L-plastin nanobodies perturb matrix degradation, podosome formation, stability and lifetime in THP-1 macrophages

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  De Clercq, Sarah ^a   Boucherie, Ciska ^a   Vandekerckhove, Joël ^a   Gettemans, Jan ^a   Guillabert, Aude ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN CYTOSKELETON; CELL LINE, TUMOR; EXTRACELLULAR MATRIX; GELATIN; GELSOLIN; HUMANS; MACROPHAGES; MATRIX METALLOPROTEINASES, SECRETED; MEMBRANE GLYCOPROTEINS; MICROFILAMENT PROTEINS; ORGANELLES; PHOSPHOPROTEINS; PROTEIN TRANSPORT; PROTEOLYSIS; SINGLE-DOMAIN ANTIBODIES;

EID: 84893560207     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078108     Document Type: Article

References (79)

1. Burns S, Thrasher AJ, Blundell MP, Machesky L, Jones GE (2001) Configuration of human dendritic cell cytoskeleton by Rho GTPases, the WAS protein, and differentiation. Blood 98: 1142-1149.
2. Destaing O, Saltel F, Geminard JC, Jurdic P, Bard F (2003) Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin-green fluorescent protein. Mol Biol Cell 14: 407-416.
3. Linder S, Nelson D, Weiss M, Aepfelbacher M (1999) Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc Natl Acad Sci U S A 96: 9648-9653.
4. Osiak AE, Zenner G, Linder S (2005) Subconfluent endothelial cells form podosomes downstream of cytokine and RhoGTPase signaling. Exp Cell Res 307: 342-353.
5. Varon C, Tatin F, Moreau V, Van Obberghen-Schilling E, Fernandez-Sauze S, et al. (2006) Transforming growth factor beta induces rosettes of podosomes in primary aortic endothelial cells. Mol Cell Biol 26: 3582-3594.
6. 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.
7. Tatin F, Varon C, Genot E, Moreau V (2006) A signalling cascade involving PKC, Src and Cdc42 regulates podosome assembly in cultured endothelial cells in response to phorbol ester. J Cell Sci 119: 769-781.
8. Weaver AM (2006) Invadopodia: specialized cell structures for cancer invasion. Clin Exp Metastasis 23: 97-105.
9. Calle Y, Burns S, Thrasher AJ, Jones GE (2006) The leukocyte podosome. Eur J Cell Biol 85: 151-157.
10. Linder S, Aepfelbacher M (2003) Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol 13: 376-385.
11. Ochs HD (2001) The Wiskott-Aldrich syndrome. Clin Rev Allergy Immunol 20: 61-86.
12. Luxenburg C, Geblinger D, Klein E, Anderson K, Hanein D, et al. (2007) The architecture of the adhesive apparatus of cultured osteoclasts: from podosome formation to sealing zone assembly. PLoS One 2: e179.
13. Leavitt J (1994) Discovery and characterization of two novel human cancer-related proteins using two-dimensional gel electrophoresis. Electrophoresis 15: 345-357.
14. Park T, Chen ZP, Leavitt J (1994) Activation of the leukocyte plastin gene occurs in most human cancer cells. Cancer Res 54: 1775-1781.
15. Namba Y, Ito M, Zu Y, Shigesada K, Maruyama K (1992) Human T cell L-plastin bundles actin filaments in a calcium-dependent manner. J Biochem 112: 503-507.
16. 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.
17. Khurana S, George SP (2008) Regulation of cell structure and function by actin-binding proteins: villin's perspective. FEBS Lett 582: 2128-2139.
18. Yin HL, Stossel TP (1979) Control of cytoplasmic actin gel-sol transformation by gelsolin, a calcium-dependent regulatory protein. Nature 281: 583-586.
19. Yin HL, Stossel TP (1980) Purification and structural properties of gelsolin, a Ca2+-activated regulatory protein of macrophages. J Biol Chem 255: 9490-9493.
20. Young CL, Southwick FS, Weber A (1990) Kinetics of the interaction of a 41-kilodalton macrophage capping protein with actin: promotion of nucleation during prolongation of the lag period. Biochemistry 29: 2232-2240.
21. Yu FX, Johnston PA, Sudhof TC, Yin HL (1990) gCap39, a calcium ion- and polyphosphoinositide-regulated actin capping protein. Science 250: 1413-1415.
22. Silacci P, Mazzolai L, Gauci C, Stergiopulos N, Yin HL, et al. (2004) Gelsolin superfamily proteins: key regulators of cellular functions. Cell Mol Life Sci 61: 2614-2623.
23. Cooper JA, Schafer DA (2000) Control of actin assembly and disassembly at filament ends. Curr Opin Cell Biol 12: 97-103.
24. Witke W, Li W, Kwiatkowski DJ, Southwick FS (2001) Comparisons of CapG and gelsolin-null macrophages: demonstration of a unique role for CapG in receptor-mediated ruffling, phagocytosis, and vesicle rocketing. J Cell Biol 154: 775-784.
25. De Corte V, Bruyneel E, Boucherie C, Mareel M, Vandekerckhove J, et al. (2002) Gelsolin-induced epithelial cell invasion is dependent on Ras-Rac signaling. EMBO J 21: 6781-6790.
26. Van den Abbeele A, De Corte V, Van Impe K, Bruyneel E, Boucherie C, et al. (2007) Downregulation of gelsolin family proteins counteracts cancer cell invasion in vitro. Cancer Lett 255: 57-70.
27. Parikh SS, Litherland SA, Clare-Salzler MJ, Li W, Gulig PA, et al. (2003) CapG(-/-) mice have specific host defense defects that render them more susceptible than CapG(+/+) mice to Listeria monocytogenes infection but not to Salmonella enterica serovar Typhimurium infection. Infect Immun 71: 6582-6590.
28. Sun HQ, Kwiatkowska K, Wooten DC, Yin HL (1995) Effects of CapG overexpression on agonist-induced motility and second messenger generation. J Cell Biol 129: 147-156.
29. Chellaiah M, Fitzgerald C, Alvarez U, Hruska K (1998) c-Src is required for stimulation of gelsolin-associated phosphatidylinositol 3-kinase. J Biol Chem 273: 11908-11916.
30. Chellaiah M, Kizer N, Silva M, Alvarez U, Kwiatkowski D, et al. (2000) Gelsolin deficiency blocks podosome assembly and produces increased bone mass and strength. J Cell Biol 148: 665-678.
31. Linder S, Kopp P (2005) Podosomes at a glance. J Cell Sci 118: 2079-2082.
32. Hammarfjord O, Falet H, Gurniak C, Hartwig JH, Wallin RP (2011) Gelsolin-independent podosome formation in dendritic cells. PLoS One 6: e21615.
33. Harmsen MM, De Haard HJ (2007) Properties, production, and applications of camelid single-domain antibody fragments. Appl Microbiol Biotechnol 77: 13-22.
34. Van Bockstaele F, Holz JB, Revets H (2009) The development of nanobodies for therapeutic applications. Curr Opin Investig Drugs 10: 1212-1224.
35. Hmila I, Saerens D, Ben Abderrazek R, Vincke C, Abidi N, et al. (2010) A bispecific nanobody to provide full protection against lethal scorpion envenoming. FASEB J 24: 3479-3489.
36. Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY, et al. (2011) Crystal structure of the beta2 adrenergic receptor-Gs protein complex. Nature 477: 549-555.
37. Hultberg A, Temperton NJ, Rosseels V, Koenders M, Gonzalez-Pajuelo M, et al. (2011) Llama-derived single domain antibodies to build multivalent, superpotent and broadened neutralizing anti-viral molecules. PLoS One 6: e17665.
38. De Clercq S, Zwaenepoel O, Martens E, Vandekerckhove J, Guillabert A, et al. (2013) Nanobody-induced perturbation of LFA-1/L-plastin phosphorylation impairs MTOC docking, immune synapse formation and T cell activation. Cell Mol Life Sci 70: 909-922.
39. Delanote V, Vanloo B, Catillon M, Friederich E, Vandekerckhove J, et al. (2010) An alpaca single-domain antibody blocks filopodia formation by obstructing L-plastin-mediated F-actin bundling. FASEB J 24: 105-118.
40. Van den Abbeele A, De Clercq S, De Ganck A, De Corte V, Van Loo B, et al. (2010) A llama-derived gelsolin single-domain antibody blocks gelsolin-G-actin interaction. Cell Mol Life Sci 67: 1519-1535.
41. Buccione R, Orth JD, McNiven MA (2004) Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat Rev Mol Cell Biol 5: 647-657.
42. Morley SC (2012) The actin-bundling protein L-plastin: a critical regulator of immune cell function. Int J Cell Biol 2012: 935173.
43. Auwerx J (1991) The human leukemia cell line, THP-1: a multifacetted model for the study of monocyte-macrophage differentiation. Experientia 47: 22-31.
44. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, et al. (1980) Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer 26: 171-176.
45. Abrink M, Gobl AE, Huang R, Nilsson K, Hellman L (1994) Human cell lines U-937, THP-1 and Mono Mac 6 represent relatively immature cells of the monocyte-macrophage cell lineage. Leukemia 8: 1579-1584.
46. Tsuchiya S, Kobayashi Y, Goto Y, Okumura H, Nakae S, et al. (1982) Induction of maturation in cultured human monocytic leukemia cells by a phorbol diester. Cancer Res 42: 1530-1536.
47. Tsuboi S (2007) Requirement for a complex of Wiskott-Aldrich syndrome protein (WASP) with WASP interacting protein in podosome formation in macrophages. J Immunol 178: 2987-2995.
48. Burger KL, Davis AL, Isom S, Mishra N, Seals DF (2011) The podosome marker protein Tks5 regulates macrophage invasive behavior. Cytoskeleton (Hoboken) 68: 694-711.
49. Kelly T, Mueller SC, Yeh Y, Chen WT (1994) Invadopodia promote proteolysis of a wide variety of extracellular matrix proteins. J Cell Physiol 158: 299-308.
50. Yamaguchi H, Pixley F, Condeelis J (2006) Invadopodia and podosomes in tumor invasion. Eur J Cell Biol 85: 213-218.
51. Linder S (2007) The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol 17: 107-117.
52. Linder S, Wiesner C, Himmel M (2011) Degrading devices: invadosomes in proteolytic cell invasion. Annu Rev Cell Dev Biol 27: 185-211.
53. Dreier R, Grässel S, Fuchs S, Schaumburger J, Bruckner P (2004) Pro-MMP-9 is a specific macrophage product and is activated by osteoarthritic chondrocytes via MMP-3 or a MT1-MMP/MMP-13 cascade. Exp Cell Res 297: 303-312.
54. Banon-Rodriguez I, Monypenny J, Ragazzini C, Franco A, Calle Y, et al. (2011) The cortactin-binding domain of WIP is essential for podosome formation and extracellular matrix degradation by murine dendritic cells. Eur J Cell Biol 90: 213-223.
55. Esparza J, Vilardell C, Calvo J, Juan M, Vives J, et al. (1999) Fibronectin upregulates gelatinase B (MMP-9) and induces coordinated expression of gelatinase A (MMP-2) and its activator MT1-MMP (MMP-14) by human T lymphocyte cell lines. A process repressed through RAS/MAP kinase signaling pathways. Blood 94: 2754-2766.
56. Murphy DA, Courtneidge SA (2011) The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol 12: 413-426.
57. Evans JG, Correia I, Krasavina O, Watson N, Matsudaira P (2003) Macrophage podosomes assemble at the leading lamella by growth and fragmentation. J Cell Biol 161: 697-705.
58. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, et al. (2008) Lifeact: a versatile marker to visualize F-actin. Nat Methods 5: 605-607.
59. Ma T, Sadashivaiah K, Madayiputhiya N, Chellaiah MA (2010) Regulation of sealing ring formation by L-plastin and cortactin in osteoclasts. J Biol Chem 285: 29911-29924.
60. Bhuwania R, Cornfine S, Fang Z, Kruger M, Luna EJ, et al. (2012) Supervillin couples myosin-dependent contractility to podosomes and enables their turnover. J Cell Sci 125: 2300-2314.
61. Jones SL, Brown EJ (1996) FcgammaRII-mediated adhesion and phagocytosis induce L-plastin phosphorylation in human neutrophils. J Biol Chem 271: 14623-14630.
62. 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.
63. Babb SG, Matsudaira P, Sato M, Correia I, Lim SS (1997) Fimbrin in podosomes of monocyte-derived osteoclasts. Cell Motil Cytoskeleton 37: 308-325.
64. Wernimont SA, Cortesio CL, Simonson WT, Huttenlocher A (2008) Adhesions ring: a structural comparison between podosomes and the immune synapse. Eur J Cell Biol 87: 507-515.
65. Cougoule C, Le Cabec V, Poincloux R, Al Saati T, Mege JL, et al. (2010) Three-dimensional migration of macrophages requires Hck for podosome organization and extracellular matrix proteolysis. Blood 115: 1444-1452.
66. Xiao H, Bai XH, Kapus A, Lu WY, Mak AS, et al. (2010) The protein kinase C cascade regulates recruitment of matrix metalloprotease 9 to podosomes and its release and activation. Mol Cell Biol 30: 5545-5561.
67. Alexander NR, Branch KM, Parekh A, Clark ES, Iwueke IC, et al. (2008) Extracellular matrix rigidity promotes invadopodia activity. Curr Biol 18: 1295-1299.
68. 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.
69. Al Tanoury Z, Schaffner-Reckinger E, Halavatyi A, Hoffmann C, Moes M, et al. (2010) Quantitative kinetic study of the actin-bundling protein L-plastin and of its impact on actin turn-over. PLoS One 5: e9210.
70. Labernadie A, Thibault C, Vieu C, Maridonneau-Parini I, Charriere GM (2010) Dynamics of podosome stiffness revealed by atomic force microscopy. Proc Natl Acad Sci U S A 107: 21016-21021.
71. Luxenburg C, Winograd-Katz S, Addadi L, Geiger B (2012) Involvement of actin polymerization in podosome dynamics. J Cell Sci 125: 1666-1672.
72. Guiet R, Verollet C, Lamsoul I, Cougoule C, Poincloux R, et al. (2012) Macrophage mesenchymal migration requires podosome stabilization by filamin A. J Biol Chem 287: 13051-13062.
73. Yamakita Y, Matsumura F, Lipscomb MW, Chou PC, Werlen G, et al. (2011) Fascin1 promotes cell migration of mature dendritic cells. J Immunol 186: 2850-2859.
74. Li A, Dawson JC, Forero-Vargas M, Spence HJ, Yu X, et al. (2010) The actin-bundling protein fascin stabilizes actin in invadopodia and potentiates protrusive invasion. Curr Biol 20: 339-345.
75. Rizvi SA, Neidt EM, Cui J, Feiger Z, Skau CT, et al. (2009) Identification and characterization of a small molecule inhibitor of formin-mediated actin assembly. Chem Biol 16: 1158-1168.
76. Gauvin TJ, Fukui J, Peterson JR, Higgs HN (2009) Isoform-selective chemical inhibition of mDia-mediated actin assembly. Biochemistry 48: 9327-9329.
77. Nolen BJ, Tomasevic N, Russell A, Pierce DW, Jia Z, et al. (2009) Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460: 1031-1034.
78. Van Audenhove I, Van Impe K, Ruano-Gallego D, De Clercq S, De Muynck K, et al. (2013) Mapping cytoskeletal protein function in cells by means of nanobodies. Cytoskeleton: doi: 10.1002/cm.21122.
79. Irobi J, Van Impe K, Seeman P, Jordanova A, Dierick I, et al. (2004) Hot-spot residue in small heat-shock protein 22 causes distal motor neuropathy. Nat Genet 36: 597-601.