The tyrosine phosphatase PTPN14 (Pez) inhibits metastasis by altering protein trafficking

Science Signaling

Volumn 8, Issue 364, 2015, Pages

  Belle, Leila ^a,b   Ali, Naveid ^c   Lonic, Ana ^a,b   Li, Xiaochun ^a   Paltridge, James L ^a,b   Roslan, Suraya ^a   Herrmann, David ^c   Conway, James R W ^c   Gehling, Freya K ^a   Bert, Andrew G ^a   Crocker, Lesley A ^a   Tsykin, Anna ^a   Farshid, Gelareh ^d   Goodall, Gregory J ^a,b   Timpson, Paul ^c   Daly, Roger J ^c,e   Khew Goodall, Yeesim ^a,b  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d SA PATHOLOGY   (Australia)

^e MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CELL SURFACE RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; INTERLEUKIN 8; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 14; PROTEIN KINASE C DELTA; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 3; CYTOKINE; PRKCD PROTEIN, MOUSE; PTPN14 PROTEIN, MOUSE; RAB PROTEIN; RIN1 PROTEIN, MOUSE; SIGNAL PEPTIDE;

ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CELL CULTURE; CELL SURFACE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE RELEASE; ENDOTHELIUM CELL; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; METASTASIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SECRETORY PATHWAY; TUMOR CELL; TUMOR GROWTH; TUMOR INVASION; XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST TUMOR; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; GENETICS; IMMUNOPRECIPITATION; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; METABOLISM; NEOPLASM METASTASIS; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT; TANDEM MASS SPECTROMETRY; TUMOR CELL LINE; TUMOR MICROENVIRONMENT; WESTERN BLOTTING;

MUS;

ANIMALS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCKDOWN TECHNIQUES; HETEROGRAFTS; HUMANS; IMMUNOPRECIPITATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; ISOTOPE LABELING; MICE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PROTEIN KINASE C-DELTA; PROTEIN TRANSPORT; PROTEIN TYROSINE PHOSPHATASES, NON-RECEPTOR; RAB GTP-BINDING PROTEINS; TANDEM MASS SPECTROMETRY; TUMOR MICROENVIRONMENT;

EID: 84923068934     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2005547     Document Type: Article

References (62)

1. D. Hanahan, R. A. Weinberg, Hallmarks of cancer: The next generation. Cell 144, 646-674 (2011).
2. H. Peinado, S. Lavotshkin, D. Lyden, The secreted factors responsible for pre-metastatic niche formation: Old sayings and new thoughts. Semin. Cancer Biol. 21, 139-146 (2011).
3. R. N. Kaplan, R. D. Riba, S. Zacharoulis, A. H. Bramley, L. Vincent, C. Costa, D. D. MacDonald, D. K. Jin, K. Shido, S. A. Kerns, Z. Zhu, D. Hicklin, Y. Wu, J. L. Port, N. Altorki, E. R. Port, D. Ruggero, S. V. Shmelkov, K. K. Jensen, S. Rafii, D. Lyden, VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438, 820-827 (2005).
4. H. Peinado, M. Alečković, S. Lavotshkin, I. Matei, B. Costa-Silva, G. Moreno-Bueno, M. Hergueta-Redondo, C. Williams, G. García-Santos, C. Ghajar, A. Nitadori-Hoshino, C. Hoffman, K. Badal, B. A. Garcia, M. K. Callahan, J. Yuan, V. R. Martins, J. Skog, R. N. Kaplan, M. S. Brady, J. D. Wolchok, P. B. Chapman, Y. Kang, J. Bromberg, D. Lyden, Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 18, 883-891 (2012).
5. M. Makridakis, A. Vlahou, Secretome proteomics for discovery of cancer biomarkers. J. Proteomics 73, 2291-2305 (2010).
6. L. Sepiashvili, A. Hui, V. Ignatchenko, W. Shi, S. Su, W. Xu, S. H. Huang, B. O'Sullivan, J. Waldron, J. C. Irish, B. Perez-Ordonez, F. F. Liu, T. Kislinger, Potentially novel candidate biomarkers for head and neck squamous cell carcinoma identified using an integrated cell line-based discovery strategy. Mol. Cell. Proteomics 11, 1404-1415 (2012).
7. D. Hanahan, L. M. Coussens, Accessories to the crime: Functions of cells recruited to the tumor microenvironment. Cancer Cell 21, 309-322 (2012).
8. G. Pocsfalvi, G. Votta, A. De Vincenzo, I. Fiume, D. A. Raj, G. Marra, M. P. Stoppelli, I. Iaccarino, Analysis of secretome changes uncovers an autocrine/paracrine component in the modulation of cell proliferation and motility by c-Myc. J. Proteome Res. 10, 5326-5337 (2011).
9. P. M. Neilsen, J. E. Noll, R. J. Suetani, R. B. Schulz, F. Al-Ejeh, A. Evdokiou, D. P. Lane, D. F. Callen, Mutant p53 uses p63 as a molecular chaperone to alter gene expression and induce a pro-invasive secretome. Oncotarget 2, 1203-1217 (2011).
10. A. Bronisz, J. Godlewski, J. A. Wallace, A. S. Merchant, M. O. Nowicki, H. Mathsyaraja, R. Srinivasan, A. J. Trimboli, C. K. Martin, F. Li, L. Yu, S. A. Fernandez, T. Pécot, T. J. Rosol, S. Cory, M. Hallett, M. Park, M. G. Piper, C. B. Marsh, L. D. Yee, R. E. Jimenez, G. Nuovo, S. E. Lawler, E. A. Chiocca, G. Leone, M. C. Ostrowski, Reprogramming of the tumour microenvironment by stromal PTEN-regulated miR-320. Nat. Cell Biol. 14, 159-167 (2012).
11. Y. Khew-Goodall, G. J. Goodall, Stromal miR-320 keeps an oncogenic secretome in check. Nat. Cell Biol. 14, 124-125 (2012).
12. A. L. Smith, P. J. Mitchell, J. Shipley, B. A. Gusterson, M. V. Rogers, M. R. Crompton, Pez: A novel human cDNA encoding protein tyrosine phosphatase- and ezrin-like domains. Biochem. Biophys. Res. Commun. 209, 959-965 (1995).
13. L. Wyatt, C. Wadham, L. A. Crocker, M. Lardelli, Y. Khew-Goodall, The protein tyrosine phosphatase Pez regulates TGFb, epithelial-mesenchymal transition, and organ development. J. Cell Biol. 178, 1223-1235 (2007).
14. I. Poernbacher, R. Baumgartner, S. K. Marada, K. Edwards, H. Stocker, Drosophila Pez acts in Hippo signaling to restrict intestinal stem cell proliferation. Curr. Biol. 22, 389-396 (2012).
15. A. C. Au, P. A. Hernandez, E. Lieber, A. M. Nadroo, Y. M. Shen, K. A. Kelley, B. D. Gelb, G. A. Diaz, Protein tyrosine phosphatase PTPN14 is a regulator of lymphatic function and choanal development in humans. Am. J. Hum. Genet. 87, 436-444 (2010).
16. Z. Wang, D. Shen, D. W. Parsons, A. Bardelli, J. Sager, S. Szabo, J. Ptak, N. Silliman, B. A. Peters, M. S. van der Heijden, G. Parmigiani, H. Yan, T. L. Wang, G. Riggins, S. M. Powell, J. K. Willson, S. Markowitz, K. W. Kinzler, B. Vogelstein, V. E. Velculescu, Mutational analysis of the tyrosine phosphatome in colorectal cancers. Science 304, 1164-1166 (2004).
17. T. Sjöblom, S. Jones, L. D. Wood, D. W. Parsons, J. Lin, T. D. Barber, D. Mandelker, R. J. Leary, J. Ptak, N. Silliman, S. Szabo, P. Buckhaults, C. Farrell, P. Meeh, S. D. Markowitz, J. Willis, D. Dawson, J. K. Willson, A. F. Gazdar, J. Hartigan, L. Wu, C. Liu, G. Parmigiani, B. H. Park, K. E. Bachman, N. Papadopoulos, B. Vogelstein, K. W. Kinzler, V. E. Velculescu, The consensus coding sequences of human breast and colorectal cancers. Science 314, 268-274 (2006).
18. M. Li, H. Zhao, X. Zhang, L. D. Wood, R. A. Anders, M. A. Choti, T. M. Pawlik, H. D. Daniel, R. Kannangai, G. J. A. Offerhaus, V. E. Velculescu, L. Wang, S. Zhou, B. Vogelstein, R. H. Hruban, N. Papadopoulos, J. Cai, M. S. Torbenson, K. W. Kinzler, Inactivating mutations of the chromatin remodeling gene ARID2 in hepatocellular carcinoma. Nat. Genet. 43, 828-829 (2011).
19. C. Wadham, J. R. Gamble, M. A. Vadas, Y. Khew-Goodall, The protein tyrosine phosphatase Pez is a major phosphatase of adherens junctions and dephosphorylates β-catenin. Mol. Biol. Cell 14, 2520-2529 (2003).
20. X. Liu, N. Yang, S. A. Figel, K. E. Wilson, C. D. Morrison, I. H. Gelman, J. Zhang, PTPN14 interacts with and negatively regulates the oncogenic function of YAP. Oncogene 32, 1266-1273 (2013).
21. P. Zhang, A. Guo, A. Possemato, C. Wang, L. Beard, C. Carlin, S. D. Markowitz, R. D. Polakiewicz, Z. Wang, Identification and functional characterization of p130Cas as a substrate of protein tyrosine phosphatase nonreceptor 14. Oncogene 32, 2087-2095 (2013).
22. M. Ogata, T. Takada, Y. Mori, M. Oh-hora, Y. Uchida, A. Kosugi, K. Miyake, T. Hamaoka, Effects of overexpression of PTP36, a putative protein tyrosine phosphatase, on cell adhesion, cell growth, and cytoskeletons in HeLa cells. J. Biol. Chem. 274, 12905-12909 (1999).
23. C. Michaloglou, W. Lehmann, T. Martin, C. Delaunay, A. Hueber, L. Barys, H. Niu, E. Billy, M. Wartmann, M. Ito, C. J. Wilson, M. E. Digan, A. Bauer, H. Voshol, G. Christofori, W. R. Sellers, F. Hofmann, T. Schmelzle, The tyrosine phosphatase PTPN14 is a negative regulator of YAP activity. PLOS One 8, e61916 (2013).
24. W. Wang, J. Huang, X. Wang, J. Yuan, X. Li, L. Feng, J. I. Park, J. Chen, PTPN14 is required for the density-dependent control of YAP1. Genes Dev. 26, 1959-1971 (2012).
25. J. M. Huang, I. Nagatomo, E. Suzuki, T. Mizuno, T. Kumagai, A. Berezov, H. Zhang, B. Karlan, M. I. Greene, Q. Wang, YAP modifies cancer cell sensitivity to EGFR and survivin inhibitors and is negatively regulated by the non-receptor type protein tyrosine phosphatase 14. Oncogene 32, 2220-2229 (2013).
26. P. A. Gregory, C. P. Bracken, E. Smith, A. G. Bert, J. A. Wright, S. Roslan, M. Morris, L. Wyatt, G. Farshid, Y. Y. Lim, G. J. Lindeman, M. F. Shannon, P. A. Drew, Y. Khew-Goodall, G. J. Goodall, An autocrine TGF- b/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol. Biol. Cell 22, 1686-1698 (2011).
27. R. M. Neve, K. Chin, J. Fridlyand, J. Yeh, F. L. Baehner, T. Fevr, L. Clark, N. Bayani, J. P. Coppe, F. Tong, T. Speed, P. T. Spellman, S. DeVries, A. Lapuk, N. J. Wang, W. L. Kuo, J. L. Stilwell, D. Pinkel, D. G. Albertson, F. M. Waldman, F. McCormick, R. B. Dickson, M. D. Johnson, M. Lippman, S. Ethier, A. Gazdar, J. W. Gray, A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10, 515-527 (2006).
28. 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).
29. P. Timpson, E. J. McGhee, Z. Erami, M. Nobis, J. A. Quinn, M. Edward, K. I. Anderson, Organotypic collagen I assay: A malleable platform to assess cell behaviour in a 3-dimensional context. J. Vis. Exp., e3089 (2011).
30. J. A. Joyce, J. W. Pollard, Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252 (2009).
31. B. Psaila, D. Lyden, The metastatic niche: Adapting the foreign soil. Nat. Rev. Cancer 9, 285-293 (2009).
32. T. Tiganis, A. M. Bennett, Protein tyrosine phosphatase function: The substrate perspective. Biochem. J. 402, 1-15 (2007).
33. G. G. Tall, M. A. Barbieri, P. D. Stahl, B. F. Horazdovsky, Ras-activated endocytosis is mediated by the Rab5 guanine nucleotide exchange activity of RIN1. Dev. Cell 1, 73-82 (2001).
34. M. A. Barbieri, C. Kong, P. I. Chen, B. F. Horazdovsky, P. D. Stahl, The SRC homology 2 domain of Rin1 mediates its binding to the epidermal growth factor receptor and regulates receptor endocytosis. J. Biol. Chem. 278, 32027-32036 (2003).
35. K. Deininger, M. Eder, E. R. Kramer, W. Zieglgänsberger, H. U. Dodt, K. Dornmair, J. Colicelli, R. Klein, The Rab5 guanylate exchange factor Rin1 regulates endocytosis of the EphA4 receptor in mature excitatory neurons. Proc. Natl. Acad. Sci. U.S.A. 105, 12539-12544 (2008).
36. K. Balaji, C. Mooser, C. M. Janson, J. M. Bliss, H. Hojjat, J. Colicelli, RIN1 orchestrates the activation of Rab5 GTPases and ABL tyrosine kinases to determine the fate of EGFR. J. Cell Sci. 125, 5887-5896 (2012).
37. A. Basu, D. Pal, Two faces of protein kinase Cd: The contrasting roles of PKCδ in cell survival and cell death. ScientificWorldJournal 10, 2272-2284 (2010).
38. S. R. Sampson, D. R. Cooper, Specific protein kinase C isoforms as transducers and modulators of insulin signaling. Mol. Genet. Metab. 89, 32-47 (2006).
39. A. Lladó, P. Timpson, S. Vilà de Muga, J. Moretó, A. Pol, T. Grewal, R. J. Daly, C. Enrich, F. Tebar, Protein kinase Cd and calmodulin regulate epidermal growth factor receptor recycling from early endosomes through Arp2/3 complex and cortactin. Mol. Biol. Cell 19, 17-29 (2008).
40. M. Park, W. K. Kim, M. Song, M. Park, H. Kim, H. J. Nam, S. H. Baek, H. Kim, Protein kinase C-δ-mediated recycling of active KIT in colon cancer. Clin. Cancer Res. 19, 4961-4971 (2013).
41. B. L. Allen-Petersen, C. J. Carter, A. M. Ohm, M. E. Reyland, Protein kinase Cδ is required for ErbB2-driven mammary gland tumorigenesis and negatively correlates with prognosis in human breast cancer. Oncogene 33, 1306-1315 (2014).
42. P. Fang, Z. Zhao, H. Tian, X. Zhang, RIN1 exhibits oncogenic property to suppress apoptosis and its aberrant accumulation associates with poor prognosis in melanoma. Tumour Biol. 33, 1511-1518 (2012).
43. H. F. Yu, G. Zhao, Z. J. Ge, D. R. Wang, J. Chen, Y. Zhang, T. Z. Zha, K. Zhang, M. Zhang, Y. F. Tan, S. J. Zhou, C. Jiang, High RIN1 expression is associated with poor prognosis in patients with gastric adenocarcinoma. Tumour Biol. 33, 1557-1563 (2012).
44. G. Y. Shan, Z. Zhang, Q. G. Chen, X. Y. Yu, G. B. Liu, C. Z. Kong, Overexpression of RIN1 associates with tumor grade and progression in patients of bladder urothelial carcinoma. Tumour Biol. 33, 847-855 (2012).
45. Q. Wang, Y. Gao, Y. Tang, L. Ma, M. Zhao, X. Wang, Prognostic significance of RIN1 gene expression in human non-small cell lung cancer. Acta Histochem. 114, 463-468 (2012).
46. H. Hu, J. M. Bliss, Y. Wang, J. Colicelli, RIN1 is an ABL tyrosine kinase activator and a regulator of epithelial-cell adhesion and migration. Curr. Biol. 15, 815-823 (2005).
47. X. Cao, K. Q. Tanis, A. J. Koleske, J. Colicelli, Enhancement of ABL kinase catalytic efficiency by a direct binding regulator is independent of other regulatory mechanisms. J. Biol. Chem. 283, 31401-31407 (2008).
48. X. Li, S. Roslan, C. N. Johnstone, J. A. Wright, C. P. Bracken, M. Anderson, A. G. Bert, L. A. Selth, R. L. Anderson, G. J. Goodall, P. A. Gregory, Y. Khew-Goodall, MiR-200 can repress breast cancer metastasis through ZEB1-independent but moesindependent pathways. Oncogene 33, 4077-4088 (2014).
49. F. Hochgräfe, L. Zhang, S. A. O ' Toole, B. C. Browne, M. Pinese, A. Porta Cubas, G. M. Lehrbach, D. R. Croucher, D. Rickwood, A. Boulghourjian, R. Shearer, R. Nair, A. Swarbrick, D. Faratian, P. Mullen, D. J. Harrison, A. V. Biankin, R. L. Sutherland, M. J. Raftery, R. J. Daly, Tyrosine phosphorylation profiling reveals the signaling network characteristics of basal breast cancer cells. Cancer Res. 70, 9391-9401 (2010).
50. 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).
51. J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, A. Cardona, Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
52. R. Roskoski, ERK1/2 MAP kinases: Structure, function, and regulation. Pharmacol. Res. 66, 105-143 (2012).
53. E. Kida, M. Walus, K. Jarza¸bek, S. Palminiello, G. Albertini, A. Rabe, Y. W. Hwang, A. Golabek, A form of dual-specificity tyrosine-(Y)-phosphorylation-regulated kinase 1A nonphosphorylated at tyrosine 145 and 147 is enriched in the nuclei of astroglial cells, adult hippocampal progenitors, and some cholinergic axon terminals. Neuroscience 195, 112-127 (2011).
54. K. Balaji, C. Mooser, C. M. Janson, J. M. Bliss, H. Hojjat, J. Colicelli, RIN1 orchestrates the activation of Rab5 GTPases and ABL tyrosine kinases to determine EGFR fate. J. Cell Sci. 125, 5887-5896 (2012).
55. H. Shen, S. M. Ferguson, N. Dephoure, R. Park, Y. Yang, L. Volpicelli-Daley, S. Gygi, J. Schlessinger, P. De Camilli, Constitutive activated Cdc42-associated kinase (Ack) phosphorylation at arrested endocytic clathrin-coated pits of cells that lack dynamin. Mol. Biol. Cell 22, 493-502 (2011).
56. C. Corti, E. Leclerc L'Hostis, M. Quadroni, H. Schmid, I. Durussel, J. Cox, P. Dainese Hatt, P. James, E. Carafoli, Tyrosine phosphorylation modulates the interaction of calmodulin with its target proteins. Eur. J. Biochem. 262, 790-802 (1999).
57. S. Himpel, P. Panzer, K. Eirmbter, H. Czajkowska, M. C. P. L. Sayed, T. Blundell, H. Kentrup, J. Gro, Identification of the autophosphorylation sites and characterization of their effects in the protein kinase DYRK1A. J. Biochem. 505, 497-505 (2001).
58. K. Hughes, E. Nikolakaki, S. E. Plyte, N. F. Totty, J. R. Woodgett, Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J. 12, 803-808 (1993).
59. N. K. Prasad, M. E. Werner, S. J. Decker, Specific tyrosine phosphorylations mediate signal-dependent stimulation of SHIP2 inositol phosphatase activity, while the SH2 domain confers an inhibitory effect to maintain the basal activity. Biochemistry 48, 6285-6287 (2009).
60. J. De Schutter, A. Guillabert, V. Imbault, C. Degraef, C. Erneux, D. Communi, I. Pirson, SHIP2 (SH2 domain-containing inositol phosphatase 2) SH2 domain negatively controls SHIP2 monoubiquitination in response to epidermal growth factor. J. Biol. Chem. 284, 36062-36076 (2009).
61. L. Delahaye, I. Mothe-Satney, M. G. Myers, M. F. White, E. Van Obberghen, Interaction of insulin receptor substrate-1 (IRS-1) with phosphatidylinositol 3-kinase: Effect of substitution of serine for alanine in potential IRS-1 serine phosphorylation sites. Endocrinology 139, 4911-4919 (1998).
62. J. Bao, I. Alroy, H. Waterman, E. D. Schejter, C. Brodie, J. Gruenberg, Y. Yarden, Threonine phosphorylation diverts internalized epidermal growth factor receptors from a degradative pathway to the recycling endosome. J. Biol. Chem. 275, 26178-26186 (2000).