G9a is essential for EMT-mediated metastasis and maintenance of cancer stem cell-like characters in head and neck squamous cell carcinoma

Oncotarget

Volumn 6, Issue 9, 2015, Pages 6887-6901

  Liu, Shuli ^a   Ye, Dongxia ^a   Guo, Wenzheng ^a   Yu, Wenwen ^a   He, Yue ^a   Hu, Jingzhou ^a   Wang, Yanan ^a   Zhang, Ling ^a   Liao, Yueling ^a   Song, Hongyong ^a   Zhong, Shuangshuang ^a   Xu, Dongliang ^a   Yin, Huijing ^a   Sun, Beibei ^b   Wang, Xiaofei ^b   Liu, Jingyi ^c   Wu, Yadi ^c   Zhou, Binhua P ^c   Zhang, Zhiyuan ^a   Deng, Jiong ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Cancer stem cell; EMT; G9a; HNSCC; Lymph node metastasis

Indexed keywords

G9A PROTEIN; HERMES ANTIGEN; HISTONE H3; HISTONE METHYLTRANSFERASE; MESSENGER RNA; N (1 BENZYL 4 PIPERIDINYL) 2 (HEXAHYDRO 4 METHYL 1H 1,4 DIAZEPIN 1 YL) 6,7 DIMETHOXY 4 QUINAZOLINAMINE; NERVE CELL ADHESION MOLECULE; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; CADHERIN; CDH1 PROTEIN, HUMAN; EHMT2 PROTEIN, HUMAN; HISTOCOMPATIBILITY ANTIGEN; HISTONE; HISTONE LYSINE METHYLTRANSFERASE;

ARTICLE; CANCER PROGNOSIS; CANCER STEM CELL; CANCER SURVIVAL; CELL MOTILITY; CELL STRUCTURE; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENE SILENCING; HEAD AND NECK CARCINOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA CELL LINE; HISTONE METHYLATION; LYMPH NODE METASTASIS; MIGRATION INHIBITION; MOLECULAR DYNAMICS; PHENOTYPE; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SQUAMOUS CELL CARCINOMA CELL LINE; SURVIVAL RATE; SURVIVAL TIME; TUMOR SPHEROID; UPREGULATION; CANCER TRANSPLANTATION; CELL MOTION; CHEMISTRY; CYTOLOGY; FLOW CYTOMETRY; HEAD AND NECK TUMOR; HUMAN; METABOLISM; METASTASIS; METHYLATION; PATHOLOGY; PROGNOSIS; SQUAMOUS CELL CARCINOMA; STEM CELL; TREATMENT OUTCOME; TUMOR RECURRENCE; WOUND HEALING;

CADHERINS; CARCINOMA, SQUAMOUS CELL; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HISTOCOMPATIBILITY ANTIGENS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; LYMPHATIC METASTASIS; METHYLATION; NEOPLASM METASTASIS; NEOPLASM RECURRENCE, LOCAL; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; PROGNOSIS; STEM CELLS; TRANSFORMING GROWTH FACTOR BETA; TREATMENT OUTCOME; WOUND HEALING;

EID: 84927133961     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3159     Document Type: Article

References (63)

1. Leemans CR, Braakhuis BJ, Brakenhoff RH. The molecular biology of head and neck cancer. Nature Reviews Cancer. 2011; 11:9-22.
2. Pantel K, Brakenhoff RH. Dissecting the metastatic cascade. Nature Reviews Cancer. 2004; 4:448-456.
3. DiTroia JF. Nodal metastases and prognosis in carcinoma of the oral cavity. Otolaryngologic clinics of North America. 1972; 5:333-342.
4. Cerezo L, Millan I, Torre A, Aragon G, Otero J. Prognostic factors for survival and tumor control in cervical lymph node metastases from head and neck cancer. A multivariate study of 492 cases. Cancer. 1992; 69:1224-1234.
5. Leemans CR, Tiwari R, Nauta JJ, van der Waal I, Snow GB. Recurrence at the primary site in head and neck cancer and the significance of neck lymph node metastases as a prognostic factor. Cancer. 1994; 73:187-190.
6. Roepman P, Wessels LF, Kettelarij N, Kemmeren P, Miles AJ, Lijnzaad P, Tilanus MG, Koole R, Hordijk GJ, van der Vliet PC, Reinders MJ, Slootweg PJ, Holstege FC. An expression profile for diagnosis of lymph node metastases from primary head and neck squamous cell carcinomas. Nature genetics. 2005; 37:182-186.
7. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. The Journal of clinical investigation. 2009; 119:1420-1428.
8. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009; 139:871-890.
9. Wu Y, Zhou BP. Snail: more than EMT. Cell adhesion & migration. 2010; 4:199-203.
10. Berx G, Raspe E, Christofori G, Thiery JP, Sleeman JP. Pre-EMTing metastasis? Recapitulation of morphogenetic processes in cancer. Clinical & experimental metastasis. 2007; 24:587-597.
11. Christofori G. New signals from the invasive front. Nature. 2006; 441:444-450.
12. Lopez-Novoa JM, Nieto MA. Inflammation and EMT: an alliance towards organ fibrosis and cancer progression. EMBO molecular medicine. 2009; 1:303-314.
13. Wu Y, Zhou BP. Inflammation: a driving force speeds cancer metastasis. Cell cycle. 2009; 8:3267-3273.
14. Miettinen PJ, Ebner R, Lopez AR, Derynck R. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. The Journal of cell biology. 1994; 127:2021-2036.
15. Wu Y, Deng J, Rychahou PG, Qiu S, Evers BM, Zhou BP. Stabilization of snail by NF-kappaB is required for inflammation- induced cell migration and invasion. Cancer Cell. 2009; 15:416-428.
16. Roberts AB, Wakefield LM. The two faces of transforming growth factor beta in carcinogenesis. Proceedings of the National Academy of Sciences of the United States of America. 2003; 100:8621-8623.
17. Yao D, Dai C, Peng S. Mechanism of the mesenchymal-epithelial transition and its relationship with metastatic tumor formation. Molecular cancer research. 2011; 9:1608-1620.
18. de Krijger I, Mekenkamp LJ, Punt CJ, Nagtegaal ID. MicroRNAs in colorectal cancer metastasis. The Journal of pathology. 2011; 224:438-447.
19. Diniz-Freitas M, Garcia-Caballero T, Antunez-Lopez J, Gandara-Rey JM, Garcia-Garcia A. Reduced E-cadherin expression is an indicator of unfavourable prognosis in oral squamous cell carcinoma. Oral oncology. 2006; 42:190-200.
20. Lombaerts M, van Wezel T, Philippo K, Dierssen JW, Zimmerman RM, Oosting J, van Eijk R, Eilers PH, van de Water B, Cornelisse CJ, Cleton-Jansen AM. E-cadherin transcriptional downregulation by promoter methylation but not mutation is related to epithelial-to-mesenchymal transition in breast cancer cell lines. British journal of cancer. 2006; 94:661-671.
21. Ginos MA, Page GP, Michalowicz BS, Patel KJ, Volker SE, Pambuccian SE, Ondrey FG, Adams GL, Gaffney PM. Identification of a gene expression signature associated with recurrent disease in squamous cell carcinoma of the head and neck. Cancer research. 2004; 64:55-63.
22. Campos EI, Reinberg D. Histones: annotating chromatin. Annual review of genetics. 2009; 43:559-599.
23. Shi Y. Histone lysine demethylases: emerging roles in development, physiology and disease. Nature reviews genetics. 2007; 8:829-833.
24. Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, Fukuda M, Takeda N, Niida H, Kato H, Shinkai Y. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes & development. 2002; 16:1779-1791.
25. Shankar SR, Bahirvani AG, Rao VK, Bharathy N, Ow JR, Taneja R. G9a, a multipotent regulator of gene expression. Epigenetics official journal of the DNA Methylation Society. 2013; 8:16-22.
26. Lehnertz B, Pabst C, Su L, Miller M, Liu F, Yi L, Zhang R, Krosl J, Yung E, Kirschner J, Rosten P, Underhill TM, Jin J, Hebert J, Sauvageau G, Humphries RK, et al. The methyltransferase G9a regulates HoxA9-dependent transcription in AML. Genes & development. 2014; 28:317-327.
27. Dong C, Wu Y, Yao J, Wang Y, Yu Y, Rychahou PG, Evers BM, Zhou BP. G9a interacts with snail and is critical for snail-mediated E-cadherin repression in human breast cancer. The Journal of clinical investigation. 2012; 122:1469-1486.
28. Kondo Y, Shen L, Ahmed S, Boumber Y, Sekido Y, Haddad BR, Issa JP. Downregulation of histone H3 lysine 9 methyltransferase G9a induces centrosome disruption and chromosome instability in cancer cells. PloS one. 2008; 3:e2037.
29. Chen H, Yan Y, Davidson TL, Shinkai Y, Costa M. Hypoxic stress induces dimethylated histone H3 lysine 9 through histone methyltransferase G9a in mammalian cells. Cancer research. 2006; 66:9009-9016.
30. Ding J, Li T, Wang X, Zhao E, Choi JH, Yang L, Zha Y, Dong Z, Huang S, Asara JM, Cui H, Ding HF. The histone H3 methyltransferase G9A epigenetically activates the serine- glycine synthesis pathway to sustain cancer cell survival and proliferation. Cell metabolism. 2013; 18:896-907.
31. Chen MW, Hua KT, Kao HJ, Chi CC, Wei LH, Johansson G, Shiah SG, Chen PS, Jeng YM, Cheng TY, Lai TC, Chang JS, Jan YH, Chien MH, Yang CJ, Huang MS, et al. H3K9 histone methyltransferase G9a promotes lung cancer invasion and metastasis by silencing the cell adhesion molecule Ep-CAM. Cancer research. 2010; 70:7830-7840.
32. Li KC, Hua KT, Lin YS, Su CY, Ko JY, Hsiao M, Kuo ML, Tan CT. Inhibition of G9a induces DUSP4-dependent autophagic cell death in head and neck squamous cell carcinoma. Molecular cancer. 2014; 13:172.
33. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, Weissman IL, Clarke MF, Ailles LE. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104:973-978.
34. Gao L, Yan L, Lin B, Gao J, Liang X, Wang Y, Liu J, Zhang S, Iwamori M. Enhancive effects of Lewis y antigen on CD44-mediated adhesion and spreading of human ovarian cancer cell line RMG-I. Journal of experimental & clinical cancer research : CR. 2011; 30:15.
35. Biddle A, Liang X, Gammon L, Fazil B, Harper LJ, Emich H, Costea DE, Mackenzie IC. Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer research. 2011; 71:5317-5326.
36. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008; 133:704-715.
37. Kim SY, Chu KC, Lee HR, Lee KS, Carey TE. Establishment and characterization of nine new head and neck cancer cell lines. Acta oto-laryngologica. 1997; 117:775-784.
38. Cromer A, Carles A, Millon R, Ganguli G, Chalmel F, Lemaire F, Young J, Dembele D, Thibault C, Muller D, Poch O, Abecassis J, Wasylyk B. Identification of genes associated with tumorigenesis and metastatic potential of hypopharyngeal cancer by microarray analysis. Oncogene. 2004; 23:2484-2498.
39. Lopes FF, da Costa Miguel MC, Pereira AL, da Cruz MC, de Almeida Freitas R, Pinto LP, de Souza LB. Changes in immunoexpression of E-cadherin and beta-catenin in oral squamous cell carcinoma with and without nodal metastasis. Annals of diagnostic pathology. 2009; 13:22-29.
40. Kudo Y, Kitajima S, Ogawa I, Hiraoka M, Sargolzaei S, Keikhaee MR, Sato S, Miyauchi M, Takata T. Invasion and metastasis of oral cancer cells require methylation of E-cadherin and/or degradation of membranous beta-catenin. Clinical cancer research: an official journal of the American Association for Cancer Research. 2004; 10:5455-5463.
41. De Craene B, Gilbert B, Stove C, Bruyneel E, van Roy F, Berx G. The transcription factor snail induces tumor cell invasion through modulation of the epithelial cell differentiation program. Cancer research. 2005; 65:6237-6244.
42. Nieto MA. The snail superfamily of zinc-finger transcription factors. Nature reviews Molecular cell biology. 2002; 3:155-166.
43. Kim YH, Kim G, Kwon CI, Kim JW, Park PW, Hahm KB. TWIST1 and SNAI1 as markers of poor prognosis in human colorectal cancer are associated with the expression of ALDH1 and TGF-beta1. Oncology reports. 2014; 31:1380-1388.
44. Reichl P, Haider C, Grubinger M, Mikulits W. TGF-beta in epithelial to mesenchymal transition and metastasis of liver carcinoma. Current pharmaceutical design. 2012; 18:4135-4147.
45. Mendelsohn AH, Lai CK, Shintaku IP, Fishbein MC, Brugman K, Elashoff DA, Abemayor E, Dubinett SM, St John MA. Snail as a novel marker for regional metastasis in head and neck squamous cell carcinoma. American journal of otolaryngology. 2012; 33:6-13.
46. Ling BM, Gopinadhan S, Kok WK, Shankar SR, Gopal P, Bharathy N, Wang Y, Taneja R. G9a mediates sharp-1-dependent inhibition of skeletal muscle differentiation. Molecular biology of the cell. 2012; 23:4778-4785.
47. Nishio H, Walsh MJ. CCAAT displacement protein/cut homolog recruits G9a histone lysine methyltransferase to repress transcription. Proceedings of the National Academy of Sciences of the United States of America. 2004; 101:11257-11262.
48. Roopra A, Qazi R, Schoenike B, Daley TJ, Morrison JF. Localized domains of G9a-mediated histone methylation are required for silencing of neuronal genes. Molecular cell. 2004; 14:727-738.
49. Duan Z, Zarebski A, Montoya-Durango D, Grimes HL, Horwitz M. Gfi1 coordinates epigenetic repression of p21Cip/WAF1 by recruitment of histone lysine methyltransferase G9a and histone deacetylase 1. Molecular and cellular biology. 2005; 25:10338-10351.
50. Chen X, El Gazzar M, Yoza BK, McCall CE. The NF-kappaB factor RelB and histone H3 lysine methyltransferase G9a directly interact to generate epigenetic silencing in endotoxin tolerance. The Journal of biological chemistry. 2009; 284:27857-27865.
51. Chaturvedi CP, Hosey AM, Palii C, Perez-Iratxeta C, Nakatani Y, Ranish JA, Dilworth FJ, Brand M. Dual role for the methyltransferase G9a in the maintenance of beta-globin gene transcription in adult erythroid cells. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106:18303-18308.
52. Purcell DJ, Khalid O, Ou CY, Little GH, Frenkel B, Baniwal SK, Stallcup MR. Recruitment of coregulator G9a by Runx2 for selective enhancement or suppression of transcription. Journal of cellular biochemistry. 2012; 113:2406-2414.
53. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nature reviews cancer. 2008; 8:755-768.
54. Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY, Bapat SA. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem cells (Dayton, Ohio). 2009; 27:2059-2068.
55. Santisteban M, Reiman JM, Asiedu MK, Behrens MD, Nassar A, Kalli KR, Haluska P, Ingle JN, Hartmann LC, Manjili MH, Radisky DC, Ferrone S, Knutson KL. Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer research. 2009; 69:2887-2895.
56. Yang MH, Hsu DS, Wang HW, Wang HJ, Lan HY, Yang WH, Huang CH, Kao SY, Tzeng CH, Tai SK, Chang SY, Lee OK, Wu KJ. Bmi1 is essential in twist1-induced epithelial-mesenchymal transition. Nature cell biology. 2010; 12:982-992.
57. Hua KT, Wang MY, Chen MW, Wei LH, Chen CK, Ko CH, Jeng YM, Sung PL, Jan YH, Hsiao M, Kuo ML, Yen ML. The H3K9 methyltransferase G9a is a marker of aggressive ovarian cancer that promotes peritoneal metastasis. Molecular cancer. 2014; 13:189.
58. Lee DY, Northrop JP, Kuo MH, Stallcup MR. Histone H3 lysine 9 methyltransferase G9a is a transcriptional coactivator for nuclear receptors. The Journal of biological chemistry. 2006; 281:8476-8485.
59. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, Waldvogel B, Vannier C, Darling D, zur Hausen A, Brunton VG, Morton J, Sansom O, Schuler J, Stemmler MP, Herzberger C, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness- inhibiting microRNAs. Nature cell biology. 2009; 11:1487-1495.
60. Xu Q, Sun Q, Zhang J, Yu J, Chen W, Zhang Z. Downregulation of miR-153 contributes to epithelial-mesenchymal transition and tumor metastasis in human epithelial cancer. Carcinogenesis. 2013; 34:539-549.
61. Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M, Hung MC. Dual regulation of snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nature cell biology. 2004; 6:931-940.
62. Li J, Zhou BP. Activation of beta-catenin and Akt pathways by twist are critical for the maintenance of EMT associated cancer stem cell-like characters. BMC cancer. 2011; 11:49.
63. Liu SL, Zhong SS, Ye DX, Chen WT, Zhang ZY, Deng J. Repression of G protein-coupled receptor family C group 5 member A is associated with pathologic differentiation grade of oral squamous cell carcinoma. Journal of oral pathology & medicine : official publication of the International Association of Oral Pathologists and the American Academy of Oral Pathology. 2013; 42:761-768.