Sequestration of phosphoinositides by mutated MARCKS effector domain inhibits stimulated Ca 2+ mobilization and degranulation in mast cells

Molecular Biology of the Cell

Volumn 22, Issue 24, 2011, Pages 4908-4917

  Gadi, Deepti ^a   Wagenknecht Wiesner, Alice ^a   Holowka, David ^a   Baird, Barbara ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; INOSITOL 1,4,5 TRISPHOSPHATE; MARCKS PROTEIN; PHOSPHATIDYLINOSITIDE; PROTEIN KINASE C BETA; RED FLUORESCENT PROTEIN; SERINE; THAPSIGARGIN;

ADHERENT CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CELL MEMBRANE; CONTROLLED STUDY; EXOCYTOSIS; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; MAST CELL DEGRANULATION; MEMBRANE BINDING; MUTATIONAL ANALYSIS; PHOSPHORYLATION; PRIORITY JOURNAL;

ANIMALS; ANTIGENS; CALCIUM; CELL DEGRANULATION; CELL LINE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOYLATION; MAST CELLS; MEMBRANE PROTEINS; MICE; MUTATION; PHOSPHATIDYLINOSITOLS; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN STRUCTURE, TERTIARY; SECRETORY VESICLES;

EID: 84055194029     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-07-0614     Document Type: Article

References (51)

1. Aderem A (1992). The MARCKS brothers: a family of protein kinase C substrates. Cell 71, 713-716.
2. Bai J, Tucker WC, Chapman ER (2004). PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane. Nat Struct Mol Biol 11, 36-44. (Pubitemid 38173439)
3. Barclay JW (2008). Munc-18-1 regulates the initial release rate of exocytosis. Biophys J 94, 1084-1093.
4. Blackshear PJ (1993). The MARCKS family of cellular protein kinase C substrates. J Biol Chem 268, 1501-1504.
5. Blank U, Rivera J (2004). The ins and outs of IgE-dependent mast-cell exocytosis. Trends Immunol 25, 266-273.
6. Calloway N, Vig M, Kinet JP, Holowka D, Baird B (2009). Molecular clustering of STIM1 with Orai1/CRACM1 at the plasma membrane depends dynamically on depletion of Ca2+ stores and on electrostatic interactions. Mol Biol Cell 20, 389-399.
7. Chapman ER (2002). Synaptotagmin: a Ca(2+) sensor that triggers exocytosis?. Nat Rev Mol Cell Biol 3, 498-508.
8. Cohen R, Torres A, Ma HT, Holowka D, Baird B (2009). Ca2+ waves initiate antigen-stimulated Ca2+ responses in mast cells. J Immunol 183, 6478-6488.
9. Dai H, Shen N, Arac D, Rizo J (2007). A quaternary SNARE-synaptotagmin- Ca2+-phospholipid complex in neurotransmitter release. J Mol Biol 367, 848-863. (Pubitemid 46330381)
10. Daily NJ, Boswell KL, James DJ, Martin TF (2010). Novel interactions of CAPS (Ca2+-dependent activator protein for secretion) with the three neuronal SNARE proteins required for vesicle fusion. J Biol Chem 285, 35320-35329.
11. Di Paolo G, De Camilli P (2006). Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657. (Pubitemid 44564702)
12. Dragonetti A, Baldassarre M, Castino R, Demoz M, Luini A, Buccione R, Isidoro C (2000). The lysosomal protease cathepsin D is efficiently sorted to and secreted from regulated secretory compartments in the rat basophilic/mast cell line RBL. J Cell Sci 113, 3289-3298.
13. Gambhir A, Hangyas-Mihalyne G, Zaitseva I, Cafiso DS, Wang J, Murray D, Pentyala SN, Smith SO, McLaughlin S (2004). Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys J 86, 2188-2207. (Pubitemid 38524409)
14. Gilfillan AM, Tkaczyk C (2006). Integrated signalling pathways for mast-cell activation. Nat Rev Immunol 6, 218-230.
15. Graff JM, Gordon JI, Blackshear PJ (1989a). Myristoylated and nonmyristoylated forms of a protein are phosphorylated by protein kinase C. Science 246, 503-506.
16. Graff JM, Stumpo DJ, Blackshear PJ (1989b). Characterization of the phosphorylation sites in the chicken and bovine myristoylated alanine-rich C kinase substrate protein, a prominent cellular substrate for protein kinase C. J Biol Chem 264, 11912-11919. (Pubitemid 19185362)
17. Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T (2006). PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314, 1458-1461. (Pubitemid 44871952)
18. Kim J, Blackshear PJ, Johnson JD, McLaughlin S (1994). Phosphorylation reverses the membrane association of peptides that correspond to the basic domains of MARCKS and neuromodulin. Biophys J 67, 227-237. (Pubitemid 24197888)
19. Lee H, Park C, Lee Y, Suk H, Clemons T, Choi O (2005). Antigen-induced Ca mobilization in RBL-2H3 cells: role of I(1,4,5)P and S1P and necessity of I(1,4,5)P production. Cell Calcium 38, 581-592. (Pubitemid 41614437)
20. Li L, Shin OH, Rhee JS, Arac D, Rah JC, Rizo J, Sudhof T, Rosenmund C (2006). Phosphatidylinositol phosphates as co-activators of Ca2+ binding to C2 domains of synaptotagmin 1. J Biol Chem 281, 15845-15852. (Pubitemid 43848475)
21. Ma HT, Beaven MA (2009). Regulation of Ca2+ signaling with particular focus on mast cells. Crit Rev Immunol 29, 155-186.
22. Ma HT, Peng Z, Hiragun T, Iwaki S, Gilfillan AM, Beaven MA (2008). Canonical transient receptor potential 5 channel in conjunction with Orai1 and STIM1 allows Sr2+ entry, optimal influx of Ca2+, and degranulation in a rat mast cell line. J Immunol 180, 2233-2239.
23. McLaughlin S, Murray D (2005). Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438, 605-611. (Pubitemid 41740564)
24. Melicoff E et al. (2009). Synaptotagmin-2 controls regulated exocytosis but not other secretory responses of mast cells. J Biol Chem 284, 19445-19451.
25. Metzelaar MJ, Wijngaard PL, Peters PJ, Sixma JJ, Nieuwenhuis HK, Clevers HC (1991). CD63 antigenA novel lysosomal membrane glycoprotein, cloned by a screening procedure for intracellular antigens in eukaryotic cells. J Biol Chem 266, 3239-3245. (Pubitemid 21909200)
26. Nechushtan H, Leitges M, Cohen C, Kay G, Razin E (2000). Inhibition of degranulation and interleukin-6 production in mast cells derived from mice deficient in protein kinase Cbeta. Blood 95, 1752-1757. (Pubitemid 30120839)
27. Newton AC (2010). Protein kinase C: poised to signal. Am J Physiol Endocrinol Metab 298, E395-E402. Nishizuka Y (1995). Protein kinase C and lipid signaling for sustained cellular responses. FASEB J 9, 484-496.
28. Oancea E, Meyer T (1998). Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell 95, 307-318. (Pubitemid 28507320)
29. Ozawa K, Szallasi Z, Kazanietz MG, Blumberg PM, Mischak H, Mushinski JF, Beaven MA (1993a). Ca(2+)-dependent and Ca(2+)-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. (Pubitemid 23033568)
30. Ozawa K, Yamada K, Kazanietz MG, Blumberg PM, Beaven MA (1993b). 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. (Pubitemid 23057836)
31. Paddock BE, Striegel AR, Hui E, Chapman ER, Reist NE (2008). Ca2+-dependent, phospholipid-binding residues of synaptotagmin are critical for excitation-secretion coupling in vivo. J Neurosci 28, 7458-7466.
32. Paumet F, Le Mao J, Martin S, Galli T, David B, Blank U, Roa M (2000). Soluble NSF attachment protein receptors (SNAREs) in RBL-2H3 mast cells: functional role of syntaxin 4 in exocytosis and identification of a vesicle-associated membrane protein 8-containing secretory compartment. J Immunol 164, 5850-5857. (Pubitemid 30389829)
33. Peng Z, Beaven MA (2005). An essential role for phospholipase D in the activation of protein kinase C and degranulation in mast cells. J Immunol 174, 5201-5208. (Pubitemid 40593157)
34. Posner RG, Lee B, Conrad DH, Holowka D, Baird B, Goldstein B (1992). Aggregation of IgE-receptor complexes on rat basophilic leukemia cells does not change the intrinsic affinity but can alter the kinetics of the ligand-IgE interaction. Biochemistry 31, 5350-5356.
35. Pyenta PS, Holowka D, Baird B (2001). Cross-correlation analysis of inner-leaflet-anchored green fluorescent protein co-redistributed with IgE receptors and outer leaflet lipid raft components. Biophys J 80, 2120-2132. (Pubitemid 32401978)
36. Rhee SG, Choi KD (1992). Regulation of inositol phospholipid-specific phospholipase C isozymes. J Biol Chem 267, 12393-12396.
37. Sagi-Eisenberg R (2007). The mast cell: where endocytosis and regulated exocytosis meet. Immunol Rev 217, 292-303.
38. Sagi-Eisenberg R, Lieman H, Pecht I (1985). Protein kinase C regulation of the receptor-coupled calcium signal in histamine-secreting rat basophilic leukaemia cells. Nature 313, 59-60. (Pubitemid 15192306)
39. Sander LE, Frank SP, Bolat S, Blank U, Galli T, Bigalke H, Bischoff SC, Lorentz A (2008). Vesicle associated membrane protein (VAMP)-7 and VAMP-8, but not VAMP-2 or VAMP-3, are required for activation-induced degranulation of mature human mast cells. Eur J Immunol 38, 855-863.
40. Schwarz TL (2004). Synaptotagmin promotes both vesicle fusion and recycling. Proc Natl Acad Sci USA 101, 16401-16402.
41. Smith NL, Hammond S, Gadi D, Wagenknecht-Wiesner A, Baird B, Holowka D (2010). Sphingosine derivatives inhibit cell signaling by electrostatically neutralizing polyphosphoinositides at the plasma membrane. Self Nonself 1, 133-143.
42. Stauffer TP, Ahn S, Meyer T (1998). Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Curr Biol 8, 343- 346.
43. Stumpo DJ, Graff JM, Albert KA, Greengard P, Blackshear PJ (1989). Molecular cloning, characterization, and expression of a cDNA encoding the "80- to 87-kDa" myristoylated alanine-rich C kinase substrate: a major cellular substrate for protein kinase C. Proc Natl Acad Sci USA 86, 4012-4016. (Pubitemid 19154734)
44. Suzuki R, Liu X, Olivera A, Aguiniga L, Yamashita Y, Blank U, Ambudkar I, Rivera J (2010). Loss of TRPC1-mediated Ca2+ influx contributes to impaired degranulation in Fyn-deficient mouse bone marrow-derived mast cells. J Leukoc Biol 88, 863-875.
45. Trifaro JM, Gasman S, Gutierrez LM (2008). Cytoskeletal control of vesicle transport and exocytosis in chromaffin cells. Acta Physiol (Oxf) 192, 165-172. (Pubitemid 351160992)
46. Varnai P, Balla T (1998). Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J Cell Biol 143, 501-510. (Pubitemid 28487866)
47. Vasudevan L, Jeromin A, Volpicelli-Daley L, De Camilli P, Holowka D, Baird B (2009). The beta- and gamma-isoforms of type I PIP5K regulate distinct stages of Ca2+ signaling in mast cells. J Cell Sci 122, 2567-2574.
48. Vig M, DeHaven WI, Bird GS, Billingsley JM, Wang H, Rao PE, Hutchings AB, Jouvin MH, Putney JW, Kinet JP (2008). Defective mast cell effector functions in mice lacking the CRACM1 pore subunit of store-operated calcium release-activated calcium channels. Nat Immunol 9, 89-96. (Pubitemid 350286208)
49. Wang J, Arbuzova A, Hangyas-Mihalyne G, McLaughlin S (2001). The effector domain of myristoylated alanine-rich C kinase substrate binds strongly to phosphatidylinositol 4,5-bisphosphate. J Biol Chem 276, 5012-5019.
50. Wolfe PC, Chang EY, Rivera J, Fewtrell C (1996). Differential effects of the protein kinase C activator phorbol 12-myristate 13-acetate on calcium responses and secretion in adherent and suspended RBL-2H3 mucosal mast cells. J Biol Chem 271, 6658-6665.
51. Xu K, Williams RM, Holowka D, Baird B (1998). Stimulated release of fluorescently labeled IgE fragments that efficiently accumulate in secretory granules after endocytosis in RBL-2H3 mast cells. J Cell Sci 111, 2385-2396. (Pubitemid 28434925)