Identification of an invasion and tumor-suppressing gene, Endoglin (ENG), silenced by both epigenetic inactivation and allelic loss in esophageal squamous cell carcinoma

International Journal of Cancer

Volumn 123, Issue 12, 2008, Pages 2816-2823

  Wong, Victor Chun Lam ^a   Pui, Ling Chan ^a   Bernabeu, Carmelo ^b   Law, Simon ^c   Li, Dong Wang ^d   Li, Ji N ^e   Sai, Wah Tsao ^c   Srivastava, Gopesh ^c   Lung, Maria Li ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d THE FIRST AFFILIATED HOSPITAL OF ZHENGZHOU UNIVERSITY   (China)

^e Yaocun Esophageal Cancer Hospital   (China)

Author keywords

Endoglin; Esophageal squamous cell carcinoma; Invasion; Loss of heterozygosity; Methylation; Tumorigenesis

Indexed keywords

ENDOGLIN;

ADULT; AGED; ALLELE; ARTICLE; CANCER CELL CULTURE; CHINA; CLINICAL ARTICLE; EPIGENETICS; ESOPHAGUS CARCINOMA; FEMALE; GENE EXPRESSION; GENE SILENCING; HONG KONG; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; PRIORITY JOURNAL; SQUAMOUS CELL CARCINOMA;

AGED; ANTIGENS, CD; BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL PROLIFERATION; CHINA; COLLAGEN; DNA METHYLATION; DOWN-REGULATION; DRUG COMBINATIONS; ESOPHAGEAL NEOPLASMS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HONG KONG; HUMANS; LAMININ; LOSS OF HETEROZYGOSITY; LYMPHATIC METASTASIS; MALE; MICROSATELLITE REPEATS; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PLASMIDS; PROMOTER REGIONS, GENETIC; PROTEOGLYCANS; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SURVIVAL ANALYSIS; TRANSFECTION; TUMOR STEM CELL ASSAY; TUMOR SUPPRESSOR PROTEINS;

EID: 57349117010     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23882     Document Type: Article

References (50)

1. Li JY. Epidemiology of esophageal cancer in China. Natl Cancer Inst Monogr 1982;62:113-20.
2. Xibib S, Meilan H, Moller H, Evans HS, Dixin D, Wenjie D, Jianbang L. Risk factors for oesophageal cancer in Linzhou. China: a case-control study. Asian Pac J Cancer Prev 2003;4:119-24.
3. Ah-See KW, Cooke TG, Pickford IR, Soutar D, Balmain A. An allelo-type of squamous carcinoma of the head and neck using microsatellite markers. Cancer Res 1994;54:1617-21.
4. Merlo A, Gabrielson E, Askin F, Sidransky D. Frequent loss of chromosome 9 in human primary non-small cell lung cancer. Cancer Res 1994;54:640-2.
5. Ko JM, Wong CP, Tang CM, Lau KW, Lung ML. Frequent loss of heterozygosity on multiple chromosomes in Chinese esophageal squamous cell carcinomas. Cancer Lett 2001;170:131-8.
6. Sanz-Ortega J, Hernandez S, Saez MC, Sierra E, Sanz-Ortega G, Torres A, Balibrea JL, Sanz-Esponera J, Merino MJ. 3p21, 5q21, 9p21 and 17p13.1 allelic deletions are potential markers of individuals with a high risk of developing adenocarcinoma in Barrett's epithelium without dysplasia. Hepatogastroenterology 2003;50:404-7.
7. Yang LC, Tang CMC, Lau KW, Lung ML. Frequent loss of heterozygosity on chromosome 9 in Chinese esophageal squamous cell carcinomas. Cancer Lett 2004;203:71-7.
8. Yang L, Leung AC, Ko JM, Lo PH, Tang JC, Srivastava G, Oshimura M, Stanbridge EJ, Daigo Y, Nakamura Y, Tang CM, Lau KW, et al. Tumor suppressive role of a 2.4 Mb 9q33-q34 critical region and DEC1 in esophageal squamous cell carcinoma. Oncogene 2005;24:697-705.
9. Leung AC, Wong VC, Yang LC, Chan PL, Daigo Y, Nakamura Y, Qi RZ, Miller LD, Liu ET, Wang LD, Li JL, Law S, et al. Frequent decreased expression of candidate tumor suppressor gene. DEC1, and its anchorage-independent growth properties and impact on global gene expression in esophageal carcinoma. Int J Cancer 2008;122:587-94.
10. Fernandez-Ruiz E, St-Jacques S, Bellon T, Letarte M, Bernabeu C. Assignment of the human endoglin gene (END) to 9q34->qter. Cytogenet Cell Genet 1993;64:204-7.
11. McAllister KA, Grogg KM, Johnson DW, Gallione CJ, Baldwin MA, Jackson CE, Helmbold EA, Markel DS, McKinnon WC, Murrell J, McCormick MK, Pericak-Vance MA, et al. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet 1994;8:345-51.
12. Rius C, Smith JD, Almendro N, Langa C, Botella LM, Marchuk DA, Vary CP, Bernabeu C. Cloning of the promoter region of human endoglin, the target gene for hereditary hemorrhagic telangiectasia type 1. Blood 1998;92:4677-90.
13. Gougos A, Letarte M. Primary structure of endoglin, an RGD-containing glycoprotein of human endothelial cells. J Biol Chem 1990;265:8361-4.
14. Bellon T, Corbi A, Lastres P, Cales C, Cebrian M, Vera S, Cheifetz S, Massague J, Letarte M, Bernabeu C. Identification and expression of two forms of the human transforming growth factor-beta-binding protein endoglin with distinct cytoplasmic regions. Eur J Immunol 1993;23:2340-5.
15. Botella LM, Sánchez-Elsner T, Sanz-Rodriguez F, Kojima S, Shimada J, Guerrero-Esteo M, Cooreman MP, Ratziu V, Langa C, Vary CP, Ramirez JR, Friedman S, et al. Transcriptional activation of endoglin and transforming growth factor-beta signaling components by cooperative interaction between Sp1 and KLF6: their potential role in the response to vascular injury. Blood 2002;100:4001-10.
16. Sánchez-Elsner T, Botella LM, Velasco B, Langa C, Bernabéu C. Endoglin expression is regulated by transcriptional cooperation between the hypoxia and transforming growth factor-beta pathways. J Biol Chem 2002;277:43799-808.
17. Cheifetz S, Bellon T, Cales C, Vera S, Bernabeu C, Massague J, Letarte M. Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. J Biol Chem 1992;267:19027-30.
18. Bernabeu C, Conley BA, Vary CP. Novel biochemical pathways of endoglin in vascular cell physiology. J Cell Biochem 2007;102:1375-88.
19. Li DY, Sorensen LK, Brooke BS, Urness LD, Davis EC, Taylor DG, Boak BB, Wendel DP. Defective angiogenesis in mice lacking endoglin. Science 1999;284:1534-7.
20. Pece N, Vera S, Cymerman U, White RIJ, Wrana JL, Letarte M. Mutant endoglin in hereditary hemorrhagic telangiectasia type 1 is transiently expressed intracellularly and is not a dominant negative. J Clin Invest 1997;100:2568-79.
21. Liu Y, Jovanovic B, Pins M, Lee C, Bergan RC. Over expression of endoglin in human prostate cancer suppresses cell detachment, migration and invasion. Oncogene 2002;21:8272-81.
22. Duff SE, Li C, Garland JM, Kumar S. CD105 is important for angiogenesis: evidence and potential applications. FASEB J 2003;17:984-92.
23. Fonsatti E, Altomonte M, Nicotra MR, Natali PG, Maio M. Endoglin (CD105): a powerful therapeutic target on tumor-associated angiogenetic blood vessels. Oncogene 2003;22:6557-63.
24. Fonsatti E, Del Vecchio L, Altomonte M, Sigalotti L, Nicotra MR, Coral S, Natali PG, Maio M. Endoglin: An accessory component of the TGF-beta-binding receptor-complex with diagnostic, prognostic, and bioimmunotherapeutic potential in human malignancies. J Cell Physiol 2001;188:1-7.
25. Sandlund J, Hedberg Y, Bergh A, Grankvist K, Ljungberg B, Rasmuson T. Endoglin (CD105) expression in human renal cell carcinoma. BJU Int 2006;97:706-10.
26. Li SL, Gao DL, Zhao ZH, Liu ZW, Zhao QM, Yu JX, Chen KS, Zhang YH. Correlation of matrix metalloproteinase suppressor genes RECK. VEGF, and. CD105 with angiogenesis and biological behavior in esophageal squamous cell carcinoma. World J Gastroenterol 2007;13:6076-81.
27. Bellone G, Solerio D, Chiusa L, Brondino G, Carbone A, Prati A, Scirelli T, Camandona M, Palestro G, Dei Poli M. Transforming growth factor-beta binding receptor endoglin (CD105) expression in esophageal cancer and in adjacent nontumorous esophagus as prognostic predictor of recurrence. Ann Surg Oncol 2007;14:3232-42.
28. Guerrero-Esteo M, Lastres P, Letamendia A, Perez-Alvarez MJ, Langa C, Lopez LA, Fabra A, Garcia-Pardo A, Vera S, Letarte M, Bernabeu C. Endoglin overexpression modulates cellular morphology, migration, and adhesion of mouse fibroblasts. Eur J Cell Biol 1999;78:614-23.
29. Craft CS, Romero D, Vary CP, Bergan RC. Endoglin inhibits prostate cancer motility via activation of the ALK2-Smad1 pathway. Oncogene 2007;26:7240-50.
30. Perez-Gomez E, Villa-Morales M, Santos J, Fernandez-Piqueras J, Gamallo C, Dotor J, Bernabeu C, Quintanilla M. A role for endoglin as a suppressor of malignancy during mouse skin carcinogenesis. Cancer Res 2007;67:10268-77.
31. Tang JC, Wan TS, Wong N, Pang E, Lam KY, Law SY, Chow LM, Ma ES, Chan LC, Wong J, Srivastava G. Establishment and characterization of a new xenograft-derived human esophageal squamous cell carcinoma cell line SLMT-1 of Chinese origin. Cancer Genet Cytogenet 2001;124:36-41.
32. Deng W, Tsao SW, Guan XY, Lucas JN, Si HX, Leung CS, Mak P, Wang LD, Cheung AL. Distinct profiles of critically short telomeres are a key determinant of different chromosome aberrations in immortalized human cells: whole-genome evidence from multiple cell lines. Oncogene 2004;23:9090-101.
33. Mok CH, Chew EC, Riches DJ, Lee JC, Huang DP, Hadgis C, Crofts TJ. Biological characteristics of a newly established human oesophageal carcinoma cell line. Anticancer Res 1987;7:409-15.
34. Pan QQ. Studies on esophageal cancer cells in vitro. Proc Chin Acad Med Sci Peking Union Med Coll 1989;4:52-7.
35. Hu YC, Lam KY, Law SY, Wan TS, Ma ES, Kwong YL, Chan LC, Wong J, Srivastava G. Establishment, characterization, karyotyping, and comparative genomic hybridization analysis of HKESC-2 and HKESC-3: two newly established human esophageal squamous cell carcinoma cell lines. Cancer Genet Cytogenet 2002;135:120-7.
36. Hu CP, Hsieh HG, Chien KY, Wang PY, Wang CI, Chen CY, Lo SJ, Wu KD, Chang CM. Biologic properties of three newly established human esophageal carcinoma cell lines. J Natl Cancer Inst 1984;72:577-83.
37. Shimada Y, Imamura M, Wagata T, Yamaguchi N, Tobe T. Characterization of 21 newly established esophageal cancer cell lines. Cancer 1992;69:277-84.
38. Takahashi K, Kanazawa H, Chan H, Hosono T, Takahara M, Sato K. A case of esophageal carcinoma metastatic to the mandible and characterization of two cell lines (T.T. and T.Tn.). Jpn J Oral Maxillofac Surg 1990;36:307-16.
39. Lo PH, Leung AC, Kwok CY, Cheung WS, Ko JM, Yang LC, Law S, Wang LD, Li J, Stanbridge EJ, Srivastava G, Tang JC, et al. Identification of a tumor suppressive critical region mapping to 3p14.2 in esophageal squamous cell carcinoma and studies of a candidate tumor suppressor gene. ADAMTS9. Oncogene 2007;26:148-57.
40. Lo PH, Leung AC, Xiong W, Law S, Duh FM, Lerman MI, Stanbridge EJ, Lung ML. Expression of candidate chromosome 3p21.3 tumor suppressor genes and down-regulation of BLU in some esophageal squamous cell carcinomas. Cancer Lett 2006;234:184-92.
41. Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 2002;18:1427-31.
42. Lung HL, Cheung AK, Xie D, Cheng Y, Kwong FM, Murakami Y, Guan XY, Sham JS, Chua D, Protopopov AI, Zabarovsky ER, Tsao SW, et al. TSLC1 is a tumor suppressor gene associated with metastasis in nasopharyngeal carcinoma. Cancer Res 2006;66:9385-92.
43. Ko JM, Yau WL, Chan PL, Lung HL, Yang L, Lo PH, Tang JC, Srivastava G, Stanbridge EJ, Lung ML. Functional evidence of decreased tumorigenicity associated with monochromosome transfer of chromosome 14 in esophageal cancer and the mapping of tumor-suppressive regions to 14q32. Genes Chromosomes Cancer 2005;43:284-93.
44. Postiglione L, Di Domenico G, Caraglia M, Marra M, Giuberti G, Del Vecchio L, Montagnani S, Macri M, Bruno EM, Abbruzzese A, Rossi G. Differential expression and cytoplasm/membrane distribution of endoglin (CD105) in human tumour cell lines: Implications in the modulation of cell proliferation. Int J Oncol 2005;26:1193-201.
45. Mori Y, Cai K, Cheng Y, Wang S, Paun B, Hamilton JP, Jin Z, Sato F, Berki AT, Kan T, Ito T, Mantzur C, et al. A genome-wide search identifies epigenetic silencing of somatostatin, tachykinin-1, and 5 other genes in colon cancer. Gastroenterology 2006;131:797-808.
46. Conley BA, Koleva R, Smith JD, Kacer D, Zhang D, Bernabeu C, Vary CP. Endoglin controls cell migration and composition of focal adhesions: function of the cytosolic domain. J Biol Chem 2004;279:27440-9.
47. Quintanilla M, Ramirez JR, Perez-Gomez E, Romero D, Velasco B, Letarte M, Lopez-Novoa JM, Bernabeu C. Expression of the TGF-beta coreceptor endoglin in epidermal keratinocytes and its dual role in multistage mouse skin carcinogenesis. Oncogene 2003;22:5976-85.
48. Wikstrom P, Lissbrant IF, Stattin P, Egevad L, Bergh A. Endoglin (CD105) is expressed on immature blood vessels and is a marker for survival in prostate cancer. Prostate 2002;51:268-75.
49. Minhajat R, Mori D, Yamasaki F, Sugita Y, Satoh T, Tokunaga O. Organ-specific endoglin (CD105) expression in the angiogenesis of human cancers. Pathol Int 2006;56:717-23.
50. El-Gohary YM, Silverman JF, Olson PR, Liu YL, Cohen JK, Miller R, Saad RS. Endoglin (CD105) and vascular endothelial growth factor as prognostic markers in prostatic adenocarcinoma. Am J Clin Pathol 2007;127:572-9.