A mouse model for endometrioid ovarian cancer arising from the distal oviduct

International Journal of Cancer

Volumn 135, Issue 5, 2014, Pages 1028-1037

  Van Der Horst, Paul H ^a   Van Der Zee, Marten ^a   Heijmans Antonissen, Claudia ^a   Jia, Yundan ^a   Demayo, Francesco J ^b   Lydon, John P ^b   Van Deurzen, Carolien H M ^a   Ewing, Patricia C ^a   Burger, Curt W ^a   Blok, Leen J ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

APC; endometrioid ovarian cancer; oviduct; tubal intraepithelial lesions; Wnt catenin signaling

Indexed keywords

BETA CATENIN; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER LOCALIZATION; CANCER MODEL; CARCINOGENESIS; CELL NUCLEUS; COLON POLYPOSIS; CONTROLLED STUDY; ENDOMETRIOID OVARIAN CANCER; ENDOMETRIUM; ENDOMETRIUM HYPERPLASIA; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MOUSE; MUELLERIAN DUCT; NONHUMAN; OVARIAN SURFACE EPITHELIUM CELL; OVARY CANCER; OVARY CYST; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TISSUE SECTION; TUMOR SUPPRESSOR GENE; UTERINE TUBE TUMOR;

APC; ENDOMETRIOID OVARIAN CANCER; OVIDUCT; TUBAL INTRAEPITHELIAL LESIONS; WNT/Β-CATENIN SIGNALING;

ADENOMATOUS POLYPOSIS COLI; ANIMALS; BETA CATENIN; CARCINOMA, ENDOMETRIOID; DISEASE MODELS, ANIMAL; ENDOMETRIAL HYPERPLASIA; ENDOMETRIUM; EPITHELIAL CELLS; FALLOPIAN TUBES; FEMALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASMS, EXPERIMENTAL; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84902547813     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28746     Document Type: Article

References (50)

1. Ferlay JSH, Bray F, Forman D, et al. GLOBOCAN 2008 v2.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10 [Internet]. [cited; Available from: http://globocan.iarc.fr, accessed on day/month/year].
2. Cannistra SA,. Cancer of the Ovary. N Engl J Med 2004; 351: 2519-29.
3. Dubeau L,. The cell of origin of ovarian epithelial tumors and the ovarian surface epithelium dogma: does the emperor have no clothes? Gynecol Oncol 1999; 72: 437-42.
4. Bowtell DD,. The genesis and evolution of high-grade serous ovarian cancer. Nat Rev Cancer 2010; 10: 803-8.
5. Crum CP, Drapkin R, Miron A, et al. The distal fallopian tube: a new model for pelvic serous carcinogenesis. Curr Opin Obstet Gynecol 2007; 19: 3-9.
6. Flesken-Nikitin A, Hwang CI, Cheng CY, et al. Ovarian surface epithelium at the junction area contains a cancer-prone stem cell niche. Nature 2013; 495: 241-5.
7. Piek JM, van Diest PJ, Zweemer RP, et al. Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer. J Pathol 2001; 195: 451-6.
8. Medeiros F, Muto MG, Lee Y, et al. The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome. Am J Surg Pathol 2006; 30: 230-6.
9. Kindelberger DW, Lee Y, Miron A, et al. Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship. Am J Surg Pathol 2007; 31: 161-9.
10. Wang Y, Sacchetti A, van Dijk MR, et al. Identification of quiescent, stem-like cells in the distal female reproductive tract. PLoS One 2012; 7: e40691.
11. Chen VW, Ruiz B, Killeen JL, et al. Pathology and classification of ovarian tumors. Cancer 2003; 97: 2631-42.
12. Gatcliffe TA, Monk BJ, Planutis K, et al. Wnt signaling in ovarian tumorigenesis. Int J Gynecol Cancer 2008; 18: 954-62.
13. van der Horst PH, Wang Y, van der Zee M, et al. Interaction between sex hormones and WNT/beta-catenin signal transduction in endometrial physiology and disease. Mol Cell Endocrinol 2012; 358: 176-84.
14. Palacios J, Gamallo C,. Mutations in the beta-catenin gene (CTNNB1) in endometrioid ovarian carcinomas. Cancer Res 1998; 58: 1344-7.
15. Gamallo C, Palacios J, Moreno G, et al. beta-catenin expression pattern in stage I and II ovarian carcinomas: relationship with beta-catenin gene mutations, clinicopathological features, and clinical outcome. Am J Pathol 1999; 155: 527-36.
16. Wright K, Wilson P, Morland S, et al. Beta-catenin mutation and expression analysis in ovarian cancer: exon 3 mutations and nuclear translocation in 16% of endometrioid tumours. Int J Cancer 1999; 82: 625-9.
17. Moreno-Bueno G, Gamallo C, Perez-Gallego L, et al. Beta-catenin expression pattern, beta-catenin gene mutations, and microsatellite instability in endometrioid ovarian carcinomas and synchronous endometrial carcinomas. Diagn Mol Pathol 2001; 10: 116-22.
18. Saegusa M, Okayasu I,. Frequent nuclear beta-catenin accumulation and associated mutations in endometrioid-type endometrial and ovarian carcinomas with squamous differentiation. J Pathol 2001; 194: 59-67.
19. Wu R, Zhai Y, Fearon ER, et al. Diverse mechanisms of beta-catenin deregulation in ovarian endometrioid adenocarcinomas. Cancer Res 2001; 61: 8247-55.
20. Kildal W, Risberg B, Abeler VM, et al. Beta-catenin expression, DNA ploidy and clinicopathological features in ovarian cancer: a study in 253 patients. Eur J Cancer 2005; 41: 1127-34.
21. Jacob F, Ukegjini K, Nixdorf S, et al. Loss of secreted frizzled-related protein 4 correlates with an aggressive phenotype and predicts poor outcome in ovarian cancer patients. PLoS One 2012; 7: e31885.
22. Yoshioka S, King ML, Ran S, et al. WNT7A regulates tumor growth and progression in ovarian cancer through the WNT/beta-catenin pathway. Mol Cancer Res 2012; 10: 469-82.
23. Soyal SM, Mukherjee A, Lee KY, et al. Cre-mediated recombination in cell lineages that express the progesterone receptor. Genesis 2005; 41: 58-66.
24. Robanus-Maandag EC, Koelink PJ, Breukel C, et al. A new conditional Apc-mutant mouse model for colorectal cancer. Carcinogenesis 2010; 31: 946-52.
25. Wang Y, Jia Y, Franken P, et al. Loss of APC function in mesenchymal cells surrounding the Mullerian duct leads to myometrial defects in adult mice. Mol Cell Endocrinol 2011; 341: 48-54.
26. Daniels DL, Weis WI,. Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat Struct Mol Biol 2005; 12: 364-71.
27. van der Zee M, Jia Y, Wang Y, et al. Alterations in Wnt/beta-catenin and Pten signaling play distinct roles in endometrial cancer initiation and progression. J Pathol 2013; 230: 48-58.
28. Conneely OM, Mulac-Jericevic B, Lydon JP,. Progesterone-dependent regulation of female reproductive activity by two distinct progesterone receptor isoforms. Steroids 2003; 68: 771-8.
29. Jarboe EA, Folkins AK, Drapkin R, et al. Tubal and ovarian pathways to pelvic epithelial cancer: a pathological perspective. Histopathology 2008; 53: 127-38.
30. Vang R, Visvanathan K, Gross A, et al. Validation of an algorithm for the diagnosis of serous tubal intraepithelial carcinoma. Int J Gynecol Pathol 2012; 31: 243-53.
31. Drewelus I, Gopfert C, Hippel C, et al. p63 Antagonizes Wnt-induced transcription. Cell Cycle 2010; 9: 580-7.
32. Boerboom D, Paquet M, Hsieh M, et al. Misregulated Wnt/beta-catenin signaling leads to ovarian granulosa cell tumor development. Cancer Res 2005; 65: 9206-15.
33. Al-Agha OM, Huwait HF, Chow C, et al. FOXL2 is a sensitive and specific marker for sex cord-stromal tumors of the ovary. Am J Surg Pathol 2011; 35: 484-94.
34. Chan KK, Wei N, Liu SS, et al. Estrogen receptor subtypes in ovarian cancer: a clinical correlation. Obstet Gynecol 2008; 111: 144-51.
35. Foulkes WD, Smith IE, Reis-Filho JS,. Triple-negative breast cancer. N Engl J Med 2010; 363: 1938-48.
36. Jeon YT, Park IA, Kim YB, et al. Steroid receptor expressions in endometrial cancer: clinical significance and epidemiological implication. Cancer Lett 2006; 239: 198-204.
37. Dinulescu DM, Ince TA, Quade BJ, et al. Role of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat Med 2005; 11: 63-70.
38. Wu R, Hendrix-Lucas N, Kuick R, et al. Mouse model of human ovarian endometrioid adenocarcinoma based on somatic defects in the Wnt/beta-catenin and PI3K/Pten signaling pathways. Cancer Cell 2007; 11: 321-33.
39. Kurman RJ, Shih Ie M,. Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer-shifting the paradigm. Hum Pathol 2011; 42: 918-31.
40. Romero I, Bast RC, Jr,. Minireview: human ovarian cancer: biology, current management, and paths to personalizing therapy. Endocrinology 2012; 153: 1593-1602.
41. Fan HY, Liu Z, Paquet M, et al. Cell type-specific targeted mutations of Kras and Pten document proliferation arrest in granulosa cells versus oncogenic insult to ovarian surface epithelial cells. Cancer Res 2009; 69: 6463-72.
42. Mullany LK, Fan HY, Liu Z, et al. Molecular and functional characteristics of ovarian surface epithelial cells transformed by KrasG12D and loss of Pten in a mouse model in vivo. Oncogene 2011; 30: 3522-36.
43. Kim J, Coffey DM, Creighton CJ, et al. High-grade serous ovarian cancer arises from fallopian tube in a mouse model. Proc Natl Acad Sci USA 2012; 109: 3921-6.
44. Tanwar PS, Kaneko-Tarui T, Lee HJ, et al. PTEN loss and HOXA10 expression are associated with ovarian endometrioid adenocarcinoma differentiation and progression. Carcinogenesis 2013; 34: 893-901.
45. Mehrad M, Ning G, Chen EY, et al. A pathologist's road map to benign, precancerous, and malignant intraepithelial proliferations in the fallopian tube. Adv Anat Pathol 2010; 17: 293-302.
46. Seidman JD, Zhao P, Yemelyanova A,. "Primary peritoneal" high-grade serous carcinoma is very likely metastatic from serous tubal intraepithelial carcinoma: assessing the new paradigm of ovarian and pelvic serous carcinogenesis and its implications for screening for ovarian cancer. Gynecol Oncol 2011; 120: 470-3.
47. Poli Neto OB, Candido Dos Reis FJ, Zambelli Ramalho LN, et al. p63 Expression in epithelial ovarian tumors. Int J Gynecol Cancer 2006; 16: 152-5.
48. Higashikawa K, Yoneda S, Tobiume K, et al. DeltaNp63alpha-dependent expression of Id-3 distinctively suppresses the invasiveness of human squamous cell carcinoma. Int J Cancer 2009; 124: 2837-44.
49. van der Horst PH, Wang YY, Vandenput I, et al. Progesterone inhibits epithelial-to-mesenchymal transition in endometrial cancer. PLoS One 2012; 7: e30840.
50. Dubeau L,. The cell of origin of ovarian epithelial tumours. Lancet Oncol 2008; 9: 1191-7.