Neutrophil signaling pathways activated by bacterial DNA stimulation

Journal of Immunology

Volumn 177, Issue 6, 2006, Pages 4037-4046

  Alvarez, María E ^a,b   Bass, Juan I Fuxman ^a,b   Geffner, Jorge R ^a,b   Calotti, Paula X Fernández ^a,b   Costas, Mónica ^d   Coso, Omar A ^c   Gamberale, Romina ^a,b   Vermeulen, Mónica E ^a,b   Salamone, Gabriela ^a,b   Martinez, Diego ^a,b   Tanos, Tamara ^c   Trevani, Analía S ^a,b  

^a ACADEMIA NACIONAL DE MEDICINA   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c INSTITUTO DE FISIOLOGÍA   (Argentina)

^d INSTITUTO DE INVESTIGACIONES MÉDICAS ALFREDO LANARI   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; CD11B ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR AP 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; GENE; HUMAN; HUMAN CELL; IMMUNOMODULATION; LEUKOCYTE ACTIVATION; MALE; MOUSE; MYD88 GENE; NEUTROPHIL; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TLR9 GENE;

EID: 33748478585     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.6.4037     Document Type: Article

References (51)

1. Trevani, A. S., A. Chorny, G. Salamone, M. Vermeulen, R. Gamberale, J. Schettini, S. Raiden, and J. Geffner. 2003. Bacterial DNA activates human neutrophils by a CpG-independent pathway. Eur. J. Immunol. 33: 3164-3174.
2. Yasuda, K., Y. Ogawa, M. Kishimoto, T. Takagi, M. Hashida, and Y. Takakura. 2002. Plasmid DNA activates murine macrophages to induce inflammatory cytokines in a CpG motif-independent manner by complex formation with cationic liposomes. Biochem. Biophys. Res. Commun. 293: 344-348.
3. Zhao, H., H. Hemmi, S. Akira, S. H. Cheng, R. K. Scheule, and N. S. Yew. 2004. Contribution of Toll-like receptor 9 signaling to the acute inflammatory response to nonviral vectors. Mol. Ther. 9: 241-248.
4. Wang, Y., and A. M. Krieg. 2003. Synergy between CpG- or non-CpG DNA and specific antigen for B cell activation. Int. Immunol. 15: 223-231.
5. Elias, F., J. Flo, R. A. Lopez, J. Zorzopulos, A. Montaner, and J. M. Rodriguez. 2003. Strong cytosine-guanosine-independent immunostimulation in humans and other primates by synthetic oligodeoxynucleotides with PyNTTTTGT motifs. J. Immunol. 171: 3697-3704.
6. Parker, L. C., M. K. Whyte, S. K. Dower, and I. Sabroe. 2005. The expression and roles of Toll-like receptors in the biology of the human neutrophil. J. Leukocyte Biol. 77: 886-892.
7. Janssens, S., and R. Beyaert. 2003. Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol. Cell 11: 293-302.
8. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4: 499-511.
9. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5: 987-995.
10. Trevani, A. S., G. Andonegui, M. Giordano, D. H. Lopez, R. Gamberale, F. Minucci, and J. R. Geffner. 1999. Extracellular acidification induces human neutrophil activation. J. Immunol. 162: 4849-4857.
11. Soler-Rodriguez, A. M., H. Zhang, H. S. Lichenstein, N. Qureshi, D. W. Niesel, S. E. Crowe, J. W. Peterson, and G. R. Kumpel. 2000. Neutrophil activation by bacterial lipoprotein versus lipopolysaccharide: differential requirements for serum and CD14. J. Immunol. 164: 2674-2683.
12. Hailman, E., H. S. Lichenstein, M. M. Wurfel, D. S. Miller, D. A. Johnson, M. Kelley, L. A. Busse, M. M. Zukowski, and S. D. Wright. 1994. Lipopolysaccharide (LPS)-binding protein accelerates the binding of LPS to CD14. J. Exp. Mea. 179: 269-277.
13. Costas, M., T. Trapp, M. P. Pereda, J. Sauer, R. Rupprecht, V. E. Nahmod, J. M. Reul, F. Holsboer, and E. Arzt. 1996. Molecular and functional evidence for in vitro cytokine enhancement of human and murine target cell sensitivity to glucocorticoids: TNF-α priming increases glucocorticoid inhibition of TNF-α-induced cytotoxicity/apoptosis. J. Clin. Invest. 98: 1409-1416.
14. Tumpey, T. M., R. Fenton, S. Molesworth-Kenyon, J. E. Oakes, and R. N. Lausch. 2002. Role for macrophage inflammatory protein 2 (MIP-2), MIP-1α, and interleukin-1α in the delayed-type hypersensitivity response to viral antigen. J. Virol. 76: 8050-8057.
15. Suzuki, K., M. Hino, F. Hato, N. Tatsumi, and S. Kitagawa. 1999. Cytokine-specific activation of distinct mitogen-activated protein kinase subtype cascades in human neutrophils stimulated by granulocyte colony-stimulating factor, granulocyte-macrophage colony-stimulating factor, and tumor necrosis factor α. Blood 93: 341-349.
16. Suzuki, K., M. Hino, H. Kutsuna, F. Hato, C. Sakamoto, T. Takahashi, N. Tatsumi, and S. Kitagawa. 2001. Selective activation of p38 mitogen-activated protein kinase cascade in human neutrophils stimulated by IL-1β. J. Immunol. 167: 5940-5947.
17. Nick, J. A., N. J. Avdi, S. K. Young, L. A. Lehman, P. P. McDonald, S. C. Frasch, M. A. Billstrom, P. M. Henson, G. L. Johnson, and G. S. Worthen. 1999. Selective activation and functional significance of p38α mitogen-activated protein kinase in lipopolysaccharide-stimulated neutrophils. J. Clin. Invest. 103: 851-858.
18. Suzuki, K., T. Hasegawa, C. Sakamoto, Y. M. Zhou, F. Hato, M. Hino, N. Tatsumi, and S. Kitagawa. 2001. Cleavage of mitogen-activated protein kinases in human neutrophils undergoing apoptosis: role in decreased responsiveness to inflammatory cytokines. J. Immunol. 166: 1185-1192.
19. Kutsuna, H., K. Suzuki, N. Kamata, T. Kato, F. Hato, K. Mizuno, H. Kobayashi, M. Ishii, and S. Kitagawa. 2004. Actin reorganization and morphological changes in human neutrophils stimulated by TNF, GM-CSF, and G-CSF: the role of MAP kinases. Am. J. Physiol. 286: C55-C64.
20. Huang, Q., J. Yang, Y. Lin, C. Walker, J. Cheng, Z. G. Liu, and B. Su. 2004. Differential regulation of interleukin 1 receptor and Toll-like receptor signaling by MEKK3. Nat. Immunol. 5: 98-103.
21. Arndt, P. G., N. Suzuki, N. J. Avdi, K. C. Malcolm, and G. S. Worthen. 2004. Lipopolysaccharide-induced c-Jun NH2-terminal kinase activation in human neutrophils: role of phosphatidylinositol 3-Kinase and Syk-mediated pathways. J. Biol. Chem. 279: 10883-10891.
22. Hirsch, E., V. L. Katanaev, C. Garlanda, O. Azzolino, L. Pirola, L. Silengo, S. Sozzani, A. Mantovani, F. Altruda, and M. P. Wymann. 2000. Central role for G protein-coupled phosphoinositide 3-kinase γ in inflammation. Science 287: 1049-1053.
23. Capodici, C., S. Hanft, M. Feoktistov, and M. H. Pillinger. 1998. Phosphatidylinositol 3-kinase mediates chemoattractant-stimulated, CD11b/CD18-dependent cell-cell adhesion of human neutrophils: evidence for an ERK-independent pathway. J. Immunol. 160: 1901-1909.
24. Wymann, M. P., S. Sozzani, F. Altruda, A. Mantovani, and E. Hirsch. 2000. Lipids on the move: phosphoinositide 3-kinases in leukocyte function. Immunol. Today 21: 260-264.
25. Fukao, T., and S. Koyasu. 2003. PI3K and negative regulation of TLR signaling. Trends Immunol. 24: 358-363.
26. Guha, M., and N. Mackman. 2002. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J. Biol. Chem. 277: 32124-32132.
27. Strassheim, D., K. Asehnoune, J. S. Park, J. Y. Kim, Q. He, D. Richter, K. Kuhn, S. Mitra, and E. Abraham. 2004. Phosphoinositide 3-kinase and Akt occupy central roles in inflammatory responses of Toll-like receptor 2-stimulated neutrophils. J. Immunol. 172: 5727-5733.
28. Mukaida, N., S. Okamoto, Y. Ishikawa, and K. Matsushima. 1994. Molecular mechanism of interleukin-8 gene expression. J. Leukocyte Biol. 56: 554-558.
29. Hess, J., P. Angel, and M. Schorpp-Kistner. 2004. AP-1 subunits: quarrel and harmony among siblings. J. Cell Sci. 117: 5965-5973.
30. Takeda, K., and S. Akira. 2004. TLR signaling pathways. Semin. Immunol. 16: 3-9.
31. Akazawa, T., H. Masuda, Y. Saeki, M. Matsumoto, K. Takeda, K. Tsujimura, K. Kuzushima, T. Takahashi, I. Azuma, S. Akira, et al. 2004. Adjuvant-mediated tumor regression and tumor-specific cytotoxic response are impaired in MyD88-deficient mice. Cancer Res. 64: 757-764.
32. Takaesu, G., J. Ninomiya-Tsuji, S. Kishida, X. Li, G. R. Stark, and K. Matsumoto. 2001. Interleukin-1 (IL-1) receptor-associated kinase leads to activation of TAK1 by inducing TAB2 translocation in the IL-1 signaling pathway. Mol. Cell. Biol. 21: 2475-2484.
33. high subset of bone marrow derived granulocytes. Int. Immunol. 16: 1675-1683.
34. Witko-Sarsat, V., P. Rieu, B. Descamps-Latscha, P. Lesavre, and L. Halbwachs-Mecarelli. 2000. Neutrophils: molecules, functions and pathophysiological aspects. Lab. Invest. 80: 617-653.
35. Hayashi, F., T. K. Means, and A. D. Luster. 2003. Toll-like receptors stimulate human neutrophil function. Blood 102: 2660-2669.
36. Itou, T., T. Endo, T. Sakai, A. Karlsson, and L. V. Collins. 2005. Immunostimulatory oligodeoxynucleotides induce dolphin neutrophil NADPH-oxidase activation in a CpG-independent but phosphorothioate backbone-dependent manner. Dev. Comp. Immunol. 29: 583-588.
37. Vollmer, J., R. D. Weeratna, M. Jurk, U. Samulowitz, M. J. McCluskie, P. Payette, H. L. Davis, C. Schetter, and A. M. Krieg. 2004. Oligodeoxynucleotides lacking CpG dinucleotides mediate Toll-like receptor 9 dependent T helper type 2 biased immune stimulation. Immunology 113: 212-223.
38. Vollmer, J., A. Janosch, M. Laucht, Z. K. Ballas, C. Schetter, and A. M. Krieg. 2002. Highly immunostimulatory CpG-free oligodeoxynucleotides for activation of human leukocytes. Antisense Nucleic Acid Drug Dev. 12: 165-175.
39. Wang, J., R. Alvarez, G. Roderiquez, E. Guan, Q. Caldwell, J. Wang, M. Phelan, and M. A. Norcross. 2005. CpG-independent synergistic induction of β-chemokines and a dendritic cell phenotype by orthophosphorothioate oligodeoxynucleotides and granulocyte-macrophage colony-stimulating factor in elutriated human primary monocytes. J. Immunol. 174: 6113-6121.
40. Filion, M. C., N. Saha, M. Gueddi, and N. C. Phillips. 2003. Development of short non-CpG phosphodiester oligonucleotides as immune stimulatory agents. Vaccine 21: 983-989.
41. Verthelyi, D., and R. A. Zeuner. 2003. Differential signaling by CpG DNA in DCs and B cells: not just TLR9. Trends Immunol. 24: 519-522.
42. Yasuda, K., P. Yu, C. J. Kirschning, B. Schlatter, F. Schmitz, A. Heit, S. Bauer, H. Hochrein, and H. Wagner. 2005. Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and -independent pathways. J. Immunol. 174: 6129-6136.
43. Tsujimura, H., T. Tamura, H. J. Kong, A. Nishiyama, K. J. Ishii, D. M. Klinman, and K. Ozato. 2004. Toll-like receptor 9 signaling activates NF-κB through IFN regulatory factor-8/IFN consensus sequence binding protein in dendritic cells. J. Immunol. 172: 6820-6827.
44. Takeshita, F., I. Gursel, K. J. Ishii, K. Suzuki, M. Gursel, and D. M. Klinman. 2004. Signal transduction pathways mediated by the interaction of CpG DNA with Toll-like receptor 9. Semin. Immunol. 16: 17-22.
45. Sanchez-Perez, I., S. A. Benitah, M. Martinez-Gomariz, J. C. Lacal, and R. Perona. 2002. Cell stress and MEKK1-mediated c-Jun activation modulate NFκB activity and cell viability. Mol. Biol. Cell 13: 2933-2945.
46. Jozsef, L., T. Khreiss, and J. G. Filep. 2004. CpG motifs in bacterial DNA delay apoptosis of neutrophil granulocytes. FASEB J. 18: 1776-1778.
47. Jozsef, L., T. Khreiss, D. El Kebir, and J. G. Filep. 2006. Activation of TLR-9 induces IL-8 secretion through peroxynitrite signaling in human neutrophils. J. Immunol. 176: 1195-1202.
48. Bylund, J., M. Samuelsson, A. Tarkowski, A. Karlsson, and L. V. Collins. 2002. Immunostimulatory DNA induces degranulation and NADPH-oxidase activation in human neutrophils while concomitantly inhibiting chemotaxis and phagocytosis. Eur. J. Immunol. 32: 2847-2856.
49. Akira, S. 2003. Mammalian Toll-like receptors. Curr. Opin. Immunol. 15: 5-11.
50. Shi, C., X. Zhang, Z. Chen, M. K. Robinson, and D. I. Simon. 2001. Leukocyte integrin Mac-1 recruits toll/interleukin-1 receptor superfamily signaling intermediates to modulate NF-κB activity. Circ. Res. 89: 859-865.
51. Benimetskaya, L., J. D. Loike, Z. Khaled, G. Loike, S. C. Silverstein, L. Cao, J. el Khoury, T. Q. Cai, and C. A. Stein. 1997. Mac-1 (CD11b/CD18) is an oligodeoxynucleotide-binding protein. Nat Med. 3: 414-420.