IRX1 hypomethylation promotes osteosarcoma metastasis via induction of CXCL14/NF-κB signaling

Journal of Clinical Investigation

Volumn 125, Issue 5, 2015, Pages 1839-1856

  Lu, Jinchang ^a   Song, Guohui ^a   Tang, Qinglian ^a   Zou, Changye ^a   Han, Feng ^b   Zhao, Zhiqiang ^a   Yong, Bicheng ^a,c   Yin, Junqiang ^a   Xu, Huaiyuan ^a   Xie, Xianbiao ^a   Kang, Tiebang ^d   Lam, YingLee ^b   Yang, Huiling ^e   Shen, Jingnan ^a   Wang, Jin ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c Guangzhou Women and Children's Hospital   (China)

^d SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^e SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

3 (4 TERT BUTYLPHENYLSULFONYL) 2 PROPENENITRILE; CXCL14 CHEMOKINE; DNA; EPITHELIAL CELL ADHESION MOLECULE; GRANULOCYTE CHEMOTACTIC PROTEIN 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IROQUOIS HOMEOBOX 1; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ALPHA CHEMOKINE; CXCL14 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; IRX1 PROTEIN, HUMAN; MESSENGER RNA; RNA; TUMOR PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANOIKIS; ARTICLE; BINDING SITE; CANCER GENE THERAPY; CANCER PATIENT; CANCER PROGNOSIS; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DNA METHYLATION; DNA MODIFICATION; DOWN REGULATION; EPIGENETICS; EXPRESSION VECTOR; FEMALE; GENE INDUCTION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; LUNG METASTASIS; MALE; METASTASIS FREE SURVIVAL; METASTASIS POTENTIAL; MICROARRAY ANALYSIS; MICROMETASTASIS; MOUSE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NUCLEOTIDE SEQUENCE; OSTEOSARCOMA; OSTEOSARCOMA CELL LINE; OVERALL SURVIVAL; PRIMARY CELL LINE; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR INVASION; UPREGULATION; ANIMAL; BIOSYNTHESIS; BLOOD; BONE TUMOR; CANCER TRANSPLANTATION; CELL MOTION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HIGH THROUGHPUT SCREENING; LUNG TUMOR; METABOLISM; MOLECULAR GENETICS; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; SCID MOUSE; SECONDARY; TUMOR CELL LINE;

ANIMALS; ANOIKIS; BASE SEQUENCE; BONE NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINES, CXC; DNA METHYLATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HIGH-THROUGHPUT SCREENING ASSAYS; HOMEODOMAIN PROTEINS; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED NOD; MICE, SCID; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NF-KAPPA B; OSTEOSARCOMA; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; RNA, NEOPLASM; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84929012059     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI78437     Document Type: Article

References (69)

1. Siegel HJ, Pressey JG. Current concepts on the surgical and medical management of osteosarcoma. Expert Rev Anticancer Ther. 2008;8(8):1257-1269.
2. Esteller M. Epigenetics in cancer. N Engl J Med. 2008;358(11):1148-1159.
3. Al-Romaih K, Sadikovic B, Yoshimoto M, Wang Y, Zielenska M, Squire JA. Decitabine-induced demethylation of 5′ CpG island in GADD45A leads to apoptosis in osteosarcoma cells. Neoplasia. 2008;10(5):471.
4. Al-Romaih K, et al. Modulation by decitabine of gene expression and growth of osteosarcoma U2OS cells in vitro and in xenografts: Identification of apoptotic genes as targets for demethylation. Cancer Cell Int. 2007;7(1):14.
5. Cavodeassi F, Modolell J, Gómez-Skarmeta JL. The Iroquois family of genes: from body building to neural patterning. Development. 2001;128(15):2847-2855.
6. Guo X, et al. Homeobox gene IRX1 is a tumor suppressor gene in gastric carcinoma. Oncogene. 2010;29(27):3908-3920.
7. Bennett KL, et al. Frequently methylated tumor suppressor genes in head and neck squamous cell carcinoma. Cancer Res. 2008;68(12):4494-4499.
8. Zulch A, Becker MB, Gruss P. Expression pattern of Irx1 and Irx2 during mouse digit development. Mech Dev. 2001;106(1-2):159-162.
9. Miller NH, et al. Linkage analysis of genetic loci for kyphoscoliosis on chromosomes 5p13, 13q13.3, and 13q32. Am J Med Genet A. 2006;140(10):1059-1068.
10. Selvarajah S, et al. Identification of cryptic microaberrations in osteosarcoma by high-definition oligonucleotide array comparative genomic hybridization. Cancer Genet Cytogenet. 2007;179(1):52-61.
11. Hromas R, et al. Cloning of BRAK, a novel divergent CXC chemokine preferentially expressed in normal versus malignant cells. Biochem Biophys Res Commun. 1999;255(3):703-706.
12. Frederick MJ, et al. In Vivo Expression of the Novel CXC Chemokine BRAK in Normal and Cancerous Human Tissue. Am J Pathol. 2000;156(6):1937-1950.
13. Schwarze SR, Luo J, Isaacs WB, Jarrard DF. Modulation of CXCL14 (BRAK) expression in prostate cancer. Prostate. 2005;64(1):67-74.
14. Ozawa S, Kato Y, Komori R, Maehata Y, Kubota E, Hata R. BRAK/CXCL14 expression suppresses tumor growth in vivo in human oral carcinoma cells. Biochem Biophys Res Commun. 2006;348(2):406-412.
15. Allinen M, et al. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell. 2004;6(1):17-32.
16. Oler G, Camacho CP, Hojaij FC, Michaluart P, Riggins GJ, Cerutti JM. Gene expression profiling of papillary thyroid carcinoma identifies transcripts correlated with BRAF mutational status and lymph node metastasis. Clin Cancer Res. 2008;14(15):4735-4742.
17. Wente MN, et al. CXCL14 expression and potential function in pancreatic cancer. Cancer Lett. 2008;259(2):209-217.
18. Zeng J, et al. Chemokine CXCL14 is associated with prognosis in patients with colorectal carcinoma after curative resection. J Transl Med. 2013;11(1):6.
19. Lu J, et al. [Expression of chemokine CXCL14 in primary osteosarcoma and its association with prognosis]. Nan Fang Yi Ke Da Xue Xue Bao. 2013;33(6):798-803.
20. Zou CY, et al. Establishment and characteristics of two syngeneic human osteosarcoma cell lines from primary tumor and skip metastases. Acta Pharmacol Sin. 2008;29(3):325-332.
21. Tan P, et al. Expression and prognostic relevance of PRAME in primary osteosarcoma. Biochem Biophys Res Commun. 2012;419(4):801-808.
22. Luu HH, et al. An orthotopic model of human osteosarcoma growth and spontaneous pulmonary metastasis. Clin Exp Metastasis. 2005;22(4):319-329.
23. Detich N, Hamm S, Just G, Knox JD, Szyf M. The methyl donor S-Adenosylmethionine inhibits active demethylation of DNA: a candidate novel mechanism for the pharmacological effects of S-Adenosylmethionine. J Biol Chem. 2003;278(23):20812-20820.
24. Simpson CD, Anyiwe K, Schimmer AD. Anoikis resistance and tumor metastasis. Cancer Lett. 2008;272(2):177-185.
25. Kim YN, Koo KH, Sung JY, Yun UJ, Kim H. Anoikis resistance: an essential prerequisite for tumor metastasis. Int J Cell Biol. 2012;2012:306879.
26. Bilioni A, Craig G, Hill C, McNeill H. Iroquois transcription factors recognize a unique motif to mediate transcriptional repression in vivo. Proc Natl Acad Sci U S A. 2005;102(41):14671-14676.
27. Zhao Z, et al. Downregulation of MCT1 inhibits tumor growth, metastasis and enhances chemotherapeutic efficacy in osteosarcoma through regulation of the NF-kappaB pathway. Cancer Lett. 2014;342(1):150-158.
28. Tang QL, et al. Glycogen synthase kinase-3beta, NF-kappaB signaling, and tumorigenesis of human osteosarcoma. J Natl Cancer Inst. 2012;104(10):749-763.
29. Safa AR. c-FLIP, a master anti-apoptotic regulator. Exp Oncol. 2012;34(3):176-184.
30. Micheau O, Lens S, Gaide O, Alevizopoulos K, Tschopp J. NF-kappaB signals induce the expression of c-FLIP. Mol Cell Biol. 2001;21(16):5299-5305.
31. Park SH, Riley Pt, Frisch SM. Regulation of anoikis by deleted in breast cancer-1 (DBC1) through NF-kappaB. Apoptosis. 2013;18(8):949-962.
32. Pierce JW, et al. Novel inhibitors of cytokine-induced IkappaBalpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J Biol Chem. 1997;272(34):21096-21103.
33. Schwarzenbach H, Hoon DS, Pantel K. Cell-free nucleic acids as biomarkers in cancer patients. Nat Rev Cancer. 2011;11(6):426-437.
34. Müller HM, Fiegl H, Widschwendter A, Widschwendter M. Prognostic DNA methylation marker in serum of cancer patients. Ann N Y Acad Sci. 2004;1022(1):44-49.
35. Gupta GP, Massagué J. Cancer metastasis: building a framework. Cell. 2006;127(4):679-695.
36. Nguyen DX, Massagué J. Genetic determinants of cancer metastasis. Nat Rev Genet. 2007;8(5):341-352.
37. Rodenhiser DI. Epigenetic contributions to cancer metastasis. Clin Exp Metastasis. 2009;26(1):5-18.
38. Adamowicz M, et al. Frequent amplifications and abundant expression of TRIO, NKD2, and IRX2 in soft tissue sarcomas. Genes Chromosomes Cancer. 2006;45(9):829-838.
39. Asaka S, Fujimoto T, Akaishi J, Ogawa K, Onda M. Genetic prognostic index influences patient outcome for node-positive breast cancer. Surg Today. 2006;36(9):793-801.
40. Myrthue A, et al. The iroquois homeobox gene 5 is regulated by 1,25-dihydroxyvitamin D3 in human prostate cancer and regulates apoptosis and the cell cycle in LNCaP prostate cancer cells. Clin Cancer Res. 2008;14(11):3562-3570.
41. Nguyen HH, et al. IRX4 at 5p15 suppresses prostate cancer growth through the interaction with vitamin D receptor, conferring prostate cancer susceptibility. Hum Mol Genet. 2012;21(9):2076-2085.
42. Bosch-Presegue L, Vaquero A. The dual role of sirtuins in cancer. Genes Cancer. 2011;2(6):648-662.
43. Robbs BK, Cruz AL, Werneck MB, Mognol GP, Viola JP. Dual roles for NFAT transcription factor genes as oncogenes and tumor suppressors. Mol Cell Biol. 2008;28(23):7168-7181.
44. Su Y, et al. Insulin-like growth factor binding protein 5 suppresses tumor growth and metastasis of human osteosarcoma. Oncogene. 2011;30(37):3907-3917.
45. Butt AJ, Dickson KA, McDougall F, Baxter RC. Insulin-like growth factor-binding protein-5 inhibits the growth of human breast cancer cells in vitro and in vivo. J Biol Chem. 2003;278(32):29676-29685.
46. Xu C, et al. Regulation of global gene expression in the bone marrow microenvironment by androgen: androgen ablation increases insulin-like growth factor binding protein-5 expression. Prostate. 2007;67(15):1621-1629.
47. Itoh M, Kudoh T, Dedekian M, Kim CH, Chitnis AB. A role for iro1 and iro7 in the establishment of an anteroposterior compartment of the ectoderm adjacent to the midbrain-hindbrain boundary. Development. 2002;129(10):2317-2327.
48. Matsumoto K, et al. The prepattern transcription factor Irx2, a target of the FGF8/MAP kinase cascade, is involved in cerebellum formation. Nat Neurosci. 2004;7(6):605-612.
49. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer. 2004;4(7):540-550.
50. Sun X, et al. CXCL12 / CXCR4 / CXCR7 chemokine axis and cancer progression. Cancer Metastasis Rev. 2010;29(4):709-722.
51. Balkwill FR. The chemokine system and cancer. J Pathol. 2012;226(2):148-157.
52. Pelicano H, et al. Mitochondrial dysfunction and reactive oxygen species imbalance promote breast cancer cell motility through a CXCL14-mediated mechanism. Cancer Res. 2009;69(6):2375-2383.
53. O'Dea E, Hoffmann A. NF-kappaB signaling. Wiley Interdiscip Rev Syst Biol Med. 2009;1(1):107-115.
54. Razin A, Riggs AD. DNA methylation and gene function. Science. 1980;210(4470):604-610.
55. Razin A, Cedar H. DNA methylation and gene expression. Microbiol Rev. 1991;55(3):451-458.
56. Wajed SA, Laird PW, DeMeester TR. DNA methylation: an alternative pathway to cancer. Ann Surg. 2001;234(1):10-20.
57. Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene. 2002;21(35):5400-5413.
58. Ehrlich M. DNA hypomethylation in cancer cells. Epigenomics. 2009;1(2):239-259.
59. Egger G, Liang G, Aparicio A, Jones PA. Epigenetics in human disease and prospects for epigenetic therapy. Nature. 2004;429(6990):457-463.
60. Delle Chiaie R, Pancheri P, Scapicchio P. Efficacy and tolerability of oral and intramuscular S-adenosyl-L-methionine 1,4-butanedisulfonate (SAMe) in the treatment of major depression: comparison with imipramine in 2 multicenter studies. Am J Clin Nutr. 2002;76(5):1172S-1176S.
61. Najm WI, Reinsch S, Hoehler F, Tobis JS, Harvey PW. S-adenosyl methionine (SAMe) versus celecoxib for the treatment of osteoarthritis symptoms: a double-blind cross-over trial. [ISRCTN36233495]. BMC Musculoskelet Disord. 2004;5(1):6.
62. Mato JM, Lu SC. Role of S-adenosyl-L-methionine in liver health and injury. Hepatology. 2007;45(5):1306-1312.
63. Pakneshan P, Szyf M, Farias-Eisner R, Rabbani SA. Reversal of the hypomethylation status of urokinase (uPA) promoter blocks breast cancer growth and metastasis. J Biol Chem. 2004;279(30):31735-31744.
64. Shukeir N, Pakneshan P, Chen G, Szyf M, Rabbani SA. Alteration of the methylation status of tumor-promoting genes decreases prostate cancer cell invasiveness and tumorigenesis in vitro and in vivo. Cancer Res. 2006;66(18):9202-9210.
65. Alix-Panabieres C, Schwarzenbach H, Pantel K. Circulating tumor cells and circulating tumor DNA. Annu Rev Med. 2012;63:199-215.
66. Sidransky D. Emerging molecular markers of cancer. Nat Rev Cancer. 2002;2(3):210-219.
67. Laird PW. The power and the promise of DNA methylation markers. Nat Rev Cancer. 2003;3(4):253-266.
68. Tang QL, et al. Salinomycin inhibits osteosarcoma by targeting its tumor stem cells. Cancer Lett. 2011;311(1):113-121.
69. Su Y, et al. Establishment and characterization of a new highly metastatic human osteosarcoma cell line. Clin Exp Metastasis. 2009;26(7):599-610.