Evidence that formation of vimentin·mitogen-activated protein kinase (MAPK) complex mediates mast cell activation following FcεRI/CC chemokine receptor 1 cross-talk

Journal of Biological Chemistry

Volumn 287, Issue 29, 2012, Pages 24516-24524

  Toda, Masako ^a   Kuo, Chuan Hui ^a   Borman, Satty K ^b   Richardson, Ricardo Micheler ^c   Inoko, Akihito ^d   Inagaki, Masaki ^a   Collins, Andrea ^a   Schneider, Klaus ^b,e   Ono, Santa Jeremy ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b GLAXOSMITHKLINE   (United Kingdom)

^c NORTH CAROLINA CENTRAL UNIVERSITY   (United States)

^d AICHI CANCER CENTER HOSPITAL   (Japan)

^e MERCK KGAA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGIC INFLAMMATION; CHEMOKINE RECEPTORS; CHEMOKINES; IMMUNOPRECIPITATION ANALYSIS; INTERMEDIATE FILAMENTS; MAST CELLS; MEDIATED SIGNALING PATHWAYS; MITOGEN ACTIVATED PROTEIN KINASE; P38 MAPK; VIMENTIN;

CROSSTALK; CYTOLOGY; PHOSPHORYLATION; RECOMBINANT PROTEINS; WELL STIMULATION;

CELLS;

CHEMOKINE RECEPTOR CCR1; FC EPSILON RI; FC RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; UNCLASSIFIED DRUG; VIMENTIN;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOPRECIPITATION; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; UPREGULATION;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; CHEMOKINE CCL2; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMIDAZOLES; IMMUNOPRECIPITATION; MAST CELLS; MICE; MICE, INBRED BALB C; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; ORGANIC CHEMICALS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN BINDING; PYRIDINES; RATS; RECEPTORS, CCR1; RECEPTORS, IGG; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VIMENTIN;

MURINAE; RATTUS;

EID: 84863793854     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.319624     Document Type: Article

References (45)

1. Abramson, J., and Pecht, I. (2007) Regulation of the mast cell response to the type 1 Fc ε receptor. Immunol. Rev. 217, 231-254 (Pubitemid 46718151)
2. Gilfillan, A. M., and Tkaczyk, C. (2006) Integrated signaling pathways for mast cell activation. Nat. Rev. Immunol. 6, 218-230 (Pubitemid 43290991)
3. Ono, S. J., Nakamura, T., Miyazaki, D., Ohbayashi, M., Dawson, M., and Toda, M. (2003) Chemokines. Roles in leukocyte development, trafficking, and effector function. J. Allergy Clin. Immunol. 111, 1185-1199; quiz 1200
4. Beer, F., Kuo, C. H., Morohoshi, K., Goodliffe, J., Munro, P., Aye, C. C., Dawson, M., Richardson, R. M., Jones, L. H., Ikeda, Y., Nakamura, T., Toda, M., Flynn, T., Ohbayashi, M., Miyazaki, D., and Ono, S. J. (2007) Role of β-chemokines in mast cell activation and type I hypersensitivity reactions in the conjunctiva. In vivo and in vitro studies. Immunol. Rev. 217, 96-104 (Pubitemid 46718154)
5. Tominaga, T., Miyazaki, D., Sasaki, S., Mihara, S., Komatsu, N., Yakura, K., and Inoue, Y. (2009) Blocking mast cell-mediated type I hypersensitivity in experimental allergic conjunctivitis by monocyte chemoattractant protein-1/CCR2. Invest. Ophthalmol. Vis. Sci. 50, 5181-5188
6. Campbell, E. M., Charo, I. F., Kunkel, S. L., Strieter, R. M., Boring, L., Gosling, J., and Lukacs, N. W. (1999) Monocyte chemoattractant protein-1 mediates cockroach allergen-induced bronchial hyperreactivity in normal but not CCR2-/- mice. The role of mast cells. J. Immunol. 163, 2160-2167 (Pubitemid 29382223)
7. Sousa, A. R., Lane, S. J., Nakhosteen, J. A., Yoshimura, T., Lee, T. H., and Poston, R. N. (1994) Increased expression of the monocyte chemoattractant protein-1 in bronchial tissue from asthmatic subjects. Am. J. Respir. Cell Mol. Biol. 10, 142-147
8. Holgate, S. T., Bodey, K. S., Janezic, A., Frew, A. J., Kaplan, A. P., and Teran, L. M. (1997) Release of RANTES, MIP-1α, and MCP-1 into asthmatic airways following endobronchial allergen challenge. Am. J. Respir. Crit. Care Med. 156, 1377-1383 (Pubitemid 27505497)
9. Toda, M., Nakamura, T., Ohbayashi, M., Ikeda, Y., Dawson, M., Aye, C. C., Miyazaki, D., and Ono, S. J. (2007) Mechanisms of leukocyte trafficking in allergic diseases. Insights into new therapies targeting chemokines and chemokine receptors. Expert Rev. Clin. Immunol. 3, 351-364 (Pubitemid 46839311)
10. Miyazaki, D., Nakamura, T., Toda, M., Cheung-Chau, K. W., Richardson, R. M., and Ono, S. J. (2005) Macrophage inflammatory protein-1α as a costimulatory signal for mast cell-mediated immediate hypersensitivity reactions. J. Clin. Invest. 115, 434-442 (Pubitemid 40385485)
11. Toda, M., Dawson, M., Nakamura, T., Munro, P. M., Richardson, R. M., Bailly, M., and Ono, S. J. (2004) Impact of engagement of FcεRI and CC chemokine receptor 1 on mast cell activation and motility. J. Biol. Chem. 279, 48443-48448 (Pubitemid 39541002)
12. Fifadara, N. H., Aye, C. C., Raghuwanshi, S. K., Richardson, R. M., and Ono, S. J. (2009) CCR1 expression and signal transduction by murine BMMC results in secretion of TNF-α, TGFβ-1, and IL-6. Int. Immunol. 21, 991-1001
13. Laffargue, M., Calvez, R., Finan, P., Trifilieff, A., Barbier, M., Altruda, F., Hirsch, E., and Wymann, M. P. (2002) Phosphoinositide 3-kinase γ is an essential amplifier of mast cell function. Immunity 16, 441-451 (Pubitemid 34260921)
14. Aye, C. C., Toda, M., Morohoshi, K., and Ono, S. J. (2012) Identification of genes and proteins specifically regulated by costimulation of mast cell Fcεreceptor I and chemokine receptor 1. Exp. Mol. Pathol. 92, 267-274
15. Gaga, M., Ong, Y. E., Benyahia, F., Aizen, M., Barkans, J., and Kay, A. B. (2008) Skin reactivity and local cell recruitment in human atopic and nonatopic subjects by CCL2/MCP-1 and CCL3/MIP-1α. Allergy 63, 703-711 (Pubitemid 351591843)
16. Richardson, R. M., Pridgen, B. C., Haribabu, B., and Snyderman, R. (2000) Regulation of the human chemokine receptor CCR1. Cross-regulation by CXCR1 and CXCR2. J. Biol. Chem. 275, 9201-9208 (Pubitemid 30185137)
17. Groschwitz, K. R., Ahrens, R., Osterfeld, H., Gurish, M. F., Han, X., Abrink, M., Finkelman, F. D., Pejler, G., and Hogan, S. P. (2009) Mast cells regulate homeostatic intestinal epithelial migration and barrier function by a chymase/Mcpt4-dependent mechanism. Proc. Natl. Acad. Sci. U.S.A. 106, 22381-22386
18. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
19. Wilm, M., Shevchenko, A., Houthaeve, T., Breit, S., Schweigerer, L., Fotsis, T., and Mann, M. (1996) Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379, 466-469
20. Suckau, D., Resemann, A., Schuerenberg, M., Hufnagel, P., Franzen, J., and Holle, A. (2003) A novel MALDI LIFT-TOF/TOF mass spectrometer for proteomics. Anal. Bioanal. Chem. 376, 952-965 (Pubitemid 40877913)
21. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 (Pubitemid 30007252)
22. Valgeirsdottir, S., Claesson-Welsh, L., Bongcam-Rudloff, E., Hellman, U., Westermark, B., and Heldin, C. H. (1998) J. Cell Sci. 111, 1973-1980
23. Tsujimura, K., Ogawara, M., Takeuchi, Y., Imajoh-Ohmi, S., Ha, M. H., and Inagaki, M. (1994) Visualization and function of vimentin phosphorylation by cdc2 kinase during mitosis. J. Biol. Chem. 269, 31097-31106 (Pubitemid 24377604)
24. Yasui, Y., Goto, H., Matsui, S., Manser, E., Lim, L., Nagata, K., and Inagaki, M. (2001) Protein kinases required for segregation of vimentin filaments in mitotic process. Oncogene 20, 2868-2876 (Pubitemid 33027754)
25. Ogawara, M., Inagaki, N., Tsujimura, K., Takai, Y., Sekimata, M., Ha, M. H., Imajoh-Ohmi, S., Hirai, S., Ohno, S., and Sugiura, H. (1995) Differential targeting of protein kinase C and CaM kinase II signalings to vimentin. J. Cell Biol. 131, 1055-1066
26. McDonald, J. R., Finck, B. K., McIntosh, L. M., and Wilson, S. E. (2011) Anti-inflammatory approaches that target the chemokine network. Recent Pat. Inflamm. Allergy Drug Discov. 5, 1-16
27. Chang, L., and Goldman, R. D. (2004) Intermediate filaments mediate cytoskeletal cross-talk. Nat. Rev. Mol. Cell Biol. 5, 601-613 (Pubitemid 39025061)
28. Inagaki, M., Nishi, Y., Nishizawa, K., Matsuyama, M., and Sato, C. (1987) Site-specific phosphorylation induces disassembly of vimentin filaments in vitro. Nature 328, 649-652 (Pubitemid 17103974)
29. Eriksson, J. E., He, T., Trejo-Skalli, A. V., Härmälä- Braskén, A. S., Hellman, J., Chou, Y. H., and Goldman, R. D. (2004) Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J. Cell Sci. 117, 919-932 (Pubitemid 38386949)
30. Li, Q. F., Spinelli, A. M., Wang, R., Anfinogenova, Y., Singer, H. A., and Tang, D. D. (2006) Critical role of vimentin phosphorylation at Ser-56 by p21-activated kinase in vimentin cytoskeleton signaling. J. Biol. Chem. 281, 34716-34724 (Pubitemid 46036677)
31. Sihag, R. K., Inagaki, M., Yamaguchi, T., Shea, T. B., and Pant, H. C. (2007) Role of phosphorylation in the structural dynamics and function of types III and IV intermediate filaments. Exp. Cell Res. 313, 2098-2109 (Pubitemid 46842988)
32. Chou, Y. H., Opal, P., Quinlan, R. A., and Goldman, R. D. (1996) The relative roles of specific N- and C-terminal phosphorylation sites in the disassembly of intermediate filament in mitotic BHK-21 cells. J. Cell Sci. 109, 817-826 (Pubitemid 26134384)
33. Ivaska, J., Pallari, H. M., Nevo, J., and Eriksson, J. E. (2007) Novel functions of vimentin in cell adhesion, migration, and signaling. Exp. Cell Res. 313, 2050-2062 (Pubitemid 46842979)
34. Helfand, B. T., Chou, Y. H., Shumaker, D. K., and Goldman, R. D. (2005) Intermediate filament proteins participate in signal transduction. Trends Cell Biol. 15, 568-570 (Pubitemid 41619419)
35. Perlson, E., Michaelevski, I., Kowalsman, N., Ben-Yaakov, K., Shaked, M., Seger, R., Eisenstein, M., and Fainzilber, M. (2006) Vimentin binding to phosphorylated Erk sterically hinders enzymatic dephosphorylation of the kinase. J. Mol. Biol. 364, 938-944 (Pubitemid 44765042)
36. Perlson, E., Hanz, S., Ben-Yaakov, K., Segal-Ruder, Y., Seger, R., and Fainzilber, M. (2005) Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45, 715-726 (Pubitemid 40320706)
37. Kumar, N., Robidoux, J., Daniel, K. W., Guzman, G., Floering, L. M., and Collins, S. (2007) Requirement of vimentin filament assembly for β3-adrenergic receptor activation of ERK MAP kinase and lipolysis. J. Biol. Chem. 282, 9244-9250 (Pubitemid 47093532)
38. Galigniana, M. D., Scruggs, J. L., Herrington, J., Welsh, M. J., Carter-Su, C., Housley, P. R., and Pratt, W. B. (1998) Heat shock protein 90-dependent (geldanamycin-inhibited) movement of the glucocorticoid receptor through the cytoplasm to the nucleus requires intact cytoskeleton. Mol. Endocrinol. 12, 1903-1913 (Pubitemid 28544185)
39. Nahm, D. H., Tkaczyk, C., Fukuishi, N., Colucci-Guyon, E., Gilfillan, A. M., and Metcalfe, D. D. (2003) Identification of Fyn-binding proteins in MC/9 mast cells using mass spectrometry. Biochem. Biophys. Res. Commun. 310, 202-208 (Pubitemid 37162783)
40. 2+ATPase inhibitors on MCP-1 release from bone marrow-derived mast cells and the involvement of p38 MAP kinase activation. Int. Arch. Allergy Immunol. 121, 34-43
41. Wong, C. K., Tsang, C. M., Ip, W. K., and Lam, C. W. (2006) Molecular mechanisms for the release of chemokines from human leukemic mast cell line (HMC)-1 cells activated by SCF and TNF-α. Roles of ERK, p38 MAPK, and NF-κB. Allergy 61, 289-297
42. Gonzalez-Espinosa, C., Odom, S., Olivera, A., Hobson, J. P., Martinez, M. E., Oliveira-Dos-Santos, A., Barra, L., Spiegel, S., Penninger, J. M., and Rivera, J. (2003) Preferential signaling and induction of allergy-promoting lymphokines upon weak stimulation of the high affinity IgE receptor on mast cells. J. Exp. Med. 197, 1453-1465 (Pubitemid 36682544)
43. Cargnello, M., and Roux, P. P. (2011) Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 75, 50-83
44. Sahara, N., Siraganian, R. P., and Oliver, C. (1990) Morphological changes induced by the calcium ionophore A23187 in rat basophilic leukemia (2H3) cells. J. Histochem. Cytochem. 38, 975-983 (Pubitemid 20186202)
45. Izushi, K., Fujiwara, Y., and Tasaka, K. (1992) Identification of vimentin in rat peritoneal mast cells and its phosphorylation in association with histamine release. Immunopharmacology 23, 153-161