Attenuation of Krüppel-Like Factor 4 Facilitates Carcinogenesis by Inducing G1/S Phase Arrest in Clear Cell Renal Cell Carcinoma

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Song, Erlin ^a,b   Ma, Xin ^a   Li, Hongzhao ^a   Zhang, Peng ^a   Ni, Dong ^a   Chen, Weihao ^a   Gao, Yu ^a   Fan, Yang ^a   Pang, Haigang ^a   Shi, Taoping ^a   Ding, Qiang ^a   Wang, Baojun ^a   Zhang, Yu ^a   Zhang, Xu ^a  

^a CHINESE PLA GENERAL HOSPITAL   (China)

^b The 211 Hospital of PLA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1; KRUPPEL LIKE FACTOR 4; MESSENGER RNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER STAGING; CARCINOGENESIS; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY CARCINOMA; KIDNEY TUBULE CELL; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; TUMOR VOLUME; UPREGULATION;

ADULT; AGED; ANIMALS; CARCINOMA, RENAL CELL; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CPG ISLANDS; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA METHYLATION; FEMALE; G1 PHASE CELL CYCLE CHECKPOINTS; GENE SILENCING; HETEROGRAFTS; HUMANS; KIDNEY NEOPLASMS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MICE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM STAGING; PROMOTER REGIONS, GENETIC; S PHASE CELL CYCLE CHECKPOINTS; TUMOR BURDEN;

EID: 84879801109     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067758     Document Type: Article

References (59)

1. Jemal A, Bray F, (2011) Center MM, Ferlay J, Ward E, et al (2011) Global cancer statistics. CA Cancer J Clin 61: 69-90.
2. Zbar B, Klausner R, Linehan WM, (2003) Studying cancer families to identify kidney cancer genes. Annu Rev Med 54: 217-233.
3. Gossage L, Eisen T, (2010) Alterations in VHL as potential biomarkers in renal-cell carcinoma. Nat Rev Clin Oncol 7: 277-288.
4. Allory Y, Culine S, de la Taille A, (2011) Kidney cancer pathology in the new context of targeted therapy. Pathobiology 78: 90-98.
5. Dang DT, Pevsner J, Yang VW, (2000) The biology of the mammalian Kruppel-like family of transcription factors. Int J Biochem Cell Biol 32: 1103-1121.
6. Bieker JJ, (2001) Kruppel-like factors: three fingers in many pies. J Biol Chem 276: 34355-34358.
7. Ghaleb AM, Nandan MO, Chanchevalap S, Dalton WB, Hisamuddin IM, et al. (2005) Kruppel-like factors 4 and 5: the yin and yang regulators of cellular proliferation. Cell Res 15: 92-96.
8. Evans PM, Liu C, (2008) Roles of Krupel-like factor 4 in normal homeostasis, cancer and stem cells. Acta Biochim Biophys Sin (Shanghai) 40: 554-564.
9. Wei DY, Kanai M, Huang SY, Xie KP, (2006) Emerging role of KLF4 in human gastrointestinal cancer. Carcinogenesis 27: 23-31.
10. Yu F, Li J, Chen H, Fu J, Ray S, et al. (2011) Kruppel-like factor 4 (KLF4) is required for maintenance of breast cancer stem cells and for cell migration and invasion. Oncogene 30: 2161-2172.
11. Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
12. Coqueret O, (2003) New roles for p21 and p27 cell-cycle inhibitors: a function for each cell compartment? Trends Cell Biol 13: 65-70.
13. Yang WT, Zheng PS, (2012) Kruppel-like factor 4 functions as a tumor suppressor in cervical carcinoma. cancer 118: 3691-3702.
14. Wei DY, Kanai M, Jia ZL, Le XD, Xie KP, (2008) Kruppel-like factor 4 induces p27Kip1 expression in and suppresses the growth and metastasis of human pancreatic cancer cells. Cancer Research 68: 4631-4639.
15. Shie JL, Chen ZY, Fu M, Pestell RG, Tseng CC, (2000) Gut-enriched Kruppel-like factor represses cyclin D1 promoter activity through Sp1 motif. Nucleic Acids Res 28: 2969-2976.
16. Yoon HS, Yang VW, (2004) Requirement of Kruppel-like factor 4 in preventing entry into mitosis following DNA damage. J Biol Chem 279: 5035-5041.
17. Zhao WD, Hisamuddin IM, Nandan MO, Babbin BA, Lamb NE, et al. (2004) Identification of Kruppel-like factor 4 as a potential tumor suppressor gene in colorectal cancer. Oncogene 23: 395-402.
18. Wang J, Place RF, Huang V, Wang XL, Noonan EJ, et al. (2010) Prognostic Value and Function of KLF4 in Prostate Cancer: RNAa and Vector-Mediated Overexpression Identify KLF4 as an Inhibitor of Tumor Cell Growth and Migration. Cancer Research 70: 10182-10191.
19. Li Q, Gao Y, Jia Z, Mishra L, Guo K, et al. (2012) Dysregulated Kruppel-like factor 4 and vitamin D receptor signaling contribute to progression of hepatocellular carcinoma. Gastroenterology 143: 799-810 e791-792.
20. Kanai M, Wei DY, Li Q, Jia ZL, Ajani J, et al. (2006) Loss of Kruppel-like factor 4 expression contributes to Sp1 overexpression and human gastric cancer development and progression. Clinical Cancer Research 12: 6395-6402.
21. Ghaleb AM, McConnell BB, Nandan MO, Katz JP, Kaestner KH, et al. (2007) Haploinsufficiency of Kruppel-like factor 4 promotes adenomatous polyposis coli-dependent intestinal tumorigenesis. Cancer Research 67: 7147-7154.
22. Hu WX, Hofstetter WL, Li H, Zhou YB, He Y, et al. (2009) Putative Tumor-Suppressive Function of Kruppel-Like Factor 4 in Primary Lung Carcinoma. Clinical Cancer Research 15: 5688-5695.
23. Foster KW, Frost AR, McKie-Bell P, Lin CY, Engler JA, et al. (2000) Increase of GKLF messenger RNA and protein expression during progression of breast cancer. Cancer Res 60: 6488-6495.
24. Chen YJ, Wu CY, Chang CC, Ma CJ, Li MC, et al. (2008) Nuclear Kruppel-like factor 4 expression is associated with human skin squamous cell carcinoma progression and metastasis. Cancer Biol Ther 7: 777-782.
25. Tai SK, Yang MH, Chang SY, Chang YC, Li WY, et al. (2011) Persistent Kruppel-like factor 4 expression predicts progression and poor prognosis of head and neck squamous cell carcinoma. Cancer Science 102: 895-902.
26. Patel NV, Ghaleb AM, Nandan MO, Yang VW, (2010) Expression of the Tumor Suppressor Kruppel-Like Factor 4 as a Prognostic Predictor for Colon Cancer. Cancer Epidemiology Biomarkers & Prevention 19: 2631-2638.
27. Pandya AY, Talley LI, Frost AR, Fitzgerald TJ, Trivedi V, et al. (2004) Nuclear localization of KLF4 is associated with an aggressive phenotype in early-stage breast cancer. Clinical Cancer Research 10: 2709-2719.
28. Foster KW, Liu ZL, Nail CD, Li XN, Fitzgerald TJ, et al. (2005) Induction of KLF4 in basal keratinocytes blocks the proliferation- differentiation switch and initiates squamous epithelial dysplasia. Oncogene 24: 1491-1500.
29. Li J, Zheng H, Yu F, Yu T, Liu C, et al. (2012) Deficiency of the Kruppel-like factor KLF4 correlates with increased cell proliferation and enhanced skin tumorigenesis. Carcinogenesis 33: 1239-1246.
30. Wei DY, Gong WD, Kanai M, Schlunk C, Wang LW, et al. (2005) Drastic down-regulation of Kruppel-like factor 4 expression is critical in human gastric cancer development and progression. Cancer Research 65: 2746-2754.
31. Chen X, Johns DC, Geiman DE, Marban E, Dang DT, et al. (2001) Kruppel-like factor 4 (gut-enriched Kruppel-like factor) inhibits cell proliferation by blocking G1/S progression of the cell cycle. J Biol Chem 276: 30423-30428.
32. Zhang W, Geiman DE, Shields JM, Dang DT, Mahatan CS, et al. (2000) The gut-enriched Kruppel-like factor (Kruppel-like factor 4) mediates the transactivating effect of p53 on the p21WAF1/Cip1 promoter. J Biol Chem 275: 18391-18398.
33. Ai Q, Ma X, Huang Q, Liu S, Shi T, et al. (2012) High-level expression of Notch1 increased the risk of metastasis in T1 stage clear cell renal cell carcinoma. PLoS One 7: e35022.
34. Wang J, Wang Q, Cui Y, Liu ZY, Zhao W, et al. (2012) Knockdown of cyclin D1 inhibits proliferation, induces apoptosis, and attenuates the invasive capacity of human glioblastoma cells. J Neurooncol 106: 473-484.
35. Liu S, Ma X, Ai Q, Huang Q, Shi T, et al. (2011) NOTCH1 functions as an oncogene by regulating the PTEN/PI3K/AKT pathway in clear cell renal cell carcinoma. Urol Oncol: [Epub ahead of print].
36. Wei S, Xiong M, Zhan DQ, Liang BY, Wang YY, et al. (2012) Ku80 functions as a tumor suppressor in hepatocellular carcinoma by inducing S-phase arrest through a p53-dependent pathway. Carcinogenesis 33: 538-547.
37. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB, (1996) Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci U S A 93: 9821-9826.
38. Yuen JS, Akkaya E, Wang Y, Takiguchi M, Peak S, et al. (2009) Validation of the type 1 insulin-like growth factor receptor as a therapeutic target in renal cancer. Mol Cancer Ther 8: 1448-1459.
39. Villarreal G Jr, Zhang Y, Larman HB, Gracia-Sancho J, Koo A, et al. (2010) Defining the regulation of KLF4 expression and its downstream transcriptional targets in vascular endothelial cells. Biochem Biophys Res Commun 391: 984-989.
40. Wei D, Wang L, Kanai M, Jia Z, Le X, et al. (2010) KLF4alpha up-regulation promotes cell cycle progression and reduces survival time of patients with pancreatic cancer. Gastroenterology 139: 2135-2145.
41. Leng Z, Tao K, Xia Q, Tan J, Yue Z, et al. (2013) Kruppel-like factor 4 acts as an oncogene in colon cancer stem cell-enriched spheroid cells. PLoS One 8: e56082.
42. Le Magnen C, Bubendorf L, Ruiz C, Zlobec I, Bachmann A, et al. (2013) Klf4 transcription factor is expressed in the cytoplasm of prostate cancer cells. Eur J Cancer 49: 955-963.
43. Miura K, Suzuki K, Tokino T, Isomura M, Inazawa J, et al. (1996) Detailed deletion mapping in squamous cell carcinomas of the esophagus narrows a region containing a putative tumor suppressor gene to about 200 kilobases on distal chromosome 9q. Cancer Res 56: 1629-1634.
44. Roth MJ, Hu N, Emmert-Buck MR, Wang QH, Dawsey SM, et al. (2001) Genetic progression and heterogeneity associated with the development of esophageal squamous cell carcinoma. Cancer Res 61: 4098-4104.
45. Rowland BD, Peeper DS, (2006) KLF4, p21 and context-dependent opposing forces in cancer. Nature Reviews Cancer 6: 11-23.
46. Baldin V, Lukas J, Marcote MJ, Pagano M, Draetta G, (1993) Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev 7: 812-821.
47. Dulic V, Kaufmann WK, Wilson SJ, Tlsty TD, Lees E, et al. (1994) p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76: 1013-1023.
48. Jiang H, Lin J, Su ZZ, Collart FR, Huberman E, et al. (1994) Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p53. Oncogene 9: 3397-3406.
49. Macleod KF, Sherry N, Hannon G, Beach D, Tokino T, et al. (1995) p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev 9: 935-944.
50. Rowland BD, Bernards R, Peeper DS, (2005) The KLF4 tumour suppressor is a transcriptional repressor of p53 that acts as a context-dependent oncogene. Nat Cell Biol 7: 1074-1082.
51. Coppin C, Kollmannsberger C, Le L, Porzsolt F, Wilt TJ, (2011) Targeted therapy for advanced renal cell cancer (RCC): a Cochrane systematic review of published randomised trials. BJU Int 108: 1556-1563.
52. Delahunt B, Bethwaite PB, Nacey JN, (2007) Outcome prediction for renal cell carcinoma: evaluation of prognostic factors for tumours divided according to histological subtype. Pathology 39: 459-465.
53. Park SH, Wang X, Liu R, Lam KS, Weiss RH, (2008) High throughput screening of a small molecule one-bead-one-compound combinatorial library to identify attenuators of p21 as chemotherapy sensitizers. Cancer Biol Ther 7: 2015-2022.
54. Barroca H, Castedo S, Vieira J, Teixeira M, Muller-Hocker J, (2009) Altered expression of key cell cycle regulators in renal cell carcinoma associated with Xp11.2 translocation. Pathol Res Pract 205: 466-472.
55. Weiss RH, Borowsky AD, Seligson D, Lin PY, Dillard-Telm L, et al. (2007) p21 is a prognostic marker for renal cell carcinoma: implications for novel therapeutic approaches. J Urol 177: 63-68; discussion 68-69.
56. Muriel Lopez C, Esteban E, Berros JP, Pardo P, Astudillo A, et al. (2012) Prognostic factors in patients with advanced renal cell carcinoma. Clin Genitourin Cancer 10: 262-270.
57. Lian X, Duan X, Wu X, Li C, Chen S, et al. (2012) Expression and clinical significance of von Hippel-Lindau downstream genes: Jade-1 and beta-catenin related to renal cell carcinoma. Urology 80: 485 e487-413.
58. Yori JL, Johnson E, Zhou G, Jain MK, Keri RA, (2010) Kruppel-like factor 4 inhibits epithelial-to-mesenchymal transition through regulation of E-cadherin gene expression. J Biol Chem 285: 16854-16863.
59. Lin ZS, Chu HC, Yen YC, Lewis BC, Chen YW, (2012) Kruppel-like factor 4, a tumor suppressor in hepatocellular carcinoma cells reverts epithelial mesenchymal transition by suppressing slug expression. PLoS One 7: e43593.