Calcineurin-Rcan1 interaction contributes to stem cell factor-mediated mast cell activation

Journal of Immunology

Volumn 191, Issue 12, 2013, Pages 5885-5894

  Wu, Zhengli ^a   Li, Yanhong ^a   MacNeil, Adam J ^a   Junkins, Robert D ^a   Berman, Jason N ^a   Lin, Tong Jun ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; EARLY GROWTH RESPONSE FACTOR 1; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; RCAN1 PROTEIN; STEM CELL FACTOR; TRANSCRIPTION FACTOR NFAT; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REPRESSION; HEMATOPOIETIC STEM CELL; HUMAN; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

EID: 84890327702     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301271     Document Type: Article

References (41)

1. Broudy, V. C. 1997. Stem cell factor and hematopoiesis. Blood 90: 1345-1364.
2. Kirshenbaum, A. S., J. P. Goff, T. Semere, B. Foster, L. M. Scott, and D. D. Metcalfe. 1999. Demonstration that human mast cells arise from a progenitor cell population that is CD34(+), c-kit(+), and expresses aminopeptidase N (CD13). Blood 94: 2333-2342.
3. Metcalfe, D. D., D. Baram, and Y. A. Mekori. 1997. Mast cells. Physiol. Rev. 77: 1033-1079.
4. Galli, S. J., K. M. Zsebo, and E. N. Geissler. 1994. The kit ligand, stem cell factor. Adv. Immunol. 55: 1-96.
5. Okayama, Y., and T. Kawakami. 2006. Development, migration, and survival of mast cells. Immunol. Res. 34: 97-115.
6. Rönnstrand, L. 2004. Signal transduction via the stem cell factor receptor/c-Kit. Cell. Mol. Life Sci. 61: 2535-2548.
7. Roskoski, R., Jr. 2005. Signaling by Kit protein-tyrosine kinase - the stem cell factor receptor. Biochem. Biophys. Res. Commun. 337: 1-13.
8. Fukao, T., T. Yamada, M. Tanabe, Y. Terauchi, T. Ota, T. Takayama, T. Asano, T. Takeuchi, T. Kadowaki, J. Hata Ji, and S. Koyasu. 2002. Selective loss of gastrointestinal mast cells and impaired immunity in PI3K-deficient mice. Nat. Immunol. 3: 295-304.
9. Krishnan, S., R. S. Mali, B. Ramdas, E. Sims, P. Ma, J. Ghosh, V. Munugalavadla, P. Hanneman, J. D. Beane, and R. Kapur. 2012. p85b regulatory subunit of class IA PI3 kinase negatively regulates mast cell growth, maturation, and leukemogenesis. Blood 119: 3951-3961.
10. Krishnan, S., R. S. Mali, K. R. Koehler, S. Vemula, A. Chatterjee, J. Ghosh, B. Ramdas, P. Ma, E. Hashino, and R. Kapur. 2012. Class I(A) PI3Kinase regulatory subunit, p85a, mediates mast cell development through regulation of growth and survival related genes. PLoS ONE 7: e28979.
11. O'Laughlin-Bunner, B., N. Radosevic, M. L. Taylor, C. Shivakrupa, C. DeBerry, D. D. Metcalfe, M. Zhou, C. Lowell, and D. Linnekin. 2001. Lyn is required for normal stem cell factor-induced proliferation and chemotaxis of primary hematopoietic cells. Blood 98: 343-350.
12. Kalesnikoff, J., E. J. Rios, C. C. Chen, S. Nakae, B. A. Zabel, E. C. Butcher, M. Tsai, S. Y. Tam, and S. J. Galli. 2006. RabGEF1 regulates stem cell factor/c-Kit-mediated signaling events and biological responses in mast cells. Proc. Natl. Acad. Sci. USA 103: 2659-2664.
13. Iwaki, S., C. Tkaczyk, A. B. Satterthwaite, K. Halcomb, M. A. Beaven, D. D. Metcalfe, and A. M. Gilfillan. 2005. Btk plays a crucial role in the amplification of Fc epsilonRI-mediated mast cell activation by kit. J. Biol. Chem. 280: 40261-40270.
14. Kahl, C. R., and A. R. Means. 2003. Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr. Rev. 24: 719-736.
15. Schulz, R. A., and K. E. Yutzey. 2004. Calcineurin signaling and NFAT activation in cardiovascular and skeletal muscle development. Dev. Biol. 266: 1-16.
16. Hogan, P. G., L. Chen, J. Nardone, and A. Rao. 2003. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17: 2205-2232.
17. Davies, K. J., G. Ermak, B. A. Rothermel, M. Pritchard, J. Heitman, J. Ahnn, F. Henrique-Silva, D. Crawford, S. Canaider, P. Strippoli, et al. 2007. Renaming the DSCR1/Adapt78 gene family as RCAN: regulators of calcineurin. FASEB J. 21: 3023-3028.
18. Vega, R. B., J. Yang, B. A. Rothermel, R. Bassel-Duby, and R. S. Williams. 2002. Multiple domains of MCIP1 contribute to inhibition of calcineurin activity. J. Biol. Chem. 277: 30401-30407.
19. Chan, B., G. Greenan, F. McKeon, and T. Ellenberger. 2005. Identification of a peptide fragment of DSCR1 that competitively inhibits calcineurin activity in vitro and in vivo. Proc. Natl. Acad. Sci. USA 102: 13075-13080.
20. Ryeom, S., R. J. Greenwald, A. H. Sharpe, and F. McKeon. 2003. The threshold pattern of calcineurin-dependent gene expression is altered by loss of the endogenous inhibitor calcipressin. Nat. Immunol. 4: 874-881.
21. Vega, R. B., B. A. Rothermel, C. J. Weinheimer, A. Kovacs, R. H. Naseem, R. Bassel-Duby, R. S.Williams, and E. N. Olson. 2003. Dual roles of modulatory calcineurin-interacting protein 1 in cardiac hypertrophy. Proc. Natl. Acad. Sci. USA 100: 669-674.
22. Fox, D. S., and J. Heitman. 2005. Calcineurin-binding protein Cbp1 directs the specificity of calcineurin-dependent hyphal elongation during mating in Cryptococcus neoformans. Eukaryot. Cell 4: 1526-1538.
23. Sanna, B., E. B. Brandt, R. A. Kaiser, P. Pfluger, S. A.Witt, T. R. Kimball, E. van Rooij, L. J. De Windt, M. E. Rothenberg, M. H. Tschop, et al. 2006. Modulatory calcineurin-interacting proteins 1 and 2 function as calcineurin facilitators in vivo. Proc. Natl. Acad. Sci. USA 103: 7327-7332.
24. Yang, Y. J., W. Chen, A. Edgar, B. Li, J. D. Molkentin, J. N. Berman, and T. J. Lin. 2009. Rcan1 negatively regulates Fc epsilonRI-mediated signaling and mast cell function. J. Exp. Med. 206: 195-207.
25. Yang, Y. J., A. J. Macneil, R. Junkins, S. O. Carrigan, J. T. Tang, N. Forward, D. Hoskin, J. N. Berman, and T. J. Lin. 2011. Regulator of calcineurin 1 (Rcan1) is required for the development of pulmonary eosinophilia in allergic inflammation in mice. Am. J. Pathol. 179: 1199-1210.
26. Dahl, C., H. Saito, H. V. Nielsen, and P. O. Schiøtz. 2002. The establishment of a combined serum-free and serum-supplemented culture method of obtaining functional cord blood-derived human mast cells. J. Immunol. Methods 262: 137-143.
27. Wu, Z., A. J. Macneil, R. Junkins, B. Li, J. N. Berman, and T. J. Lin. 2013. Mast cell Fc åRI- induced early growth response 2 regulates CC chemokine ligand 1-dependent CD4+ T cell migration. J. Immunol. 190: 4500-4507.
28. Yang, F. C., R. Kapur, A. J. King, W. Tao, C. Kim, J. Borneo, R. Breese, M. Marshall, M. C. Dinauer, and D. A. Williams. 2000. Rac2 stimulates Akt activation affecting BAD/Bcl-XL expression while mediating survival and actin function in primary mast cells. Immunity 12: 557-568.
29. Furitsu, T., T. Tsujimura, T. Tono, H. Ikeda, H. Kitayama, U. Koshimizu, H. Sugahara, J. H. Butterfield, L. K. Ashman, Y. Kanayama, et al. 1993. Identification of mutations in the coding sequence of the proto-oncogene c-kit in a human mast cell leukemia cell line causing ligand-independent activation of c-kit product. J. Clin. Invest. 92: 1736-1744.
30. Macian, F. 2005. NFAT proteins: key regulators of T-cell development and function. Nat. Rev. Immunol. 5: 472-484.
31. Marquardt, D. L., and L. L. Walker. 2000. Dependence of mast cell IgE-mediated cytokine production on nuclear factor-kappaB activity. J. Allergy Clin. Immunol. 105: 500-505.
32. Frantz, B., E. C. Nordby, G. Bren, N. Steffan, C. V. Paya, R. L. Kincaid, M. J. Tocci, S. J. O'Keefe, and E. A. O'Neill. 1994. Calcineurin acts in synergy with PMA to inactivate I kappa B/MAD3, an inhibitor of NF-kappa B. EMBO J. 13: 861-870.
33. Kim, Y. S., K. O. Cho, H. J. Lee, S. Y. Kim, Y. Sato, and Y. J. Cho. 2006. Down syndrome candidate region 1 increases the stability of the IkappaBalpha protein: implications for its anti-inflammatory effects. J. Biol. Chem. 281: 39051-39061.
34. Li, B., J. Berman, J. T. Tang, and T. J. Lin. 2007. The early growth response factor-1 is involved in stem cell factor (SCF)-induced interleukin 13 production by mast cells, but is dispensable for SCF-dependent mast cell growth. J. Biol. Chem. 282: 22573-22581.
35. Blume-Jensen, P., L. Rönnstrand, I. Gout, M. D. Waterfield, and C. H. Heldin. 1994. Modulation of Kit/stem cell factor receptor-induced signaling by protein kinase C. J. Biol. Chem. 269: 21793-21802.
36. Blume-Jensen, P., C. Wernstedt, C. H. Heldin, and L. Rönnstrand. 1995. Identification of the major phosphorylation sites for protein kinase C in kit/stem cell factor receptor in vitro and in intact cells. J. Biol. Chem. 270: 14192-14200.
37. Lorenz, U., A. D. Bergemann, H. N. Steinberg, J. G. Flanagan, X. Li, S. J. Galli, and B. G. Neel. 1996. Genetic analysis reveals cell type-specific regulation of receptor tyrosine kinase c-Kit by the protein tyrosine phosphatase SHP1. J. Exp. Med. 184: 1111-1126.
38. De Sepulveda, P., K. Okkenhaug, J. L. Rose, R. G. Hawley, P. Dubreuil, and R. Rottapel. 1999. Socs1 binds to multiple signalling proteins and suppresses steel factor-dependent proliferation. EMBO J. 18: 904-915.
39. Nonami, A., R. Kato, K. Taniguchi, D. Yoshiga, T. Taketomi, S. Fukuyama, M. Harada, A. Sasaki, and A. Yoshimura. 2004. Spred-1 negatively regulates interleukin-3-mediated ERK/mitogen-activated protein (MAP) kinase activation in hematopoietic cells. J. Biol. Chem. 279: 52543-52551.
40. Ishizuka, T., K. Chayama, K. Takeda, E. Hamelmann, N. Terada, G. M. Keller, G. L. Johnson, and E. W. Gelfand. 1999. Mitogen-activated protein kinase activation through Fc epsilon receptor I and stem cell factor receptor is differentially regulated by phosphatidylinositol 3-kinase and calcineurin in mouse bone marrow-derived mast cells. J. Immunol. 162: 2087-2094.
41. Hundley, T. R., A. M. Gilfillan, C. Tkaczyk, M. V. Andrade, D. D. Metcalfe, and M. A. Beaven. 2004. Kit and FcepsilonRI mediate unique and convergent signals for release of inflammatory mediators from human mast cells. Blood 104: 2410-2417.