Canonical and noncanonical Wnt proteins program dendritic cell responses for tolerance

Journal of Immunology

Volumn 190, Issue 12, 2013, Pages 6126-6134

  Oderup, Cecilia ^a,b   LaJevic, Melissa ^a,b   Butcher, Eugene C ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; ENDOTOXIN; INTERLEUKIN 10; INTERLEUKIN 6; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; WNT PROTEIN; WNT3A PROTEIN; WNT5A PROTEIN;

ANIMAL CELL; ARTICLE; CANONICAL ANALYSIS; CELL MATURATION; CELLULAR IMMUNITY; COMPLEMENT ALTERNATIVE PATHWAY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; IMMUNOLOGICAL TOLERANCE; LIGAND BINDING; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; MICROBIAL VIABILITY; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGEN PRESENTATION; CELL DIFFERENTIATION; CYTOKINES; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNE TOLERANCE; MICE; MICE, INBRED C57BL; PROTEIN ARRAY ANALYSIS; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84879114342     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203002     Document Type: Article

References (53)

1. Medzhitov, R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449: 819-826. (Pubitemid 47598622)
2. Steinman, R. M., D. Hawiger, K. Liu, L. Bonifaz, D. Bonnyay, K. Mahnke, T. Iyoda, J. Ravetch, M. Dhodapkar, K. Inaba, and M. Nussenzweig. 2003. Dendritic cell function in vivo during the steady state: a role in peripheral tolerance. Ann. N. Y. Acad. Sci. 987: 15-25. (Pubitemid 36584003)
3. Fathke, C., L. Wilson, K. Shah, B. Kim, A. Hocking, R. Moon, and F. Isik. 2006. Wnt signaling induces epithelial differentiation during cutaneous wound healing. BMC Cell Biol. 7: 4.
4. Reya, T., and H. Clevers. 2005. Wnt signalling in stem cells and cancer. Nature 434: 843-850. (Pubitemid 40558990)
5. Staal, F. J., T. C. Luis, and M. M. Tiemessen. 2008. WNT signalling in the immune system: WNT is spreading its wings. Nat. Rev. Immunol. 8: 581-593.
6. Zhou, J., P. Cheng, J. I. Youn, M. J. Cotter, and D. I. Gabrilovich. 2009. Notch and wingless signaling cooperate in regulation of dendritic cell differentiation. Immunity 30: 845-859.
7. Blumenthal, A., S. Ehlers, J. Lauber, J. Buer, C. Lange, T. Goldmann, H. Heine, E. Brandt, and N. Reiling. 2006. The Wingless homolog WNT5A and its receptor Frizzled-5 regulate inflammatory responses of human mononuclear cells induced by microbial stimulation. Blood 108: 965-973. (Pubitemid 44154632)
8. Neumann, J., K. Schaale, K. Farhat, T. Endermann, A. J. Ulmer, S. Ehlers, and N. Reiling. 2010. Frizzled1 is a marker of inflammatory macrophages, and its ligand Wnt3a is involved in reprogramming Mycobacterium tuberculosis- infected macrophages. FASEB J. 24: 4599-4612.
9. Pereira, C., D. J. Schaer, E. B. Bachli, M. O. Kurrer, and G. Schoedon. 2008. Wnt5A/CaMKII signaling contributes to the inflammatory response of macrophages and is a target for the antiinflammatory action of activated protein C and interleukin-10. Arterioscler. Thromb. Vasc. Biol. 28: 504-510.
10. Bergenfelz, C., C. Medrek, E. Ekström, K. Jirström, H. Janols, M. Wullt, A. Bredberg, and K. Leandersson. 2012. Wnt5a induces a tolerogenic phenotype of macrophages in sepsis and breast cancer patients. J. Immunol. 188: 5448-5458.
11. Manicassamy, S., B. Reizis, R. Ravindran, H. Nakaya, R. M. Salazar-Gonzalez, Y. C. Wang, and B. Pulendran. 2010. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 329: 849-853.
12. Jiang, A., O. Bloom, S. Ono, W. Cui, J. Unternaehrer, S. Jiang, J. A. Whitney, J. Connolly, J. Banchereau, and I. Mellman. 2007. Disruption of E-cadherin-mediated adhesion induces a functionally distinct pathway of dendritic cell maturation. Immunity 27: 610-624. (Pubitemid 47615505)
13. Vander Lugt, B., Z. T. Beck, R. C. Fuhlbrigge, N. Hacohen, J. J. Campbell, and M. Boes. 2011. TGF-β suppresses β-catenin-dependent tolerogenic activation program in dendritic cells. PLoS ONE 6: e20099.
14. Halleskog, C., J. P. Dijksterhuis, M. B. Kilander, J. Becerril-Ortega, J. C. Villaescusa, E. Lindgren, E. Arenas, and G. Schulte. 2012. Heterotrimeric G protein-dependent WNT-5A signaling to ERK1/2 mediates distinct aspects of microglia proinflammatory transformation. J. Neuroinflammation 9: 111.
15. Gordon, M. D., M. S. Dionne, D. S. Schneider, and R. Nusse. 2005. WntD is a feedback inhibitor of Dorsal/NF-kappaB in Drosophila development and immunity. Nature 437: 746-749. (Pubitemid 41486544)
16. Mach, N., S. Gillessen, S. B. Wilson, C. Sheehan, M. Mihm, and G. Dranoff. 2000. Differences in dendritic cells stimulated in vivo by tumors engineered to secrete granulocyte-macrophage colony-stimulating factor or Flt3-ligand. Cancer Res. 60: 3239-3246. (Pubitemid 30407923)
17. Gilliet, M., A. Boonstra, C. Paturel, S. Antonenko, X. L. Xu, G. Trinchieri, A. O'Garra, and Y. J. Liu. 2002. The development of murine plasmacytoid dendritic cell precursors is differentially regulated by FLT3-ligand and granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 195: 953-958. (Pubitemid 34286765)
18. Cheadle, C., M. P. Vawter, W. J. Freed, and K. G. Becker. 2003. Analysis of microarray data using Z score transformation. J. Mol. Diagn. 5: 73-81. (Pubitemid 36553428)
19. Miller, J. C., B. D. Brown, T. Shay, E. L. Gautier, V. Jojic, A. Cohain, G. Pandey, M. Leboeuf, K. G. Elpek, J. Helft, D. Hashimoto, et al. 2012. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13: 888-899.
20. Gabrilovich, D. I., H. L. Chen, K. R. Girgis, H. T. Cunningham, G. M. Meny, S. Nadaf, D. Kavanaugh, and D. P. Carbone. 1996. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat. Med. 2: 1096-1103. (Pubitemid 26338628)
21. Ziogas, A. C., N. G. Gavalas, M. Tsiatas, O. Tsitsilonis, E. Politi, E. Terpos, A. Rodolakis, G. Vlahos, N. Thomakos, D. Haidopoulos, et al. 2012. VEGF directly suppresses activation of T cells from ovarian cancer patients and healthy individuals via VEGF receptor Type 2. Int. J. Cancer 130: 857-864.
22. Li, B., A. S. Lalani, T. C. Harding, B. Luan, K. Koprivnikar, G. Huan Tu, R. Prell, M. J. VanRoey, A. D. Simmons, and K. Jooss. 2006. Vascular endothelial growth factor blockade reduces intratumoral regulatory T cells and enhances the efficacy of a GM-CSF-secreting cancer immunotherapy. Clin. Cancer Res. 12: 6808-6816. (Pubitemid 44876851)
23. Annacker, O., J. L. Coombes, V. Malmstrom, H. H. Uhlig, T. Bourne, B. Johansson-Lindbom, W. W. Agace, C. M. Parker, and F. Powrie. 2005. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J. Exp. Med. 202: 1051-1061. (Pubitemid 41464499)
24. van Amerongen, R., and R. Nusse. 2009. Towards an integrated view of Wnt signaling in development. Development 136: 3205-3214.
25. Nemeth, M. J., L. Topol, S. M. Anderson, Y. Yang, and D. M. Bodine. 2007. Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation. Proc. Natl. Acad. Sci. USA 104: 15436-15441. (Pubitemid 47502935)
26. MacLeod, R. J., M. Hayes, and I. Pacheco. 2007. Wnt5a secretion stimulated by the extracellular calcium-sensing receptor inhibits defective Wnt signaling in colon cancer cells. Am. J. Physiol. Gastrointest. Liver Physiol. 293: G403-G411. (Pubitemid 47105201)
27. Carthy, J. M., F. S. Garmaroudi, Z. Luo, and B. M. McManus. 2011. Wnt3a induces myofibroblast differentiation by upregulating TGF-β signaling through SMAD2 in a β-catenin-dependent manner. PLoS ONE 6: e19809.
28. Martin, M., K. Rehani, R. S. Jope, and S. M. Michalek. 2005. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6: 777-784. (Pubitemid 43090463)
29. Notani, D., K. P. Gottimukkala, R. S. Jayani, A. S. Limaye, M. V. Damle, S. Mehta, P. K. Purbey, J. Joseph, and S. Galande. 2010. Global regulator SATB1 recruits beta-catenin and regulates T(H)2 differentiation in Wnt-dependent manner. PLoS Biol. 8: e1000296.
30. Sanjabi, S., L. A. Zenewicz, M. Kamanaka, and R. A. Flavell. 2009. Anti-inflammatory and pro-inflammatory roles of TGF-beta, IL-10, and IL-22 in immunity and autoimmunity. Curr. Opin. Pharmacol. 9: 447-453.
31. Madsen, K. L., S. A. Lewis, M. M. Tavernini, J. Hibbard, and R. N. Fedorak. 1997. Interleukin 10 prevents cytokine-induced disruption of T84 monolayer barrier integrity and limits chloride secretion. Gastroenterology 113: 151-159. (Pubitemid 27281769)
32. Coffman, R. L., D. A. Lebman, and B. Shrader. 1989. Transforming growth factor beta specifically enhances IgA production by lipopolysaccharidestimulated murine B lymphocytes. J. Exp. Med. 170: 1039-1044. (Pubitemid 19226686)
33. Sonoda, E., R. Matsumoto, Y. Hitoshi, T. Ishii, M. Sugimoto, S. Araki, A. Tominaga, N. Yamaguchi, and K. Takatsu. 1989. Transforming growth factor beta induces IgA production and acts additively with interleukin 5 for IgA production. J. Exp. Med. 170: 1415-1420. (Pubitemid 19250703)
34. Zheng, S. G., J. D. Gray, K. Ohtsuka, S. Yamagiwa, and D. A. Horwitz. 2002. Generation ex vivo of TGF-beta-producing regulatory T cells from CD4+CD25-precursors. J. Immunol. 169: 4183-4189. (Pubitemid 35178188)
35. Chen, W., W. Jin, N. Hardegen, K. J. Lei, L. Li, N. Marinos, G. McGrady, and S. M. Wahl. 2003. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886. (Pubitemid 38032120)
36. Tokuda, H., S. Adachi, R. Matsushima-Nishiwaki, K. Kato, H. Natsume, T. Otsuka, and O. Kozawa. 2011. Enhancement of basic fibroblast growth factor-stimulated VEGF synthesis by Wnt3a in osteoblasts. Int. J. Mol. Med. 27: 859-864.
37. Zhou, T., Y. Hu, Y. Chen, K. K. Zhou, B. Zhang, G. Gao, and J. X. Ma. 2010. The pathogenic role of the canonical Wnt pathway in age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 51: 4371-4379.
38. Sato, T., J. H. van Es, H. J. Snippert, D. E. Stange, R. G. Vries, M. van den Born, N. Barker, N. F. Shroyer, M. van de Wetering, and H. Clevers. 2011. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469: 415-418.
39. Gregorieff, A., D. Pinto, H. Begthel, O. Destrée, M. Kielman, and H. Clevers. 2005. Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology 129: 626-638. (Pubitemid 41096648)
40. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
41. Li, Q., and I. M. Verma. 2002. NF-kappaB regulation in the immune system. Nat. Rev. Immunol. 2: 725-734.
42. Kaneko, T., Y. Saito, T. Kotani, H. Okazawa, H. Iwamura, M. Sato-Hashimoto, Y. Kanazawa, S. Takahashi, K. Hiromura, S. Kusakari, et al. 2012. Dendritic cell-specific ablation of the protein tyrosine phosphatase Shp1 promotes Th1 cell differentiation and induces autoimmunity. J. Immunol. 188: 5397-5407.
43. Shinohara, H., A. Inoue, N. Toyama-Sorimachi, Y. Nagai, T. Yasuda, H. Suzuki, R. Horai, Y. Iwakura, T. Yamamoto, H. Karasuyama, et al. 2005. Dok-1 and Dok-2 are negative regulators of lipopolysaccharide-induced signaling. J. Exp. Med. 201: 333-339. (Pubitemid 40229408)
44. Martin, M., R. E. Schifferle, N. Cuesta, S. N. Vogel, J. Katz, and S. M. Michalek. 2003. Role of the phosphatidylinositol 3 kinase-Akt pathway in the regulation of IL-10 and IL-12 by Porphyromonas gingivalis lipopolysaccharide. J. Immunol. 171: 717-725. (Pubitemid 36871381)
45. Alvarez, Y., C. Municio, S. Alonso, M. Sánchez Crespo, and N. Fernández. 2009. The induction of IL-10 by zymosan in dendritic cells depends on CREB activation by the coactivators CREB-binding protein and TORC2 and autocrine PGE2. J. Immunol. 183: 1471-1479.
46. Sudan, R., N. Srivastava, S. P. Pandey, S. Majumdar, and B. Saha. 2012. Reciprocal regulation of protein kinase C isoforms results in differential cellular responsiveness. J. Immunol. 188: 2328-2337.
47. Hack, K., L. Reilly, C. Proby, C. Fleming, I. Leigh, and J. Foerster. 2012. Wnt5a inhibits the CpG oligodeoxynucleotide-triggered activation of human plasmacytoid dendritic cells. Clin. Exp. Dermatol. 37: 557-561.
48. Valencia, J., C. Hernández-López, V. G. Martínez, L. Hidalgo, A. G. Zapata, A. Vicente, A. Varas, and R. Sacedón. 2011. Wnt5a skews dendritic cell differentiation to an unconventional phenotype with tolerogenic features. J. Immunol. 187: 4129-4139.
49. Nanbara, H., N. Wara-aswapati, T. Nagasawa, Y. Yoshida, R. Yashiro, Y. Bando, H. Kobayashi, J. Khongcharoensuk, D. Hormdee, W. Pitiphat, et al. 2012. Modulation of Wnt5a expression by periodontopathic bacteria. PLoS ONE 7: e34434.
50. Sen, M., K. Lauterbach, H. El-Gabalawy, G. S. Firestein, M. Corr, and D. A. Carson. 2000. Expression and function of wingless and frizzled homologs in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 97: 2791-2796. (Pubitemid 30159250)
51. Christman, M. A., II, D. J. Goetz, E. Dickerson, K. D. McCall, C. J. Lewis, F. Benencia, M. J. Silver, L. D. Kohn, and R. Malgor. 2008. Wnt5a is expressed in murine and human atherosclerotic lesions. Am. J. Physiol. Heart Circ. Physiol. 294: H2864-H2870.
52. Gudjonsson, J. E., A. Johnston, S. W. Stoll, M. B. Riblett, X. Xing, J. J. Kochkodan, J. Ding, R. P. Nair, A. Aphale, J. J. Voorhees, and J. T. Elder. 2010. Evidence for altered Wnt signaling in psoriatic skin. J. Invest. Dermatol. 130: 1849-1859.
53. You, J., A. V. Nguyen, C. G. Albers, F. Lin, and R. F. Holcombe. 2008. Wnt pathway-related gene expression in inflammatory bowel disease. Dig. Dis. Sci. 53: 1013-1019. (Pubitemid 351379836)