Lineage infidelity of epithelial ovarian cancers is controlled by HOX genes that specify regional identity in the reproductive tract

Nature Medicine

Volumn 11, Issue 5, 2005, Pages 531-537

  Cheng, Wenjun ^a,b   Liu, Jinsong ^a   Yoshida, Hiroyuki ^a   Rosen, Daniel ^a   Naora, Honami ^a  

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

^b JIANGSU CANCER HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL LINEAGE; CONTROLLED STUDY; FEMALE; FEMALE GENITAL SYSTEM; GENE; GENE EXPRESSION; HOX GENE; HOXA10 GENE; HOXA11 GENE; HOXA7 GENE; HOXA9 GENE; HUMAN; HUMAN TISSUE; MOUSE; MUELLERIAN DUCT; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; TUMOR DIFFERENTIATION;

ANIMALS; CELL DIFFERENTIATION; DNA PRIMERS; DNA, COMPLEMENTARY; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MICE; MULLERIAN DUCTS; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION;

ANIMALIA;

EID: 18344373769     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm1230     Document Type: Article

References (40)

1. Feeley, K.M. & Wells, M. Precursor lesions of ovarian epithelial malignancy. Histopathology 38, 87-95 (2001).
2. Auersperg, N., Wong, A.S., Choi, K.C., Kang, S.K. & Leung, P.C. Ovarian surface epithelium: Biology, endocrinology, and pathology. Endocr. Rev. 22, 255-288 (2001).
3. Shih, I. & Kurman, R.J. Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am. J. Pathol. 164, 1511-1518 (2004).
4. Mills, G.B. et al. The role of genetic abnormalities of PTEN and the phosphatidylinositol 3-kinase pathway in breast and ovarian tumorigenesis, prognosis, and therapy. Semin. Oncol. 28, 125-141 (2001).
5. Enomoto, T., Weghorst, C.M., Inoue, M., Tanizawa, O. & Rice, J.M. K-ras activation occurs frequently in mucinous adenocarcinomas and rarely in other common epithelial tumors of the human ovary. Am J Pathol. 139, 777-785 (1991).
6. Dinulescu, D.M. et al. Role of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat. Med. 11, 63-70 (2005).
7. Orsulic, S. et al. Induction of ovarian cancer by defined multiple genetic changes in a mouse model system. Cancer Cell 1, 53-62 (2002).
8. Connolly, D.C. et al. Female mice chimeric for expression of the simian virus 40 TAg under control of the MISIIR promoter develop epithelial ovarian cancer. Cancer Res. 63, 1389-1397 (2003).
9. Fleshken-Nikitin, A., Choi, K., Eng, J.P., Shmidt, E.N. & Nikitin, A.Y. Induction of carcinogenesis by concurrent inactivation of p53 and Rb1 in the mouse ovarian surface epithelium. Cancer Res. 63, 3459-3463 (2003).
10. McGinnis, W., Levine, M.S., Hafen, E., Kuroiwa, A. & Gehring, W.J. A conserved DNA sequence in homeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 308, 428-433 (1984).
11. Hsieh-Li, H.M. et al. Hoxa-11 structure, extensive antisense transcription and function in male and female sterility. Development 121, 1373-1385 (1995).
12. Benson, G.V. et al. Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development 122, 2687-2696 (1996).
13. Taylor, H.S., Vanden Heuvel, G.B. & Igarashi, P. A conserved Hox axis in the mouse and human female reproductive system: late establishment and persistent adult expression of the Hoxa cluster genes. Biol. Reprod. 57, 1338-1345 (1997).
14. Roby, K.F. et al. Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis 21, 585-591 (2000).
15. Schwartz, D.R. et al. Gene expression in ovarian cancer reflects both morphology and biological behavior, distinguishing clear cell from other poor-prognosis ovarian carcinomas. Cancer Res. 62, 4722-4729 (2002).
16. Lu, K.H. et al. Selection of potential markers for epithelial ovarian cancer with gene expression arrays and recursive descent partition analysis. Clin. Cancer Res. 10, 3291-3300 (2004).
17. Drapkin, R., Crum, C.P. & Hecht, J.L. Expression of candidate tumor markers in ovarian carcinoma and benign ovary: evidence for a link between epithelial phenotype and neoplasia. Hum. Pathol. 35, 1014-1021 (2004).
18. Hough, C.D. et al. Large-scale serial analysis of gene expression reveals genes differentially expressed in ovarian cancer. Cancer Res. 60, 6281-6287 (2000).
19. Bradgate, M.G. et al. Binding of anti-EMA, AGF 4:48 and the lectin UEA-1 to human ovarian carcinomas: histological and clinical correlations. Br. J. Obstet. Gynecol. 96, 854-860 (1989).
20. Albarracin, C.T., Jafri, J., Montag, A.G., Hart, J. & Kuan, S.F. Differential expression of MUC2 and MUC5AC mucin genes in primary ovarian and metastatic colonic carcinoma. Hum. Pathol. 31, 672-677 (2000).
21. Ordonez, N.G. Application of mesothelin immunostaining in tumor diagnosis. Am. J. Surg. Pathol. 27, 1418-1428 (2003).
22. Naora, H., Montz, F.J., Chai, C.Y. & Roden, R.B.S. Aberrant expression of homeobox gene HOXA7 is associated with müllerian-like differentiation of epithelial ovarian tumors and the generation of a specific autologous antibody response. Proc. Natl. Acad. Sci. USA 98, 15209-15214 (2001).
23. kip1 and Ki-67 expression provides independent information on overall survival of ovarian carcinoma patients. Gynecol. Oncol. 85, 404-414 (2002).
24. Naora, H. et al. A serologically identified tumor antigen encoded by a homeobox gene promotes growth of ovarian epithelial cells. Proc. Natl. Acad. Sci. USA 98, 4060-4065 (2001).
25. Care, A. et al. Enforced expression of HOXB7 promotes hematopoietic stem cell proliferation and myeloid-restricted progenitor differentiation. Oncogene 18, 1993-2001 (1999).
26. Liu, J. et al. A genetically defined model for human ovarian cancer. Cancer Res. 64, 1655-1663 (2004).
27. Dubeau, L. The cell of origin of ovarian epithelial tumors and the ovarian surface epithelium dogma: Does the emperor have no clothes? Gynecol. Oncol. 72, 437-442 (1999).
28. Magli, M.C., Largman, C. & Lawrence, H.J. Effects of HOX homeobox genes in blood cell differentiation. J. Cell. Pnysiol. 173, 168-177 (1997).
29. Ma, L., Benson, G.V., Lim, H., Dey, S.K. & Maas, R.L. AbdominalB (AbdB) Hoxa genes: regulation in adult uterus by estrogen and progesterone and repression in müllerian duct by the synthetic estrogen diethylstillbestrol (DES). Dev. Biol. 197, 141-154 (1998).
30. Sato, N. et al. Loss of heterozygosity on 10q23.3 and mutation of the tumor suppressor gene PTEN in benign endometrial cyst of the ovary: possible sequence progression from benign endometrial cyst to endometrioid and clear cell carcinoma of the ovary. Cancer Res. 60, 7052-7056 (2000).
31. Capo-chichi, C.D. et al. Anomalous expression of epithelial differentiation-determining GATA factors in ovarian tumorigenesis. Cancer Res. 63, 4967-4977 (2003).
32. Kroon, E. et al. Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. EMBO J. 17, 3714-3725 (1998).
33. Lim, H., Ma, L., Ma, W.G., Maas, R.L. & Dey, S.K. Hoxa10 regulates uterine stromal cell responsiveness to progesterone during implantation and decidualization in the mouse. Mol. Endocrinol. 13, 1005-1017 (1999).
34. Kobayashi, A. & Behringer, R.R. Developmental genetics of the female reproductive tract in mammals. Nat. Rev. Genet. 4, 969-980 (2003).
35. He, W.W. et al. A novel human prostate-specific, androgen-regulated homeobox gene (NKX3.1) that maps to 8p21, a region frequently deleted in prostate cancer. Genomics 43, 69-77 (1997).
36. Kim, M.J. et al. Cooperativity of Nkx3.1 and Pten loss of function in a mouse model of prostate carcinogenesis. Proc. Natl. Acad. Sci. USA 99, 2884-2889 (2002).
37. Bonhomme, C. et al. The Cdx2 homeobox gene has a tumor suppressor function in the distal colon in addition to a homeotic role during gut development. Gut 52, 1465-1471 (2003).
38. Abate-Shen, C. Deregulated homeobox gene expression in cancer: cause or consequence? Nature Rev. Cancer 2, 777-785 (2002).
39. Ford, H.L., Kabingu, E.N., Bump, E.A., Mutter, G.L. & Pardee, A.B. Abrogation of the G2 cell cycle checkpoint associated with overexpression of HSIX1: a possible mechanism of breast carcinogenesis. Proc. Natl. Acad. Sci. USA 95, 12608-12613 (1998).
40. Thorsteinsdottir, U. et al. Overexpression of HOXA10 in murine hematopoietic cells perturbs both myeloid and lymphoid differentiation and leads to acute myeloid leukemia. Mol. Cell. Biol. 17, 495-505 (1997).