Nonreceptor Tyrosine Kinase BMX Maintains Self-Renewal and Tumorigenic Potential of Glioblastoma Stem Cells by Activating STAT3

Cancer Cell

Volumn 19, Issue 4, 2011, Pages 498-511

  Guryanova, Olga A ^a   Wu, Qiulian ^a   Cheng, Lin ^a,b   Lathia, Justin D ^a   Huang, Zhi ^a   Yang, Jinbo ^a   MacSwords, Jennifer ^a   Eyler, Christine E ^a,d   McLendon, Roger E ^d   Heddleston, John M ^a   Shou, Weinian ^c   Hambardzumyan, Dolores ^a   Lee, Jeongwu ^a   Hjelmeland, Anita B ^a   Sloan, Andrew E ^e   Bredel, Markus ^f   Stark, George R ^a   Rich, Jeremy N ^a   Bao, Shideng ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^f UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MARROW X LINKED PROTEIN; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CELL RENEWAL; CONTROLLED STUDY; DOWN REGULATION; GENE ACTIVATION; GENE EXPRESSION; GENE TARGETING; GLIOBLASTOMA; HISTOPATHOLOGY; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTRACRANIAL TUMOR; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR GROWTH;

EID: 79953757100     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2011.03.004     Document Type: Article

References (54)

1. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. GBM stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
2. Bao S., Wu Q., Sathornsumetee S., Hao Y., Li Z., Hjelmeland A.B., Shi Q., McLendon R.E., Bigner D.D., Rich J.N. Stem cell-like GBM cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 2006, 66:7843-7848.
3. Beier D., Hau P., Proescholdt M., Lohmeier A., Wischhusen J., Oefner P.J., Aigner L., Brawanski A., Bogdahn U., Beier C.P. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 2007, 67:4010-4015.
4. Bromberg J.F., Wrzeszczynska M.H., Devgan G., Zhao Y., Pestell R.G., Albanese C., Darnell J.E. Stat3 as an oncogene. Cell 1999, 98:295-303.
5. Bromberg J. Stat proteins and oncogenesis. J. Clin. Invest. 2002, 109:1139-1142.
6. Calabrese C., Poppleton H., Kocak M., Hogg T.L., Fuller C., Hamner B., Oh E.Y., Gaber M.W., Finklestein D., Allen M., et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007, 11:69-82.
7. Carro M.S., Lim W.K., Alvarez M.J., Bollo R.J., Zhao X., Snyder E.Y., Sulman E.P., Anne S.L., Doetsch F., Colman H., et al. The transcriptional network for mesenchymal transformation of brain tumours. Nature 2010, 463:318-325.
8. Chan K.S., Sano S., Kiguchi K., Anders J., Komazawa N., Takeda J., DiGiovanni J. Disruption of Stat3 reveals a critical role in both the initiation and the promotion stages of epithelial carcinogenesis. J. Clin. Invest. 2004, 114:720-728.
9. Chau C.H., Clavijo C.A., Deng H.T., Zhang Q., Kim K.J., Qiu Y., Le A.D., Ann D.K. Etk/Bmx mediates expression of stress-induced adaptive genes VEGF, PAI-1, and iNOS via multiple signaling cascades in different cell systems. Am. J. Physiol. Cell Physiol. 2005, 289:C444-C454.
10. Chen R., Kim O., Li M., Xiong X., Guan J.L., Kung H.J., Chen H., Shimizu Y., Qiu Y. Regulation of the PH-domain-containing tyrosine kinase Etk by focal adhesion kinase through the FERM domain. Nat. Cell Biol. 2001, 3:439-444.
11. Dai B., Kim O., Xie Y., Guo Z., Xu K., Wang B., Kong X., Melamed J., Chen H., Bieberich C.J., et al. Tyrosine kinase Etk/BMX is up-regulated in human prostate cancer and its overexpression induces prostate intraepithelial neoplasia in mouse. Cancer Res. 2006, 66:8058-8064.
12. Dasgupta A., Raychaudhuri B., Haqqi T., Prayson R., Van Meir E.G., Vogelbaum M., Haque S.J. Stat3 activation is required for the growth of U87 cell-derived tumours in mice. Eur. J. Cancer 2009, 45:677-684.
13. de la Iglesia N., Puram S.V., Bonni A. STAT3 regulation of glioblastoma pathogenesis. Curr. Mol. Med. 2009, 9:580-590.
14. Fan X., Khaki L., Zhu T.S., Soules M.E., Talsma C.E., Gul N., Koh C., Zhang J., Li Y.M., Maciaczyk J., et al. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor tumorspheres and xenografts. Stem Cells 2010, 28:5-16.
15. Frank N.Y., Schatton T., Frank M.H. The therapeutic promise of the cancer stem cell concept. J. Clin. Invest. 2010, 120:41-50.
16. Furnari F.B., Fenton T., Bachoo R.M., Mukasa A., Stommel J.M., Stegh A., Hahn W.C., Ligon K.L., Louis D.N., Brennan C., et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 2007, 21:2683-2710.
17. Gilbertson R.J., Rich J.N. Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat. Rev. Cancer 2007, 7:733-736.
18. Grivennikov S., Karin E., Terzic J., Mucida D., Yu G.Y., Vallabhapurapu S., Scheller J., Rose-John S., Cheroutre H., Eckmann L., Karin M. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009, 15:103-113.
19. Guo L., Guo Y., Xiao S. Expression of tyrosine kinase Etk/Bmx and its relationship with AP-1- and NF-kappaB-associated proteins in hepatocellular carcinoma. Oncology 2007, 72:410-416.
20. Guo L., Zhou Y., Sun Y., Zhang F. Non-receptor tyrosine kinase Etk regulation of drug resistance in small-cell lung cancer. Eur. J. Cancer 2010, 46:636-641.
21. Gupta P.B., Onder T.T., Jiang G., Tao K., Kuperwasser C., Weinberg R.A., Lander E.S. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009, 138:645-659.
22. Hambardzumyan D., Amankulor N.M., Helmy K.Y., Becher O.J., Holland E.C. Modeling adult gliomas using RCAS/t-va technology. Transl. Oncol. 2009, 2:89-95.
23. He Y., Luo Y., Tang S., Rajantie I., Salven P., Heil M., Zhang R., Luo D., Li X., Chi H., et al. Critical function of Bmx/Etk in ischemia-mediated arteriogenesis and angiogenesis. J. Clin. Invest. 2006, 116:2344-2355.
24. Jiang X., Borgesi R.A., McKnight N.C., Kaur R., Carpenter C.L., Balk S.P. Activation of nonreceptor tyrosine kinase Bmx/Etk mediated by phosphoinositide 3-kinase, epidermal growth factor receptor, and ErbB3 in prostate cancer cells. J. Biol. Chem. 2007, 282:32689-32698.
25. Lathia J.D., Gallagher J., Heddleston J.M., Wang J., Eyler C.E., MacSwords J., Wu Q., Vasanji A., McLendon R.E., Hjelmeland A.B., Rich J.N. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 2010, 6:421-432.
26. Levy D.E., Darnell J.E. Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 2002, 3:651-662.
27. Li Z., Bao S., Wu Q., Wang H., Eyler C., Sathornsumetee S., Shi Q., Cao Y., Lathia J., Mclendon R.E., et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioblastoma stem cells. Cancer Cell 2009, 15:501-513.
28. Li G.H., Wei H., Chen Z.T., Lu S.Q., Yin C.L., Wang D.L. STAT3 silencing with lentivirus inhibits growth and induces apoptosis and differentiation of U251 cells. J. Neurooncol. 2009, 91:165-174.
29. Liu G., Yuan X., Zeng Z., Tunici P., Ng H., Abdulkadir I.R., Lu L., Irvin D., Black K.L., Yu J.S. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol. Cancer 2006, 5:67.
30. Lo H.W., Cao X., Zhu H., Ali-Osman F. Constitutively activated STAT3 frequently coexpresses with epidermal growth factor receptor in high-grade gliomas and targeting STAT3 sensitizes them to Iressa and alkylators. Clin. Cancer Res. 2008, 14:6042-6054.
31. Lobo N.A., Shimono Y., Qian D., Clarke M.F. The biology of cancer stem cells. Annu. Rev. Cell Dev. Biol. 2007, 23:675-699.
32. Paavonen K., Ekman N., Wirzenius M., Rajantie I., Poutanen M., Alitalo K. Bmx tyrosine kinase transgene induces skin hyperplasia, inflammatory angiogenesis, and accelerated wound healing. Mol. Biol. Cell 2004, 15:4226-4233.
33. Pan S., An P., Zhang R., He X., Yin G., Min W. Etk/Bmx as a tumor necrosis factor receptor type 2-specific kinase: role in endothelial cell migration and angiogenesis. Mol. Cell. Biol. 2002, 22:7512-7523.
34. Park D.M., Rich J.N. Biology of glioma cancer stem cells. Mol. Cells 2009, 28:7-12.
35. Paz K., Brennan L.A., Iacolina M., Doody J., Hadari Y.R., Zhu Z. Human single-domain neutralizing intrabodies directed against Etk kinase: a novel approach to impair cellular transformation. Mol. Cancer Ther. 2005, 4:1801-1809.
36. Rahaman S.O., Harbor P.C., Chernova O., Barnett G.H., Vogelbaum M.A., Haque S.J. Inhibition of constitutively active Stat3 suppresses proliferation and induces apoptosis in glioblastoma multiforme cells. Oncogene 2002, 21:8404-8413.
37. Rajantie I., Ekman N., Iljin K., Arighi E., Gunji Y., Kaukonen J., Palotie A., Dewerchin M., Carmeliet P., Alitalo K. Bmx tyrosine kinase has a redundant function downstream of angiopoietin and vascular endothelial growth factor receptors in arterial endothelium. Mol. Cell. Biol. 2001, 21:4647-4655.
38. Rietze R.L., Reynolds B.A. Neural stem cell isolation and characterization. Methods Enzymol. 2006, 419:3-23.
39. Rosen J.M., Jordan C.T. The increasing complexity of the cancer stem cell paradigm. Science 2009, 324:1670-1673.
40. Saharinen P., Ekman N., Sarvas K., Parker P., Alitalo K., Silvennoinen O. The Bmx tyrosine kinase induces activation of the Stat signaling pathway, which is specifically inhibited by protein kinase Cdelta. Blood 1997, 90:4341-4353.
41. Sathornsumetee S., Rich J.N. Antiangiogenic therapy in malignant glioma: promise and challenge. Curr. Pharm. Des. 2007, 13:3545-3558.
42. Sherry M.M., Reeves A., Wu J.K., Cochran B.H. STAT3 is required for proliferation and maintenance of multipotency in glioblastoma stem cells. Stem Cells 2009, 27:2383-2392.
43. Smith C.I., Islam T.C., Mattsson P.T., Mohamed A.J., Nore B.F., Vihinen M. The Tec family of cytoplasmic tyrosine kinases: mammalian Btk, Bmx, Itk, Tec, Txk and homologs in other species. Bioessays 2001, 23:436-446.
44. Son M.J., Woolard K., Nam D.H., Lee J., Fine H.A. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 2009, 4:440-452.
45. Stommel J.M., Kimmelman A.C., Ying H., Nabioullin R., Ponugoti A.H., Wiedemeyer R., Stegh A.H., Bradner J.E., Ligon K.L., Brennan C., et al. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 2007, 318:287-290.
46. Tsai Y.T., Su Y.H., Fang S.S., Huang T.N., Qiu Y., Jou Y.S., Shih H.M., Kung H.J., Chen R.H. Etk, a Btk family tyrosine kinase, mediates cellular transformation by linking Src to STAT3 activation. Mol. Cell. Biol. 2000, 20:2043-2054.
47. Vescovi A.L., Galli R., Reynolds B.A. Brain tumour stem cells. Nat. Rev. Cancer 2006, 6:425-436.
48. Wang H., Lathia J.D., Wu Q., Wang J., Li Z., Heddleston J.M., Eyler C.E., Elderbroom J., Gallagher J., Schuschu J., et al. Targeting interleukin 6 signaling suppresses glioma stem cell survival and tumor growth. Stem Cells 2009, 27:2393-2404.
49. Wei J., Barr J., Kong L.Y., Wang Y., Wu A., Sharma A.K., Gumin J., Henry V., Colman H., Sawaya R., et al. Glioma-associated cancer-initiating cells induce immunosuppression. Clin. Cancer Res. 2010, 16:461-473.
50. Wen P.Y., Kesari S. Malignant gliomas in adults. N. Engl. J. Med. 2008, 359:492-507.
51. Wu Y.M., Huang C.L., Kung H.J., Huang C.H.F. Proteolytic activation of Etk/Bmx tyrosine kinase by caspases. J. Biol. Chem. 2001, 276:17672-17678.
52. Xue L.Y., Qiu Y., He J., Kung H.J., Oleinick N.L. Etk/Bmx, a PH-domain containing tyrosine kinase, protects prostate cancer cells from apoptosis induced by photodynamic therapy or thapsigargin. Oncogene 1999, 18:3391-3398.
53. Yang J., van Oosten A.L., Theunissen T.W., Guo G., Silva J.C.R., Smith A. Stat3 activation is limiting for reprogramming to ground state pluripotency. Cell Stem Cell 2010, 7:319-328.
54. Zhou B.B., Zhang H., Damelin M., Geles K.G., Grindley J.C., Dirks P.B. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat. Rev. Drug Discov. 2009, 8:806-823.