Leishmania donovani inhibits macrophage apoptosis and pro-inflammatory response through AKT-mediated regulation of β-catenin and FOXO-1

Cell Death and Differentiation

Volumn 23, Issue 11, 2016, Pages 1815-1826

  Gupta, Purnima ^a   Srivastav, Supriya ^b   Saha, Shriya ^a   Das, Pijush K ^b   Ukil, Anindita ^a  

^a UNIVERSITY OF CALCUTTA   (India)

^b INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; BETA CATENIN; CASPASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR FKHR; TUMOR NECROSIS FACTOR; FOXO1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CELL NUCLEUS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOPLASM; CYTOSOL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; FEMALE; GENETIC TRANSFECTION; IMMUNOMODULATION; IN VIVO STUDY; INFLAMMATION; LEISHMANIA DONOVANI; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PARASITE LOAD; PARASITE SURVIVAL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RAW 264.7 CELL LINE; SPLEEN WEIGHT; UBIQUITINATION; UPREGULATION; VISCERAL LEISHMANIASIS; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; DISEASE MODEL; INTRACELLULAR SPACE; MACROPHAGE; METABOLISM; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; REPRODUCIBILITY;

ANIMALS; APOPTOSIS; BETA CATENIN; CYTOSOL; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FORKHEAD BOX PROTEIN O1; GLYCOGEN SYNTHASE KINASE 3 BETA; IMMUNOMODULATION; INFLAMMATION; INTRACELLULAR SPACE; LEISHMANIA DONOVANI; LEISHMANIASIS, VISCERAL; MACROPHAGES; MICE; MICE, INBRED BALB C; MODELS, BIOLOGICAL; PROTO-ONCOGENE PROTEINS C-AKT; RAW 264.7 CELLS; REPRODUCIBILITY OF RESULTS;

EID: 84988662487     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2016.101     Document Type: Article

References (45)

1. Bhardwaj S, Srivastava N, Sudan R, Saha B. Leishmania interferes with host cell signaling to devise a survival strategy. J Biomed Biotechnol 2010; 2010: 109189.
2. Cecilio P, Perez-Cabezas B, Santarem N, Maciel J, Rodrigues V, Cordeiro da Silva A et al. Deception and manipulation: the arms of Leishmania, a successful parasite. Front Immunol 2014; 5: 480.
3. Zhang Y, Wang X, Yang H, Liu H, Lu Y, Han L et al. Kinase AKT controls innate immune cell development and function. Immunology 2013; 140: 143-152.
4. Neves BM, Silvestre R, Resende M, Ouaissi A, Cunha J, Tavares J et al. Activation of phosphatidylinositol 3-kinase/Akt and impairment of nuclear factor-kappaB: molecular mechanisms behind the arrested maturation/activation state of Leishmania infantum-infected dendritic cells. Am J Pathol 2010; 177: 2898-2911.
5. Ruhland A, Leal N, Kima PE. Leishmania promastigotes activate PI3K/Akt signalling to confer host cell resistance to apoptosis. Cell Microbiol 2007; 9: 84-96.
6. Faherty CS, Maurelli AT. Staying alive: bacterial inhibition of apoptosis during infection. Trends Microbiol 2008; 16: 173-180.
7. Chuenkova MV, PereiraPerrin M. Trypanosoma cruzi targets Akt in host cells as an intracellular antiapoptotic strategy. Sci Signal 2009; 2: ra74.
8. Thi EP, Lambertz U, Reiner NE. Sleeping with the enemy: how intracellular pathogens cope with a macrophage lifestyle. PLoS Pathog 2012; 8: e1002551.
9. Antoniv TT, Ivashkiv LB. Interleukin-10-induced gene expression and suppressive function are selectively modulated by the PI3K-Akt-GSK3 pathway. Immunology 2011; 132: 567-577.
10. Guha M, Mackman N. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J Biol Chem 2002; 277: 32124-32132.
11. Fang D, Hawke D, Zheng Y, Xia Y,Meisenhelder J, Nika H et al. Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity. J Biol Chem 2007; 282: 11221-11229.
12. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995; 378: 785-789.
13. Monick MM, Carter AB, Robeff PK, Flaherty DM, Peterson MW, Hunninghake GW. Lipopolysaccharide activates Akt in human alveolar macrophages resulting in nuclear accumulation and transcriptional activity of beta-catenin. J Immunol 2001; 166: 4713-4720.
14. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT et al. Identification of c-MYC as a target of the APC pathway. Science 1998; 281: 1509-1512.
15. Yuan L, Choi K, Khosla C, Zheng X, Higashikubo R, Chicoine MR et al. Tissue transglutaminase 2 inhibition promotes cell death and chemosensitivity in glioblastomas. Mol Cancer Ther 2005; 4: 1293-1302.
16. Kaga S, Zhan L, Altaf E, Maulik N. Glycogen synthase kinase-3beta/beta-catenin promotes angiogenic and anti-apoptotic signaling through the induction of VEGF, Bcl-2 and survivin expression in rat ischemic preconditioned myocardium. J Mol Cell Cardiol 2006; 40: 138-147.
17. Tzivion G, Dobson M, Ramakrishnan G. FoxO transcription factors; Regulation by AKT and 14-3-3 proteins. Biochim Biophys Acta 2011; 1813: 1938-1945.
18. Wang Y, Zhou Y, Graves DT. FOXO transcription factors: their clinical significance and regulation. Biomed Res Int 2014; 2014: 925350.
19. Fan W, Morinaga H, Kim JJ, Bae E, Spann NJ, Heinz S et al. FoxO1 regulates Tlr4 inflammatory pathway signalling in macrophages. EMBO J 2010; 29: 4223-4236.
20. Seiler F, Hellberg J, Lepper PM, Kamyschnikow A, Herr C, Bischoff M et al. FOXO transcription factors regulate innate immune mechanisms in respiratory epithelial cells. J Immunol 2013; 190: 1603-1613.
21. Duan Y, Liao AP, Kuppireddi S, Ye Z, Ciancio MJ, Sun J. beta-Catenin activity negatively regulates bacteria-induced inflammation. Lab Invest 2007; 87: 613-624.
22. Beurel E, Jope RS. The paradoxical pro- and anti-apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways. Prog Neurobiol 2006; 79: 173-189.
23. Sasaki T, Irie-Sasaki J, Jones RG, Oliveira-dos-Santos AJ, Stanford WL, Bolon B et al. Function of PI3Kgamma in thymocyte development, T cell activation, and neutrophil migration. Science 2000; 287: 1040-1046.
24. Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol 2009; 1: a001651.
25. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 2009; 461: 614-620.
26. Haq S, Michael A, Andreucci M, Bhattacharya K, Dotto P, Walters B et al. Stabilization of beta-catenin by a Wnt-independent mechanism regulates cardiomyocyte growth. Proc Natl Acad Sci USA 2003; 100: 4610-4615.
27. Sakanaka C. Phosphorylation and regulation of beta-catenin by casein kinase I epsilon. J Biochem 2002; 132: 697-703.
28. Kamo N, Ke B, Busuttil RW, Kupiec-Weglinski JW. PTEN-mediated Akt/beta-catenin/Foxo1 signaling regulates innate immune responses in mouse liver ischemia/reperfusion injury. Hepatology 2013; 57: 289-298.
29. Qiang L, Banks AS, Accili D. Uncoupling of acetylation from phosphorylation regulates FoxO1 function independent of its subcellular localization. J Biol Chem 2010; 285: 27396-27401.
30. Vazquez-Lopez R, Argueta-Donohue J, Wilkins-Rodriguez A, Escalona-Montano A, Aguirre-Garcia M, Gutierrez-Kobeh L. Leishmania mexicana amastigotes inhibit p38 and JNK and activate PI3K/AKT: role in the inhibition of apoptosis of dendritic cells. Parasite Immunol 2015; 37: 579-589.
31. Nandan D, Camargo de Oliveira C, Moeenrezakhanlou A, Lopez M, Silverman JM, Subek J et al. Myeloid cell IL-10 production in response to Leishmania involves inactivation of glycogen synthase kinase-3beta downstream of phosphatidylinositol-3 kinase. J Immunol 2012; 188: 367-378.
32. Jacobs KM, Bhave SR, Ferraro DJ, Jaboin JJ, Hallahan DE, Thotala D. GSK-3beta: A Bifunctional Role in Cell Death Pathways. Int J Cell Biol 2012; 2012: 930710.
33. Manning BD, Cantley LC. AKT/PKB signaling: navigating downstream. Cell 2007; 129: 1261-1274.
34. Orr SJ, Burg AR, Chan T, Quigley L, Jones GW, Ford JW et al. LAB/NTAL facilitates fungal/ PAMP-induced IL-12 and IFN-gamma production by repressing beta-catenin activation in dendritic cells. PLoS Pathog 2013; 9: e1003357.
35. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO et al. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 2004; 14: 395-403.
36. Hoogeboom D, Essers MA, Polderman PE, Voets E, Smits LM, Burgering BM. Interaction of FOXO with beta-catenin inhibits beta-catenin/T cell factor activity. J Biol Chem 2008; 283: 9224-9230.
37. Fukao T, Koyasu S. PI3K and negative regulation of TLR signaling. Trends Immunol 2003; 24: 358-363.
38. Gupta P, Giri J, Srivastav S, Chande AG, Mukhopadhyaya R, Das PK et al. Leishmania donovani targets tumor necrosis factor receptor-associated factor (TRAF) 3 for impairing TLR4-mediated host response. FASEB J 2014; 28: 1756-1768.
39. Srivastav S, Kar S, Chande AG, Mukhopadhyaya R, Das PK. Leishmania donovani exploits host deubiquitinating enzyme A20, a negative regulator of TLR signaling, to subvert host immune response. J Immunol 2012; 189: 924-934.
40. Kar S, Ukil A, Sharma G, Das PK. MAPK-directed phosphatases preferentially regulate proand anti-inflammatory cytokines in experimental visceral leishmaniasis: involvement of distinct protein kinase C isoforms. J Leukoc Biol 2010; 88: 9-20.
41. Murray HW, Miralles GD, Stoeckle MY, McDermott DF. Role and effect of IL-2 in experimental visceral leishmaniasis. J Immunol 1993; 151: 929-938.
42. Kuijl C, Savage ND, Marsman M, Tuin AW, Janssen L, Egan DA et al. Intracellular bacterial growth is controlled by a kinase network around PKB/AKT1. Nature 2007; 450: 725-730.
43. He X, Saint-Jeannet JP, Woodgett JR, Varmus HE, Dawid IB. Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature 1995; 374: 617-622.
44. Stambolic V, Woodgett JR. Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation. Biochem J 1994; 303: 701-704.
45. Frescas D, Valenti L, Accili D. Nuclear trapping of the forkhead transcription factor FoxO1 via Sirt-dependent deacetylation promotes expression of glucogenetic genes. J Biol Chem 2005; 280: 20589-20595.