Characterization of the 3p12.3-pcen region associated with tumor suppression in a novel ovarian cancer cell line model genetically modified by chromosome 3 fragment transfer

Molecular Carcinogenesis

Volumn 48, Issue 12, 2009, Pages 1077-1092

  Cody, Neal A L ^a   Shen, Zhen ^b   Ripeau, Jean Sebastien ^a   Provencher, Diane M ^c,d   Mes Masson, Anne Marie ^c,d   Chevrette, Mario ^a,b   Tonin, Patricia N ^a,b  

^a MCGILL UNIVERSITY   (Canada)

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

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

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

Author keywords

Chromosome 3p; Haploinsufficiency; Ovarian cancer; Tumor suppressor genes

Indexed keywords

MICROSATELLITE DNA; PRIMER DNA;

ARTICLE; BENIGN TUMOR; CANCER CELL CULTURE; CANCER INHIBITION; CHROMOSOME 3P; CONTROLLED STUDY; DNA MODIFICATION; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE MUTATION; GENE TRANSFER; GENETIC CODE; GENETIC MARKER; GENETIC POLYMORPHISM; HUMAN; HUMAN CELL; HUMAN TISSUE; HYBRID; NUCLEOTIDE SEQUENCE; OVARY CANCER; PRIORITY JOURNAL; SEQUENCE ANALYSIS; TUMOR SUPPRESSOR GENE; VGLL3 GENE; ZNF654 GENE; ALTERNATIVE RNA SPLICING; CASE CONTROL STUDY; CHEMISTRY; CHROMOSOME 3; COMPARATIVE STUDY; CYSTADENOCARCINOMA; DNA METHYLATION; GENETICS; HETEROZYGOSITY LOSS; METABOLISM; OVARY; OVARY TUMOR; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ALTERNATIVE SPLICING; CASE-CONTROL STUDIES; CELL LINE, TUMOR; CHROMOSOMES, HUMAN, PAIR 3; CYSTADENOCARCINOMA, SEROUS; DNA METHYLATION; DNA PRIMERS; FEMALE; GENES, TUMOR SUPPRESSOR; HUMANS; LOSS OF HETEROZYGOSITY; MICROSATELLITE REPEATS; OVARIAN NEOPLASMS; OVARY;

EID: 73349127475     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20535     Document Type: Article

References (91)

1. Bernardini M, Weberpals J, Squire JA. The use of cytogenetics in understanding ovarian cancer. Biomed Pharmacother 2004;58:17-23.
2. Mertens F, Johansson B, Hoglund M, Mitelman F. Chromosomal imbalance maps of malignant solid tumors: A cytogenetic survey of 3185 neoplasms. Cancer Res 1997;57:2765-2780.
3. Pejovic T, Heim S, Mandahl N, et al. Chromosome aberrations in 35 primary ovarian carcinomas. Genes Chromosomes Cancer 1992;4:58-68.
4. Whang-Peng J, Knutsen T, Douglass EC, et al. Cytogenetic studies in ovarian cancer. Cancer Genet Cytogenet 1984;11:91-106.
5. Yonescu R, Currie JL, Hedrick L, Campbell J, Griffin CA. Chromosome abnormalities in primary endometrioid ovarian carcinoma. Cancer Genet Cytogenet 1996;87:167-171.
6. Mitelman Database of Chromosome Aberrations in Cancer. Mitelman F, Johansson B, Mertens F, editors. 2009. http://cgap.nci.nih.gov/Chromosomes/ Mitelman.
7. Dodson MK, Hartmann LC, Cliby WA, et al. Comparison of loss of heterozygosity patterns in invasive low-grade and high-grade epithelial ovarian carcinomas. Cancer Res 1993;53:4456-4460.
8. Ehlen T, Dubeau L. Loss of heterozygosity on chromosomal segments 3p, 6q and 11p in human ovarian carcinomas. Oncogene 1990;5:219-223.
9. Fullwood P, Marchini S, Rader JS, et al. Detailed genetic and physical mapping of tumor suppressor loci on chromosome 3p in ovarian cancer. Cancer Res 1999;59:4662-4667.
10. Lounis H, Mes-Masson AM, Dion F, et al. Mapping of chromosome 3p deletions in human epithelial ovarian tumors. Oncogene 1998;17:2359-2365.
11. Petursdottir TE, Thorsteinsdottir U, Jonasson JG, et al. Interstitial deletions including chromosome 3 common eliminated region 1 (C3CER1) prevail in human solid tumors from 10 different tissues. Genes Chromosomes Cancer 2004;41:232-242.
12. Agathanggelou A, Honorio S, Macartney DP, et al. Methylation associated inactivation of RASSF1A from region 3p21.3 in lung, breast and ovarian tumours. Oncogene 2001;20:1509-1518.
13. Imura M, Yamashita S, Cai LY, et al. Methylation and expression analysis of 15 genes and three normally-methylated genes in 13 Ovarian cancer cell lines. Cancer Lett 2006;241:213-220.
14. Kwong J, Lee JY, Wong KK, et al. Candidate tumor-suppressor gene DLEC1 is frequently downregulated by promoter hypermethylation and histone hypoacetylation in human epithelial ovarian cancer. Neoplasia 2006;8:268-278.
15. Teodoridis JM, Hall J, Marsh S, et al. CpG island methylation of DNA damage response genes in advanced ovarian cancer. Cancer Res 2005;65:8961-8967.
16. Wang L, Darling J, Zhang JS, et al. Loss of expression of the DRR 1 gene at chromosomal segment 3p21.1 in renal cell carcinoma. Genes Chromosomes Cancer 2000;27:1-10.
17. Dallol A, Forgacs E, Martinez A, et al. Tumour specific promoter region methylation of the human homologue of the Drosophila Roundabout gene DUTT1 (ROBO1) in human cancers. Oncogene 2002;21:3020-3028.
18. Huebner K. Tumor suppressors on 3p: A neoclassic quartet. Proc Natl Acad Sci USA 2001;98:14763-14765.
19. Imreh S, Klein G, Zabarovsky ER. Search for unknown tumor-antagonizing genes. Genes Chromosomes Cancer 2003;38:307-321.
20. Zabarovsky ER, Lerman MI, Minna JD. Tumor suppressor genes on chromosome 3p involved in the pathogenesis of lung and other cancers. Oncogene 2002;21:6915-6935.
21. Rimessi P, Gualandi F, Morelli C, et al. Transfer of human chromosome 3 to an ovarian carcinoma cell line identifies three regions on 3p involved in ovarian cancer. Oncogene 1994;9:3467-3474.
22. Tse C, Xiang RH, Bracht T, Naylor SL. Human Semaphorin 3B (SEMA3B) located at chromosome 3p21.3 suppresses tumor formation in an adenocarcinoma cell line. Cancer Res 2002;62:542-546.
23. Xiang R, Davalos AR, Hensel CH, Zhou XJ, Tse C, Naylor SL. Semaphorin 3F gene from human 3p21.3 suppresses tumor formation in nude mice. Cancer Res 2002;62:2637-2643.
24. 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.
25. Narayan G, Goparaju C, Arias-Pulido H, et al. Promoter hypermethylation-mediated inactivation of multiple Slit-Robo pathway genes in cervical cancer progression. Mol Cancer 2006;5:16.
26. Xian J, Aitchison A, Bobrow L, et al. Targeted disruption of the 3p12 gene, Dutt1/Robo1, predisposes mice to lung adenocarcinomas and lymphomas with methylation of the gene promoter. Cancer Res 2004;64:6432-6437.
27. Knudson AG. Hereditary cancer: Two hits revisited. J Cancer Res Clin Oncol 1996;122:135-140.
28. 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.
29. 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.
30. Kruk PA, Maines-Bandiera SL, Auersperg N. A simplified method to culture human ovarian surface epithelium. Lab Invest 1990;63:132-136.
31. 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.
32. 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.
33. Le Page C, Ouellet V, Madore J, et al. Gene expression profiling of primary cultures of ovarian epithelial cells identifies novel molecular classifiers of ovarian cancer. Br J Cancer 2006;94:436-445.
34. 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.
35. Bardelli A, Parsons DW, Silliman N, et al. Mutational analysis of the tyrosine kinome in colorectal cancers. Science 2003;300:949.
36. Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: Biology, endocrinology, and pathology. Endocr Rev 2001;22:255-288.
37. Biade S, Marinucci M, Schick J, et al. Gene expression profiling of human ovarian tumours. Br J Cancer 2006;95:1092-1100.
38. McCluggage WG. My approach to and thoughts on the typing of ovarian carcinomas. J Clin Pathol 2008;61:152-163.
39. Payne SR, Kemp CJ. Tumor suppressor genetics. Carcinogenesis 2005;26:2031-2045.
40. Santarosa M, Ashworth A. Haploinsufficiency for tumour suppressor genes: When you don't need to go all the way. Biochim Biophys Acta 2004;1654:105-122.
41. Smilenov LB. Tumor development: Haploinsufficiency and local network assembly. Cancer Lett 2006;240:17-28.
42. Devilee P, Cleton-Jansen AM, Cornelisse CJ. Ever since Knudson. Trends Genet 2001;17:569-573.
43. Haber D, Harlow E. Tumour-suppressor genes: Evolving definitions in the genomic age. Nat Genet 1997;16:320-322.
44. Robertson GP, Huang HJ, Cavenee WK. Identification and validation of tumor suppressor genes. Mol Cell Biol Res Commun 1999;2:1-10.
45. Lott ST, Lovell M, Naylor SL, Killary AM. Physical and functional mapping of a tumor suppressor locus for renal cell carcinoma within chromosome 3p12. Cancer Res 1998;58:3533-3537.
46. Lovell M, Lott ST, Wong P, El-Naggar A, Tucker S, Killary AM. The genetic locus NRC-1 within chromosome 3p12 mediates tumor suppression in renal cell carcinoma independently of histological type, tumor microenvironment, and VHL mutation. Cancer Res 1999;59:2182-2189.
47. Sanchez Y, el-Naggar A, Pathak S, Killary AM. A tumor suppressor locus within 3p14-p12 mediates rapid cell death of renal cell carcinoma in vivo. Proc Natl Acad Sci USA 1994;91:3383-3387.
48. Andrews W, Liapi A, Plachez C, et al. Robo1 regulates the development of major axon tracts and interneuron migration in the forebrain. Development 2006;133:2243-2252.
49. Clark K, Hammond E, Rabbitts P. Temporal and spatial expression of two isoforms of the Dutt1/Robo1 gene in mouse development. FEBS Lett 2002;523:12-16.
50. Hannula-Jouppi K, Kaminen-Ahola N, Taipale M, et al. The axon guidance receptor gene ROBO1 is a candidate gene for developmental dyslexia. PLoS Genet 2005;1:e50.
51. Nural HF, Todd Farmer W, Mastick GS. The Slit receptor Robo1 is predominantly expressed via the Dutt1 alternative promoter in pioneer neurons in the embryonic mouse brain and spinal cord. Gene Expr Patterns 2007;7:837-845.
52. Sundaresan V, Roberts I, Bateman A, et al. The DUTT1 gene, a novel NCAM family member is expressed in developing murine neural tissues and has an unusually broad pattern of expression. Mol Cell Neurosci 1998;11:29-35.
53. Grone J, Doebler O, Loddenkemper C, Hotz B, Buhr HJ, Bhargava S. Robo1/Robo4: Differential expression of angiogenic markers in colorectal cancer. Oncol Rep 2006;15:1437-1443.
54. Ito H, Funahashi S, Yamauchi N, et al. Identification of ROBO1 as a novel hepatocellular carcinoma antigen and a potential therapeutic and diagnostic target. Clin Cancer Res 2006;12:3257-3264.
55. Zhang K, Lott ST, Jin L, Killary AM. Fine mapping of the NRC-1 tumor suppressor locus within chromosome 3p12. Biochem Biophys Res Commun 2007;360:531-538.
56. Wang L, Lu W, Chen YG, Zhou XM, Gu JR. Comparison of gene expression between normal colon mucosa and colon carcinoma by means of messenger RNA differential display. World J Gastroenterol 1999;5:533-534.
57. Maeda T, Chapman DL, Stewart AF. Mammalian vestigial-like 2, a cofactor of TEF-1 and MEF2 transcription factors that promotes skeletal muscle differentiation. J Biol Chem 2002;277:48889-48898.
58. Legent K, Dutriaux A, Delanoue R, Silber J. Cell cycle genes regulate vestigial and scalloped to ensure normal proliferation in the wing disc of Drosophila melanogaster. Genes Cells 2006;11:907-918.
59. Vaudin P, Delanoue R, Davidson I, Silber J, Zider A. TONDU (TDU), a novel human protein related to the product of vestigial (vg) gene of Drosophila melanogaster interacts with vertebrate TEF factors and substitutes for Vg function in wing formation. Development 1999;126:4807-4816.
60. Kitagawa M. A Sveinsson's chorioretinal atrophy-associated missense mutation in mouse Tead1 affects its interaction with the co-factors YAP and TAZ. Biochem Biophys Res Commun 2007;361:1022-1026.
61. Brayer KJ, Segal DJ. Keep your fingers off my DNA: Protein-protein interactions mediated by C2H2 zinc finger domains. Cell Biochem Biophys 2008;50:111-131.
62. Coleman JE. Zinc proteins: Enzymes, storage proteins, transcription factors, and replication proteins. Annu Rev Biochem 1992;61:897-946.
63. Bao Y, Kishnani P, Wu JY, Chen YT. Hepatic and neuromuscular forms of glycogen storage disease type IV caused by mutations in the same glycogen-branching enzyme gene. J Clin Invest 1996;97:941-948.
64. Janecke AR, Dertinger S, Ketelsen UP, et al. Neonatal type IV glycogen storage disease associated with "null" mutations in glycogen branching enzyme 1. J Pediatr 2004;145:705-709.
65. Moses SW, Parvari R. The variable presentations of glycogen storage disease type IV: A review of clinical, enzymatic and molecular studies. Curr Mol Med 2002;2:177-188.
66. Alshak NS, Cocjin J, Podesta L, et al. Hepatocellular adenoma in glycogen storage disease type IV. Arch Pathol Lab Med 1994;118:88-91.
67. de Moor RA, Schweizer JJ, van Hoek B, Wasser M, Vink R, Maaswinkel-Mooy PD. Hepatocellular carcinoma in glycogen storage disease type IV. Arch Dis Child 2000;82:479-480.
68. Skibinski G, Parkinson NJ, Brown JM, et al. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in fronto-temporal dementia. Nat Genet 2005;37:806-808.
69. Momeni P, Bell J, Duckworth J, et al. Sequence analysis of all identified open reading frames on the frontal temporal dementia haplotype on chromosome 3 fails to identify unique coding variants except in CHMP2B. Neurosci Lett 2006;410:77-79.
70. Naumann F, Remus R, Schmitz B, Doerfler W. Gene structure and expression of the 50-(CGG)(n)-30-binding protein (CGGBP1). Genomics 2004;83:106-118.
71. Biederer T. Bioinformatic characterization of the SynCAM family of immunoglobulin-like domain-containing adhesion molecules. Genomics 2006;87:139-150.
72. Lu W, van Eerde AM, Fan X, et al. Disruption of ROBO2 is associated with urinary tract anomalies and confers risk of vesicoureteral reflux. Am J Hum Genet 2007;80:616-632.
73. Grieshammer U, Le M, Plump AS, Wang F, Tessier-Lavigne M, Martin GR. SLIT2-mediated ROBO2 signaling restricts kidney induction to a single site. Dev Cell 2004;6:709-717.
74. Latil A, Chene L, Cochant-Priollet B, et al. Quantification of expression of netrins, slits and their receptors in human prostate tumors. Int J Cancer 2003;103:306-315.
75. Bieche I, Lerebours F, Tozlu S, Espie M, Marty M, Lidereau R. Molecular profiling of inflammatory breast cancer: Identification of a poor-prognosis gene expression signature. Clin Cancer Res 2004;10:6789-6795.
76. Wu W, Cogan JD, Pfaffle RW, et al. Mutations in PROP1 cause familial combined pituitary hormone deficiency. Nat Genet 1998;18:147-149.
77. Asa SL, Puy LA, Lew AM, Sundmark VC, Elsholtz HP. Cell type-specific expression of the pituitary transcription activator pit-1 in the human pituitary and pituitary adenomas. J Clin Endocrinol Metab 1993;77:1275-1280.
78. Lloyd RV, Osamura RY. Transcription factors in normal and neoplastic pituitary tissues. Microsc Res Tech 1997;39:168-181.
79. Nakamura S, Ohtsuru A, Takamura N, et al. Prop-1 gene expression in human pituitary tumors. J Clin Endocrinol Metab 1999;84:2581-2584.
80. Gil-Puig C, Seoane S, Blanco M, et al. Pit-1 is expressed in normal and tumorous human breast and regulates GH secretion and cell proliferation. Eur J Endocrinol 2005;153:335-344.
81. Wilkinson DG. Multiple roles of EPH receptors and ephrins in neural development. Nat Rev Neurosci 2001;2:155-164.
82. Vearing C, Lee FT, Wimmer-Kleikamp S, et al. Concurrent binding of anti-EphA3 antibody and ephrin-A5 amplifies EphA3 signaling and downstream responses: Potential as EphA3-specific tumor-targeting reagents. Cancer Res 2005;65:6745-6754.
83. Wood LD, Calhoun ES, Silliman N, et al. Somatic mutations of GUCY2F, EPHA3, and NTRK3 in human cancers. Hum Mutat 2006;27:1060-1061.
84. Shao RX, Kato N, Lin LJ, et al. Absence of tyrosine kinase mutations in Japanese colorectal cancer patients. Oncogene 2007;26:2133-2135.
85. Forbes S, Clements J, Dawson E, et al. Cosmic 2005. Br J Cancer 2006;94:318-322.
86. Greenman C, Stephens P, Smith R, et al. Patterns of somatic mutation in human cancer genomes. Nature 2007;446:153-158.
87. Sjoblom T, Jones S, Wood LD, et al. The consensus coding sequences of human breast and colorectal cancers. Science 2006;314:268-274.
88. Wood LD, Parsons DW, Jones S, et al. The genomic landscapes of human breast and colorectal cancers. Science 2007;318:1108-1113.
89. Muzny DM, Scherer SE, Kaul R, et al. The DNA sequence, annotation and analysis of human chromosome 3. Nature 2006;440:1194-1198.
90. Angeloni D, ter Elst A, Wei MH, et al. Analysis of a new homozygous deletion in the tumor suppressor region at 3p12.3 reveals two novel intronic noncoding RNA genes. Genes Chromosomes Cancer 2006;45:676-691.
91. 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.