Phosphoproteomic analysis of interacting tumor and endothelial cells identifies regulatory mechanisms of transendothelial migration

Science Signaling

Volumn 9, Issue 414, 2016, Pages

  Locard Paulet, Marie ^a,b,c,d   Lim, Lindsay ^a,e   Veluscek, Giulia ^b   McMahon, Kelly ^b   Sinclair, John ^a   Van Weverwijk, Antoinette ^a   Worboys, Jonathan D ^a,b   Yuan, Yinyin ^a   Isacke, Clare M ^a   Jørgensen, Claus ^a,b  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^d UNIVERSITÉ DE TOULOUSE   (France)

^e ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN A1; EPHRIN RECEPTOR A2; PHOSPHATASE; PHOSPHOPROTEIN; TUMOR PROTEIN;

ARTICLE; BREAST CANCER CELL LINE; CANCER CELL; CELL ADHESION; CELL INTERACTION; COCULTURE; CONTROLLED STUDY; ENDOTHELIUM; ENDOTHELIUM CELL; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; LUNG METASTASIS; METASTASIS POTENTIAL; PHOSPHOPROTEOMICS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STABLE ISOTOPE LABELING OF CELLS IN CULTURE; TANDEM MASS SPECTROMETRY; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; UMBILICAL VEIN ENDOTHELIAL CELL; CELL COMMUNICATION; METABOLISM; NEOPLASM; TUMOR CELL LINE;

CELL COMMUNICATION; CELL LINE, TUMOR; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; NEOPLASM PROTEINS; NEOPLASMS; PHOSPHOPROTEINS; PROTEOMICS; RECEPTOR, EPHA2; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84958535067     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aac5820     Document Type: Article

References (77)

1. N. Reymond, B. B. d'Água, A. J. Ridley, Crossing the endothelial barrier during metastasis. Nat. Rev. Cancer 13, 858-870 (2013).
2. H. S. Leong, A. E. Robertson, K. Stoletov, S. J. Leith, C. A. Chin, A. E. Chien, M. N. Hague, A. Ablack, K. Carmine-Simmen, V. A. McPherson, C. O. Postenka, E. A. Turley, S. A. Courtneidge, A. F. Chambers, J. D. Lewis, Invadopodia are required for cancer cell extravasation and are a therapeutic target for metastasis. Cell Rep. 8, 1-3 (2014).
3. Y. Kienast, L. von Baumgarten, M. Fuhrmann, W. E. F. Klinkert, R. Goldbrunner, J. Herms, F. Winkler, Real-time imaging reveals the single steps of brain metastasis formation. Nat. Med. 16, 116-122 (2010).
4. K. Stoletov, H. Kato, E. Zardouzian, J. Kelber, J. Yang, S. Shattil, R. Klemke, Visualizing extravasation dynamics of metastatic tumor cells. J. Cell Sci. 123, 2332-2341 (2010).
5. L. Biancone, M. Araki, K. Araki, P. Vassalli, I. Stamenkovic, Redirection of tumor metastasis by expression of E-selectin in vivo. J. Exp. Med. 183, 581-587 (1996).
6. S. Rousseau, F. Houle, J. Landry, J. Huot, p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene 15, 2169-2177 (1997).
7. P.-L. Tremblay, F. A. Auger, J. Huot, Regulation of transendothelial migration of colon cancer cells by E-selectin-mediated activation of p38 and ERK MAP kinases. Oncogene 25, 6563-6573 (2006).
8. F. L. Miles, F. L. Pruitt, K. L. van Golen, C. R. Cooper, Stepping out of the flow: Capillary extravasation in cancer metastasis. Clin. Exp. Metastasis 25, 305-324 (2007).
9. H. Wang, W. Fu, J. H. Im, Z. Zhou, S. A. Santoro, V. Iyer, C. M. DiPersio, Q.-C. Yu, V. Quaranta, A. Al-Mehdi, R. J. Muschel, Tumor cell a3b1 integrin and vascular laminin-5 mediate pulmonary arrest and metastasis. J. Cell Biol. 164, 935-941 (2004).
10. M. Klemke, T. Weschenfelder, M. H. Konstandin, Y. Samstag, High affinity interaction of integrin a4b1 (VLA-4) and vascular cell adhesion molecule 1 (VCAM-1) enhances migration of human melanoma cells across activated endothelial cell layers. J. Cell. Physiol. 212, 368-374 (2007).
11. M. Iiizumi, S. Bandyopadhyay, K. Watabe, Interaction of duffy antigen receptor for chemokines andKAI1:Acritical step in metastasis suppression. CancerRes. 67, 1411-1414 (2007).
12. P. Khanna, C.-Y. Chung, R. I. Neves, G. P. Robertson, C. Dong, CD82/KAI expression prevents IL-8-mediated endothelial gap formation in late-stage melanomas. Oncogene 33, 2898-2908 (2013).
13. N. Murugaesu, M. Iravani, A. van Weverwijk, A. Ivetic, D. A. Johnson, A. Antonopoulos, A. Fearns, M. Jamal-Hanjani, D. Sims, K. Fenwick, C. Mitsopoulos, Q. Gao, N. Orr, M. Zvelebil, S. M. Haslam, A. Dell, H. Yarwood, C. J. Lord, A. Ashworth, C. M. Isacke, An in vivo functional screen identifies ST6GalNAc2 sialyltransferase as a breast cancer metastasis suppressor. Cancer Discov. 4, 304-317 (2014).
14. 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).
15. H. Zhu, S. Pan, S. Gu, E. M. Bradbury, X. Chen, Amino acid residue specific stable isotope labeling for quantitative proteomics. Rapid Commun. Mass Spectrom. 16, 2115-2123 (2002).
16. C. Jørgensen, A. Sherman, G. I. Chen, A. Pasculescu, A. Poliakov, M. Hsiung, B. Larsen, D. G. Wilkinson, R. Linding, T. Pawson, Cell-specific information processing in segregating populations of Eph receptor ephrin-expressing cells. Science 326, 1502-1509 (2009).
17. A. J. Minn, G. P. Gupta, P. M. Siegel, P. D. Bos,W. Shu, D. D. Giri, A. Viale, A. B. Olshen, W. L. Gerald, J. Massagué, Genes that mediate breast cancer metastasis to lung. Nature 436, 518-524 (2005).
18. G. P. Gupta, D. X. Nguyen, A. C. Chiang, P. D. Bos, J. Y. Kim, C. Nadal, R. R. Gomis, K. Manova-Todorova, J. Massagué, Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 446, 765-770 (2007).
19. M. Kanehisa, S. Goto, Y. Sato, M. Furumichi, M. Tanabe, KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40, D109-D114 (2012).
20. D. Dunon, L. Piali, B. A. Imhof, To stick or not to stick: The new leukocyte homing paradigm. Curr. Opin. Cell Biol. 8, 714-723 (1996).
21. E. B. Pasquale, Eph receptors and ephrins in cancer: Bidirectional signalling and beyond. Nat. Rev. Cancer 10, 165-180 (2010).
22. A. M. Mercurio, I. Rabinovitz, Towards a mechanistic understanding of tumor invasion - Lessons from the α6β4 integrin. Semin. Cancer Biol. 11, 129-141 (2001).
23. H. Miao, E. Burnett, M. Kinch, E. Simon, B. Wang, Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nat. Cell Biol. 2, 62-69 (2000).
24. B.T. Beaty, Y. Wang, J. J. Bravo-Cordero, V. P. Sharma,V.Miskolci, L.Hodgson, J.Condeelis, Talin regulates moesin-NHE-1 recruitment to invadopodia and promotes mammary tumor metastasis. J. Cell Biol. 205, 737-751 (2014).
25. C. L. Hyder, G. Lazaro, J. W. Pylvänäinen, M.W.G. Roberts, S.M. Qvarnström, J.E. Eriksson, Nestin regulates prostate cancer cell invasion by influencing the localisation and functions of FAK and integrins. J. Cell Sci. 127, 2161-2173 (2014).
26. H. Tran, R. Pankov, S. D. Tran, B. Hampton, W. H. Burgess, K. M. Yamada, Integrin clustering induces kinectin accumulation. J. Cell Sci. 115, 2031-2040 (2002).
27. J. van Rijssel, J. Kroon, M. Hoogenboezem, F. P. J. van Alphen, R. J. de Jong, E. Kostadinova, D. Geerts, P. L. Hordijk, J. D. van Buul, The Rho-guanine nucleotide exchange factor Trio controls leukocyte transendothelial migration by promoting docking structure formation. Mol. Biol. Cell 23, 2831-2844 (2012).
28. N. V. Belkina, Y. Liu, J.-J. Hao, H. Karasuyama, S. Shaw, LOK is a major ERM kinase in resting lymphocytes and regulates cytoskeletal rearrangement through ERM phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 106, 4707-4712 (2009).
29. W. A. Muller, S. A. Weigl, X. Deng, D. M. Phillips, PECAM-1 is required for transendothelial migration of leukocytes. J. Exp. Med. 178, 449-460 (1993).
30. F. Liao, J. Ali, T. Greene, W. A. Muller, Soluble domain 1 of platelet-endothelial cell adhesion molecule (PECAM) is sufficient to block transendothelial migration in vitro and in vivo. J. Exp. Med. 185, 1349-1357 (1997).
31. E. Boeri Erba, E. Bergatto, S. Cabodi, L. Silengo, G. Tarone, P. Defilippi, O. N. Jensen, Systematic analysis of the epidermal growth factor receptor by mass spectrometry reveals stimulation-dependent multisite phosphorylation. Mol. Cell. Proteomics 4, 1107-1121 (2005).
32. J.-K. Jin, P.-C. Tien, C.-J. Cheng, J. H. Song, C. Huang, S.-H. Lin, G. E. Gallick, Talin1 phosphorylation activates b1 integrins: A novel mechanism to promote prostate cancer bone metastasis. Oncogene 34, 1811-1821 (2014).
33. T. K. Kwak, M.-S. Lee, J. Ryu, Y.-J. Choi, M. Kang, D. Jeong, J. W. Lee, Cell adhesiondependent serine 85 phosphorylation of paxillin modulates focal adhesion formation and haptotactic migration via association with the C-terminal tail domain of talin. J. Biol. Chem. 287, 27499-27509 (2012).
34. A. Zagórska, M. Deak, D. G. Campbell, S. Banerjee, M. Hirano, S. Aizawa, A. R. Prescott, D. R. Alessi, New roles for the LKB1-NUAK pathway in controlling myosin phosphatase complexes and cell adhesion. Sci. Signal. 3, ra25 (2010).
35. S. A. Eccles, The epidermal growth factor receptor/Erb-B/HER family in normal and malignant breast biology. Int. J. Dev. Biol. 55, 685-696 (2011).
36. N. Galjart, CLIPs and CLASPs and cellular dynamics. Nat. Rev. Mol. Cell Biol. 6, 487-498 (2005).
37. M. Hu, K. L. Carles-Kinch, D. P. Zelinski, M. S. Kinch, EphA2 induction of fibronectin creates a permissive microenvironment for malignant cells. Mol. Cancer Res. 2, 533-540 (2004).
38. B. P. Fox, R. P. Kandpal, Invasiveness of breast carcinoma cells and transcript profile: Eph receptors and ephrin ligands as molecular markers of potential diagnostic and prognostic application. Biochem. Biophys. Res. Commun. 318, 882-892 (2004).
39. K. J. Martin, D. R. Patrick, M. J. Bissell, M. V. Fournier, Prognostic breast cancer signature identified from 3D culture model accurately predicts clinical outcome across independent datasets. PLOS One 3, e2994 (2008).
40. D. M. Brantley-Sieders, A. Jiang, K. Sarma, A. Badu-Nkansah, D. L. Walter, Y. Shyr, J. Chen, Eph/Ephrin profiling in human breast cancer reveals significant associations between expression level and clinical outcome. PLOS One 6, e24426 (2011).
41. S. A. Hammond, R. Lutterbuese, S. Roff, P. Lutterbuese, B. Schlereth, E. Bruckheimer, M. S. Kinch, S. Coats, P. A. Baeuerle, P. Kufer, P. A. Kiener, Selective targeting and potent control of tumor growth using an EphA2/CD3-Bispecific single-chain antibody construct. Cancer Res. 67, 3927-3935 (2007).
42. L. Zhao, L. Qu, J. Zhou, Z. Sun, H. Zou, Y.-Y. Chen, J. D. Marks, Y. Zhou, High throughput identification of monoclonal antibodies to membrane bound and secreted proteins using yeast and phage display. PLOS One 9, e111339 (2014).
43. M. Macrae, R. M. Neve, P. Rodriguez-Viciana, C. Haqq, J. Yeh, C. Chen, J. W. Gray, F. McCormick, A conditional feedback loop regulates Ras activity through EphA2. Cancer Cell 8, 111-118 (2005).
44. F. Forozan, R. Veldman, C. A. Ammerman, N. Z. Parsa, A. Kallioniemi, O. P. Kallioniemi, S. P. Ethier, Molecular cytogenetic analysis of 11 new breast cancer cell lines. Br. J. Cancer 81, 1328-1334 (1999).
45. R. Cailleau, M. Olivé, Q. V. Cruciger, Long-term human breast carcinoma cell lines of metastatic origin: Preliminary characterization. In Vitro 14, 911-915 (1978).
46. K. Kullander, R. Klein, Mechanisms and functions of eph and ephrin signalling. Nat. Rev. Mol. Cell Biol. 3, 475-486 (2002).
47. D. G. Wilkinson, How attraction turns to repulsion. Nat. Cell Biol. 5, 851-853 (2003).
48. M. Hattori, M. Osterfield, J. G. Flanagan, Regulated cleavage of a contact-mediated axon repellent. Science 289, 1360-1365 (2000).
49. P. W. Janes, N. Saha, W. A. Barton, M. V. Kolev, S. H. Wimmer-Kleikamp, E. Nievergall, C. P. Blobel, J.-P. Himanen, M. Lackmann, D. B. Nikolov, Adam Meets Eph: An ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans. Cell 123, 291-304 (2005).
50. K. L. Binns, P. P. Taylor, F. Sicheri, T. Pawson, S. J. Holland Phosphorylation of tyrosine residues in the kinase domain and juxtamembrane region regulates the biological and catalytic activities of Eph receptors. Mol. Cell Biol. 20, 4791-4805 (2000).
51. L. E. Wybenga-Groot, B. Baskin, S. H. Ong, J. Tong, T. Pawson, F. Sicheri, Structural basis for autoinhibition of the EphB2 receptor tyrosine kinase by the unphosphorylated juxtamembrane region. Cell 106, 745-757 (2001).
52. S. Wiesner, L. E. Wybenga-Groot, N. Warner, H. Lin, T. Pawson, J. D. Forman-Kay, F. Sicheri, A change in conformational dynamics underlies the activation of Eph receptor tyrosine kinases. EMBO J. 25, 4686-4696 (2006).
53. P. D. Bos, X. H.-F. Zhang, C. Nadal, W. Shu, R. R. Gomis, D. X. Nguyen, A. J. Minn, M. J. van de Vijver, W. L. Gerald, J. A. Foekens, J. Massagué, Genes that mediate breast cancer metastasis to the brain. Nature 459, 1005-1009 (2009).
54. Y. Kang, P. M. Siegel, W. Shu, M. Drobnjak, S.M. Kakonen, C. Cordón-Cardo, T. A. Guise, J. Massagué, A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537-549 (2003).
55. M. Parri, F. Buricchi, M. Letizia Taddei, E. Giannoni, G. Raugei, G. Ramponi, P. Chiarugi, EphrinA1 repulsive response is regulated by an EphA2 tyrosine phosphatase. J. Biol. Chem. 280, 34008-34018 (2005).
56. P. Chiarugi,M. L. Taddei, N. Schiavone, L. Papucci, E.Giannoni, T. Fiaschi, S. Capaccioli, G. Raugei, G. Ramponi, LMW-PTP is a positive regulator of tumor onset and growth. Oncogene 23, 3905-3914 (2004).
57. K. D. Kikawa, D. R. Vidale, R. L. Van Etten, M. S. Kinch, Regulation of the EphA2 kinase by the low molecular weight tyrosine phosphatase induces transformation. J. Biol. Chem. 277, 39274-39279 (2002).
58. D. Balasubramaniam, L. N. Paul, K. T. Homan, M. C. Hall, C. V. Stauffacher, Specificity of HCPTP variants toward EphA2 tyrosines by quantitative selected reaction monitoring. Protein Sci. 20, 1172-1181 (2011).
59. R. K. Vadlamudi, F. Li, L. Adam, D. Nguyen, Y. Ohta, T. P. Stossel, R. Kumar, Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat. Cell Biol. 4, 681-690 (2002).
60. M. S. Woo, Y. Ohta, I. Rabinovitz, T. P. Stossel, J. Blenis, Ribosomal S6 kinase (RSK) regulates phosphorylation of filamin A on an important regulatory site. Mol. Cell Biol. 24, 3025-3035 (2004).
61. D. P. Zelinski, N. D. Zantek, J. C. Stewart, A. R. Irizarry, M. S. Kinch, EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res. 61, 2301-2306 (2001).
62. N. D. Zantek, J. Walker-Daniels, J. Stewart, R. K. Hansen, D. Robinson, H. Miao, B. Wang, H.-J. Kung, M. J. Bissell, M. S. Kinch, MCF-10A-NeoST: A new cell system for studying cell-ECM and cell-cell interactions in breast cancer. Clin. Cancer Res. 7, 3640-3648 (2001).
63. W. B. Fang, D. M. Brantley-Sieders, M. A. Parker, A. D. Reith, J. Chen, A kinasedependent role for EphA2 receptor in promoting tumor growth and metastasis. Oncogene 24, 7859-7868 (2005).
64. D. M. Brantley-Sieders, G. Zhuang, D. Hicks, W. B. Fang, Y. Hwang, J. M. M. Cates, K. Coffman, D. Jackson, E. Bruckheimer, R. S. Muraoka-Cook, J. Chen, The receptor tyrosine kinase EphA2 promotes mammary adenocarcinoma tumorigenesis and metastatic progression in mice by amplifying ErbB2 signaling. J. Clin. Invest. 118, 64-78 (2008).
65. N. D. Zantek, M. Azimi, M. Fedor-Chaiken, B. Wang, R. Brackenbury, M. S. Kinch, Ecadherin regulates the function of the EphA2 receptor tyrosine kinase. Cell Growth Differ. 10, 629-638 (1999).
66. J. Wykosky, D. M. Gibo, C. Stanton, W. Debinski, EphA2 as a novel molecular marker and target in glioblastoma multiforme. Mol. Cancer Res. 3, 541-551 (2005).
67. H. Miao, D.-Q. Li, A. Mukherjee, H. Guo, A. Petty, J. Cutter, J. P. Basilion, J. Sedor, J. Wu, D. Danielpour, A. E. Sloan, M. L. Cohen, B. Wang, EphA2 mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and invasion via a reciprocal regulatory loop with Akt. Cancer Cell 16, 9-20 (2009).
68. T. Tawadros, M. D. Brown, C. A. Hart, N. W. Clarke, Ligand-independent activation of EphA2 by arachidonic acid induces metastasis-like behaviour in prostate cancer cells. Br. J. Cancer 107, 1737-1744 (2012).
69. A. J. Minn, G. P. Gupta, D. Padua, P. Bos, D. X. Nguyen, D. Nuyten, B. Kreike, Y. Zhang, Y. Wang, H. Ishwaran, J. A. Foekens, M. van de Vijver, J. Massagué, Lung metastasis genes couple breast tumor size and metastatic spread. Proc. Natl. Acad. Sci. U.S.A. 104, 6740-6745 (2007).
70. G. Palmisano, S. E. Lendal, K. Engholm-Keller, R. Leth-Larsen, B. L. Parker, M. R. Larsen, Selective enrichment of sialic acid-containing glycopeptides using titanium dioxide chromatography with analysis by HILIC and mass spectrometry. Nat. Protoc. 5, 1974-1982 (2010).
71. J. R. Wis̈niewski, A. Zougman, N. Nagaraj, M. Mann, Universal sample preparation method for proteome analysis. Nat. Methods 6, 359-362 (2009).
72. K. Engholm-Keller, T. A. Hansen, G. Palmisano, M. R. Larsen, Multidimensional strategy for sensitive phosphoproteomics incorporating protein prefractionation combined with SIMAC, HILIC, and TiO2 chromatography applied to proximal EGF signaling. J. Proteome Res. 10, 5383-5397 (2011).
73. J. D. Worboys, J. Sinclair, Y. Yuan, C. O. Jørgensen, Systematic evaluation of quantotypic peptides for targeted analysis of the human kinome. Nat. Methods 11, 1041-1044 (2014).
74. B. MacLean, D. M. Tomazela, N. Shulman, M. Chambers, G. L. Finney, B. Frewen, R. Kern, D. L. Tabb, D. C. Liebler, M. J. MacCoss, Skyline: An open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966-968 (2010).
75. S. J. Holland, N. W. Gale, G. D. Gish, R. A. Roth, Z. Songyang, L. C. Cantley, M. Henkemeyer, G. D. Yancopoulos, T. Pawson, Juxtamembrane tyrosine residues couple the Eph family receptor EphB2/Nuk to specific SH2 domain proteins in neuronal cells. EMBO J. 16, 3877-3888 (1997).
76. J. A. Vizcaíno, R. G. Côté, A. Csordas, J. A. Dianes, A. Fabregat, J. M. Foster, J. Griss, E. Alpi, M. Birim, J. Contell, G. O'Kelly, A. Schoenegger, D. Ovelleiro, Y. Pérez-Riverol, F. Reisinger, D. Ríos, R. Wang, H. Hermjakob, The PRoteomics IDEntifications (PRIDE) database and associated tools: Status in 2013. Nucleic Acids Res. 41, D1063-D1069 (2013).
77. T. Farrah, E. W. Deutsch,R. Kreisberg, Z. Sun, D.S.Campbell, L. Mendoza, U. Kusebauch, M.-Y. Brusniak, R. Hüttenhain, R. Schiess, N. Selevsek, R. Aebersold, R. L. Moritz, PASSEL: The PeptideAtlas SRMexperiment library. Proteomics 12, 1170-1175 (2012).