subvert macrophage IL-12 production by targeting ERK MAP kinase. Journal of Immunology 163 (1999) 6403-6412
16. Fukao T., and Koyasu S. PI3K and negative regulation of TLR signaling. Trends in Immunology 24 (2003) 358-363
17. Fukao T., Tanabe M., Terauchi Y., Ota T., Matsuda S., Asano T., Kadowaki T., Takeuchi T., and Koyasu S. PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nature Immunology 3 (2002) 875-881
18. He J., Gurunathan S., Iwasaki A., Ash-Shaheed B., and Kelsall B.L. Primary role for Gi protein signaling in the regulation of interleukin 12 production and the induction of T helper cell type 1 responses. Journal of Experimental Medicine 191 (2000) 1605-1610
19. Jones D.E., Elloso M.M., and Scott P. Host susceptibility factors to cutaneous leishmaniasis. Frontiers in Bioscience 3 (1998) D1171-1180
20. Kane M.M., and Mosser D.M. The role of IL-10 in promoting disease progression in leishmaniasis. Journal of Immunology 166 (2001) 1141-1147
21. Kim L., Del Rio L., Butcher B.A., Mogensen T.H., Paludan S.R., Flavell R.A., and Denkers E.Y. P38 MAPK autophosphorylation drives macrophage IL-12 production during intracellular infection. Journal of Immunology 174 (2005) 4178-4184
22. Kuroda S., Nishio M., Sasaki T., Horie Y., Kawahara K., Sasaki M., Natsui M., Matozaki T., Tezuka H., Ohteki T., Förster I., Mak T.W., Nakano T., and Suzuki A. Effective clearance of intracellular Leishmania major in vivo requires Pten in macrophages. European Journal of Immunology 38 (2008) 1331-1340
23. Lu H.T., Yang D.D., Wysk M., Gatti E., Mellman I., Davis R.J., and Flavell R.A. Defective IL-12 production in mitogen-activated protein (MAP) kinase kinase 3 (Mkk3)-deficient mice. EMBO Journal 18 (1999) 1845-1857
24. la Sala A., Gadina M., and Kelsall B.L. G(i)-protein-dependent inhibition of IL-12 production is mediated by activation of the phosphatidylinositol 3-kinase-protein 3 kinase B/Akt pathway and JNK. Journal of Immunology 175 (2005) 2994-2999
25. Ma X., and Trinchieri G. Regulation of interleukin-12 production in antigen-presenting cells. Advances in Immunology 79 (2001) 55-92
26. Martin M., Schifferle R.E., Cuesta N., Vogel S.N., Katz J., and Michalek S.M. Role of the phosphatidylinositol 3 kinase-Akt pathway in the regulation of IL-10 and IL-12 by Porphyromonas gingivalis lipopolysaccharide. Journal of Immunology 171 (2003) 717-725
27. Marth T., and Kelsall B.L. Regulation of interleukin-12 by complement receptor 3 signaling. Journal of Experimental Medicine 185 (1997) 1987-1995
28. Mason N.J., Fiore J., Kobayashi T., Masek K.S., Choi Y., and Hunter C.A. TRAF6-dependent mitogen-activated protein kinase activation differentially regulates the production of interleukin-12 by macrophages in response to Toxoplasma gondii. Infection and Immunity 72 (2004) 5662-5667
29. Mattner F., Di Padova K., and Alber G. Interleukin-12 is indispensable for protective immunity against Leishmania major. Infection and Immunity 65 (1997) 4378-4383
30. McDowell M.A., Marovich M., Lira R., Braun M., and Sacks D. Leishmania priming of human dendritic cells for CD40 ligand-induced interleukin-12p70 secretion is strain and species dependent. Infection and Immunity 70 (2002) 3994-4001
31. McMahon-Pratt D., and Alexander J. Does the Leishmania major paradigm of pathogenesis and protection hold for New World cutaneous leishmaniases or the visceral disease?. Immunology Reviews 201 (2004) 206-224
32. kip1. Nature 404 (2000) 782-787
33. Murphy T.L., Cleveland M.G., Kulesza P., Magram J., and Murphy K.M. Regulation of interleukin 12 p40 expression through an NF-kappa B half-site. Molecular and Cellular Biology 15 (1995) 5258-5267
34. Piedrafita D., Proudfoot L., Nikolaev A.V., Xu D., Sands W., Feng G.J., Thomas E., Brewer J., Ferguson M.A., Alexander J., and Liew F.Y. Regulation of macrophage IL-12 synthesis by Leishmania phosphoglycans. European Journal of Immunology 29 (1999) 235-244
35. Reiner S.L., Zheng S., Wang Z.E., Stowring L., and Locksley R.M. Leishmania promastigotes evade interleukin 12 (IL-12) induction by macrophages and stimulate a broad range of cytokines from CD4+ T cells during initiation of infection. Journal of Experimental Medicine 179 (1994) 447-456
36. Reiner SL., and Locksley R.M. The Regulation of immunity to Leishmania major. Annual Review of Immunology 13 (1995) 151-177
37. Ruhland A.M., Leal N., and Kima P.E. Leishmania promastigotes activate PI3K/Akt signaling to confer host cell resistance to apoptosis. Cellular Microbiology 9 (2007) 84-96
38. Soong L., Xu J.C., Grewal I.S., Kima P., Sun J., Longley Jr. B.J., Ruddle N.H., McMahon-Pratt D., and Flavell R.A. Disruption of CD40-CD40 ligand interactions results in an enhanced susceptibility to Leishmania amazonensis infection. Immunity 4 (1996) 263-273
39. Thomas B.N., and Buxbaum L.U. FcgammaRIII mediates immunoglobulin G-induced interleukin-10 and is required for chronic Leishmania mexicana lesions. Infection and Immunity 76 (2008) 623-631
40. Torrentera A.F., Laman J.D., Van Meurs M., Adorini L., Muraille E., and Carlier Y. Endogenous interleukin-12 is critical for controlling the late but not the early stage of Leishmania mexicana infection in C57BL/6 mice. Infection and Immunity 70 (2002) 5075-5080
41. Trinchieri G., and Scott P. Interleukin-12: basic principles and clinical applications. Current Topics in Microbiology and Immunology 238 (1999) 57-78
42. Waggoner S.N., Cruise M.W., Kassel R., and Hahn Y.S. GC1q receptor ligation selectively down-regulates human IL-12 production through activation of the phosphoinositide 3-kinase pathway. Journal of Immunology 175 (2005) 4706-4714
43. Yang C.S., Song C.H., Lee J.S., Jung S.B., Oh J.H., Park J., Kim H.J., Park J.K., Paik T.H., and Jo E.K. 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 8 (2006) 1158-1171