LPS induces phosphorylation of actin-regulatory proteins leading to actin reassembly and macrophage motility

Journal of Cellular Biochemistry

Volumn 113, Issue 1, 2012, Pages 80-92

  Kleveta, Galyna ^a,b   Borzȩcka, Kinga ^a   Zdioruk, Mykola ^a,b   Czerkies, MacIej ^a   Kuberczyk, Hanna ^a   Sybirna, Natalia ^b   Sobota, Andrzej ^a   Kwiatkowska, Katarzyna ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b IVAN FRANKO NATIONAL UNIVERSITY OF LVIV   (Ukraine)

Author keywords

actin cytoskeleton; cell motility; LPS; N WASP; paxillin; Src kinases

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; ACTIN; CD14 ANTIGEN; CYTOCHALASIN D; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PAXILLIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; SERINE; TOLL LIKE RECEPTOR 4; TRITON X 100; TUMOR NECROSIS FACTOR ALPHA; TYROSINE;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL MOTILITY; CELL MOTION; CYTOSKELETON; ENZYME ACTIVITY; LAMELLAR BODY; MACROPHAGE; MICROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WOUND HEALING;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; ANTIGENS, CD14; CELL LINE; CELL MOVEMENT; CYTOCHALASIN D; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; NF-KAPPA B; PAXILLIN; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHORYLATION; PYRIMIDINES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 84055177155     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.23330     Document Type: Article

References (50)

1. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P,. 2007. The selectivity of protein kinase inhibitors: A further update. Biochem J 408: 297-315.
2. Bellis SL, Miller JT, Turner CE,. 1995. Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J Biol Chem 270: 17437-17441.
3. Brown MC, Turner CE,. 2004. Paxillin: Adapting to change. Physiol Rev 84: 1315-1339. (Pubitemid 39287952)
4. Cai X, Li M, Vrana J, Schaller MD,. 2006. Glycogen synthase kinase 3- and extracellular signal-regulated kinase-dependent phosphorylation of paxillin regulates cytoskeletal rearrangement. Mol Cell Biol 26: 2857-2868.
5. Continolo S, Baruzzi A, Majeed M, Caveggion E, Fumagalli L, Lowell CA, Berton G,. 2005. The proto-oncogene Fgr regulates cell migration and this requires its plasma membrane localization. Exp Cell Res 302: 253-269. (Pubitemid 39550467)
6. Cory GO, Cramer R, Blanchoin L, Ridley AJ,. 2003. Phosphorylation of the WASP-VCA domain increases its affinity for the Arp2/3 complex and enhances actin polymerization by WASP. Mol Cell 11: 1229-1239. (Pubitemid 36645142)
7. Fox JE, Boyles JK, Berndt MC, Steffen PK, Anderson LK,. 1988. Identification of a membrane skeleton in platelets. J Cell Biol 106: 1525-1538.
8. Fumagalli L, Zhang H, Baruzzi A, Lowell CA, Berton G,. 2007. The Src family kinases Hck and Fgr regulate neutrophil responses to N-formyl-methionyl- leucyl-phenylalanine. J Immunol 178: 3874-3885. (Pubitemid 46417657)
9. Hartwig JH, Shevlin P,. 1986. The architecture of actin filaments and the ultrastructural location of actin-binding protein in the periphery of lung macrophages. J Cell Biol 103: 1007-1020. (Pubitemid 17177349)
10. Hazeki K, Masuda N, Funami K, Sukenobu N, Matsumoto M, Akira S, Takeda K, Seya T, Hazeki O,. 2003. Toll-like receptor-mediated tyrosine phosphorylation of paxillin via MyD88-dependent and -independent pathways. Eur J Immunol 33: 740-747. (Pubitemid 36367677)
11. Heacock CS, Eidsvoog KE, Bamburg JR,. 1984. The influence of contact-inhibited growth and of agents which alter cell morphology on the levels of G- and F-actin in cultured cells. Exp Cell Res 153: 402-412. (Pubitemid 14089831)
12. 2 of Wiskott-Aldrich syndrome protein (WASp) stimulates actin nucleation by Arp2/3 complex. J Cell Biol 150: 1311-1320.
13. Kagan JC, Medzhitov R,. 2006. Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125: 943-955. (Pubitemid 43795199)
14. Kagan JC, Su T, Horng T, Chow A, Akira S, Medzhitov R,. 2008. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-β. Nat Immunol 9: 361-368. (Pubitemid 351405105)
15. 2 metabolism and directed cell movement in vascular epithelial cell. J Biol Chem 286: 2320-2330.
16. Kawai T, Takeuchi O, Fujita T, Inoue J, Mühlradt PF, Sato S, Hoshino K, Akira S,. 2001. Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J Immunol 167: 5887-5894. (Pubitemid 33062783)
17. Kim JY, Lee YG, Kim MY, Byeon SE, Rhee MH, Park J, Katz DR, Chain BM, Cho JY,. 2010. Src-mediated regulation of inflammatory responses by actin polymerization. Biochem Pharmacol 79: 431-443.
18. Koestler SA, Rottner K, Lai F, Block J, Vinzenz M, Small JV,. 2009. F- and G-actin concentrations in lamellipodia of moving cells. PLoS ONE 4: e4810.
19. Kong L, Ge BX,. 2008. MyD88-independent activation of a novel actin-Cdc42/Rac pathway is required for Toll-like receptor-stimulated phagocytosis. Cell Res 18: 745-755. (Pubitemid 351948225)
20. Kulma M, Herec M, Grudzinski W, Anderluh G, Gruszecki WI, Kwiatkowska K, Sobota A,. 2010. Sphingomyelin-rich domains are sites of lysenin oligomerization: Implications for raft studies. Biochim Biophys Acta 1798: 471-481.
21. Kwiatkowska K, Frey J, Sobota A,. 2003. Phosphorylation of FcγRIIA is required for the receptor-induced actin rearrangement and capping: The role of membrane rafts. J Cell Sci 116: 537-550. (Pubitemid 36236121)
22. Laukaitis CM, Webb DJ, Donais K, Horwitz AF,. 2001. Differential dynamics of α5 integrin, paxillin, and alpha-actinin during formation and disassembly of adhesions in migrating cells. J Cell Biol 153: 1427-1440. (Pubitemid 34286127)
23. Lowell CA, Berton G,. 1988. Resistance to endotoxic shock and reduced neutrophil migration in mice deficient for the Src-family kinases Hck and Fgr. Proc Natl Acad Sci USA 95: 7580-7584.
24. Lu YC, Yeh WC, Ohashi PS,. 2008. LPS/TLR4 signal transduction pathway. Cytokine 42: 145-151.
25. Maa MC, Chang MY, Chen YJ, Lin CH, Yu CJ, Yang YL, Li J, Chen PR, Tang CH, Lei HY, Leu TH,. 2008. Requirement of inducible nitric-oxide synthase in lipopolysaccharide-mediated Src induction and macrophage migration. J Biol Chem 283: 31408-31416.
26. Machesky LM, Insall RH,. 1998. Scar1 and the related Wiskott-Aldrich syndrome protein WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr Biol 8: 1347-1356. (Pubitemid 29020143)
27. Manders EMM, Verbkeed FJ, Aten JA,. 1993. Measurements of co-localization of objects in dual-color confocal images. J Microsc 169: 375-382. (Pubitemid 23119681)
28. McGettrick AF, O'Neill LA,. 2010. Regulators of TLR4 signaling by endotoxins. Subcell Biochem 53: 153-171.
29. Medvedev AE, Piao W, Shoenfelt J, Rhee SH, Chen H, Basu S, Wahl LM, Fenton MJ, Vogel S,. 2007. Role of TLR4 tyrosine phosphorylation in signal transduction and endotoxin tolerance. J Biol Chem 282: 16042-16453.
30. Miki H, Miura K, Takenawa T,. 1996. N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases. EMBO J 15: 5326-5335. (Pubitemid 26336215)
31. Nakagawa H, Miki H, Ito M, Ohashi K, Takenawa T, Miyamoto S,. 2001. N-WASP, WAVE and Mena play different roles in the organization of actin cytoskeleton in lamellipodia. J Cell Sci 114: 1555-1565. (Pubitemid 32427841)
32. Nakamura K, Yano H, Uchida H, Hashimoto S, Schaefer E, Sabe H,. 2000. Tyrosine phosphorylation of paxillin α is involved in temporospatial regulation of paxillin-containing focal adhesion formation and F-actin organization in motile cells. J Biol Chem 275: 27155-27164.
33. Park BS, Song DH, Kim HM, Choi BS, Lee H, Lee JO,. 2009. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458: 1191-1195.
34. Petit V, Boyer B, Lentz D, Turner CE, Thiery JP, Valles AM,. 2000. Phosphorylation of tyrosine residues 31 and 118 on paxillin regulates cell migration through an association with CRK in NBT-II cells. J Cell Biol 148: 957-970.
35. Pollard TD, Borisy GG,. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465. (Pubitemid 36263079)
36. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B,. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science 282: 2085-2088. (Pubitemid 29001265)
37. Rohatgi R, Ho HY, Kirschner MW,. 2000. Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4,5-bisphosphate. J Cell Biol 150: 1299-1310.
38. Rossol M, Gartner D, Hauschildt S,. 2001. Diverse regulation of microfilament assembly, production of TNF-α, and reactive oxygen intermediates by actib modulating substance and inhibitors of ADP-ribosylation in human monocytes stimulated with LPS. Cell Motil Cytoskeleton 48: 96-108. (Pubitemid 32116357)
39. Schaller MD, Parsons JT,. 1995. pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol Cell Biol 15: 2635-2645.
40. Schaller MD, Schaefer EM,. 2001. Multiple stimuli induce tyrosine phosphorylation of the Crk-binding sites of paxillin. Biochem J 360: 57-66. (Pubitemid 33081949)
41. Suen PW, Ilic D, Caveggion E, Berton G, Damsky CH, Lowell CA,. 1999. Impaired integrin-mediated signal transduction, altered cytoskeletal structure and reduced motility in Hck/Fgr deficient macrophages. J Cell Sci 112: 4067-4078. (Pubitemid 30119775)
42. Szymanska E, Korzeniowski M, Raynal P, Sobota A, Kwiatkowska K,. 2009. Contribution of PIP-5 kinase Iα to raft-based FcγRIIA signaling. Exp Cell Res 315: 981-995.
43. 2. J Pharmacol Exp Ther 326: 493-501.
44. 2. Biochemistry 46: 3494-3502. (Pubitemid 46449166)
45. Vindis C, Teli T, Cerretti DP, Turner CE, Huynh-Do U,. 2004. EphB1-mediated cell migration requires the phosphorylation of paxillin at Tyr-31/Tyr-118. J Biol Chem 279: 27965-27970. (Pubitemid 38900065)
46. Weintz G, Olsen JV, Fruhauf K, Niedzielska M, Amit I, Jantsch J, Mages J, Frech C, Dolken L, Mann M, Lang R,. 2010. The phosphoproteome of toll-like receptor-activated macrophages. Mol Syst Biol 6: 371.
47. Williams LM, Ridley AJ,. 2000. Lipopolysaccharide induces actin reorganization and tyrosine phosphorylation of Pyk2 and paxillin in monocytes and macrophages. J Immunol 164: 2028-2036. (Pubitemid 30108760)
48. Wu X, Suetsugu S, Cooper LA, Takenawa T, Guan J-L,. 2004. Focal adhesion kinase regulation of N-WASP subcellular localization and function. J Biol Chem 279: 9565-9576. (Pubitemid 38296025)
49. Yano H, Uchida H, Iwasaki T, Mukai M, Akedo H, Nakamura K, Hashimoto S, Sabe H,. 2000. Paxillin α and Crk-associated substrate exert opposing effects on cell migration and contact inhibition of growth through tyrosine phosphorylation. Proc Natl Acad Sci USA 97: 9076-9081. (Pubitemid 30626676)
50. Zemans RL, Arndt PG,. 2009. Tec kinases regulate actin assembly and cytokine expression in LPS-stimulated human neutrophils via JNK activation. Cell Immunol 258: 90-97.