Infection with Anaplasma phagocytophilum activates the phosphatidylinositol 3-Kinase/Akt and NF-κB survival pathways in neutrophil granulocytes

Infection and Immunity

Volumn 80, Issue 4, 2012, Pages 1615-1623

  Sarkar, Arup ^a   Hellberg, Lars ^a   Bhattacharyya, Asima ^b   Behnen, Martina ^a   Wang, Keqing ^c   Lord, Janet M ^c   Möller, Sonja ^a   Kohler, Maja ^a   Solbach, Werner ^a   Laskay, Tamás ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

^b NATIONAL INSTITUTE OF SCIENCE EDUCATION AND RESEARCH   (India)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN MCL 1; BIRC3 PROTEIN, HUMAN; INHIBITOR OF APOPTOSIS PROTEIN; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PROTEIN BCL 2;

ANAPLASMA PHAGOCYTOPHILUM; ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN GRANULOCYTIC ANAPLASMOSIS; NEUTROPHIL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVAL; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHAGOCYTOSIS; SIGNAL TRANSDUCTION;

ANAPLASMA PHAGOCYTOPHILUM; APOPTOSIS; CELLS, CULTURED; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; INTERLEUKIN-8; NEUTROPHILS; NF-KAPPA B; PHAGOCYTOSIS; PHOSPHATIDYLINOSITOL 3-KINASE; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION;

EID: 84860797888     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05219-11     Document Type: Article

References (54)

1. Aga E, et al. 2002. Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. J. Immunol. 169:898 -905.
2. Aggarwal BB. 2000. Apoptosis and nuclear factor-kappa B: a tale of association and dissociation. Biochem. Pharmacol. 60:1033-1039.
3. Akgul C, Moulding DA, Edwards SW. 2001. Molecular control of neutrophil apoptosis. FEBS Lett. 487:318-322.
4. Akkoyunlu M, Malawista SE, Anguita J, Fikrig E. 2001. Exploitation of interleukin-8-induced neutrophil chemotaxis by the agent of human granulocytic ehrlichiosis. Infect. Immun. 69:5577-5588.
5. Asanovich KM, et al. 1997. Antigenic diversity of granulocytic Ehrlichia isolates from humans in Wisconsin and New York and a horse in California. J. Infect. Dis. 176:1029 -1034.
6. Barkett M, Gilmore TD. 1999. Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 18:6910-6924.
7. Binnicker MJ, Williams RD, Apicella MA. 2004. Gonococcal porin IB activates NF-kappaB in human urethral epithelium and increases the expression of host anti-apoptotic factors. Infect. Immun. 72:6408-6417.
8. Bussmeyer U, et al. 2010. Impairment of gamma interferon signaling in human neutrophils infected with Anaplasma phagocytophilum. Infect. Immun. 78:358 -363.
9. Carlyon JA, Fikrig E. 2003. Invasion and survival strategies of Anaplasma phagocytophilum. Cell. Microbiol. 5:743-754.
10. Choi KS, Park JT, Dumler JS. 2005. Anaplasma phagocytophilum delay of neutrophil apoptosis through the p38 mitogen-activated protein kinase signal pathway. Infect. Immun. 73:8209-8218.
11. Choi KS, Scorpio DG, Dumler JS. 2004. Anaplasma phagocytophilum ligation to toll-like receptor (TLR) 2, but not to TLR4, activates macrophages for nuclear factor-kappa B nuclear translocation. J. Infect. Dis. 189:1921-1925.
12. Cowburn AS, Cadwallader KA, Reed BJ, Farahi N, Chilvers ER. 2002. Role of PI3-kinase-dependent Bad phosphorylation and altered transcription in cytokine-mediated neutrophil survival. Blood 100:2607-2616.
13. Cowburn AS, Deighton J, Walmsley SR, Chilvers ER. 2004. The survival effect of TNF-alpha in human neutrophils is mediated via NF-kappa Bdependent IL-8 release. Eur. J. Immunol. 34:1733-1743.
14. Datta SR, et al. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241.
15. Derouet M, Thomas L, Cross A, Moots RJ, Edwards SW. 2004. Granulocyte macrophage colony-stimulating factor signaling and proteasome inhibition delay neutrophil apoptosis by increasing the stability of Mcl-1. J. Biol. Chem. 279:26915-26921.
16. Dumler JS, Madigan JE, Pusterla N, Bakken JS. 2007. Ehrlichioses in humans: epidemiology, clinical presentation, diagnosis, and treatment. Clin. Infect. Dis. 45(Suppl. 1):S45-S51.
17. Esmann L, et al. 2010. Phagocytosis of apoptotic cells by neutrophil granulocytes: diminished proinflammatory neutrophil functions in the presence of apoptotic cells. J. Immunol. 184:391- 400.
18. Francois S, et al. 2005. Inhibition of neutrophil apoptosis by TLR agonists in whole blood: involvement of the phosphoinositide 3-kinase/Akt and NF-kappaB signaling pathways, leading to increased levels of Mcl-1, A1, and phosphorylated Bad. J. Immunol. 174:3633-3642.
19. Gagnon A, Dods P, Roustan-Delatour N, Chen CS, Sorisky A. 2001. Phosphatidylinositol-3,4,5-trisphosphate is required for insulin-like growth factor 1-mediated survival of 3T3-L1 preadipocytes. Endocrinology 142:205-212.
20. Gainet J, et al. 1998. Interleukin-8 production by polymorphonuclear neutrophils in patients with rapidly progressive periodontitis: an amplifying loop of polymorphonuclear neutrophil activation. Lab. Invest. 78: 755-762.
21. Ge Y, Rikihisa Y. 2006. Anaplasma phagocytophilum delays spontaneous human neutrophil apoptosis by modulation of multiple apoptotic pathways. Cell. Microbiol. 8:1406-1416.
22. Granick JL, Reneer DV, Carlyon JA, Borjesson DL. 2008. Anaplasma phagocytophilum infects cells of the megakaryocytic lineage through sialylated ligands but fails to alter platelet production. J. Med. Microbiol. 57:416-423.
23. Henkel T, et al. 1993. Rapid proteolysis of I kappa B-alpha is necessary for activation of transcription factor NF-kappa B. Nature 365:182-185.
24. Herron MJ, Ericson ME, Kurtti TJ, Munderloh UG. 2005. The interactions of Anaplasma phagocytophilum, endothelial cells, and human neutrophils. Ann. N. Y. Acad. Sci. 1063:374-382.
25. Kettritz R, et al. 1998. Interleukin-8 delays spontaneous and tumor necrosis factor-alpha-mediated apoptosis of human neutrophils. Kidney Int. 53:84 -91.
26. Kilpatrick LE, et al. 2006. Regulation of TNF mediated anti-apoptotic signaling in human neutrophils: role of delta-PKC and ERK1/2. J. Leukoc. Biol. 80:1512-1521.
27. Kim HY, Rikihisa Y. 2002. Roles of p38 mitogen-activated protein kinase, NF-kappaB, and protein kinase C in proinflammatory cytokine mRNA expression by human peripheral blood leukocytes, monocytes, and neutrophils in response to Anaplasma phagocytophila. Infect. Immun. 70: 4132-4141.
28. Klein JB, et al. 2000. Granulocyte-macrophage colony-stimulating factor delays neutrophil constitutive apoptosis through phosphoinositide 3-kinase and extracellular signal-regulated kinase pathways. J. Immunol. 164: 4286-4291.
29. Lee HC, Goodman JL. 2006. Anaplasma phagocytophilum causes global induction of anti-apoptosis in human neutrophils. Genomics 88:496- 503.
30. Lee HC, Kioi M, Han J, Puri RK, Goodman JL. 2008. Anaplasma phagocytophilum-induced gene expression in both human neutrophils and HL-60 cells. Genomics 92:144-151.
31. Lotz S, et al. 2004. Highly purified lipoteichoic acid activates neutrophil granulocytes and delays their spontaneous apoptosis via CD14 and TLR2. J. Leukoc. Biol. 75:467-477.
32. Manning BD, Cantley LC. 2007. AKT/PKB signaling: navigating downstream. Cell 129:1261-1274.
33. Mansell A, Khelef N, Cossart P, O'Neill LA. 2001. Internalin B activates nuclear factor-kappa B via Ras, phosphoinositide 3-kinase, and Akt. J. Biol. Chem. 276:43597-43603.
34. Mishra S, et al. 2005. Distinct role of calmodulin and calmodulindependent protein kinase-II in lipopolysaccharide and tumor necrosis factor-alpha-mediated suppression of apoptosis and anti-apoptotic c-IAP2 gene expression in human monocytic cells. J. Biol. Chem. 280: 37536-37546.
35. Oganesian A, et al. 2003. Protein tyrosine phosphatase RQ is a phosphatidylinositol phosphatase that can regulate cell survival and proliferation. Proc. Natl. Acad. Sci. U. S. A. 100:7563-7568.
36. Ozes ON, et al. 1999. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401:82- 85.
37. Park J, Kim KJ, Grab DJ, Dumler JS. 2003. Anaplasma phagocytophilum major surface protein-2 (Msp2) forms multimeric complexes in the bacterial membrane. FEMS Microbiol. Lett. 227:243-247.
38. Pluskota E, et al. 2008. Expression, activation, and function of integrin alphaMbeta2 (Mac-1) on neutrophil-derived microparticles. Blood 112: 2327-2335.
39. Power CP, et al. 2004. Bacterial lipoprotein delays apoptosis in human neutrophils through inhibition of caspase-3 activity: regulatory roles for CD14 and TLR-2. J. Immunol. 173:5229-5237.
40. Romashkova JA, Makarov SS. 1999. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401:86-90.
41. Roy N, Deveraux QL, Takahashi R, Salvesen GS, Reed JC. 1997. The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J. 16:6914-6925.
42. Scapini P, et al. 2000. The neutrophil as a cellular source of chemokines. Immunol. Rev. 177:195-203.
43. Strassheim D, et al. 2004. Phosphoinositide 3-kinase and Akt occupy central roles in inflammatory responses of Toll-like receptor 2-stimulated neutrophils. J. Immunol. 172:5727-5733.
44. Sukumaran B, Carlyon JA, Cai JL, Berliner N, Fikrig E. 2005. Early transcriptional response of human neutrophils to Anaplasma phagocytophilum infection. Infect. Immun. 73:8089-8099.
45. Thomas V, Fikrig E. 2007. Anaplasma phagocytophilum specifically induces tyrosine phosphorylation of ROCK1 during infection. Cell. Microbiol. 9:1730-1737.
46. Troese MJ, Carlyon JA. 2009. Anaplasma phagocytophilum dense-cored organisms mediate cellular adherence through recognition of human Pselectin glycoprotein ligand 1. Infect. Immun. 77:4018-4027.
47. van Zandbergen G, et al. 2004. Chlamydia pneumoniae multiply in neutrophil granulocytes and delay their spontaneous apoptosis. J. Immunol. 172:1768-1776.
48. Walmsley SR, et al. 2005. Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J. Exp. Med. 201:105-115.
49. Wang K, et al. 2003. Inhibition of neutrophil apoptosis by type 1 IFN depends on cross-talk between phosphoinositol 3-kinase, protein kinase C-delta, and NF-kappa B signaling pathways. J. Immunol. 171:1035-1041.
50. Wang Q, Wang X, Evers BM. 2003. Induction of cIAP-2 in human colon cancer cells through PKC delta/NF-kappa B. J. Biol. Chem. 278:51091-51099.
51. Yanai A, et al. 2003. Helicobacter pylori induces anti apoptosis through nuclear factor-kappaB activation. J. Infect. Dis. 188:1741-1751.
52. Zhang JZ, Sinha M, Luxon BA, Yu XJ. 2004. Survival strategy of obligately intracellular Ehrlichia chaffeensis: novel modulation of immune response and host cell cycles. Infect. Immun. 72:498 -507.
53. Zhou H, Li XM, Meinkoth J, Pittman RN. 2000. Akt regulates cell survival and apoptosis at a postmitochondrial level. J. Cell Biol. 151:483-494.
54. Zhu D, et al. 2006. Deactivation of phosphatidylinositol 3,4,5-trisphosphate/Akt signaling mediates neutrophil spontaneous death. Proc. Natl. Acad. Sci. U. S. A. 103:14836 -14841.