Characterization of the 78 kDa mast cell protein phosphorylated by the antiallergic drug cromolyn and homology to moesin

Biochemical Pharmacology

Volumn 52, Issue 3, 1996, Pages 413-424

  Correia, Ivan ^a   Wang, Linghua ^a   Pang, Xinzhu ^a   Theoharides, Theoharis C ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cromolyn; inhibition; mast cells; phosphorylation; protein kinase C; secretion

Indexed keywords

1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; ANTIALLERGIC AGENT; COMPLEMENTARY DNA; CROMOGLYCATE DISODIUM; MEMBRANE PROTEIN; MOESIN; N (2 METHYLAMINOETHYL) 5 ISOQUINOLINESULFONAMIDE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PHOSPHOPROTEIN; POLYCLONAL ANTIBODY; PROTEIN ANTIBODY; PROTEIN KINASE C; PROTEIN KINASE INHIBITOR; STAUROSPORINE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL SECRETION; CONTROLLED STUDY; DRUG MECHANISM; ESCHERICHIA COLI; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; MALE; MAST CELL LEUKEMIA; MOUSE; NONHUMAN; PERITONEUM MAST CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; RAT; TWO DIMENSIONAL GEL ELECTROPHORESIS;

EID: 0030576658     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/0006-2952(96)00243-2     Document Type: Article

References (73)

1. 1. Beaven MA and Metzger H, Signal transduction by Fc receptors: The FcεRi case. Immunol Today 14: 222-226, 1993.
2. 2. Scharenberg AM and Kinet J-P, Initial events in FcεRi signal transduction. J Allergy Clin Immunol 94: 1142-1154b, 1994.
3. 3. Serafin WE and Austen KF, Mediators of immediate hypersensitivity reactions. N Engl J Med 317: 30-34, 1987.
4. 4. Galli SJ, New insights into "the riddle of the mast cells": Microenvironmental regulation of mast cell development and phenotypic heterogeneity. Lab Invest 62: 5-33, 1990.
5. 5. Theoharides TC, Mast cells: The immune gate to the brain. Life Sci 46: 607-617, 1990.
6. 6. Sant GR and Theoharides TC, The role of the mast cell in interstitial cystitis. Uroi Clin North Am 21: 41-53, 1994.
7. 7. Burgoyne RD, G-proteins: Control of exocytosis. Nature 328: 112-113, 1987.
8. 8. Clapham DE, Calcium signaling. Cell 80: 259-268, 1995.
9. 9. Saito H, Okajima F, Molski TF, Sha'afi RI, Ui M and Ishizaka T, Effects of ADP-ribosylation of GTP-binding protein by pertussis toxin on immunoglobulin E-dependent and -independent histamine release from mast cells and basophils. J Immunol 138: 3927-3934, 1987.
10. 10. Mousli M, Bueb J-L, Bronner C, Rouot B and Landry Y, G protein activation: A receptor-independent mode of action for cationic amphiphilic neuropeptides and venom peptides. Trends Pharmacol Sci 11: 358-362, 1990.
11. i3. Science 262: 1569-1572, 1993.
12. 12. Oberhauser AF, Monck JR, Balch WE and Fernandez JM, Exocytotic fusion is activated by Rab3a peptides. Nature 360: 270-273, 1992.
13. E: A GTP-binding protein mediating exocytosis. Annu Rev Physiol 52: 591-606, 1990.
14. 14. Sieghart W, Theoharides TC, Alper SL, Douglas WW and Greengard P, Calcium-dependent protein phosphorylation during secretion by exocytosis in the mast cell. Nature 275: 329-331, 1978.
15. 15. Theoharides TC, Sieghart W, Greengard P and Douglas WW, Somatostatin-induced protein phosphorylation of mast cell proteins. Biochem Pharmacol 30: 2735-2736, 1981.
16. 16. Wells E and Mann J, Phosphorylation of a mast cell protein in response to treatment with anti-allergic compounds. Implications for the mode of action of sodium cromoglycate. Biochem Pharmacol 32: 837-842, 1983.
17. 17. Izushi K, Fujiwara Y and Tasaka K, Identification of vimentin in rat peritoneal mast cells and its phosphorylation in association with histamine release. Immunopharmacology 23: 153-161, 1992.
18. 18. Theoharides TC, Sieghart W, Greengard P and Douglas WW, Antiallergic drug cromolyn may inhibit histamine secretion by regulating phosphorylation of a mast cell protein. Science 207: 80-82, 1980.
19. 19. Shapiro GG and Konig P, Cromolyn sodium: A review. Pharmacotherapy 5: 156-170, 1985.
20. 20. Ennis M, Truneh A, White JR and Pearce FL, Inhibition of histamine secretion from mast cells. Nature 289: 186-187, 1981.
21. 21. Cairns H, Cox D, Gould KJ, Ingall AH and Suschitzky JL, New antiallergic pyrano[3,2-g]quinoline-2,8-dicarboxylic acids with potential for the topical treatment of asthma. J Med Chem 28: 1832-1842, 1985.
22. 22. Sieghart W, Theoharides TC, Douglas WW and Greengard P, Phosphorylation of a single mast cell protein in response to drugs that inhibit secretion. Biochem Pharmacol 30: 2737-2738, 1981.
23. 3H]serotonin. J Cell Biol 93: 638-647, 1982.
24. 4. Nature 227: 680-685, 1970.
25. 25. Schägger H and von Jagow G, Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166: 368-379, 1987.
26. 26. O'Farrell PH, High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007-4021, 1975.
27. 27. Hurkman WJ and Tanaka CK, Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 81: 802-806, 1986.
28. 28. Imada M and Sueoka N, A two-dimensional polyacrylamide gel electrophoresis system for the analysis of mammalian cell surface proteins. Biochim Biophys Acta 625: 179-192, 1980.
29. 29. Matsudaira P, Sequence from picomole quantities of proteins electro-blotted onto polyvinylidene difluoride membranes. J Biol Chem 262: 10035-10038, 1987.
30. 30. Harlow E and Lane D, Antibodies: A Laboratory Manual. Cold Springs Harbor Laboratory, Cold Springs Harbor, NY, 1988.
31. 31. Lankes WT and Furthmayr H, Moesin: A member of the protein 4.1-talin-ezrin family of proteins. Proc Natl Acad Sci USA 88: 8297-8301, 1991.
32. 32. Altounyan RE, Review of the clinical activity and modes of action of sodium cromoglycate. In: The Mast Cell, Its Role in Health and Disease, (Eds. Pepys J and Edwards AM) pp. 199-229. Pitman Medical, London, 1979.
33. 33. Djukanović R and Holgate ST, Lessons to be learned from sodium cromoglycate and related drugs. In: The Mast Cell in Health and Disease, (Eds. Kaliner MA and Metcalfe DD), pp. 467-481. Marcel Dekker, New York, 1993.
34. 34. Pearce FL and Truneh A, Inhibition of histamine release from rat peritoneal mast cells treated with the ionophore A23187. Implications for the mode of action of anti-allergic compounds. Agents Actions 11: 44-50, 1981.
35. 35. Pearce FL, Ali H, Barrett KE, Befus AD, Bienenstock J, Brostoff J, Ennis M, Flint KC, Hudspith B and Johnson NM, Functional characteristics of mucosal and connective tissue mast cells of man, the rat and other animals. Int Arch Allergy Appl Immunol 77: 274-276, 1985.
36. 36. Ennis M, Atkinson G and Pearce FL, Inhibition of histamine release induced by compound 48/80 and peptide 401 in the presence and absence of calcium. Agents Actions 10: 222-228, 1980.
37. 37. Orr TS, Hall DE, Gwillaim JN and Cox JS, The effect of disodium cromoglycate on the release of histamine and degranulation of rat mast cells induced by compound 48/80. Life Sci 10: 805-812, 1971.
38. 38. Mazurek N, Bashkin P and Pecht I, Isolation of a basophilic membrane protein binding the anti-allergic drug cromolyn. EMBO J 1: 585-590, 1982.
39. 2+ influx and degranulation capacity of variant RBL-2H3 cells upon implantation of isolated cromolyn binding protein. Proc Natl Acad Sci USA 80: 6014-6018, 1983.
40. 2+ channel of basophils opening upon immunological stimulus. Proc Natl Acad Sci USA 81: 6841-6845, 1984.
41. 2+ influx and mediator secretion in rat mucosal mast cells. Biochemistry 30: 1523-1532, 1991.
42. 42. Lankes W, Griesmacher A, Grünwald J, Schwartz-Albiez R and Keller R, A heparin-binding protein involved in inhibition of smooth-muscle cell proliferation. Biochem J 251: 831-842, 1988.
43. 43. Furthmayr H, Lankes W and Amieva M, Moesin, a new cytoskeletal protein and constitutent of filopodia: Its role in cellular functions. Kidney Int 41: 665-670, 1992.
44. 44. Eder PS, Soong C-J and Tao M, Phosphorylation reduces the affinity of protein 4.1 for spectrin. Biochemistry 25: 1764-1770, 1986.
45. 45. Horne WC, Leto TL and Marchesi VT, Differential phosphorylation of multiple sites in protein 4.1 and protein 4.9 by phorbol ester-activated and cyclic AMP-dependent protein kinases. J Biol Chem 260: 9073-9076, 1985.
46. 46. Palfrey HC and Waseem A, Protein kinase C in the human erythrocyte. J Biol Chem 260: 16021-16029, 1985.
47. 47. Baines AJ and Bennett V, Synapsin I is a spectrin-binding protein immunologically related to erythrocyte protein 4-1 Nature 315: 410-413, 1985.
48. 48. Franck Z, Gary R and Bretscher A, Moesin, like ezrin, colocalizes with actin in the cortical cytoskeleton in cultured cells, but its expression is more variable. J Cell Sci 105: 219-231, 1993.
49. 49. Krieg J and Hunter T, Identification of the two major epidermal growth factor-induced tyrosine phosphorylation sites in the microvillar core protein ezrin. J Biol Chem 267: 19258-19265, 1992.
50. 50. Hanzel D, Reggio H, Bretscher A, Forte JG and Mangeat P, The secretion-stimulated 80K phosphoprotein of parietal cells is ezrin, and has properties of a membrane cytoskeletal linker in the induced apical microvilli. EMBO J 10: 2363-2373, 1991.
51. 51. Berryman M, Franck Z and Bretscher A, Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cells whereas moesin is found primarily in endothelial cells. J Cell Sci 105: 1025-1043, 1993.
52. 52. Pestonjamasp K, Amieva MR, Strassel CP, Nauseef WM, Furthmayr H and Luna EJ, Moesin, ezrin and p205 are actin-binding proteins associated with neutrophil plasma membranes. Mol Biol Cell 6: 247-259, 1995.
53. 53. Sato N, Funayama N, Nagafuchi A, Yonemura S and Tsukita S, A gene family consisting of ezrin, radixin, and moesin. Its specific localization at actin filament/plasma membrane association sites. J Cell Sci 103: 131-143, 1992.
54. 54. Sato N, Yonemura S, Obinata T and Tsukita S, Radixin, a barbed end-capping actin-modulating protein, is concentrated at the cleavage furrow during cytokinesis. J Cell Biol 113: 321-330, 1991.
55. 55. Rouleau GA, Merel P, Lutchman M, Sanson M, Zucman J, Marineau C, Hoang-Xuan K, Demczuk S, Desmaze C, Plougastel B, Pulst SM, Lenoir G, Bijlsma E, Fashold R, Dumanski J, de Jong P, Parry D, Eldrige R, Aurias A, Delattre O and Thomas G, Alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2. Nature 363: 515-521, 1993.
56. 56. Trofatter JA, MacCollin MM, Rutter JL, Murrell JR, Duyao MP, Parry DM, Eldridge R, Kley N, Menon AG, Pulaski K, Haase VH, Ambrose CM, Munroe D, Bove C, Haines JL, Martuza RL, MacDonald ME, Seizinger BR, Short MP, Buckler AJ and Gusella JF, A novel moesin-, ezrin-, and radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell 72: 791-800, 1993.
57. 57. Raff MC and Lawson D, Membrane events in cell signaling. In: Immune System: Genetics and Regulation ICN-UCLA Symposia on Molecular and Cellular Biology (Eds. Sercarz EE, Herzenberg LA and Fox CF), Vol. 6, pp. 669-678. Academic Press, New York, 1977.
58. 58. Sagi-Eisenberg R, Possible role for a calcium-activated phospholipid-dependent protein kinase in mode of action of DSCG. Trends Pharmacol Sci 6: 198-200, 1985.
59. 59. Zhou G, Wooten MW and Coleman ES, Regulation of atypical ζ-protein kinase C in cellular signalling. Exp Cell Res 214: 1-11, 1994.
60. 2+-independent isozymes of protein kinase C mediate exocytosis in antigen-stimulated rat basophilic RBL-2H3 cells. J Biol Chem 268: 1749-1756, 1993.
61. 61. Ozawa K, Yamada K, Kazanietz MG, Blumberg PM and Beaven MA, Different isozymes of protein kinase C mediate feedback inhibition of phospholipase C and stimulatory signals for exocytosis in rat RBL-2H3 cells. J Biol Chem 268: 2280-2283, 1993.
62. 62. Aunis D and Bader M-F, The cytoskeleton as a barrier to exocytosis in secretory cells. J Exp Biol 139: 253-266, 1988.
63. 63. Koffer A, Tatham PER and Gomperts BD, Changes in the state of actin during the exocytotic reaction of permeabilized rat mast cells. J Cell Biol 111: 919-927, 1990.
64. 64. Vitale ML, Del Castillo AR, Tchakarov L and Trifaró J-M, Cortical filamentous actin disassembly and scinderin redistribution during chromaffin eel stimulation precede exocytosis, a phenomenon not exhibited by gelsolin. J Cell Biol 113: 1057-1067, 1991.
65. 65. Greengard P, Valtorta F, Czernik AJ and Benfenati F, Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259: 780-785, 1993.
66. 66. Hartwig JH, Thelen M, Rosen A, Janmey PA, Nairn AC and Aderem A, MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature 356: 618-622, 1992.
67. 67. Turunen O, Wahlström T and Vaheri A, Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J Cell Biol 126: 1445-1453, 1994.
68. 68. Funayama N, Nagafuchi A, Sato N and Tsukita S, Radixin is a novel member of the band 4.1 family. J Cell Biol 115: 1039-1048, 1991.
69. 69. Shuster CB and Herman IM, Indirect association of ezrin with F-actin: Isoform specificity and calcium sensitivity. J Cell Biol 128: 837-848, 1995.
70. 70. Gary R and Bretscher A, Heterotypic and homotypic associations between ezrin and moesin, two putative membrane-cytoskeletal linking proteins. Proc Natl Acad Sci USA 90: 10846-10850, 1993.
71. 71. Andréoli C, Martin M, LeBorgne R, Reggio H and Mangeat P, Ezrin has properties to self-associate at the plasma membrane. J Cell Sci 107: 2509-2521, 1994.
72. 72. Gary R and Bretscher A, Ezrin self-association involves binding of an N-terminal domain to a normally masked C-terminal domain that includes the F-actin binding site. Mol Biol Cell 6: 1061-1075, 1995.
73. 2-terminal domain inhibits the cell extension activity of the COOH-terminal domain. J Cell Biol 128: 1081-1093, 1995.