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Swiprosin-1 Regulates Cytokine Expression of Human Mast Cell Line HMC-1 through Actin Remodeling

  • Ramesh, T.P. (Department of Life Science, Gwangju Institute of Science and Technology) ;
  • Kim, Young-Dae (Department of Life Science, Gwangju Institute of Science and Technology) ;
  • Kwon, Min-Sung (Department of Life Science, Gwangju Institute of Science and Technology) ;
  • Jun, Chang-Duk (Department of Life Science, Gwangju Institute of Science and Technology) ;
  • Kim, Sang-Wook (Department of Internal Medicine, Chonbuk National University College of Medicine)
  • Received : 2009.12.09
  • Accepted : 2009.12.21
  • Published : 2009.12.31

Abstract

Background: Swiprosin-1 was identified in human CD8+ lymphocytes, mature B cells and non-lymphonoid tissue. We have recently reported that swiprosin-1 is expressed in mast cells and up-regulated in both in vitro and in vivo. Methods: The expression of cytokines and swiprosin-1 were determined by by real time PCR and conventional PCR. Pharmacological inhibitors were treated to investigate potential mechanism of swiprosin-1 in mast cell activation. Actin content was evaluated by confocal microscopy and flow cytometry. Results: The swiprosin-1 augmented PMA/A23187-induced expression of cytokines and release of histamine. However, knock-down of swiprosin-1 showed only a modest effect on PMA/A23187-induced cytokine expression, suggesting that swiprosin-1 has gain-of-function characteristics. Swiprosin-1 was found in microvilli-like membrane protrusions and highly co-localized with F-actin. Importantly, either disruption of actin by cytochalasin B or inhibition of PI3 kinase, an enzyme involved in actin remodeling, by wortmannin blocked cytokine expression only in swiprosin-1-overexpressing cells. Conclusion: These results suggest that swiprosin-1 modulates mast cell activation potentially through actin regulation.

Keywords

References

  1. Vuadens F, Rufer N, Kress A, Corthesy P, Schneider P, Tissot JD: Identification of swiprosin 1 in human lymphocytes. Proteomics 4;2216-2220, 2004 https://doi.org/10.1002/pmic.200300779
  2. Avramidou A, Kroczek C, Lang C, Schuh W, Jack HM, Mielenz D: The novel adaptor protein Swiprosin-1 enhances BCR signals and contributes to BCR-induced apoptosis. Cell Death Differ 14;1936-1947, 2007 https://doi.org/10.1038/sj.cdd.4402206
  3. Thylur RP, Kim YD, Kwon MS, Oh HM, Kwon HK, Kim SH, Im SH, Chun JS, Park ZY, Jun CD: Swiprosin-1 is expressed in mast cells and up-regulated through the protein kinase C beta I/eta pathway. J Cell Biochem 108;705-715, 2009 https://doi.org/10.1002/jcb.22307
  4. Mielenz D, Vettermann C, Hampel M, Lang C, Avramidou A, Karas M, Jack HM: Lipid rafts associate with intracellular B cell receptors and exhibit a B cell stage-specific protein composition. J Immunol 174;3508-3517, 2005 https://doi.org/10.4049/jimmunol.174.6.3508
  5. Kemp SF, Lockey RF: Anaphylaxis: a review of causes and mechanisms. J Allergy Clin Immunol 110;341-348, 2002 https://doi.org/10.1067/mai.2002.126811
  6. Metzger H, Alcaraz G, Hohman R, Kinet JP, Pribluda V, Quarto R: The receptor with high affinity for immunoglobulin E. Annu Rev Immunol 4;419-470, 1986 https://doi.org/10.1146/annurev.iy.04.040186.002223
  7. Rivera J, Gilfillan AM: Molecular regulation of mast cell activation. J Allergy Clin Immunol 117;1214-1226, 2006 https://doi.org/10.1016/j.jaci.2006.04.015
  8. Metcalfe DD, Baram D, Mekori YA: Mast cells. Physiol Rev 77;1033-1079, 1997 https://doi.org/10.1152/physrev.1997.77.4.1033
  9. Church MK, Levi-Schaffer F: The human mast cell. J Allergy Clin Immunol 99;155-160, 1997 https://doi.org/10.1016/S0091-6749(97)70089-7
  10. Plaut M, Pierce JH, Watson CJ, Hanley-Hyde J, Nordan RP, Paul WE: Mast cell lines produce lymphokines in response to cross-linkage of Fc epsilon RI or to calcium ionophores. Nature 339;64-67, 1989 https://doi.org/10.1038/339064a0
  11. Wodnar-Filipowicz A, Heusser CH, Moroni C: Production of the haemopoietic growth factors GM-CSF and interleukin-3 by mast cells in response to IgE receptor-mediated activation. Nature 339;150-152, 1989 https://doi.org/10.1038/339150a0
  12. Gordon JR, Galli SJ: Mast cells as a source of both preformed and immunologically inducible TNF-alpha/cachectin. Nature 346;274-276, 1990 https://doi.org/10.1038/346274a0
  13. Blagoev B, Ong SE, Kratchmarova I, Mann M: Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics. Nat Biotechnol 22;1139-1145, 2004 https://doi.org/10.1038/nbt1005
  14. Marquardt DL, Walker LL: Dependence of mast cell IgE-mediated cytokine production on nuclear factor-kappaB activity. J Allergy Clin Immunol 105;500-505, 2000 https://doi.org/10.1067/mai.2000.104942
  15. Kaye RE, Fruman DA, Bierer BE, Albers MW, Zydowsky LD, Ho SI, Jin YJ, Castells MC, Schreiber SL, Walsh CT, et al.: Effects of cyclosporin A and FK506 on Fc epsilon receptor type I-initiated increases in cytokine mRNA in mouse bone marrow-derived progenitor mast cells: resistance to FK506 is associated with a deficiency in FK506-binding protein FKBP12. Proc Natl Acad Sci U S A 89;8542-8546, 1992 https://doi.org/10.1073/pnas.89.18.8542
  16. Feoktistov I, Goldstein AE, Biaggioni I: Role of p38 mitogen-activated protein kinase and extracellular signal-regulated protein kinase kinase in adenosine A2B receptor-mediated interleukin-8 production in human mast cells. Mol Pharmacol 55;726-734, 1999
  17. Park HH, Lee S, Oh JM, Lee MS, Yoon KH, Park BH, Kim JW, Song H, Kim SH: Anti-inflammatory activity of fisetin in human mast cells (HMC-1). Pharmacol Res 55;31-37, 2007 https://doi.org/10.1016/j.phrs.2006.10.002
  18. Boudreau RT, Hoskin DW, Lin TJ: Phosphatase inhibition potentiates IL-6 production by mast cells in response to FcepsilonRI-mediated activation: involvement of p38 MAPK. J Leukoc Biol 76;1075-1081, 2004 https://doi.org/10.1189/jlb.1003498
  19. Samayawardhena LA, Kapur R, Craig AW: Involvement of Fyn kinase in Kit and integrin-mediated Rac activation, cytoskeletal reorganization, and chemotaxis of mast cells. Blood 109;3679-3686, 2007 https://doi.org/10.1182/blood-2006-11-057315
  20. Vosseller K, Stella G, Yee NS, Besmer P: c-kit receptor signaling through its phosphatidylinositide-3'-kinase-binding site and protein kinase C: role in mast cell enhancement of degranulation, adhesion, and membrane ruffling. Mol Biol Cell 8;909-922, 1997 https://doi.org/10.1091/mbc.8.5.909
  21. Frigeri L, Apgar JR: The role of actin microfilaments in the down-regulation of the degranulation response in RBL-2H3 mast cells. J Immunol 162;2243-2250, 1999
  22. Oka T, Hori M, Tanaka A, Matsuda H, Karaki H, Ozaki H: IgE alone-induced actin assembly modifies calcium signaling and degranulation in RBL-2H3 mast cells. Am J Physiol Cell Physiol 286;C256-263, 2004 https://doi.org/10.1152/ajpcell.00197.2003
  23. Oka T, Hori M, Ozaki H: Microtubule disruption suppresses allergic response through the inhibition of calcium influx in the mast cell degranulation pathway. J Immunol 174; 4584-4589, 2005 https://doi.org/10.4049/jimmunol.174.8.4584
  24. Edgar AJ, Bennett JP: Circular ruffle formation in rat basophilic leukemia cells in response to antigen stimulation. Eur J Cell Biol 73;132-140, 1997
  25. Wong CK, Tsang CM, Ip WK, Lam CW: Molecular mechanisms for the release of chemokines from human leukemic mast cell line (HMC)-1 cells activated by SCF and TNF-alpha: roles of ERK, p38 MAPK, and NF-kappaB. Allergy 61;289-297, 2006 https://doi.org/10.1111/j.1398-9995.2006.00972.x
  26. Rivera J, Arudchandran R, Gonzalez-Espinosa C, Manetz TS, Xirasagar S: A perspective: regulation of IgE receptor-mediated mast cell responses by a LAT-organized plasma membrane-localized signaling complex. Int Arch Allergy Immunol 124;137-141, 2001 https://doi.org/10.1159/000053692
  27. Silverman MA, Shoag J, Wu J, Koretzky GA: Disruption of SLP-76 interaction with Gads inhibits dynamic clustering of SLP-76 and FcepsilonRI signaling in mast cells. Mol Cell Biol 26;1826-1838, 2006 https://doi.org/10.1128/MCB.26.5.1826-1838.2006
  28. Altman A, Villalba M: Protein kinase C-theta (PKCtheta): it's all about location, location, location. Immunol Rev 192; 53-63, 2003 https://doi.org/10.1034/j.1600-065X.2003.00027.x
  29. Mayer BJ: SH3 domains: complexity in moderation. J Cell Sci 114;1253-1263, 2001
  30. Daly RJ: Cortactin signalling and dynamic actin networks. Biochem J 382;13-25, 2004 https://doi.org/10.1042/BJ20040737

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