SILAC identifies LAD1 as a filamin-binding regulator of actin dynamics in response to EGF and a marker of aggressive breast tumors

Science Signaling

Volumn 11, Issue 515, 2018, Pages

  Roth, Lee ^a   Srivastava, Swati ^a   Lindzen, Moshit ^a   Sas Chen, Aldema ^a   Sheffer, Michal ^a,e   Lauriola, Mattia ^a,f   Enuka, Yehoshua ^a   Noronha, Ashish ^a   Mancini, Maicol ^a,g   Lavi, Sara ^a   Tarcic, Gabi ^a,h   Pines, Gur ^a,i   Nevo, Nava ^a   Heyman, Ori ^a   Ziv, Tamar ^b   Rueda, Oscar M ^c   Gnocchi, Davide ^a   Pikarski, Eli ^d   Admon, Arie ^b   Caldas, Carlos ^c   Yarden, Yosef ^a   more..

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d HEBREW UNIVERSITY   (Israel)

^e HARVARD MEDICAL SCHOOL   (United States)

^f UNIVERSITY OF BOLOGNA   (Italy)

^g INSTITUT DE RECHERCHE EN CANCÉROLOGIE DE MONTPELLIER   (France)

^h HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

ⁱ UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BINDING PROTEIN; EPIDERMAL GROWTH FACTOR; FILAMIN; LADININ 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; SMALL INTERFERING RNA; STRATIFIN; UNCLASSIFIED DRUG; AUTOANTIGEN; COLLAGEN TYPE 17; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; NONFIBRILLAR COLLAGEN; PROTEIN BINDING;

ACTIN FILAMENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST EPITHELIUM CELL; CANCER INHIBITION; CELL ADHESION; CELL FRACTIONATION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CROSS LINKING; DYNAMICS; FEMALE; GENETIC TRANSFECTION; GENOMICS; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MCF10A CELL LINE; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEOMICS; RNA PURIFICATION; RNA SEQUENCE; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; ANIMAL; BREAST; BREAST TUMOR; CELL CULTURE; CELL MOTION; DRUG EFFECT; DRUG SCREENING; GENETICS; ISOTOPE LABELING; METABOLISM; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; PROCEDURES;

ACTIN CYTOSKELETON; ANIMALS; AUTOANTIGENS; BREAST; BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; EPIDERMAL GROWTH FACTOR; ERBB RECEPTORS; FEMALE; FILAMINS; HUMANS; ISOTOPE LABELING; MICE; MICE, NUDE; NON-FIBRILLAR COLLAGENS; PHOSPHORYLATION; PROTEIN BINDING; PROTEOMICS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85041279814     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aan0949     Document Type: Article

References (59)

1. N. E. Hynes, G. MacDonald, ErbB receptors and signaling pathways in cancer. Curr. Opin. Cell Biol. 21, 177–184 (2009).
2. Y. Yarden, G. Pines, The ERBB network: At last, cancer therapy meets systems biology. Nat. Rev. Cancer 12, 553–563 (2012).
3. W. D. Foulkes, I. E. Smith, J. S. Reis-Filho, Triple-negative breast cancer. N. Engl. J. Med. 363, 1938–1948 (2010).
4. Y. Samuels, Z. Wang, A. Bardelli, N. Silliman, J. Ptak, S. Szabo, H. Yan, A. Gazdar, S. M. Powell, G. J. Riggins, J. K. V. Willson, S. Markowitz, K. W. Kinzler, B. Vogelstein, V. E. Velculescu, High frequency of mutations of the PIK3CA gene in human cancers. Science 304, 554 (2004).
5. E. Kovacs, J. A. Zorn, Y. Huang, T. Barros, J. Kuriyan, A structural perspective on the regulation of the epidermal growth factor receptor. Annu. Rev. Biochem. 84, 739–764 (2015).
6. S.-E. Ong, B. Blagoev, I. Kratchmarova, D. B. Kristensen, H. Steen, A. Pandey, M. Mann, Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376–386 (2002).
7. J. V. Olsen, B. Blagoev, F. Gnad, B. Macek, C. Kumar, P. Mortensen, M. Mann, Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635–648 (2006).
8. A. Wolf-Yadlin, N. Kumar, Y. Zhang, S. Hautaniemi, M. Zaman, H. D. Kim, V. Grantcharova, D. A. Lauffenburger, F. M. White, Effects of HER2 overexpression on cell signaling networks governing proliferation and migration. Mol. Syst. Biol. 2, 54 (2006).
9. H. Yamaguchi, J. Condeelis, Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim. Biophys. Acta 1773, 642–652 (2007).
10. A. J. Ridley, Life at the leading edge. Cell 145, 1012–1022 (2011).
11. C. Ciobanasu, B. Faivre, C. Le Clainche, Integrating actin dynamics, mechanotransduction and integrin activation: The multiple functions of actin binding proteins in focal adhesions. Eur. J. Cell Biol. 92, 339–348 (2013).
12. Q.-Q. Shao, T.-P. Zhang, W.-J. Zhao, Z.-W. Liu, L. You, L. Zhou, J.-C. Guo, Y.-P. Zhao, Filamin A: Insights into its exact role in cancers. Pathol. Oncol. Res. 22, 245–252 (2016).
13. T. P. Stossel, J. Condeelis, L. Cooley, J. H. Hartwig, A. Noegel, M. Schleicher, S. S. Shapiro, Filamins as integrators of cell mechanics and signalling. Nat. Rev. Mol. Cell Biol. 2, 138–145 (2001).
14. A. van der Flier, A. Sonnenberg, Structural and functional aspects of filamins. Biochim. Biophys. Acta 1538, 99–117 (2001).
15. G. Tarcic, R. Avraham, G. Pines, I. Amit, T. Shay, Y. Lu, Y. Zwang, M. Katz, N. Ben-Chetrit, J. Jacob-Hirsch, L. Virgilio, G. Rechavi, G. Mavrothalassitis, G. B. Mills, E. Domany, Y. Yarden, EGR1 and the ERK-ERF axis drive mammary cell migration in response to EGF. FASEB J. 26, 1582–1592 (2011).
16. Y. Zwang, A. Sas-Chen, Y. Drier, T. Shay, R. Avraham, M. Lauriola, E. Shema, E. Lidor-Nili, J. Jacob-Hirsch, N. Amariglio, Y. Lu, G. B. Mills, G. Rechavi, M. Oren, E. Domany, Y. Yarden, Two phases of mitogenic signaling unveil roles for p53 and EGR1 in elimination of inconsistent growth signals. Mol. Cell 42, 524–535 (2011).
17. K. Motoki, M. Megahed, S. LaForgia, J. Uitto, Cloning and chromosomal mapping of mouse ladinin, a novel basement membrane zone component. Genomics 39, 323–330 (1997).
18. I. Amit, A. Citri, T. Shay, Y. Lu, M. Katz, F. Zhang, G. Tarcic, D. Siwak, J. Lahad, J. Jacob-Hirsch, N. Amariglio, N. Vaisman, E. Segal, G. Rechavi, U. Alon, G. B. Mills, E. Domany, Y. Yarden, A module of negative feedback regulators defines growth factor signaling. Nat. Genet. 39, 503–512 (2007).
19. M. P. Marinkovich, T. B. Taylor, D. R. Keene, R. E. Burgeson, J. J. Zone, LAD-1, the linear IgA bullous dermatosis autoantigen, is a novel 120-kDa anchoring filament protein synthesized by epidermal cells. J. Invest. Dermatol. 106, 734–738 (1996).
20. W. Sun, K. Kesavan, B. C. Schaefer, T. P. Garrington, M. Ware, N. L. Johnson, E. W. Gelfand, G. L. Johnson, MEKK2 associates with the adapter protein Lad/RIBP and regulates the MEK5-BMK1/ERK5 pathway. J. Biol. Chem. 276, 5093–5100 (2001).
21. N. Ben-Chetrit, D. Chetrit, R. Russell, C. Körner, M. Mancini, A. Abdul-Hai, T. Itkin, S. Carvalho, H. Cohen-Dvashi, W. J. Koestler, K. Shukla, M. Lindzen, M. Kedmi, M. Lauriola, Z. Shulman, H. Barr, D. Seger, D. A. Ferraro, F. Pareja, H. Gil-Henn, T. Lapidot, R. Alon, F. Milanezi, M. Symons, R. Ben-Hamo, S. Efroni, F. Schmitt, S. Wiemann, C. Caldas, M. Ehrlich, Y. Yarden, Synaptojanin 2 is a druggable mediator of metastasis and the gene is overexpressed and amplified in breast cancer. Sci. Signal. 8, ra7 (2015).
22. S. A. Courtneidge, Cell migration and invasion in human disease: The Tks adaptor proteins. Biochem. Soc. Trans. 40, 129–132 (2012).
23. S. K. Muthuswamy, D. Li, S. Lelievre, M. J. Bissell, J. S. Brugge, ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat. Cell Biol. 3, 785–792 (2001).
24. O. M. Lancaster, B. Baum, Shaping up to divide: Coordinating actin and microtubule cytoskeletal remodelling during mitosis. Semin. Cell Dev. Biol. 34, 109–115 (2014).
25. G. B. Alsop, D. Zhang, Microtubules are the only structural constituent of the spindle apparatus required for induction of cell cleavage. J. Cell Biol. 162, 383–390 (2003).
26. M. Fromont-Racine, J.-C. Rain, P. Legrain, Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat. Genet. 16, 277–282 (1997).
27. O. Söderberg, M. Gullberg, M. Jarvius, K. Ridderstråle, K.-J. Leuchowius, J. Jarvius, K. Wester, P. Hydbring, F. Bahram, L.-G. Larsson, U. Landegren, Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995–1000 (2006).
28. A.-X. Zhou, A. Toylu, R. K. Nallapalli, G. Nilsson, N. Atabey, C.-H. Heldin, J. Borén, M. O. Bergo, L. M. Akyürek, Filamin a mediates HGF/c-MET signaling in tumor cell migration. Int. J. Cancer 128, 839–846 (2011).
29. A. Benzinger, N. Muster, H. B. Koch, J. R. Yates III, H. Hermeking, Targeted proteomic analysis of 14-3-3ς, a p53 effector commonly silenced in cancer. Mol. Cell. Proteomics 4, 785–795 (2005).
30. J. Xu, S. Acharya, O. Sahin, Q. Zhang, Y. Saito, J. Yao, H. Wang, P. Li, L. Zhang, F. J. Lowery, W.-L. Kuo, Y. Xiao, J. Ensor, A. A. Sahin, X. H.-F. Zhang, M.-C. Hung, J. David Zhang, D. Yu, 14-3-3 turns TGF-’s function from tumor suppressor to metastasis promoter in breast cancer by contextual changes of Smad partners from p53 to Gli2. Cancer Cell 27, 177–192 (2015).
31. A. Boudreau, K. Tanner, D. Wang, F. C. Geyer, J. S. Reis-Filho, M. J. Bissell, 14-3-3 stabilizes a complex of soluble actin and intermediate filament to enable breast tumor invasion. Proc. Natl. Acad. Sci. U.S.A. 110, E3937–E3944 (2013).
32. H.-M. Tian, X.-H. Liu, W. Han, L.-L. Zhao, B. Yuan, C.-J. Yuan, Differential expression of filamin A and its clinical significance in breast cancer. Oncol. Lett. 6, 681–686 (2013).
33. R. K. Nallapalli, M. X. Ibrahim, A. X. Zhou, S. Bandaru, S. Naresh Sunkara, B. Redfors, D. Pazooki, Y. Zhang, J. Borén, Y. Cao, M. O. Bergo, L. M. Akyürek, Targeting filamin A reduces K-RAS–induced lung adenocarcinomas and endothelial response to tumor growth in mice. Mol. Cancer 11, 50 (2012).
34. B. D. Lehmann, J. A. Bauer, X. Chen, M. E. Sanders, A. B. Chakravarthy, Y. Shyr, J. A. Pietenpol, Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J. Clin. Invest. 121, 2750–2767 (2011).
35. C. Curtis, S. P. Shah, S.-F. Chin, G. Turashvili, O. M. Rueda, M. J. Dunning, D. Speed, A. G. Lynch, S. Samarajiwa, Y. Yuan, S. Gräf, G. Ha, G. Haffari, A. Bashashati, R. Russell, S. McKinney; METABRIC Group, A. Langerød, A. Green, E. Provenzano, G. Wishart, S. Pinder, P. Watson, F. Markowetz, L. Murphy, I. Ellis, A. Purushotham, A.-L. Børresen-Dale, J. D. Brenton, S. Tavaré, C. Caldas, S. Aparicio, The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 486, 346–352 (2012).
36. H. Raza Ali, O. M. Rueda, S.-F. Chin, C. Curtis, M. J. Dunning, S. A. J. R. Aparicio, C. Caldas, Genome-driven integrated classification of breast cancer validated in over 7,500 samples. Genome Biol. 15, 431 (2014).
37. B. Pereira, S.-F. Chin, O. M. Rueda, H.-K. M. Vollan, E. Provenzano, H. A. Bardwell, M. Pugh, L. Jones, R. Russell, S.-J. Sammut, D. W. Y. Tsui, B. Liu, S.-J. Dawson, J. Abraham, H. Northen, J. F. Peden, A. Mukherjee, G. Turashvili, A. R. Green, S. McKinney, A. Oloumi, S. Shah, N. Rosenfeld, L. Murphy, D. R. Bentley, I. O. Ellis, A. Purushotham, S. E. Pinder, A.-L. Børresen-Dale, H. M. Earl, P. D. Pharoah, M. T. Ross, S. Aparicio, C. Caldas, The somatic mutation profiles of 2,433 breast cancers refines their genomic and transcriptomic landscapes. Nat. Commun. 7, 11479 (2016).
38. H. Dvinge, A. Git, S. Gräf, M. Salmon-Divon, C. Curtis, A. Sottoriva, Y. Zhao, M. Hirst, J. Armisen, E. A. Miska, S.-F. Chin, E. Provenzano, G. Turashvili, A. Green, I. Ellis, S. Aparicio, C. Caldas, The shaping and functional consequences of the microRNA landscape in breast cancer. Nature 497, 378–382 (2013).
39. S. J. Dawson, O. M. Rueda, S. Aparicio, C. Caldas, A new genome-driven integrated classification of breast cancer and its implications. EMBO J. 32, 617–628 (2013).
40. E. Witsch, M. Sela, Y. Yarden, Roles for growth factors in cancer progression. Physiology (Bethesda) 25, 85–101 (2010).
41. A. Z. Lai, J. V. Abella, M. Park, Crosstalk in Met receptor oncogenesis. Trends Cell Biol. 19, 542–551 (2009).
42. M. A. Lemmon, J. Schlessinger, Cell signaling by receptor tyrosine kinases. Cell 141, 1117–1134 (2010).
43. S.-E. Ong, M. Mann, A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat. Protoc. 1, 2650–2660 (2006).
44. T. Abé, S. Maruyama, M. Yamazaki, B. Xu, H. Babkair, Y. Sumita, J. Cheng, T. Yamamoto, T. Saku, Proteomic and histopathological characterization of the interface between oral squamous cell carcinoma invasion fronts and non-cancerous epithelia. Exp. Mol. Pathol. 102, 327–336 (2017).
45. A. D. Santin, F. Zhan, S. Bellone, M. Palmieri, S. Cane, E. Bignotti, S. Anfossi, M. Gokden, D. Dunn, J. J. Roman, T. J. O’Brien, E. Tian, M. J. Cannon, J. Shaughnessy Jr., S. Pecorelli, Gene expression profiles in primary ovarian serous papillary tumors and normal ovarian epithelium: Identification of candidate molecular markers for ovarian cancer diagnosis and therapy. Int. J. Cancer 112, 14–25 (2004).
46. Y. Ohta, N. Suzuki, S. Nakamura, J. H. Hartwig, T. P. Stossel, The small GTPase RalA targets filamin to induce filopodia. Proc. Natl. Acad. Sci. U.S.A. 96, 2122–2128 (1999).
47. G. Alexe, G. S. Dalgin, R. Ramaswamy, C. DeLisi, G. Bhanot, Data perturbation independent diagnosis and validation of breast cancer subtypes using clustering and patterns. Cancer Inform. 2, 243–274 (2007).
48. X. Wang, C. Guda, Integrative exploration of genomic profiles for triple negative breast cancer identifies potential drug targets. Medicine (Baltimore) 95, e4321 (2016).
49. D. Rusinek, M. Swierniak, E. Chmielik, M. Kowal, M. Kowalska, R. Cyplinska, A. Czarniecka, W. Piglowski, J. Korfanty, M. Chekan, J. Krajewska, S. Szpak-Ulczok, M. Jarzab, W. Widlak, B. Jarzab, BRAFV600E-associated gene expression profile: Early changes in the transcriptome, based on a transgenic mouse model of papillary thyroid carcinoma. PLOS ONE 10, e0143688 (2015).
50. M. Klobučar, M. Sedić, P. Gehrig, J. Grossmann, M. Bilić, L. Kovač-Bilić, K. Pavelić, S. Kraljević Pavelić, Basement membrane protein ladinin-1 and the MIF-CD44-B1 integrin signaling axis are implicated in laryngeal cancer metastasis. Biochim. Biophys. Acta 1862, 1938–1954 (2016).
51. H. Cohen‐Dvashi, N. Ben‐Chetrit, R. Russell, S. Carvalho, M. Lauriola, S. Nisani, M. Mancini, N. Nataraj, M. Kedmi, L. Roth, W. Köstler, A. Zeisel, A. Yitzhaky, J. Zylberg, G. Tarcic, R. Eilam, Y. Wigelman, R. Will, S. Lavi, Z. Porat, S. Wiemann, S. Ricardo, F. Schmitt, C. Caldas, Y. Yarden, Navigator-3, a modulator of cell migration, may act as a suppressor of breast cancer progression. EMBO Mol. Med. 7, 299–314 (2015).
52. M. Kammann, J. Laufs, J. Schell, B. Gronenborn, Rapid insertional mutagenesis of DNA by polymerase chain reaction (PCR). Nucleic Acids Res. 17, 5404 (1989).
53. J. Cox, M. Mann, MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008).
54. J. Cox, N. Neuhauser, A. Michalski, R. A. Scheltema, J. V. Olsen, M. Mann, Andromeda: A peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794–1805 (2011).
55. E. Formstecher, S. Aresta, V. Collura, A. Hamburger, A. Meil, A. Trehin, C. Reverdy, V. Betin, S. Maire, C. Brun, B. Jacq, M. Arpin, Y. Bellaiche, S. Bellusci, P. Benaroch, M. Bornens, R. Chanet, P. Chavrier, O. Delattre, V. Doye, R. Fehon, G. Faye, T. Galli, J.-A. Girault, B. Goud, J. de Gunzburg, L. Johannes, M.-P. Junier, V. Mirouse, A. Mukherjee, D. Papadopoulo, F. Perez, A. Plessis, C. Rossé, S. Saule, D. Stoppa-Lyonnet, A. Vincent, M. White, P. Legrain, J. Wojcik, J. Camonis, L. Daviet, Protein interaction mapping: A Drosophila case study. Genome Res. 15, 376–384 (2005).
56. R. Blecher-Gonen, Z. Barnett-Itzhaki, D. Jaitin, D. Amann-Zalcenstein, D. Lara-Astiaso, I. Amit, High-throughput chromatin immunoprecipitation for genome-wide mapping of in vivo protein-DNA interactions and epigenomic states. Nat. Protoc. 8, 539–554 (2013).
57. B. Langmead, S. L. Salzberg, Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
58. A. Dobin, C. A. Davis, F. Schlesinger, J. Drenkow, C. Zaleski, S. Jha, P. Batut, M. Chaisson, T. R. Gingeras, STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
59. E. Eden, R. Navon, I. Steinfeld, D. Lipson, Z. Yakhini, GOrilla: A tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10, 48 (2009).