Blockade of EGFR signaling promotes glioma stem-like cell invasiveness by abolishing ID3-mediated inhibition of p27KIP1 and MMP3 expression

Cancer Letters

Volumn 328, Issue 2, 2013, Pages 235-242

  Jin, Xun ^a   Jin, Xiong ^a   Sohn, Young Woo ^a   Yin, Jinlong ^b   Kim, Sung Hak ^a   Joshi, Kaushal ^d   Nam, Do Hyun ^c   Nakano, Ichiro ^d   Kim, Hyunggee ^a  

^a Korea University   (South Korea)

^b National Cancer Center   (South Korea)

^c Sungkyunkwan University School of Medicine   (South Korea)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

EGFR; Glioblastoma; Glioma stem cells; ID3; Invasion

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; CYCLIN DEPENDENT KINASE INHIBITOR 1B; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; GEFITINIB; INHIBITOR OF DIFFERENTIATION 3; RHO KINASE; STROMELYSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; GLIOBLASTOMA; GLIOMA STEM LIKE CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CYCLIN-DEPENDENT KINASE INHIBITOR P27; GLIOMA; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEINS; MATRIX METALLOPROTEINASE 3; MICE; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TYRPHOSTINS;

EID: 84870313535     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.09.005     Document Type: Article

References (44)

1. Wen P.Y., Kesari S. Malignant gliomas in adults. N. Engl. J. Med. 2008, 359:492-507.
2. Nakano I., Kornblum H.I. Brain tumor stem cells. Pediatr. Res. 2006, 59:54R-58R.
3. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
4. Chalmers A.J. Radioresistant glioma stem cells-therapeutic obstacle or promising target?. DNA Repair (Amst) 2007, 6:1391-1394.
5. Johannessen T.C., Bjerkvig R., Tysnes B.B. DNA repair and cancer stem-like cells-potential partners in glioma drug resistance?. Cancer Treat. Rev. 2008, 34:558-567.
6. Cancer Genome Atlas Research Network Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008, 455:1061-1068.
7. Parsons D.W., Jones S., Zhang X., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Siu I.M., Gallia G.L., Olivi A., McLendon R., Rasheed B.A., Keir S., Nikolskaya T., Nikolsky Y., Busam D.A., Tekleab H., Diaz L.A., Hartigan J., Smith D.R., Strausberg R.L., Marie S.K., Shinjo S.M., Yan H., Riggins G.J., Bigner D.D., Karchin R., Papadopoulos N., Parmigiani G., Vogelstein B., Velculescu V.E., Kinzler K.W. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812.
8. Inda M.M., Bonavia R., Mukasa A., Narita Y., Sah D.W., Vandenberg S., Brennan C., G Johns T., Bachoo R., Hadwiger P., Tan P., Depinho R.A., Cavenee W., Furnari F. Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev. 2010, 24:1731-1745.
9. Jin X., Yin J., Kim S.H., Sohn Y.W., Beck S., Lim Y.C., Nam D.H., Choi Y.J., Kim H. EGFR-AKT-Smad signaling promotes formation of glioma stem-like cells and tumor angiogenesis by ID3-driven cytokine induction. Cancer Res. 2011, 71:7125-7134.
10. Hasselbalch B., Eriksen J.G., Broholm H., Christensen I.J., Grunnet K., Horsman M.R., Poulsen H.S., Stockhausen M.T., Lassen U. Prospective evaluation of angiogenic, hypoxic and EGFR-related biomarkers in recurrent glioblastoma multiforme treated with cetuximab, bevacizumab and irinotecan. APMIS 2010, 118:585-594.
11. Hegi M.E., Diserens A.C., Bady P., Kamoshima Y., Kouwenhoven M.C., Delorenzi M., Lambiv W.L., Hamou M.F., Matter M.S., Koch A., Heppner F.L., Yonekawa Y., Merlo A., Frei K., Mariani L., Hofer S. Pathway analysis of glioblastoma tissue after preoperative treatment with the EGFR tyrosine kinase inhibitor gefitinib - a phase II trial. Mol. Cancer Ther. 2011, 10:1102-1112.
12. J Raizer J., Abrey L.E., Lassman A.B., M Chang S., Lamborn K.R., Kuhn J.G., Yung W.K., Gilbert M.R., Aldape K.A., Wen P.Y., Fine H.A., Mehta M., Deangelis L.M., Lieberman F., Cloughesy T.F., Robins H.I., Dancey J., Prados M.D. North American Brain Tumor Consortium, A phase II trial of erlotinib in patients with recurrent malignant gliomas and nonprogressive glioblastoma multiforme postradiation therapy. Neuro. Oncol. 2010, 12:95-103.
13. Teodorczyk M., Martin-Villalba A. Sensing invasion: cell surface receptors driving spreading of glioblastoma. J. Cell Physiol. 2010, 222:1-10.
14. Alexander S., Friedl P. Cancer invasion and resistance. interconnected processes of disease progression and therapy failure. Trends Mol. Med. 2012, 18:13-26.
15. Lu K.V., Zhu S., Cvrljevic A., Huang T.T., Sarkaria S., Ahkavan D., Dang J., Dinca E.B., Plaisier S.B., Oderberg I., Lee Y., Chen Z., Caldwell J.S., Xie Y., Loo J.A., Seligson D., Chakravari A., Lee F.Y., Weinmann R., Cloughesy T.F., Nelson S.F., Bergers G., Graeber T., Furnari F.B., James C.D., Cavenee W.K., Johns T.G., Mischel P.S. Fyn and SRC are effectors of oncogenic epidermal growth factor receptor signaling in glioblastoma patients. Cancer Res. 2009, 69:6889-6898.
16. Soeda A., Park M., Lee D., Mintz A., Androutsellis-Theotokis A., McKay R.D., Engh J., Iwama T., Kunisada T., Kassam A.B., Pollack I.F., Park D.M. Hypoxia promotes expansion of the CD133-positive glioma stemcells through activation of HIF-1alpha. Oncogene 2009, 28:3949-3959.
17. Joo K.M., Kim S.Y., Jin X., Song S.Y., Kong D.S., Lee J.I., Jeon J.W., Kim M.H., Kang B.G., Jung Y., Jin J., Hong S.C., Park W.Y., Lee D.S., Kim H., Nam D.H. Clinical and biological implication of CD133-positive and CD133-negative cells in glioblastomas. Lab. Invest. 2008, 88:808-815.
18. Miyazaki T., Pan Y., Joshi K., Purohit D., Hu B., Demir H., Mazumder S., Okabe S., Yamori T., Viapiano M., Shin-ya K., Seimiya H., Nakano I. Telomestatin impairs glioma stem cell survival and growth through the disruption of telomeric G-quadruplex and inhibition of the proto-oncogene, c-Myb. Clin. Cancer Res. 2012, 18:1268-1280.
19. Jijiwa M., Demir H., Gupta S., Leung C., Joshi K., Orozco N., Huang T., Yildiz V.O., Shibahara I., de Jesus J.A., Yong W.H., Mischel P.S., Fernandez S., Kornblum H.I., Nakano I. CD44v6 regulates growth of brain tumor stem cells partially through the AKT-mediated pathway. PLoS ONE 2011, 6:e24217.
20. Pollard S.M., Yoshikawa K., Clarke I.D., Danovi D., Stricker S., Russell R., Bayani J., Head R., Lee M., Bernstein M., Squire J.A., Smith A., Dirks P. Glioma stem cell lines expanded in adherent culture have tumor-specificphenotypesand are suitable for chemical and genetic screens. Cell Stem Cell 2009, 4:568-580.
21. Dignam J.D., Lebovitz R.M., Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 1983, 11:1475-1489.
22. Mellinghoff I.K., Wang M.Y., Vivanco I., Haas-Kogan D.A., Zhu S., Dia E.Q., Lu K.V., Yoshimoto K., Huang J.H., Chute D.J., Riggs B.L., Horvath S., Liau L.M., Cavenee W.K., Rao P.N., Beroukhim R., Peck T.C., Lee J.C., Sellers W.R., Stokoe D., Prados M., Cloughesy T.F., Sawyers C.L., Mischel P.S. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N. Engl. J. Med. 2005, 353:2012-2024.
23. Onishi M., Ichikawa T., Kurozumi K., Date I. Angiogenesis and invasion in glioma. Brain Tumor Pathol. 2011, 28:13-24.
24. Sheaff R.J., Groudine M., Gordon M., Roberts J.M., Clurman B.E. Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev. 1997, 11:1464-1478.
25. Besson A., Gurian-West M., Schmidt A., Hall A., Roberts J.M. P27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev. 2004, 18:862-876.
26. Chassot A.A., Turchi L., Virolle T., Fitsialos G., Batoz M., Deckert M., Dulic V., Meneguzzi G., Buscà R., Ponzio G. Id3 is a novel regulator of p27kip1 mRNA in early G1 phase and is required for cell-cycle progression. Oncogene 2007, 26:5772-5783.
27. Page-McCaw A., Edwald A.J., Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 2007, 8:221-233.
28. Friedl P., Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 2011, 147:992-1009.
29. Ramnarain D.B., Park S., Lee D.Y., Hatanpaa K.J., Scoggin S.O., Out H., Libermann T.A., Raisanen J.M., Ashfaq R., Wong E.T., Wu J., Elliott R., Habib A.A. Differential gene expression analysis reveals generation of an autocrine loop by a mutant epidermal growth factor receptor in glioma cells. Cancer Res. 2006, 66:867-874.
30. Heimberger A.B., Hlatky R., Suki D., Yang D., Weinberg J., Gilbert M., Sawaya R., Aldape K. Prognostic effect of epidermal growth factor receptor and EGFRvIII in glioblastoma multiforme patients. Clin. Cancer Res. 2005, 11:1462-1466.
31. Guillamo J., Boüard S., Valable S., Marteau L., Leuraud P., Marie Y., Poupon M., Parienti J., Raymond E., Peschanski M. Molecular mechanisms underlying effects of epidermal growth factor receptor inhibition on invasion, proliferation, and angiogenesis in experimental glioma. Clin. Cancer Res. 2009, 15:3697-3704.
32. Micallef J., Taccone M., Mukherjee J., Croul S., Busby J., Moran M.F., Guha A. Epidermal growth factor receptor variant III-induced glioma invasion is mediated through myristoylated alanine-rich protein kinase c substrate overexpression. Cancer Res. 2009, 69:7548-7556.
33. Niola F., Zhao X., Singh D., Castano A., Sullivan R., Lauria M., Nam H.S., Zhuang Y., Benezra R., Bernardo D.D., Iavarone A., Lasorella A. Id proteins synchronize stemness and anchorage to the niche of neural stem cells. Nature Cell Biol. 2012, 14:477-487.
34. Phillipp-Staheli J., Kim K.H., Payne S.R., Gurley K.E., Liggitt D., Longton G., Kemp C.J. Pathway-specific tumor suppression. Reduction of p27 accelerates gastrointestinal tumorigenesis in Apc mutant mice, but not in Smad3 mutant mice. Cancer Cell 2002, 1:355-368.
35. Phillipp J., Vo K., Gurley K.E., Seidel K., Kemp C.J. Tumor suppression by p27Kip1 and p21Kip1 during chemically induced skin carcinogenesis. Oncogene 1999, 18:4689-4698.
36. Kawamata N., Morosetti R., Miller C.W., Park D., Spirin K.S., Nakamaki T., Takeuchi S., Simpson J. Molecular analysis of the cyclin-dependent kinase inhibitor gene p27/Kip1 in human malignancies. Cancer Res. 1995, 55:2266-2269.
37. Denicourt C., Saenz C.C., Datnow B., Cui X.S., Dowdy S.F. Relocalized p27Kip1 tumor suppressor functions as a cytoplasmic metastatic oncogene in melanoma. Cancer Res. 2007, 67:9238-9243.
38. Larrea M.D., Wander S.A., Slingerland J.M. P27 as JekyII and Hyde: regulation of cell cycle and cell motility. Cell Cycle 2009, 8:3455-3461.
39. Rosen D.G., Yang G., Cai K.Q., Bast R.C., Gershenson D.M., Silva E.G., Liu J. Subcellular localization of p27kip1 expression predicts poor prognosis in human ovarian cancer. Clin. Cancer Res. 2005, 11:632-637.
40. Shin I., Yakes F.M., Rojo F., Shin N.Y., Bakin A.V., Baselga J., Arteaga C.L. PKB/Akt mediates cell-cycle progression by phosphorylation of p27(Kip1) at threonine 157 and modulation of its cellular localization. Nat. Med. 2002, 8:1145-1152.
41. Chintala S.K., Rao J.K. Invasion of human glioma: role of extracellular matrix proteins. Front Biosci. 1996, 1:d324-d339.
42. De Witt Hamer P.C. Small molecule kinase inhibitors in glioblastoma: a systematic review of clinical studies. Neuro. Oncol. 2010, 12:304-316.
43. Larrea M.D., Hong F., Wander S.A., da Silva T.G., Helfman D., Lannigan D., Smith J.A., Slingerland J.M. RSK1 drives p27Kip1 phosphorylation at T198 to promote RhoA inhibition and increase cell motility. Proc. Nat. Acad. Sci. USA 2009, 106:9268-9273.
44. Smith J.A., Poteet-Smith C.E., Xu Y., Errington T.M., Hecht S.M., Lannigan D.A. Identification of the first specific inhibitor of p90 ribosomal S6 kinase (RSK) reveals an unexpected role for RSK in cancer cell proliferation. Cancer Res. 2005, 65:1027-1034.