The tyrosine phosphatase PTPRO sensitizes colon cancer cells to anti-EGFR therapy through activation of SRC-mediated EGFR signaling

Oncotarget

Volumn 5, Issue 20, 2014, Pages 10070-10083

  Asbagh, Layka Abbasi ^a,b   Vazquez, Iria ^a,b   Vecchione, Loredana ^a   Budinska, Eva ^c   De Vriendt, Veerle ^a   Baietti, Maria Francesca ^a,b   Steklov, Mikhail ^a,b   Jacobs, Bart ^a   Hoe, Nicholas ^d   Singh, Sharat ^d   Imjeti, Naga Sailaja ^a,e   Zimmermann, Pascale ^a,e   Sablina, Anna ^a,b   Tejpar, Sabine ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c MASARYK UNIVERSITY   (Czech Republic)

^d Prometheus Laboratories   (United States)

^e AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Colon cancer; EGFR; EGFR inhibitor; Phosphatase; PTPRO; SRC kinase

Indexed keywords

CBL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; GEFITINIB; PHOSPHATASE; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE RECEPTOR TYPE O; SARACATINIB; UNCLASSIFIED DRUG; CBL PROTEIN, HUMAN; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR; MESSENGER RNA; PROTEIN KINASE INHIBITOR; PTPRO PROTEIN, HUMAN; QUINAZOLINE DERIVATIVE; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER RESISTANCE; COLON CANCER; CONTROLLED STUDY; DRUG SENSITIZATION; DRUG TARGETING; ENZYME ACTIVATION; GENE LOSS; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CACO 2 CELL LINE; COLONIC NEOPLASMS; ENZYMOLOGY; GENETICS; HCT116 CELL LINE; HEK293 CELL LINE; HT 29 CELL LINE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

CACO-2 CELLS; CELL LINE, TUMOR; COLONIC NEOPLASMS; EPIDERMAL GROWTH FACTOR; HCT116 CELLS; HEK293 CELLS; HT29 CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-CBL; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 3; RNA, MESSENGER; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84930253902     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2458     Document Type: Article

References (50)

1. Avraham R, Yarden Y. Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat Rev Mol Cell Biol. 2011; 12:104-117.
2. Citri A, Yarden Y. EGF-ERBB signalling: towards the systems level. Nat Rev Mol Cell Biol. 2006; 7:505-516.
3. Baselga J, Arteaga CL. Critical update and emerging trends in epidermal growth factor receptor targeting in cancer. J Clin Oncol. 2005; 23:2445-2459.
4. Yarden Y, Pines G. The ERBB network: at last, cancer therapy meets systems biology. Nat Rev Cancer. 2012; 12:553-563.
5. Berset TA, Hoier EF, Hajnal A. The C. elegans homolog of the mammalian tumor suppressor Dep-1/Scc1 inhibits EGFR signaling to regulate binary cell fate decisions. Genes Dev. 2005; 19:1328-1340.
6. Jeon M, Scott MP, Zinn K. Interactions between Type III receptor tyrosine phosphatases and growth factor receptor tyrosine kinases regulate tracheal tube formation in Drosophila. Biol Open. 2012; 1:548-558.
7. Jeon M, Zinn K. Receptor tyrosine phosphatases control tracheal tube geometries through negative regulation of Egfr signaling. Development. 2009; 136:3121-3129.
8. Brady-Kalnay SM, Tonks NK. Protein tyrosine phosphatases as adhesion receptors. Curr Opin Cell Biol. 1995; 7:650-657.
9. Murata Y, Mori M, Kotani T, Supriatna Y, Okazawa H, Kusakari S, Saito Y, Ohnishi H, Matozaki T. Tyrosine phosphorylation of R3 subtype receptor-type protein tyrosine phosphatases and their complex formations with Grb2 or Fyn. Genes Cells. 2010; 15:513-524.
10. Matozaki T, Murata Y, Mori M, Kotani T, Okazawa H, Ohnishi H. Expression, localization, and biological function of the R3 subtype of receptor-type protein tyrosine phosphatases in mammals. Cell Signal. 2010; 22: 1811-1817.
11. Tarcic G, Boguslavsky SK, Wakim J, Kiuchi T, Liu A, Reinitz F, Nathanson D, Takahashi T, Mischel PS, Ng T, Yarden Y. An unbiased screen identifies DEP-1 tumor suppressor as a phosphatase controlling EGFR endocytosis. Curr Biol. 2009; 19:1788-1798.
12. Vecchione L, Jacobs B, Normanno N, Ciardiello F, Tejpar S. EGFR-targeted therapy. Exp Cell Res. 2011; 317:2765-2771.
13. Wheeler DL, Dunn EF, Harari PM. Understanding resistance to EGFR inhibitors-impact on future treatment strategies. Nat Rev Clin Oncol. 2010; 7:493-507.
14. Popovici V, Budinska E, Tejpar S, Weinrich S, Estrella H, Hodgson G, Van Cutsem E, Xie T, Bosman FT, Roth AD, Delorenzi M. Identification of a poor-prognosis BRAF-mutant-like population of patients with colon cancer. J Clin Oncol. 2012; 30:1288-1295.
15. Yu M, Lin G, Arshadi N, Kalatskaya I, Xue B, Haider S, Nguyen F, Boutros PC, Elson A, Muthuswamy LB, Tonks NK, Muthuswamy SK. Expression profiling during mammary epithelial cell three-dimensional morphogenesis identifies PTPRO as a novel regulator of morphogenesis and ErbB2-mediated transformation. Mol Cell Biol. 2012; 32:3913-3924.
16. Blanchetot C, Chagnon M, Dube N, Halle M, Tremblay ML. Substrate-trapping techniques in the identification of cellular PTP targets. Methods. 2005; 35:44-53.
17. Mercan F, Bennett AM. Analysis of protein tyrosine phosphatases and substratesCurr Protoc Mol Biol. 2010; Chapter 18:Unit 18 16.
18. Biscardi JS, Maa MC, Tice DA, Cox ME, Leu TH, Parsons SJ. c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J Biol Chem. 1999; 274:8335-8343.
19. Flint AJ, Tiganis T, Barford D, Tonks NK. Development of "substrate-trapping" mutants to identify physiological substrates of protein tyrosine phosphatases. Proc Natl Acad Sci U S A. 1997; 94:1680-1685.
20. Wu W, Graves LM, Gill GN, Parsons SJ, Samet JM. Src-dependent phosphorylation of the epidermal growth factor receptor on tyrosine 845 is required for zinc-induced Ras activation. J Biol Chem. 2002; 277:24252-24257.
21. Tice DA, Biscardi JS, Nickles AL, Parsons SJ. Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc Natl Acad Sci U S A. 1999; 96:1415-1420.
22. Motiwala T, Datta J, Kutay H, Roy S, Jacob ST. Lyn kinase and ZAP70 are substrates of PTPROt in B-cells: Lyn inactivation by PTPROt sensitizes leukemia cells to VEGF-R inhibitor pazopanib. J Cell Biochem. 2010; 110:846-856.
23. Smart JE, Oppermann H, Czernilofsky AP, Purchio AF, Erikson RL, Bishop JM. Characterization of sites for tyrosine phosphorylation in the transforming protein of Rous sarcoma virus (pp60v-src) and its normal cellular homologue (pp60c-src). Proc Natl Acad Sci U S A. 1981; 78:6013-6017.
24. Yeatman TJ. A renaissance for SRC. Nat Rev Cancer. 2004; 4:470-480.
25. Bao J, Gur G, Yarden Y. Src promotes destruction of c-Cbl: implications for oncogenic synergy between Src and growth factor receptors. Proc Natl Acad Sci U S A. 2003; 100:2438-2443.
26. Yokouchi M, Kondo T, Sanjay A, Houghton A, Yoshimura A, Komiya S, Zhang H, Baron R. Src-catalyzed phosphorylation of c-Cbl leads to the interdependent ubiquitination of both proteins. J Biol Chem. 2001; 276:35185-35193.
27. Wilde A, Beattie EC, Lem L, Riethof DA, Liu SH, Mobley WC, Soriano P, Brodsky FM. EGF receptor signaling stimulates SRC kinase phosphorylation of clathrin, influencing clathrin redistribution and EGF uptake. Cell. 1999; 96:677-687.
28. Ahn S, Kim J, Lucaveche CL, Reedy MC, Luttrell LM, Lefkowitz RJ, Daaka Y. Src-dependent tyrosine phosphorylation regulates dynamin self-assembly and ligand-induced endocytosis of the epidermal growth factor receptor. J Biol Chem. 2002; 277:26642-26651.
29. Lee H, Volonte D, Galbiati F, Iyengar P, Lublin DM, Bregman DB, Wilson MT, Campos-Gonzalez R, Bouzahzah B, Pestell RG, Scherer PE, Lisanti MP. Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo: identification of a c-Src/Cav-1/Grb7 signaling cassette. Mol Endocrinol. 2000; 14:1750-1775.
30. Kim P, Liu X, Lee T, Liu L, Barham R, Kirkland R, Leesman G, Kuller A, Ybarrondo B, Ng SC, Singh S. Highly sensitive proximity mediated immunoassay reveals HER2 status conversion in the circulating tumor cells of metastatic breast cancer patients. Proteome Sci. 2011; 9:75.
31. Logue JS, Morrison DK. Complexity in the signaling network: insights from the use of targeted inhibitors in cancer therapy. Genes Dev. 2012; 26:641-650.
32. Knuechel R Cancer cell lines part 1. In: Human cell culture. Volume 1, edn. Edited by Masters J. Dordrecht: Kluwer Academic; 1999: 213-230.
33. Chen YR, Fu YN, Lin CH, Yang ST, Hu SF, Chen YT, Tsai SF, Huang SF. Distinctive activation patterns in constitutively active and gefitinib-sensitive EGFR mutants. Oncogene. 2006; 25:1205-1215.
34. Chun PY, Feng FY, Scheurer AM, Davis MA, Lawrence TS, Nyati MK. Synergistic effects of gemcitabine and gefitinib in the treatment of head and neck carcinoma. Cancer Res. 2006; 66:981-988.
35. Koizumi F, Shimoyama T, Taguchi F, Saijo N, Nishio K. Establishment of a human non-small cell lung cancer cell line resistant to gefitinib. Int J Cancer. 2005; 116:36-44.
36. Lu Y, Li X, Liang K, Luwor R, Siddik ZH, Mills GB, Mendelsohn J, Fan Z. Epidermal growth factor receptor (EGFR) ubiquitination as a mechanism of acquired resistance escaping treatment by the anti-EGFR monoclonal antibody cetuximab. Cancer Res. 2007; 67:8240-8247.
37. E. Budinska MD, W. De Roock, B. Jacobs, S. Walker, C. Wilson, T. Davison, R. D. Kennedy, S. Tejpar. New insights to gene expression signatures from primary FFPE tumors for the prediction of response to cetuximab in KRAS and BRAF wild-type colorectal cancer (CRC). In: 2010 ASCO Annual Meeting: 2010: J Clin Oncol.; 2010: 243s.
38. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003; 4:249-264.
39. Lee H, Bennett AM. Receptor protein tyrosine phosphatase-receptor tyrosine kinase substrate screen identifies EphA2 as a target for LAR in cell migration. Mol Cell Biol. 2013; 33:1430-1441.
40. Shintani T, Ihara M, Sakuta H, Takahashi H, Watakabe I, Noda M. Eph receptors are negatively controlled by protein tyrosine phosphatase receptor type O. Nat Neurosci. 2006; 9:761-769.
41. Bolen JB, Veillette A, Schwartz AM, DeSeau V, Rosen N. Activation of pp60c-src protein kinase activity in human colon carcinoma. Proc Natl Acad Sci U S A. 1987; 84:2251-2255.
42. Cartwright CA, Kamps MP, Meisler AI, Pipas JM, Eckhart W. pp60c-src activation in human colon carcinoma. J Clin Invest. 1989; 83:2025-2033.
43. Cartwright CA, Meisler AI, Eckhart W. Activation of the pp60c-src protein kinase is an early event in colonic carcinogenesis. Proc Natl Acad Sci U S A. 1990; 87:558-562.
44. Cartwright CA, Coad CA, Egbert BM. Elevated c-Src tyrosine kinase activity in premalignant epithelia of ulcerative colitis. J Clin Invest. 1994; 93:509-515.
45. Summy JM, Gallick GE. Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev. 2003; 22:337-358.
46. Brunton VG, Ozanne BW, Paraskeva C, Frame MC. A role for epidermal growth factor receptor, c-Src and focal adhesion kinase in an in vitro model for the progression of colon cancer. Oncogene. 1997; 14:283-293.
47. Sato K. Cellular Functions Regulated by Phosphorylation of EGFR on Tyr845. Int J Mol Sci. 2013; 14:10761-10790.
48. Wheeler DL, Iida M, Kruser TJ, Nechrebecki MM, Dunn EF, Armstrong EA, Huang S, Harari PM. Epidermal growth factor receptor cooperates with Src family kinases in acquired resistance to cetuximab. Cancer Biol Ther. 2009; 8:696-703.
49. Jones HE, Gee JM, Barrow D, Tonge D, Holloway B, Nicholson RI. Inhibition of insulin receptor isoform-A signalling restores sensitivity to gefitinib in previously de novo resistant colon cancer cells. Br J Cancer. 2006; 95:172-180.
50. Lorenz U. Protein tyrosine phosphatase assays. Curr Protoc Immunol. 2011; Chapter 11:Unit 11 17.