Epigenetic silencing of MAL, a putative tumor suppressor gene, can contribute to human epithelium cell carcinoma

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Cao, Wei ^a,b   Zhang, Zhi yuan ^a,b   Xu, Qin ^a,b   Sun, Qiang ^a,b   Yan, Ming ^a,b   Zhang, Jun ^a,b   Zhang, Ping ^a,b   Han, Ze guang ^b,c   Chen, Wan tao ^a,b  

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

^b Shanghai Research Institute of Stomatology   (China)

^c CHINESE NATIONAL HUMAN GENOME CENTER AT SHANGHAI   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MATRIGEL; MESSENGER RNA; CARRIER PROTEIN; MAL PROTEIN, T CELL; MAL PROTEIN, T-CELL; MYELIN PROTEIN; PROTEOLIPID;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL INVASION; CELL PROLIFERATION; CPG ISLAND; DNA SEQUENCE; DOWN REGULATION; GENE EXPRESSION; GENE SILENCING; GENE TRANSFER; HEAD AND NECK CARCINOMA; HUMAN; HUMAN CELL; MOUSE; MYELIN AND LYMPHOCYTE ASSOCIATED GENE; NONHUMAN; PHENOTYPE; PROMOTER REGION; SQUAMOUS CELL CARCINOMA; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; CARCINOMA; CONFOCAL MICROSCOPY; DNA METHYLATION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HEAD AND NECK TUMOR; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; CARCINOMA; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HUMANS; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, CONFOCAL; MYELIN PROTEINS; NEOPLASMS, SQUAMOUS CELL; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; PROTEOLIPIDS; RNA, MESSENGER;

EID: 78549250768     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-296     Document Type: Article

References (40)

1. Mignogna MD, Fedele S, Lo Russo L. The World Cancer Report and the burden of oral cancer. Eur J Cancer Prev 2004, 13(2):139-142. 10.1097/00008469-200404000-00008, 15100581.
2. Mohr S, Leikauf GD, Keith G, Rihn BH. Microarrays as cancer keys: an array of possibilities. J Clin Oncol 2002, 20(14):3165-3175. 10.1200/JCO.2002.12.073, 12118031.
3. Alevizos I, Mahadevappa M, Zhang X, Ohyama H, Kohno Y, Posner M, Gallagher GT, Varvares M, Cohen D, Kim D. Oral cancer in vivo gene expression profiling assisted by laser capture microdissection and microarray analysis. Oncogene 2001, 20(43):6196-6204. 10.1038/sj.onc.1204685, 11593428.
4. Belbin TJ, Singh B, Smith RV, Socci ND, Wreesmann VB, Sanchez-Carbayo M, Masterson J, Patel S, Cordon-Cardo C, Prystowsky MB. Molecular profiling of tumor progression in head and neck cancer. Archives of otolaryngology-head & neck surgery 2005, 131(1):10-18.
5. Carles A, Millon R, Cromer A, Ganguli G, Lemaire F, Young J, Wasylyk C, Muller D, Schultz I, Rabouel Y. Head and neck squamous cell carcinoma transcriptome analysis by comprehensive validated differential display. Oncogene 2006, 25(12):1821-1831. 10.1038/sj.onc.1209203, 16261155.
6. Chin D, Boyle GM, Williams RM, Ferguson K, Pandeya N, Pedley J, Campbell CM, Theile DR, Parsons PG, Coman WB. Novel markers for poor prognosis in head and neck cancer. Int J Cancer 2005, 113(5):789-797. 10.1002/ijc.20608, 15499618.
7. Kuriakose MA, Chen WT, He ZM, Sikora AG, Zhang P, Zhang ZY, Qiu WL, Hsu DF, McMunn-Coffran C, Brown SM, Elango EM, Delacure MD, Chen FA. Selection and validation of differentially expressed genes in head and neck cancer. CMLS, Cell Mol Life Sc 2004, 61(11):1372-1383.
8. Mimori K, Shiraishi T, Mashino K, Sonoda H, Yamashita K, Yoshinaga K, Masuda T, Utsunomiya T, Alonso MA, Inoue H, Mori M. MAL gene expression in esophageal cancer suppresses motility, invasion and tumorigenicity and enhances apoptosis through the Fas pathway. Oncogene 2003, 22(22):3463-3471. 10.1038/sj.onc.1206378, 12776198.
9. Lind GE, Ahlquist T, Kolberg M, Berg M, Eknaes M, Alonso MA, Kallioniemi A, Meling GI, Skotheim RI, Rognum TO, Thiis-Evensen E, Lothe RA. Hypermethylated MAL gene - a silent marker of early colon tumorigenesis. J Transl Med 2008, 6:13. 10.1186/1479-5876-6-13, 2292685, 18346269.
10. Buffart TE, Overmeer RM, Steenbergen RD, Tijssen M, Van Grieken NC, Snijders PJ, Grabsch HI, Van de Velde CJ, Carvalho B, Meijer GA. MAL promoter hypermethylation as a novel prognostic marker in gastric cancer. Br J Cancer 2008, 99(11):1802-1807. 10.1038/sj.bjc.6604777, 2600687, 19002170.
11. Horne HN, Lee PS, Murphy SK, Alonso MA, Olson JA, Marks JR. Inactivation of the MAL gene in breast cancer is a common event that predicts benefit from adjuvant chemotherapy. Mol Cancer Res 2009, 7(2):199-209. 10.1158/1541-7786.MCR-08-0314, 2700346, 19208741.
12. Hatta M, Nagai H, Okino K, Onda M, Yoneyama K, Ohta Y, Nakayama H, Araki T, Emi M. Down-regulation of members of glycolipid-enriched membrane raft gene family, MAL and BENE, in cervical squamous cell cancers. J Obstet Gynaecol Res 2004, 30(1):53-58. 10.1111/j.1341-8076.2004.00156.x, 14718022.
13. Maruya S, Kim HW, Weber RS, Lee JJ, Kies M, Luna MA, Batsakis JG, El-Naggar AK. Gene expression screening of salivary gland neoplasms: molecular markers of potential histogenetic and clinical significance. J Mol Diagn 2004, 6(3):180-90. 1867638, 15269293.
14. Alonso MA, Weissman SM. cDNA cloning and sequence of MAL, a hydrophobic protein associated with human T-cell differentiation. Proc Natl Acad Sic USA 1987, 84(7):1997-2001.
15. Kim T, Fiedler K, Madison DL, Krueger WH, Pfeiffer SE. Cloning and characterization of MVP17: a developmentally regulated myelin protein in oligodendrocytes. J Neurosci Res 1995, 42(3):413-422. 10.1002/jnr.490420316, 8583510.
16. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997, 387(6633):569-572. 10.1038/42408, 9177342.
17. Cheong KH, Zacchetti D, Schneeberger EE, Simons K. VIP17/MAL, a lipid raft-associated protein, is involved in apical transport in MDCK cells. Pro Natl Acad Sci USA 1999, 96(11):6241-6248.
18. Puertollano R, Martín-Belmonte F, Millán J, de Marco MC, Albar JP, Kremer L, Alonso MA. The MAL proteolipid is necessary for normal apical transport and accurate sorting of the influenza virus hemagglutinin in Madin-Darby canine kidney cells. J Cell Biol 1999, 145(1):141-151. 10.1083/jcb.145.1.141, 2148211, 10189374.
19. Wong YF, Cheung TH, Tsao GS, Lo KW, Yim SF, Wang VW, Heung MM, Chan SC, Chan LK, Ho TW, Wong KW, Guo Y, Chung TK, Smith DI. Genome-wide gene expression profiling of cervical cancer in Hong Kong women by oligonucleotide microarray. Int J Cancer 2006, 118(10):2461-2469. 10.1002/ijc.21660, 16353136.
20. Mori Y, Cai K, Cheng Y, Wang S, Paun B, Hamilton JP, Jin Z, Sato F, Berki AT, Kan T, Ito T, Mantzur C, Abraham JM, Meltzer SJ. A Genome-wide search identifies epigenetic sliencing of somatostain, tachykinin-1 and 5 other genes in colon cancer. Gastroenterology 2006, 131(3):797-808. 10.1053/j.gastro.2006.06.006, 16952549.
21. Beder LB, Gunduz M, Hotomi M, Fujihara K, Shimada J, Tamura S, Gunduz E, Fukushima K, Yaykasli K, Grenman R, Shimizu K, Yamanaka N. T-lymphocyte maturation-associated protein gene as a candidate metastasis suppressor for head and neck squamous cell carcinomas. Cancer Sci 2009, 100(5):873-880. 10.1111/j.1349-7006.2009.01132.x, 19445022.
22. Berchuck A, Iversen ES, Luo J, Clarke JP, Horne H, Levine DA, Boyd J, Alonso MA, Secord AA, Bernardini MQ, Barnett JC, Boren T, Murphy SK, Dressman HK, Marks JR, Lancaster JM. Microarray analysis of early stage serous ovarian cancers shows profiles predictive of favorable outcome. Clin Cancer Res 2009, 15(7):2448-2455. 10.1158/1078-0432.CCR-08-2430, 19318476.
23. Rancaño C, Rubio T, Alonso MA. Alternative splicing of human T-cell-specific MAL mRNA and its correlation with the exon/intron organization of the gene. Genomics 1994, 21(2):447-450. 10.1006/geno.1994.1294, 8088843.
24. Herman JG, Graff JR, Myöhänen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996, 93(18):9821-9826. 10.1073/pnas.93.18.9821, 38513, 8790415.
25. Boulares AH, Yakovlev AG, Ivanova V, Stoica BA, Wang G, Iyer S, Smulson M. Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J Biol Chem 1999, 274(33):22932-22940. 10.1074/jbc.274.33.22932, 10438458.
26. Tomioka H, Morita K, Hasegawa S, Omura K. Gene expression analysis by cDNA microarray in oral squamous cell carcinoma. J Oral Pathol Med 2006, 35(4):206-211. 10.1111/j.1600-0714.2006.00410.x, 16519767.
27. Ziober AF, Patel KR, Alawi F, Gimotty P, Weber RS, Feldman MM, Chalian AA, Weinstein GS, Hunt J, Ziober BL. Identification of a gene signature for rapid screening of oral squamous cell carcinoma. Clin Cancer Res 2006, 12(20 Pt 1):5960-5971. 10.1158/1078-0432.CCR-06-0535, 17062667.
28. Ye H, Yu T, Temam S, Ziober BL, Wang J, Schwartz JL, Mao L, Wong DT, Zhou X. Transcriptomic dissection of tongue squamous cell carcinoma. BMC Genomics 2008, 9:69. 10.1186/1471-2164-9-69, 2262071, 18254958.
29. Choi P, Jordan CD, Mendez E, Houck J, Yueh B, Farwell DG, Futran N, Chen C. Examination of oral cancer biomarkers by tissue microarray analysis. Arch Otolaryngol Head Neck Surg 2008, 134(5):539-546. 10.1001/archotol.134.5.539, 2578846, 18490578.
30. Marte B, Eccleston A, Nath D. Molecular cancer diagnostics. Nature 2008, 452(7187):547. 10.1038/452547a, 18385727.
31. Lallemant B, Evrard A, Combescure C, Chapuis H, Chambon G, Raynal C, Reynaud C, Sabra O, Joubert D, Hollande F, Lallemant JG, Lumbroso S, Brouillet JP. Clinical relevance of nine transcriptional molecular markers for the diagnosis of head and neck squamous cell carcinoma in tissue and saliva rinse. BMC Cancer 2009, 9:370. 10.1186/1471-2407-9-370, 2767357, 19835631.
32. Martín-Belmonte F, Arvan P, Alonso MA. MAL mediates apical transport of secretory proteins in polarized epithelial Madin-Darby canine kidney cells. J Biol Chem 2001, 276(52):49337-49342. 10.1074/jbc.M106882200, 11673461.
33. Martín-Belmonte F, Puertollano R, Millán J, Alonso MA. The MAL proteolipid is necessary for the overall apical delivery of membrane proteins in the polarized epithelial Madin-Darby canine kidney and fischer rat thyroid cell lines. Mol Biol Cell 2000, 11(6):2033-2045. 14901, 10848627.
34. O'Regan EM, Toner ME, Finn SP, Fan CY, Ring M, Hagmar B, Timon C, Smyth P, Cahill S, Flavin R, Sheils OM, O'Leary JJ. p16(INK4A) genetic and epigenetic profiles differ in relation to age and site in head and neck squamous cell carcinomas. Hum Pathol 2008, 39(3):452-458. 10.1016/j.humpath.2007.08.004, 18261630.
35. Konrad M, Saunier S, Heidet L, Silbermann F, Benessy F, Calado J, Le Paslier D, Broyer M, Gubler MC, Antignac C. Large homozygous deletions of the 2q13 region are a major cause of juvenile nephronophthisis. Hum Mol Genet 1996, 5(3):367-371. 10.1093/hmg/5.3.367, 8852662.
36. Overmeer RM, Henken FE, Bierkens M, Wilting SM, Timmerman I, Meijer CJ, Snijder PJ, Steenbergen RD. Repression of MAL tumour suppressor activity by promoter methylation during cervical carcinogenesis. J Pathol 2009, 219(3):327-336. 10.1002/path.2598, 19662663.
37. Lee PS, Teaberry VS, Bland AE, Huang Z, Whitaker RS, Baba T, Fujii S, Secord AA, Berchuck A, Murphy SK. Elevated MAL expression is accompanied by promoter hypomethylation and platinum resistance in epithelial ovarian cancer. Int J Cancer 2010, 126(6):1378-1389.
38. Ahlquist T, Lind GE, Costa VL, Meling GI, Vatn M, Hoff GS, Rognum TO, Skotheim RI, Thiis-Evensen E, Lothe RA. Gene methylation profiles of normal mucosa, and benign and malignant colorectal tumors identify early onset markers. Mol Cancer 2008, 7:94. 10.1186/1476-4598-7-94, 2639620, 19117505.
39. Sobin LH, Fleming ID. TNM Classification of Malignant Tumors, fifth edition (1997). Union Internationale Contre le Cancer and the American Joint Committee on Cancer. Cancer 1997, 80(9):1803-1804. 10.1002/(SICI)1097-0142(19971101)80:9<1803::AID-CNCR16>3.0.CO;2-9, 9351551.
40. Loiaconi G, Berth AF. Current aspects of histological typing of carcinomas of the oral cavity. Riv Ital Stomatol 1982, 51(5):415-421.