Cancer stem-like cell properties are regulated by EGFR/AKT/β-catenin signaling and preferentially inhibited by gefitinib in nasopharyngeal carcinoma

FEBS Journal

Volumn 280, Issue 9, 2013, Pages 2027-2041

  Ma, Lei ^a   Zhang, Gong ^a   Miao, Xiao Bo ^a   Deng, Xu Bin ^a   Wu, Yue ^a   Liu, Ying ^a   Jin, Zhi Ru ^a   Li, Xi Qing ^a   Liu, Qiu Zhen ^a   Sun, Du Xin ^b   Testa, Joseph R ^c   Yao, Kai Tai ^a   Xiao, Guang Hui ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF MICHIGAN   (United States)

^c FOX CHASE CANCER CENTER   (United States)

Author keywords

catenin; cancer stem like cells; EGFR; gefitinib; nasopharyngeal carcinoma

Indexed keywords

BETA CATENIN; CISPLATIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; PROTEIN KINASE B; TRANSCRIPTION FACTOR NANOG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER MODEL; CANCER PATIENT; CANCER STEM CELL; CARCINOMA CELL; CONTROLLED STUDY; ENZYME ACTIVATION; GROWTH RATE; MOUSE; NASOPHARYNX CARCINOMA; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REIMPLANTATION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; BETA CATENIN; CARCINOMA; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; CISPLATIN; GENE KNOCKDOWN TECHNIQUES; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; NASOPHARYNGEAL NEOPLASMS; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; PROTO-ONCOGENE PROTEINS C-AKT; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIDE-POPULATION CELLS; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MUS;

EID: 84876912182     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12226     Document Type: Article

References (49)

1. Normanno N, De Luca A, Bianco C, Strizzi L, Mancino M, Maiello MR, Carotenuto A, De Feo G, Caponigro F, &, Salomon DS, (2006) Epidermal growth factor receptor (EGFR) signaling in cancer. Gene (Amsterdam) 366, 2-16. (Pubitemid 43199589)
2. Mangelberger D, Kern D, Loipetzberger A, Eberl M, &, Aberger F, (2012) Cooperative Hedgehog-EGFR signaling. Front Biosci 17, 90-99.
3. Eccles SA, (2011) The epidermal growth factor receptor/Erb-B/HER family in normal and malignant breast biology. Int J Dev Biol 55, 685-696.
4. Reynolds BA, &, Weiss S, (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710.
5. Reynolds BA, Tetzlaff W, &, Weiss S, (1992) A multipotent Egf-responsive striatal embryonic progenitor-cell produces neurons and astrocytes. J Neurosci 12, 4565-4574.
6. Dumstrei K, Nassif C, Abboud G, Aryai A, Aryai A, &, Hartenstein V, (1998) EGFR signaling is required for the differentiation and maintenance of neural progenitors along the dorsal midline of the Drosophila embryonic head. Development 125, 3417-3426. (Pubitemid 28458341)
7. Maric D, Maric I, Chang YH, &, Barker JL, (2003) Prospective cell sorting of embryonic rat neural stem cells and neuronal and glial progenitors reveals selective effects of basic fibroblast growth factor and epidermal growth factor on self-renewal and differentiation. J Neurosci 23, 240-251. (Pubitemid 36050424)
8. Chen JS, Pardo FS, Wang-Rodriguez J, Chu TS, Lopez JP, Aguilera J, Altuna X, Weisman RA, &, Ongkeko WM, (2006) EGFR regulates the side population in head and neck squamous cell carcinoma. Laryngoscope 116, 401-406. (Pubitemid 44318100)
9. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CHM, Jones DL, Visvader J, Weissman IL, &, Wahl GM, (2006) Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 66, 9339-9344. (Pubitemid 44623625)
10. Garvalov BK, &, Acker T, (2011) Cancer stem cells: a new framework for the design of tumor therapies. J Mol Med (Berl) 89, 95-107.
11. Fodde R, &, Brabletz T, (2007) Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 19, 150-158. (Pubitemid 46386404)
12. He XC, Yin T, Grindley JC, Tian Q, Sato T, Tao WA, Dirisina R, Porter-Westpfahl KS, Hembree M, Johnson T, et al,. (2007) PTEN-deficient intestinal stem cells initiate intestinal polyposis. Nat Genet 39, 189-198. (Pubitemid 46184349)
13. Lee G, Goretsky T, Managlia E, Dirisina R, Singh AP, Brown JB, May R, Yang GY, Ragheb JW, Evers BM, et al,. (2010) Phosphoinositide 3-kinase signaling mediates beta-catenin activation in intestinal epithelial stem and progenitor cells in colitis. Gastroenterology 139, 869-881, 881 e1-9.
14. Korkaya H, Paulson A, Charafe-Jauffret E, Ginestier C, Brown M, Dutcher J, Clouthier SG, &, Wicha MS, (2009) Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol 7, 1-14.
15. Yost C, Torres M, Miller RR, Huang E, Kimelman D, &, Moon RT, (1996) The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev 10, 1443-1454. (Pubitemid 26260702)
16. Yu MC, &, Yuan JM, (2002) Epidemiology of nasopharyngeal carcinoma. Semin Cancer Biol 12, 421-429. (Pubitemid 35370755)
17. Chen WZ, Zhou DL, &, Luo KS, (1989) Long-term observation after radiotherapy for nasopharyngeal carcinoma (Npc). Int J Radiat Oncol Biol Phys 16, 311-314.
18. Wei WI, &, Kwong DL, (2010) Current management strategy of nasopharyngeal carcinoma. Clin Exp Otorhinolaryngol 3, 1-12.
19. Wang J, Guo UP, Chen LZ, Zeng YX, &, Lu SH, (2007) Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line. Cancer Res 67, 3716-3724. (Pubitemid 46762157)
20. Liang Y, Zhong Z, Huang Y, Deng W, Cao J, Tsao G, Liu Q, Pei D, Kang T, &, Zeng YX, (2010) Stem-like cancer cells are inducible by increasing genomic instability in cancer cells. J Biol Chem 285, 4931-4940.
21. Xia H, Cheung WK, Sze J, Lu G, Jiang S, Yao H, Bian XW, Poon WS, Kung HF, &, Lin MC, (2010) miR-200a regulates epithelial-mesenchymal to stem-like transition via ZEB2 and beta-catenin signaling. J Biol Chem 285, 36995-37004.
22. Ratushny V, Astsaturov I, Burtness BA, Golemis EA, &, Silverman JS, (2009) Targeting EGFR resistance networks in head and neck cancer. Cell Signal 21, 1255-1268.
23. Ma BBT, Poon TCW, To KF, Zee B, Mo FKF, Chan CML, Ho S, Teo PML, Johnson PJ, &, Chan ATC, (2003) Prognostic significance of tumor angiogenesis, Ki 67, p53 oncoprotein, epidermal growth factor receptor and HER2 receptor protein expression in undifferentiated nasopharyngeal carcinoma-a prospective study. Head Neck 25, 864-872. (Pubitemid 37139899)
24. Sizhong Z, Xiukung G, &, Yi Z, (1983) Cytogenetic studies on an epithelial cell line derived from poorly differentiated nasopharyngeal carcinoma. Int J Cancer 31, 587-590. (Pubitemid 13058335)
25. Golebiewska A, Brons NH, Bjerkvig R, &, Niclou SP, (2011) Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell 8, 136-147.
26. Challen GA, &, Little MH, (2006) A side order of stem cells: the SP phenotype. Stem Cells 24, 3-12.
27. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, Osawa M, Nakauchi H, et al,. (2001) The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 7, 1028-1034. (Pubitemid 32937383)
28. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, &, Wicha MS, (2003) In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 17, 1253-1270. (Pubitemid 36583168)
29. Bellacosa A, Kumar CC, Di Cristofano A, &, Testa JR, (2005) Activation of AKT kinases in cancer: implications for therapeutic targeting. Adv Cancer Res 94, 29-86. (Pubitemid 41202364)
30. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, &, Kinzler KW, (1998) Identification of c-MYC as a target of the APC pathway. Science 281, 1509-1512. (Pubitemid 28425575)
31. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, &, Yamanaka S, (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872. (Pubitemid 350138099)
32. Takao Y, Yokota T, &, Koide H, (2007) Beta-catenin up-regulates Nanog expression through interaction with Oct-3/4 in embryonic stem cells. Biochem Biophys Res Commun 353, 699-705. (Pubitemid 46048726)
33. Li Y, Zhang T, Korkaya H, Liu S, Lee HF, Newman B, Yu Y, Clouthier SG, Schwartz SJ, Wicha MS, et al,. (2010) Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin Cancer Res 16, 2580-2590.
34. Yanase K, Tsukahara S, Asada S, Ishikawa E, Imai Y, &, Sugimoto Y, (2004) Gefitinib reverses breast cancer resistance protein-mediated drug resistance. Mol Cancer Ther 3, 1119-1125. (Pubitemid 39295009)
35. Leggas M, Panetta JC, Zhuang Y, Schuetz JD, Johnston B, Bai F, Sorrentino B, Zhou S, Houghton PJ, &, Stewart CF, (2006) Gefitinib modulates the function of multiple ATP-binding cassette transporters in vivo. Cancer Res 66, 4802-4807.
36. Herbst RS, Fukuoka M, &, Baselga J, (2004) Gefitinib-a novel targeted approach to treating cancer. Nat Rev Cancer 4, 956-965. (Pubitemid 39626219)
37. Maemondo M, Inoue A, Kobayashi K, Sugawara S, Oizumi S, Isobe H, Gemma A, Harada M, Yoshizawa H, Kinoshita I, et al,. (2010) Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med 362, 2380-2388.
38. Mitsudomi T, Morita S, Yatabe Y, Negoro S, Okamoto I, Tsurutani J, Seto T, Satouchi M, Tada H, Hirashima T, et al,. (2010) Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol 11, 121-128.
39. Tiseo M, Bartolotti M, Gelsomino F, &, Bordi P, (2010) Emerging role of gefitinib in the treatment of non-small-cell lung cancer (NSCLC). Drug Des Devel Ther 4, 81-98.
40. Ma B, Hui EP, King A, To KF, Mo F, Leung SF, Kam M, Lo YM, Zee B, Mok T, et al,. (2008) A phase II study of patients with metastatic or locoregionally recurrent nasopharyngeal carcinoma and evaluation of plasma Epstein-Barr virus DNA as a biomarker of efficacy. Cancer Chemother Pharmacol 62, 59-64. (Pubitemid 351537846)
41. Ma BB, Kam MK, Leung SF, Hui EP, King AD, Chan SL, Mo F, Loong H, Yu BK, Ahuja A, et al,. (2011) A phase II study of concurrent cetuximab-cisplatin and intensity-modulated radiotherapy in locoregionally advanced nasopharyngeal carcinoma. Ann Oncol 23, 1287-1292.
42. Nguyen KS, Kobayashi S, &, Costa DB, (2009) Acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancers dependent on the epidermal growth factor receptor pathway. Clin Lung Cancer 10, 281-289.
43. Wheeler DL, Dunn EF, &, Harari PM, (2010) Understanding resistance to EGFR inhibitors-impact on future treatment strategies. Nat Rev Clin Oncol 7, 493-507.
44. Aguirre A, Rubio ME, &, Gallo V, (2010) Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 467, 323-327.
45. Peignon G, Durand A, Cacheux W, Ayrault O, Terris B, Laurent-Puig P, Shroyer NF, Van Seuningen I, Honjo T, Perret C, et al,. (2011) Complex interplay between beta-catenin signalling and Notch effectors in intestinal tumorigenesis. Gut 60, 166-176.
46. Yu S, Zhang R, Liu F, Wang H, Wu J, &, Wang Y, (2012) Notch inhibition suppresses nasopharyngeal carcinoma by depleting cancer stem-like side population cells. Oncol Rep 28, 561-566.
47. Altomare DA, You H, Xiao GH, Ramos-Nino ME, Skele KL, De Rienzo A, Jhanwar SC, Mossman BT, Kane AB, &, Testa JR, (2005) Human and mouse mesotheliomas exhibit elevated AKT/PKB activity, which can be targeted pharmacologically to inhibit tumor cell growth. Oncogene 24, 6080-6089. (Pubitemid 43080058)
48. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, &, Weinberg RA, (2008) Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 68, 3645-3654.
49. Wiznerowicz M, &, Trono D, (2003) Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J Virol 77, 8957-8961. (Pubitemid 36936105)