Role of Hsp90 in CpG ODN mediated immunostimulation in avian macrophages

Molecular Immunology

Volumn 47, Issue 6, 2010, Pages 1337-1346

  Bhat, Audesh ^a   Gomis, Susantha ^a   Potter, Andrew ^a,b,c   Tikoo, Suresh K ^a,b,c  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Chicken; CpG oligonucleotide; Cytokines chemokines; HD11 cells; Hsp90; MAPK ERK; PI3K AKT

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; GAMMA INTERFERON; HEAT SHOCK PROTEIN 90; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FOWL; IMMUNOSTIMULATION; MACROPHAGE ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TH1 CELL;

ANIMALS; BLOTTING, WESTERN; CHEMOKINES; CHICKENS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENZYME ACTIVATION; HSP90 HEAT-SHOCK PROTEINS; IMMUNIZATION; MACROPHAGES; MASS SPECTROMETRY; MITOGEN-ACTIVATED PROTEIN KINASE 1; NITRIC OXIDE; OLIGODEOXYRIBONUCLEOTIDES; PHOSPHORYLATION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; SILVER STAINING; UP-REGULATION;

AVES; MAMMALIA;

EID: 76949084946     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2009.12.011     Document Type: Article

References (60)

1. Aderem A., and Ulevitch R.J. Toll-like receptors in the induction of the innate immune response. Nature 406 (2000) 782-787
2. Al-Aoukaty A., Rolstad B., Giaid A., and Maghazachi A.A. MIP-3alpha, MIP-3beta and fractalkine induce the locomotion and the mobilization of intracellular calcium, and activate the heterotrimeric G proteins in human natural killer cells. Immunology 95 (1998) 618-624
3. Bandholtz L., Guo Y., Palmberg C., Mattsson K., Ohlsson B., High A., Shabanowitz L., Hunt D.F., Jornvall H., Wigzell H., Agerberth B., and Gudmundsson G.H. Hsp90 binds CpG oligonucleotides directly: implications for hsp90 as a missing link in CpG signaling and recognition. Cell Mol. Life Sci. 60 (2003) 422-429
4. Basso A.D., Solit D.B., Chiosis G., Giri B., Tsichlis P., and Rosen N. Akt forms an intracellular complex with Heat Shock Protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. J. Biol. Chem. 277 (2002) 39858-39866
5. Beug H., von Kirchbach A., Doderlein G., Conscience J.F., and Graf T. Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell 18 (1979) 375-390
6. Beutler B. Toll-like receptors: how they work and what they do. Curr. Opin. Hematol. 9 (2002) 2-10
7. Binato R., Pizzatti L., and Abdelhay E. Otx2 is a putative candidate to activate mice Msx1 gene from distal enhancer. Biochem. Biophys. Res. Commun. 358 (2007) 655-660
8. Brownlie R., Zhu J., Allan B., Mutwiri G.K., Babiuk L.A., Potter A., and Griebel P. Chicken TLR21 acts as a functional homologue to mammalian TLR9 in the recognition of CpG oligonucleotides. Mol. Immunol. 46 (2009) 3163-317019
9. Buchner J. Hsp90 & Co.-a holding for folding. Trends Biochem. Sci. 24 (1999) 136-141
10. Chen B., Zhong D., and Monteiro A. Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BMC Genom. 7 (2006) 156
11. Dieu-Nosjean M.C., Vicari A., Lebecque S., and Caux C. Regulation of dendritic cell trafficking: a process that involves the participation of selective chemokines. J. Leukoc. Biol. 66 (1999) 252-262
12. Ding A.H., Nathan C.F., and Stuehr D.J. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141 (1988) 2407-2412
13. Fahy O.L., Townley S.L., Coates N.J., Clark-Lewis I., and McColl S.R. Control of Salmonella dissemination in vivo by macrophage inflammatory protein (MIP)-3alpha/CCL20. Lab. Invest. 84 (2004) 1501-1511
14. Gao J.J., Zuvanich E.G., Xue Q., Horn D.L., Silverstein R., and Morrison D.C. Cutting edge: bacterial DNA and LPS act in synergy in inducing nitric oxide production in RAW 264.7 macrophages. J. Immunol. 163 (1999) 4095-4099
15. Ghosh D.K., Misukonis M.A., Reich C., Pisetsky D.S., and Weinberg J.B. Host response to infection: the role of CpG DNA in induction of cyclooxygenase 2 and nitric oxide synthase 2 in murine macrophages. Infect. Immun. 69 (2001) 7703-7710
16. 4+ T cells in the chicken: conservation of a Th1-like system in a nonmammalian species. J. Immunol. 171 (2003) 1809-1815
17. Gomis S., Babiuk L., Godson D.L., Allan B., Thrush T., Townsend H., Wilson P., Waters E., Hecker R., and Potter A. Protection of chickens against Escherichia coli infections by DNA containing CpG motifs. Infect. Immun. 71 (2003) 857-863
18. Hacker H., Vabulas R.M., Takeuchi O., Hoshino K., Akira S., and Wagner H. Immune cell activation by bacterial CpG-DNA through myeloid differentiation marker 88 and tumor necrosis factor receptor-associated factor (TRAF) 6. J. Exp. Med. 192 (2000) 595-600
19. He H., Crippen T.L., Farnell M.B., and Kogut M.H. Identification of CpG oligodeoxynucleotide motifs that stimulate nitric oxide and cytokine production in avian macrophage and peripheral blood mononuclear cells. Dev. Comp. Immunol. 27 (2003) 621-627
20. He H., Genovese K.J., Nisbet D.J., and Kogut M.H. Phospholipase C, phosphatidylinositol 3-kinase, and intracellular [Ca(2+)] mediate the activation of chicken HD11 macrophage cells by CpG oligodeoxynucleotide. Dev. Comp. Immunol. 32 (2008) 1111-1118
21. He H., and Kogut M.H. CpG-ODN-induced nitric oxide production is mediated through clathrin-dependent endocytosis, endosomal maturation, and activation of PKC, MEK1/2 and p38 MAPK, and NF-kappaB pathways in avian macrophage cells (HD11). Cell Signal 15 (2003) 911-917
22. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H., Takeda K., and Akira S. A toll-like receptor recognizes bacterial DNA. Nature 408 (2000) 740-745
23. Ikeda M., Kito H., and Sumpio B.E. Phosphatidylinositol-3 kinase dependent MAP kinase activation via p21ras in endothelial cells exposed to cyclic strain. Biochem. Biophys. Res. Commun. 257 (1999) 668-671
24. Jabbari K., and Bernardi G. Cytosine methylation and CpG, TpG (CpA) and TpA frequencies. Gene 333 (2004) 143-149
25. Jeon Y.K., Park C.H., Kim K.Y., Li Y.C., Kim J., Kim Y.A., Paik J.H., Park B.K., Kim C.W., and Kim Y.N. The heat-shock protein 90 inhibitor, geldanamycin, induces apoptotic cell death in Epstein-Barr virus-positive NK/T-cell lymphoma by Akt down-regulation. J. Pathol. 213 (2007) 170-179
26. Kleinert H., Pautz A., Linker K., and Schwarz P.M. Regulation of the expression of inducible nitric oxide synthase. Eur. J. Pharmacol. 500 (2004) 255-266
27. Kleinert H., Schwarz P.M., and Forstermann U. Regulation of the expression of inducible nitric oxide synthase. Biol. Chem. 384 (2003) 1343-1364
28. Klinman D.M. Immunotherapeutic uses of CpG oligodeoxynucleotides. Nat. Rev. Immunol. 4 (2004) 249-258
29. Klinman D.M., Yi A.K., Beaucage S.L., Conover J., and Krieg A.M. CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 2879-2883
30. Krieg A.M., Yi A.K., Matson S., Waldschmidt T.J., Bishop G.A., Teasdale R., Koretzky G.A., and Klinman D.M. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374 (1995) 546-549
31. Kuo C.C., Liang C.M., Lai C.Y., and Liang S.M. Involvement of heat shock protein (Hsp) 90 beta but not Hsp90 alpha in antiapoptotic effect of CpG-B oligodeoxynucleotide. J. Immunol. 178 (2007) 6100-6108
32. Kuo C.C., Lin W.T., Liang C.M., and Liang S.M. Class I and III phosphatidylinositol 3′-kinase play distinct roles in TLR signaling pathway. J. Immunol. 176 (2006) 5943-5949
33. Lefloch R., Pouyssegur J., and Lenormand P. Single and combined silencing of ERK1 and ERK2 reveals their positive contribution to growth signaling depending on their expression levels. Mol. Cell. Biol. 28 (2008) 511-527
34. Llorens F., Garcia L., Itarte E., and Gomez N. Apigenin and LY294002 prolong EGF-stimulated ERK1/2 activation in PC12 cells but are unable to induce full differentiation. FEBS Lett. 510 (2002) 149-153
35. Machida H., Matsumoto Y., Shirai M., and Kubota N. Geldanamycin, an inhibitor of Hsp90, sensitizes human tumour cells to radiation. Int. J. Radiat. Biol. 79 (2003) 973-980
36. MacMicking J., Xie Q.W., and Nathan C. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15 (1997) 323-350
37. Marshall C.J. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80 (1995) 179-185
38. Marshall J.D., Fearon K., Abbate C., Subramanian S., Yee P., Gregorio J., Coffman R.L., and Van Nest G. Identification of a novel CpG DNA class and motif that optimally stimulate B cell and plasmacytoid dendritic cell functions. J. Leukoc. Biol. 73 (2003) 781-792
39. Messina J.P., Gilkeson G.S., and Pisetsky D.S. Stimulation of in vitro murine lymphocyte proliferation by bacterial DNA. J. Immunol. 147 (1991) 1759-1764
40. Moon D.O., Park C., Heo M.S., Park Y.M., Choi Y.H., and Kim G.Y. PD98059 triggers G1 arrest and apoptosis in human leukemic U937 cells through downregulation of Akt signal pathway. Int. Immunopharmacol. 7 (2007) 36-45
41. Patel B.A., Gomis S., Dar A., Wilson P.J., Babiuk L.A., Potter A., Mutwiri G., and Tikoo S.K. Oligodeoxynucleotides containing CpG motifs (CpG-ODN) predominantly induce Th1-type immune response in neonatal chicks. Dev. Comp. Immunol. 32 (2008) 1041-1049
42. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (2001) e45
43. Picard D., Khursheed B., Garabedian M.J., Fortin M.G., Lindquist S., and Yamamoto K.R. Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348 (1990) 166-168
44. Pratt W.B. The role of the hsp90-based chaperone system in signal transduction by nuclear receptors and receptors signaling via MAP kinase. Annu. Rev. Pharmacol. Toxicol. 37 (1997) 297-326
45. Rankin R., Pontarallo R., Ioannou X., Krieg A.M., Hecker R., Babiuk L.A., and van Drunen Littel-van den Hurk S. CpG motif identification for veterinary and laboratory species demonstrates that sequence recognition is highly conserved. Antisense Nucleic Acid Drug Dev. 11 (2001) 333-340
46. Rutz M., Metzger J., Gellert T., Luppa P., Lipford G.B., Wagner H., and Bauer S. Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur. J. Immunol. 34 (2004) 2541-2550
47. Shevchenko A., Wilm M., Vorm O., and Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68 (1996) 850-858
48. Shimada S., Yano O., Inoue H., Kuramoto E., Fukuda T., Yamamoto H., Kataoka T., and Tokunaga T. Antitumor activity of the DNA fraction from Mycobacterium bovis BCG. II. Effects on various syngeneic mouse tumors. J. Natl. Cancer Inst. 74 (1985) 681-688
49. Shinomiya H., Hirata H., and Nakano M. Purification and characterization of the 65-kDa protein phosphorylated in murine macrophages by stimulation with bacterial lipopolysaccharide. J. Immunol. 146 (1991) 3617-3625
50. Taghavi A., Allan B., Mutwiri G., Van Kessel A., Wilson P., Babiuk L., Potter A., and Gomis S. Protection of neonatal broiler chicks against Salmonella typhimurium septicemia by DNA containing CpG motifs. Avian Dis. 52 (2008) 398-406
51. Takeshita F., Leifer C.A., Gursel I., Ishii K.J., Takeshita S., Gursel M., and Klinman D.M. Cutting edge: role of toll-like receptor 9 in CpG DNA-induced activation of human cells. J. Immunol. 167 (2001) 3555-3558
52. Temperley N.D., Berlin S., Paton I.R., Griffin D.K., and Burt D.W. Evolution of the chicken toll-like receptor gene family: a story of gene gain and gene loss. BMC Genom. 9 (2008) 62
53. Tokunaga T., Yamamoto S., and Namba K. A synthetic single-stranded DNA, poly(dG,dC), induces interferon-alpha/beta and -gamma, augments natural killer activity, and suppresses tumor growth. Jpn. J. Cancer Res. 79 (1988) 682-686
54. Underhill D.M., and Ozinsky A. Toll-like receptors: key mediators of microbe detection. Curr. Opin. Immunol. 14 (2002) 103-110
55. Vasselon T., and Detmers P.A. Toll receptors: a central element in innate immune responses. Infect. Immun. 70 (2002) 1033-1041
56. Verthelyi D., Ishii K.J., Gursel M., Takeshita F., and Klinman D.M. Human peripheral blood cells differentially recognize and respond to two distinct CPG motifs. J. Immunol. 166 (2001) 2372-2377
57. Weinberg J.B. Nitric oxide production and nitric oxide synthase type 2 expression by human mononuclear phagocytes: a review. Mol. Med. 4 (1998) 557-591
58. Xie H., Raybourne R.B., Babu U.S., Lillehoj H.S., and Heckert R.A. CpG-induced immunomodulation and intracellular bacterial killing in a chicken macrophage cell line. Dev. Comp. Immunol. 27 (2003) 823-834
59. Yang D., Chen Q., Hoover D.M., Staley P., Tucker K.D., Lubkowski J., and Oppenheim J.J. Many chemokines including CCL20/MIP-3alpha display antimicrobial activity. J. Leukoc. Biol. 74 (2003) 448-455
60. Zhu F.G., and Pisetsky D.S. Role of the heat shock protein 90 in immune response stimulation by bacterial DNA and synthetic oligonucleotides. Infect. Immun. 69 (2001) 5546-5552