Chlamydial infection of immune cells: Altered function and implications for disease

Critical Reviews in Immunology

Volumn 29, Issue 4, 2009, Pages 275-305

  Beagley, Kenneth ^a   Huston, Wilhelmina M ^a   Hansbro, Philip M ^b   Timms, Peter ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b HUNTER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Chlamydia pneumoniae; Chlamydia psittaci; Chlamydia trachcomatis; Dendritic cell; Macrophage; Monocyte; Polymorphonuclear leukocyte

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ALZHEIMER DISEASE; APOPTOSIS; ASTHMA; ASTROCYTE; BACTERIAL GROWTH; BACTERIAL PNEUMONIA; BACTERIAL VIRULENCE; BONE MARROW CELL; CELL ADHESION; CELL LINE; CELLULAR IMMUNITY; CHLAMYDIA; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; CHLAMYDOPHILA PNEUMONIAE; COMMUNITY ACQUIRED PNEUMONIA; CORONARY ARTERY DISEASE; CYTOKINE PRODUCTION; DENDRITIC CELL; FOAM CELL; GLIA CELL; HUMAN; INFERTILITY; LUNG ALVEOLUS MACROPHAGE; LYMPHOMA; MACROPHAGE; MACROPHAGE MIGRATION; MAST CELL; MONOCYTE; MULTIPLE SCLEROSIS; NERVE CELL; NEUTROPHIL; NONHUMAN; PELVIC INFLAMMATORY DISEASE; PERITONEUM MACROPHAGE; PERSISTENT INFECTION; PRIORITY JOURNAL; REACTIVE ARTHRITIS; REVIEW; T LYMPHOCYTE; TRACHOMA;

ANIMALS; CHLAMYDIA; CHLAMYDIA INFECTIONS; DENDRITIC CELLS; EVOLUTION; HUMANS; INFLAMMATION; MACROPHAGES; MONOCYTES;

EID: 69149083126     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (162)

1. Corsaro D, Valassina M, Venditti D. Increasing diversity within Chlamydiae. Crit Rev Microbiol. 2003;29(1):37-78.
2. Everett KD, Bush RM, Andersen AA. Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. Int J Syst Bacteriol. 1999;49 Pt 2:415-40.
3. Schachter J, Stephens RS, Timms P, Kuo C, Bavoil PM, Birkelund S, Boman J, Caldwell H, Campbell LA, Chernesky M, Christiansen G, Clarke IN, Gaydos C, Grayston JT, Hackstadt T, Hsia R, Kaltenboeck B, Leinonnen M, Ojcius D, McClarty G, Orfila J, Peeling R, Puolakkainen M, Quinn TC, Rank RG, Raulston J, Ridgeway GL, Saikku P, Stamm WE, Taylor-Robinson DT, Wang SP, Wyrick PB. Radical changes to chlamydial taxonomy are not necessary just yet. Int J Syst Evol Microbiol. 2001;51(Pt 1):249; author reply 51-3.
4. Boman J, Hammerschlag MR. Chlamydia pneumoniae and atherosclerosis: critical assessment of diagnostic methods and relevance to treatment studies. Clin Microbiol Rev. 2002;15(1):1-20.
5. Stratton CW, Sriram S. Association of Chlamydia pneumoniae with central nervous system disease. Microbes Infect. 2003;5(13):1249-53.
6. Berger L, Volp K, Mathews S, Speare R, Timms P. Chlamydia pneumoniae in a free-ranging giant barred frog (Mixophyes iteratus) from Australia. J Clin Microbiol. 1999;37(7):2378-80.
7. Bodetti TJ, Jacobson E, Wan C, Hafner L, Pospischil A, Rose K, Timms P. Molecular evidence to support the expansion of the hostrange of Chlamydophila pneumoniae to include reptiles as well as humans, horses, koalas and amphibians. Syst Appl Microbiol. 2002;25(1):146-52.
8. Greub G. Parachlamydia acanthamoebae, an emerging agent of pneumonia. Clin Microbiol Infect. 2009;15(1):18-28.
9. Corsaro D, Venditti D. Emerging chlamydial infections. Crit Rev Microbiol. 2004;30(2):75-106.
10. Kahane S, Metzer E, Friedman MG. Evidence that the novel microorganism "Z" may belong to a new genus in the family Chlamydiaceae. FEMS Microbiol Lett. 1995;126(2):203-7.
11. Lieberman D, Kahane S, Lieberman D, Friedman MG. Pneumonia with serological evidence of acute infection with the Chlamydia-like microorganism "Z". Am J Respir Crit Care Med. 1997;156(2 Pt 1): 578-82.
12. Kahane S, Everett KD, Kimmel N, Friedman MG. Simkania negevensis strain ZT: growth, antigenic and genome characteristics. Int J Syst Bacteriol. 1999;49(Pt 2):815-20.
13. Kahane S, Dvoskin B, Mathias M, Friedman MG. Infection of Acanthamoeba polyphaga with Simkania negevensis and S. negevensis survival within amoebal cysts. Appl Environ Microbiol. 2001;67(10):4789-95.
14. Rurangirwa FR, Dilbeck PM, Crawford TB, McGuire TC, McElwain TF. Analysis of the 16S rRNA gene of micro-organism WSU 86-1044 from an aborted bovine foetus reveals that it is a member of the order Chlamydiales: proposal of Waddliaceae fam. nov., Waddlia chondrophila gen. nov., sp. nov. Int J Syst Bacteriol. 1999;49(Pt 2):577-81.
15. Goy G, Croxatto A, Greub G. Waddlia chondrophila enters and multiplies within human macrophages. Microbes Infect. 2008;10(5):556-62.
16. Zhang JP, Stephens RS. Mechanism of C. trachomatis attachment to eukaryotic host cells. Cell. 1992;69(5):861-9.
17. Su H, Raymond L, Rockey DD, Fischer E, Hackstadt T, Caldwell HD. A recombinant Chlamydia trachomatis major outer membrane protein binds to heparan sulfate receptors on epithelial cells. Proc Natl Acad Sci U S A. 1996;93(20):11143-8.
18. Ward ME, Murray A. Control mechanisms governing the infectivity of Chlamydia trachomatis for HeLa cells: mechanisms of endocytosis. J Gen Microbiol. 1984;130(7):1765-80.
19. Hodinka RL, Davis CH, Choong J, Wyrick PB. Ultrastructural study of endocytosis of Chlamydia trachomatis by McCoy cells. Infect Immun. 1988;56(6): 1456-63.
20. Prain CJ, Pearce JH. Ultrastructural studies on the intracellular fate of Chlamydia psittaci (strain guinea pig inclusion conjunctivitis) and Chlamydia trachomatis (strain lymphogranuloma venereum 434): modulation of intracellular events and relationship with endocytic mechanism. J Gen Microbiol. 1989;135(7):2107-23.
21. Hackstadt T, Scidmore MA, Rockey DD. Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc Natl Acad Sci U S A. 1995;92(11):4877-81.
22. Hoare A, Timms P, Bavoil PM, Wilson DP. Spatial constraints within the chlamydial host cell inclusion predict interrupted development and persistence. BMC Microbiol. 2008;8:5.
23. Hybiske K, Stephens RS. Mechanisms of host cell exit by the intracellular bacterium Chlamydia. Proc Natl Acad Sci U S A. 2007;104(27):11430-5.
24. Kuo CC, Puolakkainen M, Lin TM, Witte M, Campbell LA. Mannose-receptor positive and negative mouse macrophages differ in their susceptibility to infection by Chlamydia species. Microb Pathog. 2002;32(1):43-8.
25. Rockey DD, Fischer ER, Hackstadt T. Temporal analysis of the developing Chlamydia psittaci inclusion by use of fluorescence and electron microscopy. Infect Immun. 1996;64(10):4269-78.
26. Hogan RJ, Mathews SA, Mukhopadhyay S, Summersgill JT, Timms P. Chlamydial persistence: beyond the biphasic paradigm. Infect Immun. 2004;72(4):1843-55.
27. Koehler L, Nettelnbreker E, Hudson AP, Ott N, Gerard HC, Branigan PJ, Schumacher HR, Drommer W, Zeidler H. Ultrastructural and molecular analyses of the persistence of Chlamydia trachomatis (serovar K) in human monocytes. Microb Pathog. 1997;22(3):133-42.
28. Airenne S, Surcel HM, Alakarppa H, Laitinen K, Paavonen J, Saikku P, Laurila A. Chlamydia pneumoniae infection in human monocytes. Infect Immun. 1999;67(3):1445-9.
29. Nanagara R, Li F, Beutler A, Hudson A, Schumacher HR Jr. Alteration of Chlamydia trachomatis biologic behavior in synovial membranes. Suppression of surface antigen production in reactive arthritis and Reiter's syndrome. Arthritis Rheum. 1995;38(10):1410-7.
30. Skowasch D, Yeghiazaryan K, Schrempf S, Golubnitschaja O, Welsch U, Preusse CJ, Likungu JA, Welz A, Lüderitz B, Bauriedel G. Persistence of Chlamydia pneumoniae in degenerative aortic valve stenosis indicated by heat shock protein 60 homologues. J Heart Valve Dis. 2003;12(1):68-75.
31. Mazzoli S, Bani A, Salvi A, Ramacciotti I, Romeo C, Bani T. In vivo evidence of Chlamydia trachomatis miniature reticulate bodies as persistence markers in patients with chronic chlamydial prostatitis. Proceedings of 4th European Society for Chlamydia Research, August 20-23, 2000, Helsinki, Finland. 2000.
32. Phillips DM, Swenson CE, Schachter J. Ultrastructure of Chlamydia trachomatis infection of the mouse oviduct. J Ultrastruct Res. 1984 Sep;88(3):244-56.
33. Pospischil A, Borel N, Chowdhury EH, Guscetti F. Aberrant chlamydial developmental forms in the gastrointestinal tract of pigs spontaneously and experimentally infected with Chlamydia suis. Vet Microbiol. 2009;135(1-2):147- 156.
34. Patton DL, Askienazy-Elbhar M, Henry-Suchet J, Campbell LA, Cappuccio A, Tannous W, Wang SP, Kuo CC. Detection of Chlamydia trachomatis in fallopian tube tissue in women with postinfectious tubal infertility. Am J Obstet Gynecol. 1994;171(1):95-101.
35. Holland SM, Hudson AP, Bobo L, Whittum-Hudson JA, Viscidi RP, Quinn TC, Taylor HR. Demonstration of chlamydial RNA and DNA during a culture-negative state. Infect Immun. 1992;60(5):2040-7.
36. Gerard HC, Branigan PJ, Schumacher HR Jr., Hudson AP. Synovial Chlamydia trachomatis in patients with reactive arthritis/Reiter's syndrome are viable but show aberrant gene expression. J Rheumatol. 1998;25(4):734-42.
37. Dean D, Suchland RJ, Stamm WE. Evidence for long-term cervical persistence of Chlamydia trachomatis by omp1 genotyping. J Infect Dis. 2000;182(3):909-16.
38. Hammerschlag MR, Chirgwin K, Roblin PM, Gelling M, Dumornay W, Mandel L, Smith P, Schachter J. Persistent infection with Chlamydia pneumoniae following acute respiratory illness. Clin Infect Dis. 1992;14(1):178-82.
39. Matyszak MK, Young JL, Gaston JS. Uptake and processing of Chlamydia trachomatis by human dendritic cells. Eur J Immunol. 2002;32(3):742-51.
40. Haranaga S, Yamaguchi H, Friedman H, Izumi S, Yamamoto Y. Chlamydia pneumoniae infects and multiplies in lymphocytes in vitro. Infect Immun. 2001;69(12):7753-9.
41. Yong EC, Chi EY, Kuo CC. Differential antimicrobial activity of human mononuclear phagocytes against the human biovars of Chlamydia trachomatis. J Immunol. 1987;139(4):1297-302.
42. Gerard HC, Kohler L, Branigan PJ, Zeidler H, Schumacher HR, Hudson AP. Viability and gene expression in Chlamydia trachomatis during persistent infection of cultured human monocytes. Med Microbiol Immunol. 1998;187(2):115-20.
43. Schmitz E, Nettelnbreker E, Zeidler H, Hammer M, Manor E, Wollenhaupt J. Intracellular persistence of chlamydial major outer-membrane protein, lipopolysaccharide and ribosomal RNA after non-productive infection of human monocytes with Chlamydia trachomatis serovar K. J Med Microbiol. 1993;38(4):278-85.
44. Schrader S, Klos A, Hess S, Zeidler H, Kuipers JG, Rihl M. Expression of inflammatory host genes in Chlamydia trachomatis-infected human monocytes. Arthritis Res Ther. 2007;9(3):R54.
45. Jendro MC, Deutsch T, Korber B, Kohler L, Kuipers JG, Krausse-Opatz B, Westermann J, Raum E, Zeidler H. Infection of human monocyte-derived macrophages with Chlamydia trachomatis induces apoptosis of T cells: a potential mechanism for persistent infection. Infect Immun. 2000;68(12):6704-11.
46. Jendro MC, Fingerle F, Deutsch T, Liese A, Kohler L, Kuipers JG, Raum E, Martin M, Zeidler H. Chlamydia trachomatis-infected macrophages induce apoptosis of activated T cells by secretion of tumor necrosis factor-alpha in vitro. Med Microbiol Immunol. 2004;193(1):45-52.
47. Poikonen K, Lajunen T, Silvennoinen-Kassinen S, Paldanius M, Leinonen M, Saikku P. Susceptibility of human monocyte-macrophages to Chlamydia pneumoniae infection in vitro is highly variable and associated with levels of soluble CD14 and C. pneumoniae IgA and human HSP-IgG antibodies in serum. Scand J Immunol. 2008;67(3):279-84.
48. Geng Y, Shane RB, Berencsi K, Gonczol E, Zaki MH, Margolis DJ, Trinchieri G, Rook AH. Chlamydia pneumoniae inhibits apoptosis in human peripheral blood mononuclear cells through induction of IL-10. J Immunol. 2000;164(10):5522-9.
49. Yamaguchi H, Haranaga S, Widen R, Friedman H, Yamamoto Y. Chlamydia pneumoniae infection induces differentiation of monocytes into macrophages. Infect Immun. 2002;70(5):2392-8.
50. Kaukoranta-Tolvanen SS, Teppo AM, Laitinen K, Saikku P, Linnavuori K, Leinonen M. Growth of Chlamydia pneumoniae in cultured human peripheral blood mononuclear cells and induction of a cytokine response. Microb Pathog. 1996;21(3):215-21.
51. Klos A, Thalmann J, Peters J, Gerard HC, Hudson AP. The transcript profile of persistent Chlamydophila (Chlamydia) pneumoniae in vitro depends on the means by which persistence is induced. FEMS Microbiol Lett. 2009;291(1):120-6.
52. Hearst JE, Warr GA, Jakab GJ. Characterization of murine lung and peritoneal macrophages. J Reticuloendothel Soc. 1980;27(5):443-54.
53. Nakajo MN, Roblin PM, Hammerschlag MR, Smith P, Nowakowski M. Chlamydicidal activity of human alveolar macrophages. Infect Immun. 1990;58(11):3640-4.
54. Redecke V, Dalhoff K, Bohnet S, Braun J, Maass M. Interaction of Chlamydia pneumoniae and human alveolar macrophages: infection and inflammatory response. Am J Respir Cell Mol Biol. 1998;19(5): 721-7.
55. Gaydos CA, Summersgill JT, Sahney NN, Ramirez JA, Quinn TC. Replication of Chlamydia pneumoniae in vitro in human macrophages, endothelial cells, and aortic artery smooth muscle cells. Infect Immun. 1996;64(5):1614-20.
56. Mpiga P, Ravaoarinoro M. Effects of sustained antibiotic bactericidal treatment on Chlamydia trachomatis-infected epithelial-like cells (HeLa) and monocyte-like cells (THP-1 and U-937). Int J Antimicrob Agents. 2006;27(4):316-24.
57. Numazaki K, Suzuki K, Chiba S. Replication of Chlamydia trachomatis and C. pneumoniae in the human monocytic cell line U-937. J Med Microbiol. 1995;42(3):191-5.
58. Yamaguchi H, Haranaga S, Friedman H, Moor JA, Muffly KE, Yamamoto Y. A Chlamydia pneumoniae infection model using established human lymphocyte cell lines. FEMS Microbiol Lett. 2002;216(2):229-34.
59. Heinemann M, Susa M, Simnacher U, Marre R, Essig A. Growth of Chlamydia pneumoniae induces cytokine production and expression of CD14 in a human monocytic cell line. Infect Immun. 1996;64(11):4872-5.
60. Shemer-Avni Y, Wallach D, Sarov I. Inhibition of Chlamydia trachomatis growth by recombinant tumor necrosis factor. Infect Immun. 1988;56(9):2503-6.
61. Wahl C, Oswald F, Simnacher U, Weiss S, Marre R, Essig A. Survival of Chlamydia pneumoniae-infected Mono Mac 6 cells is dependent on NF-kappaB binding activity. Infect Immun. 2001;69(11):7039-45.
62. Paland N, Bohme L, Gurumurthy RK, Maurer A, Szczepek AJ, Rudel T. Reduced display of tumor necrosis factor receptor I at the host cell surface supports infection with Chlamydia trachomatis. J Biol Chem. 2008 Mar 7;283(10):6438-48.
63. Shirey KA, Carlin JM. Chlamydiae modulate gamma interferon, interleukin-1 beta, and tumor necrosis factor alpha receptor expression in HeLa cells. Infect Immun. 2006;74(4):2482-6.
64. Kuo CC. Immediate cytotoxicity of Chlamydia trachomatis for mouse peritoneal macrophages. Infect Immun. 1978;20(3):613-8.
65. Kuo CC. Cultures of Chlamydia trachomatis in mouse peritoneal macrophages: factors affecting organism growth. Infect Immun. 1978;20(2):439-45.
66. Wyrick PB, Brownridge EA. Growth of Chlamydia psittaci in macrophages. Infect Immun. 1978;19(3):1054-60.
67. Wyrick PB, Brownridge EA, Ivins BE. Interaction of Chlamydia psittaci with mouse peritoneal macrophages. Infect Immun. 1978;19(3):1061-7.
68. Haranaga S, Yamaguchi H, Ikejima H, Friedman H, Yamamoto Y. Chlamydia pneumoniae infection of alveolar macrophages: a model. J Infect Dis. 2003;187(7):1107-15.
69. Rothfuchs AG, Gigliotti D, Palmblad K, Andersson U, Wigzell H, Rottenberg ME. IFN-alpha beta-dependent, IFN-gamma secretion by bone marrow-derived macrophages controls an intracellular bacterial infection. J Immunol. 2001 Dec 1;167(11):6453-61.
70. Trumstedt C, Eriksson E, Lundberg AM, Yang TB, Yan ZQ, Wigzell H, Rottenberg ME. Role of IRAK4 and IRF3 in the control of intracellular infection with Chlamydia pneumoniae. J Leukoc Biol. 2007;81(6):1591-8.
71. Rothfuchs AG, Trumstedt C, Wigzell H, Rottenberg ME. Intracellular bacterial infection-induced IFN-gamma is critically but not solely dependent on Toll-like receptor 4-myeloid differentiation factor 88-IFN-alpha beta-STAT1 signaling. J Immunol. 2004;172(10):6345-53.
72. Kalayoglu MV, Perkins BN, Byrne GI. Chlamydia pneumoniae-infected monocytes exhibit increased adherence to human aortic endothelial cells. Microbes Infect. 2001;3(12):963-9.
73. Kaul R, Wenman WM. Chlamydia pneumoniae facilitates monocyte adhesion to endothelial and smooth muscle cells. Microb Pathog. 2001;30(3):149-55.
74. May AE, Redecke V, Gruner S, Schmidt R, Massberg S, Miethke T, Ryba B, Prazeres da Costa C, Schömig A, Neumann FJ. Recruitment of Chlamydia pneumoniae-infected macrophages to the carotid artery wall in noninfected, nonatherosclerotic mice. Arterioscler Thromb Vasc Biol. 2003 May 1;23(5): 789-94.
75. Takaoka N, Campbell LA, Lee A, Rosenfeld ME, Kuo CC. Chlamydia pneumoniae infection increases adherence of mouse macrophages to mouse endothelial cells in vitro and to aortas ex vivo. Infect Immun. 2008;76(2):510-4.
76. Azenabor AA, Job G, Adedokun OO. Chlamydia pneumoniae infected macrophages exhibit enhanced plasma membrane fluidity and show increased adherence to endothelial cells. Mol Cell Biochem. 2005;269(1-2):69-84.
77. Hatch GM, McClarty G. C. trachomatis-infection accelerates metabolism of phosphatidylcholine derived from low density lipoprotein but does not affect phosphatidylcholine secretion from hepatocytes. BMC Microbiol. 2004 Feb 17;4:8.
78. Cocchiaro JL, Kumar Y, Fischer ER, Hackstadt T, Valdivia RH. Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc Natl Acad Sci U S A. 2008 Jul 8;105(27):9379-84.
79. Heuer D, Lipinski AR, Machuy N, Karlas A, Wehrens A, Siedler F, Brinkmann V, Meyer TF. Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature. 2009;457 (7230):731-5.
80. MacIntyre A, Abramov R, Hammond CJ, Hudson AP, Arking EJ, Little CS, Appelt DM, Balin BJ. Chlamydia pneumoniae infection promotes the transmigration of monocytes through human brain endothelial cells. J Neurosci Res. 2003;71(5):740-50.
81. Kalayoglu MV, Byrne GI. Induction of macrophage foam cell formation by Chlamydia pneumoniae. J Infect Dis. 1998;177(3):725-9.
82. Kalayoglu MV, Byrne GI. A Chlamydia pneumoniae component that induces macrophage foam cell formation is chlamydial lipopolysaccharide. Infect Immun. 1998;66(11):5067-72.
83. Cao F, Castrillo A, Tontonoz P, Re F, Byrne GI. Chlamydia pneumoniae-induced macrophage foam cell formation is mediated by toll-like receptor 2. Infect Immun. 2007;75(2):753-9.
84. Chen S, Sorrentino R, Shimada K, Bulut Y, Doherty TM, Crother TR, Arditi M. Chlamydia pneumoniae-induced foam cell formation requires MyD88-dependent and -independent signaling and is reciprocally modulated by liver X receptor activation. J Immunol. 2008;181(10):7186-93.
85. He P, Mei C, Cheng B, Liu W, Wang Y, Wan J. Chlamydia pneumoniae induces macrophage-derived foam cell formation by up-regulating acyl-coenzyme A: cholesterol acyltransferase 1. Microbes Infect. 2008;11(2):157-63.
86. Chang TY, Chang CC, Cheng D. Acyl-coenzyme A: cholesterol acyltransferase. Annu Rev Biochem. 1997;66:613-38.
87. Gervassi A, Alderson MR, Suchland R, Maisonneuve JF, Grabstein KH, Probst P. Differential regulation of inflammatory cytokine secretion by human dendritic cells upon Chlamydia trachomatis infection. Infect Immun. 2004;72(12):7231-9.
88. Wittkop U, Krausse-Opatz B, Gust TC, Kirsch T, Hollweg G, Kohler L, Zenke M, Gérard HC, Hudson AP, Zeidler H, Wagner AD. Fate of Chlamydophila pneumoniae in human monocyte-derived dendritic cells: long lasting infection. Microb Pathog. 2006;40(3):101-9.
89. Rey-Ladino J, Jiang X, Gabel BR, Shen C, Brunham RC. Survival of Chlamydia muridarum within dendritic cells. Infect Immun. 2007;75(8): 3707-14.
90. Kaiko GE, Phipps S, Hickey DK, Lam CE, Hansbro PM, Foster PS, Beagley KW. Chlamydia muridarum infection subverts dendritic cell function to promote Th2 immunity and airways hyperreactivity. J Immunol. 2008;180(4):2225-32.
91. Wittkop U, Peppmueller M, Njau F, Leibold W, Klos A, Krausse-Opatz B, Hudson AP, Zeidler H, Haller H, Wagner AD. Transmission of Chlamydophila pneumoniae from dendritic cells to macrophages does not require cell-to-cell contact in vitro. J Microbiol Methods. 2008;72(3):288-95.
92. Kis Z, Treso B, Burian K, Endresz V, Pallinger E, Nagy A, Toth A, Takacs M, Falus A, Gonczol E. Expression of bacterial genes and induction of INF-gamma in human myeloid dendritic cells during persistent infection with Chlamydophila pneumoniae. FEMS Immunol Med Microbiol. 2008;52(3): 324-34.
93. Jiang X, Shen C, Rey-Ladino J, Yu H, Brunham RC. Characterization of murine dendritic cell line JAWS II and primary bone marrow-derived dendritic cells in Chlamydia muridarum antigen presentation and induction of protective immunity. Infect Immun. 2008;76(6):2392-401.
94. Su H, Messer R, Whitmire W, Fischer E, Portis JC, Caldwell HD. Vaccination against chlamydial genital tract infection after immunization with dendritic cells pulsed ex vivo with nonviable Chlamydiae. J Exp Med. 1998 Sep 7;188(5):809-18.
95. Igietseme JU, Ananaba GA, Bolier J, Bowers S, Moore T, Belay T, Eko FO, Lyn D, Black CM. Suppression of endogenous IL-10 gene expression in dendritic cells enhances antigen presentation for specific Th1 induction: potential for cellular vaccine development. J Immunol. 2000;164(8):4212-9.
96. Lu H, Zhong G. Interleukin-12 production is required for chlamydial antigen-pulsed dendritic cells to induce protection against live Chlamydia trachomatis infection. Infect Immun. 1999;67(4):1763-9.
97. Rey-Ladino J, Koochesfahani KM, Zaharik ML, Shen C, Brunham RC. A live and inactivated Chlamydia trachomatis mouse pneumonitis strain induces the maturation of dendritic cells that are phenotypically and immunologically distinct. Infect Immun. 2005;73(3):1568-77.
98. Zaharik ML, Nayar T, White R, Ma C, Vallance BA, Straka N, Jiang X, Rey-Ladino J, Shen C, Brunham RC. Genetic profiling of dendritic cells exposed to live-or ultraviolet-irradiated Chlamydia muridarum reveals marked differences in CXC chemokine profiles. Immunology. 2007;120(2):160-72.
99. Karunakaran KP, Rey-Ladino J, Stoynov N, Berg K, Shen C, Jiang X, Gabel BR, Yu H, Foster LJ, Brunham RC. Immunoproteomic discovery of novel T cell antigens from the obligate intracellular pathogen Chlamydia. J Immunol. 2008;180(4):2459-65.
100. Yu H, Jiang X, Shen C, Karunakaran KP, Brunham RC. Novel Chlamydia muridarum T cell antigens induce protective immunity against lung and genital tract infection in murine models. J Immunol. 2009;182(3):1602-8.
101. Hansbro PM, Beagley KW, Horvat JC, Gibson PG. Role of atypical bacterial infection of the lung in predisposition/protection of asthma. Pharmacol Ther. 2004;101(3):193-210.
102. Horvat JC, Beagley KW, Wade MA, Preston JA, Hansbro NG, Hickey DK, Kaiko GE, Gibson PG, Foster PS, Hansbro PM. Neonatal chlamydial infection induces mixed T-cell responses that drive allergic airway disease. Am J Respir Crit Care Med. 2007;176(6):556-64.
103. Register KB, Morgan PA, Wyrick PB. Interaction between Chlamydia spp. and human polymorphonuclear leukocytes in vitro. Infect Immun. 1986;52(3):664-70.
104. Yong EC, Chi EY, Chen WJ, Kuo CC. Degradation of Chlamydia trachomatis in human polymorphonuclear leukocytes: an ultrastructural study of peroxidase-positive phagolysosomes. Infect Immun. 1986;53(2):427-31.
105. van Zandbergen G, Gieffers J, Kothe H, Rupp J, Bollinger A, Aga E, Klinger M, Brade H, Dalhoff K, Maass M, Solbach W, Laskay T. Chlamydia pneumoniae multiply in neutrophil granulocytes and delay their spontaneous apoptosis. J Immunol. 2004;172(3):1768-76.
106. Rank RG, Whittimore J, Bowlin AK, Dessus-Babus S, Wyrick PB. Chlamydiae and polymorphonuclear leukocytes: unlikely allies in the spread of chlamydial infection. FEMS Immunol Med Microbiol. 2008;54(1):104-13.
107. Martin RJ, Kraft M, Chu HW, Berns EA, Cassell GH. A link between chronic asthma and chronic infection. J Allergy Clin Immunol. 2001;107(4): 595-601.
108. Oksaharju A, Lappalainen J, Tuomainen AM, Pussinen PJ, Puolakkainen M, Kovanen PT, Lindstedt KA. Proatherogenic lung and oral pathogens induce an inflammatory response in human and mouse mast cells. J Cell Mol Med. 2009;13(1):103-13.
109. Fainardi E, Castellazzi M, Seraceni S, Granieri E, Contini C. Under the microscope: focus on Chlamydia pneumoniae infection and multiple sclerosis. Curr Neurovasc Res. 2008;5(1):60-70.
110. Balin BJ, Little CS, Hammond CJ, Appelt DM, Whittum-Hudson JA, Gerard HC, Hudson AP. Chlamydophila pneumoniae and the etiology of late-onset Alzheimer's disease. J Alzheimers Dis. 2008;13(4):371-80.
111. Boelen E, Steinbusch HW, Pronk I, Grauls G, Rennert P, Bailly V, Bruggeman CA, Stassen FR. Inflammatory responses following Chlamydia pneumoniae infection of glial cells. Eur J Neurosci. 2007;25(3):753-60.
112. Boelen E, Steinbusch HW, van der Ven AJ, Grauls G, Bruggeman CA, Stassen FR. Chlamydia pneumoniae infection of brain cells: an in vitro study. Neurobiol Aging. 2007;28(4):524-32.
113. Appelt DM, Roupas MR, Way DS, Bell MG, Albert EV, Hammond CJ, Balin BJ. Inhibition of apoptosis in neuronal cells infected with Chlamydophila (Chlamydia) pneumoniae. BMC Neurosci. 2008;9:13.
114. Ikejima H, Friedman H, Yamamoto Y. Chlamydia pneumoniae infection of microglial cells in vitro: a model of microbial infection for neurological disease. J Med Microbiol. 2006;55(Pt 7):947-52.
115. Bar-Or A, Oliveira EM, Anderson DE, Hafler DA. Molecular pathogenesis of multiple sclerosis. J Neuroimmunol. 1999;100(1-2):252-9.
116. Rosenberg GA. Matrix metalloproteinases in neuroinflammation. Glia. 2002;39(3):279-91.
117. Dreses-Werringloer U, Gerard HC, Whittum-Hudson JA, Hudson AP. Chlamydophila (Chlamydia) pneumoniae infection of human astrocytes and microglia in culture displays an active, rather than a persistent, phenotype. Am J Med Sci. 2006;332(4): 168-74.
118. Blasi F, Boman J, Esposito G, Melissano G, Chiesa R, Cosentini R, Tarsia P, Tshomba Y, Betti M, Alessi M, Morelli N, Allegra L. Chlamydia pneumoniae DNA detection in peripheral blood mononuclear cells is predictive of vascular infection. J Infect Dis. 1999;180(6):2074-6.
119. Sessa R, Di Pietro M, Santino I, del Piano M, Varveri A, Dagianti A, Penco M. Chlamydia pneumoniae infection and atherosclerotic coronary disease. Am Heart J. 1999;137(6):1116-9.
120. Maass M, Jahn J, Gieffers J, Dalhoff K, Katus HA, Solbach W. Detection of Chlamydia pneumoniae within peripheral blood monocytes of patients with unstable angina or myocardial infarction. J Infect Dis. 2000;181 Suppl 3:S449-51.
121. Berger M, Schroder B, Daeschlein G, Schneider W, Busjahn A, Buchwalow I, Luft FC, Haller H. Chlamydia pneumoniae DNA in non-coronary atherosclerotic plaques and circulating leukocytes. J Lab Clin Med. 2000;136(3):194-200.
122. Boman J, Soderberg S, Forsberg J, Birgander LS, Allard A, Persson K, Jidell E, Kumlin U, Juto P, Waldenström A, Wadell G. High prevalence of Chlamydia pneumoniae DNA in peripheral blood mononuclear cells in patients with cardiovascular disease and in middle-aged blood donors. J Infect Dis. 1998;178(1):274-7.
123. Kaul R, Uphoff J, Wiedeman J, Yadlapalli S, Wenman WM. Detection of Chlamydia pneumoniae DNA in CD3+ lymphocytes from healthy blood donors and patients with coronary artery disease. Circulation. 2000;102(19):2341-6.
124. Wong YK, Dawkins KD, Ward ME. Circulating Chlamydia pneumoniae DNA as a predictor of coronary artery disease. J Am Coll Cardiol. 1999;34(5):1435-9.
125. Haranaga S, Yamaguchi H, Leparc GF, Friedman H, Yamamoto Y. Detection of Chlamydia pneumoniae antigenin PBMNCs of healthy blood donors. Transfusion. 2001;41(9):1114-9.
126. Sessa R, Di Pietro M, Schiavoni G, Petrucca A, Cipriani P, Zagaglia C, Nicoletti M, Santino I, del Piano M. Measurement of Chlamydia pneumoniae bacterial load in peripheral blood mononuclear cells may be helpful to assess the state of chlamydial infection in patients with carotid atherosclerotic disease. Atherosclerosis. 2007;195(1):e224-30.
127. Smieja M, Mahony J, Petrich A, Boman J, Chernesky M. Association of circulating Chlamydia pneumoniae DNA with cardiovascular disease: a systematic review. BMC Infect Dis. 2002;2:21.
128. Cirino F, Webley WC, West C, Croteau NL, Andrzejewski C Jr, Stuart ES. Detection of Chlamydia in the peripheral blood cells of normal donors using in vitro culture, immunofluorescence microscopy and flow cytometry techniques. BMC Infect Dis. 2006;6:23.
129. Webley WC, Salva PS, Andrzejewski C, Cirino F, West CA, Tilahun Y, Stuart ES. The bronchial lavage of pediatric patients with asthma contains infectious Chlamydia. Am J Respir Crit Care Med. 2005;171(10):1083-8.
130. Webley WC, Tilahun Y, Lay K, Patel K, Stuart ES, Andrzejewski C, Salva PS. Occurrence of Chlamydia trachomatis and Chlamydia pneumoniae in paediatric respiratory infections. Eur Respir J. 2009;33(2):360-7.
131. Beeckman DS, Vanrompay DC. Zoonotic Chlamydophila psittaci infections from a clinical perspective. Clin Microbiol Infect. 2009;15(1):11-7.
132. Ferreri AJ, Guidoboni M, Ponzoni M, De Conciliis C, Dell'Oro S, Fleischhauer K, Caggiari L, Lettini AA, Dal Cin E, Ieri R, Freschi M, Villa E, Boiocchi M, Dolcetti R. Evidence for an association between Chlamydia psittaci and ocular adnexal lymphomas. J Natl Cancer Inst. 2004;96(8):586-94.
133. Ferreri AJ, Ponzoni M, Guidoboni M, Resti AG, Politi LS, Cortelazzo S, Demeter J, Zallio F, Palmas A, Muti G, Dognini GP, Pasini E, Lettini AA, Sacchetti F, De Conciliis C, Doglioni C, Dolcetti R. Bacteria-eradicating therapy with doxycycline in ocular adnexal MALT lymphoma: a multicenter prospective trial. J Natl Cancer Inst. 2006;98(19):1375-82.
134. Ponzoni M, Ferreri AJ, Guidoboni M, Lettini AA, Cangi MG, Pasini E, Sacchi L, Pecciarini L, Grassi S, Dal Cin E, Stefano R, Magnino S, Dolcetti R, Doglioni C. Chlamydia infection and lymphomas: association beyond ocular adnexal lymphomas highlighted by multiple detection methods. Clin Cancer Res. 2008;14(18):5794-800.
135. Ferreri AJ, Dognini GP, Ponzoni M, Pecciarini L, Cangi MG, Santambrogio G, Resti AG, De Conciliis C, Magnino S, Pasini E, Vicari N, Dolcetti R, Doglioni C. Chlamydia-psittaci-eradicating antibiotic therapy in patients with advanced-stage ocular adnexal MALT lymphoma. Ann Oncol. 2008;19(1):194-5.
136. Ferreri AJ, Dolcetti R, Dognini GP, Malabarba L, Vicari N, Pasini E, Ponzoni M, Cangi MG, Pecciarini L, Resti AG, Doglioni C, Rossini S, Magnino S. Chlamydophila psittaci is viable and infectious in the conjunctiva and peripheral blood of patients with ocular adnexal lymphoma: results of a single-center prospective case-control study. Int J Cancer. 2008;123(5):1089-93.
137. Ferreri AJ, Ponzoni M, Dognini GP, Du MQ, Doglioni C, Radford J, Dolcetti R, Cavalli F. Bacteria-eradicating therapy for ocular adnexal MALT lymphoma: questions for an open international prospective trial. Ann Oncol. 2006;17(11):1721-2.
138. Vargas RL, Fallone E, Felgar RE, Friedberg JW, Arbini AA, Andersen AA, Rothberg PG. Is there an association between ocular adnexal lymphoma and infection with Chlamydia psittaci? The University of Rochester experience. Leuk Res. 2006;30(5):547-51.
139. Matthews JM, Moreno LI, Dennis J, Byrne GE, Jr., Ruiz P, Dubovy SR, Lossos IS. Ocular adnexal lymphoma: no evidence for bacterial DNA associated with lymphoma pathogenesis. Br J Haematol. 2008 May 19 [Epub ahead of print].
140. Decaudin D, Dolcetti R, de Cremoux P, Ponzoni M, Vincent-Salomon A, Doglioni C, Dendale R, Escande MC, Lumbroso-Le Rouic L, Ferreri AJ. Variable association between Chlamydophila psittaci infection and ocular adnexal lymphomas: methodological biases or true geographical variations? Anticancer Drugs. 2008;19(8):761-5.
141. Hadfield TL, Lamy Y, Wear DJ. Demonstration of Chlamydia trachomatis in inguinal lymphadenitis of lymphogranuloma venereum: a light microscopy, electron microscopy and polymerase chain reaction study. Mod Pathol. 1995;8(9):924-9.
142. Kapoor S. Re-emergence of lymphogranuloma venereum. J Eur Acad Dermatol Venereol. 2008;22(4):409-16.
143. Gerard HC, Dreses-Werringloer U, Wildt KS, Deka S, Oszust C, Balin BJ, Frey WH 2nd, Bordayo EZ, Whittum-Hudson JA, Hudson AP. Chlamydophila (Chlamydia) pneumoniae in the Alzheimer's brain. FEMS Immunol Med Microbiol. 2006;48(3):355-66.
144. Dreses-Werringloer U, Bhuiyan M, Zhao Y, Gerard HC, Whittum-Hudson JA, Hudson AP. Initial characterization of Chlamydophila (Chlamydia) pneumoniae cultured from the late-onset Alzheimer brain. Int J Med Microbiol. 2009;299(3):187-201.
145. Little CS, Hammond CJ, MacIntyre A, Balin BJ, Appelt DM. Chlamydia pneumoniae induces Alzheimer-like amyloid plaques in brains of BALB/c mice. Neurobiol Aging. 2004;25(4):419-29.
146. Sriram S, Ljunggren-Rose A, Yao SY, Whetsell WO Jr. Detection of chlamydial bodies and antigens in the central nervous system of patients with multiple sclerosis. J Infect Dis. 2005 Oct 1;192(7):1219-28.
147. Contini C, Cultrera R, Seraceni S, Castellazzi M, Granieri E, Fainardi E. Cerebrospinal fluid molecular demonstration of Chlamydia pneumoniae DNA is associated to clinical and brain magnetic resonance imaging activity in a subset of patients with relapsing-remitting multiple sclerosis. Mult Scler. 2004;10(4):360-9.
148. Dong-Si T, Weber J, Liu YB, Buhmann C, Bauer H, Bendl C, Schnitzler P, Grond-Ginsbach C, Grau AJ. Increased prevalence of and gene transcription by Chlamydia pneumoniae in cerebrospinal fluid of patients with relapsing-remitting multiple sclerosis. J Neurol. 2004;251(5):542-7.
149. Contini C, Seraceni S, Cultrera R, Castellazzi M, Granieri E, Fainardi E. Molecular detection of Parachlamydia-like organisms in cerebrospinal fluid of patients with multiple sclerosis. Mult Scler. 2008;14(4):564-6.
150. Parratt J, Tavendale R, O'Riordan J, Parratt D, Swingler R. Chlamydia pneumoniae-specific serum immune complexes in patients with multiple sclerosis. Mult Scler. 2008;14(3):292-9.
151. Lindsey J, Patel S. PCR for bacterial 16S ribosomal DNA in multiple sclerosis cerebrospinal fluid. Mult Scler. 2008;14(2):147-52.
152. Stratton CW, Wheldon DB. Multiple sclerosis: an infectious syndrome involving Chlamydophila pneumoniae. Trends Microbiol. 2006;14(11):474-9.
153. Bagos PG, Nikolopoulos G, Ioannidis A. Chlamydia pneumoniae infection and the risk of multiple sclerosis: a meta-analysis. Mult Scler. 2006;12(4):397-411.
154. Zeidler H, Kuipers J, Kohler L. Chlamydia-induced arthritis. Curr Opin Rheumatol. 2004;16(4):380-92.
155. Rihl M, Kohler L, Klos A, Zeidler H. Persistent infection of Chlamydia in reactive arthritis. Ann Rheum Dis. 2006;65(3):281-4.
156. Schumacher HR, Jr., Magge S, Cherian PV, Sleckman J, Rothfuss S, Clayburne G, Sieck M. Light and electron microscopic studies on the synovial membrane in Reiter's syndrome. Immunocytochemical identification of chlamydial antigen in patients with early disease. Arthritis Rheum. 1988;31(8):937-46.
157. Hammerschlag MR. The intracellular life of chlamydiae. Semin Pediatr Infect Dis. 2002;13(4):239-48.
158. Schaefer TM, Fahey JV, Wright JA, Wira CR. Migration inhibitory factor secretion by polarized uterine epithelial cells is enhanced in response to the TLR3 agonist poly (I:C). Am J Reprod Immunol. 2005;54(4):193-202.
159. Fahey JV, Schaefer TM, Channon JY, Wira CR. Secretion of cytokines and chemokines by polarized human epithelial cells from the female reproductive tract. Hum Reprod. 2005;20(6):1439-46.
160. Wolf K, Plano GV, Fields KA. A protein secreted by the respiratory pathogen Chlamydia pneumoniae impairs IL-17 signaling via interaction with human Act1. Cell Microbiol. 2009 Jan 21 [Epub ahead of print].
161. Lad SP, Li J, da Silva Correia J, Pan Q, Gadwal S, Ulevitch RJ, Li E. Cleavage of p65/RelA of the NF-kappaB pathway by Chlamydia. Proc Natl Acad Sci U S A. 2007;104(8):2933-8.
162. Le Negrate G, Krieg A, Faustin B, Loeffler M, Godzik A, Krajewski S, Reed JC. ChlaDub1 of Chlamydia trachomatis suppresses NF-kappaB activation and inhibits IkappaBalpha ubiquitination and degradation. Cell Microbiol. 2008;10(9):1879-92.