Leishmania donovani-induced ceramide as the key mediator of Akt dephosphorylation in murine macrophages: Role of protein kinase Cζ and phosphatase

Infection and Immunity

Volumn 75, Issue 5, 2007, Pages 2136-2142

  Dey, Ranadhir ^a   Majumder, Nivedita ^a   Bhattacharjee, Surajit ^a   Majumdar, Suchandra Bhattacharyya ^a   Banerjee, Rajdeep ^b   Ganguly, Sandipan ^b   Das, Pradeep ^b   Majumdar, Subrata ^a  

^a BOSE INSTITUTE   (India)

^b NATIONAL INSTITUTE OF CHOLERA AND ENTERIC DISEASES   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE B; PROTEIN KINASE C; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL MEMBRANE; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DEPHOSPHORYLATION; LEISHMANIA DONOVANI; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR NECROSIS;

ANIMALS; CELLS, CULTURED; CERAMIDES; ENZYME ACTIVATION; FEMALE; LEISHMANIA DONOVANI; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED BALB C; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 34248402756     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01589-06     Document Type: Article

References (43)

1. Alexander, J., R. A. Satoskar, and D. G. Russel. 1999. Leishmania species: models of intracellular parasitism. J. Cell Sci. 112:2993-3002.
2. Andjelkovic, M., R. D. Alessi, R. Meier, A. Fernandez, J. C. Lamb, J. Ned, M. Frech, P. Cron, P. Cohen, M. J. Lucocq, and B. A. Hemmings. 1997. Role of translocation in the activation and function of protein kinase B. J. Biol. Chem. 272:31515-31524.
3. Avota, E., A. Avots, S. Niewiesk, P. L. Kane, U. Bommhardt, V. Meulen, and S. Schneider-Schaulies. 2001. Disruption of Akt kinase activation is important for immunosuppression induced by measles virus. Nat. Med. 7:725-731.
4. Bates, P. A. 1994. The developmental biology of Leishmania promastigotes. Exp. Parasitol. 79:215-218.
5. Bhattacharyya, S., S. Ghosh, P. L. Jhonson, S. Bhattacharya, and S. Majumdar. 2001. Immunomodulatory role of interleukin-10 in visceral leishmaniasis: defective activation of protein kinase C-mediated signal transduction events. Infect. Immun. 69:1499-1507.
6. Bhattacharyya, S., S. Ghosh, P. Sen, S. Roy, and S. Majumdar. 2001. Selective impairment of protein kinase C isotypes in murine macrophage by Leishmania donovani. Mol. Cell. Biochem. 216:47-57.
7. Bourbon, A. N., J. Yun, and M. Kester. 2000. Ceramide directly activates protein kinase Cζ to regulate a stress-activated protein kinase signaling complex. J. Biol. Chem. 275:35617-35623.
8. Bourbon, A. N., L. Sandirasegarane, and M. Kester. 2002. Ceramide-induced inhibition of Akt is mediated through protein kinase Cζ. J. Biol. Chem. 277:3286-3292.
9. Chakraborty, D., S. Banerjee, A. Sen, K. K. Banerjee, P. Das, and S. Roy. 2005. Leishmania donovani affects antigen presentation of macrophage by disrupting lipid rafts. J. Immunol. 175:3214-3224.
10. Chang, K. P., and G. Choudhuri. 1990. Molecular determinates of Leishmania virulence. Annu. Rev. Microbiol. 44:499-529.
11. phox and mediates respiratory burst activity in human neutrophils. J. Immunol. 170:5302-5308.
12. Das, S., S. Bhattacharyya, S. Ghosh, and S. Majumdar. 2000. Signal transduction mechanism in human neutrophil: comparatative study between the z and b-protein kinase isotypes. Mol. Cell. Biochem. 203:143-151.
13. Datta, R. S., A. Brunet, and E. M. Greenberg. 1999. Cellular survival: a play in three Akts. Genes Dev. 13:2905-2927.
14. Dey, R., A. Sarkar, N. Majumder, S. M. Bhattacharyya, K. Roychoudhury, S. Bhttacharyya, S. Roy, and S. Majumdar. 2005. Regulation of impaired protein kinase C signaling by chemokines in murine macrophages during visceral leishmaniasis. Infect. Immun. 73:8334-8344.
15. Doornbos, R. P., M. Thelen, P. C. van der Hoeven, W. J. van Blitterswijk. A. J. Verkleij, and P. M. van Bergen en Henegouwen. 1999. Protein kinase Cζ is a negative regulator of Protein Kinase B activity. J. Biol. Chem. 274:8589-8596.
16. Edwards, J. L., and M. A. Apicella. 2006. Neisseria gonorrhoeae PLD directly interacts with Akt kinase upon infection of primary, human cervical epithelial cells. Cell. Microbiol. 8:1253-1271.
17. Fahey, J. T., K. J. Tracey, P. T. Olson, L. S. Cousens, W. G. Jones, G. T. Shires, and B. Sherry. 1992. Macrophage inflammatory protein 1 modulates macrophage function. J. Immunol. 148:2764-2769.
18. Ghosh, S., S. Bhattacharyya, M. Sirkar, G. S. Sa, T. Das, D. Majumdar, S. Roy, and S. Majumdar. 2002. Leishmania donovani suppresses activated protein 1 and NF-κB in host macrophages via ceramide generation: involvement of extracellular signal-regulated kinase. Infect. Immun. 70:6828-6838.
19. Ghosh, S., S. Bhattacharyya, S. Das, S. Raha, N. Maulik, K. D. Das, S. Roy, and S. Majumdar. 2001. Generation of ceramide in murine macrophages infected with Leishmania donovani alters macrophage signaling events and aids intracellular parasitic survival. Mol. Cell. Biochem. 223:47-60.
20. Guha, M., and N. Mackman. 2001. LPS induction of gene expression in human monocytes. Cell Signal. 13:85-94.
21. Hannun, Y. A. 1996. Functions of ceramide in coordinating cellular response to stress. Science 274:1855-1859.
22. Hannun, Y. A., and L. M. Obeid. 1995. Ceramide: an intracellular signal for apoptosis. Trends Biochem. Sci. 20:73-77.
23. Hart, T. D., K. Vickerman, G. H. Coombs, and A. Quick. 1981. Simple method for purifying L. mexicana amastigotes in large numbers. Parasitology 82:345-355.
24. Kane, L. P., P. G. Andres, K. C. Howland, A. K. Abbas, and A. Weiss. 2001. Akt provides the CD28 co-stimulatory signal for up-regulation of IL-2 and IFN-γ but not Th2 cytokines. Nat. Immunol. 2:37-44.
25. Majumdar, S., M. W. Rossi, T. Fujiki, W. A. Phillips, S. Disn, C. F. Queen, R. B. Jhonston, O. M. Rosen, B. E. Corkey, and H. M. Korchak. 1991. Protein kinase C isotypes and signaling in neutrophils. J. Biol. Chem. 266:9285-9294.
26. Mao, M., X. Fang, U. L. Yiling., R. LaPushin, C. R. Bast, and G. B. Mills. 2000. Inhibition of growth factor induced phosphorylation and activation of protein kinase B/Akt by atypical protein kinase C in breast cancer cells. Biochem. J. 352:475-482.
27. Mathias, S., A. L. Pena, and R. N. Kolesnick. 1998. Signal transduction of stress via ceramide. Biochem. J. 335:465-480.
28. Mellor, H., and P. J. Parker. 1998. The extended protein kinase C superfamily. Biochem. J. 332:281-292.
29. Mookerjee Basu, J., A. Mookerjee, P. Sen, S. Bhaumik, P. Sen, S. Banerjee, K. Naskar, S. K. Choudhury, B. Saha, S. Raha, and S. Roy. 2006. Sodium antimony gluconate induces the generation of reactive oxygen species and nitric oxide via phosphoinositide-3-kinase and mitogen-activated protein kinase activation in Leishmania donovani-infected macrophages. Antimicrob Agents Chemother. 50:1788-1797.
30. Newton, A. C. 1995. Protein kinase C: structure, function and regulation. J. Biol. Chem. 270:28495-28498.
31. Nishizuka, Y. 1995. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J. 9:484-496.
32. Olivier, M., D. J. Gregory, and G. Forget. 2005. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin. Microbiol. Rev. 18:293-305.
33. Powell, J. D., E. Hajduch, G. Kular, and H. S. Hundal. 2003. Ceramide disables 3-phosphoinositide binding to the pleckstrin homology domain of protein kinase B (PKB)/Akt by a PKCζ-dependent mechanism. Mol. Cell. Biol. 23:7794-7808.
34. Russell, D. G., S. Xu, and P. Chakraborty. 1992. Intracellular trafficking and the parasitophorous vacuole of Leishmania mexicana infected macrophages. J. Cell Sci. 103:1193-1210.
35. Saba, J. D., L. M. Obeid, and Y. A. Hannun. 1996. Ceramide: an intracellular mediator of apoptosis and growth suppression. Philos. Trans. R. Soc. London B 351:233-240.
36. Schubert, M. K., P. M. Scheid, and V. Duronio. 2000. Ceramide inhibits protein kinase B/Akt by promoting dephosphorylation of serine 473. J. Biol. Chem. 275:13330-13335.
37. Sengupta, S., P. M. Chilton, and T. C. Mitchell. 2005. Adjuvant-induced survival signaling in clonally expanded T cells is associated with transient increases in pAkt levels and sustained uptake of glucose. Immunobiology 210:647-659.
38. Stratford, S., L. K. Hoehn, F. Liu, and S. A. Summers. 2004. Regulation of insulin action by ceramide, dual mechanisms linking ceramide accumulation to the inhibition of Akt/protein kinase B. J. Biol. Chem. 279:36608-366615.
39. Ugi, S., T. Imamura, H. Maegawa, K. Egawa, T. Yoshizaki, K. Shi, T. Obata, Y. Ebina, A. Kashiwagi, and J. M. Olefsky. 2004. Protein phosphatase 2A negatively regulates insulin's metabolic signaling pathway by inhibiting Akt (protein kinase B) activity in 3T3-L1 adipocytes. Mol. Cell. Biol. 24:8778-8789.
40. van Blitterswijk, W. J., A. H. van der Luit, R. J. Veldman, M. Verhelj, and J. Borst. 2003. Ceramide: second messenger or modulator of membrane structure and dynamics? Biochem. J. 369:199-211.
41. Violin, J. D., and A. C. Newton. 2003. Pathway illuminated: visualising protein kinase C signaling. IUBMB Life 55:653-660.
42. Wang, E., W. P. Norred, C. W. Bacon, R. T. Riley, and A. H. Merril. 1991. Inhibition of sphingolipid biosynthesis by fumonisins: implication for disease associated with Fusarium moniliforme. J. Biol. Chem. 266:14486-14490.
43. Xagorari, A., A. Papapetropoulos, A. Mauromatis, M. Economou, T. Fotsis, and C. Roussos. 2001. Luteolin inhibits an endotoxin-stimulated phosphorylation cascade and proinflammatory cytokine production in macrophages. J. Pharmacol. Exp. Ther. 296:181-187.