Antigen-pulsed bone marrow-derived and pulmonary dendritic cells promote Th2 cell responses and immunopathology in lungs during the pathogenesis of murine mycoplasma pneumonia

Journal of Immunology

Volumn 193, Issue 3, 2014, Pages 1353-1363

  Dobbs, Nicole A ^a   Zhou, Xia ^b   Pulse, Mark ^c   Hodge, Lisa M ^c   Schoeb, Trenton R ^d   Simecka, Jerry W ^c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; INTERLEUKIN 13;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW DERIVED DENDRITIC CELL; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; IMMUNE RESPONSE; IMMUNOPATHOLOGY; INOCULATION; LYMPHOCYTE; MOUSE; MYCOPLASMA PNEUMONIA; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PULMONARY DENDRITIC CELL; TH2 CELL;

ADMINISTRATION, INTRANASAL; ANIMALS; ANTIGENS, BACTERIAL; BONE MARROW CELLS; DENDRITIC CELLS; FEMALE; INTUBATION, INTRATRACHEAL; LUNG; MICE; MICE, INBRED BALB C; MICE, SCID; MYCOPLASMA PULMONIS; PNEUMONIA, MYCOPLASMA; TH2 CELLS;

EID: 84906075965     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301772     Document Type: Article

References (79)

1. Dobbs, N. A., A. N. Odeh, X. Sun, and J. W. Simecka. 2009. The multifaceted role of T cell-mediated immunity in pathogenesis and resistance to mycoplasma respiratory disease. Curr. Trends Immunol. 10: 1-19.
2. Krause, D. C., and D. Taylor-Robinson. 1993. Mycoplasmas which infect humans. In Mycoplasmas: Molecular biology and pathogenesis. J. Maniloff, R. N. McElhaney, L. R. Finch, and J. B. Baseman, eds. American Society of Microbiology, Washington, DC, p. 417-444.
3. Waites, K. B., J. W. Simecka, and D. F. Talkington. 2007. Pathogenesis of Mycoplasma pneumoniae infections:adaptive immunity, innate immunity, cell biology, and virulence factors. In Community-Acquired Pneumonia. N. Suttorp, T. Welte, and R. Marre, eds. Birkhäuser, Basel, Switzerland, p. 183-199.
4. Mogabgab, W. J. 1968. Mycoplasma pneumoniae and adenovirus respiratory illnesses in military and university personnel, 1959-1966. Am. Rev. Respir. Dis. 97: 345-358.
5. Foy, H. M. 1993. Infections caused by Mycoplasma pneumoniae and possible carrier state in different populations of patients. Clin. Infect. Dis. 17(Suppl 1): S37-S46.
6. Foy, H. M., G. E. Kenny, M. K. Cooney, and I. D. Allan. 1979. Long-term epidemiology of infections with Mycoplasma pneumoniae. J. Infect. Dis. 139: 681-687.
7. Gray, G. C., L. B. Duffy, R. J. Paver, S. D. Putnam, R. J. Reynolds, and G. H. Cassell. 1997. Mycoplasma pneumoniae: a frequent cause of pneumonia among U.S. Marines in southern California. Mil. Med. 162: 524-526.
8. Martin, R. J., 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.
9. Simecka, J. W., J. K. Davis, M. K. Davidson, S. E. Ross, C. Stadtlander, and G. H. Cassell. 1992. Mycoplasma diseases of animals. In Mycoplasmas. Molecular Biology and Pathogenesis. J. Maniloff, R. N. McElhaney, L. R. Finch, and J. B. Baseman, eds. American Society for Microbiology, Washington, DC, p. 391-415.
10. Cassell, G. H. 1982. Derrick Edward Award Lecture. The pathogenic potential of mycoplasmas: Mycoplasma pulmonis as a model. Rev. Infect. Dis. 4(Suppl.): S18-S34.
11. Dajani, A. S., W. A. Clyde, Jr., and F. W. Denny. 1965. Experimental infection with Mycoplasma pneumoniae (Eaton's agent). J. Exp. Med. 121: 1071-1086.
12. Cassell, G. H., J. R. Lindsey, R. G. Overcash, and H. J. Baker. 1973. Murine mycoplasma respiratory disease. Ann. N. Y. Acad. Sci. 225: 395-412.
13. Cartner, S. C., J.W. Simecka, J. R. Lindsey, G. H. Cassell, and J. K. Davis. 1995. Chronic respiratory mycoplasmosis in C3H/HeN and C57BL/6N mice: lesion severity and antibody response. Infect. Immun. 63: 4138-4142.
14. Yancey, A. L., H. L. Watson, S. C. Cartner, and J. W. Simecka. 2001. Gender is a major factor in determining the severity of mycoplasma respiratory disease in mice. Infect. Immun. 69: 2865-2871.
15. Evengard, B., K. Sandstedt, G. Bölske, R. Feinstein, I. Riesenfelt-Orn, and C. I. Smith. 1994. Intranasal inoculation of Mycoplasma pulmonis in mice with severe combined immunodeficiency (SCID) causes a wasting disease with grave arthritis. Clin. Exp. Immunol. 98: 388-394.
16. Keystone, E. C., D. Taylor-Robinson, M. F. Osborn, L. Ling, C. Pope, and V. Fornasier. 1980. Effect of T-cell deficiency on the chronicity of arthritis induced in mice by Mycoplasma pulmonis. Infect. Immun. 27: 192-196.
17. Taylor, G., D. Taylor-Robinson, and G. W. Fernald. 1974. Reduction in the severity of Mycoplasma pneumoniae-induced pneumonia in hamsters by immunosuppressive treatment with antithymocyte sera. J. Med. Microbiol. 7: 343-348.
18. Cartner, S. C., J. R. Lindsey, J. Gibbs-Erwin, G. H. Cassell, and J. W. Simecka. 1998. Roles of innate and adaptive immunity in respiratory mycoplasmosis. Infect. Immun. 66: 3485-3491.
19. Jones, H. P., L. Tabor, X. Sun, M. D.Woolard, and J.W. Simecka. 2002. Depletion of CD8+ T cells exacerbates CD4+ Th cell-associated inflammatory lesions during murine mycoplasma respiratory disease. J. Immunol. 168: 3493-3501.
20. Bodhankar, S., X. Sun, M. D. Woolard, and J. W. Simecka. 2010. Interferon g and interleukin 4 have contrasting effects on immunopathology and the development of protective adaptive immunity against mycoplasma respiratory disease. J. Infect. Dis. 202: 39-51.
21. Woolard, M. D., L. M. Hodge, H. P. Jones, T. R. Schoeb, and J. W. Simecka. 2004. The upper and lower respiratory tracts differ in their requirement of IFN-g and IL-4 in controlling respiratory mycoplasma infection and disease. J. Immunol. 172: 6875-6883.
22. Roncarolo, M.-G., M. K. Levings, and C. Traversari. 2001. Differentiation of T regulatory cells by immature dendritic cells. J. Exp. Med. 193: F5-F9.
23. Dhodapkar, M. V., R. M. Steinman, J. Krasovsky, C. Munz, and N. Bhardwaj. 2001. Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J. Exp. Med. 193: 233-238.
24. Bilyk, N., and P. G. Holt. 1995. Cytokine modulation of the immunosuppressive phenotype of pulmonary alveolar macrophage populations. Immunology 86: 231-237.
25. McWilliam, A. S., D. J. Nelson, and P. G. Holt. 1995. The biology of airway dendritic cells. Immunol. Cell Biol. 73: 405-413.
26. Stumbles, P. A., J. A. Thomas, C. L. Pimm, P. T. Lee, T. J. Venaille, S. Proksch, and P. G. Holt. 1998. Resting respiratory tract dendritic cells preferentially stimulate T helper cell type 2 (Th2) responses and require obligatory cytokine signals for induction of Th1 immunity. J. Exp. Med. 188: 2019-2031.
27. Nicod, L. P., M. F. Lipscomb, J. C. Weissler, C. R. Lyons, J. Albertson, and G. B. Toews. 1987. Mononuclear cells in human lung parenchyma. Characterization of a potent accessory cell not obtained by bronchoalveolar lavage. Am. Rev. Respir. Dis. 136: 818-823.
28. Pollard, A. M., and M. F. Lipscomb. 1990. Characterization of murine lung dendritic cells: similarities to Langerhans cells and thymic dendritic cells. J. Exp. Med. 172: 159-167.
29. Masten, B. J., J. L. Yates, A. M. Pollard Koga, and M. F. Lipscomb. 1997. Characterization of accessory molecules in murine lung dendritic cell function: roles for CD80, CD86, CD54, and CD40L. Am. J. Respir. Cell Mol. Biol. 16: 335-342.
30. Masten, B. J., and M. F. Lipscomb. 1999. Comparison of lung dendritic cells and B cells in stimulating naive antigen-specific T cells. J. Immunol. 162: 1310-1317.
31. Simecka, J. W., R. B. Thorp, and G. H. Cassell. 1992. Dendritic cells are present in the alveolar region of lungs from specific pathogen-free rats. Reg. Immunol. 4: 18-24.
32. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
33. Cochand, L., P. Isler, F. Songeon, and L. P. Nicod. 1999. Human lung dendritic cells have an immature phenotype with efficient mannose receptors. Am. J. Respir. Cell Mol. Biol. 21: 547-554.
34. Sun, X., H. P. Jones, N. Dobbs, S. Bodhankar, and J. W. Simecka. 2013. Dendritic cells are the major antigen presenting cells in inflammatory lesions of murine Mycoplasma respiratory disease. PLoS ONE 8: e55984.
35. Hammad, H., C. Duez, O. Fahy, A. Tsicopoulos, C. André, B. Wallaert, S. Lebecque, A. B. Tonnel, and J. Pestel. 2000. Human dendritic cells in the severe combined immunodeficiency mouse model: their potentiating role in the allergic reaction. Lab. Invest. 80: 605-614.
36. Lambrecht, B. N., M. De Veerman, A. J. Coyle, J. C. Gutierrez-Ramos, K. Thielemans, and R. A. Pauwels. 2000. Myeloid dendritic cells induce Th2 responses to inhaled antigen, leading to eosinophilic airway inflammation. J. Clin. Invest. 106: 551-559.
37. Lambrecht, B. N., I. Carro-Muino, K. Vermaelen, and R. A. Pauwels. 1999. Allergen-induced changes in bone-marrow progenitor and airway dendritic cells in sensitized rats. Am. J. Respir. Cell Mol. Biol. 20: 1165-1174.
38. Sung, S., C. E. Rose, and S. M. Fu. 2001. Intratracheal priming with ovalbuminand ovalbumin 323-339 peptide-pulsed dendritic cells induces airway hyperresponsiveness, lung eosinophilia, goblet cell hyperplasia, and inflammation. J. Immunol. 166: 1261-1271.
39. Xiong, X., Y. Meng, X. Wang, Y. Qi, J. Li, C. Duan, and B. Wen. 2012. Mice immunized with bone marrow-derived dendritic cells stimulated with recombinant Coxiella burnetii Com1 and Mip demonstrate enhanced bacterial clearance in association with a Th1 immune response. Vaccine 30: 6809-6815.
40. Cohen, N., R. Margalit, M. Pevsner-Fischer, S. Yona, S. Jung, L. Eisenbach, and I. R. Cohen. 2012. Mouse dendritic cells pulsed with capsular polysaccharide induce resistance to lethal pneumococcal challenge: roles of T cells and B cells. PLoS ONE 7: e39193.
41. Ashley, D. M., B. Faiola, S. Nair, L. P. Hale, D. D. Bigner, and E. Gilboa. 1997. Bone marrow-generated dendritic cells pulsed with tumor extracts or tumor RNA induce antitumor immunity against central nervous system tumors. J. Exp. Med. 186: 1177-1182.
42. Demangel, C., A. G. Bean, E. Martin, C. G. Feng, A. T. Kamath, and W. J. Britton. 1999. Protection against aerosol Mycobacterium tuberculosis infection using Mycobacterium bovis bacillus Calmette Guérin-infected dendritic cells. Eur. J. Immunol. 29: 1972-1979.
43. Flamand, V., T. Sornasse, K. Thielemans, C. Demanet, O. Leo, J. Urbain, and M. Moser. 1993. Vaccination with tumor-antigen-pulsed dendritic cells induces in vivo resistance to a B cell lymphoma. Adv. Exp. Med. Biol. 329: 611-616.
44. Su, H., R. Messer, W. Whitmire, E. Fischer, J. C. Portis, and H. D. Caldwell. 1998. Vaccination against chlamydial genital tract infection after immunization with dendritic cells pulsed ex vivo with nonviable Chlamydiae. J. Exp. Med. 188: 809-818.
45. Geissmann, F., P. Revy, A. Regnault, Y. Lepelletier, M. Dy, N. Brousse, S. Amigorena, O. Hermine, and A. Durandy. 1999. TGF-b1 prevents the noncognate maturation of human dendritic Langerhans cells. J. Immunol. 162: 4567-4575.
46. Faulkner, L., G. Buchan, and M. Baird. 2000. Interleukin-10 does not affect phagocytosis of particulate antigen by bone marrow-derived dendritic cells but does impair antigen presentation. Immunology 99: 523-531.
47. Steinbrink, K., M. Wölfl, H. Jonuleit, J. Knop, and A. H. Enk. 1997. Induction of tolerance by IL-10-treated dendritic cells. J. Immunol. 159: 4772-4780.
48. Sato, M., K. Iwakabe, S. Kimura, and T. Nishimura. 1999. Functional skewing of bone marrow-derived dendritic cells by Th1-or Th2-inducing cytokines. Immunol. Lett. 67: 63-68.
49. Sato, M., K. Iwakabe, A. Ohta, M. Sekimoto, M. Nakui, T. Koda, S. Kimura, and T. Nishimura. 2000. Functional heterogeneity among bone marrow-derived dendritic cells conditioned by Th1-and Th2-biasing cytokines for the generation of allogeneic cytotoxic T lymphocytes. Int. Immunol. 12: 335-342.
50. Davidson, M. K., S. E. Ross, J. R. Lindsey, and G. H. Cassell. 1988. Colony opacity, hemadsorption, hemolysis, and mitogenicity are not associated with virulence of Mycoplasma pulmonis. Infect. Immun. 56: 2169-2173.
51. Simecka, J. W., and G. H. Cassell. 1987. Serum antibody and cellular responses in LEW and F344 rats after immunization with Mycoplasma pulmonis antigens. Infect. Immun. 55: 731-735.
52. Lutz, M. B., N. Kukutsch, A. L. Ogilvie, S. Rössner, F. Koch, N. Romani, and G. Schuler. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223: 77-92.
53. Inaba, K., W. J. Swiggard, R. M. Steinman, N. Romani, G. Schuler, and C. Brinster. 2001. Isolation of dendritic cells. Curr. Protoc. Immunol. Chapter 3: Unit 3.7.doi: 10.1002/0471142735.im0307s25
54. Kruisbeek, A. 1999. Isolation and fractionation of mononuclear cell populations. In Current Protocols in Immunology. J. E. Coligan, A. Kruisbeek, D. Margulies, E. Shevach, and W. Strober, eds. Wiley, New York, p. 3.1.1-3.1.5.
55. Overcash, R. G., J. R. Lindsey, G. H. Cassel, and H. J. Baker. 1976. Enhancement of natural and experimental respiratory mycoplasmosis in rats by hexamethylphosphoramide. Am. J. Pathol. 82: 171-190.
56. Pinson, D. M., T. R. Schoeb, J. R. Lindsey, and J. K. Davis. 1986. Evaluation by scoring and computerized morphometry of lesions of early Mycoplasma pulmonis infection and ammonia exposure in F344/N rats. Vet. Pathol. 23: 550-555.
57. Lappin, M. B., J. M. Weiss, V. Delattre, B. Mai, H. Dittmar, C. Maier, K. Manke, S. Grabbe, S. Martin, and J. C. Simon. 1999. Analysis of mouse dendritic cell migration in vivo upon subcutaneous and intravenous injection. Immunology 98: 181-188.
58. Simecka, J. W. 2005. Immune responses following mycoplasma infection. In Mycoplasmas. Molecular Biology, Pathogenicity and Strategies for Control. A. Blanchard, and G. Browning, eds. Horizon Bioscience: , Norfolk, U.K., p. 485-534.
59. Simecka, J. W. 2003. Contrasting roles of immunity in mycoplasma respiratory disease. In Recent Research Developments in Infection and Immunity. S. G. Pandalai, ed. Transworld Research Network, Kerala, India, p. 203-219.
60. Jones, H. P., and J. W. Simecka. 2003. T lymphocyte responses are critical determinants in the pathogenesis and resistance to mycoplasma respiratory disease. Front. Biosci. 8: d930-d945.
61. Jiang, X., C. Shen, J. Rey-Ladino, H. Yu, and R. C. Brunham. 2008. Characterization of murine dendritic cell line JAWS II and primary bone marrowderived dendritic cells in Chlamydia muridarum antigen presentation and induction of protective immunity. Infect. Immun. 76: 2392-2401.
62. Otsu, S., K. Gotoh, T. Yamashiro, J. Yamagata, K. Shin, T. Fujioka, and A. Nishizono. 2006. Transfer of antigen-pulsed dendritic cells induces specific TCell proliferation and a therapeutic effect against long-term Helicobacter pylori infection in mice. Infect. Immun. 74: 984-993.
63. Huang, F. P., Y. X. Chen, and C. K. To. 2011. Guiding the "misguided": functional conditioning of dendritic cells for the DC-based immunotherapy against tumours. Eur. J. Immunol. 41: 18-25.
64. van Rijt, L. S., and B. N. Lambrecht. 2005. Dendritic cells in asthma: a function beyond sensitization. Clin. Exp. Allergy 35: 1125-1134.
65. Kaiko, G. E., S. Phipps, D. K. Hickey, C. E. Lam, P. M. Hansbro, P. S. Foster, and K.W. Beagley. 2008. Chlamydia muridarum infection subverts dendritic cell function to promote Th2 immunity and airways hyperreactivity. J. Immunol. 180: 2225-2232.
66. Phythian-Adams, A. T., P. C. Cook, R. J. Lundie, L. H. Jones, K. A. Smith, T. A. Barr, K. Hochweller, S. M. Anderton, G. J. Hämmerling, R. M. Maizels, and A. S. MacDonald. 2010. CD11c depletion severely disrupts Th2 induction and development in vivo. J. Exp. Med. 207: 2089-2096.
67. Plantinga, M., M. Guilliams, M. Vanheerswynghels, K. Deswarte, F. Branco-Madeira, W. Toussaint, L. Vanhoutte, K. Neyt, N. Killeen, B. Malissen, et al. 2013. Conventional and monocyte-derived CD11b+ dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 38: 322-335.
68. Maldonado-López, R., T. De Smedt, P. Michel, J. Godfroid, B. Pajak, C. Heirman, K. Thielemans, O. Leo, J. Urbain, and M. Moser. 1999. CD8a+ and CD8a2 subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 189: 587-592.
69. Maldonado-López, R., T. De Smedt, B. Pajak, C. Heirman, K. Thielemans, O. Leo, J. Urbain, C. R. Maliszewski, and M. Moser. 1999. Role of CD8a+ and CD8a2 dendritic cells in the induction of primary immune responses in vivo. J. Leukoc. Biol. 66: 242-246.
70. Hodge, L. M., and J.W. Simecka. 2002. Role of upper and lower respiratory tract immunity in resistance to Mycoplasma respiratory disease. J. Infect. Dis. 186: 290-294.
71. Hopkins, M., B. G. Lees, D. G. Richardson, S. R. Woroniecki, and A. W. Wheeler. 2001. Standardisation of glutaraldehyde-modified tyrosineadsorbed tree pollen vaccines containing the Th1-inducing adjuvant, monophosphoryl lipid A (MPL). Allergol. Immunopathol. (Madr.) 29: 245-254.
72. Moore, A., L. McCarthy, and K. H. Mills. 1999. The adjuvant combination monophosphoryl lipid A and QS21 switches T cell responses induced with a soluble recombinant HIV protein from Th2 to Th1. Vaccine 17: 2517-2527.
73. Puggioni, F., S. R. Durham, and J. N. Francis. 2005. Monophosphoryl lipid A (MPL) promotes allergen-induced immune deviation in favour of Th1 responses. Allergy 60: 678-684.
74. Choi, S. S., E. Chung, and Y. J. Jung. 2010. Newly identified CpG ODNs, M5-30 and M6-395, stimulate mouse immune cells to secrete TNF- A and enhance Th1-mediated immunity. J. Microbiol. 48: 512-517.
75. Ming, F., J. Yang, P. Chu, M. Ma, J. Shi, H. Cai, C. Huang, H. Li, Z. Jiang, H. Wang, et al. 2013. Immunization of aged pigs with attenuated pseudorabies virus vaccine combined with CpG oligodeoxynucleotide restores defective Th1 immune responses. PLoS ONE 8: e65536.
76. Tengvall, S., A. Lundqvist, R. J. Eisenberg, G. H. Cohen, and A. M. Harandi. 2006. Mucosal administration of CpG oligodeoxynucleotide elicits strong CC and CXC chemokine responses in the vagina and serves as a potent Th1-tilting adjuvant for recombinant gD2 protein vaccination against genital herpes. J. Virol. 80: 5283-5291.
77. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449: 419-426.
78. Jiang, H. L., M. L. Kang, J. S. Quan, S. G. Kang, T. Akaike, H. S. Yoo, and C. S. Cho. 2008. The potential of mannosylated chitosan microspheres to target macrophage mannose receptors in an adjuvant-delivery system for intranasal immunization. Biomaterials 29: 1931-1939.
79. Abraham, R., N. Singh, A. Mukhopadhyay, S. K. Basu, V. Bal, and S. Rath. 1995. Modulation of immunogenicity and antigenicity of proteins by maleylation to target scavenger receptors on macrophages. J. Immunol. 154: 1-8.