Rotavirus infection activates dendritic cells from Peyer's patches in adult mice

Journal of Virology

Volumn 84, Issue 4, 2010, Pages 1856-1866

  Lopez Guerrero, Delia V ^a,b   Meza Perez, Selene ^d,e   Ramirez Pliego, Oscar ^a   Santana Calderon, Maria A ^a   Espino Solis, Pavel ^b   Gutierrez Xicotencatl, Lourdes ^c   Flores Romo, Leopoldo ^d   Esquivel Guadarrama, Fernando R ^a  

^a UNIVERSIDAD AUTÓNOMA DEL ESTADO DE MORELOS   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^d DEPARTAMENTO DE FÍSICA   (Mexico)

^e INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; BETA INTERFERON; CD40 ANTIGEN; CD86 ANTIGEN; CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 23P40; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; GENE EXPRESSION; IMMUNE RESPONSE; IN VIVO STUDY; INFECTION CONTROL; INFLAMMATION; INOCULATION; NONHUMAN; PEYER PATCH; PHENOTYPE; PRIORITY JOURNAL; ROTAVIRUS; TIME; VIRUS INFECTION; VIRUS REPLICATION; WILD TYPE;

ANIMALS; ANTIGENS, CD40; ANTIGENS, CD80; ANTIGENS, CD86; BASE SEQUENCE; CELL MOVEMENT; CYTOKINES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; DNA PRIMERS; FEMALE; INFLAMMATION MEDIATORS; MICE; MICE, INBRED BALB C; PEYER'S PATCHES; RNA, MESSENGER; ROTAVIRUS INFECTIONS;

MURINE ROTAVIRUS EDIM; MUS; ROTAVIRUS;

EID: 75449100697     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02640-08     Document Type: Article

References (52)

1. Anjuère, F., C. Luci, M. Lebens, D. Rousseau, C. Hervouet, G. Milon, J. Holmgren, C. Ardavin, and C. Czerkinsky. 2004. In vivo adjuvant-induced mobilization and maturation of gut dendritic cells after oral administration of cholera toxin. J. Immunol. 173:5103-5111.
2. Arias, C. F., M. Lizano, and S. Lopez. 1987. Synthesis in Escherichia coli and immunological characterization of a polypeptide containing the cleavage sites associated with trypsin enhancement of rotavirus SA11 infectivity. J. Gen. Virol. 68:633-642.
3. Barro, M., and J. T. Patton. 2005. Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3. Proc. Natl. Acad. Sci. USA 102:4114-4119.
4. Barro, M., and J. T. Patton. 2007. Rotavirus NSP1 inhibits expression of type I interferon by antagonizing the function of interferon regulatory factors IRF3, IRF5, and IRF7. J. Virol. 81:4473-4481.
5. Berberich, C., J. R. Ramirez-Pineda, C. Hambrecht, G. Alber, Y. A. Skeiky, and H. Moll. 2003. Dendritic cell (DC)-based protection against an intracellular pathogen is dependent upon DC-derived IL-12 and can be induced by molecularly defined antigens. J. Immunol. 170:3171-3179.
6. Blutt, S. E., C. D. Kirkwood, V. Parreno, K. L. Warfield, M. Ciarlet, M. K. Estes, K. Bok, R. F. Bishop, and M. E. Conner. 2003. Rotavirus antigenaemia and viraemia: a common event? Lancet 362:1445-1449.
7. Blutt, S. E., D. O. Matson, S. E. Crawford, M. A. Staat, P. Azimi, B. L. Bennett, P. A. Piedra, and M. E. Conner. 2007. Rotavirus antigenemia in children is associated with viremia. PLoS Med. 4:e121.
8. Blutt, S. E., K. L. Warfield, D. E. Lewis, and M. E. Conner. 2002. Early response to rotavirus infection involves massive B cell activation. J. Immunol. 168:5716-5721.
9. Burns, J. W., A. A. Krishnaney, P. T. Vo, R. V. Rouse, L. J. Anderson, and H. B. Greenberg. 1995. Analyses of homologous rotavirus infection in the mouse model. Virology 207:143-153.
10. Burns, J. W., M. Siadat-Pajouh, A. A. Krishnaney, and H. B. Greenberg. 1996. Protective effect of rotavirus VP6-specific IgA monoclonal antibodies that lack neutralizing activity. Science 272:104-107.
11. Contractor, N., J. Louten, L. Kim, C. A. Biron, and B. L. Kelsall. 2007. Cutting edge: Peyer's patch plasmacytoid dendritic cells (pDCs) produce low levels of type I interferons: possible role for IL-10, TGFbeta, and prostaglandin E2 in conditioning a unique mucosal pDC phenotype. J. Immunol. 179:2690-2694.
12. Cook, D. N., D. M. Prosser, R. Forster, J. Zhang, N. A. Kuklin, S. J. Abbondanzo, X. D. Niu, S. C. Chen, D. J. Manfra, M. T. Wiekowski, L. M. Sullivan, S. R. Smith, H. B. Greenberg, S. K. Narula, M. Lipp, and S. A. Lira. 2000. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 12:495-503.
13. Douagi, I., G. M. McInerney, A. S. Hidmark, V. Miriallis, K. Johansen, L. Svensson, and G. B. Karlsson Hedestam. 2007. Role of interferon regulatory factor 3 in type I interferon responses in rotavirus-infected dendritic cells and fibroblasts. J. Virol. 81:2758-2768.
14. Fleeton, M. N., N. Contractor, F. Leon, J. D. Wetzel, T. S. Dermody, and B. L. Kelsall. 2004. Peyer's patch dendritic cells process viral antigen from apoptotic epithelial cells in the intestine of reovirus-infected mice. J. Exp. Med. 200:235-245.
15. Franco, M. A., N. Feng, and H. B. Greenberg. 1996. Rotavirus immunity in the mouse. Arch. Virol. Suppl. 12:141-152.
16. Franco, M. A., and H. B. Greenberg. 1999. Immunity to rotavirus infection in mice. J. Infect. Dis. 179(Suppl. 3):S466-S469.
17. Franco, M. A., C. Tin, L. S. Rott, J. L. VanCott, J. R. McGhee, and H. B. Greenberg. 1997. Evidence for CD8+ T-cell immunity to murine rotavirus in the absence of perforin, fas, and gamma interferon. J. Virol. 71:479-486.
18. Istrate, C., I. Douagi, A. Charpilienne, G. M. McInerney, A. Hidmark, K. Johansen, M. Larsson, K. E. Magnusson, D. Poncet, L. Svensson, and J. Hinkula. 2007. Bone marrow dendritic cells internalize live RF-81 bovine rotavirus and rotavirus-like particles (RF 2/6-GFP-VLP and RF 8*2/6/7-VLP) but are only activated by live bovine rotavirus. Scand. J. Immunol. 65:494-502.
19. Iwasaki, A. 2007. Mucosal dendritic cells. Annu. Rev. Immunol. 25:381-418.
20. Iwasaki, A., and B. L. Kelsall. 2001. Unique functions of CD11b+, CD8 alpha+, and double-negative Peyer's patch dendritic cells. J. Immunol. 166: 4884-4890.
21. Johansson, C., and B. L. Kelsall. 2005. Phenotype and function of intestinal dendritic cells. Semin. Immunol. 17:284-294.
22. Krüger, T., D. Benke, F. Eitner, A. Lang, M. Wirtz, E. E. Hamilton-Williams, D. Engel, B. Giese, G. Muller-Newen, J. Floege, and C. Kurts. 2004. Identification and functional characterization of dendritic cells in the healthy murine kidney and in experimental glomerulonephritis. J. Am. Soc. Nephrol. 15:613-621.
23. Kuklin, N. A., L. Rott, J. Darling, J. J. Campbell, M. Franco, N. Feng, W. Muller, N. Wagner, J. Altman, E. C. Butcher, and H. B. Greenberg. 2000. Alpha(4)beta(7) independent pathway for CD8(+) T cell-mediated intestinal immunity to rotavirus. J. Clin. Investig. 106:1541-1552.
24. Kushnir, N., N. A. Bos, A. W. Zuercher, S. E. Coffin, C. A. Moser, P. A. Offit, and J. J. Cebra. 2001. B2 but not B1 cells can contribute to CD4+ T-cellmediated clearance of rotavirus in SCID mice. J. Virol. 75:5482-5490.
25. Lien, E., and D. T. Golenbock. 2003. Adjuvants and their signaling pathways: beyond TLRs. Nat. Immunol. 4:1162-1164.
26. López, S., and C. F. Arias. 2004. Multistep entry of rotavirus into cells: a Versaillesque dance. Trends Microbiol. 12:271-278.
27. Matsumoto, M., K. Funami, M. Tanabe, H. Oshiumi, M. Shingai, Y. Seto, A. Yamamoto, and T. Seya. 2003. Subcellular localization of Toll-like receptor 3 in human dendritic cells. J. Immunol. 171:3154-3162.
28. McNeal, M. M., M. N. Rae, and R. L. Ward. 1997. Evidence that resolution of rotavirus infection in mice is due to both CD4 and CD8 cell-dependent activities. J. Virol. 71:8735-8742.
29. Mesa, M. C., L. S. Rodriguez, M. A. Franco, and J. Angel. 2007. Interaction of rotavirus with human peripheral blood mononuclear cells: plasmacytoid dendritic cells play a role in stimulating memory rotavirus specific T cells in vitro. Virology 366:174-184.
30. Narváez, C. F., J. Angel, and M. A. Franco. 2005. Interaction of rotavirus with human myeloid dendritic cells. J. Virol. 79:14526-14535.
31. Niedergang, F., and J. P. Kraehenbuhl. 2000. Much ado about M cells. Trends Cell Biol. 10:137-141.
32. Niedergang, F., and M. N. Kweon. 2005. New trends in antigen uptake in the gut mucosa. Trends Microbiol. 13:485-490.
33. Niess, J. H., and H. C. Reinecker. 2006. Dendritic cells in the recognition of intestinal microbiota. Cell Microbiol. 8:558-564.
34. Niess, J. H., and H. C. Reinecker. 2005. Lamina propria dendritic cells in the physiology and pathology of the gastrointestinal tract. Curr. Opin. Gastroenterol. 21:687-691.
35. Parashar, U. D., C. J. Gibson, J. S. Bresse, and R. I. Glass. 2006. Rotavirus and severe childhood diarrhea. Emerg. Infect. Dis. 12:304-306.
36. Pérez-Vargas, J., P. Isa, S. Lopez, and C. F. Arias. 2006. Rotavirus vaccine: early introduction in Latin America-risks and benefits. Arch. Med. Res. 37:1-10.
37. Platt, A. M., and A. M. Mowat. 2008. Mucosal macrophages and the regulation of immune responses in the intestine. Immunol. Lett. 119:22-31.
38. Ruedl, C., C. Rieser, G. Bock, G. Wick, and H. Wolf. 1996. Phenotypic and functional characterization of CD11c+ dendritic cell population in mouse Peyer's patches. Eur. J. Immunol. 26:1801-1806.
39. Salazar-Gonzalez, R. M., J. H. Niess, D. J. Zammit, R. Ravindran, A. Srinivasan, J. R. Maxwell, T. Stoklasek, R. Yadav, I. R. Williams, X. Gu, B. A. McCormick, M. A. Pazos, A. T. Vella, L. Lefrancois, H. C. Reinecker, and S. J. McSorley. 2006. CCR6-mediated dendritic cell activation of pathogen-specific T cells in Peyer's patches. Immunity 24:623-632.
40. Sato, A., and A. Iwasaki. 2005. Peyer's patch dendritic cells as regulators of mucosal adaptive immunity. Cell Mol. Life Sci. 62:1333-1338.
41. Sestak, K., M. M. McNeal, A. Choi, M. J. Cole, G. Ramesh, X. Alvarez, P. P. Aye, R. P. Bohm, M. Mohamadzadeh, and R. L. Ward. 2004. Defining T-cell-mediated immune responses in rotavirus-infected juvenile rhesus macaques. J. Virol. 78:10258-10264.
42. Sierro, F., B. Dubois, A. Coste, D. Kaiserlian, J. P. Kraehenbuhl, and J. C. Sirard. 2001. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc. Natl. Acad. Sci. USA 98:13722-13727.
43. Steinman, R. M., and H. Hemmi. 2006. Dendritic cells: translating innate to adaptive immunity. Curr. Top. Microbiol. Immunol. 311:17-58.
44. Tailor, P., T. Tamura, and K. Ozato. 2006. IRF family proteins and type I interferon induction in dendritic cells. Cell Res. 16:134-140.
45. Torres-Medina, A. 1984. Effect of rotavirus and/or Escherichia coli infection on the aggregated lymphoid follicles in the small intestine of neonatal gnotobiotic calves. Am. J. Vet. Res. 45:652-660.
46. Trombetta, E. S., and I. Mellman. 2005. Cell biology of antigen processing in vitro and in vivo. Annu. Rev. Immunol. 23:975-1028.
47. van den Berg, T. K., and G. Kraal. 2005. A function for the macrophage F4/80 molecule in tolerance induction. Trends Immunol. 26:506-509.
48. Vancott, J. L., M. M. McNeal, A. H. Choi, and R. L. Ward. 2003. The role of interferons in rotavirus infections and protection. J. Interferon Cytokine Res. 23:163-170.
49. Wallet, M. A., P. Sen, and R. Tisch. 2005. Immunoregulation of dendritic cells. Clin. Med. Res. 3:166-175.
50. Ward, R. L., M. M. McNeal, and J. F. Sheridan. 1990. Development of an adult mouse model for studies on protection against rotavirus. J. Virol. 64:5070-5075.
51. Zhang, W., K. Wen, M. S. Azevedo, A. Gonzalez, L. J. Saif, G. Li, A. E. Yousef, and L. Yuan. 2008. Lactic acid bacterial colonization and human rotavirus infection influence distribution and frequencies of monocytes/macrophages and dendritic cells in neonatal gnotobiotic pigs. Vet. Immunol. Immunopathol. 121:222-231.
52. Zhao, X., A. Sato, C. S. Dela Cruz, M. Linehan, A. Luegering, T. Kucharzik, A. K. Shirakawa, G. Marquez, J. M. Farber, I. Williams, and A. Iwasaki. 2003. CCL9 is secreted by the follicle-associated epithelium and recruits dome region Peyer's patch CD11b+ dendritic cells. J. Immunol. 171:2797-2803.