Potential involvement of miR-375 in the premalignant progression of oral squamous cell carcinoma mediated via transcription factor KLF5

Oncotarget

Volumn 6, Issue 37, 2015, Pages 40172-40185

  Shi, Wen ^a,b   Yang, Jing ^b   Li, Siyuan ^a   Shan, Xiaofeng ^a   Liu, Xiaosong ^a   Hua, Hong ^a   Zhao, Chuanke ^b   Feng, Zhendong ^b   Cai, Zhigang ^a   Zhang, Lihe ^b   Zhou, Demin ^b  

^a PEKING UNIVERSITY SCHOOL AND HOSPITAL OF STOMATOLOGY   (China)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

KLF5; Malignant progression; miR 375; OLP; OSCC

Indexed keywords

BIOLOGICAL MARKER; KRUPPEL LIKE FACTOR 5; MICRORNA 375; SURVIVIN; 3' UNTRANSLATED REGION; BIRC5 PROTEIN, HUMAN; INHIBITOR OF APOPTOSIS PROTEIN; KLF5 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; MICRORNA; MIRN375 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; BINDING AFFINITY; CANCER GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE MARKER; DOWN REGULATION; EPITHELIUM CELL; GENE CONTROL; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE TARGETING; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; LICHEN PLANUS; MOUTH SQUAMOUS CELL CARCINOMA; PRECANCER; PROTEIN TARGETING; UPREGULATION; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HIGH THROUGHPUT SEQUENCING; METABOLISM; MOUTH TUMOR; PATHOLOGY; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE; WESTERN BLOTTING;

3' UNTRANSLATED REGIONS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE PROGRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LICHEN PLANUS, ORAL; MICRORNAS; MOUTH NEOPLASMS; PRECANCEROUS CONDITIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84950153717     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5502     Document Type: Article

References (64)

1. Warnakulasuriya S. Global epidemiology of oral and oropharyngeal cancer. Oral Oncol. 2009; 45:309-316.
2. Siegel RL, Miller KD, Jemal A. Cancer statistics!. CA: A Cancer Journal for Clinicians.2015; 65:5-29.
3. Scully C, Carrozzo M. Oral mucosal disease: Lichen planus. British Journal of Oral and Maxillofacial Surgery. 2008; 46:15-21.
4. Lee JJ HW, Hittelman WN, Mao L, Lotan R, Shin DM, Benner SE, Xu XC, Lee JS, Papadimitrakopoulou VM, Geyer C, Perez C, Martin JW, El-Naggar AK, Lippman SM. Predicting cancer development in oral leukoplakia: 10 years of translational research. Clin Cancer Res. 2000; 6:1702-1710.
5. Warnakulasuriya S JN, van der Waal I. Nomenclature and classification of potentially malignant disorders of the oral mucosa. J Oral Pathol Med. 2007; 36:575-580.
6. A Z. An updated overview of HPV-associated head and neck carcinomas. Oncotarget. 2014; 5:3956-3969.
7. Grivennikov SI GF, Karin M. Immunity, inflammation, and cancer. Cell. 2010; 140:883-899.
8. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
9. Mantovani A AP, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008; 454:436-444.
10. Ha PK BN, Yochem R, Sciubba J, Zahurak M, Sidransky D, Pevsner J, Westra WH, Califano J. A transcriptional progression model for head and neck cancer. Clin Cancer Res. 2003; 9:3058-3064.
11. Gassling V, Hampe J, Acil Y, Braesen JH, Wiltfang J, Hasler R. Disease-associated miRNA-mRNA networks in oral lichen planus. PloS one. 2013; 8:e63015.
12. Cervigne NK, Reis PP, Machado J, Sadikovic B, Bradley G, Galloni NN, Pintilie M, Jurisica I, Perez-Ordonez B, Gilbert R, Gullane P, Irish J, Kamel-Reid S. Identification of a microRNA signature associated with progression of leukoplakia to oral carcinoma. Human molecular genetics. 2009; 18:4818-4829.
13. Lujambio A, Lowe SW. The microcosmos of cancer. Nature. 2012; 482:347-355.
14. Ambros V CX. The regulation of genes and genomes by small RNAs. Development. 2007; 134:1635-1641.
15. Mendell JT OE. MicroRNAs in stress signaling and human disease. Cell. 2012; 148:1172-1187.
16. Lindenbergh-van der Plas M, Martens-de Kemp SR, de Maaker M, van Wieringen WN, Ylstra B, Agami R, Cerisoli F, Leemans CR, Braakhuis BJ, Brakenhoff RH. Identification of lethal microRNAs specific for head and neck cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2013; 19:5647-5657.
17. CM. C. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet. 2009; 10:704-714.
18. O'Connell RM RD, Baltimore D. microRNA regulation of inflammatory responses. Annu Rev Immunol. 2012; 30:295-312.
19. Tili E MJ, Croce CM. MicroRNAs play a central role in molecular dysfunctions linking inflammation with cancer. Immunol Rev. 2013; 253:167-184.
20. Calin GA CC. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006; 6:857-866.
21. Tili E CC, Michaille JJ. miR-155: On the Crosstalk Between Inflammation and Cancer.pdf. Int Rev Immunol. 2009; 28:264-284.
22. Rather MI, Nagashri MN, Swamy SS, Gopinath KS, Kumar A. Oncogenic microRNA-155 down-regulates tumor suppressor CDC73 and promotes oral squamous cell carcinoma cell proliferation: implications for cancer therapeutics. The Journal of biological chemistry. 2013; 288:608-618.
23. Chen C ZY, Zhang L, Weakley SM, Yao Q. MicroRNA-196: critical roles and clinical applications in development and cancer. J Cell Mol Med. 2011; 15:14-23.
24. Taddei ML, Cavallini L, Comito G, Giannoni E, Folini M, Marini A, Gandellini P, Morandi A, Pintus G, Raspollini MR, Zaffaroni N, Chiarugi P. Senescent stroma promotes prostate cancer progression: the role of miR-210. Molecular oncology. 2014; 8:1729-1746.
25. Kim HS, Lee KS, Bae HJ, Eun JW, Shen Q, Park SJ, Shin WC, Yang HD, Park M, Park WS, Kang YK, Nam SW. MicroRNA-31 functions as a tumor suppressor by regulating cell cycle and epithelial-mesenchymal transition regulatory proteins in liver cancer. Oncotarget. 2015; 6:8089-8102.
26. Keklikoglou I, Koerner C, Schmidt C, Zhang JD, Heckmann D, Shavinskaya A, Allgayer H, Gückel B, Fehm T, Schneeweiss A, Sahin O, Wiemann S, Tschulena U. MicroRNA-520/373 family functions as a tumor suppressor in estrogen receptor negative breast cancer by targeting NF-κB and TGF-β signaling pathways. Oncogene. 2012; 31:4150-4163.
27. Kozaki K-i Imoto I, Mogi S, Omura K, Inazawa J. Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer research. 2008; 68:2094-2105.
28. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, Macdonald PE, Pfeffer S, Tuschl T, Rajewsky N, Rorsman P, Stoffel M. A pancreatic islet-specific microRNA regulates insulin secretion. Nature. 2004; 432:226-230.
29. He XX, Chang Y, Meng FY, Wang MY, Xie QH, Tang F, Li PY, Song YH, Lin JS. MicroRNA-375 targets AEG-1 in hepatocellular carcinoma and suppresses liver cancer cell growth in vitro and in vivo. Oncogene. 2012; 31:3357-3369.
30. Ding L, Xu Y, Zhang W, Deng Y, Si M, Du Y, Yao H, Liu X, Ke Y, Si J, Zhou T. MiR-375 frequently downregulated in gastric cancer inhibits cell proliferation by targeting JAK2. Cell research. 2010; 20:784-793.
31. Mathe EA, Nguyen GH, Bowman ED, Zhao Y, Budhu A, Schetter AJ, Braun R, Reimers M, Kumamoto K, Hughes D, Altorki NK, Casson AG, Liu CG, Wang XW, Yanaihara N, Hagiwara N, et al. MicroRNA expression in squamous cell carcinoma and adenocarcinoma of the esophagus: associations with survival. Clinical cancer research: an official journal of the American Association for Cancer Research. 2009; 15:6192-6200.
32. Avissar M, Christensen BC, Kelsey KT, Marsit CJ. MicroRNA expression ratio is predictive of head and neck squamous cell carcinoma. Clinical cancer research: an official journal of the American Association for Cancer Research. 2009; 15:2850-2855.
33. Chang C, Shi H, Wang C, Wang J, Geng N, Jiang X, Wang X. Correlation of microRNA-375 downregulation with unfavorable clinical outcome of patients with glioma. Neuroscience letters. 2012; 531:204-208.
34. Lajer CB NF, Friis-Hansen L, Norrild B, Borup R, Garnæs E, Rossing M, Specht L, Therkildsen MH, Nauntofte B, Dabelsteen S, von Buchwald C. Different miRNA signatures of oral and pharyngeal squamous cell carcinomas: a prospective translational study. Br J Cancer. 2011; 104:830-840.
35. Yan JW, Lin JS, He XX. The emerging role of miR-375 in cancer. International journal of cancer Journal international du cancer. 2013;.
36. Biton M LA, Slyper M, Alkalay I, Horwitz E, Mor H, Kredo-Russo S, Avnit-Sagi T, Cojocaru G, Zreik F, Bentwich Z, Poy MN, Artis D, Walker MD, Hornstein E, Pikarsky E, Ben-Neriah Y. Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat Immunol. 2011; 12:239-246.
37. Dong JT, Chen C. Essential role of KLF5 transcription factor in cell proliferation and differentiation and its implications for human diseases. Cellular and molecular life sciences: CMLS. 2009; 66:2691-2706.
38. Goldstein BG, Chao HH, Yang Y, Yermolina YA, Tobias JW, Katz JP. Overexpression of Kruppel-like factor 5 in esophageal epithelia in vivo leads to increased proliferation in basal but not suprabasal cells. American journal of physiology Gastrointestinal and liver physiology. 2007; 292:G1784-1792.
39. Chanchevalap S, Nandan MO, Merlin D, Yang VW. All-trans retinoic acid inhibits proliferation of intestinal epithelial cells by inhibiting expression of the gene encoding Kruppel-like factor 5. FEBS letters. 2004; 578:99-105.
40. Sun R, Chen X, Yang VW. Intestinal-enriched Kruppel-like factor is a positive regulator of cellular proliferation. The Journal of biological chemistry. 2001; 276:6897-6900.
41. Suzuki T, Sawaki D, Aizawa K, Munemasa Y, Matsumura T, Ishida J, Nagai R. Kruppel-like factor 5 shows proliferation-specific roles in vascular remodeling, direct stimulation of cell growth, and inhibition of apoptosis. The Journal of biological chemistry. 2009; 284:9549-9557.
42. Yang Y, Goldstein BG, Nakagawa H, Katz JP. Kruppellike factor 5 activates MEK/ERK signaling via EGFR in primary squamous epithelial cells. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2007; 21:543-550.
43. Diakiw SM, D'Andrea RJ, Brown AL. The double life of KLF5: Opposing roles in regulation of gene-expression, cellular function, and transformation. IUBMB life. 2013; 65:999-1011.
44. Yang Y, Goldstein BG, Chao HH, Katz JP. KLF and KLF5 regulate proliferation, apoptosis and invasion in esophageal cancer cells. Cancer biology & therapy. 2005; 4:1216-1221.
45. Chen C, Bhalala HV, Vessella RL, Dong JT. KLF5 is frequently deleted and down-regulated but rarely mutated in prostate cancer. The Prostate. 2003; 55:81-88.
46. Dong JT, Chen C, Stultz BG, Isaacs JT, Frierson HF Jr. Deletion at 13q21 is associated with aggressive prostate cancers. Cancer research. 2000; 60:3880-3883.
47. Chen C, Zhou Y, Zhou Z, Sun X, Otto KB, Uht RM, Dong JT. Regulation of KLF5 involves the Sp1 transcription factor in human epithelial cells. Gene. 2004; 330:133-142.
48. Chen C, Bhalala HV, Qiao H, Dong JT. A possible tumor suppressor role of the KLF5 transcription factor in human breast cancer. Oncogene. 2002; 21:6567-6572.
49. Segditsas S, Tomlinson I. Colorectal cancer and genetic alterations in the Wnt pathway. Oncogene. 2006; 25:7531-7537.
50. Nandan MO, McConnell BB, Ghaleb AM, Bialkowska AB, Sheng H, Shao J, Babbin BA, Robine S, Yang VW. Kruppel-like factor 5 mediates cellular transformation during oncogenic KRAS-induced intestinal tumorigenesis. Gastroenterology. 2008; 134:120-130.
51. Suzuki T, Nishi T, Nagino T, Sasaki K, Aizawa K, Kada N, Sawaki D, Munemasa Y, Matsumura T, Muto S, Sata M, Miyagawa K, Horikoshi M, Nagai R. Functional interaction between the transcription factor Kruppel-like factor 5 and poly(ADP-ribose) polymerase-1 in cardiovascular apoptosis. J Biol Chem. 2007; 282:9895-9901.
52. Courboulin A, Tremblay VL, Barrier M, Meloche J, Jacob MH, Chapolard M, Bisserier M, Paulin R, Lambert C, Provencher S, Bonnet S. Kruppel-like factor 5 contributes to pulmonary artery smooth muscle proliferation and resistance to apoptosis in human pulmonary arterial hypertension. Respiratory research. 2011; 12:128.
53. Zhu N, Gu L, Findley HW, Chen C, Dong JT, Yang L, Zhou M. KLF5 Interacts with p53 in regulating survivin expression in acute lymphoblastic leukemia. The Journal of biological chemistry. 2006; 281:14711-14718.
54. Tian Q LY, Wang F, Li Y, Xu J, Shen Y, Ye F, Wang X, Cheng X, Chen Y, Wan X, Lu W, Xie X. MicroRNA detection in cervical exfoliated cells as a triage for human papillomavirus-positive women. J Natl Cancer Inst. 2014; 106:pii: dju241. doi: 10.1093/jnci/dju1241.
55. Mattila R RJ, Syrjänen S. Human papillomavirus in oral atrophic lichen planus lesions. Oral Oncol. 2012; 48:980-984.
56. Hübbers CU AB. HPV and cancer of the oral cavity. Virulence. 2015; 6:244-248.
57. Kreppel M, Eich HT, Kubler A, Zoller JE, Scheer M. Prognostic value of the sixth edition of the UICC's TNM classification and stage grouping for oral cancer. Journal of surgical oncology. 2010; 102:443-449.
58. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics (Oxford, England). 2009; 25:1966-1967.
59. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature methods. 2008; 5:621-628.
60. Audic S, Claverie JM. The significance of digital gene expression profiles. Genome research. 1997; 7:986-995.
61. Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. The Annals of Statistics. 2001; 29:1165-1188.
62. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic acids research. 2002; 30:207-210.
63. Lu CD, Altieri DC, Tanigawa N. Expression of a novel antiapoptosis gene, survivin, correlated with tumor cell apoptosis and p53 accumulation in gastric carcinomas. Cancer research. 1998; 58:1808-1812.
64. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25:402-408.