Regulation and dysregulation of innate immunity by NFAT signaling downstream of pattern recognition receptors (PRRs)

European Journal of Immunology

Volumn 42, Issue 8, 2012, Pages 1924-1931

  Zanoni, Ivan ^a   Granucci, Francesca ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Dectin 1; Dendritic cells; LPS; Macrophages; Neutrophils; NFAT

Indexed keywords

BETA GLUCAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; LIPOPOLYSACCHARIDE; PATTERN RECOGNITION RECEPTOR; TRANSCRIPTION FACTOR NFAT;

ADAPTIVE IMMUNITY; BONE MARROW CELL; DENDRITIC CELL; GRANULOCYTE; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INFLAMMATION; INNATE IMMUNITY; LYMPHOCYTE; MACROPHAGE; MAST CELL; MICROORGANISM; NEUTROPHIL; PRIORITY JOURNAL; REVIEW; TISSUE INJURY; VERTEBRATE;

ANIMALS; BETA-GLUCANS; DENDRITIC CELLS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGES; MAST CELLS; NEUTROPHILS; NFATC TRANSCRIPTION FACTORS; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION;

EID: 84864749527     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242580     Document Type: Review

References (56)

1. Medzhitov, R., Origin and physiological roles of inflammation. Nature 2008. 454: 428-435.
2. Sorci, G. and Faivre, B., Inflammation and oxidative stress in vertebrate host-parasite systems. Philos. Trans. R Soc. Lond. B Biol. Sci. 2009. 364: 71-83.
3. Muller, M. R. and Rao, A., NFAT, immunity and cancer: a transcription factor comes of age. Nat. Rev. Immunol. 2010. 10: 645-656.
4. Liu, Z., Lee, J., Krummey, S., Lu, W., Cai, H. and Lenardo, M. J., The kinase LRRK2 is a regulator of the transcription factor NFAT that modulates the severity of inflammatory bowel disease. Nat. Immunol. 2011. 12: 1063-1070.
5. Graef, I. A., Gastier, J. M., Francke, U. and Crabtree, G. R., Evolutionary relationships among Rel domains indicate functional diversification by recombination. Proc. Natl. Acad. Sci. USA 2001. 98: 5740-5745.
6. Shaw, J. P., Utz, P. J., Durand, D. B., Toole, J. J., Emmel, E. A. and Crabtree, G. R., Identification of a putative regulator of early T cell activation genes. Science 1988. 241: 202-205.
7. Wu, H., Peisley, A., Graef, I. A. and Crabtree, G. R., NFAT signaling and the invention of vertebrates. Trends Cell Biol. 2007. 17: 251-260.
8. Beals, C. R., Sheridan, C. M., Turck, C. W., Gardner, P. and Crabtree, G. R., Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 1997. 275: 1930-1934.
9. Arron, J. R., Winslow, M. M., Polleri, A., Chang, C. P., Wu, H., Gao, X., Neilson, J. R. et al., NFAT dysregulation by increased dosage of DSCR1 and DYRK1A on chromosome 21. Nature 2006. 441: 595-600.
10. Lopez-Rodriguez, C., Aramburu, J., Rakeman, A. S. and Rao, A., NFAT5, a constitutively nuclear NFAT protein that does not cooperate with Fos and Jun. Proc. Natl. Acad. Sci. USA 1999. 96: 7214-7219.
11. Buxade, M., Lunazzi, G., Minguillon, J., Iborra, S., Berga-Bolanos, R., Del Val, M., Aramburu, J. et al., Gene expression induced by Toll-like receptors in macrophages requires the transcription factor NFAT5. J. Exp. Med. 2012. 209: 379-393.
12. Goodridge, H. S., Simmons, R. M. and Underhill, D. M., Dectin-1 stimulation by Candida albicans yeast or zymosan triggers NFAT activation in macrophages and dendritic cells. J. Immunol. 2007. 178: 3107-3115.
13. Ariizumi, K., Shen, G. L., Shikano, S., Xu, S., Ritter 3rd, R., Kumamoto, T., Edelbaum, D. et al., Identification of a novel, dendritic cell-associated molecule, dectin-1, by subtractive cDNA cloning. J. Biol. Chem. 2000. 275: 20157-20167.
14. Slack, E. C., Robinson, M. J., Hernanz-Falcon, P., Brown, G. D., Williams, D. L., Schweighoffer, E., Tybulewicz V. L. et al., Syk-dependent ERK activation regulates IL-2 and IL-10 production by DC stimulated with zymosan. Eur. J. Immunol. 2007. 37: 1600-1612.
15. Underhill, D. M., Rossnagle, E., Lowell, C. A. and Simmons, R. M., Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production. Blood 2005. 106: 2543-2550.
16. Rogers, N. C., Slack, E. C., Edwards, A. D., Nolte, M. A., Schulz, O., Schweighoffer, E., Williams, D. L. et al., Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 2005. 22: 507-517.
17. Tassi, I., Cella, M., Castro, I., Gilfillan, S., Khan, W. N. and Colonna, M., Requirement of phospholipase C-gamma2 (PLCgamma2) for Dectin-1-induced antigen presentation and induction of TH1/TH17 polarization. Eur. J. Immunol. 2009. 39: 1369-1378.
18. Mourao-Sa, D., Robinson, M. J., Zelenay, S., Sancho, D., Chakravarty, P., Larsen, R., Plantinga, M. et al., CLEC-2 signaling via Syk in myeloid cells can regulate inflammatory responses. Eur. J. Immunol. 2011. 41: 3040-3053.
19. Gross, O., Gewies, A., Finger, K., Schafer, M., Sparwasser, T., Peschel, C., Forster, I. et al., Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature 2006. 442: 651-656.
20. Zanoni, I., Ostuni, R., Capuano, G., Collini, M., Caccia, M., Ronchi, A. E., Rocchetti, M. et al., CD14 regulates the dendritic cell life cycle after LPS exposure through NFAT activation. Nature 2009. 460: 264-268.
21. Suzuki, K. G., Fujiwara, T. K., Sanematsu, F., Iino, R., Edidin, M. and Kusumi, A., GPI-anchored receptor clusters transiently recruit Lyn and G alpha for temporary cluster immobilization and Lyn activation: single-molecule tracking study 1. J. Cell Biol. 2007. 177: 717-730.
22. Zanoni, I., Ostuni, R., Marek, L. R., Barresi, S., Barbalat, R., Barton, G. M., Granucci, F. et al., CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 2011. 147: 868-880.
23. Zanoni, I., Bodio, C., Broggi, A., Ostuni, R., Caccia, M., Collini, M., Venkatesh, A. et al., Similarities and differences of innate immune responses elicited by smooth and rough LPS. Immunol. Lett. 2012. 142: 41-47.
24. Itano, A. A., McSorley, S. J., Reinhardt, R. L., Ehst, B. D., Ingulli, E., Rudensky, A. Y. and Jenkins, M. K., Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 2003. 19: 47-57.
25. Klechevsky, E., Kato, H. and Sponaas, A. M., Dendritic cells star in Vancouver. J. Exp. Med. 2005. 202: 5-10.
26. Allenspach, E. J., Lemos, M. P., Porrett, P. M., Turka, L. A. and Laufer, T. M., Migratory and lymphoid-resident dendritic cells cooperate to efficiently prime naive CD4 T cells. Immunity 2008. 29: 795-806.
27. Legler, D. F., Bruckner, M., Uetz-von Allmen, E. and Krause, P., Prostaglandin E2 at new glance: novel insights in functional diversity offer therapeutic chances. Int. J. Biochem. Cell Biol. 2010. 42: 198-201.
28. Zanoni, I., Ostuni, R., Barresi, S., Gioia, M. D., Broggi, A., Costa, B., Marzi, R. et al., CD14 and NFAT mediate lipopolysaccharide-induced skin edema formation in mice. J. Clin. Invest. 2012. 122: 1747-1757.
29. Chen, F., Liu, Z., Wu, W., Rozo, C., Bowdridge, S., Millman, A., Van Rooijen, N. et al., An essential role for TH2-type responses in limiting acute tissue damage during experimental helminth infection. Nat. Med. 2012. 18: 260-266.
30. Chen, M., Wang, Y. H., Wang, Y., Huang, L., Sandoval, H., Liu, Y. J. and Wang, J., Dendritic cell apoptosis in the maintenance of immune tolerance. Science 2006. 311: 1160-1164.
31. Stranges, P. B., Watson, J., Cooper, C. J., Choisy-Rossi, C. M., Stonebraker, A. C., Beighton, R. A., Hartig, H. et al., Elimination of antigen-presenting cells and autoreactive T cells by Fas contributes to prevention of autoimmunity. Immunity 2007. 26: 629-641.
32. Greenblatt, M. B., Aliprantis, A., Hu, B. and Glimcher, L. H., Calcineurin regulates innate antifungal immunity in neutrophils. J. Exp. Med. 2010. 207: 923-931.
33. Hofer, S., Rescigno, M., Granucci, F., Citterio, S., Francolini, M. and Ricciardi-Castagnoli, P., Differential activation of NF-kappa B subunits in dendritic cells in response to Gram-negative bacteria and to lipopolysaccharide. Microbes Infect. 2001. 3: 259-265.
34. Kaisho, T. and Tanaka, T., Turning NF-kappaB and IRFs on and off in DC. Trends Immunol. 2008. 29: 329-336.
35. Wuest, S. C., Edwan, J. H., Martin, J. F., Han, S., Perry, J. S., Cartagena, C. M., Matsuura, E. et al., A role for interleukin-2 trans-presentation in dendritic cell-mediated T cell activation in humans, as revealed by daclizumab therapy. Nat. Med. 2011. 17: 604-609.
36. Granucci, F., Vizzardelli, C., Pavelka, N., Feau, S., Persico, M., Virzi, E., Rescigno, M. et al., Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat. Immunol. 2001. 2: 882-888.
37. Hamilton-Williams, E. E., Martinez, X., Clark, J., Howlett, S., Hunter, K. M., Rainbow, D. B., Wen, L. et al., Expression of diabetes-associated genes by dendritic cells and CD4 T cells drives the loss of tolerance in nonobese diabetic mice. J. Immunol. 2009. 183: 1533-1541.
38. Sgouroudis, E., Kornete, M. and Piccirillo, C. A., IL-2 production by dendritic cells promotes Foxp3(+) regulatory T-cell expansion in autoimmune-resistant NOD congenic mice. Autoimmunity 2010. 44: 406-414.
39. Bugeon, L., Gardner, L. M., Rose, A., Gentle, M. and Dallman, M. J., Cutting edge: notch signaling induces a distinct cytokine profile in dendritic cells that supports T cell-mediated regulation and IL-2-dependent IL-17 production. J. Immunol. 2008. 181: 8189-8193.
40. Nagamachi, M., Sakata, D., Kabashima, K., Furuyashiki, T., Murata, T., Segi-Nishida, E., Soontrapa, K. et al., Facilitation of Th1-mediated immune response by prostaglandin E receptor EP1. J. Exp. Med. 2007. 204: 2865-2874.
41. Harizi, H. and Gualde, N., The impact of eicosanoids on the crosstalk between innate and adaptive immunity: the key roles of dendritic cells. Tissue Antigens 2005. 65: 507-514.
42. Betz, M. and Fox, B. S., Prostaglandin E2 inhibits production of Th1 lymphokines but not of Th2 lymphokines. J. Immunol. 1991. 146: 108-113.
43. Granucci, F., Zanoni, I., Pavelka, N., Van Dommelen, S. L., Andoniou, C. E., Belardelli, F., Degli Esposti M. A. et al., A contribution of mouse dendritic cell-derived IL-2 for NK cell activation. J. Exp. Med. 2004. 200: 287-295.
44. Fujii, S., Shimizu, K., Kronenberg, M. and Steinman, R. M., Prolonged IFN-gamma-producing NKT response induced with alpha-galactosylceramide-loaded DCs. Nat. Immunol. 2002. 3: 867-874.
45. Martin-Fontecha, A., Thomsen, L. L., Brett, S., Gerard, C., Lipp, M., Lanzavecchia, A. and Sallusto, F., Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 2004. 5: 1260-1265.
46. Zanoni, I., Foti, M., Ricciardi-Castagnoli, P. and Granucci, F., TLR-dependent activation stimuli associated with Th1 responses confer NK cell stimulatory capacity to mouse dendritic cells. J. Immunol. 2005. 175: 286-292.
47. Ito, T., Liu, Y. J. and Arima, K., Cellular and molecular mechanisms of TSLP function in human allergic disorders - TSLP programs the Th2 code in dendritic cells. Allergol. Int. 2012. 61: 35-43.
48. Barrett, N. A., Rahman, O. M., Fernandez, J. M., Parsons, M. W., Xing, W., Austen, K. F. and Kanaoka, Y., Dectin-2 mediates Th2 immunity through the generation of cysteinyl leukotrienes. J. Exp. Med. 2011. 208: 593-604.
49. Nhu, Q. M., Shirey, K. A., Pennini, M. E., Stiltz, J. and Vogel, S. N., Proteinase-activated receptor 2 activation promotes an anti-inflammatory and alternatively activated phenotype in LPS-stimulated murine macrophages. Innate Immun. 2012. 18: 193-203.
50. Park, M. K., Cho, M. K., Kang, S. A., Park, H. K., Kim, Y. S., Kim, K. U., Ahn, S. C. et al., Protease-activated receptor 2 is involved in Th2 responses against Trichinella spiralis infection. Korean J. Parasitol. 2011. 49: 235-243.
51. Minematsu, H., Shin, M. J., Celil Aydemir, A. B., Kim, K. O., Nizami, S. A., Chung, G. J. and Lee, F. Y., Nuclear presence of nuclear factor of activated T cells (NFAT) c3 and c4 is required for Toll-like receptor-activated innate inflammatory response of monocytes/macrophages. Cell Signal 2011. 23: 1785-1793.
52. Yarilina, A., Xu, K., Chen, J. and Ivashkiv, L. B., TNF activates calcium-nuclear factor of activated T cells (NFAT)c1 signaling pathways in human macrophages. Proc. Natl. Acad. Sci. USA 2011. 108: 1573-1578.
53. Willingham, A. T., Orth, A. P., Batalov, S., Peters, E. C., Wen, B. G., Aza-Blanc, P., Hogenesch, J. B. et al., A strategy for probing the function of noncoding RNAs finds a repressor of NFAT. Science 2005. 309: 1570-1573.
54. Barrett, J. C., Hansoul, S., Nicolae, D. L., Cho, J. H., Duerr, R. H., Rioux, J. D., Brant, S. R. et al., Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat. Genet. 2008. 40: 955-962.
55. West, A. B., Moore, D. J., Biskup, S., Bugayenko, A., Smith, W. W., Ross, C. A., Dawson, V. L. et al., Parkinson's disease-associated mutations in leucine-rich repeat kinase 2 augment kinase activity. Proc. Natl. Acad. Sci. USA 2005. 102: 16842-16847.
56. Graef, I. A., Chen, F. and Crabtree, G. R., NFAT signaling in vertebrate development. Curr. Opin. Genet. Dev. 2001. 11: 505-512.