Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection

Journal of Experimental Medicine

Volumn 203, Issue 7, 2006, Pages 1805-1815

  Khader, Shabaana A ^a   Partida Sanchez, Santiago ^a,c   Bell, Guy ^a   Jelley Gibbs, Dawn M ^a   Swain, Susan ^a   Pearl, John E ^a   Ghilardi, Nico ^b   DeSauvage, Frederic J ^b   Lund, Frances E ^a   Cooper, Andrea M ^a  

^a TRUDEAU INSTITUTE   (United States)

^b GENENTECH INC   (United States)

^c THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; HOMODIMER; INTERLEUKIN 12P40;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; LUNG; LYMPH NODE; MOUSE; MYCOBACTERIOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELLS, CULTURED; DENDRITIC CELLS; INTERLEUKIN-12; INTERLEUKIN-12 SUBUNIT P40; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOBACTERIUM TUBERCULOSIS; PROTEIN SUBUNITS; TUBERCULOSIS, PULMONARY;

EID: 33745812070     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20052545     Document Type: Article

References (52)

1. Flynn, J.L., M.M. Goldstein, K.J. Triebold, J. Sypek, S. Wolf, and B.R. Bloom. 1995. IL-12 increases resistance of BALB/c mice to Mycobacterium tuberculosis infection. J. Immunol. 155:2515-2524.
2. Holscher, C., R. Atkinson, B. Arendse, N. Brown, E. Myburgh, G. Alber, and F. Brombacher. 2001. A protective and agonistic function of IL-12p40 in mycobacterial infection. J. Immunol. 167:6957-6966.
3. Cooper, A.M., A. Kipnis, J. Turner, J. Magram, J. Ferrante, and I.M. Orme. 2002. Mice lacking bioactive IL-12 can generate protective, antigen-specific cellular responses to mycobacterial infection only if the IL-12 p40 subunit is present. J. Immunol. 168:1322-1327.
4. Akahoshi, M., H. Nakashima, K. Miyake, Y. Inoue, S. Shimizu, Y. Tanaka, K. Okada, T. Otsuka, and M. Harada. 2003. Influence of interleukin-12 receptor β1 polymorphisms on tuberculosis. Hum. Genet. 112:237-243.
5. Tso, H.W., Y.L. Lau, C.M. Tam, H.S. Wong, and A.K. Chiang. 2004. Associations between IL-12β1 polymorphisms and tuberculosis in the Hong Kong chinese population. J. Infect. Dis. 190:913-919.
6. Doffinger, R., S. Dupius, C. Picard, C. Fieschi, J. Feinberg, G. Barcenas-Morales, and J.L. Casanova. 2002. Inherited disorders of IL-12 and IFN-γ mediated immunity: a molecular genetics update. Mol. Immunol. 38:903-909.
7. Fieschi, C., M. Bosticardo, L. de Beaucoudrey, S. Boisson-Dupuis, J. Feinberg, O.F. Santos, J. Bustamante, J. Levy, F. Candotti, and J. Casanova. 2004. A novel form of complete IL-12/IL-23 receptor β1-deficiency with cell surface-expressed non-functional receptors. Blood. 104:2095-2101.
8. Sakai, T., M. Matsuoka, M. Aoki, K. Nosaka, and H. Mitsuya. 2001. Missense mutation of the interleukin-12 receptor B1 chain-encoding gene is associated with impaired immunity against Mycobacterium avium complex infection. Blood. 97:2688-2694.
9. Gately, M., L. Renzetti, J. Magram, A. Stern, L. Adorini, U. Gubler, and D. Presky. 1998. The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu. Rev. Immunol. 16:495-521.
10. Oppmann, B., R. Lesley, B. Blom, J. Timans, Y. Xu, B. Hunte, F. Vega, N. Yu, J. Wang, K. Singh, et al. 2000. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity. 13:715-725.
11. Khader, S., J. Pearl, K. Sakamoto, L. Gilmartin, G. Bell, D. Jelley-Gibbs, N. Ghilardi, F. deSauvage, and A. Cooper. 2005. IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-gamma responses if IL-12p70 is available. J. Immunol. 175:788-795.
12. Grohmann, U., M.L. Belladonna, R. Bianchi, C. Orabona, E. Ayroldi, M.C. Fioretti, and P. Puccetti. 1998. IL-12 acts directly on DC to promote nuclear localization of NF-κB and primes DC for IL-12 production. Immunity. 9:315-323.
13. Belladonna, M., J. Renauld, R. Bianchi, C. Vacca, F. Fallarino, C. Orabona, M. Fioretti, U. Grohmann, and P. Puccetti. 2002. IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells. J. Immunol. 168:5448-5454.
14. Russell, T.D., Q. Yan, G. Fan, A.P. Khalifah, D.K. Bishop, S.L. Brody, and M.J. Walter. 2003. IL-12p40 homodimer-dependent macrophage chemotaxis and respiratory viral inflammation are mediated through IL-12 receptor β1. J. Immunol. 171:6866-6874.
15. Grohmann, U., M. Belladonna, C. Vacca, R. Bianchi, F. Fallarino, C. Orabona, M. Fioretti, and P. Puccetti. 2001. Positive regulatory role of IL-12 in macrophages and modulation by IFN-gamma. J. Immunol. 167:221-227.
16. Grohmann, U., C. Orabona, R. Bianchi, M.L. Belladonna, M.C. Fioretti, and P. Puccetti. 2000. IL-12 induces SDS-stable class II αβ dimers in murine dendritic cells. Cytokine. 12:401-404.
17. Jana, M., S. Dasgupta, R.N. Saha, X. Liu, and K. Pahan. 2003. Induction of tumor necrosis factor-alpha (TNF-alpha) by interleukin-12 p40 monomer and homodimer in microglia and macrophages. J. Neurochem. 86:519-528.
18. Pahan, K., F.G. Sheikh, X. Liu, S. Hilger, M. McKinney, and T.M. Petro. 2001. Induction of nitric-oxide synthase and activation of NF-kB by interleukin-12 p40 in microglial cells. J. Biol. Chem. 276:7899-7905.
19. Stumbles, P., J. Upham, and P. Holt. 2003. Airway dendritic cells: coordinators of immunological homeostasis and immunity in the respiratory tract. APMIS. 111:741-755.
20. Lambrecht, B., and H. Hammad. 2003. Taking our breath away: dendritic cells in the pathogenesis of asthma. Nat. Rev. Immunol. 3:994-1003.
21. Vermaelen, K., I. Carro-Muino, B. Lambrecht, and R. Pauwels. 2001. Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J. Exp. Med. 193:51-60.
22. Stumbles, P., J. Thomas, C. Pimm, P. Lee, T. Venaille, S. Proksch, and P. 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.
23. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y.J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767-811.
24. Heinzel, F.P., R.M. Rerko, P. Ling, J. Hakimi, and D.S. Schoenhaut. 1994. Interleukin-12 is produced in vivo during endotoxemia and stimulates synthesis of γ interferon. Infect. Immun. 62:4244-4249.
25. Walter, M., N. Kajiwara, P. Karanja, M. Castro, and M. Holtzman. 2001. Interleukin 12 p40 production by barrier epithelial cells during airway inflammation. J. Exp. Med. 193:339-351.
26. Huaux, F., M. Arras, D. Tomasi, V. Barbarin, M. Delos, J.-P. Coutelier, A. Vink, S.H. Phan, J.-C. Renauld, and D. Lison. 2002. A profibrotic function of IL-12 p40 in experimental pulmonary fibrosis. J. Immunol. 169:2653-2661.
27. Steinman, R., M. Pack, and K. Inaba. 1997. Dendritic cells in the T-cell areas of lymphoid organs. Immunol. Rev. 156:25-37.
28. Vermaelen, K., and R. Pauwels. 2004. Accurate and simple discrimination of mouse pulmonary dendritic cell and macrophage populations by flow cytometry: methodology and new insights. Cytometry. 61:170-177.
29. Mikols, C., L. Yan, J. Norris, T. Russell, A. Khalifah, R. Hachem, M. Chakinala, R. Yusen, M. Castro, E. Kuo, et al. 2006. IL-12 p80 is an innate epithelial cell effector that mediates chronic allograft dysfunction. Am. J. Respir. Crit. Care Med. In press.
30. D'Andrea, A., M. Rengaraju, N.M. Valiante, J. Chehimi, M. Kubin, M. Aste, S.H. Chan, M. Kobayashi, D. Young, E. Nickbarg, et al. 1992. Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells. J. Exp. Med. 176:1387-1398.
31. Gillessen, S., D. Carvajal, P. Ling, F. Podlaski, D. Stremlo, P. Familletti, U. Gubler, D. Presky, A. Stern, and M. Gately. 1995. Mouse interleukin-12 (IL-12) p40 homodimer: a potent IL-12 antagonist. Eur. J. Immunol. 25:200-206.
32. Heinzel, F., A. Hujer, F. Ahmed, and R. Rerko. 1997. In vivo production and function of p40 homodimers. J. Immunol. 158:4381-4388.
33. D'Amico, G., G. Frascaroli, G. Bianchi, P. Transidico, A. Doni, A. Vecchi, S. Sozzani, P. Allavena, and A. Mantovani. 2000. Uncoupling of inflammatory chemokine receptors by IL-10: generation of functional decoys. Nat. Immunol. 1:387-391.
34. Demangel, C., P. Bertolino, and W.J. Britton. 2002. Autocrine IL-10 impairs dendritic cell (DC)-derived immune responses to mycobacterial infection by suppressing DC trafficking to draining lymph nodes and local IL-12 production. Eur. J. Immunol. 32:994-1002.
35. Wang, X., V. Wilkinson, F. Podlaski, C. Wu, A. Stern, D. Presky, and J. Magram. 1999. Characterization of mouse interleukin-12 p40 homodimer binding to the interleukin-12 receptor subunits. Eur. J. Immunol. 29:2007-2013.
36. Presky, D.H., H. Yang, L.J. Minetti, A.O. Chua, N. Nabavi, C.Y. Wu, M.K. Gately, and U. Gubler. 1996. A functional interleukin 12 receptor complex is composed of two β-type cytokine receptor subunits. Proc. Natl. Acad. Sci. USA. 93:14002-14007.
37. Presky, D., L. Minetti, S. Gillessen, V. Wilkinson, C. Wu, U. Gubler, R. Chizzonite, and M. Gately. 1998. Analysis of the multiple interactions between IL-12 and the high affinity IL-12 receptor complex. J. Immunol. 160:2174-2179.
38. Elkins, K., A. Cooper, S. Colombini, S. Cowley, and T. Kieffer. 2002. In vivo clearance of an intracellular bacterium, Francisella tularensis LVS, is dependent on the p40 subunit of interleukin-12 (IL-12) but not on IL-12 p70. Infect. Immun. 70:1936-1948.
39. Decken, K., G. Kohler, K. Palmer-Lehmann, A. Wunderlin, F. Mattner, J. Magram, M. Gately, and G. Alber. 1998. Interleukin-12 is essential for a protective Th1 response in mice infected with Cryptococcus neoformans. Infect. Immun. 66:4994-5000.
40. Lehmann, J., S. Bellmann, C. Werner, R. Schroder, N. Schutze, and G. Alber. 2001. IL-12p40-dependent agonistic effects on the development of protective innate and adaptive immunity against Salmonella enteritidis. J. Immunol. 167:5304-5315.
41. Morelli, A., J. Rubin, G. Erdos, O. Tkacheva, A. Mathers, A. Zahorchak, A. Thomson, L.J. Falo, and A. Larregina. 2005. CD4+ T cell responses elicited by different subsets of human skin migratory dendritic cells. J. Immunol. 175:7905-7915.
42. Fujii, S., K. Liu, C. Smith, A. Bonito, and R. Steinman. 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.
43. Lieberman, L., F. Cardillo, A. Owyang, D. Rennick, D. Cua, R. Kastelein, and C. Hunter. 2004. IL-23 provides a limited mechanism of resistance to acute toxoplasmosis in the absence of IL-12. J. Immunol. 173:1887-1893.
44. Ghilardi, N., N. Kljavin, Q. Chen, S. Lucas, A. Gurney, and F. de Sauvage. 2004. Compromised humoral and delayed-type hypersensitivity responses in IL-23-deficient mice. J. Immunol. 172:2827-2833.
45. Barnden, M.J., J. Allison, W.R. Heath, and F.R. Carbone. 1998. Defective TCR expression in transgenic mice constructed using cDNA based alpha and beta chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76:34-40.
46. Roberts, A., A. Cooper, J. Belisle, J. Turner, M. Gonzalez-Juarerro, and I. Orme. 2002. Murine models of tuberculosis. In Methods in Microbiology. S. Kaufmann and D. Kabelitz, editors. Academic Press, London. 433-462.
47. Andersen, P. 1997. Host responses and antigens involved in protective immunity to Mycobacterium tuberculosis. Scand. J. Immunol. 45:115-131.
48. Winslow, G.M., A.D. Roberts, M.A. Blackman, and D.L. Woodland. 2003. Persistence and turnover of antigen-specific CD4 T cells during chronic tuberculosis infection in the mouse. J. Immunol. 170:2046-2052.
49. Lutz, M.B., N. Kukutsch, A. Ogilvie, S. Rossner, 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.
50. Lambrecht, B., R. Pauwels, and B. Fazekas De St Groth. 2000. Induction of rapid T cell activation, division, and recirculation by intratracheal injection of dendritic cells in a TCR transgenic model. J. Immunol. 164:2937-2946.
51. Bhatt, K., S.P. Hickman, and P. Salgame. 2004. Cutting edge: a new approach to modeling early lung immunity in murine tuberculosis. J. Immunol. 172:2748-2751.
52. Partida-Sanchez, S., S. Goodrich, K. Kusser, N. Oppenheimer, T. Randall, and F. Lund. 2004. Regulation of dendritic cell trafficking by the ADP-ribosyl cyclase CD38: impact on the development of humoral immunity. Immunity. 20:279-291.