VGLL3 expression is associated with a tumor suppressor phenotype in epithelial ovarian cancer

Molecular Oncology

Volumn 7, Issue 3, 2013, Pages 513-530

  Gambaro, Karen ^a   Quinn, Michael C J ^b   Wojnarowicz, Paulina M ^a   Arcand, Suzanna L ^c   de Ladurantaye, Manon ^b   Barrès, Véronique ^b   Ripeau, Jean Sébastien ^c   Killary, Ann M ^d   Davis, Elaine C ^e   Lavoie, Josée ^a,f   Provencher, Diane M ^b,g   Mes Masson, Anne Marie ^b,g   Chevrette, Mario ^a,c   Tonin, Patricia N ^a,c  

^a MONTREAL GENERAL HOSPITAL   (Canada)

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

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

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e MCGILL UNIVERSITY   (Canada)

^f MONTREAL CHILDREN S HOSPITAL   (Canada)

^g UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

3p12; Chromosome 3; Gene expression; Gene transfection; High grade ovarian serous carcinomas; Microcell mediated chromosome transfer; Tumor suppressor gene; VGLL3

Indexed keywords

PROTEIN; UNCLASSIFIED DRUG; VESTIGIAL LIKE 3 PROTEIN;

AMINO ACID SUBSTITUTION; ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CARCINOGENICITY; CELL SURVIVAL; CELLULAR DISTRIBUTION; CHROMOSOME 3P; CLONOGENIC ASSAY; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC COMPLEMENTATION; GENETIC TRANSFECTION; GENOMIC INSTABILITY; GENOTYPE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MICROSATELLITE MARKER; MOLECULAR CLONING; MOUSE; NONHUMAN; OVARY CARCINOMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR SUPPRESSOR GENE; TUMOR XENOGRAFT; VGLL3 GENE; WESTERN BLOTTING;

LENTIVIRUS; MUS MUSCULUS;

EID: 84878113852     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2012.12.006     Document Type: Article

References (65)

1. Ahmed A.A., Etemadmoghadam D., Temple J., Lynch A.G., Riad M., Sharma R., Stewart C., Fereday S., Caldas C., Defazio A., Bowtell D., Brenton J.D. Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J. Pathol. 2010, 221:49-56.
2. Aletti G.D., Gallenberg M.M., Cliby W.A., Jatoi A., Hartmann L.C. Current management strategies for ovarian cancer. Mayo Clin. Proc. 2007, 82:751-770.
3. Anglesio M.S., Arnold J.M., George J., Tinker A.V., Tothill R., Waddell N., Simms L., Locandro B., Fereday S., Traficante N., Russell P., Sharma R., Birrer M.J., deFazio A., Chenevix-Trench G., Bowtell D.D. Mutation of ERBB2 provides a novel alternative mechanism for the ubiquitous activation of RAS-MAPK in ovarian serous low malignant potential tumors. Mol. Cancer Res. 2008, 6:1678-1690.
4. Antonescu C.R., Zhang L., Nielsen G.P., Rosenberg A.E., Dal Cin P., Fletcher C.D. Consistent t(1;10) with rearrangements of TGFBR3 and MGEA5 in both myxoinflammatory fibroblastic sarcoma and hemosiderotic fibrolipomatous tumor. Genes Chromosomes Cancer 2011, 50:757-764.
5. Arcand S.L., Mes-Masson A.M., Provencher D., Hudson T.J., Tonin P.N. Gene expression microarray analysis and genome databases facilitate the characterization of a chromosome 22 derived homogeneously staining region. Mol. Carcinog 2004, 41:17-38.
6. Auersperg N., Wong A.S., Choi K.C., Kang S.K., Leung P.C. Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr. Rev. 2001, 22:255-288.
7. Berger A.H., Knudson A.G., Pandolfi P.P. A continuum model for tumour suppression. Nature 2011, 476:163-169.
8. Birch A.H., Quinn M.C., Filali-Mouhim A., Provencher D.M., Mes-Masson A.M., Tonin P.N. Transcriptome analysis of serous ovarian cancers identifies differentially expressed chromosome 3 genes. Mol. Carcinog. 2008, 47:56-65.
9. Birch A.H., Arcand S.L., Oros K.K., Rahimi K., Watters A.K., Provencher D., Greenwood C.M., Mes-Masson A.M., Tonin P.N. Chromosome 3 anomalies investigated by genome wide SNP analysis of benign, low malignant potential and low grade ovarian serous tumours. PLoS One 2011, 6:e28250.
10. Bonome T., Lee J.Y., Park D.C., Radonovich M., Pise-Masison C., Brady J., Gardner G.J., Hao K., Wong W.H., Barrett J.C., Lu K.H., Sood A.K., Gershenson D.M., Mok S.C., Birrer M.J. Expression profiling of serous low malignant potential, low-grade, and high-grade tumors of the ovary. Cancer Res. 2005, 65:10602-10612.
11. Bowen N.J., Walker L.D., Matyunina L.V., Logani S., Totten K.A., Benigno B.B., McDonald J.F. Gene expression profiling supports the hypothesis that human ovarian surface epithelia are multipotent and capable of serving as ovarian cancer initiating cells. BMC Med. Genomics 2009, 2:71.
12. Brasaemle D.L., Rubin B., Harten I.A., Gruia-Gray J., Kimmel A.R., Londos C. Perilipin A increases triacylglycerol storage by decreasing the rate of triacylglycerol hydrolysis. J. Biol. Chem. 2000, 275:38486-38493.
13. Browne T.J., Fletcher C.D. Haemosiderotic fibrolipomatous tumour (so-called haemosiderotic fibrohistiocytic lipomatous tumour): analysis of 13 new cases in support of a distinct entity. Histopathology 2006, 48:453-461.
14. Campeau E., Ruhl V.E., Rodier F., Smith C.L., Rahmberg B.L., Fuss J.O., Campisi J., Yaswen P., Cooper P.K., Kaufman P.D. A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS One 2009, 4:e6529.
15. Chen V.W., Ruiz B., Killeen J.L., Cote T.R., Wu X.C., Correa C.N. Pathology and classification of ovarian tumors. Cancer 2003, 97:2631-2642.
16. Codogno P., Mehrpour M., Proikas-Cezanne T. Canonical and non-canonical autophagy: variations on a common theme of self-eating?. Nat. Rev. Mol. Cell. Biol. 2011, 13:7-12.
17. Cody N.A., Ouellet V., Manderson E.N., Quinn M.C., Filali-Mouhim A., Tellis P., Zietarska M., Provencher D.M., Mes-Masson A.M., Chevrette M., Tonin P.N. Transfer of chromosome 3 fragments suppresses tumorigenicity of an ovarian cancer cell line monoallelic for chromosome 3p. Oncogene 2007, 26:618-632.
18. Cody N.A., Shen Z., Ripeau J.S., Provencher D.M., Mes-Masson A.M., Chevrette M., Tonin P.N. 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. Mol. Carcinog. 2009, 48:1077-1092.
19. DiDonato D., Brasaemle D.L. Fixation methods for the study of lipid droplets by immunofluorescence microscopy. J. Histochem. Cytochem. 2003, 51:773-780.
20. Dion F., Mes-Masson A.M., Seymour R.J., Provencher D., Tonin P.N. Allelotyping defines minimal imbalance at chromosomal region 17q25 in non-serous epithelial ovarian cancers. Oncogene 2000, 19:1466-1472.
21. Fink T., Zachar V. Adipogenic differentiation of human mesenchymal stem cells. Methods Mol. Biol. 2011, 698:243-251.
22. Gat-Yablonski G., Frumkin-Ben David R., Bar M., Potievsky O., Phillip M., Lazar L. Homozygous microdeletion of the POU1F1, CHMP2B, and VGLL3 genes in chromosome 3 - A novel syndrome. Am. J. Med. Genet. A 2011, 155A:2242-2246.
23. Gorringe K.L., Campbell I.G. Large-scale genomic analysis of ovarian carcinomas. Mol. Oncol. 2009, 3:157-164.
24. Hallor K.H., Sciot R., Staaf J., Heidenblad M., Rydholm A., Bauer H.C., Astrom K., Domanski H.A., Meis J.M., Kindblom L.G., Panagopoulos I., Mandahl N., Mertens F. Two genetic pathways, t(1;10) and amplification of 3p11-12, in myxoinflammatory fibroblastic sarcoma, haemosiderotic fibrolipomatous tumour, and morphologically similar lesions. J. Pathol. 2009, 217:716-727.
25. Helias-Rodzewicz Z., Perot G., Chibon F., Ferreira C., Lagarde P., Terrier P., Coindre J.M., Aurias A. YAP1 and VGLL3, encoding two cofactors of TEAD transcription factors, are amplified and overexpressed in a subset of soft tissue sarcomas. Genes Chromosomes Cancer 2010, 49:1161-1171.
26. Henne W.M., Buchkovich N.J., Emr S.D. The ESCRT pathway. Dev. Cell. 2011, 21:77-91.
27. Jiang X., Zhu T., Yang J., Li S., Ye S., Liao S., Meng L., Lu Y., Ma D. Identification of novel epithelial ovarian cancer biomarkers by cross-laboratory microarray analysis. J. Huazhong Univ. Sci. Technolog. Med. Sci. 2010, 30:354-359.
28. Kabeya Y., Mizushima N., Yamamoto A., Oshitani-Okamoto S., Ohsumi Y., Yoshimori T. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell. Sci. 2004, 117:2805-2812.
29. Karolchik D., Baertsch R., Diekhans M., Furey T.S., Hinrichs A., Lu Y.T., Roskin K.M., Schwartz M., Sugnet C.W., Thomas D.J., Weber R.J., Haussler D., Kent W.J. The UCSC genome browser database. Nucleic Acids Res. 2003, 31:51-54.
30. Katzmann D.J., Odorizzi G., Emr S.D. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell. Biol. 2002, 3:893-905.
31. Killary A.M., Wolf M.E., Giambernardi T.A., Naylor S.L. Definition of a tumor suppressor locus within human chromosome 3p21-p22. Proc. Natl. Acad. Sci. USA 1992, 89:10877-10881.
32. Lalli C., Galasso C., Lo Castro A., Nardone A.M., Di Paolo A., Curatolo P. Interstitial deletion of a proximal 3p: a clinically recognisable syndrome. Brain Dev. 2007, 29:312-316.
33. 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.
34. Lott S.T., Lovell M., Naylor S.L., Killary A.M. Physical and functional mapping of a tumor suppressor locus for renal cell carcinoma within chromosome 3p12. Cancer Res. 1998, 58:3533-3537.
35. Lounis H., Mes-Masson A.M., Dion F., Bradley W.E., Seymour R.J., Provencher D., Tonin P.N. Mapping of chromosome 3p deletions in human epithelial ovarian tumors. Oncogene 1998, 17:2359-2365.
36. Maeda T., Chapman D.L., Stewart A.F. 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.
37. Manderson E.N., Presneau N., Provencher D., Mes-Masson A.M., Tonin P.N. Comparative analysis of loss of heterozygosity of specific chromosome 3, 13, 17, and X loci and TP53 mutations in human epithelial ovarian cancer. Mol. Carcinog. 2002, 34:78-90.
38. Manning A.P., Mes-Masson A.M., Seymour R.J., Tetrault M., Provencher D.M., Tonin P.N. Expression of FHIT in primary cultures of human epithelial ovarian tumors and malignant ovarian ascites. Mol. Carcinog. 1999, 24:218-225.
39. Marshall-Taylor C., Fanburg-Smith J.C. Fibrohistiocytic lipoma: twelve cases of a previously undescribed benign fatty tumor. Ann. Diagn. Pathol. 2000, 4:354-360.
40. Meis-Kindblom J.M., Kindblom L.G. Acral myxoinflammatory fibroblastic sarcoma: a low-grade tumor of the hands and feet. Am. J. Surg. Pathol. 1998, 22:911-924.
41. Montgomery E.A., Devaney K.O., Giordano T.J., Weiss S.W. Inflammatory myxohyaline tumor of distal extremities with virocyte or Reed-Sternberg-like cells: a distinctive lesion with features simulating inflammatory conditions, Hodgkin's disease, and various sarcomas. Mod. Pathol. 1998, 11:384-391.
42. Payne S.R., Kemp C.J. Tumor suppressor genetics. Carcinogenesis 2005, 26:2031-2045.
43. Pejovic T., Himmelmann A., Heim S., Mandahl N., Floderus U.M., Furgyik S., Elmfors B., Helm G., Willen H., Mitelman F. Prognostic impact of chromosome aberrations in ovarian cancer. Br. J. Cancer 1992, 65:282-286.
44. Presneau N., Mes-Masson A.M., Ge B., Provencher D., Hudson T.J., Tonin P.N. Patterns of expression of chromosome 17 genes in primary cultures of normal ovarian surface epithelia and epithelial ovarian cancer cell lines. Oncogene 2003, 22:1568-1579.
45. Provencher D.M., Lounis H., Champoux L., Tetrault M., Manderson E.N., Wang J.C., Eydoux P., Savoie R., Tonin P.N., Mes-Masson A.M. Characterization of four novel epithelial ovarian cancer cell lines. In Vitro Cell. Dev. Biol. Anim. 2000, 36:357-361.
46. Puck T.T., Cieciura S.J., Robinson A. Genetics of somatic mammalian cells. III. Long-term cultivation of euploid cells from human and animal subjects. J. Exp. Med. 1958, 108:945-956.
47. Quinn M.C., Filali-Mouhim A., Provencher D.M., Mes-Masson A.M., Tonin P.N. 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. Mol. Carcinog. 2009, 48:648-661.
48. Quinn M.C., Wilson D.J., Young F., Dempsey A.A., Arcand S.L., Birch A.H., Wojnarowicz P.M., Provencher D., Mes-Masson A.M., Englert D., Tonin P.N. The chemiluminescence based Ziplex automated workstation focus array reproduces ovarian cancer Affymetrix GeneChip expression profiles. J. Transl. Med. 2009, 7:55.
49. Salvador S., Gilks B., Kobel M., Huntsman D., Rosen B., Miller D. The fallopian tube: primary site of most pelvic high-grade serous carcinomas. Int. J. Gynecol. Cancer 2009, 19:58-64.
50. Sanchez Y., el-Naggar A., Pathak S., Killary A.M. 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.
51. 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.
52. Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9:671-675.
53. Seidman J.D., Horkayne-Szakaly I., Haiba M., Boice C.R., Kurman R.J., Ronnett B.M. The histologic type and stage distribution of ovarian carcinomas of surface epithelial origin. Int. J. Gynecol. Pathol. 2004, 23:41-44.
54. Singer G., Stohr R., Cope L., Dehari R., Hartmann A., Cao D.F., Wang T.L., Kurman R.J., Shih Ie M. Patterns of p53 mutations separate ovarian serous borderline tumors and low- and high-grade carcinomas and provide support for a new model of ovarian carcinogenesis: a mutational analysis with immunohistochemical correlation. Am. J. Surg. Pathol. 2005, 29:218-224.
55. Smilenov L.B. Tumor development: haploinsufficiency and local network assembly. Cancer Lett. 2006, 240:17-28.
56. TCGA Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474:609-615.
57. Therasse P., Arbuck S.G., Eisenhauer E.A., Wanders J., Kaplan R.S., Rubinstein L., Verweij J., Van Glabbeke M., van Oosterom A.T., Christian M.C., Gwyther S.G. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J. Natl. Cancer Inst. 2000, 92:205-216.
58. Tung C.S., Mok S.C., Tsang Y.T., Zu Z., Song H., Liu J., Deavers M.T., Malpica A., Wolf J.K., Lu K.H., Gershenson D.M., Wong K.K. PAX2 expression in low malignant potential ovarian tumors and low-grade ovarian serous carcinomas. Mod. Pathol. 2009, 22:1243-1250.
59. Vanderhyden B.C., Shaw T.J., Ethier J.F. Animal models of ovarian cancer. Reprod. Biol. Endocrinol. 2003, 1:67.
60. 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.
61. Wang L., Lu W., Chen Y.G., Zhou X.M., Gu J.R. 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.
62. Wojnarowicz P., Gambaro K., de Ladurantaye M., Quinn M.C.J., Provencher D., Mes-Masson A.-M., Tonin P.N. Overexpressing the CCL2 chemokine in an epithelial ovarian cancer cell line results in latency of in vivo tumourigenicity. Oncogenesis 2012, 1.
63. Wojnarowicz P.M., Oros K.K., Quinn M.C.J., Arcand S.L., Gambaro K., Madore J., Birch A.H., de Ladurantaye M., Rahimi K., Provencher D.M., Mes-Masson A.-M., Greenwood C.M.T., Tonin P.N. The genomic landscape of TP53 and p53 annotated high grade ovarian serous carcinomas from a defined founder population associated with patient outcome. PLoS ONE 2012, 7.
64. Zhang K., Lott S.T., Jin L., Killary A.M. Fine mapping of the NRC-1 tumor suppressor locus within chromosome 3p12. Biochem. Biophys. Res. Commun. 2007, 360:531-538.
65. Zietarska M., Maugard C.M., Filali-Mouhim A., Alam-Fahmy M., Tonin P.N., Provencher D.M., Mes-Masson A.M. Molecular description of a 3D in vitro model for the study of epithelial ovarian cancer (EOC). Mol. Carcinog. 2007, 46:872-885.