Reprogramming of the transcriptome in a novel chromosome 3 transfer tumor suppressor ovarian cancer cell line model affected molecular networks that are characteristic of ovarian cancer

Molecular Carcinogenesis

Volumn 48, Issue 7, 2009, Pages 648-661

  Quinn, Michael C J ^a   Filali Mouhim, Abdelali ^b   Provencher, Diane M ^b,c   Mes Masson, Anne Marie ^b,c   Tonin, Patricia N ^a,d,e  

^a MCGILL UNIVERSITY   (Canada)

^b CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^e MONTREAL GENERAL HOSPITAL   (Canada)

Author keywords

Benign ovarian cancer; Chromosome 3; Microarray; Serous ovarian cancer; Tumor suppressor gene

Indexed keywords

OSTEONECTIN; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA; MESSENGER RNA;

ADULT; AGED; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER MODEL; CHROMOSOME 3P; CLINICAL ARTICLE; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; OVARY CANCER; OVARY CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; CHROMOSOME 3; DNA MICROARRAY; GENETICS; OVARY TUMOR; PATHOLOGY; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE;

CELL LINE, TUMOR; CHROMOSOMES, HUMAN, PAIR 3; FEMALE; GENES, TUMOR SUPPRESSOR; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OVARIAN NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 67649203201     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20511     Document Type: Article

References (79)

1. Ozols RF. Update on the management of ovarian cancer. Cancer J 2002;8:S22-S30.
2. Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: Biology, endocrinology, and pathology. Endocr Rev 2001;22:255-288. (Pubitemid 32458162)
3. Bell DA. Origins and molecular pathology of ovarian cancer. Mod Pathol 2005;18:S19-S32. (Pubitemid 40188615)
4. Jordan S, Green A, Webb P. Benign epithelial ovarian tumours-cancer precursors or markers for ovarian cancer risk? Cancer Causes Control 2006;17:623-632.
5. McCluggage G. My thoughts on and approach to the typing of Ovarian carcinomas. J Clin Pathol 2007.
6. Biade S, Marinucci M, Schick J, et al. Gene expression profiling of human ovarian tumours. Br J Cancer 2006;95: 1092-1100. (Pubitemid 44606838)
7. Aletti GD, Gallenberg MM, Cliby WA, Jatoi A, Hartmann LC. Current management strategies for ovarian cancer. Mayo Clin Proc 2007;82:751-770. (Pubitemid 46878099)
8. Schwartz DR, Kardia SL, Shedden KA, et al. Gene expression in ovarian cancer reflects both morphology and biological behavior, distinguishing clear cell from other poorprognosis ovarian carcinomas. Cancer Res 2002;62:4722-4729. (Pubitemid 34898601)
9. Zorn KK, Bonome T, Gangi L, et al. Gene expression profiles of serous, endometrioid, and clear cell subtypes of ovarian and endometrial cancer. Clin Cancer Res 2005;11:6422-6430. (Pubitemid 41338978)
10. Ouellet V, Provencher DM, Maugard CM, et al. Discrimination between serous low malignant potential and invasive epithelial ovarian tumors using molecular profiling. Oncogene 2005;24:4672-4687. (Pubitemid 41032604)
11. Arcand SL, Mes-Masson AM, Provencher D, Hudson TJ, Tonin PN. Gene expression microarray analysis and genome databases facilitate the characterization of a chromosome 22 derived homogeneously staining region. Mol Carcinog 2004; 41:17-38. (Pubitemid 39195598)
12. Benoit MH, Hudson TJ, Maire G, et al. Global analysis of chromosome X gene expression in primary cultures of normal ovarian surface epithelial cells and epithelial ovarian cancer cell lines. Int J Oncol 2007;30:5-17.
13. Presneau N, Dewar K, Forgetta V, Provencher D, Mes- Masson AM, Tonin PN. Loss of heterozygosity and transcriptome analyses of a 1.2 Mb candidate ovarian cancer tumor suppressor locus region at 17q25.1-q25.2. Mol Carcinog 2005;43:141-154. (Pubitemid 40944239)
14. Tonin PN, Hudson TJ, Rodier F, et al. Microarray analysis of gene expression mirrors the biology of an ovarian cancer model. Oncogene 2001;20:6617-6626. (Pubitemid 32980288)
15. Hibbs K, Skubitz KM, Pambuccian SE, et al. Differential gene expression in ovarian carcinoma: Identification of potential biomarkers. Am J Pathol 2004;165:397-414. (Pubitemid 38971371)
16. Ono K, Tanaka T, Tsunoda T, et al. Identification by cDNA microarray of genes involved in ovarian carcinogenesis. Cancer Res 2000;60:5007-5011. (Pubitemid 30739750)
17. Welsh JB, Zarrinkar PP, Sapinoso LM, et al. Analysis of gene expression profiles in normal and neoplastic ovarian tissue samples identifies candidate molecular markers of epithelial ovarian cancer. Proc Natl Acad Sci USA 2001;98:1176-1181. (Pubitemid 32121206)
18. Bignotti E, Tassi RA, Calza S, et al. Differential gene expression profiles between tumor biopsies and short-term primary cultures of ovarian serous carcinomas: identification of novel molecular biomarkers for early diagnosis and therapy. Gynecol Oncol 2006;103:405-416. (Pubitemid 44602159)
19. Birch AH, Quinn MC, Filali-Mouhim A, Provencher DM, Mes-Masson AM, Tonin PN. Transcriptome analysis of serous ovarian cancers identifies differentially expressed chromosome 3 genes. Mol Carcinog 2008;47:56-65.
20. Santin AD, Zhan F, Bellone S, et al. Gene expression profiles in primary ovarian serous papillary tumors and normal ovarian epithelium: Identification of candidate molecular markers for ovarian cancer diagnosis and therapy. Int J Cancer 2004; 112:14-25. (Pubitemid 39249487)
21. Wojnarowicz PM, Breznan A, Arcand SL, et al. Construction of a chromosome 17 transcriptome in serous ovarian cancer identifies differentially expressed genes. Int J Gynecol Cancer 2008;18: 963-975.
22. Le Page C, Provencher D, Maugard CM, Ouellet V, Mes- Masson AM. Signature of a silent killer: Expression profiling in epithelial ovarian cancer. Expert Rev Mol Diagn 2004;4:157-167. (Pubitemid 38327246)
23. Seitz S, Frege R, Jacobsen A, et al. A network of clinically and functionally relevant genes is involved in the reversion of the tumorigenic phenotype of MDA-MB-231 breast cancer cells after transfer of human chromosome 8. Oncogene 2005;24: 869-879. (Pubitemid 40216095)
24. Klebig C, Seitz S, Korsching E, et al. Profile of differentially expressed genes after transfer of chromosome 17 into the breast cancer cell line CAL51. Genes Chromosomes Cancer 2005;44:233-246. (Pubitemid 41397092)
25. Stronach EA, Sellar GC, Blenkiron C, et al. Identification of clinically relevant genes on chromosome 11 in a functional model of ovarian cancer tumor suppression. Cancer Res 2003;63:8648-8655. (Pubitemid 38064039)
26. Cody NA, Ouellet V, Manderson EN, et al. Transfer of chromosome 3 fragments suppresses tumorigenicity of an ovarian cancer cell line monoallelic for chromosome 3p. Oncogene 2007;26:618-632. (Pubitemid 46160975)
27. Provencher DM, Lounis H, Champoux L, et al. Characterization of four novel epithelial ovarian cancer cell lines. In Vitro Cell Dev Biol Anim 2000;36:357-361. (Pubitemid 30626747)
28. Garson K, Shaw TJ, Clark KV, Yao DS, Vanderhyden BC. Models of ovarian cancer - Are we there yet? Mol Cell Endocrinol 2005;239:15-26.
29. Kruk PA, Maines-Bandiera SL, Auersperg N. A simplified method to culture human ovarian surface epithelium. Lab Invest 1990;63:132-136. (Pubitemid 20234682)
30. Lounis H, Provencher D, Godbout C, Fink D, Milot MJ, Mes- Masson AM. Primary cultures of normal and tumoral human ovarian epithelium: A powerful tool for basic molecular studies. Exp Cell Res 1994;215:303-309. (Pubitemid 24381080)
31. Presneau N, Mes-Masson AM, Ge B, Provencher D, Hudson TJ, Tonin PN. Patterns of expression of chromosome17 genes in primary cultures of normal ovarian surface epithelia and epithelial ovarian cancer cell lines. Oncogene 2003;22: 1568-1579. (Pubitemid 36390606)
32. Novak JP, Sladek R, Hudson TJ. Characterization of variability in large-scale gene expression data: Implications for study design. Genomics 2002;79:104-113.
33. Gentleman RC, Carey VJ, Bates DM, et al. Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol 2004;5:R80.
34. Benjamini Y, Yekutieli D. Quantitative trait Loci analysis using the false discovery rate. Genetics 2005;171:783-790. (Pubitemid 43156463)
35. Zorn KK, Jazaeri AA, Awtrey CS, et al. Choice of normal ovarian control influences determination of differentially expressed genes in ovarian cancer expression profiling studies. Clin Cancer Res 2003;9:4811-4818. (Pubitemid 37323284)
36. Le Page C, Ouellet V, Quinn MC, Tonin PN, Provencher DM, Mes-Masson AM. BTF4/BTNA3.2 and GCS as candidate mRNA prognostic markers in epithelial ovarian cancer. Cancer Epidemiol Biomarkers Prev 2008;17:913-920.
37. Huddleston HG, Wong KK, Welch WR, Berkowitz RS, Mok SC. Clinical applications of microarray technology: Creatine kinase B is an up-regulated gene in epithelial ovarian cancer and shows promise as a serum marker. Gynecol Oncol 2005;96:77-83. (Pubitemid 39612421)
38. Smith JS, Tachibana I, Pohl U, et al. A transcript map of the chromosome 19q-arm glioma tumor suppressor region. Genomics 2000;64:44-50. (Pubitemid 30165073)
39. Heinzelmann-Schwarz VA, Gardiner-Garden M, Henshall SM, et al. Overexpression of the cell adhesion molecules DDR1, Claudin 3, and Ep-CAM in metaplastic ovarian epithelium and ovarian cancer. Clin Cancer Res 2004;10:4427-4436.
40. Spizzo G, Went P, Dirnhofer S, et al. Overexpression of epithelial cell adhesion molecule (Ep-CAM) is an independent prognostic marker for reduced survival of patients with epithelial ovarian cancer. Gynecol Oncol 2006;103:483-488. (Pubitemid 44602156)
41. Rosano L, Spinella F, Di Castro V, et al. Endothelin-1 promotes epithelial-to-mesenchymal transition in human ovarian cancer cells. Cancer Res 2005;65:11649-11657. (Pubitemid 41821725)
42. Berx G, Becker K-F, Hofler H, Roy F. Mutations of the human E-cadherin (CDH1) gene. Human Mutation 1998;12:226-237. (Pubitemid 28418891)
43. Imura M, Yamashita S, Cai LY, et al. Methylation and expression analysis of 15 genes and three normallymethylated genes in 13 Ovarian cancer cell lines. Cancer Lett 2006;241:213-220. (Pubitemid 44163031)
44. Sundfeldt K. Cell-cell adhesion in the normal ovary and ovarian tumors of epithelial origin; an exception to the rule. Mol Cell Endocrinol 2003;202:89-96. (Pubitemid 36593398)
45. Reddy P, Liu L, Ren C, et al. Formation of E-cadherinmediated cell-cell adhesion activates AKT and mitogen activated protein kinase via phosphatidylinositol 3 kinase and ligand-independent activation of epidermal growth factor receptor in ovarian cancer cells. Mol Endocrinol 2005;19:2564-2578. (Pubitemid 41362669)
46. Fazili Z, Sun W, Mittelstaedt S, Cohen C, Xu XX. Disabled-2 inactivation is an early step in ovarian tumorigenicity. Oncogene 1999;18:3104-3113. (Pubitemid 29261231)
47. Daponte A, Kostopoulou E, Minas M, Koukoulis G, Messinis IE. Prognostic significance of fascin expression in advanced poorly differentiated serous ovarian cancer. Anticancer Res 2008;28:1905-1910. (Pubitemid 351892904)
48. Gabriel B, Mildenberger S, Weisser CW, et al. Focal adhesion kinase interacts with the transcriptional coactivator FHL2 and both are overexpressed in epithelial ovarian cancer. Anticancer Res 2004;24:921-927. (Pubitemid 38625040)
49. Gurusinghe CJ, Healy DL, Jobling T, Mamers P, Burger HG. Inhibin and activin are demonstrable by immunohistochemistry in ovarian tumor tissue. Gynecol Oncol 1995;57:27-32.
50. Gery S, Xie D, Yin D, et al. Ovarian carcinomas: CCN genes are aberrantly expressed and CCN1 promotes proliferation of these cells. Clin Cancer Res 2005;11:7243-7254. (Pubitemid 41507681)
51. Sun W, Fujimoto J, Tamaya T. Coexpression of Gas6/Axl in human ovarian cancers. Oncology 2004;66:450-457. (Pubitemid 39370236)
52. Chan QK, Ngan HY, Ip PP, Liu VW, Xue WC, Cheung AN. Tumor suppressor effect of follistatin-like 1 in ovarian and endometrial carcinogenesis - A differential expression and functional analysis. Carcinogenesis 2008; [Epub ahead of print].
53. Yiu GK, Chan WY, Ng SW, et al. SPARC (secreted protein acidic and rich in cysteine) induces apoptosis in ovarian cancer cells. Am J Pathol 2001;159:609-622. (Pubitemid 32751091)
54. Yuecheng Y, Hongmei L, Xiaoyan X. Clinical evaluation of E-cadherin expression and its regulation mechanism in epithelial ovarian cancer. Clin Exp Metastasis 2006; 23:65-74. (Pubitemid 44576780)
55. Engwegen JY, Helgason HH, Cats A, et al. Identification of serum proteins discriminating colorectal cancer patients and healthy controls using surface-enhanced laser desorption ionisation-time of flight mass spectrometry. World J Gastroenterol 2006;12:1536-1544.
56. Mok SC, Chao J, Skates S, et al. Prostasin, a potential serum marker for ovarian cancer: Identification through microarray technology. J Natl Cancer Inst 2001;93:1458-1464. (Pubitemid 32982674)
57. Nanjundan M, Nakayama Y, Cheng KW, et al. Amplification of MDS1/EVI1 and EVI1, located in the 3q26.2 amplicon, is associated with favorable patient prognosis in ovarian cancer. Cancer Res 2007;67:3074-3084. (Pubitemid 46724844)
58. Chen B, Athanasiou M, Gu Q, Blair DG. Drm/Gremlin transcriptionally activates p21(Cip1) via a novel mechanism and inhibits neoplastic transformation. Biochem Biophys Res Commun 2002;295:1135-1141. (Pubitemid 34936896)
59. Khokha MK, Hsu D, Brunet LJ, Dionne MS, Harland RM. Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat Genet 2003; 34:303-307. (Pubitemid 36792863)
60. Topol LZ, Bardot B, Zhang Q, et al. Biosynthesis, posttranslation modification, and functional characterization of Drm/Gremlin. J Biol Chem 2000;275:8785-8793. (Pubitemid 30180233)
61. Topol LZ, Marx M, Laugier D, et al. Identification of drm, a novel gene whose expression is suppressed in transformed cells and which can inhibit growth of normal but not transformed cells in culture. Mol Cell Biol 1997;17:4801-4810. (Pubitemid 27318155)
62. Panman L, Galli A, Lagarde N, et al. Differential regulation of gene expression in the digit forming area of the mouse limb bud by SHH and gremlin 1/FGF-mediated epithelial-mesenchymal signalling. Development 2006;133:3419-3428. (Pubitemid 44501844)
63. Topol LZ, Modi WS, Koochekpour S, Blair DG. DRM/ GREMLIN (CKTSF1B1) maps to human chromosome 15 and is highly expressed in adult and fetal brain. Cytogenet Cell Genet 2000;89:79-84. (Pubitemid 30435263)
64. Yamashita S, Tsujino Y, Moriguchi K, Tatematsu M, Ushijima T. Chemical genomic screening for methylation-silenced genes in gastric cancer cell lines using 5-aza-2′-deoxycytidine treatment and oligonucleotide microarray. Cancer Sci 2006;97:64-71. (Pubitemid 43257029)
65. Suzuki M, Shigematsu H, Shivapurkar N, et al. Methylation of apoptosis related genes in the pathogenesis and prognosis of prostate cancer. Cancer Lett 2006;242:222-230. (Pubitemid 44485305)
66. Suzuki M, Shigematsu H, Shames DS, et al. DNA methylation- associated inactivation of TGFbeta-related genes DRM/Gremlin, RUNX3, and HPP1 in human cancers. Br J Cancer 2005;93:1029-1037. (Pubitemid 41548398)
67. Oue N, Hamai Y, Mitani Y, et al. Gene expression profile of gastric carcinoma: identification of genes and tags potentially involved in invasion, metastasis, and carcinogenesis by serial analysis of gene expression. Cancer Res 2004;64: 2397-2405. (Pubitemid 38523892)
68. Yau TO, Chan CY, Chan KL, et al. HDPR1, a novel inhibitor of the WNT/beta-catenin signaling, is frequently downregulated in hepatocellular carcinoma: Involvement of methylation- mediated gene silencing. Oncogene 2005;24:1607-1614. (Pubitemid 40396090)
69. Zhang L, Gao X, Wen J, Ning Y, Chen YG. Dapper 1 antagonizes Wnt signaling by promoting dishevelled degradation. J Biol Chem 2006;281:8607-8612. (Pubitemid 43847964)
70. Kerley-Hamilton JS, Pike AM, Hutchinson JA, Freemantle SJ, Spinella MJ. The direct p53 target gene, FLJ11259/DRAM, is a member of a novel family of transmembrane proteins. Biochim Biophys Acta 2007;1769:209-219. (Pubitemid 46711213)
71. Balemans W, Van Hul W. Extracellular regulation of BMP signaling in vertebrates: A cocktail of modulators. Dev Biol 2002;250:231-250. (Pubitemid 35216412)
72. Massague J, Blain SW, Lo RS. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 2000;103:295-309.
73. Sunde JS, Donninger H, Wu K, et al. Expression profiling identifies altered expression of genes that contribute to the inhibition of transforming growth factor-beta signaling in ovarian cancer. Cancer Res 2006;66:8404-8412. (Pubitemid 44449151)
74. Kurokawa M, Mitani K, Irie K, et al. The oncoprotein Evi-1 represses TGF-beta signalling by inhibiting Smad3. Nature 1998;394:92-96. (Pubitemid 28321809)
75. Michos O, Goncalves A, Lopez-Rios J, et al. Reduction of BMP4 activity by gremlin 1 enables ureteric bud outgrowth and GDNF/WNT11 feedback signalling during kidney branching morphogenesis. Development 2007;134:2397-2405. (Pubitemid 47074134)
76. Wordinger RJ, Fleenor DL, Hellberg PE, et al. Effects of TGF-beta2, BMP-4, and gremlin in the trabecular meshwork: Implications for glaucoma. Invest Ophthalmol Vis Sci 2007; 48:1191-1200.
77. Lee HJ, Chang JH, Kim YS, Kim SJ, Yang HK. Effect of etsrelated transcription factor (ERT) on transforming growth factor (TGF)-beta type II receptor gene expression in human cancer cell lines. J Exp Clin Cancer Res 2003;22:477-480. (Pubitemid 37205407)
78. Lounis H, Mes-Masson AM, Dion F, et al. Mapping of chromosome 3p deletions in human epithelial ovarian tumors. Oncogene 1998;17:2359-2365. (Pubitemid 28515389)
79. Samouelian V, Maugard CM, Jolicoeur M, et al. Chemosensitivity and radiosensitivity profiles of four new human epithelial ovarian cancer cell lines exhibiting genetic alterations in BRCA2, TGFbeta-RII, KRAS2, TP53 and/or CDNK2A. Cancer Chemother Pharmacol 2004;54:497-504. (Pubitemid 40022245)