Immunoproteomic identification and serological responses to novel Chlamydia pneumoniae antigens that are associated with persistent C. pneumoniae infections

Journal of Immunology

Volumn 180, Issue 8, 2008, Pages 5490-5498

  Bunk, Sebastian ^a   Susnea, Iuliana ^a   Rupp, Jan ^b   Summersgill, James T ^c   Maass, Matthias ^d   Stegmann, Werner ^e   Schrattenholz, Andre ^e   Wendel, Albrecht ^a   Przybylski, Michael ^a   Hermann, Corinna ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF LÜBECK   (Germany)

^c University of Louisville School of Medicine   (United States)

^d PARACELSUS MEDICAL UNIVERSITY   (Austria)

^e PROTEOSYS AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CHAPERONIN; ELONGATION FACTOR TU; EPITOPE; OUTER MEMBRANE PROTEIN; PMP6 PROTEIN; PROTEIN; PROTEIN DNAK; RHO FACTOR; RNA POLYMERASE; UNCLASSIFIED DRUG; BACTERIUM ANTIBODY;

ANTIBODY RESPONSE; ARTICLE; CHLAMYDIAL PNEUMONIA; CHLAMYDOPHILA PNEUMONIAE; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; GOLD STANDARD; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOREACTIVITY; IN VITRO STUDY; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; SERODIAGNOSIS; SEROLOGY; SERUM; BLOOD; CHLAMYDIASIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; ISOLATION AND PURIFICATION; MICROBIOLOGY; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BLOTTING, WESTERN; CHLAMYDIA INFECTIONS; CHLAMYDOPHILA PNEUMONIAE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; PROTEOMICS;

EID: 45949086517     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.8.5490     Document Type: Article

References (60)

1. Grayston, J. T., L. A. Campbell, C. C. Kuo, C. H. Mordhorst, P. Saikku, D. H. Thorn, and S. P. Wang. 1990. A new respiratory tract pathogen: Chlamydia pneumoniae strain TWAR. J. Infect. Dis. 161: 618-625.
2. Hammerschlag, M. R. 2002. The intracellular life of chlamydiae. Semin. Pediatr. Infect. Dis. 13: 239-248.
3. Hogan, R. J., S. A. Mathews, S. Mukhopadhyay, J. T. Summers gill, and P. Timms. 2004. Chlamydial persistence: beyond the biphasic paradigm. Infect. Immun. 72: 1843-1855.
4. Wu, L., S. J. Skinner, N. Lambie, J. C. Vuletic, F. Blasi, and P. N. Black. 2000. Immunohistochemical staining for Chlamydia pneumoniae is increased in lung tissue from subjects with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care M Ed. 162: 1148-1151.
5. Martin, R. I, M. Kraft, H. W. Chu, E. A. Berns, and G. H. Cassell. 2001. A link between chronic asthma and chronic infection. J. Allergy Clin. Immunol. 107: 595-601.
6. Miyashita, N., H. Fukano, H. Hara, K. Yoshida, Y. Niki, and T. Matsushima. 2002. Recurrent pneumonia due to persistent Chlamydia pneumoniae infection. Intern. Med. 41: 30-33.
7. Ramirez, J. A. 1996. Isolation of Chlamydia pneumoniae from the coronary artery of a patient with coronary atherosclerosis. The Chlamydia pneumoniae/'Atherosclerosis Study Group. Ann. Intern. Med. 125: 979-982.
8. Maass, M., C. Bartels, S. Kruger, E. Krause, P. M. Engel, and K. Dalhoff. 1998. Endovascular presence of Chlamydia pneumoniae DNA is a generalized phenomenon in atherosclerotic vascular disease. Atherosclerosis 140 (Suppl. 1) : S25-S30.
9. Johnston, S. C, H. Zhang, L. M. Messina, M. T. Lawton, and D. Dean. 2005. Chlamydia pneumoniae burden in carotid arteries is associated with upregulation of plaque interleukin-6 and elevated C-reactive protein in serum. Arterioscler. Thromb. Vasc. Biol. 25: 2648-2653.
10. Kaperonis, E. A., C. D. Liapis, J. D. Kakisis, D. Dimitroulis, V. G. Papavassiliou D. Perrea, and A. G. Kostakis. 2006. Inflammation and Chlamydia pneumoniae infection correlate with the severity of peripheral arterial disease. Eur. J. Vasc. Endovasc. Surg. 31: 509-515.
11. Nystrom-Rosander, C., M. Edvinsson, S. Thelin, E. Hjelm, and G. Friman. 2006. Chlamydophila pneumonia: Specific mRNA in aorta ascendens in patients undergoing coronary artery by-pass grafting. Scand. J. Infect. Dis. 38: 758-763.
12. Blasi, F., D. Legnani, V. M. Lombardo, G. G. Negretto, E. Magliano, R. Pozzoli, F. Chiodo, A. Fasoli, and L. Allegra. 1993. Chlamydia pneumoniae infection in acute exacerbations of COPD. Eur. Respir. J. 6: 19-22.
13. Laurila, A. L., L. Von Hertzen, and P. Saikku. 1997. Chlamydia pneumoniae and chronic lung diseases. Scand J. Infect. Dis. 104 (Suppl.) : 34-36.
14. Hahn, D. L., and R. McDonald. 1998. Can acute Chlamydia pneumoniae respiratory tract infection initiate chronic asthma? Ann. Allergy Asthma Immunol. 81: 339-344.
15. Campbell, L. A., and C. C. Kuo. 2004. Chlamydia pneumoniae-an infectious risk factor for atherosclerosis? Nat. Rev. Micro Biol. 2: 23-32.
16. Moazed, T. C, C. C. Kuo, J. T. Grayston, and L. A. Campbell. 1998. Evidence of systemic dissemination of Chlamydia pneumoniae via macrophages in the mouse. J. Infect. Dis. 177: 1322-1325.
17. Gieffers, J., G. van Zandbergen, J. Rupp, F. Sayk, S. Kruger, S. Ehlers, W. Solbach, and M. Maass. 2004. Phagocytes transmit Chlamydia pneumoniae from the lungs to the vasculature. Eur. Respir. J. 23: 506-510.
18. Boman, J., S. Soderberg, J. Forsberg, L. S. Birgander, A. Allard, K. Persson, E. Jidell, U. Kumlin, P. Juto, A. Waldenstrom, and G. Wadell. 1998. 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. 178: 274-277.
19. Gieffers, J., H. Fullgraf, J. Jahn, M. Klinger, K. Dalhoff, H. A. Katus, W. Solbach, and M. Maass. 2001. Chlamydia pneumoniae infection in circulating human monocytes is refractory to antibiotic treatment. Circulation 103: 351-356.
20. Aso, N., A. Tamura, J. Kadota, and M. Nasu. 2004. Association of peripheral mononuclear cells containing Chlamydia pneumoniae DNA with acute coronary syndrome and stable coronary artery disease in Japanese subjects. Clin. Infect. Dis. 39: 366-372.
21. Saikku, P., M. Leinonen, K. Mattila, M. R. Ekman, M. S. Nieminen, P. H. Makela, J. K. Huttunen, and V. Valtonen. 1988. Serological evidence of an association of a novel Chlamydia, TWAR, with chronic coronary heart disease and acute myocardial infarction. Lancet 2: 983-986.
22. Boman, J., and M. R. Hammerschlag. 2002. Chlamydia pneumoniae and atherosclerosis: critical assessment of diagnostic methods and relevance to treatment studies. Clin. Microbiol. Rev. 15: 1-20.
23. Ieven, M. M., and V. Y. Hoymans. 2005. Involvement of Chlamydia pneumoniae in atherosclerosis: more evidence for lack of evidence. J. Clin. Micro Biol. 43: 19-24.
24. Apfalter, P. 2006. Chlamydia pneumoniae, stroke, and serological associations: anything learned from the atherosclerosis-cardiovascular literature or do we have to start over again? Stroke 37: 756-758.
25. Hermann, C., K. Graf, A. Groh, E. Straube, and T. Hartung. 2002. Comparison of eleven commercial tests for Chlamydia pneumoniae-specific immunoglobulin G in asymptomatic healthy individuals. J. Clin. Micro Biol. 40: 1603-1609.
26. Dowell, S. F., R. W. Peeling, J. Boman, G. M. Carlone, B. S. Fields, J. Guarner, M. R. Hammerschlag, L. A. Jackson, C. C. Kuo, M. Maass, et al. 2001. Standardizing Chlamydia pneumoniae assays: recommendations from the Centers for Disease Control and Prevention (USA) and the Laboratory Centre for Disease Control (Canada). Clin. Infect. Dis. 33: 492-503.
27. Peeling, R. W., S. P. Wang, J. T. Grayston, F. Blasi, J. Boman, A. Clad, H. Freidank, C. A. Gaydos, J. Gnarpe, T. Hagiwara, et al. 2000. Chlamydia pneumoniae serology: interlaboratory variation in microimmunofluorescence assay results. J. Infect. Dis. 181: S426-S429.
28. Maass, M., J. Gieffers, E. Krause, P. M. Engel, C. Bartels, and W. Solbach. 1998. Poor correlation between microimmunofluorescence serology and polymerase chain reaction for detection of vascular Chlamydia pneumoniae infection in coronary artery disease patients. Med. Microbiol. Immunol. 187: 103-106.
29. Blasi, F., J. Boman, G. Esposito, G. Melissano, R. Chiesa, R. Cosentini, P. Tarsia, Y. Tshomba, M. Betti, M. Alessi, et al. 1999. Chlamydia pneumoniae DNA detection in peripheral blood mononuclear cells is predictive of vascular infection. J. Infect. Dis. 180: 2074-2076.
30. Bartels, C., M. Maass, G. Bein, N. Brill, J. F. Bechtel, R. Leyh, and H. H. Sievers. 2000. Association of serology with the endovascular presence of Chlamydia pneumoniae and cytomegalovirus in coronary artery and vein graft disease. Circulation 101: 137-141.
31. Berger, M., B. Schroder, G. Daeschlein, W. Schneider, A. Busjahn, I. Buchwalow, F. C. Luft, and H. Haller. 2000. Chlamydia pneumoniae DNA in non-coronary atherosclerotic plaques and circulating leukocytes. J. Lab. Clin. Med. 136: 194-200.
32. Campbell, L. A., C. C. Kuo, S. P. Wang, and J. T. Grayston. 1990. Serological response to Chlamydia pneumoniae infection. J. Clin. Micro Biol. 28: 1261-1264.
33. Iijima, Y., N. Miyashita, T. Kishimoto, Y. Kanamoto, R. Soejima, and A. Matsumoto. 1994. Characterization of Chlamydia pneumoniae species-specific proteins immuno dominant in humans. J. Clin. Micro Biol. 32: 583-588.
34. Jantos, C. A., S. Heck, R. Roggendorf, M. Sen-Gupta, and J. H. Hegemann. 1997. Antigenic and molecular analyses of different Chlamydia pneumoniae strains. J. Clin. Micro Biol. 35: 620-623.
35. Essig, A., U. Simnacher, M. Susa, and R. Marre. 1999. Analysis of the humoral immune response to Chlamydia pneumoniae by immunoblotting and immunoprecipitation. Clin. Diagn. Lab. Immunol. 6: 819-825.
36. Mygind, P., G. Christiansen, K. Persson, and S. Birkelund. 1998. Analysis of the humoral immune response to Chlamydia outer membrane protein 2. Clin. Diagn. Lab. Immunol. 5: 313-318.
37. Wolf, K., E. Fischer, D. Mead, G. Zhong, R. Peeling, B. Whitmire, and H. D. Caldwell. 2001. Chlamydia pneumoniae major outer membrane protein is a surface-exposed antigen that elicits antibodies primarily directed against conformation-dependent determinants. Infect. Immun. 69: 3082-3091.
38. Klein, M., A. Kotz, K. Bernardo, and M. Kronke. 2003. Detection of Chlamydia pneumoniae-specific antibodies binding to the VD2 and VD3 regions of the major outer membrane protein. J. Clin. Micro Biol. 41: 1957-1962.
39. Mitusch, R., J. Luedemann, W. G. Wood, K. Berger, U. Schminke, M. Suter, C. Kessler, U. John, J. Rupp, M. Kentsch, and M. Maass. 2005. Asymptomatic carotid atherosclerosis is associated with circulating Chlamydia pneumoniae DNA in younger normotensive subjects in a general population survey. Arterioscler. Thromb. Vasc. Biol. 25: 386-391.
40. Neuhoff, V., N. Arold, D. Taube, and W. Ehrhardt. 1988. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9: 255-262.
41. Mortz, E., O. Vorm, M. Mann, and P. Roepstorff. 1994. Identification of proteins in polyacrylamide gels by mass spectrometric peptide mapping combined with database search. Biol. Mass Spectrom. 23: 249-261.
42. Vogt, J. A., C. Hunzinger, K. Schroer, K. Holzer, A. Bauer, A. Schrattenholz, M. A. Cahill, S. Schillo, G. Schwall, W. Stegmann, and G. Albuszies. 2005. Determination of fractional synthesis rates of mouse hepatic proteins via metabolic 13C-labeling, MALDI-TOF MS and analysis of relative isotopologue abundances using average masses. Anal. Chem. 77: 2034-2042.
43. Molestina, R. E., J. B. Klein, R. D. Miller, W. H. Pierce, J. A. Ramirez, and J. T. Summersgill. 2002. Proteomic analysis of differentially expressed Chlamydia pneumonias genes during persistent infection of HEp-2 cells. Infect. Immun. 70: 2976-2981.
44. Vandahl, B. B., S. Birkelund, and G. Christiansen. 2002. Proteome analysis of Chlamydia pneumoniae. Methods Enzymol. 358: 277-288.
45. Shaw, A. C, B. B. Vandahl, M. R. Larsen, P. Roepstorff, K. Gevaert, J. Vandekerckhove, G. Christiansen, and S. Birkelund. 2002. Characterization of a secreted Chlamydia protease. Cell. Micro Biol. 4: 411-424.
46. Wehrl, W., V. Brinkmann, P. R. Jungblut, T. F. Meyer, and A. J. Szczepek. 2004. From the inside out-processing of the Chlamydial autotransporter PmpD and its role in bacterial adhesion and activation of human host cells. Mol. Micro Biol. 51: 319-334.
47. Knudsen, K., A. S. Madsen, P. Mygind, G. Christiansen, and S. Birkelund. 1999. Identification of two novel genes encoding 97- to 99-kilodalton outer membrane proteins of Chlamydia pneumoniae. Infect. Immun. 67: 375-383.
48. Kubo, A., and R. S. Stephens. 2000. Characterization and functional analysis of PorB, a Chlamydia porin and neutralizing target. Mol. Micro Biol. 38: 772-780.
49. Airaksinen, U., T. Penttila, E. Wahlstrom, J. M. Vuola, M. Puolakkainen, and M. Sarvas. 2003. Production of Chlamydia pneumoniae proteins in Bacillus subtilis and their use in characterizing immune responses in the experimental infection model. Clin. Diagn. Lab. Immunol. 10: 367-375.
50. Sanchez-Campillo, M., L. Bini, M. Comanducci, R. Raggiaschi, B. Marzocchi, V. Pallini, and G. Ratti. 1999. Identification of immunoreactive proteins of Chlamydia trachomatis by Western blot analysis of a two-dimensional electrophoresis map with patient sera. Electrophoresis 20: 2269-2279.
51. Sharma, J., Y. Zhong, F. Dong, J. M. Piper, G. Wang, and G. Zhong. 2006. Profiling of human antibody responses to Chlamydia trachomatis urogenital tract infection using microplates arrayed with 156 chlamydial fusion proteins. Infect. Immun. 74: 1490-1499.
52. Crane, D. D., J. H. Carlson, E. R. Fischer, P. Bavoil, R. C. Hsia, C. Tan, C. C. Kuo, and H. D. Caldwell. 2006. Chlamydia trachomatis polymorphic membrane protein D is a species-common pan-neutralizing antigen. Proc. Natl. Acad. Sci. USA 103: 1894-1899.
53. Mukhopadhyay, S., R. D. Miller, E. D. Sullivan, C. Theodoropoulos, S. A. Mathews, P. Timms, and J. T. Summersgill. 2006. Protein expression profiles of Chlamydia pneumoniae in models of persistence versus those of heat shock stress response. Infect. Immun. 74: 3853-3863.
54. Lugert, R., M. Kuhns, T. Polch, and U. Gross. 2004. Expression and localization of type III secretion-related proteins of Chlamydia pneumoniae. Med. Microbiol. Immunol. 193: 163-171.
55. Ouellette, S. P., Y. M. Abdelrahman, R. J. Belland, and G. I. Byrne. 2005. The Chlamydia pneumoniae type III secretion-related lcrH gene clusters are developmentally expressed operons. J. Bacteriol. 187: 7853-7856.
56. Slepenkin, A., V. Motin, L. M. de la Maza, and E. M. Peterson. 2003. Temporal expression of type III secretion genes of Chlamydia pneumoniae. Infect. Immun. 71: 2555-2562.
57. Sessa, R., M. Di Pietro, G. Schiavoni, M. Galdiero, P. Cipriani, S. Romano, C. Zagaglia, I. Santino, S. Faccilongo, and M. Del Piano. 2006. Chlamydia pneumoniae in asymptomatic carotid atherosclerosis. Int. J. Immunopathol. Pharmacol. 19: 111-118.
58. Sessa, R., M. Di Pietro, G. Schiavoni, A. Petrucca, P. Cipriani, C. Zagaglia, M. Nicoletti, I. Santino, and M. Del Piano. 2007. 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 195: e224-e230.
59. Smieja, M., J. Mahony, A. Petrich, J. Boman, and M. Chernesky. 2002. Association of circulating Chlamydia pneumoniae DNA with cardiovascular disease: a systematic review. BMC Infect. Dis. 2: 21.
60. Montigiani, S., F. Falugi, M. Scarselli, O. Finco, R. Petracca, G. Galli, M. Mariani, R. Manetti, M. Agnusdei, R. Cevenini, et al. 2002. Genomic approach for analysis of surface proteins in Chlamydia pneumoniae. Infect. Immun. 70: 368-379.