Impairing squamous differentiation by Klf4 deletion is sufficient to initiate tongue carcinoma development upon K-Ras activation in mice

Carcinogenesis

Volumn 35, Issue 3, 2014, Pages 662-669

  Abrigo, Marianela ^a   Alvarez, Romina ^a   Paparella, María L ^b   Calb, Diego E ^a   Joffe, Elisa Bal de Kier ^a   Silvio Gutkind, J ^c   Raimondi, Ana R ^a  

^a Instituto de Oncologia Angel H Roffo   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLINE; CYTOKERATIN 1; CYTOKERATIN 6; GENOMIC DNA; KRUPPEL LIKE FACTOR 4; PROTEIN P21; PROTEIN P27; SUNFLOWER OIL; TAMOXIFEN;

ACANTHOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; BASEMENT MEMBRANE; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DYSKERATOSIS; EPITHELIUM CELL; GENE DELETION; GENE EXPRESSION; HISTOLOGY; HYPERKERATOSIS; HYPERPLASIA; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INVASIVE CARCINOMA; KERATINOCYTE; LABELING INDEX; MOUSE; NONHUMAN; ONCOGENE K RAS; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; SQUAMOUS CELL CARCINOMA; SQUAMOUS EPITHELIUM; TONGUE; TONGUE CARCINOMA; TONGUE HYPERPLASIA; VERRUCOUS CARCINOMA; WILD TYPE;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL DIFFERENTIATION; GENE DELETION; GENES, CDC; GENES, RAS; HOMEOSTASIS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; PHENOTYPE; TONGUE NEOPLASMS;

EID: 84895798175     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgt349     Document Type: Article

References (43)

1. Leemans,C.R. et al. (2011) The molecular biology of head and neck cancer. Nat. Rev. Cancer, 11, 9-22.
2. Massano,J. et al. (2006) Oral squamous cell carcinoma: review of prognostic and predictive factors. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod., 102, 67-76.
3. Rothenberg,S.M. et al. (2012) The molecular pathogenesis of head and neck squamous cell carcinoma. J. Clin. Invest., 122, 1951-1957.
4. Molinolo,A.A. et al. (2009) Dysregulated molecular networks in head and neck carcinogenesis. Oral Oncol., 45, 324-334.
5. Stransky,N. et al. (2011) The mutational landscape of head and neck squamous cell carcinoma. Science, 333, 1157-1160.
6. Agrawal,N. et al. (2011) Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science, 333, 1154-1157.
7. Guruharsha,K.G. et al. (2012) The Notch signalling system: recent insights into the complexity of a conserved pathway. Nat. Rev. Genet., 13, 654-666.
8. Roozen,P.P. et al. (2012) Differential requirements for Wnt and Notch signaling in hematopoietic versus thymic niches. Ann. N. Y. Acad. Sci., 1266, 78-93.
9. Puente,X.S. et al. (2011) Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia. Nature, 475, 101-105.
10. Lee,S.Y. et al. (2009) Gain-of-function mutations and copy number increases of Notch2 in diffuse large B-cell lymphoma. Cancer Sci., 100, 920-926.
11. Nicolas,M. et al. (2003) Notch1 functions as a tumor suppressor in mouse skin. Nat. Genet., 33, 416-421.
12. Dotto,G.P. (2008) Notch tumor suppressor function. Oncogene, 27, 5115-5123.
13. Black,A.R. et al. (2001) Sp1 and kruppel-like factor family of transcription factors in cell growth regulation and cancer. J. Cell. Physiol., 188, 143-160.
14. Evans,P.M. et al. (2008) Roles of Krupel-like factor 4 in normal homeostasis, cancer and stem cells. Acta Biochim. Biophys. Sin. (Shanghai)., 40, 554-564.
15. Schuh,R. et al. (1986) A conserved family of nuclear proteins containing structural elements of the finger protein encoded by Kruppel, a Drosophila segmentation gene. Cell, 47, 1025-1032.
16. Shields,J.M. et al. (1996) Identification and characterization of a gene encoding a gut-enriched Kruppel-like factor expressed during growth arrest. J. Biol. Chem., 271, 20009-20017.
17. Garrett-Sinha,L.A. et al. (1996) A gene for a novel zinc-finger protein expressed in differentiated epithelial cells and transiently in certain mesenchymal cells. J. Biol. Chem., 271, 31384-31390.
18. Segre,J.A. et al. (1999) Klf4 is a transcription factor required for establishing the barrier function of the skin. Nat. Genet., 22, 356-360.
19. Takahashi,K. et al. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126, 663-676.
20. Segre,J.A. (2006) Epidermal barrier formation and recovery in skin disorders. J. Clin. Invest., 116, 1150-1158.
21. Rowland,B.D. et al. (2006) KLF4, p21 and context-dependent opposing forces in cancer. Nat. Rev. Cancer, 6, 11-23.
22. Chen,X. et al. (2003) Transcriptional profiling of Kruppel-like factor 4 reveals a function in cell cycle regulation and epithelial differentiation. J. Mol. Biol., 326, 665-677.
23. Patel,S. et al. (2003) Mouse Sprr locus: a tandem array of coordinately regulated genes. Mamm. Genome, 14, 140-148.
24. Raimondi,A.R. et al. (2009) Rapamycin prevents early onset of tumorigenesis in an oral-specific K-ras and p53 two-hit carcinogenesis model. Cancer Res., 69, 4159-4166.
25. Katz,J.P. et al. (2002) The zinc-finger transcription factor Klf4 is required for terminal differentiation of goblet cells in the colon. Development, 129, 2619-2628.
26. Raimondi,A.R. et al. (2006) Rapid development of salivary gland carcinomas upon conditional expression of K-ras driven by the cytokeratin 5 promoter. Am. J. Pathol., 168, 1654-1665.
27. Tang,X.H. et al. (2004) Oral cavity and esophageal carcinogenesis modeled in carcinogen-treated mice. Clin. Cancer Res., 10(1 Pt 1), 301-313.
28. Rothnagel,J.A. et al. (1999) The mouse keratin 6 isoforms are differentially expressed in the hair follicle, footpad, tongue and activated epidermis. Differentiation., 65, 119-130.
29. Choi,W.J. et al. (2011) The role of KLF4 in UVB-induced murine skin tumor development and its correlation with cyclin D1, p53, and p21(Waf1/ Cip1) in epithelial tumors of the human skin. Arch. Dermatol. Res., 303, 191-200.
30. Shie,J.L. et al. (2000) Role of gut-enriched Kruppel-like factor in colonic cell growth and differentiation. Am. J. Physiol. Gastrointest. Liver Physiol., 279, G806-G814.
31. Wei,D. et al. (2008) Kruppel-like factor 4 induces p27Kip1 expression in and suppresses the growth and metastasis of human pancreatic cancer cells. Cancer Res., 68, 4631-4639.
32. Roop,D.R. et al. (1988) Transcriptional control of high molecular weight keratin gene expression in multistage mouse skin carcinogenesis. Cancer Res., 48, 3245-3252.
33. Tetreault,M.P. et al. (2010) Esophageal squamous cell dysplasia and delayed differentiation with deletion of kruppel-like factor 4 in murine esophagus. Gastroenterology, 139, 171-81.e9.
34. Bureau,C. et al. (2009) Expression and function of Kruppel like-factors (KLF) in carcinogenesis. Curr. Genomics, 10, 353-360.
35. Foster,K.W. et al. (2005) Induction of KLF4 in basal keratinocytes blocks the proliferation-differentiation switch and initiates squamous epithelial dysplasia. Oncogene, 24, 1491-1500.
36. Rowland,B.D. et al. (2005) The KLF4 tumour suppressor is a transcriptional repressor of p53 that acts as a context-dependent oncogene. Nat. Cell Biol., 7, 1074-1082.
37. Foster,K.W. et al. (1999) Oncogene expression cloning by retroviral transduction of adenovirus E1A-immortalized rat kidney RK3E cells: transformation of a host with epithelial features by c-MYC and the zinc finger protein GKLF. Cell Growth Differ., 10, 423-434.
38. Katz,J.P. et al. (2005) Loss of Klf4 in mice causes altered proliferation and differentiation and precancerous changes in the adult stomach. Gastroenterology, 128, 935-945.
39. Zhang,W. 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.
40. Chen,X. 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.
41. Brakenhoff,R.H. (2011) Cancer. Another NOTCH for cancer. Science, 333, 1102-1103.
42. Yang,W.T. et al. (2012) Kruppel-like factor 4 functions as a tumor suppressor in cervical carcinoma. Cancer, 118, 3691-3702.
43. Vitale-Cross,L. et al. (2009) Chemical carcinogenesis models for evaluating molecular-targeted prevention and treatment of oral cancer. Cancer Prev. Res. (Phila)., 2, 419-422.