A urokinase receptor-bim signaling axis emerges during EGFR inhibitor resistance in mutant EGFR glioblastoma

Cancer Research

Volumn 75, Issue 2, 2015, Pages 394-404

  Wykosky, Jill ^a   Hu, Jingjing ^b,c   Gomez, German G ^a   Taylor, Tiffany ^a   Villa, Genaro R ^a   Pizzo, Donald ^b   Van Den Berg, Scott R ^b   Thorne, Amy Haseley ^a   Chen, Clark C ^c   Mischel, Paul S ^a,b,c   Gonias, Steven L ^b,c   Cavenee, Webster K ^a,c   Furnari, Frank B ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; BIM PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GEFITINIB; UROKINASE RECEPTOR; APOPTOSIS REGULATORY PROTEIN; BCL-2-LIKE PROTEIN 11; MEMBRANE PROTEIN; ONCOPROTEIN; QUINAZOLINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL PROLIFERATION; CELL VIABILITY; CHRONIC DRUG ADMINISTRATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; DRUG DOSE REDUCTION; DRUG EFFECT; FEMALE; GLIOBLASTOMA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN NEOPLASMS; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; NUDE MOUSE; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; BRAIN NEOPLASMS; CELL LINE, TUMOR; ERLOTINIB HYDROCHLORIDE; FEMALE; GLIOBLASTOMA; HETEROGRAFTS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, NUDE; PROTO-ONCOGENE PROTEINS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; SIGNAL TRANSDUCTION;

EID: 84920996740     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2004     Document Type: Article

References (50)

1. Dunn GP, Rinne ML, Wykosky J, Genovese G, Quayle SN, Dunn IF, et al. Emerging insights into the molecular and cellular basis of glioblastoma. Genes Dev 2012;26:756-84.
2. Nishikawa R, Ji XD, Harmon RC, Lazar CS, Gill GN, Cavenee WK, et al. A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity. Proc Natl Acad Sci U S A 1994;91: 7727-31.
3. Mukasa A, Wykosky J, Ligon KL, Chin L, Cavenee WK, Furnari F. Mutant EGFR is required formaintenance of glioma growth in vivo, and its ablation leads to escape from receptor dependence. Proc Natl Acad Sci U S A 2010;107:2616-21.
4. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004;350:2129-39.
5. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004;304:1497-500.
6. Wykosky J, Fenton T, Furnari F, Cavenee WK. Therapeutic targeting of epidermal growth factor receptor in human cancer: successes and limitations. Chin J Cancer 2011;30:5-12.
7. Engelman JA, Janne PA. Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res 2008;14:2895-9.
8. Diaz LA Jr, Williams RT,WuJ, Kinde I, Hecht JR, Berlin J, et al. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 2012;486:537-40.
9. Karapetis CS, Khambata-Ford S, Jonker DJ, O'Callaghan CJ, Tu D, Tebbutt NC, et al. K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med 2008;359:1757-65.
10. Misale S, Yaeger R, Hobor S, Scala E, Janakiraman M, Liska D, et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 2012;486:532-6.
11. Bean J, Brennan C, Shih JY, Riely G, Viale A, Wang L, et al. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib. Proc Natl Acad Sci U S A 2007;104:20932-7.
12. Kobayashi S, Boggon TJ, Dayaram T, Janne PA, KocherO,MeyersonM, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 2005;352:786-92.
13. Mellinghoff IK, Wang MY, Vivanco I, Haas-Kogan DA, Zhu S, Dia EQ, et al. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 2005;353:2012-24.
14. Stommel JM, Kimmelman AC, Ying H, Nabioullin R, Ponugoti AH, Wiedemeyer R, et al. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 2007;318:287-90.
15. Fenton TR, Nathanson D, Ponte de Albuquerque C, Kuga D, Iwanami A, Dang J, et al. Resistance to EGF receptor inhibitors in glioblastoma mediated by phosphorylation of the PTEN tumor suppressor at tyrosine 240. Proc Natl Acad Sci U S A 2012;109:14164-9.
16. Blasi F, Carmeliet P. uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol 2002;3:932-43.
17. Jo M, Thomas KS, Marozkina N, Amin TJ, Silva CM, Parsons SJ, et al. Dynamic assembly of the urokinase-type plasminogen activator signaling receptor complex determines the mitogenic activity of urokinase-type plasminogen activator. J Biol Chem 2005;280:17449-57.
18. Aguirre-Ghiso JA, Liu D, Mignatti A, Kovalski K, Ossowski L. Urokinase receptor and fibronectin regulate the ERKMAPK to p38MAPK activity ratios that determine carcinoma cell proliferation or dormancy in vivo. Mol Biol Cell 2001;12:863-79.
19. Ma Z, Webb DJ, Jo M, Gonias SL. Endogenously produced urokinase-type plasminogen activator is a major determinant of the basal level of activated ERK/MAP kinase and prevents apoptosis in MDA-MB-231 breast cancer cells. J Cell Sci 2001;114:3387-96.
20. Smith HW, Marra P, Marshall CJ. uPAR promotes formation of the p130Cas-Crk complex to activate Rac through DOCK180. J Cell Biol 2008;182:777-90.
21. Adachi Y, Chandrasekar N, Kin Y, Lakka SS, Mohanam S, Yanamandra N, et al. Suppression of glioma invasion and growth by adenovirus-mediated delivery of a bicistronic construct containing antisense uPAR and sense p16 gene sequences. Oncogene 2002;21:87-95.
22. Jo M, Eastman BM, Webb DL, Stoletov K, Klemke R, Gonias SL. Cell signaling by urokinase-type plasminogen activator receptor induces stem cell-like properties in breast cancer cells. Cancer Res 2010;70: 8948-58.
23. Hu J, Jo M, Cavenee WK, Furnari F, VandenBerg SR, Gonias SL. Crosstalk between the urokinase-type plasminogen activator receptor and EGF receptor variant III supports survival and growth of glioblastoma cells. Proc Natl Acad Sci U S A 2011;108:15984-9.
24. Bachoo RM, Maher EA, Ligon KL, Sharpless NE, Chan SS, You MJ, et al. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell 2002;1:269-77.
25. Sarkaria JN, Carlson BL, Schroeder MA, Grogan P, Brown PD, Giannini C, et al. Use of an orthotopic xenograft model for assessing the effect of epidermal growth factor receptor amplification on glioblastoma radiation response. Clin Cancer Res 2006;12:2264-71.
26. Shah K, Hingtgen S, Kasmieh R, Figueiredo JL, Garcia-Garcia E, Martinez-Serrano A, et al. Bimodal viral vectors and in vivo imaging reveal the fate of human neural stem cells in experimental glioma model. J Neurosci 2008;28:4406-13.
27. Deutsch DG, Mertz ET. Plasminogen: purification from human plasma by affinity chromatography. Science 1970;170:1095-6.
28. Creighton CJ, Hilger AM, Murthy S, Rae JM, Chinnaiyan AM, El-Ashry D. Activation of mitogen-activated protein kinase in estrogen receptor a-positive breast cancer cells in vitro induces an in vivo molecular phenotype of estrogen receptor a-negative human breast tumors. Cancer Res 2006;66:3903-11.
29. Nathanson DA, Gini B, Mottahedeh J, Visnyei K, Koga T, Gomez G, et al. Targeted therapy resistance mediated by dynamic regulation of extrachromosomal mutant EGFR DNA. Science 2014;343:72-6.
30. Adams JM, Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007;26:1324-37.
31. Hu J, Muller KA, Furnari F, Cavenee WK, VandenBerg SR, Gonias SL. Targeting the EGF receptor in glioblastoma cells stimulates cell migration by activating uPAR-initiated cell signaling. Oncogene 2014 Oct 27. [Epub ahead of print].
32. Janjigian YY, Viola-Villegas N, Holland JP, Divilov V, Carlin SD, Gomes-DaGama EM, et al. Monitoring afatinib treatment in HER2-positive gastric cancer with 18F-FDG and 89Zr-trastuzumab PET. J Nucl Med 2013;54: 936-43.
33. Salajegheh M, Rudnicki A, Smith TW. Expression of urokinase-type plasminogen activator receptor (uPAR) in primary central nervous system neoplasms. Appl Immunohistochem Mol Morphol 2005;13:184-9.
34. Chonghaile TN, Letai A. Mimicking the BH3 domain to kill cancer cells. Oncogene 2009;27:S149-S57.
35. Cragg MS, Kuroda J, Puthalakath H, Huang DC, Strasser A. Gefitinibinduced killing of NSCLC cell lines expressing mutant EGFR requires BIM and can be enhanced by BH3 mimetics. PLoS Med 2007;4:1681-89.
36. Gong Y, Somwar R, Politi K, Balak M, Chmielecki J, Jiang X, et al. Induction of BIM is essential for apoptosis triggered by EGFR kinase inhibitors in mutant EGFR-dependent lung adenocarcinomas. PLoS Med 2007;4:e294.
37. OsmakM, Vrhovec I, Skrk J. Cisplatin resistant glioblastoma cells may have increased concentration of urokinase plasminogen activator and plasminogen activator inhibitor type 1. J neurooncol 1999;42:95-102.
38. Francis JM, Zhang C-Z, Maire CL, Jung J, Manzo VE, Adalsteinsson VA, et al. EGFR variant heterogeneity in glioblastoma resolved through single-nucleus sequencing. Cancer Discov 2014;4:956-71.
39. Sunters A, Fern-andez de Mattos S, Stahl M, Brosens JJ, Zoumpoulidou G, Saunders CA, et al. FoxO3a transcriptional regulation of bim controls apoptosis in paclitaxel-treated breast cancer cell lines. J Biol Chem 2003;278:49795-805.
40. Harada H, Quearry B, Ruiz-Vela A, Korsmeyer SJ. Survival factor-induced extracellular signal-regulated kinase phosphorylates BIM, inhibiting its association with BAX and proapoptotic activity. Proc Natl Acad Sci U S A 2004;101:15313-7.
41. Ley R, Balmanno K, Hadfield K, Weston C, Cook SJ. Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein, bim. J Biol Chem 2003;278: 18811-6.
42. Puthalakath H, Huang DCS, O'Reilly LA, King SM, Strasser A. The proapoptotic activity of the Bcl-2 family member bim is regulated by interaction with the dynein motor complex. Mol Cell 1999;3:287-96.
43. Billard C. BH3 mimetics: status of the field and new developments. Mol Cancer Ther 2013;12:1691-700.
44. Yuan Z, Wang F, Zhao Z, Zhao X, Qiu J, Nie C, et al. BIM-mediated AKT phosphorylation is a key modulator of arsenic trioxide-induced apoptosis in cisplatin-sensitive and-resistant ovarian cancer cells. PLoS ONE 2011;6: e20586.
45. Brunet A, Bonni A, ZigmondMJ, Lin MZ, Juo P, Hu LS, et al. Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 1999;96:857-68.
46. Tanizaki J,Okamoto I, Fumita S,Okamoto W, Nishio K, Nakagawa K. Roles of BIM induction and survivin downregulation in lapatinib-induced apoptosis in breast cancer cells with HER2 amplification. Oncogene 2011;30:4097-106.
47. Huang M-H, Lee J-H, Chang Y-J, Tsai H-H, Lin Y-L, Lin AM-Y, et al. MEK inhibitors reverse resistance in epidermal growth factor receptor mutation lung cancer cells with acquired resistance to gefitinib. Mol Oncol 2013; 7:112-20.
48. Paland N, Aharoni S, Fuhrman B. Urokinase-type plasminogen activator (uPA) modulates monocyte-to-macrophage differentiation and prevents Ox-LDL-induced macrophage apoptosis. Atherosclerosis 2013;231:29-38.
49. Lund IK, Jogi A, Rùnù B, Rasch MG, Lund LR, Almholt K, et al. Antibodymediated targeting of the urokinase-type plasminogen activator proteolytic function neutralizes fibrinolysis in vivo. J Biol Chem 2008;283:32506-15.
50. Ghamande SA, Silverman MH, Huh W, Behbakht K, Ball G, Cuasay L, et al. A phase 2, randomized, double-blind, placebo-controlled trial of clinical activity and safety of subcutaneous Å6 in women with asymptomatic CA125 progression after first-line chemotherapy of epithelial ovarian cancer. Gynecol Oncol 2008;111: 89-94.