Role of iPLA2 in the regulation of Src trafficking and microglia chemotaxis

Traffic

Volumn 12, Issue 7, 2011, Pages 878-889

  Lee, Sang Hyun ^a   Schneider, Claus ^a   Higdon, Ashlee N ^b   Darley Usmar, Victor M ^b   Chung, Chang Y ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Arachidonic acid; Chemotaxis; cSrc; Microglia; Phospholipase A2; Recycling endosome

Indexed keywords

ADENOSINE DIPHOSPHATE; ARACHIDONIC ACID; CALCIUM INDEPENDENT PHOSPHOLIPASE A2; CALCIUM ION; GREEN FLUORESCENT PROTEIN; LACTONE DERIVATIVE; PHOSPHATIDYLINOSITOL 3 KINASE; STEROID RECEPTOR COACTIVATOR 1;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CHEMOTAXIS; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FOCAL ADHESION; GENE SILENCING; HOMEOSTASIS; INTRACELLULAR TRANSPORT; MICROGLIA; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT;

ADENOSINE DIPHOSPHATE; ANIMALS; ARACHIDONIC ACID; BIOLOGICAL TRANSPORT; BORON COMPOUNDS; CELL LINE; CELL MEMBRANE; CELL SURFACE EXTENSIONS; CHEMOTAXIS; ENDOSOMES; ENZYME ACTIVATION; ENZYME INHIBITORS; FLUORESCENT DYES; FOCAL ADHESIONS; MICROGLIA; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOLIPASES A2, CALCIUM-INDEPENDENT; RECOMBINANT FUSION PROTEINS; SRC-FAMILY KINASES;

EID: 79958765853     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01195.x     Document Type: Article

References (54)

1. Haugh JM, Codazzi F, Teruel M, Meyer T. Spatial sensing in fibroblasts mediated by 3' phosphoinositides. J Cell Biol 2000;151: 1269-1280.
2. Parent CA, Blacklock BJ, Froehlich WM, Murphy DB, Devreotes PN. G protein signaling events are activated at the leading edge of chemotactic cells. Cell 1998;95:81-91.
3. Rickert P, Weiner OD, Wang F, Bourne HR, Servant G. Leukocytes navigate by compass: roles of PI3Kgamma and its lipid products. Trends Cell Biol 2000;10:466-473.
4. Wang F, Herzmark P, Weiner OD, Srinivasan S, Servant G, Bourne HR. Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nat Cell Biol 2002;4:513-518.
5. Weiner OD, Neilsen PO, Prestwich GD, Kirschner MW, Cantley LC, Bourne HR. A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat Cell Biol 2002;4:509-513.
6. Chen L, Iijima M, Tang M, Landree MA, Huang YE, Xiong Y, Iglesias PA, Devreotes PN. PLA2 and PI3K/PTEN pathways act in parallel to mediate chemotaxis. Dev Cell 2007;12:603-614.
7. van Haastert PJ, Keizer-Gunnink I, Kortholt A. Essential role of PI3-kinase and phospholipase A2 in Dictyostelium discoideum chemotaxis. J Cell Biol 2007;177:809-816.
8. Chakraborti S. Phospholipase A(2) isoforms: a perspective. Cell Signal 2003;15:637-665.
9. Balsinde J, Balboa MA, Insel PA, Dennis EA. Regulation and inhibition of phospholipase A2. Annu Rev Pharmacol Toxicol 1999;39:175-189.
10. Jenkins CM, Mancuso DJ, Yan W, Sims HF, Gibson B, Gross RW. Identification, cloning, expression, and purification of three novel human calcium-independent phospholipase A2 family members possessing triacylglycerol lipase and acylglycerol transacylase activities. J Biol Chem 2004;279:48968-48975.
11. Jenkins CM, Han X, Mancuso DJ, Gross RW. Identification of calcium-independent phospholipase A2 (iPLA2) beta, and not iPLA2gamma, as the mediator of arginine vasopressin-induced arachidonic acid release in A-10 smooth muscle cells. Enantioselective mechanism-based discrimination of mammalian iPLA2s. J Biol Chem 2002;277:32807-32814.
12. Carnevale KA, Cathcart MK. Calcium-independent phospholipase A(2) is required for human monocyte chemotaxis to monocyte chemoattractant protein 1. J Immunol 2001;167:3414-3421.
13. Mishra RS, Carnevale KA, Cathcart MK. iPLA2beta: front and center in human monocyte chemotaxis to MCP-1. J Exp Med 2008;205: 347-359.
14. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka S. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 2001; 21:1975-1982.
15. Inoue K. Microglial activation by purines and pyrimidines. Glia 2002; 40:156-163.
16. Ohsawa K, Irino Y, Nakamura Y, Akazawa C, Inoue K, Kohsaka S. Involvement of P2X4 and P2Y12 receptors in ATP-induced microglial chemotaxis. Glia 2007;55:604-616.
17. Lee S, Chung CY. Role of VASP phosphorylation for the regulation of microglia chemotaxis via the regulation of focal adhesion formation/maturation Mol Cell Neurosci 2009;42:382-390.
18. Rodriguez-Viciana P, Warne PH, Dhand R, Vanhaesebroeck B, Gout I, Fry MJ, Waterfield MD, Downward J. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 1994;370:527-532.
19. Pleiman CM, Hertz WM, Cambier JC. Activation of phosphatidylino sitol-3' kinase by Src-family kinase SH3 binding to the p85 subunit. Science 1994;263:1609-1612.
20. Bjorge JD, Jakymiw A, Fujita DJ. Selected glimpses into the activation and function of Src kinase. Oncogene 2000;19:5620-5635.
21. Huveneers S, Danen EHJ. Adhesion signaling-crosstalk between integrins, Src and Rho. J Cell Sci 2009;122:1059-1069.
22. Kaplan KB, Swedlow JR, Varmus HE, Morgan DO. Association of p60c-src with endosomal membranes in mammalian fibroblasts. J Cell Biol 1992;118:321-333.
23. Fincham VJ, Unlu M, Brunton VG, Pitts JD, Wyke JA, Frame MC. Translocation of Src kinase to the cell periphery is mediated by the actin cytoskeleton under the control of the Rho family of small G proteins. J Cell Biol 1996;135:1551-1564.
24. Sandilands E, Cans C, Fincham VJ, Brunton VG, Mellor H, Prendergast GC, Norman JC, Superti-Furga G, Frame MC. RhoB and actin polymerization coordinate Src activation with endosome-mediated delivery to the membrane. Dev Cell 2004;7:855-869.
25. Nakamura N, Rabouille C, Watson R, Nilsson T, Hui N, Slusarewicz P, Kreis TE, Warren G. Characterization of a cis-Golgi matrix protein, GM130. J Cell Biol 1995;131:1715-1726.
26. Lippincott-Schwartz J, Yuan LC, Bonifacino JS, Klausner RD. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 1989;56:801-813.
27. Kaplan KB, Bibbins KB, Swedlow JR, Arnaud M, Morgan DO, Varmus HE. Association of the amino-terminal half of c-Src with focal adhesions alters their properties and is regulated by phosphorylation of tyrosine 527. EMBO J 1994;13:4745-4756.
28. Sandilands E, Frame MC. Endosomal trafficking of Src tyrosine kinase. Trends Cell Biol 2008;18:322-329.
29. Feng Y, Press B, Wandinger-Ness A. Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 1995;131:1435-1452.
30. Vonderheit A, Helenius A. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 2005;3:e233.
31. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 1996;135:913-924.
32. Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol 2004;5:121-132.
33. Hirschberg K, Lippincott-Schwartz J. Secretory pathway kinetics and in vivo analysis of protein traffic from the Golgi complex to the cell surface. FASEB J. 1999;S2:S251-256.
34. Higdon AN, Dranka BP, Hill BG, Oh JY, Johnson MS, Landar A, Darley-Usmar VM. Methods for imaging and detecting modification of proteins by reactive lipid species. Free Radic Biol Med 2009;47:201-212.
35. Baruzzi A, Caveggion E, Berton G. Regulation of phagocyte migration and recruitment by Src-family kinases. Cell Mol Life Sci 2008;65:2175-2190.
36. Brown WJ, Chambers K, Doody A. Phospholipase A2 (PLA2) enzymes in membrane trafficking: mediators of membrane shape and function. Traffic 2003;4:214-221.
37. Christiansson A, Kuypers FA, Roelofsen B, Op den Kamp JA, van Deenen LL. Lipid molecular shape affects erythrocyte morphology: a study involving replacement of native phosphatidylcholine with different species followed by treatment of cells with sphingomyelinase C or phospholipase A2. J Cell Biol 1985;101:1455-1462.
38. Israelachvili JN, Marcelja S, Horn RG. Physical principles of membrane organization. Q Rev Biophys 1980;13:121-200.
39. Mui BL, Dobereiner HG, Madden TD, Cullis PR. Influence of transbilayer area asymmetry on the morphology of large unilamellar vesicles. Biophys J 1995;69:930-941.
40. de Figueiredo P, Drecktrah D, Katzenellenbogen JA, Strang M, Brown WJ. Evidence that phospholipase A2 activity is required for Golgi complex and trans Golgi network membrane tubulation. Proc Natl Acad Sci U S A 1998;95:8642-8647.
41. Drecktrah D, Brown WJ. Phospholipase A(2) antagonists inhibit nocodazole-induced Golgi ministack formation: evidence of an ER intermediate and constitutive cycling. Mol Biol Cell 1999;10: 4021-4032.
42. Chambers K, Judson B, Brown WJ. A unique lysophospholipid acyltransferase (LPAT) antagonist, CI-976, affects secretory and endocytic membrane trafficking pathways. J Cell Sci 2005;118:3061-3071.
43. de Figueiredo P, Doody A, Polizotto ReS, Drecktrah D, Wood S, Banta M, Strang MS, Brown WJ. Inhibition of transferrin recycling and endosome tubulation by phospholipase A2 antagonists. J Biol Chem 2001;276:47361-47370.
44. Wilcke M, Johannes L, Galli T, Mayau V, Goud B, Salamero J. Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J Cell Biol 2000;151:1207-1220.
45. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000;1:31-39.
46. Gagescu R, Demaurex N, Parton RG, Hunziker W, Huber LA, Gruenberg J. The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol Biol Cell 2000;11:2775-2791.
47. Seong J, Lu S, Ouyang M, Huang H, Zhang J, Frame MC, Wang Y. Visualization of Src activity at different compartments of the plasma membrane by FRET imaging. Chem Biol 2009;16:48-57.
48. Klopfenstein DR, Holleran EA, Vale RD. Kinesin motors and microtubule-based organelle transport in Dictyostelium discoideum. J Muscle Res Cell Motil 2002;23:631-638.
49. Klopfenstein DR, Vale RD. The lipid binding pleckstrin homology domain in UNC-104 kinesin is necessary for synaptic vesicle transport in Caenorhabditis elegans. Mol Biol Cell 2004;15:3729-3739.
50. Hoepfner S, Severin F, Cabezas A, Habermann B, Runge A, Gillooly D, Stenmark H, Zerial M. Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 2005;121:437-450.
51. Kasahara K, Nakayama Y, Kihara A, Matsuda D, Ikeda K, Kuga T, Fukumoto Y, Igarashi Y, Yamaguchi N. Rapid trafficking of c-Src, a non-palmitoylated Src-family kinase, between the plasma membrane and late endosomes/lysosomes. Exp Cell Res 2007;313: 2651-2666.
52. Liang X, Nazarian A, Erdjument-Bromage H, Bornmann W, Tempst P, Resh MD. Heterogeneous fatty acylation of Src family kinases with polyunsaturated fatty acids regulates raft localization and signal transduction. J Biol Chem 2001;276:30987-30994.
53. Berthiaume L, Resh MD. Biochemical characterization of a palmitoyl acyltransferase activity that palmitoylates myristoylated proteins. J Biol Chem 1995;270:22399-22405.
54. O'Connor KL, Shaw LM, Mercurio AM. Release of cAMP gating by the alpha6beta4 integrin stimulates lamellae formation and the chemotactic migration of invasive carcinoma cells. J Cell Biol 1998; 143:1749-1760.