Krüppel-like family of transcription factor 9, a differentiation- associated transcription factor, suppresses Notch1 signaling and inhibits glioblastoma-initiating stem cells

Stem Cells

Volumn 29, Issue 1, 2011, Pages 20-31

  Ying, Mingyao ^a,b   Sang, Yingying ^a   Li, Yunqing ^a,b   Guerrero Cazares, Hugo ^b   Quinones Hinojosa, Alfredo ^b   Vescovi, Angelo L ^c   Eberhart, Charles G ^b   Xia, Shuli ^a,b   Laterra, John ^a,b  

^a KENNEDY KRIEGER INSTITUTE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Cancer stem cell; Differentiation; Notch signaling; Retinoic acid; Transcription factor

Indexed keywords

KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 9; NOTCH1 RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER STEM CELL; CONTROLLED STUDY; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BINDING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR XENOGRAFT;

BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL LINE; GENES, TUMOR SUPPRESSOR; GENETIC VECTORS; GLIOBLASTOMA; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; NEOPLASTIC STEM CELLS; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; TRANSDUCTION, GENETIC; TRANSFECTION;

EID: 79951836097     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.561     Document Type: Article

References (67)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70. (Pubitemid 30046295)
2. Park CH, Bergsagel DE, McCulloch EA. Mouse myeloma tumor stem cells: A primary cell culture assay. J Natl Cancer Inst 1971;46:411-422.
3. Reya T, Morrison SJ, Clarke MF et al. Stem cells, cancer, and cancer stem cells. Nature 2001;414:105-111. (Pubitemid 33041634)
4. Lobo NA, Shimono Y, Qian D et al. The biology of cancer stem cells. Annu Rev Cell Dev Biol 2007;23:675-699.
5. Ward RJ, Dirks PB. Cancer stem cells: At the headwaters of tumor development. Annu Rev Pathol 2007;2:175-189. (Pubitemid 46448063)
6. Singh SK, Hawkins C, Clarke ID et al. Identification of human brain tumour initiating cells. Nature 2004;432:396-401. (Pubitemid 39551674)
7. Lee J, Kotliarova S, Kotliarov Y et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 2006;9:391-403. (Pubitemid 43668737)
8. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat Rev Cancer 2008;8:755-768.
9. Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nat Rev Cancer 2006;6:425-436.
10. Stiles CD, Rowitch DH. Glioma stem cells: A midterm exam. Neuron 2008;58:832-846. (Pubitemid 351842757)
11. Bao S, Wu Q, McLendon RE et al. Glioma stem cells promote radio-resistance by preferential activation of the DNA damage response. Nature 2006;444:756-760. (Pubitemid 44949604)
12. Al-Hajj M, Wicha MS, Benito-Hernandez A et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003;100:3983-3988. (Pubitemid 36418143)
13. Bao S, Wu Q, Sathornsumetee S et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 2006;66:7843-7848. (Pubitemid 44299144)
14. Galli R, Binda E, Orfanelli U et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004;64:7011-7021. (Pubitemid 39331011)
15. Hemmati HD, Nakano I, Lazareff JA et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 2003;100:15178-15183. (Pubitemid 37518036)
16. Park IK, Qian D, Kiel M et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003;423:302-305. (Pubitemid 40852701)
17. Lessard J, Sauvageau G. BMI-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003;423:255-260. (Pubitemid 40852690)
18. Panchision DM, McKay RD. The control of neural stem cells by morphogenic signals. Curr Opin Genet Dev 2002;12:478-487.
19. Piccirillo SG, Reynolds BA, Zanetti N et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006;444:761-765. (Pubitemid 44949605)
20. Androutsellis-Theotokis A, Leker RR, Soldner F et al. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 2006;442:823-826. (Pubitemid 44258913)
21. Fan X, Khaki L, Zhu TS et al. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 2010;28:5-16.
22. Heo JS, Lee MY, Han HJ. Sonic hedgehog stimulates mouse embryonic stem cell proliferation by cooperation of Ca2+/protein kinase C and epidermal growth factor receptor as well as Gli1 activation. Stem Cells 2007;25:3069-3080.
23. Bar EE, Chaudhry A, Lin A et al. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 2007;25:2524-2533. (Pubitemid 47582744)
24. Abdouh M, Facchino S, Chatoo W et al. BMI1 sustains human glioblastoma multiforme stem cell renewal. J Neurosci 2009;29:8884-8896.
25. Boyer LA, Lee TI, Cole MF et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005;122:947-956. (Pubitemid 41345211)
26. Wang J, Rao S, Chu J et al. A protein interaction network for pluripotency of embryonic stem cells. Nature 2006;444:364-368. (Pubitemid 44764111)
27. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676. (Pubitemid 44233629)
28. Wernig M, Meissner A, Foreman R et al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 2007;448:318-324.
29. Gangemi RM, Griffero F, Marubbi D et al. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells 2009;27:40-48.
30. Kaczynski J, Cook T, Urrutia R. Sp1- and Kruppel-like transcription factors. Genome Biol 2003;4:206.1-206.8.
31. Pearson R, Fleetwood J, Eaton S et al. Kruppel-like transcription factors: A functional family. Int J Biochem Cell Biol 2008;40:1996-2001. (Pubitemid 352004270)
32. Simmen RC, Pabona JM, Velarde MC et al. The emerging role of Kruppel-like factors in endocrine-responsive cancers of female reproductive tissues. J Endocrinol 2010;204:223-231.
33. Jiang J, Chan YS, Loh YH et al. A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat Cell Biol 2008;10:353-360. (Pubitemid 351331023)
34. Rowland BD, Bernards R, Peeper DS. The KLF4 tumour suppressor is a transcriptional repressor of p53 that acts as a context-dependent oncogene. Nat Cell Biol 2005;7:1074-1082.
35. Zhang W, Geiman DE, Shields JM et al. The gut-enriched Kruppel-like factor (Kruppel-like factor 4) mediates the transactivating effect of p53 on the p21WAF1/Cip1 promoter. J Biol Chem 2000;275:18391-18398. (Pubitemid 30414796)
36. Kimmelman AC, Qiao RF, Narla G et al. Suppression of glioblastoma tumorigenicity by the Kruppel-like transcription factor KLF6. Oncogene 2004;23:5077-5083. (Pubitemid 38938741)
37. Narla G, Heath KE, Reeves HL et al. KLF6, a candidate tumor suppressor gene mutated in prostate cancer. Science 2001;294:2563-2566. (Pubitemid 34027299)
38. Kang L, Lu B, Xu J et al. Downregulation of Kruppel-like factor 9 in human colorectal cancer. Pathol Int 2008;58:334-338. (Pubitemid 351677534)
39. Simmen FA, Su Y, Xiao R et al. The Kruppel-like factor 9 (KLF9) network in HEC-1-A endometrial carcinoma cells suggests the carcinogenic potential of dys-regulated KLF9 expression. Reprod Biol Endocrinol 2008;6:41-51.
40. Lal B, Xia S, Abounader R et al. Targeting the c-Met pathway potentiates glioblastoma responses to gamma-radiation. Clin Cancer Res 2005;11:4479-4486. (Pubitemid 40825638)
41. Liu Z, Teng L, Bailey SK et al. Epithelial transformation by KLF4 requires Notch1 but not canonical Notch1 signaling. Cancer Biol Ther 2009;8:1840-1851.
42. Sun P, Xia S, Lal B et al. DNER, an epigenetically modulated gene, regulates glioblastoma-derived neurosphere cell differentiation and tumor propagation. Stem Cells 2009;27:1473-1486.
43. Pollard SM, Yoshikawa K, Clarke ID et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 2009;4:568-580.
44. Campos B, Wan F, Farhadi M et al. Differentiation therapy exerts antitumor effects on stem-like glioma cells. Clin Cancer Res 2010;16:2715-2728.
45. Laks DR, Masterman-Smith M, Visnyei K et al. Neurosphere formation is an independent predictor of clinical outcome in malignant glioma. Stem Cells 2009;27:980-987.
46. Bidlingmaier S, Zhu X, Liu B. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J Mol Med 2008;86:1025-1032.
47. Ligon KL, Huillard E, Mehta S et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 2007;53:503-517. (Pubitemid 46216748)
48. Imataka H, Sogawa K, Yasumoto K et al. Two regulatory proteins that bind to the basic transcription element (BTE), a GC box sequence in the promoter region of the rat P-4501A1 gene. EMBO J 1992;11:3663-3671.
49. Parsons DW, Jones S, Zhang X et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008;321:1807-1812.
50. Kobayashi A, Sogawa K, Imataka H et al. Analysis of functional domains of a GC box-binding protein, BTEB. J Biochem 1995;117:91-95.
51. Zhang D, Zhang XL, Michel FJ et al. Direct interaction of the Kruppel-like family (KLF) member, BTEB1, and Pr Mediates progesterone- responsive gene expression in endometrial epithelial cells. Endocrinology 2002;143:62-73.
52. Zhang XL, Zhang D, Michel FJ et al. Selective interactions of Kruppel- like factor 9/basic transcription element-binding protein with progesterone receptor isoforms A and B determine transcriptional activity of progesterone-responsive genes in endometrial epithelial cells. J Biol Chem 2003;278:21474-21482. (Pubitemid 36792544)
53. Pabona JM, VelardeMC, Zeng Z et al. Nuclear receptor co-regulator Kruppel-like factor 9 and prohibitin 2 expression in estrogen-induced epithelial cell proliferation in the mouse uterus. J Endocrinol 2009;200:63-73.
54. Velarde MC, Zeng Z, McQuown JR et al. Kruppel-like factor 9 is a negative regulator of ligand-dependent estrogen receptor alpha signaling in Ishikawa endometrial adenocarcinoma cells. Mol Endocrinol 2007;21:2988-3001. (Pubitemid 350223509)
55. Lai EC. Notch signaling: Control of cell communication and cell fate. Development 2004;131:965-973. (Pubitemid 38380451)
56. Bray SJ. Notch signalling: A simple pathway becomes complex. Nat Rev Mol Cell Biol 2006;7:678-689. (Pubitemid 44268213)
57. Dontu G, Jackson KW, McNicholas E et al. Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res 2004;6:R605-R615.
58. Farnie G, Clarke RB. Mammary stem cells and breast cancer - Role of Notch signalling. Stem Cell Rev 2007;3:169-175. (Pubitemid 350129719)
59. Fre S, Huyghe M, Mourikis P et al. Notch signals control the fate of immature progenitor cells in the intestine. Nature 2005;435:964-968. (Pubitemid 40896323)
60. van Es JH, van Gijn ME, Riccio O et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 2005;435:959-963. (Pubitemid 40896322)
61. Hitoshi S, Alexson T, Tropepe V et al. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 2002;16:846-858. (Pubitemid 34280108)
62. Nakamura Y, Sakakibara S, Miyata T et al. The bHLH gene hes1 as a repressor of the neuronal commitment of CNS stem cells. J Neurosci 2000;20:283-293. (Pubitemid 30220516)
63. Weng AP, Ferrando AA, LeeWet al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 2004;306:269-271.
64. Pece S, Serresi M, Santolini E et al. Loss of negative regulation by Numb over Notch is relevant to human breast carcinogenesis. J Cell Biol 2004;167:215-221. (Pubitemid 39435065)
65. Politi K, Feirt N, Kitajewski J. Notch in mammary gland development and breast cancer. Semin Cancer Biol 2004;14:341-347. (Pubitemid 38993635)
66. Kanamori M, Kawaguchi T, Nigro JM et al. Contribution of Notch signaling activation to human glioblastoma multiforme. J Neurosurg 2007;106:417-427. (Pubitemid 46354295)
67. Wang J, Wakeman TP, Lathia JD et al. Notch promotes radioresistance of glioma stem cells. Stem Cells 2010;28:17-28.