A nanobody targeting the F-actin capping protein CapG restrains breast cancer metastasis

Breast Cancer Research

Volumn 15, Issue 6, 2013, Pages

  Van Impe, Katrien ^a   Bethuyne, Jonas ^a   Cool, Steven ^a   Impens, Francis ^a,b   Ruano Gallego, David ^c   De Wever, Olivier ^a   Vanloo, Berlinda ^a,b   Van Troys, Marleen ^a   Lambein, Kathleen ^d   Boucherie, Ciska ^a   Martens, Evelien ^a   Zwaenepoel, Olivier ^a   Hassanzadeh Ghassabeh, Gholamreza ^b   Vandekerckhove, Joël ^a   Gevaert, Kris ^a,b   Fernández, Luis Ángel ^c   Sanders, Niek N ^a   Gettemans, Jan ^a  

^a GHENT UNIVERSITY   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^d GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN CAPPING PROTEIN; CAPG PROTEIN; CAPNB2 PROTEIN; EOSIN; EPITOPE; F ACTIN; G ACTIN; HEMATOXYLIN; MATRIGEL; NANOBODY; UNCLASSIFIED DRUG; VIMENTIN; VIRUS LARGE T ANTIGEN; ACTIN; ACTIN BINDING PROTEIN; CAPG PROTEIN, HUMAN; NUCLEAR PROTEIN;

ACTIN CAPPING; ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CELL CYCLE S PHASE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; EPITOPE MAPPING; ESCHERICHIA COLI; FEMALE; IMMUNOMODULATION; IN VIVO STUDY; LIMIT OF DETECTION; LUNG METASTASIS; METASTASIS; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SECRETION; TUMOR INVASION; VIRAL GENE DELIVERY SYSTEM; WESTERN BLOTTING; ANIMAL; BREAST NEOPLASMS; CELL MOTION; DRUG EFFECTS; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PROCEDURES; PROTEIN TERTIARY STRUCTURE; SCID MOUSE; TUMOR CELL LINE;

ACTINS; ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; ESCHERICHIA COLI; FEMALE; HUMANS; MICE, SCID; MICROFILAMENT PROTEINS; MOLECULAR TARGETED THERAPY; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; SINGLE-DOMAIN ANTIBODIES;

EID: 84889961827     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3585     Document Type: Article

References (47)

1. Hall A. The cytoskeleton and cancer. Cancer Metastasis Rev 2009, 28:5-14. 10.1007/s10555-008-9166-3, 19153674.
2. Nurnberg A, Kitzing T, Grosse R. Nucleating actin for invasion. Nat Rev Cancer 2011, 11:177-187. 10.1038/nrc3003, 21326322.
3. Stevenson RP, Veltman D, Machesky LM. Actin-bundling proteins in cancer progression at a glance. J Cell Sci 2012, 125:1073-1079. 10.1242/jcs.093799, 22492983.
4. Murphy DA, Courtneidge SA. The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol 2011, 12:413-426. 10.1038/nrm3141, 3423958, 21697900.
5. Bear JE, Gertler FB. Ena/VASP: towards resolving a pointed controversy at the barbed end. J Cell Sci 2009, 122:1947-1953. 10.1242/jcs.038125, 2723151, 19494122.
6. Witke W, Li W, Kwiatkowski DJ, Southwick FS. 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 2001, 154:775-784. 10.1083/jcb.200101113, 2196452, 11514591.
7. Le Clainche C, Carlier MF. Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol Rev 2008, 88:489-513. 10.1152/physrev.00021.2007, 18391171.
8. Yu FX, Johnston PA, Sudhof TC, Yin HL. gCap39, a calcium ion- and polyphosphoinositide-regulated actin capping protein. Science 1990, 250:1413-1415. 10.1126/science.2255912, 2255912.
9. Sun HQ, Kwiatkowska K, Wooten DC, Yin HL. Effects of CapG overexpression on agonist-induced motility and second messenger generation. J Cell Biol 1995, 129:147-156. 10.1083/jcb.129.1.147, 2120377, 7698981.
10. De Corte V, Van Impe K, Bruyneel E, Boucherie C, Mareel M, Vandekerckhove J, Gettemans J. Increased importin-beta-dependent nuclear import of the actin modulating protein CapG promotes cell invasion. J Cell Sci 2004, 117:5283-5292. 10.1242/jcs.01410, 15454578.
11. Van den Abbeele A, De Corte V, Van Impe K, Bruyneel E, Boucherie C, Bracke M, Vandekerckhove J, Gettemans J. Downregulation of gelsolin family proteins counteracts cancer cell invasion in vitro. Cancer Lett 2007, 255:57-70. 10.1016/j.canlet.2007.03.023, 17493746.
12. Kimura K, Ojima H, Kubota D, Sakumoto M, Nakamura Y, Tomonaga T, Kosuge T, Kondo T. Proteomic identification of the macrophage-capping protein as a protein contributing to the malignant features of hepatocellular carcinoma. J Proteomics 2012, 78:362-373.
13. Thompson CC, Ashcroft FJ, Patel S, Saraga G, Vimalachandran D, Prime W, Campbell F, Dodson A, Jenkins RE, Lemoine NR, et al. Pancreatic cancer cells overexpress gelsolin family-capping proteins, which contribute to their cell motility. Gut 2007, 56:95-106. 10.1136/gut.2005.083691, 1856675, 16847067.
14. Kang S, Kim MJ, An H, Kim BG, Choi YP, Kang KS, Gao MQ, Park H, Na HJ, Kim HK, et al. Proteomic molecular portrait of interface zone in breast cancer. J Proteome Res 2010, 9:5638-5645. 10.1021/pr1004532, 20857901.
15. Xu SG, Yan PJ, Shao ZM. Differential proteomic analysis of a highly metastatic variant of human breast cancer cells using two-dimensional differential gel electrophoresis. J Cancer Res Clin Oncol 2010, 136:1545-1556. 10.1007/s00432-010-0812-0, 20155427.
16. Voisin SN, Krakovska O, Matta A, DeSouza LV, Romaschin AD, Colgan TJ, Siu KW. Identification of novel molecular targets for endometrial cancer using a drill-down LC-MS/MS approach with iTRAQ. PLoS One 2011, 6:e16352. 10.1371/journal.pone.0016352, 3031560, 21305022.
17. Hamers-Casterman C, Atarhouch T, Muyldermans S, Robinson G, Hamers C, Songa EB, Bendahman N, Hamers R. Naturally occurring antibodies devoid of light chains. Nature 1993, 363:446-448. 10.1038/363446a0, 8502296.
18. De Clercq S, Zwaenepoel O, Martens E, Vandekerckhove J, Guillabert A, Gettemans J. Nanobody-induced perturbation of LFA-1/L-plastin phosphorylation impairs MTOC docking, immune synapse formation and T cell activation. Cell Mol Life Sci 2012, 70:909-922.
19. Delanote V, Vanloo B, Catillon M, Friederich E, Vandekerckhove J, Gettemans J. An alpaca single-domain antibody blocks filopodia formation by obstructing L-plastin-mediated F-actin bundling. FASEB J 2010, 24:105-118. 10.1096/fj.09-134304, 19726756.
20. Van den Abbeele A, De Clercq S, De Ganck A, De Corte V, Van Loo B, Soror SH, Srinivasan V, Steyaert J, Vandekerckhove J, Gettemans J. A llama-derived gelsolin single-domain antibody blocks gelsolin-G-actin interaction. Cell Mol Life Sci 2010, 67:1519-1535. 10.1007/s00018-010-0266-1, 20140750.
21. Hassanzadeh-Ghassabeh G, Saerens D, Muyldermans S. Isolation of antigen-specific nanobodies. Antibody Engineering, Volume 2 2010, 251-266. Berlin: Springer-Verlag, Kontermann R, Dübel S.
22. Blanco-Toribio A, Muyldermans S, Frankel G, Fernandez LA. Direct injection of functional single-domain antibodies from E. coli into human cells. PLoS One 2010, 5:e15227. 10.1371/journal.pone.0015227, 2999559, 21170340.
23. Van Impe K, De Corte V, Eichinger L, Bruyneel E, Mareel M, Vandekerckhove J, Gettemans J. The nucleo-cytoplasmic actin-binding protein CapG lacks a nuclear export sequence present in structurally related proteins. J Biol Chem 2003, 278:17945-17952. 10.1074/jbc.M209946200, 12637565.
24. Zhang Y, Vorobiev SM, Gibson BG, Hao B, Sidhu GS, Mishra VS, Yarmola EG, Bubb MR, Almo SC, Southwick FS. A CapG gain-of-function mutant reveals critical structural and functional determinants for actin filament severing. EMBO J 2006, 25:4458-4467. 10.1038/sj.emboj.7601323, 1589989, 16977317.
25. Van Impe K, Hubert T, De Corte V, Vanloo B, Boucherie C, Vandekerckhove J, Gettemans J. A new role for nuclear transport factor 2 and Ran: nuclear import of CapG. Traffic 2008, 9:695-707. 10.1111/j.1600-0854.2008.00720.x, 18266911.
26. Onoda K, Yin HL. gCap39 is phosphorylated: stimulation by okadaic acid and preferential association with nuclei. J Biol Chem 1993, 268:4106-4112.
27. Hubert T, Van Impe K, Vandekerckhove J, Gettemans J. The actin-capping protein CapG localizes to microtubule-dependent organelles during the cell cycle. Biochem Biophys Res Commun 2009, 380:166-170. 10.1016/j.bbrc.2009.01.064, 19166812.
28. Cho RJ, Huang M, Campbell MJ, Dong H, Steinmetz L, Sapinoso L, Hampton G, Elledge SJ, Davis RW, Lockhart DJ. Transcriptional regulation and function during the human cell cycle. Nat Genet 2001, 27:48-54.
29. Gough W, Hulkower KI, Lynch R, McGlynn P, Uhlik M, Yan L, Lee JA. A quantitative, facile, and high-throughput image-based cell migration method is a robust alternative to the scratch assay. J Biomol Screen 2011, 16:155-163. 10.1177/1087057110393340, 21297103.
30. Wong AR, Pearson JS, Bright MD, Munera D, Robinson KS, Lee SF, Frankel G, Hartland EL. Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol Microbiol 2011, 80:1420-1438. 10.1111/j.1365-2958.2011.07661.x, 21488979.
31. Croxen MA, Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 2010, 8:26-38.
32. Galan JE, Wolf-Watz H. Protein delivery into eukaryotic cells by type III secretion machines. Nature 2006, 444:567-573. 10.1038/nature05272, 17136086.
33. Charpentier X, Oswald E. Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J Bacteriol 2004, 186:5486-5495. 10.1128/JB.186.16.5486-5495.2004, 490934, 15292151.
34. Iguchi A, Thomson NR, Ogura Y, Saunders D, Ooka T, Henderson IR, Harris D, Asadulghani M, Kurokawa K, Dean P, et al. Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. J Bacteriol 2009, 191:347-354. 10.1128/JB.01238-08, 2612414, 18952797.
35. Dean P, Maresca M, Schuller S, Phillips AD, Kenny B. Potent diarrheagenic mechanism mediated by the cooperative action of three enteropathogenic Escherichia coli-injected effector proteins. Proc Natl Acad Sci USA 2006, 103:1876-1881. 10.1073/pnas.0509451103, 1413648, 16446436.
36. Quitard S, Dean P, Maresca M, Kenny B. The enteropathogenic Escherichia coli EspF effector molecule inhibits PI-3 kinase-mediated uptake independently of mitochondrial targeting. Cell Microbiol 2006, 8:972-981. 10.1111/j.1462-5822.2005.00680.x, 16681838.
37. Menna E, Fossati G, Scita G, Matteoli M. From filopodia to synapses: the role of actin-capping and anti-capping proteins. Eur J Neurosci 2011, 34:1655-1662. 10.1111/j.1460-9568.2011.07897.x, 22103422.
38. Ichikawa H, Kanda T, Kosugi SI, Kawachi Y, Sasaki H, Wakai T, Kondo T. Laser microdissection and two-dimensional difference gel electrophoresis reveal the role of a novel macrophage-capping protein in lymph node metastasis in gastric cancer. J Proteome Res 2013, 12:3780-3791. 10.1021/pr400439m, 23782053.
39. Liao SH, Zhao XY, Han YH, Zhang J, Wang LS, Xia L, Zhao KW, Zheng Y, Guo M, Chen GQ. Proteomics-based identification of two novel direct targets of hypoxia-inducible factor-1 and their potential roles in migration/invasion of cancer cells. Proteomics 2009, 9:3901-3912. 10.1002/pmic.200800922, 19637235.
40. Chen L, Yang S, Jakoncic J, Zhang JJ, Huang XY. Migrastatin analogues target fascin to block tumour metastasis. Nature 2010, 464:1062-1066. 10.1038/nature08978, 2857318, 20393565.
41. Nolen BJ, Tomasevic N, Russell A, Pierce DW, Jia Z, McCormick CD, Hartman J, Sakowicz R, Pollard TD. Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 2009, 460:1031-1034. 10.1038/nature08231, 2780427, 19648907.
42. Pollard TD, Cooper JA. Actin, a central player in cell shape and movement. Science 2009, 326:1208-1212. 10.1126/science.1175862, 3677050, 19965462.
43. Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY, Kobilka TS, Thian FS, Chae PS, Pardon E, Calinski D, et al. Crystal structure of the beta2 adrenergic receptor-Gs protein complex. Nature 2011, 477:549-555. 10.1038/nature10361, 3184188, 21772288.
44. Weibel S, Stritzker J, Eck M, Goebel W, Szalay AA. Colonization of experimental murine breast tumours by Escherichia coli K-12 significantly alters the tumour microenvironment. Cell Microbiol 2008, 10:1235-1248. 10.1111/j.1462-5822.2008.01122.x, 18208564.
45. Stritzker J, Weibel S, Hill PJ, Oelschlaeger TA, Goebel W, Szalay AA. Tumor-specific colonization, tissue distribution, and gene induction by probiotic Escherichia coli Nissle 1917 in live mice. Int J Med Microbiol 2007, 297:151-162. 10.1016/j.ijmm.2007.01.008, 17448724.
46. Sunden F, Hakansson L, Ljunggren E, Wullt B. Escherichia coli 83972 bacteriuria protects against recurrent lower urinary tract infections in patients with incomplete bladder emptying. J Urol 2010, 184:179-185. 10.1016/j.juro.2010.03.024, 20483149.
47. Schultz M. Clinical use of E. coli Nissle 1917 in inflammatory bowel disease. Inflamm Bowel Dis 2008, 14:1012-1018. 10.1002/ibd.20377, 18240278.