Identification of immunodominant antigens by probing a whole chlamydia trachomatis open reading frame proteome microarray using sera from immunized mice

Infection and Immunity

Volumn 79, Issue 1, 2011, Pages 246-257

  Cruz Fisher, Maria I ^a   Cheng, Chunmei ^a   Sun, Guifeng ^a   Pal, Sukumar ^a   Teng, Andy ^b   Molina, Douglas M ^b   Kayala, Matthew A ^c   Vigil, Adam ^d   Baldi, Pierre ^c   Felgner, Philip L ^d   Liang, Xiaowu ^b   De La Maza, Luis M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Antigen Discovery Inc   (United States)

^c Irvine   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CPG OLIGODEOXYNUCLEOTIDE; GENOMIC DNA; HEAT SHOCK PROTEIN 60; MONTANIDE ISA 51; OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN B; PLASMID DNA; PROTEIN INCA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; FEMALE; IMMUNIZATION; IMMUNOGENICITY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OPEN READING FRAME; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; SEROLOGY; TH1 CELL; TH2 CELL; TYPE III SECRETION SYSTEM;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CHLAMYDIA TRACHOMATIS; FEMALE; IMMUNODOMINANT EPITOPES; MICE; MICE, INBRED BALB C; OPEN READING FRAMES; PREGNANCY; PROTEIN ARRAY ANALYSIS; PROTEOME;

EID: 78650874308     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00626-10     Document Type: Article

References (69)

1. Baldi, P., and A. D. Long. 2001. A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17:509-519.
2. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
3. Brunham, R. C, and J. Rey-Ladino. 2005. Immunology of Chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat. Rev. Immunol. 5:149-161.
4. Caldwell, H. D., J. Kromhout, and J. Schachter. 1981. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 31:1161-1176.
5. Caldwell, H. D., and J. Schachter. 1982. Antigenic analysis of the major outer membrane protein of Chlamydia spp. Infect. Immun. 35:1024-1031.
6. Centers for Disease Control and Prevention. 2009. Chlamydia screening among sexually active young female enrollees of health plans\United States, 2000-2007. MMWR Morb. Mortal. Wkly. Rep. 58:362-365.
7. Coler, R. N., A. Bhatia, J. F. Maisonneuve, P. Probst, B. Barth, P. Ovendale, H. Fang, M. Alderson, Y. Lobet, J. Cohen, P. Mettens, and S. G. Reed. 2009. Identification and characterization of novel recombinant vaccine antigens for immunization against genital Chlamydia trachomatis. FEMS Immunol. Med. Microbiol. 55:258-270.
8. Davies, D. H., X. Liang, J. E. Hernandez, A. Randall, S. Hirst, Y. Mu, K. M. Romero, T. T. Nguyen, M. Kalantari-Dehaghi, S. Crotty, P. Baldi, L. P. Villarreal, and P. L. Felgner. 2005. Profiling the humoral immune response to infection by using proteome microarrays: high-throughput vaccine and diagnostic antigen discovery. Proc. Natl. Acad. Sci. U.S.A. 102:547-552.
9. Davies, D. H., M. M. McCausland, C. Valdez, D. Huynh, J. E. Hernandez, Y. Mu, S. Hirst, L. Villarreal, P. L. Felgner, and S. Crotty. 2005. Vaccinia virus H3L envelope protein is a major target of neutralizing antibodies in humans and elicits protection against lethal challenge in mice. J. Virol. 79:11724-11733.
10. Davies, D. H., D. M. Molina, J. Wrammert, J. Miller, S. Hirst, Y. Mu, J. Pablo, B. Unal, R. Nakajima-Sasaki, X. Liang, S. Crotty, K. L. Karem, I. K Damon, R. Ahmed, L. Villarreal, and P. L. Felgner. 2007. Proteome-wide analysis of the serological response to vaccinia and smallpox. Proteomics 7:1678-1686.
11. de la Maza, L. M., S. Pal, A. Khamesipour, and E. M. Peterson. 1994. Intravaginal inoculation of mice with the Chlamydia trachomatis mouse pneumonitis biovar results in infertility. Infect. Immun. 62:2094-2097.
12. de la Maza, L. M., and E. M. Peterson. 2002. Vaccines for Chlamydia trachomatis infections. Curr. Opin. Invest. Drugs. 3:980-986.
13. de la Maza, M. A., and L. M. de la Maza. 1995. A new computer model for estimating the impact of vaccination protocols and its application to the study of Chlamydia trachomatis genital infections. Vaccine 13:119-127.
14. Donati, M., V. Sambri, M. Comanducci, K. Di Leo, E. Storni, L. Giacani, G. Ratti, and R. Cevenini. 2003. DNA immunization withpgp3 gene of Chlamydia trachomatis inhibits the spread of chlamydial infection from the lower to the upper genital tract in C3H/HeN mice. Vaccine 21:1089-1093.
15. Felgner, P. L., M. A. Kayala, A. Vigil, C. Burk, R. Nakajima-Sasaki, J. Pablo, D. M. Molina, S. Hirst, J. S. Chew, D. Wang, G. Tan, M. Duffield, R. Yang, J. Neel, N. Chantratita, G. Bancroft, G. Lertmemongkolchai, D. H. Davies, P. Baldi, S. Peacock, and R. W. Titball. 2009. A Burkholderia pseudomallei protein microarray reveals serodiagnostic and cross-reactive antigens. Proc. Natl. Acad. Sci. U.S.A. 106:13499-13504.
16. + T cells recognize an inclusion membrane-associated protein from the vacuolar pathogen Chlamydia trachomatis. Proc. Natl. Acad. Sci. U.S.A. 98:1160-1165.
17. Follmann, F., A. W. Olsen, K. T. Jensen, P. R. Hansen, P. Andersen, and M. Theisen. 2008. Antigenic profiling of a Chlamydia trachomatis gene-expression library. J. Infect. Dis. 197:897-905.
18. Forsbach-Birk, V., U. Simnacher, K. I. Pfrepper, E. Soutschek, A. O. Kiselev, M. F. Lampe, T. Meyer, E. Straube, and A. Essig. 2010. Identification and evaluation of a combination of chlamydial antigens to support the diagnosis of severe and invasive Chlamydia trachomatis infections. Clin. Microbiol. Infect. 16:1237-1244.
19. Gardy, J. L., M. R. Laird, F. Chen, S. Rey, C. J. Walsh, M. Ester, and F. S. Brinkman. 2005. PSORTb v. 2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21:617-623.
20. Grayston, J. T., and S. P. Wang. 1978. The potential for vaccine against infection of the genital tract with Chlamydia trachomatis. Sex. Transm. Dis. 5:73-77.
21. Grayston, T., and S. Wang. 1975. New knowledge of chlamydiae and the diseases they cause. J. Infect. Dis. 132:87-105.
22. Harandi, A. M., and J. Holmgren. 2004. CpG DNA as a potent inducer of mucosal immunity: implications for immunoprophylaxis and immunotherapy of mucosal infections. Curr. Opin. Invest. Drugs 5:141-145.
23. HogenEsch, H. 2002. Mechanisms of stimulation of the immune response by aluminum adjuvants. Vaccine 20(Suppl. 3):S34-S39.
24. Huber, W., A. von Heydebreck, H. Sultmann, A. Poustka, and M. Vingron. 2002. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18(Suppl. 1):S96-S104.
25. Ionescu-Matiu, I., R. C. Kennedy, J. T. Sparrow, A. R. Culwell, Y. Sanchez, J. L. Melnick, and G. R. Dreesman. 1983. Epitopes associated with a synthetic hepatitis B surface antigen peptide. J. Immunol. 130:1947-1952.
26. Kari, L., W. M. Whitmire, D. D. Crane, N. Reveneau, J. H. Carlson, M. M. Goheen, E. M. Peterson, S. Pal, L. M. de la Maza, and H. D. Caldwell. 2009. Chlamydia trachomatis native major outer membrane protein induces partial protection in nonhuman primates: implication for a trachoma transmission- blocking vaccine. J. Immunol. 182:8063-8070.
27. Karunakaran, K. P., J. Rey-Ladino, N. Stoynov, K. Berg, C. Shen, X. Jiang, B. R. Gabel, H. Yu, L. J. Foster, and R. C. Brunham. 2008. Immunopro-teomic discovery of novel T cell antigens from the obligate intracellular pathogen Chlamydia. J. Immunol. 180:2459-2465.
28. LaVerda, D., L. N. Albanese, P. E. Ruther, S. G. Morrison, R. P. Morrison, K A. Ault, and G. I. Byrne. 2000. Seroreactivity to Chlamydia trachomatis Hsp10 correlates with severity of human genital tract disease. Infect. Immun. 68:303-309.
29. Li, Z., Y. Zhong, L. Lei, Y. Wu, S. Wang, and G. Zhong. 2008. Antibodies from women urogenitally infected with C. trachomatis predominantly recognized the plasmid protein Pgp3 in a conformation-dependent manner. BMC Microbiol. 8:90.
30. Lindblad, E. B. 2004. Aluminium adjuvants\in retrospect and prospect. Vaccine 22:3658-3668.
31. McNeilly, C. L., K. W. Beagley, R. J. Moore, V. Haring, P. Timms, and L. M. Hafner. 2007. Expression library immunization confers partial protection against Chlamydia muridarum genital infection. Vaccine 25:2643-2655.
32. + Th1 response during Chlamydia trachomatis infection in mice and humans. Infect. Immun. 77:4168-4176.
33. Miles, A. P., H. A. McClellan, K. M. Rausch, D. Zhu, M. D. Whitmore, S. Singh, L. B. Martin, Y. Wu, B. K. Giersing, A. W. Stowers, C. A. Long, and A. Saul. 2005. Montanide ISA 720 vaccines: quality control of emulsions, stability of formulated antigens, and comparative immunogenicity of vaccine formulations. Vaccine 23:2530-2539.
34. Miller, W. C, C. A. Ford, M. Morris, M. S. Handcock, J. L. Schmitz, M. M. Hobbs, M. S. Cohen, K. M. Harris, and J. R. Udry. 2004. Prevalence of chlamydial and gonococcal infections among young adults in the United States. JAMA 291:2229-2236. (Pubitemid 38608172)
35. Molina, D. M., S. Pal, M. A. Kayala, A. Teng, P. J. Kim, P. Baldi, P. L. Felgner, X. Liang, and L. M. de la Maza. 2010. Identification of immunodominant antigens of Chlamydia trachomatis using proteome microarrays. Vaccine 28:3014-3024.
36. Moller, S., M. D. Croning, and R. Apweiler. 2001. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17:646-653.
37. Morrison, R. P., R. J. Belland, K. Lyng, and H. D. Caldwell. 1989. Chlamydial disease pathogenesis. The 57-kD chlamydial hypersensitivity antigen is a stress response protein. J. Exp. Med. 170:1271-1283.
38. Morrison, R. P., and H. D. Caldwell. 2002. Immunity to murine chlamydial genital infection. Infect. Immun. 70:2741-2751.
39. Morrison, R. P., K. Feilzer, and D. B. Tumas. 1995. Gene knockout mice establish a primary protective role for major histocompatibility complex class II-restricted responses in Chlamydia trachomatis genital tract infection. Infect. Immun. 63:4661-4668.
40. Murthy, A. K., J. P. Chambers, P. A. Meier, G. Zhong, and B. P. Arulanandam 2007. Intranasal vaccination with a secreted chlamydial protein enhances resolution of genital Chlamydia muridarum infection, protects against oviduct pathology, and is highly dependent upon endogenous gamma inter-feron production. Infect. Immun. 75:666-676.
41. Pal, S., H. L. Davis, E. M. Peterson, and L. M. de la Maza. 2002. Immunization with the Chlamydia trachomatis mouse pneumonitis major outer membrane protein by use of CpG oligodeoxynucleotides as an adjuvant induces a protective immune response against an intranasal chlamydial challenge. Infect. Immun. 70:4812-4817.
42. Pal, S., T. J. Fielder, E. M. Peterson, and L. M. de la Maza. 1994. Protection against infertility in a BALB/c mouse salpingitis model by intranasal immunization with the mouse pneumonitis biovar of Chlamydia trachomatis. Infect. Immun. 62:3354-3362.
43. Pal, S., W. Hui, E. M. Peterson, and L. M. de la Maza. 1998. Factors influencing the induction of infertility in a mouse model of Chlamydia tra-chomatis ascending genital tract infection. J. Med. Microbiol. 47:599-605.
44. Pal, S., E. M. Peterson, and L. M. de la Maza. 2004. New murine model for the study of Chlamydia trachomatis genitourinary tract infections in males. Infect. Immun. 72:4210-4216.
45. Pal, S., E. M. Peterson, and L. M. de La Maza. 2000. Role of Nramp1 deletion in Chlamydia infection in mice. Infect. Immun. 68:4831-4833.
46. Pal, S., E. M. Peterson, and L. M. de la Maza. 2005. Vaccination with the Chlamydia trachomatis major outer membrane protein can elicit an immune response as protective as that resulting from inoculation with live bacteria. Infect. Immun. 73:8153-8160.
47. Pal, S., A. P. Schmidt, E. M. Peterson, C. L. Wilson, and L. M. de la Maza. 2006. Role of matrix metalloproteinase-7 in the modulation of a Chlamydia trachomatis infection. Immunology 117:213-219.
48. Pal, S., I. Theodor, E. M. Peterson, and L. M. de la Maza. 1997. Immunization with an acellular vaccine consisting of the outer membrane complex of Chlamydia trachomatis induces protection against a genital challenge. Infect. Immun. 65:3361-3369.
49. Pal, S., I. Theodor, E. M. Peterson, and L. M. de la Maza. 2001. Immunization with the Chlamydia trachomatis mouse pneumonitis major outer membrane protein can elicit a protective immune response against a genital challenge. Infect. Immun. 69:6240-6247.
50. Plotkin, S. A. 2008. Vaccines: correlates of vaccine-induced immunity. Clin. Infect. Dis. 47:401-409.
51. Read, T. D., G. S. Myers, R. C. Brunham, W. C. Nelson, I. T. Paulsen, J. Heidelberg, E. Holtzapple, H. Khouri, N. B. Federova, H. A. Carty, L. A. Umayam, D. H. Haft, J. Peterson, M. J. Beanan, O. White, S. L. Salzberg, R. C. Hsia, G. McClarty, R. G. Rank, P. M. Bavoil, and C. M. Fraser. 2003. Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydi-aceae. Nucleic Acids Res. 31:2134-2147.
52. Sanchez-Campillo, M., L. Bini, M. Comanducci, R. Raggiaschi, B. Marzoc-chi, 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.
53. Schachter, J. 1999. Infection and disease epidemiology, p. 139-170. In R. Stephens (ed.), Chlamydia: intracellular biology, pathogenesis and immunity. ASM Press, Washington, DC.
54. Schachter, J., and C. R. Dawson. 1978. Human chlamydial infections. PSG Publishing Co., Littleton, MA.
55. 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.
56. Stamm, W., and K. Holmes. 1999. Chlamydia trachomatis infections of the adult, p. 407-422. In K. K. Holmes, P. F. Sparling, P.-A. Mardh, et al. (ed.), Sexually transmitted diseases. McGraw-Hill Book Co., New York, NY.
57. + T cell response. J. Immunol. 171:4742-4749.
58. Stephens, R. S., S. Kalman, C. Lammel, J. Fan, R. Marathe, L. Aravind, W. Mitchell, L. Olinger, R. L. Tatusov, Q. Zhao, E. V. Koonin, and R. W. Davis 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754-759.
59. Sun, G., S. Pal, J. Weiland, E. M. Peterson, and L. M. de la Maza. 2009. Protection against an intranasal challenge by vaccines formulated with native and recombinant preparations of the Chlamydia trachomatis major outer membrane protein. Vaccine 27:5020-5025.
60. Suzich, J. A., S. J. Ghim, F. J. Palmer-Hill, W. I. White, J. K. Tamura, J. A. Bell, J. A. Newsome, A. B. Jenson, and R. Schlegel. 1995. Systemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas. Proc. Natl. Acad. Sci. U.S.A. 92:11553-11557.
61. Swenson, C. E., and J. Schachter. 1984. Infertility as a consequence of chlamydial infection of the upper genital tract in female mice. Sex. Transm. Dis. 11:64-67.
62. Tuffrey, M., and D. Taylor-Robinson. 1981. Progesterone as a key factor in the development of a mouse model for genital-tract infection with Chlamydia trachomatis. FEMS Microbiol. Lett. 12:111-115.
63. Vigil, A., D. H. Davies, and P. L. Felgner. 2010. Defining the humoral immune response to infectious agents using high-density protein microar-rays. Future Microbiol. 5:241-251.
64. Vigil, A., R. Ortega, R. Nakajima-Sasaki, J. Pablo, D. M. Molina, C. C. Chao, H. W. Chen, W. M. Ching, and P. L. Felgner. 2010. Genome-wide profiling of humoral immune response to Coxiella burnetii infection by protein mi-croarray. Proteomics 10:2259-2269.
65. Wang, J., L. Chen, F. Chen, X. Zhang, Y. Zhang, J. Baseman, S. Perdue, I. T. Yeh, R. Shain, M. Holland, R. Bailey, D. Mabey, P. Yu, and G. Zhong. 2009. A chlamydial type III-secreted effector protein (Tarp) is predominantly recognized by antibodies from humans infected with Chlamydia trachomatis and induces protective immunity against upper genital tract pathologies in mice. Vaccine 27:2967-2980.
66. Wang, J., Y. Zhang, C. Lu, L. Lei, P. Yu, and G. Zhong. 2010. A genome-wide profiling of the humoral immune response to Chlamydia trachomatis infection reveals vaccine candidate antigens expressed in humans. J. Immunol. 185:1670-1680.
67. Westrom, L., R. Joesoef, G. Reynolds, A. Hagdu, and S. E. Thompson. 1992. Pelvic inflammatory disease and fertility. A cohort study of 1,844 women with laparoscopically verified disease and 657 control women with normal laparoscopic results. Sex. Transm. Dis. 19:185-192.
68. Yu, H., X. Jiang, C. Shen, K. P. Karunakaran, and R. C. Brunham. 2009. Novel Chlamydia muridarum T cell antigens induce protective immunity against lung and genital tract infection in murine models. J. Immunol. 182: 1602-1608.
69. Yu, H., X. Jiang, C. Shen, K. P. Karunakaran, J. Jiang, N. L. Rosin, and R C. Brunham. 2010. Chlamydia muridarum T-cell antigens formulated with the adjuvant DDA/TDB induce immunity against infection that correlates with a high frequency of gamma interferon (IFN-7)/tumor necrosis factor alpha and IFN-7/interleukin-17 double-positive CD4+ T cells. Infect. Im-mun. 78:2272-2282.