The role of HOXB9 and miR-196a in head and neck squamous cell carcinoma

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Darda, Lav ^a   Hakami, Fahad ^a   Morgan, Richard ^b   Murdoch, Craig ^a   Lambert, Daniel W ^a   Hunter, Keith D ^a,c  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF BRADFORD   (United Kingdom)

^c UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; HOMEODOMAIN PROTEIN; MICRORNA; MICRORNA 196A; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HOXB9; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; ANTISENSE OLIGONUCLEOTIDE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; HOXB9 PROTEIN, HUMAN; MDGA2 PROTEIN, HUMAN; MIRN196 MICRORNA, HUMAN; NERVE CELL ADHESION MOLECULE; SMALL INTERFERING RNA;

3' UNTRANSLATED REGION; ARTICLE; CANCER CELL LINE; CARCINOGENICITY; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; COMPUTER MODEL; COMPUTER PREDICTION; CONTROLLED STUDY; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; GENETIC TRANSFECTION; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HOXB9 GENE; HOXC8 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; LASER MICRODISSECTION; LUCIFERASE ASSAY; MAMDC2 GENE; MICROARRAY ANALYSIS; MIR 196A GENE; MOUTH MUCOSA; MUTATIONAL ANALYSIS; NUCLEOTIDE BINDING SITE; ONCOGENE; POLYMERASE CHAIN REACTION; RNA BINDING; RNA GENE; TISSUE DISTRIBUTION; TRANSCRIPTION REGULATION; UPREGULATION; ANTAGONISTS AND INHIBITORS; BINDING SITE; CELL MOTION; CHEMISTRY; GENETICS; HEAD AND NECK TUMOR; METABOLISM; PATHOLOGY; RNA INTERFERENCE; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; BINDING SITES; CARCINOMA, SQUAMOUS CELL; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; FIBRONECTINS; GPI-LINKED PROTEINS; HEAD AND NECK NEOPLASMS; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MICRORNAS; MOUTH MUCOSA; NEURAL CELL ADHESION MOLECULES; OLIGONUCLEOTIDES, ANTISENSE; RNA INTERFERENCE; RNA, SMALL INTERFERING; UP-REGULATION;

EID: 84928797164     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122285     Document Type: Article

References (60)

1. Markovic A, Chung CH (2012) Current role of EGF receptor monoclonal antibodies and tyrosine kinase inhibitors in the management of head and neck squamous cell carcinoma. Expert Rev Anticancer Ther 12: 1149-1159. doi: 10.1586/era.12.91 PMID: 23098115
2. Leemans CR, Braakhuis BJ, Brakenhoff RH (2011) The molecular biology of head and neck cancer. Nat Rev Cancer 11: 9-22. doi: 10.1038/nrc2982 PMID: 21160525
3. Hunter KD, Thurlow JK, Fleming J, Drake PJ, Vass JK, et al. (2006) Divergent routes to oral cancer. Cancer Res 66: 7405-7413. PMID: 16885335
4. Grier DG, Thompson A, Kwasniewska A, McGonigle GJ, Halliday HL, et al. (2005) The pathophysiology of HOX genes and their role in cancer. J Pathol 205: 154-171. PMID: 15643670
5. Calvo R, West J, Franklin W, Erickson P, Bemis L, et al. (2000) Altered HOX and WNT7A expression in human lung cancer. Proc Natl Acad Sci U S A 97: 12776-12781. PMID: 11070089
6. Barber BA, Rastegar M (2010) Epigenetic control of Hox genes during neurogenesis, development, and disease. Ann Anat 192: 261-274. doi: 10.1016/j.aanat.2010.07.009 PMID: 20739155
7. Hayashida T, Takahashi F, Chiba N, Brachtel E, Takahashi M, et al. (2010) HOXB9, a gene overexpressed in breast cancer, promotes tumorigenicity and lung metastasis. Proc Natl Acad Sci U S A 107: 1100-1105. doi: 10.1073/pnas.0912710107 PMID: 20080567
8. Morgan R, Plowright L, Harrington KJ, Michael A, Pandha HS (2010) Targeting HOX and PBX transcription factors in ovarian cancer. BMC Cancer 10: 89. doi: 10.1186/1471-2407-10-89 PMID: 20219106
9. Taketani T, Taki T, Shibuya N, Kikuchi A, Hanada R, et al. (2002) Novel NUP98-HOXC11 fusion gene resulted from a chromosomal break within exon 1 of HOXC11 in acute myeloid leukemia with t(11;12) (p15;q13). Cancer Res 62: 4571-4574. PMID: 12183408
10. Raza-Egilmez SZ, Jani-Sait SN, Grossi M, Higgins MJ, Shows TB, et al. (1998) NUP98-HOXD13 gene fusion in therapy-related acute myelogenous leukemia. Cancer Res 58: 4269-4273. PMID: 9766650
11. Raman V, Martensen SA, Reisman D, Evron E, Odenwald WF, et al. (2000) Compromised HOXA5 function can limit p53 expression in human breast tumours. Nature 405: 974-978. PMID: 10879542
12. Rodriguez BA, Cheng AS, Yan PS, Potter D, Agosto-Perez FJ, et al. (2008) Epigenetic repression of the estrogen-regulated Homeobox B13 gene in breast cancer. Carcinogenesis 29: 1459-1465. doi: 10.1093/carcin/bgn115 PMID: 18499701
13. Seki H, Hayashida T, Jinno H, Hirose S, Sakata M, et al. (2012) HOXB9 expression promoting tumor cell proliferation and angiogenesis is associated with clinical outcomes in breast cancer patients. Ann Surg Oncol 19: 1831-1840. doi: 10.1245/s10434-012-2295-5 PMID: 22396001
14. Plowright L, Harrington KJ, Pandha HS, Morgan R (2009) HOX transcription factors are potential therapeutic targets in non-small-cell lung cancer (targeting HOX genes in lung cancer). Br J Cancer 100: 470-475. doi: 10.1038/sj.bjc.6604857 PMID: 19156136
15. Nguyen DX, Chiang AC, Zhang XH, Kim JY, Kris MG, et al. (2009) WNT/TCF signaling through LEF1 and HOXB9 mediates lung adenocarcinoma metastasis. Cell 138: 51-62. doi: 10.1016/j.cell.2009.04.030 PMID: 19576624
16. Tsai KW, Liao YL, Wu CW, Hu LY, Li SC, et al. (2012) Aberrant expression of miR-196a in gastric cancers and correlation with recurrence. Genes Chromosomes Cancer 51: 394-401. PMID: 22420029
17. Hassan N, Hamada J, Murai T, Seino A, Takahashi Y, et al. (2006) Aberrant expression of HOX genes in oral dysplasia and squamous cell carcinoma tissues. Oncol Res 16: 217-224. PMID: 17294802
18. Li Y, Zhang M, Chen H, Dong Z, Ganapathy V, et al. (2010) Ratio of miR-196s to HOXC8 messenger RNA correlates with breast cancer cell migration and metastasis. Cancer Res 70: 7894-7904. doi: 10.1158/0008-5472.CAN-10-1675 PMID: 20736365
19. Asli NS, Kessel M (2010) Spatiotemporally restricted regulation of generic motor neuron programs by miR-196-mediated repression of Hoxb8. Dev Biol 344: 857-868. doi: 10.1016/j.ydbio.2010.06.003 PMID: 20553899
20. Maru DM, Singh RR, Hannah C, Albarracin CT, Li YX, et al. (2009) MicroRNA-196a is a potential marker of progression during Barrett's metaplasia-dysplasia-invasive adenocarcinoma sequence in esophagus. Am J Pathol 174: 1940-1948. doi: 10.2353/ajpath.2009.080718 PMID: 19342367
21. McGlinn E, Yekta S, Mansfield JH, Soutschek J, Bartel DP, et al. (2009) In ovo application of antagomiRs indicates a role for miR-196 in patterning the chick axial skeleton through Hox gene regulation. Proc Natl Acad Sci U S A 106: 18610-18615. doi: 10.1073/pnas.0910374106 PMID: 19846767
22. Liu CJ, Tsai MM, Tu HF, Lui MT, Cheng HW, et al. (2012) miR-196a Overexpression and miR-196a2 Gene Polymorphism Are Prognostic Predictors of Oral Carcinomas. Ann Surg Oncol.
23. Yekta S, Shih IH, Bartel DP (2004) MicroRNA-directed cleavage of HOXB8 mRNA. Science 304: 594-596. PMID: 15105502
24. Braig S, Mueller DW, Rothhammer T, Bosserhoff AK (2010) MicroRNA miR-196a is a central regulator of HOX-B7 and BMP4 expression in malignant melanoma. Cell Mol Life Sci 67: 3535-3548. doi: 10.1007/s00018-010-0394-7 PMID: 20480203
25. Liu XH, Lu KH, Wang KM, Sun M, Zhang EB, et al. (2012) MicroRNA-196a promotes non-small cell lung cancer cell proliferation and invasion through targeting HOXA5. BMC Cancer 12: 348. doi: 10.1186/1471-2407-12-348 PMID: 22876840
26. Sun M, Liu XH, Li JH, Yang JS, Zhang EB, et al. (2012) MiR-196a is upregulated in gastric cancer and promotes cell proliferation by downregulating p27(kip1). Mol Cancer Ther 11: 842-852. doi: 10.1158/1535-7163.MCT-11-1015 PMID: 22343731
27. Luthra R, Singh RR, Luthra MG, Li YX, Hannah C, et al. (2008) MicroRNA-196a targets annexin A1: a microRNA-mediated mechanism of annexin A1 downregulation in cancers. Oncogene 27: 6667-6678. doi: 10.1038/onc.2008.256 PMID: 18663355
28. Hui AB, Shi W, Boutros PC, Miller N, Pintilie M, et al. (2009) Robust global micro-RNA profiling with for-malin-fixed paraffin-embedded breast cancer tissues. Lab Invest 89: 597-606. doi: 10.1038/labinvest.2009.12 PMID: 19290006
29. Mueller DW, Bosserhoff AK (2011) MicroRNA miR-196a controls melanoma-associated genes by regulating HOX-C8 expression. Int J Cancer 129: 1064-1074. doi: 10.1002/ijc.25768 PMID: 21077158
30. Severino P, Bruggemann H, Andreghetto FM, Camps C, Klingbeil Mde F, et al. (2013) MicroRNA expression profile in head and neck cancer: HOX-cluster embedded microRNA-196a and microRNA-10b dysregulation implicated in cell proliferation. BMC Cancer 13: 533. doi: 10.1186/1471-2407-13-533 PMID: 24209638
31. Burns J, Baird M, Clark L, Burns P, Edington K, et al. (1993) Gene mutations and increased levels of p53 protein in human squamous cell carcinomas and their cell lines. British Journal of Cancer 67: 1274-1284. PMID: 8390283
32. Burns JE, McFarlane R, Clark LJ, Mitchell R, Robertson G, et al. (1994) Maintenance of identical p53 mutations throughout progression of squamous cell carcinomas of the tongue. Eur J Cancer B Oral Oncol 30B: 335-337. PMID: 7703803
33. Prime SS, Nixon SV, Crane IJ, Stone A, Matthews JB, et al. (1990) The behaviour of human oral squamous cell carcinoma in cell culture. J Pathol 160: 259-269. PMID: 1692339
34. McGregor F, Muntoni A, Fleming J, Brown J, Felix DH, et al. (2002) Molecular changes associated with oral dysplasia progression and acquisition of immortality: potential for its reversal by 5-azacytidine. Cancer Res 62: 4757-4766. PMID: 12183435
35. McGregor F, Wagner E, Felix D, Soutar D, Parkinson K, et al. (1997) Inappropriate retinoic and receptor β expression in oral dysplasias: correlation with acquisition of the immortal phenotype. Cancer research 57: 3886-3889. PMID: 9307265
36. Colley HE, Hearnden V, Jones AV, Weinreb PH, Violette SM, et al. (2011) Development of tissue-engineered models of oral dysplasia and early invasive oral squamous cell carcinoma. Br J Cancer 105: 1582-1592. doi: 10.1038/bjc.2011.403 PMID: 21989184
37. Dickson MA, Hahn WC, Ino Y, Ronfard V, Wu JY, et al. (2000) Human keratinocytes that express hTERT and also bypass a p16(INK4a)-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics. Mol Cell Biol 20: 1436-1447. PMID: 10648628
38. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, et al. (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85. PMID: 3843705
39. Neves JI, Begnami MD, Arias V, Santos GC (2005) Antigen retrieval methods and estrogen receptor immunoexpression using 1D5 antibody: a comparative study. Int J Surg Pathol 13: 353-357. PMID: 16273191
40. Detre S, Saclani Jotti G, Dowsett M (1995) A "quickscore" method for immunohistochemical semiquantitation: validation for oestrogen receptor in breast carcinomas. J Clin Pathol 48: 876-878. PMID: 7490328
41. Mao L, Ding J, Zha Y, Yang L, McCarthy BA, et al. (2011) HOXC9 links cell-cycle exit and neuronal differentiation and is a prognostic marker in neuroblastoma. Cancer Res 71: 4314-4324. doi: 10.1158/0008-5472.CAN-11-0051 PMID: 21507931
42. Drabkin HA, Parsy C, Ferguson K, Guilhot F, Lacotte L, et al. (2002) Quantitative HOX expression in chromosomally defined subsets of acute myelogenous leukemia. Leukemia 16: 186-195. PMID: 11840284
43. Nonn L, Vaishnav A, Gallagher L, Gann PH (2010) mRNA and micro-RNA expression analysis in laser-capture microdissected prostate biopsies: valuable tool for risk assessment and prevention trials. Exp Mol Pathol 88: 45-51. doi: 10.1016/j.yexmp.2009.10.005 PMID: 19874819
44. Chen Z, Jin Y, Yu D, Wang A, Mahjabeen I, et al. (2012) Down-regulation of the microRNA-99 family members in head and neck squamous cell carcinoma. Oral Oncol 48: 686-691. doi: 10.1016/j.oraloncology.2012.02.020 PMID: 22425712
45. Zhang H, Su YL, Yu H, Qian BY (2012) Meta-Analysis of the Association between Mir-196a-2 Polymorphism and Cancer Susceptibility. Cancer Biol Med 9: 63-72. doi: 10.3969/j.issn.2095-3941.2012.01.012 PMID: 23691458
46. Tsai MM, Wang CS, Tsai CY, Chen CY, Chi HC, et al. (2014) MicroRNA-196a/-196b promote cell metastasis via negative regulation of radixin in human gastric cancer. Cancer Lett 351: 222-231. doi: 10.1016/j.canlet.2014.06.004 PMID: 24933454
47. Kanai M, Hamada J, Takada M, Asano T, Murakawa K, et al. (2010) Aberrant expressions of HOX genes in colorectal and hepatocellular carcinomas. Oncol Rep 23: 843-851. PMID: 20127028
48. Sha S, Gu Y, Xu B, Hu H, Yang Y, et al. (2013) Decreased expression of HOXB9 is related to poor overall survival in patients with gastric carcinoma. Dig Liver Dis.
49. Ginos MA, Page GP, Michalowicz BS, Patel KJ, Volker SE, et al. (2004) Identification of a gene expression signature associated with recurrent disease in squamous cell carcinoma of the head and neck. Cancer Res 64: 55-63. PMID: 14729608
50. Walter V, Yin X, Wilkerson MD, Cabanski CR, Zhao N, et al. (2013) Molecular subtypes in head and neck cancer exhibit distinct patterns of chromosomal gain and loss of canonical cancer genes. PLoS One 8: e56823. doi: 10.1371/journal.pone.0056823 PMID: 23451093
51. Chiba N, Comaills V, Shiotani B, Takahashi F, Shimada T, et al. (2012) Homeobox B9 induces epitheli-al-to-mesenchymal transition-associated radioresistance by accelerating DNA damage responses. Proc Natl Acad Sci U S A 109: 2760-2765. doi: 10.1073/pnas.1018867108 PMID: 21930940
52. Sha L, Dong L, Lv L, Bai L, Ji X (2014) HOXB9 promotes epithelial-to-mesenchymal transition via transforming growth factor-beta1 pathway in hepatocellular carcinoma cells. Clin Exp Med.
53. Nagel S, Burek C, Venturini L, Scherr M, Quentmeier H, et al. (2007) Comprehensive analysis of homeobox genes in Hodgkin lymphoma cell lines identifies dysregulated expression of HOXB9 mediated via ERK5 signaling and BMI1. Blood 109: 3015-3023. PMID: 17148583
54. Danen-van Oorschot AA, Kuipers JE, Arentsen-Peters S, Schotte D, de Haas V, et al. (2012) Differentially expressed miRNAs in cytogenetic and molecular subtypes of pediatric acute myeloid leukemia. Pediatr Blood Cancer 58: 715-721. doi: 10.1002/pbc.23279 PMID: 21818844
55. Mainguy G, Koster J, Woltering J, Jansen H, Durston A (2007) Extensive polycistronism and antisense transcription in the mammalian Hox clusters. PLoS One 2: e356. PMID: 17406680
56. Cismasiu VB, Denes SA, Reilander H, Michel H, Szedlacsek SE (2004) The MAM (meprin/A5-protein/PTPmu) domain is a homophilic binding site promoting the lateral dimerization of receptor-like proteintyrosine phosphatase mu. J Biol Chem 279: 26922-26931. PMID: 15084579
57. Diaz-Lopez A, Iniesta P, Moran A, Ortega P, Fernandez-Marcelo T, et al. (2010) Expression of Human MDGA1 Increases Cell Motility and Cell-Cell Adhesion and Reduces Adhesion to Extracellular Matrix Proteins in MDCK Cells. Cancer Microenviron 4: 23-32. doi: 10.1007/s12307-010-0055-2 PMID: 21505559
58. Zhang P, Becka S, Craig SE, Lodowski DT, Brady-Kalnay SM, et al. (2009) Cancer-derived mutations in the fibronectin III repeats of PTPRT/PTPrho inhibit cell-cell aggregation. Cell Commun Adhes 16: 146-153. doi: 10.3109/15419061003653771 PMID: 20230342
59. Yu J, Becka S, Zhang P, Zhang X, Brady-Kalnay SM, et al. (2008) Tumor-derived extracellular mutations of PTPRT /PTPrho are defective in cell adhesion. Mol Cancer Res 6: 1106-1113. doi: 10.1158/1541-7786.MCR-07-2123 PMID: 18644975
60. Pan W (2002) A comparative review of statistical methods for discovering differentially expressed genes in replicated microarray experiments. Bioinformatics 18: 546-554. PMID: 12016052