The scaffold protein prohibitin is required for antigen-stimulated signaling in mast cells

Science Signaling

Volumn 6, Issue 292, 2013, Pages

  Kim, Do Kyun ^a   Kim, Hyuk Soon ^a   Kim, A Ram ^a   Jang, Geun Hyo ^a   Kim, Hyun Woo ^a   Park, Young Hwan ^a   Kim, Bokyung ^a   Park, Yeong Min ^a   Beaven, Michael A ^b   Kim, Young Mi ^c   Choi, Wahn Soo ^a  

^a Konkuk University   (South Korea)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c Duksung Women's University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E; PROHIBITIN; PROTEIN KINASE SYK; SMALL INTERFERING RNA;

ALLERGIC REACTION; ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELL GRANULE; CONTROLLED STUDY; CYTOKINE RELEASE; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; GENE SILENCING; IMMUNOSTIMULATION; INTRACELLULAR SPACE; LIPID RAFT; MALE; MAST CELL; MAST CELL DEGRANULATION; MOUSE; NONHUMAN; PASSIVE SKIN ANAPHYLAXIS; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS; BLOTTING, WESTERN; CELL DEGRANULATION; CELLS, CULTURED; CYTOKINES; IMMUNOGLOBULIN E; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MAST CELLS; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; MODELS, IMMUNOLOGICAL; MUTATION; PASSIVE CUTANEOUS ANAPHYLAXIS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; RECEPTORS, IGE; REPRESSOR PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TYROSINE;

EID: 84884275234     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004098     Document Type: Article

References (42)

1. N. Patel, S. K. Chatterjee, V. Vrbanac, I. Chung, C. J. Mu, R. R. Olsen, C. Waghorne, B. R. Zetter, Rescue of paclitaxel sensitivity by repression of Prohibitin1 in drug-resistant cancer cells. Proc. Natl. Acad. Sci. U.S.A. 107, 2503-2508 (2010).
2. S. Mishra, L. C. Murphy, L. J. Murphy, The Prohibitins: Emerging roles in diverse functions. J. Cell. Mol. Med. 10, 353-363 (2006).
3. M. G. Kolonin, P. K. Saha, L. Chan, R. Pasqualini, W. Arap, Reversal of obesity by targeted ablation of adipose tissue. Nat. Med. 10, 625-632 (2004).
4. M. Terashima, K. M. Kim, T. Adachi, P. J. Nielsen, M. Reth, G. Köhler, M. C. Lamers, The IgM antigen receptor of B lymphocytes is associated with prohibitin and a prohibitinrelated protein. EMBO J. 13, 3782-3792 (1994).
5. S. Mishra, S. R. Ande, B. L. Nyomba, The role of prohibitin in cell signaling. FEBS J. 277, 3937-3946 (2010).
6. I. C. Morrow, R. G. Parton, Flotillins and the PHB domain protein family: Rafts, worms and anaesthetics. Traffic 6, 725-740 (2005).
7. K. Rajalingam, C.Wunder, V. Brinkmann, Y. Churin, M. Hekman, C. Sievers, U. R. Rapp, T. Rudel, Prohibitin is required for Ras-induced Raf-MEK-ERK activation and epithelial cell migration. Nat. Cell Biol. 8, 837-843 (2005).
8. S. R. Ande, Y. Gu, B. L. Nyomba, S. Mishra, Insulin induced phosphorylation of prohibitin at tyrosine 114 recruits Shp1. Biochim. Biophys. Acta 1793, 1372-1378 (2009).
9. S. R. Ande, S. Mishra, Prohibitin interacts with phosphatidylinositol 3,4,5-Triphosphate (PIP3) and modulates insulin signaling. Biochem. Biophys. Res. Commun. 390, 1023-1028 (2009).
10. M. Metz, M. A. Grimbaldeston, S. Nakae, A. M. Piliponsky, M. T. Sai, S. J. Galli, Mast cells in the promotion and limitation of chronic inflammation. Immunol. Rev. 217, 304-328 (2007).
11. S. J. Galli, M. Tsai, A. M. Piliponsky, The development of allergic inflammation. Nature 454, 445-454 (2008).
12. T. Kawakami, T. Ando, M. Kimura, B. S. Wilson, Y. Kawakami, Mast cells in atopic dermatitis. Curr. Opin. Immunol. 21, 666-678 (2009).
13. A. M. Gilfillan, M. A. Beaven, Regulation of mast cell responses in health and disease. Crit. Rev. Immunol. 31, 475-530 (2011).
14. E. Eiseman, J. B. Bolen, Engagement of the high-Affinity IgE receptor activates src protein-related tyrosine kinases. Nature 355, 78-80 (1992).
15. J. E. Hutchcroft, R. L. Geahlen, G. G. Deanin, J. M. Oliver, FceRI-mediated tyrosine phosphorylation and activation of the 72-kDa protein-Tyrosine kinase, PTK72, in RBL-2H3 rat tumor mast cells. Proc. Natl. Acad. Sci. U.S.A. 89, 9107-9111 (1992).
16. M. H. Jouvin, M. Adamczewski, R. Numerof, O. Letourneur, A. Vallé, J. P. Kinet, Differential control of the tyrosine kinases Lyn and Syk by the two signaling chains of the high affinity immunoglobulin E receptor. J. Biol. Chem. 269, 5918-5925 (1994).
17. A. M. Gilfillan, C. Tkaczyk, Integrated signalling pathways for mast-cell activation. Nat. Rev. Immunol. 6, 218-230 (2006).
18. J. Rivera, A. M. Gilfillan, Molecular regulation of mast cell activation. J. Allergy Clin. Immunol. 117, 1214-1225 (2006).
19. S. Saitoh, R. Arudchandran, T. S. Manetz,W. Zhang, C. L. Sommers, P. E. Love, J. Rivera, L. E. Samelson, LAT is essential for FceRI-mediated mast cell activation. Immunity 12, 525-535 (2000).
20. H. Turner, J. P. Kinet, Signalling through the high-Affinity IgE receptor FceRI. Nature 402, B24-B30 (1999).
21. W. Li, G. G. Deanin, B. Margolis, J. Schlessinger, J. M. Oliver, FceR1-mediated tyrosine phosphorylation of multiple proteins, including phospholipase Cg1 and the receptor bg2 complex, in RBL-2H3 rat basophilic leukemia cells. Mol. Cell. Biol. 12, 3176-3182 (1992).
22. D. J. Park, H. K. Min, S. G. Rhee, IgE-induced tyrosine phosphorylation of phospholipase C-g1 in rat basophilic leukemia cells. J. Biol. Chem. 266, 24237-24240 (1991).
23. L. R. Hendricks-Taylor, D. G. Motto, J. Zhang, R. P. Siraganian, G. A. Koretzky, SLP-76 is a substrate of the high affinity IgE receptor stimulated protein tyrosine kinases in rat basophilic leukemia cells. J. Biol. Chem. 272, 1363-1367 (1997).
24. M. Yu, C. A. Lowell, B. G. Neel, H. Gu, Scaffolding adapter Grb2-Associated binder 2 requires Syk to transmit signals from FceRI. J. Immunol. 176, 2421-2429 (2006).
25. S. Iwaki, C. Tkaczyk, A. B. Satterthwaite, K. Halcomb, M. A. Beaven, D. D. Metcalfe, A. M. Gilfillan, Btk plays a crucial role in the amplification of FceRI-mediated mast cell activation by kit. J. Biol. Chem. 280, 40261-40270 (2005).
26. H. Qiao, M. V. Andrade, F. A. Lisboa, K. Morgan, M. A. Beaven, FceR1 and toll-like receptors mediate synergistic signals to markedly augment production of inflammatory cytokines in murine mast cells. Blood 107, 610-618 (2006).
27. H. T. Ma, M. A. Beaven, Regulators of Ca2+ signaling in mast cells: Potential targets for treatment of mast cell-related diseases? Adv. Exp. Med. Biol. 716, 62-90 (2011).
28. S. W. Kim, D. Rai, M. R. McKeller, R. C. T. Aguiar, Rational combined targeting of phosphodiesterase 4B and SYK in DLBCL. Blood 113, 6153-6160 (2009).
29. A. M. Gilfillan, J. Rivera, The tyrosine kinase network regulating mast cell activation. Immunol. Rev. 228, 149-169 (2009).
30. V. S. Pribluda, C. Pribluda, H. Metzger, Transphosphorylation as the mechanism by which the high-Affinity receptor for IgE is phosphorylated upon aggregation. Proc. Natl. Acad. Sci. U.S.A. 91, 11246-11250 (1994).
31. S. R. Ande, S. Mishra, Palmitoylation of prohibitin at cysteine 69 facilitates its membrane translocation and interaction with Eps 15 homology domain protein 2 (EHD2). Biochem. Cell Biol. 88, 553-558 (2010).
32. B. K. Wershil, Y. A. Mekori, T. Murakami, S. J. Galli, 125I-fibrin deposition in IgE-dependent immediate hypersensitivity reactions in mouse skin. Demonstration of the role of mast cells using genetically mast cell-deficient mice locally reconstituted with cultured mast cells. J. Immunol. 139, 2605-2614 (1987).
33. J. K. McClung, E. R. Jupe, X. T. Liu, R. T. Dell'Orco, Prohibitin: Potential role in senescence, development, and tumor suppression. Exp. Gerontol. 30, 99-124 (1996).
34. C. F. Chiu, M. Y. Ho, J. M. Peng, S. W. Hung, W. H. Lee, C. M. Liang, S. M. Liang, Raf activation by Ras and promotion of cellular metastasis require phosphorylation of prohibitin in the raft domain of the plasma membrane. Oncogene 32, 777-787 (2013).
35. J. H. Lee, J. W. Kim, D. K. Kim, H. S. Kim, H. J. Park, D. K. Park, A. R. Kim, B. Kim, M. A. Beaven, K. L. Park, Y. M. Kim, W. S. Choi, The Src family kinase Fgr is critical for activation of mast cells and IgE-mediated anaphylaxis in mice. J. Immunol. 187, 1807-1815 (2011).
36. U. Grädler, D. Schwarz, V. Dresing, D. Musil, J. Bomke, M. Frech, H. Greiner, S. Jäkel, T. Rysiok, D. Müller-Pompalla, A. Wegener, Structural and biophysical characterization of the Syk activation switch. J. Mol. Biol. 425, 309-333 (2013).
37. K. A. Field, D. Holowka, B. Baird, FceRI-mediated recruitment of p53/56lyn to detergentresistant membrane domains accompanies cellular signaling. Proc. Natl. Acad. Sci. U.S.A. 92, 9201-9205 (1995).
38. X. Qu, K. Sada, S. Kyo, K. Maeno, S. M. Miah, H. Yamamura, Negative regulation of FceRI-mediated mast cell activation by a ubiquitin-protein ligase Cbl-b. Blood 103, 1779-1786 (2004).
39. V. Parravicini, M. Gadina, N. Kovarova, S. Odom, C. Gonzalez-Espinosa, Y. Furumoto, S. Saitoh, L. E. Samelson, J. J. O'Shea, J. Rivera, Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat. Immunol. 3, 741-748 (2002).
40. B. M. Jensen, E. J. Swindle, S. Iwaki, A. M. Gilfillan, Generation, isolation, and maintenance of rodent mast cells and mast cell lines. Curr. Protoc. Immunol. Chapter 3, Unit 3.23 (2006).
41. K. Ozawa, Z. Szallasi, M. G. Kazanietz, P. M. Blumberg, H. Mischak, J. F. Mushinski, M. A. Beaven, Ca2+-dependent and Ca2+-independent isozymes of protein kinase C mediate exocytosis in antigen stimulated rat basophilic RBL-2H3 cells. Reconstitution of secretory responses with Ca2+ and purified isozymes in washed permeabilized cells. J. Biol. Chem. 268, 1749-1756 (1993).
42. T. R. Martin, S. J. Galli, I. M. Katona, J. M. Drazen, Role of mast cells in anaphylaxis. Evidence for the importance of mast cells in the cardiopulmonary alterations and death induced by anti-IgE in mice. J. Clin. Invest. 83, 1375-1383 (1989).