Quantitative kinetic study of the actin-bundling protein L-plastin and of its impact on actin turn-over

PLoS ONE

Volumn 5, Issue 2, 2010, Pages

  Al Tanoury, Ziad ^a   Schaffner Reckinger, Elisabeth ^a   Halavatyi, Aliaksandr ^a   Hoffmann, Céline ^b   Moes, Michéle ^a   Hadzic, Ermin ^a   Catillon, Marie ^a   Yatskou, Mikalai ^a   Friederich, Evelyne ^a  

^a UNIVERSITY OF LUXEMBOURG   (Luxembourg)

^b LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CORTACTIN; ISOENZYME; L PLASTIN; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C DELTA; SERINE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR ETV6; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING KINETICS; CARCINOMA CELL; CYTOSKELETON; DISSOCIATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MATHEMATICAL MODEL; NONHUMAN; PROTEIN BINDING; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN POLYMERIZATION; QUANTITATIVE ANALYSIS; STEADY STATE; VERO CELL;

ACTINS; ALGORITHMS; AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; CORTACTIN; CYTOSKELETON; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FOCAL ADHESIONS; GREEN FLUORESCENT PROTEINS; HUMANS; KINETICS; MEMBRANE GLYCOPROTEINS; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE C-DELTA; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SERINE; TETRADECANOYLPHORBOL ACETATE; TRANSFECTION; VERO CELLS;

SIMIAE;

EID: 77957307723     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009210     Document Type: Article

References (59)

1. Fidler IJ (1999) Critical determinants of cancer metastasis: rationale for therapy. Cancer Chemother Pharmacol 43 Suppl: S3-10.
2. Matsushima K, Shiroo M, Kung HF, Copeland TD (1988) Purification and characterization of a cytosolic 65-kilodalton phosphoprotein in human leukocytes whose phosphorylation is augmented by stimulation with interleukin 1. Biochemistry 27: 3765-3770.
3. Lapillonne A, Coue O, Friederich E, Nicolas A, Del Maestro L, et al. (2000) Expression patterns of L-plastin isoform in normal and carcinomatous breast tissues. Anticancer Res 20: 3177-3182.
4. Park T, Chen ZP, Leavitt J (1994) Activation of the leukocyte plastin gene occurs in most human cancer cells. Cancer Res 54: 1775-1781.
5. Lin CS, Park T, Chen ZP, Leavitt J (1993) Human plastin genes. Comparative gene structure, chromosome location, and differential expression in normal and neoplastic cells. J Biol Chem 268: 2781-2792.
6. Goldstein D, Djeu J, Latter G, Burbeck S, Leavitt J (1985) Abundant synthesis of the transformation-induced protein of neoplastic human fibroblasts, plastin, in normal lymphocytes. Cancer Res 45: 5643-5647.
7. Lin CS, Chen ZP, Park T, Ghosh K, Leavitt J (1993) Characterization of the human L-plastin gene promoter in normal and neoplastic cells. J Biol Chem 268: 2793-2801.
8. Klemke M, Rafael MT, Wabnitz GH, Weschenfelder T, Konstandin MH, et al. (2007) Phosphorylation of ectopically expressed L-plastin enhances invasiveness of human melanoma cells. Int J Cancer 120: 2590-2599.
9. Janji B, Giganti A, De Corte V, Catillon M, Bruyneel E, et al. (2006) Phosphorylation on Ser5 increases the F-actin-binding activity of L-plastin and promotes its targeting to sites of actin assembly in cells. J Cell Sci 119: 1947-1960.
10. Stossel TP, Condeelis J, Cooley L, Hartwig JH, Noegel A, et al. (2001) Filamins as integrators of cell mechanics and signalling. Nat Rev Mol Cell Biol 2: 138-145.
11. Matsudaira P (1991) Modular organization of actin crosslinking proteins. Trends Biochem Sci 16: 87-92.
12. Gimona M, Djinovic-Carugo K, Kranewitter WJ, Winder SJ (2002) Functional plasticity of CH domains. FEBS Lett 513: 98-106.
13. Klein MG, Shi W, Ramagopal U, Tseng Y, Wirtz D, et al. (2004) Structure of the actin crosslinking core of fimbrin. Structure 12: 999-1013.
14. Galkin VE, Orlova A, Cherepanova O, Lebart MC, Egelman EH (2008) Highresolution cryo-EM structure of the F-actin-fimbrin/plastin ABD2 complex. Proc Natl Acad Sci U S A 105: 1494-1498.
15. Bretscher A (1981) Fimbrin is a cytoskeletal protein that crosslinks F-actin in vitro. Proc Natl Acad Sci U S A 78: 6849-6853.
16. de Arruda MV, Watson S, Lin CS, Leavitt J, Matsudaira P (1990) Fimbrin is a homologue of the cytoplasmic phosphoprotein plastin and has domains homologous with calmodulin and actin gelation proteins. J Cell Biol 111: 1069-1079.
17. Arpin M, Friederich E, Algrain M, Vernel F, Louvard D (1994) Functional differences between L- and T-plastin isoforms. J Cell Biol 127: 1995-2008.
18. Jones SL, Brown EJ (1996) FcgammaRII-mediated adhesion and phagocytosis induce L-plastin phosphorylation in human neutrophils. J Biol Chem 271: 14623-14630.
19. Babb SG, Matsudaira P, Sato M, Correia I, Lim SS (1997) Fimbrin in podosomes of monocyte-derived osteoclasts. Cell Motil Cytoskeleton 37: 308-325.
20. Lebart MC, Hubert F, Boiteau C, Venteo S, Roustan C, et al. (2004) Biochemical characterization of the L-plastin-actin interaction shows a resemblance with that of alpha-actinin and allows a distinction to be made between the two actin-binding domains of the molecule. Biochemistry 43: 2428-2437.
21. Adams AE, Shen W, Lin CS, Leavitt J, Matsudaira P (1995) Isoform-specific complementation of the yeast sac6 null mutation by human fimbrin. Mol Cell Biol 15: 69-75.
22. Lin CS, Lau A, Lue TF (1998) Analysis and mapping of plastin phosphorylation. DNA Cell Biol 17: 1041-1046.
23. Shinomiya H, Hagi A, Fukuzumi M, Mizobuchi M, Hirata H, et al. (1995) Complete primary structure and phosphorylation site of the 65-kDa macrophage protein phosphorylated by stimulation with bacterial lipopolysaccharide. J Immunol 154: 3471-3478.
24. Wang J, Brown EJ (1999) Immune complex-induced integrin activation and Lplastin phosphorylation require protein kinase A. J Biol Chem 274: 24349-24356.
25. Paclet MH, Davis C, Kotsonis P, Godovac-Zimmermann J, Segal AW, et al. (2004) N-Formyl peptide receptor subtypes in human neutrophils activate Lplastin phosphorylation through different signal transduction intermediates. Biochem J 377: 469-477.
26. Vignjevic D, Kojima S, Aratyn Y, Danciu O, Svitkina T, et al. (2006) Role of fascin in filopodial protrusion. J Cell Biol 174: 863-875.
27. Weisswange I, Newsome TP, Schleich S, Way M (2009) The rate of N-WASP exchange limits the extent of ARP2/3-complex-dependent actin-based motility. Nature 458: 87-91.
28. Lippincott-Schwartz J, Patterson GH (2003) Development and use of fluorescent protein markers in living cells. Science 300: 87-91.
29. Sprague BL, McNally JG (2005) FRAP analysis of binding: proper and fitting. Trends Cell Biol 15: 84-91.
30. Hotulainen P, Lappalainen P (2006) Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol 173: 383-394.
31. Sprague BL, Pego RL, Stavreva DA, McNally JG (2004) Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys J 86: 3473-3495.
32. Hofmann WA, de Lanerolle P (2006) Nuclear actin: to polymerize or not to polymerize. J Cell Biol 172: 495-496.
33. Messier JM, Shaw LM, Chafel M, Matsudaira P, Mercurio AM (1993) Fimbrin localized to an insoluble cytoskeletal fraction is constitutively phosphorylated on its headpiece domain in adherent macrophages. Cell Motil Cytoskeleton 25: 223-233.
34. Woodsome TP, Eto M, Everett A, Brautigan DL, Kitazawa T (2001) Expression of CPI-17 and myosin phosphatase correlates with Ca(2+) sensitivity of protein kinase C-induced contraction in rabbit smooth muscle. J Physiol 535: 553-564.
35. Zhou LY, Disatnik M, Herron GS, Mochly-Rosen D, Karasek MA (1996) Differential activation of protein kinase C isozymes by phorbol ester and collagen in human skin microvascular endothelial cells. J Invest Dermatol 107: 248-252.
36. Hai CM, Hahne P, Harrington EO, Gimona M (2002) Conventional protein kinase C mediates phorbol-dibutyrate-induced cytoskeletal remodeling in a7r5 smooth muscle cells. Exp Cell Res 280: 64-74.
37. Janji B, Vallar L, Al-Tanoury Z, Bernardin F, Vetter G, et al. (2009) The actin filament cross-linker L-plastin confers resistance to TNF-alpha in MCF-7 breast cancer cells in a phosphorylation-dependent manner. J Cell Mol Med.
38. Daly RJ (2004) Cortactin signalling and dynamic actin networks. Biochem J 382: 13-25.
39. Hiroyama M, Exton JH (2005) Studies of the roles of ADP-ribosylation factors and phospholipase D in phorbol ester-induced membrane ruffling. J Cell Physiol 202: 608-622.
40. Rothbauer U, Zolghadr K, Muyldermans S, Schepers A, Cardoso MC, et al. (2008) A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins. Mol Cell Proteomics 7: 282-289.
41. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, et al. (1993) Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976. J Biol Chem 268: 9194-9197.
42. Ono Y, Fujii T, Ogita K, Kikkawa U, Igarashi K, et al. (1989) Protein kinase C zeta subspecies from rat brain: its structure, expression, and properties. Proc Natl Acad Sci U S A 86: 3099-3103.
43. Basu A, Mohanty S, Sun B (2001) Differential sensitivity of breast cancer cells to tumor necrosis factor-alpha: involvement of protein kinase C. Biochem Biophys Res Commun 280: 883-891.
44. Liedtke CM, Hubbard M, Wang X (2003) Stability of actin cytoskeleton and PKC-delta binding to actin regulate NKCC1 function in airway epithelial cells. Am J Physiol Cell Physiol 284: C487-496.
45. Chen CL, Hsieh YT, Chen HC (2007) Phosphorylation of adducin by protein kinase Cdelta promotes cell motility. J Cell Sci 120: 1157-1167.
46. Giganti A, Plastino J, Janji B, Van Troys M, Lentz D, et al. (2005) Actin-filament cross-linking protein T-plastin increases Arp2/3-mediated actin-based movement. J Cell Sci 118: 1255-1265.
47. Pal Sharma C, Goldmann WH (2004) Phosphorylation of actin-binding protein (ABP-280; filamin) by tyrosine kinase p56lck modulates actin filament crosslinking. Cell Biol Int 28: 935-941.
48. Lacroix M, Haibe-Kains B, Hennuy B, Laes JF, Lallemand F, et al. (2004) Gene regulation by phorbol 12-myristate 13-acetate in MCF-7 and MDA-MB-231, two breast cancer cell lines exhibiting highly different phenotypes. Oncol Rep 12: 701-707.
49. Lee SO, Jeong YJ, Kim M, Kim CH, Lee IS (2008) Suppression of PMA-induced tumor cell invasion by capillarisin via the inhibition of NF-kappaB-dependent MMP-9 expression. Biochem Biophys Res Commun 366: 1019-1024.
50. Shiroo M, Matsushima K (1990) Enhanced phosphorylation of 65 and 74 kDa proteins by tumor necrosis factor and interleukin-1 in human peripheral blood mononuclear cells. Cytokine 2: 13-20.
51. Jones SL, Wang J, Turck CW, Brown EJ (1998) A role for the actin-bundling protein L-plastin in the regulation of leukocyte integrin function. Proc Natl Acad Sci U S A 95: 9331-9336.
52. Le Clainche C, Carlier MF (2008) Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol Rev 88: 489-513.
53. Delanote V, Vanloo B, Catillon M, Friederich E, Vandekerckhove J, et al. (2009) An alpaca single-domain antibody blocks filopodia formation by obstructing L-plastin-mediated F-actin bundling. Faseb J.
54. Lai FP, Szczodrak M, Oelkers JM, Ladwein M, Acconcia F, et al. (2009) Cortactin promotes migration and platelet-derived growth factor-induced actin reorganization by signaling to Rho-GTPases. Mol Biol Cell 20: 3209-3223.
55. Weed SA, Parsons JT (2001) Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20: 6418-6434.
56. Weed SA, Karginov AV, Schafer DA, Weaver AM, Kinley AW, et al. (2000) Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J Cell Biol 151: 29-40.
57. Toneguzzo F, Hayday AC, Keating A (1986) Electric field-mediated DNA transfer: transient and stable gene expression in human and mouse lymphoid cells. Mol Cell Biol 6: 703-706.
58. Friederich E, Vancompernolle K, Louvard D, Vandekerckhove J (1999) Villin function in the organization of the actin cytoskeleton. Correlation of in vivo effects to its biochemical activities in vitro. J Biol Chem 274: 26751-26760.
59. Phair RD, Gorski SA, Misteli T (2004) Measurement of dynamic protein binding to chromatin in vivo, using photobleaching microscopy. Methods Enzymol 375: 393-414.