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References

  1. Banchereau J, Steinman RM. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
    Pubmed CrossRef
  2. Birmingham CL, Higgins DE, Brumell JH. 2008. Avoiding death by autophagy: interactions of Listeria monocytogenes with the macrophage autophagy system. Autophagy 4: 368371.
  3. Choi NJ, Kim MK, Park HJ, Lim BU, Kang JS. 1998. Apoptosis of murine macrophage-like cells infected with Orientia tsutsugamushi. J. Korean Soc. Microbiol. 33: 399–406.
  4. Chu H, Lee JH, Han SH, Kim SY, Cho NH, Kim IS, et al. 2006. Exploitation of the endocytic pathway by Orientia tsutsugamushi in nonprofessional phagocytes. Infect. Immun. 74: 4246-4253.
    Pubmed CrossRef
  5. De Trez C, Pajak B, Brait M, Glaichenhaus N, Urbain J, Moser M, et al. 2005. TLR4 and Toll-IL-1 receptor domaincontaining adapter-inducing IFN-beta, but not MyD88, regulate Escherichia coli-induced dendritic cell maturation and apoptosis in vivo. J. Immunol. 175: 839-846.
    Pubmed
  6. Ehlers S, Holscher C, Scheu S, Tertilt C, Hehlgans T, Suwinski J, et al. 2003. The lymphotoxin beta receptor is critically involved in controlling infections with the intracellular pathogens Mycobacterium tuberculosis and Listeria monocytogenes. J. Immunol. 170: 5210-5218.
    Pubmed
  7. Fujii S, Liu K, Smith C, Bonito AJ, Steinman RM. 2004. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J. Exp. Med. 199:1607-1618.
    Pubmed CrossRef
  8. Hanson B. 1991. Comparative susceptibility to mouse interferons of Rickettsia tsutsugamushi strains with different virulence in mice and of Rickettsia rickettsii. Infect. Immun. 59: 4134-4141.
    Pubmed
  9. Hanson B. 1991. Susceptibility of Rickettsia tsutsugamushi Gilliam to gamma interferon in cultured mouse cells. Infect. Immun. 59: 4125-4133.
    Pubmed
  10. Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, Matsushima K. 1994. Essential involvement of interleukin-8 (IL-8) in acute inflammation. J. Leukoc. Biol. 56: 559-564.
    Pubmed
  11. Henry CJ, Ornelles DA, Mitchell LM, Brzoza-Lewis KL, Hiltbold EM. 2008. IL-12 produced by dendritic cells augments CD8+ T cell activation through the production of the chemokines CCL1 and CCL17. J. Immunol. 181: 8576-8584.
    Pubmed
  12. Ho LJ, Shaio MF, Chang DM, Liao CL, Lai JH. 2004. Infection of human dendritic cells by dengue virus activates and primes T cells towards Th0-like phenotype producing both Th1 and Th2 cytokines. Immunol. Invest. 33: 423-437.
    Pubmed CrossRef
  13. Iwasaki H, Mizoguchi J, Takada N, Tai K, Ikegaya S, Ueda T. 2010. Correlation between the concentrations of tumor necrosis factor-alpha and the severity of disease in patients infected with Orientia tsutsugamushi. Int. J. Infect. Dis. 14:e328-e333.
    Pubmed CrossRef
  14. Jeong YJ, Kim S, Wook YD, Lee JW, Kim KI, Lee SH. 2007. Scrub typhus: clinical, pathologic, and imaging findings. Radiographics 27: 161-172.
    Pubmed CrossRef
  15. Kadosaka T, Kimura E. 2003. Electron microscopic observations of Orientia tsutsugamushi in salivary gland cells of naturally infected Leptotrombidium pallidum larvae during feeding. Microbiol. Immunol. 47: 727-733.
    Pubmed
  16. Kaplanski G, Marin V, Montero-Julian F, Mantovani A, Farnarier C. 2003. IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation. Trends Immunol. 24: 25-29.
    CrossRef
  17. Kawamura A, Tanaka H, Tamura A. 1995. Tsutsugamushi Disease. University of Tokyo Press.
  18. Kee SH, Cho KA, Kim MK, Lim BU, Chang WH, Kang JS. 1999. Disassembly of focal adhesions during apoptosis of endothelial cell line ECV304 infected with Orientia tsutsugamushi. Microb. Pathog. 27: 265-271.
    Pubmed CrossRef
  19. Kim DW, Chu H, Joo DH, Jang MS, Choi JH, Park SM, et al. 2008. OspF directly attenuates the activity of extracellular signal-regulated kinase during invasion by Shigella flexneri in human dendritic cells. Mol. Immunol. 45: 3295-3301.
    Pubmed CrossRef
  20. Kim MK, Seong SY, Seoh JY, Han TH, Song HJ, Lee JE, et al. 2002. Orientia tsutsugamushi inhibits apoptosis of macrophages by retarding intracellular calcium release. Infect. Immun. 70:4692-4696.
    Pubmed CrossRef
  21. Kim SW, Ihn KS, Han SH, Seong SY, Kim IS, Choi MS. 2001. Microtubule- and dynein-mediated movement of Orientia tsutsugamushi to the microtubule organizing center. Infect. Immun. 69: 494-500.
    Pubmed CrossRef
  22. Kodama K, Kawamura S, Yasukawa M, Kobayashi Y. 1987. Establishment and characterization of a T-cell line specific for Rickettsia tsutsugamushi. Infect. Immun. 55: 2490-2495.
    Pubmed
  23. Lebre M C, B urwell T, Vieira PL, L ora J, C oyle A J, Kapsenberg ML, Clausen BE, De Jong EC. 2005. Differential expression of inflammatory chemokines by Th1- and Th2cell promoting dendritic cells: a role for different mature dendritic cell populations in attracting appropriate effector cells to peripheral sites of inflammation. Immunol. Cell Biol. 83: 525-535.
    Pubmed CrossRef
  24. Mandron M, Aries MF, Brehm RD, Tranter HS, Acharya KR, Charveron M, et al. 2006. Human dendritic cells conditioned with Staphylococcus aureus enterotoxin B promote TH2 cell polarization. J. Allergy Clin. Immunol. 117: 1141-1147.
    Pubmed CrossRef
  25. Metz G, Carlier Y, Vray B. 1993. Trypanosoma cruzi upregulates nitric oxide release by IFN-gamma-preactivated macrophages, limiting cell infection independently of the respiratory burst. Parasite Immunol. 15: 693-699.
    Pubmed CrossRef
  26. Mielke ME, Peters C, Hahn H. 1997. Cytokines in the induction and expression of T-cell-mediated granuloma formation and protection in the murine model of listeriosis. Immunol. Rev. 158: 79-93.
    Pubmed CrossRef
  27. Moron CG, Popov VL, Feng HM, Wear D, Walker DH. 2001. Identification of the target cells of Orientia tsutsugamushi in human cases of scrub typhus. Mod. Pathol. 14: 752-759.
    Pubmed CrossRef
  28. Nace G, Evankovich J, Eid R, Tsung A. 2012. Dendritic cells and damage-associated molecular patterns: endogenous danger signals linking innate and adaptive immunity. J. Innate Immun. 4: 6-15.
    Pubmed CrossRef
  29. Nacy CA, Meltzer MS. 1979. Macrophages in resistance to rickettsial infection: macrophage activation in vitro for killing of Rickettsia tsutsugamushi. J. Immunol. 123: 2544-2549.
    Pubmed
  30. Ng FK, Oaks Jr SC, Lee M, Groves MG, Lewis Jr GE. 1985. A scanning and transmission electron microscopic examination of Rickettsia tsutsugamushi-infected human endothelial, MRC-5, and L-929 cells. Jpn. J. Med. Sci. Biol. 38: 125-139.
    Pubmed
  31. Park SM, Ko HJ, Shim DH, Yang JY, Park YH, Curtiss 3rd R, et al. 2008. MyD88 signaling is not essential for induction of antigen-specific B cell responses but is indispensable for protection against Streptococcus pneumoniae infection following oral vaccination with attenuated Salmonella expressing PspA antigen. J. Immunol. 181: 6447-6455.
    Pubmed
  32. Rajapakse S, Rodrigo C, Fernando D. 2012. Scrub typhus:pathophysiology, clinical manifestations and prognosis. Asian Pac. J. Trop. Med. 5: 261-264.
    CrossRef
  33. Reis e Sousa C. 2004. Activation of dendritic cells: translating innate into adaptive immunity. Curr. Opin. Immunol. 16: 2125.
    CrossRef
  34. Santic M, Asare R, Skrobonja I, Jones S, Abu Kwaik Y. 2008. Acquisition of the vacuolar ATPase proton pump and phagosome acidification are essential for escape of Francisella tularensis into the macrophage cytosol. Infect. Immun. 76:2671-2677.
    Pubmed CrossRef
  35. Seong SY, Choi MS, Kim IS. 2001. Orientia tsutsugamushi infection: overview and immune responses. Microbes Infect. 3: 11-21.
    CrossRef
  36. Shankar A H, T itus R G. 1 997. T he i nfluence of antigenpresenting cell type and interferon-gamma on priming and cytokine secretion of Leishmania major-specific T cells. J. Infect. Dis. 175: 151-157.
    Pubmed CrossRef
  37. Suzuki T, Nakanishi K, Tsutsui H, Iwai H, Akira S, Inohara N, et al. 2005. A novel caspase-1/toll-like receptor 4independent pathway of cell death induced by cytosolic Shigella in infected macrophages. J. Biol. Chem. 280: 1404214050.
    Pubmed CrossRef
  38. Ten Brinke A, Karsten ML, Dieker MC, Zwaginga JJ, van Ham SM. 2007. The clinical grade maturation cocktail monophosphoryl lipid A plus IFNgamma generates monocytederived dendritic cells with the capacity to migrate and induce Th1 polarization. Vaccine 25: 7145-7152.
    Pubmed CrossRef
  39. Weaver JM, Sant AJ. 2009. Understanding the focused CD4 T cell response to antigen and pathogenic organisms. Immunol. Res. 45: 123-143.
    Pubmed CrossRef
  40. Yu Y, Wen B, Niu D, Chen M, Qiu L. 2005. Induction of protective immunity against scrub typhus with a 56kilodalton recombinant antigen fused with a 47-kilodalton antigen of Orientia tsutsugamushi Karp. Am. J. Trop. Med. Hyg. 72: 458-464.
    Pubmed

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Article

Research article

J. Microbiol. Biotechnol. 2013; 23(8): 1159-1166

Published online August 28, 2013 https://doi.org/10.4014/jmb.1303.03019

Copyright © The Korean Society for Microbiology and Biotechnology.

Orientia tsutsugamushi Infection Induces CD4+ T Cell Activation via Human Dendritic Cell Activity

Hyuk Chu 1, Sung-Moo Park 2, 3, In Su Cheon 2, Mi-Yeoun Park 1, Byoung-Shik Shim 3, Byoung-Cheol Gil 1, Woon Hee Jeung 2, Kyu-Jam Hwang 1, Ki-Duk Song 2, Kee-Jong Hong 4, Manki Song 3, Hang-Jin Jeong 1, Seung Hyun Han 5 and Cheol-Heui Yun 2*

1Division of Zoonoses, Center for Immunology and Pathology, Korea National Institute of Health, Osong 363-951, Republic of Korea, 2Animal Science and Biotechnology Major and WCU Biomodulation Major, Department of Agricultural Biotechnology, Research Institute for Agriculture and Life Sciences, and Center for Food and Bioconvergence, Seoul National University, Seoul, 151-921 Republic of Korea. , 3Laboratory Science Division, International Vaccine Institute, Seoul 151-818, Republic of Korea, 4Division of High-Risk Pathogen Research, Center for Infectious Diseases, Korea National Institute of Health, Osong 363-951, Republic of Korea, 5Department of Oral Microbiology and Immunology, Dental Research Institute and BK21 Program, School of Dentistry, Seoul National University, Seoul 110-749, Republic of Korea

Received: March 7, 2013; Accepted: April 26, 2013

Abstract

Orientia tsutsugamushi, a gram-negative bacterium, causes severe acute febrile illness in
humans. Despite this danger, the route of infection, infectivity, and protective mechanisms of
the host’s immune response to O. tsutsugamushi are unclear. Dendritic cells (DCs) are one of
the most important cell types in bridging the innate and adaptive immune responses. In this
study, we observed that O. tsutsugamushi infects and replicates in monocyte-derived DCs
(MODCs). During infection and replication, the expressions of the cytokines IL-12 and TNF-α,
as well as the co-stimulatory molecules CD80, CD83, CD86, and CD40, were increased in
MODCs. When O. tsutsugamushi-treated MODCs were co-cultured with autologous CD4+ T
cells, they enhanced production of IFN-γ, a major Th1 cytokine. Collectively, our results show
that O. tsutsugamushi can replicate in MODCs and can simultaneously induce MODC
maturation and increase proinflammatory cytokine levels in MODCs that subsequently
activate CD4+ T cells.

Keywords: Orientia tsutsugamushi, Dendritic cells, T cell, Pro-inflammatory cytokines

References

  1. Banchereau J, Steinman RM. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
    Pubmed CrossRef
  2. Birmingham CL, Higgins DE, Brumell JH. 2008. Avoiding death by autophagy: interactions of Listeria monocytogenes with the macrophage autophagy system. Autophagy 4: 368371.
  3. Choi NJ, Kim MK, Park HJ, Lim BU, Kang JS. 1998. Apoptosis of murine macrophage-like cells infected with Orientia tsutsugamushi. J. Korean Soc. Microbiol. 33: 399–406.
  4. Chu H, Lee JH, Han SH, Kim SY, Cho NH, Kim IS, et al. 2006. Exploitation of the endocytic pathway by Orientia tsutsugamushi in nonprofessional phagocytes. Infect. Immun. 74: 4246-4253.
    Pubmed CrossRef
  5. De Trez C, Pajak B, Brait M, Glaichenhaus N, Urbain J, Moser M, et al. 2005. TLR4 and Toll-IL-1 receptor domaincontaining adapter-inducing IFN-beta, but not MyD88, regulate Escherichia coli-induced dendritic cell maturation and apoptosis in vivo. J. Immunol. 175: 839-846.
    Pubmed
  6. Ehlers S, Holscher C, Scheu S, Tertilt C, Hehlgans T, Suwinski J, et al. 2003. The lymphotoxin beta receptor is critically involved in controlling infections with the intracellular pathogens Mycobacterium tuberculosis and Listeria monocytogenes. J. Immunol. 170: 5210-5218.
    Pubmed
  7. Fujii S, Liu K, Smith C, Bonito AJ, Steinman RM. 2004. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J. Exp. Med. 199:1607-1618.
    Pubmed CrossRef
  8. Hanson B. 1991. Comparative susceptibility to mouse interferons of Rickettsia tsutsugamushi strains with different virulence in mice and of Rickettsia rickettsii. Infect. Immun. 59: 4134-4141.
    Pubmed
  9. Hanson B. 1991. Susceptibility of Rickettsia tsutsugamushi Gilliam to gamma interferon in cultured mouse cells. Infect. Immun. 59: 4125-4133.
    Pubmed
  10. Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, Matsushima K. 1994. Essential involvement of interleukin-8 (IL-8) in acute inflammation. J. Leukoc. Biol. 56: 559-564.
    Pubmed
  11. Henry CJ, Ornelles DA, Mitchell LM, Brzoza-Lewis KL, Hiltbold EM. 2008. IL-12 produced by dendritic cells augments CD8+ T cell activation through the production of the chemokines CCL1 and CCL17. J. Immunol. 181: 8576-8584.
    Pubmed
  12. Ho LJ, Shaio MF, Chang DM, Liao CL, Lai JH. 2004. Infection of human dendritic cells by dengue virus activates and primes T cells towards Th0-like phenotype producing both Th1 and Th2 cytokines. Immunol. Invest. 33: 423-437.
    Pubmed CrossRef
  13. Iwasaki H, Mizoguchi J, Takada N, Tai K, Ikegaya S, Ueda T. 2010. Correlation between the concentrations of tumor necrosis factor-alpha and the severity of disease in patients infected with Orientia tsutsugamushi. Int. J. Infect. Dis. 14:e328-e333.
    Pubmed CrossRef
  14. Jeong YJ, Kim S, Wook YD, Lee JW, Kim KI, Lee SH. 2007. Scrub typhus: clinical, pathologic, and imaging findings. Radiographics 27: 161-172.
    Pubmed CrossRef
  15. Kadosaka T, Kimura E. 2003. Electron microscopic observations of Orientia tsutsugamushi in salivary gland cells of naturally infected Leptotrombidium pallidum larvae during feeding. Microbiol. Immunol. 47: 727-733.
    Pubmed
  16. Kaplanski G, Marin V, Montero-Julian F, Mantovani A, Farnarier C. 2003. IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation. Trends Immunol. 24: 25-29.
    CrossRef
  17. Kawamura A, Tanaka H, Tamura A. 1995. Tsutsugamushi Disease. University of Tokyo Press.
  18. Kee SH, Cho KA, Kim MK, Lim BU, Chang WH, Kang JS. 1999. Disassembly of focal adhesions during apoptosis of endothelial cell line ECV304 infected with Orientia tsutsugamushi. Microb. Pathog. 27: 265-271.
    Pubmed CrossRef
  19. Kim DW, Chu H, Joo DH, Jang MS, Choi JH, Park SM, et al. 2008. OspF directly attenuates the activity of extracellular signal-regulated kinase during invasion by Shigella flexneri in human dendritic cells. Mol. Immunol. 45: 3295-3301.
    Pubmed CrossRef
  20. Kim MK, Seong SY, Seoh JY, Han TH, Song HJ, Lee JE, et al. 2002. Orientia tsutsugamushi inhibits apoptosis of macrophages by retarding intracellular calcium release. Infect. Immun. 70:4692-4696.
    Pubmed CrossRef
  21. Kim SW, Ihn KS, Han SH, Seong SY, Kim IS, Choi MS. 2001. Microtubule- and dynein-mediated movement of Orientia tsutsugamushi to the microtubule organizing center. Infect. Immun. 69: 494-500.
    Pubmed CrossRef
  22. Kodama K, Kawamura S, Yasukawa M, Kobayashi Y. 1987. Establishment and characterization of a T-cell line specific for Rickettsia tsutsugamushi. Infect. Immun. 55: 2490-2495.
    Pubmed
  23. Lebre M C, B urwell T, Vieira PL, L ora J, C oyle A J, Kapsenberg ML, Clausen BE, De Jong EC. 2005. Differential expression of inflammatory chemokines by Th1- and Th2cell promoting dendritic cells: a role for different mature dendritic cell populations in attracting appropriate effector cells to peripheral sites of inflammation. Immunol. Cell Biol. 83: 525-535.
    Pubmed CrossRef
  24. Mandron M, Aries MF, Brehm RD, Tranter HS, Acharya KR, Charveron M, et al. 2006. Human dendritic cells conditioned with Staphylococcus aureus enterotoxin B promote TH2 cell polarization. J. Allergy Clin. Immunol. 117: 1141-1147.
    Pubmed CrossRef
  25. Metz G, Carlier Y, Vray B. 1993. Trypanosoma cruzi upregulates nitric oxide release by IFN-gamma-preactivated macrophages, limiting cell infection independently of the respiratory burst. Parasite Immunol. 15: 693-699.
    Pubmed CrossRef
  26. Mielke ME, Peters C, Hahn H. 1997. Cytokines in the induction and expression of T-cell-mediated granuloma formation and protection in the murine model of listeriosis. Immunol. Rev. 158: 79-93.
    Pubmed CrossRef
  27. Moron CG, Popov VL, Feng HM, Wear D, Walker DH. 2001. Identification of the target cells of Orientia tsutsugamushi in human cases of scrub typhus. Mod. Pathol. 14: 752-759.
    Pubmed CrossRef
  28. Nace G, Evankovich J, Eid R, Tsung A. 2012. Dendritic cells and damage-associated molecular patterns: endogenous danger signals linking innate and adaptive immunity. J. Innate Immun. 4: 6-15.
    Pubmed CrossRef
  29. Nacy CA, Meltzer MS. 1979. Macrophages in resistance to rickettsial infection: macrophage activation in vitro for killing of Rickettsia tsutsugamushi. J. Immunol. 123: 2544-2549.
    Pubmed
  30. Ng FK, Oaks Jr SC, Lee M, Groves MG, Lewis Jr GE. 1985. A scanning and transmission electron microscopic examination of Rickettsia tsutsugamushi-infected human endothelial, MRC-5, and L-929 cells. Jpn. J. Med. Sci. Biol. 38: 125-139.
    Pubmed
  31. Park SM, Ko HJ, Shim DH, Yang JY, Park YH, Curtiss 3rd R, et al. 2008. MyD88 signaling is not essential for induction of antigen-specific B cell responses but is indispensable for protection against Streptococcus pneumoniae infection following oral vaccination with attenuated Salmonella expressing PspA antigen. J. Immunol. 181: 6447-6455.
    Pubmed
  32. Rajapakse S, Rodrigo C, Fernando D. 2012. Scrub typhus:pathophysiology, clinical manifestations and prognosis. Asian Pac. J. Trop. Med. 5: 261-264.
    CrossRef
  33. Reis e Sousa C. 2004. Activation of dendritic cells: translating innate into adaptive immunity. Curr. Opin. Immunol. 16: 2125.
    CrossRef
  34. Santic M, Asare R, Skrobonja I, Jones S, Abu Kwaik Y. 2008. Acquisition of the vacuolar ATPase proton pump and phagosome acidification are essential for escape of Francisella tularensis into the macrophage cytosol. Infect. Immun. 76:2671-2677.
    Pubmed CrossRef
  35. Seong SY, Choi MS, Kim IS. 2001. Orientia tsutsugamushi infection: overview and immune responses. Microbes Infect. 3: 11-21.
    CrossRef
  36. Shankar A H, T itus R G. 1 997. T he i nfluence of antigenpresenting cell type and interferon-gamma on priming and cytokine secretion of Leishmania major-specific T cells. J. Infect. Dis. 175: 151-157.
    Pubmed CrossRef
  37. Suzuki T, Nakanishi K, Tsutsui H, Iwai H, Akira S, Inohara N, et al. 2005. A novel caspase-1/toll-like receptor 4independent pathway of cell death induced by cytosolic Shigella in infected macrophages. J. Biol. Chem. 280: 1404214050.
    Pubmed CrossRef
  38. Ten Brinke A, Karsten ML, Dieker MC, Zwaginga JJ, van Ham SM. 2007. The clinical grade maturation cocktail monophosphoryl lipid A plus IFNgamma generates monocytederived dendritic cells with the capacity to migrate and induce Th1 polarization. Vaccine 25: 7145-7152.
    Pubmed CrossRef
  39. Weaver JM, Sant AJ. 2009. Understanding the focused CD4 T cell response to antigen and pathogenic organisms. Immunol. Res. 45: 123-143.
    Pubmed CrossRef
  40. Yu Y, Wen B, Niu D, Chen M, Qiu L. 2005. Induction of protective immunity against scrub typhus with a 56kilodalton recombinant antigen fused with a 47-kilodalton antigen of Orientia tsutsugamushi Karp. Am. J. Trop. Med. Hyg. 72: 458-464.
    Pubmed