Insights into endometrial serous carcinogenesis and progression

International Journal of Clinical and Experimental Pathology

Volumn 2, Issue 5, 2009, Pages 411-432

  Fadare, Oluwole ^a,b   Zheng, Wenxin ^c,d,e  

^a WILFORD HALL MEDICAL CENTER   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF ARIZONA   (United States)

^e SHANDONG UNIVERSITY   (China)

Author keywords

Cadherins; CDKs; Claudins; Endometrial glandular dysplasia; Endometrial intraepithelial carcinoma; Endometrial serous carcinoma; MDM2 and HER2 neu (erb B2); p53

Indexed keywords

EID: 67149086990     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Review

References (172)

1. Karpas CM and Bridge MF. Endometrial Adenocarcinoma with Psammomatous Bodies. Am J Obstet Gynecol 1963;87:935-941.
2. Factor SM. Papillary adenocarcinoma of the endometrium with psammoma bodies. Arch Pathol 1974;98:201-205.
3. Hameed K and Morgan DA. Papillary adenocarcinoma of endometrium with psammoma bodies. Histology and fine structure. Cancer 1972;29:1326-1335.
4. LiVolsi VA. Adenocarcinoma of the endometrium with psammoma bodies. Obstet Gynecol 1977;50:725-728.
5. Cefis F, Carinelli SG, Marzi MM and Senzani F. Endometrial adenocarcinoma with psammoma bodies. Tumori 1979;65:359-362.
6. Hendrickson MR and Kempson RL. Surgical pathology of the uterine corpus. WB Saunders, Philadelphia, 1980.
7. Lauchlan SC. Tubal (serous) carcinoma of the endometrium. Arch Pathol Lab Med 1981; 105:615-618.
8. Hendrickson M, Ross J, Eifel P, Martinez A and Kempson R. Uterine papillary serous carcinoma: a highly malignant form of endometrial adenocarcinoma. Am J Surg Pathol 1982;6:93-108.
9. Christopherson WM, Alberhasky RC and Connelly PJ. Carcinoma of the endometrium. II. Papillary adenocarcinoma: a clinical pathological study, 46 cases. Am J Clin Pathol 1982;77:534-540.
10. Walker AN and Mills SE. Serous papillary carcinoma of the endometrium. A clinicopathologic study of 11 cases. Diagn Gynecol Obstet 1982;4:261-267.
11. Hendrickson M, Ross J, Eifel PJ, Cox RS, Martinez A and Kempson R. Adenocarcinoma of the endometrium: analysis of 256 cases with carcinoma limited to the uterine corpus. Pathology review and analysis of prognostic variables. Gynecol Oncol 1982;13:373-392.
12. Bokhman JV. Two pathogenetic types of endometrial carcinoma. Gynecol Oncol 1983; 15:10-17.
13. Lax SF and Kurman RJ. A dualistic model for endometrial carcinogenesis based on immunohistochemical and molecular genetic analyses. Verh Dtsch Ges Pathol 1997;81: 228-232.
14. Lampe B, Kurzl R and Kindermann G. [Serous papillary adenocarcinoma of the endometrium]. Geburtshilfe Frauenheilkd 1991;51:45-50.
15. Darvishian F, Hummer AJ, Thaler HT, Bhargava R, Linkov I, Asher M and Soslow RA. Serous endometrial cancers that mimic endometrioid adenocarcinomas: a clinicopathologic and immunohistochemical study of a group of problematic cases. Am J Surg Pathol 2004;28:1568-1578.
16. Slomovitz BM, Burke TW, Eifel PJ, Ramondetta LM, Silva EG, Jhingran A, Oh JC, Atkinson EN, Broaddus RR, Gershenson DM and Lu KH. Uterine papillary serous carcinoma (UPSC): a single institution review of 129 cases. Gynecol Oncol 2003;91:463-469.
17. Hamilton CA, Cheung MK, Osann K, Chen L, Teng NN, Longacre TA, Powell MA, Hendrickson MR, Kapp DS and Chan JK. Uterine papillary serous and clear cell carcinomas predict for poorer survival compared to grade 3 endometrioid corpus cancers. Br J Cancer 2006;94:642-646.
18. Jordan LB, Abdul-Kader M and Al-Nafussi A. Uterine serous papillary carcinoma: histopathologic changes within the female genital tract. Int J Gynecol Cancer 2001;11: 283-289.
19. Sherman ME and Devesa SS. Analysis of racial differences in incidence, survival, and mortality for malignant tumors of the uterine corpus. Cancer 2003;98:176-186.
20. Alektiar KM, McKee A, Lin O, Venkatraman E, Zelefsky MJ, McKee B, Hoskins WJ and Barakat RR. Is there a difference in outcome between stage I-II endometrial cancer of papillary serous/clear cell and endometrioid FIGO Grade 3 cancer? Int J Radiat Oncol Biol Phys 2002;54:79-85.
21. Soslow RA, Bissonnette JP, Wilton A, Ferguson SE, Alektiar KM, Duska LR and Oliva E. Clinicopathologic analysis of 187 high-grade endometrial carcinomas of different histologic subtypes: similar outcomes belie distinctive biologic differences. Am J Surg Pathol 2007; 31:979-987.
22. Boruta DM, 2nd, Gehrig PA, Groben PA, Bae-Jump V, Boggess JF, Fowler WC, Jr. and Van Le L. Uterine serous and grade 3 endometrioid carcinomas: is there a survival difference? Cancer 2004;101:2214-2221.
23. Sagr ER, Denschlag D, Kerim-Dikeni A, Stanimir G, Gitsch G and Gilbert L. Prognostic factors and treatment-related outcome in patients with uterine papillary serous carcinoma. Anticancer Res 2007;27:1213-1217.
24. Faratian D, Stillie A, Busby-Earle RM, Cowie VJ and Monaghan H. A review of the pathology and management of uterine papillary serous carcinoma and correlation with outcome. Int J Gynecol Cancer 2006; 16:972-978.
25. Chan JK, Loizzi V, Youssef M, Osann K, Rutgers J, Vasilev SA and Berman ML. Significance of comprehensive surgical staging in noninvasive papillary serous carcinoma of the endometrium. Gynecol Oncol 2003;90:181-185.
26. Gehrig PA, Groben PA, Fowler WC, Jr., Walton LA and Van Le L. Noninvasive papillary serous carcinoma of the endometrium. Obstet Gynecol 2001;97:153-157.
27. Carcangiu ML, Tan LK and Chambers JT. Stage IA uterine serous carcinoma: a study of 13 cases. Am J Surg Pathol 1997;21:1507-1514.
28. Hui P, Kelly M, O'Malley DM, Tavassoli F and Schwartz PE. Minimal uterine serous carcinoma: a clinicopathological study of 40 cases. Mod Pathol 2005;18:75-82.
29. Wheeler DT, Bell KA, Kurman RJ and Sherman ME. Minimal uterine serous carcinoma: diagnosis and clinicopathologic correlation. Am J Surg Pathol 2000;24:797-806.
30. Clement PB and Young RH. Endometrioid carcinoma of the uterine corpus: a review of its pathology with emphasis on recent advances and problematic aspects. Adv Anat Pathol 2002;9:145-184.
31. Kurman RJ, Kaminski PF and Norris HJ. The behavior of endometrial hyperplasia. A long-term study of "untreated" hyperplasia in 170 patients. Cancer 1985;56:403-412.
32. Mutter GL, Zaino RJ, Baak JP, Bentley RC and Robboy SJ. Benign endometrial hyperplasia sequence and endometrial intraepithelial neoplasia. Int J Gynecol Pathol 2007;26:103-114.
33. Hecht JL and Mutter GL. Molecular and pathologic aspects of endometrial carcinogenesis. J Clin Oncol 2006;24:4783-4791.
34. Lee KR and Belinson JL. Recurrence in noninvasive endometrial carcinoma. Relationship to uterine papillary serous carcinoma. Am J Surg Pathol 1991;15:965-973.
35. Sherman ME, Bitterman P, Rosenshein NB, Delgado G and Kurman RJ. Uterine serous carcinoma. A morphologically diverse neoplasm with unifying clinicopathologic features. Am J Surg Pathol 1992;16:600-610.
36. Spiegel GW. Endometrial carcinoma in situ in postmenopausal women. Am J Surg Pathol 1995;19:417-432.
37. Ambros RA, Sherman ME, Zahn CM, Bitterman P and Kurman RJ. Endometrial intraepithelial carcinoma: a distinctive lesion specifically associated with tumors displaying serous differentiation. Hum Pathol 1995;26: 1260-1267.
38. Zheng W, Khurana R, Farahmand S, Wang Y, Zhang ZF and Felix JC. p53 immunostaining as a significant adjunct diagnostic method for uterine surface carcinoma: precursor of uterine papillary serous carcinoma. Am J Surg Pathol 1998;22:1463-1473.
39. Silva EG and Jenkins R. Serous carcinoma in endometrial polyps. Mod Pathol 1990;3: 120-128.
40. Carcangiu ML and Chambers JT. Uterine papillary serous carcinoma: a study on 108 cases with emphasis on the prognostic significance of associated endometrioid carcinoma, absence of invasion, and concomitant ovarian carcinoma. Gynecol Oncol 1992;47:298-305.
41. Soslow RA, Pirog E and Isacson C. Endometrial intraepithelial carcinoma with associated peritoneal carcinomatosis. Am J Surg Pathol 2000;24:726-732.
42. Baergen RN, Warren CD, Isacson C and Ellenson LH. Early uterine serous carcinoma: clonal origin of extrauterine disease. Int J Gynecol Pathol 2001;20:214-219.
43. Euscher ED, Malpica A, Deavers MT and Silva EG. Differential expression of WT-1 in serous carcinomas in the peritoneum with or without associated serous carcinoma in endometrial polyps. Am J Surg Pathol 2005;29:1074-1078.
44. Acs G, Pasha T and Zhang PJ. WT1 is differentially expressed in serous, endometrioid, clear cell, and mucinous carcinomas of the peritoneum, fallopian tube, ovary, and endometrium. Int J Gynecol Pathol 2004;23:110-118.
45. Fadare O and Zheng W. Endometrial Glandular Dysplasia (EmGD): morphologically and biologically distinctive putative precursor lesions of Type II endometrial cancers. Diagn Pathol 2008;3:6.
46. Clement PB and Young RH. Non-endometrioid carcinomas of the uterine corpus: a review of their pathology with emphasis on recent advances and problematic aspects. Adv Anat Pathol 2004;11:117-142.
47. Zheng W and Schwartz PE. Serous EIC as an early form of uterine papillary serous carcinoma: recent progress in understanding its pathogenesis and current opinions regarding pathologic and clinical management. Gynecol Oncol 2005;96:579-582.
48. Schwartz PE. The management of serous papillary uterine cancer. Curr Opin Oncol 2006;18:494-499.
49. Zheng W, Liang SX, Yu H, Rutherford T, Chambers SK and Schwartz PE. Endometrial glandular dysplasia: a newly defined precursor lesion of uterine papillary serous carcinoma. Part I: morphologic features. Int J Surg Pathol 2004;12:207-223.
50. Liang SX, Chambers SK, Cheng L, Zhang S, Zhou Y and Zheng W. Endometrial glandular dysplasia: a putative precursor lesion of uterine papillary serous carcinoma. Part II: molecular features. Int J Surg Pathol 2004;12: 319-331.
51. Jia L, Liu Y, Yi X, Miron A, Crum CP, Kong B and Zheng W. Endometrial glandular dysplasia with frequent p53 gene mutation: a genetic evidence supporting its precancer nature for endometrial serous carcinoma. Clin Cancer Res 2008;14:2263-2269.
52. Zheng W, Liang SX, Yi X, Ulukus EC, Davis JR and Chambers SK. Occurrence of endometrial glandular dysplasia precedes uterine papillary serous carcinoma. Int J Gynecol Pathol 2007;26:38-52.
53. Yi X and Zheng W. Endometrial glandular dysplasia and endometrial intraepithelial neoplasia. Curr Opin Obstet Gynecol 2008; 20:20-25.
54. Berman JJ, Albores-Saavedra J, Bostwick D, Delellis R, Eble J, Hamilton SR, Hruban RH, Mutter GL, Page D, Rohan T, Travis W and Henson DE. Precancer: a conceptual working definition - results of a Consensus Conference. Cancer Detect Prev 2006;30: 387-394.
55. Pietsch EC, Sykes SM, McMahon SB and Murphy ME. The p53 family and programmed cell death. Oncogene 2008;27:6507-6521.
56. Harris CC. 1995 Deichmann Lecture - p53 tumor suppressor gene: at the crossroads of molecular carcinogenesis, molecular epidemiology and cancer risk assessment. Toxicol Lett 1995;82-83:1-7.
57. Tashiro H, Isacson C, Levine R, Kurman RJ, Cho KR and Hedrick L. p53 gene mutations are common in uterine serous carcinoma and occur early in their pathogenesis. Am J Pathol 1997;150:177-185.
58. King SA, Adas AA, LiVolsi VA, Takahashi H, Behbakht K, McGovern P, Benjamin I, Rubin SC and Boyd J. Expression and mutation analysis of the p53 gene in uterine papillary serous carcinoma. Cancer 1995;75:2700-2705.
59. Kovalev S, Marchenko ND, Gugliotta BG, Chalas E, Chumas J and Moll UM. Loss of p53 function in uterine papillary serous carcinoma. Hum Pathol 1998;29:613-619.
60. Lax SF, Kendall B, Tashiro H, Slebos RJ and Hedrick L. The frequency of p53, K-ras mutations, and microsatellite instability differs in uterine endometrioid and serous carcinoma: evidence of distinct molecular genetic pathways. Cancer 2000;88:814-824.
61. Sakuragi N, Hirai A, Tada M, Yamada H, Yamamoto R, Fujimoto S and Moriuchi T. Dominant-negative mutation of p53 tumor suppressor gene in endometrial carcinoma. Gynecol Oncol 2001;83:485-490.
62. Sherman ME, Bur ME and Kurman RJ. p53 in endometrial cancer and its putative precursors: evidence for diverse pathways of tumorigenesis. Hum Pathol 1995;26:1268-1274.
63. Prat J, Oliva E, Lerma E, Vaquero M and Matias-Guiu X. Uterine papillary serous adenocarcinoma. A 10-case study of p53 and c-erbB-2 expression and DNA content. Cancer 1994;74:1778-1783.
64. Moll UM, Chalas E, Auguste M, Meaney D and Chumas J. Uterine papillary serous carcinoma evolves via a p53-driven pathway. Hum Pathol 1996;27:1295-1300.
65. Bancher-Todesca D, Gitsch G, Williams KE, Kohlberger P, Neunteufel W, Obermair A, Heinze G, Breitenecker G and Hacker NF. p53 protein overexpression: a strong prognostic factor in uterine papillary serous carcinoma. Gynecol Oncol 1998;71:59-63.
66. Kounelis S, Kapranos N, Kouri E, Coppola D, Papadaki H and Jones MW. Immunohistochemical profile of endometrial adenocarcinoma: a study of 61 cases and review of the literature. Mod Pathol 2000;13: 379-388.
67. Demopoulos RI, Mesia AF, Mittal K and Vamvakas E. Immunohistochemical comparison of uterine papillary serous and papillary endometrioid carcinoma: clues to pathogenesis. Int J Gynecol Pathol 1999;18: 233-237.
68. Busmanis I, Ho TH, Tan SB and Khoo KS. p53 and bcl-2 expression in invasive and pre-invasive uterine papillary serous carcinoma and atrophic endometrium. Ann Acad Med Singapore 2005;34:421-425.
69. Lax SF, Pizer ES, Ronnett BM and Kurman RJ. Clear cell carcinoma of the endometrium is characterized by a distinctive profile of p53, Ki-67, estrogen, and progesterone receptor expression. Hum Pathol 1998;29:551-558.
70. Zheng W, Cao P, Zheng M, Kramer EE and Godwin TA. p53 overexpression and bcl-2 persistence in endometrial carcinoma: comparison of papillary serous and endometrioid subtypes. Gynecol Oncol 1996; 61:167-174.
71. Erkanli S, Eren F, Pekin S and Bagis T. BCL-2 and P53 expression in endometrial carcinoma. J Exp Clin Cancer Res 2004;23: 97-103.
72. Halperin R, Zehavi S, Habler L, Hadas E, Bukovsky I and Schneider D. Comparative immunohistochemical study of endometrioid and serous papillary carcinoma of endometrium. Eur J Gynaecol Oncol 2001;22: 122-126.
73. Soslow RA, Shen PU, Chung MH and Isacson C. Distinctive p53 and mdm2 immunohistochemical expression profiles suggest different pathogenetic pathways in poorly differentiated endometrial carcinoma. Int J Gynecol Pathol 1998;17:129-134.
74. Ambros RA, Sheehan CE, Kallakury BV, Ross JS, Malfetano J, Paunovich E and Figge J. MDM2 and p53 protein expression in the histologic subtypes of endometrial carcinoma. Mod Pathol 1996;9:1165-1169.
75. Stewart RL, Royds JA, Burton JL, Heatley MK and Wells M. Direct sequencing of the p53 gene shows absence of mutations in endometrioid endometrial adenocarcinomas expressing p53 protein. Histopathology 1998; 33:440-445.
76. Reinartz JJ, George E, Lindgren BR and Niehans GA. Expression of p53, transforming growth factor alpha, epidermal growth factor receptor, and c-erbB-2 in endometrial carcinoma and correlation with survival and known predictors of survival. Hum Pathol 1994;25:1075-1083.
77. Sung CJ, Zheng Y, Quddus MR, Kang X, Zhang ZF, Lauchlan SC and Zheng W. p53 as a significant prognostic marker in endometrial carcinoma. Int J Gynecol Cancer 2000;10: 119-127.
78. Nordstrom B, Strang P, Lindgren A, Bergstrom R and Tribukait B. Endometrial carcinoma: the prognostic impact of papillary serous carcinoma (UPSC) in relation to nuclear grade, DNA ploidy and p53 expression. Anticancer Res 1996;16:899-904.
79. Sorbe B, Risberg B and Frankendal B. DNA ploidy, morphometry, and nuclear grade as prognostic factors in endometrial carcinoma. Gynecol Oncol 1990;38:22-27.
80. Rosenberg P, Wingren S, Simonsen E, Stal O, Risberg B and Nordenskjold B. Flow cytometric measurements of DNA index and S-phase on paraffin-embedded early stage endometrial cancer: an important prognostic indicator. Gynecol Oncol 1989;35:50-54.
81. Tritz D, Pieretti M, Turner S and Powell D. Loss of heterozygosity in usual and special variant carcinomas of the endometrium. Hum Pathol 1997;28:607-612.
82. Arlt MF, Herzog TJ, Mutch DG, Gersell DJ, Liu H and Goodfellow PJ. Frequent deletion of chromosome 1p sequences in an aggressive histologic subtype of endometrial cancer. Hum Mol Genet 1996;5:1017-1021.
83. Quddus MR, Sung CJ, Zheng W and Lauchlan SC. p53 immunoreactivity in endometrial metaplasia with dysfunctional uterine bleeding. Histopathology 1999;35:44-49.
84. Crum CP, Drapkin R, Kindelberger D, Medeiros F, Miron A and Lee Y. Lessons from BRCA: the tubal fimbria emerges as an origin for pelvic serous cancer. Clin Med Res 2007; 5:35-44.
85. Saleemuddin A, Folkins AK, Garrett L, Garber J, Muto MG, Crum CP and Tworoger S. Risk factors for a serous cancer precursor ("p53 signature") in women with inherited BRCA mutations. Gynecol Oncol 2008;111:226-232.
86. Jarboe E, Folkins A, Nucci MR, Kindelberger D, Drapkin R, Miron A, Lee Y and Crum CP. Serous carcinogenesis in the fallopian tube: a descriptive classification. Int J Gynecol Pathol 2008;27:1-9.
87. Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, Garber J, Birch C, Mou H, Gordon RW, Cramer DW, McKeon FD and Crum CP. A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol 2007;211:26-35.
88. Zhang X, Liang SX, Jia L, Chen N, Fadare O, Schwartz PE, Kong B and Zheng W. Molecular identification of "latent precancers" for endometrial serous carcinoma in benign appearing dndometrium. Am J Pathol (under review)
89. Cheung AL and Deng W. Telomere dysfunction, genome instability and cancer. Front Biosci 2008;13:2075-2090.
90. Akbay EA, Contreras CM, Perera SA, Sullivan JP, Broaddus RR, Schorge JO, Ashfaq R, Saboorian H, Wong KK and Castrillon DH. Differential roles of telomere attrition in type I and II endometrial carcinogenesis. Am J Pathol 2008;173:536-544.
91. Lachance JA, Everett EN, Greer B, Mandel L, Swisher E, Tamimi H and Goff B. The effect of age on clinical/pathologic features, surgical morbidity, and outcome in patients with endometrial cancer. Gynecol Oncol 2006;101: 470-475.
92. Catasus L, Machin P, Matias-Guiu X and Prat J. Microsatellite instability in endometrial carcinomas: clinicopathologic correlations in a series of 42 cases. Hum Pathol 1998; 29:1160-1164.
93. Kurita T and Cunha GR. Roles of p63 in differentiation of Mullerian duct epithelial cells. Ann N Y Acad Sci 2001;948:9-12.
94. O'Connell JT, Mutter GL, Cviko A, Nucci M, Quade BJ, Kozakewich HP, Neffen E, Sun D, Yang A, McKeon FD and Crum CP. Identification of a basal/reserve cell immunophenotype in benign and neoplastic endometrium: a study with the p53 homologue p63. Gynecol Oncol 2001;80:30-36.
95. Idrees MT, Schlosshauer P, Li G and Burstein DE. GLUT1 and p63 expression in endometrial intraepithelial and uterine serous papillary carcinoma. Histopathology 2006;49: 75-81.
96. Casalini P and Iorio MV. ERBB2 (erythroblastic leukemia viral oncogene homolog 2, neuro/glioblastoma derived oncogene homolog (avian) ). Atlas Genet Cytogenet Oncol Haematol. December 2004. http:// AtlasGeneticsOncology.org/Genes/ERBB2ID162ch17q11.html Accessed 13 December 2008
97. Graus-Porta D, Beerli RR, Daly JM and Hynes NE. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 1997;16:1647-1655.
98. Busse D, Doughty RS and Arteaga CL. HER-2/neu (erbB-2) and the cell cycle. Semin Oncol 2000;27:3-8; discussion 92-100.
99. Lofts FJ and Gullick WJ. c-erbB2 amplification and overexpression in human tumors. Cancer Treat Res 1992;61:161-179.
100. Ferretti G, Felici A, Papaldo P, Fabi A and Cognetti F. HER2/neu role in breast cancer: from a prognostic foe to a predictive friend. Curr Opin Obstet Gynecol 2007;19:56-62.
101. Dhesy-Thind B, Pritchard KI, Messersmith H, O'Malley F, Elavathil L and Trudeau M. HER2/neu in systemic therapy for women with breast cancer: a systematic review. Breast Cancer Res Treat 2008;109:209-229.
102. Santin AD, Bellone S, Gokden M, Palmieri M, Dunn D, Agha J, Roman JJ, Hutchins L, Pecorelli S, O'Brien T, Cannon MJ and Parham GP. Overexpression of HER-2/neu in uterine serous papillary cancer. Clin Cancer Res 2002;8:1271-1279.
103. Santin AD, Bellone S, Van Stedum S, Bushen W, Palmieri M, Siegel ER, De Las Casas LE, Roman JJ, Burnett A and Pecorelli S. Amplification of c-erbB2 oncogene: a major prognostic indicator in uterine serous papillary carcinoma. Cancer 2005;104:1391-1397.
104. Santin AD, Bellone S, Siegel ER, Palmieri M, Thomas M, Cannon MJ, Kay HH, Roman JJ, Burnett A and Pecorelli S. Racial differences in the overexpression of epidermal growth factor type II receptor (HER2/neu): a major prognostic indicator in uterine serous papillary cancer. Am J Obstet Gynecol 2005; 192:813-818.
105. Villella JA, Cohen S, Smith DH, Hibshoosh H and Hershman D. HER-2/neu overexpression in uterine papillary serous cancers and its possible therapeutic implications. Int J Gynecol Cancer 2006;16:1897-1902.
106. Santin AD, Bellone S, Van Stedum S, Bushen W, De Las Casas LE, Korourian S, Tian E, Roman JJ, Burnett A and Pecorelli S. Determination of HER2/ neu status in uterine serous papillary carcinoma: Comparative analysis of immunohistochemistry and fluorescence in situ hybridization. Gynecol Oncol 2005;98:24-30.
107. Slomovitz BM, Broaddus RR, Burke TW, Sneige N, Soliman PT, Wu W, Sun CC, Munsell MF, Gershenson DM and Lu KH. Her-2/neu overexpression and amplification in uterine papillary serous carcinoma. J Clin Oncol 2004; 22:3126-3132.
108. Odicino FE, Bignotti E, Rossi E, Pasinetti B, Tassi RA, Donzelli C, Falchetti M, Fontana P, Grigolato PG and Pecorelli S. HER-2/neu overexpression and amplification in uterine serous papillary carcinoma: comparative analysis of immunohistochemistry, real-time reverse transcription-polymerase chain reaction, and fluorescence in situ hybridization. Int J Gynecol Cancer 2008;18: 14-21.
109. Singh P, Smith CL, Cheetham G, Dodd TJ and Davy ML. Serous carcinoma of the uterus-determination of HER-2/neu status using immunohistochemistry, chromogenic in situ hybridization, and quantitative polymerase chain reaction techniques: its significance and clinical correlation. Int J Gynecol Cancer 2008
110. Nofech-Mozes S, Khalifa MA, Ismiil N, Saad RS, Hanna WM, Covens A and Ghorab Z. Immunophenotyping of serous carcinoma of the female genital tract. Mod Pathol 2008; 21:1147-1155.
111. Morrison C, Zanagnolo V, Ramirez N, Cohn DE, Kelbick N, Copeland L, Maxwell GL and Fowler JM. HER-2 is an independent prognostic factor in endometrial cancer: association with outcome in a large cohort of surgically staged patients. J Clin Oncol 2006; 24:2376-2385.
112. Ejskjaer K, Sorensen BS, Poulsen SS, Forman A, Nexo E and Mogensen O. Expression of the epidermal growth factor system in endometrioid endometrial cancer. Gynecol Oncol 2007;104:158-167.
113. Macwhinnie N and Monaghan H. The use of P53, PTEN, and C-erbB-2 to differentiate uterine serous papillary carcinoma from endometrioid endometrial carcinoma. Int J Gynecol Cancer 2004;14:938-946.
114. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL, Brown PO and Botstein D. Molecular portraits of human breast tumours. Nature 2000;406:747-752.
115. Fadare O and Tavassoli FA. Clinical and pathologic aspects of basal-like breast cancers. Nat Clin Pract Oncol 2008;5:149-159.
116. Hajra KM and Fearon ER. Cadherin and catenin alterations in human cancer. Genes Chromosomes Cancer 2002;34:255-268.
117. Jeanes A, Gottardi CJ and Yap AS. Cadherins and cancer: how does cadherin dysfunction promote tumor progression? Oncogene 2008; 27:6920-6929.
118. Hirohashi S. Inactivation of the E-cadherin-mediated cell adhesion system in human cancers. Am J Pathol 1998;153:333-339.
119. Mell LK, Meyer JJ, Tretiakova M, Khramtsov A, Gong C, Yamada SD, Montag AG and Mundt AJ. Prognostic significance of E-cadherin protein expression in pathological stage I-III endometrial cancer. Clin Cancer Res 2004; 10:5546-5553.
120. Stefansson IM, Salvesen HB and Akslen LA. Prognostic impact of alterations in P-cadherin expression and related cell adhesion markers in endometrial cancer. J Clin Oncol 2004;22: 1242-1252.
121. Holcomb K, Delatorre R, Pedemonte B, McLeod C, Anderson L and Chambers J. E-cadherin expression in endometrioid, papillary serous, and clear cell carcinoma of the endometrium. Obstet Gynecol 2002;100: 1290-1295.
122. Shaco-Levy R, Sharabi S, Piura B and Sion-Vardy N. MMP-2, TIMP-1, E-cadherin, and beta-catenin expression in endometrial serous carcinoma compared with low-grade endometrial endometrioid carcinoma and proliferative endometrium. Acta Obstet Gynecol Scand 2008;87:868-874.
123. Schlosshauer PW, Ellenson LH and Soslow RA. Beta-catenin and E-cadherin expression patterns in high-grade endometrial carcinoma are associated with histological subtype. Mod Pathol 2002;15:1032-1037.
124. Guarino M, Rubino B and Ballabio G. The role of epithelial-mesenchymal transition in cancer pathology. Pathology 2007;39:305-318.
125. Singh M, Spoelstra NS, Jean A, Howe E, Torkko KC, Clark HR, Darling DS, Shroyer KR, Horwitz KB, Broaddus RR and Richer JK. ZEB1 expression in type I vs type II endometrial cancers: a marker of aggressive disease. Mod Pathol 2008;21:912-923.
126. Giehl K and Menke A. Microenvironmental regulation of E-cadherin-mediated adherens junctions. Front Biosci 2008;13:3975-3985.
127. Livasy CA, Moore D, Cance WG and Lininger RA. Focal adhesion kinase overexpression in endometrial neoplasia. Appl Immunohistochem Mol Morphol 2004;12: 342-345.
128. Abe M, Sugiura T, Takahashi M, Ishii K, Shimoda M and Shirasuna K. A novel function of CD82/KAI-1 on E-cadherin-mediated homophilic cellular adhesion of cancer cells. Cancer Lett 2008;266:163-170.
129. Briese J, Schulte HM, Sajin M, Bamberger C, Redlin K, Milde-Langosch K, Loning T and Bamberger AM. Correlations between reduced expression of the metastasis suppressor gene KAI-1 and accumulation of p53 in uterine carcinomas and sarcomas. Virchows Arch 2008;453:89-96.
130. Kanai Y, Ochiai A, Shibata T, Oyama T, Ushijima S, Akimoto S and Hirohashi S. c-erbB-2 gene product directly associates with beta-catenin and plakoglobin. Biochem Biophys Res Commun 1995;208:1067-1072.
131. Ochiai A, Akimoto S, Kanai Y, Shibata T, Oyama T and Hirohashi S. c-erbB-2 gene product associates with catenins in human cancer cells. Biochem Biophys Res Commun 1994;205:73-78.
132. Moon HS, Choi EA, Park HY, Choi JY, Chung HW, Kim JI and Park WI. Expression and tyrosine phosphorylation of E-cadherin, beta-and gamma-catenin, and epidermal growth factor receptor in cervical cancer cells. Gynecol Oncol 2001;81:355-359.
133. Tsukita S, Yamazaki Y, Katsuno T and Tamura A. Tight junction-based epithelial microenvironment and cell proliferation. Oncogene 2008;27:6930-6938.
134. Heiskala M, Peterson PA and Yang Y. The roles of claudin superfamily proteins in paracellular transport. Traffic 2001;2:93-98.
135. Facchetti F, Lonardi S, Gentili F, Bercich L, Falchetti M, Tardanico R, Baronchelli C, Lucini L, Santin A and Murer B. Claudin 4 identifies a wide spectrum of epithelial neoplasms and represents a very useful marker for carcinoma versus mesothelioma diagnosis in pleural and peritoneal biopsies and effusions. Virchows Arch 2007;451:669-680.
136. Rangel LB, Agarwal R, D'Souza T, Pizer ES, Alo PL, Lancaster WD, Gregoire L, Schwartz DR, Cho KR and Morin PJ. Tight junction proteins claudin-3 and claudin-4 are frequently overexpressed in ovarian cancer but not in ovarian cystadenomas. Clin Cancer Res 2003; 9:2567-2575.
137. Santin AD, Zhan F, Bellone S, Palmieri M, Cane S, Bignotti E, Anfossi S, Gokden M, Dunn D, Roman JJ, O'Brien TJ, Tian E, Cannon MJ, Shaughnessy J Jr and Pecorelli S. 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.
138. Agarwal R, D'Souza T and Morin PJ. Claudin-3 and claudin-4 expression in ovarian epithelial cells enhances invasion and is associated with increased matrix metalloproteinase-2 activity. Cancer Res 2005;65:7378-7385.
139. Santin AD, Zhan F, Cane S, Bellone S, Palmieri M, Thomas M, Burnett A, Roman JJ, Cannon MJ, Shaughnessy J Jr and Pecorelli S. Gene expression fingerprint of uterine serous papillary carcinoma: identification of novel molecular markers for uterine serous cancer diagnosis and therapy. Br J Cancer 2005;92: 1561-1573.
140. Konecny GE, Agarwal R, Keeney GA, Winterhoff B, Jones MB, Mariani A, Riehle D, Neuper C, Dowdy SC, Wang HJ, Morin PJ and Podratz KC. Claudin-3 and claudin-4 expression in serous papillary, clear-cell, and endometrioid endometrial cancer. Gynecol Oncol 2008;109:263-269.
141. Sobel G, Nemeth J, Kiss A, Lotz G, Szabo I, Udvarhelyi N, Schaff Z and Paska C. Claudin 1 differentiates endometrioid and serous papillary endometrial adenocarcinoma. Gynecol Oncol 2006;103:591-598.
142. Santin AD, Bellone S, Marizzoni M, Palmieri M, Siegel ER, McKenney JK, Hennings L, Comper F, Bandiera E and Pecorelli S. Overexpression of claudin-3 and claudin-4 receptors in uterine serous papillary carcinoma: novel targets for a type-specific therapy using Clostridium perfringens enterotoxin (CPE). Cancer 2007;109:1312-1322.
143. Viallard JF, Lacombe F, Belloc F, Pellegrin JL and Reiffers J. [Molecular mechanisms controlling the cell cycle: fundamental aspects and implications for oncology]. Cancer Radiother 2001;5:109-129.
144. MacLachlan TK, Sang N and Giordano A. Cyclins, cyclin-dependent kinases and cdk inhibitors: implications in cell cycle control and cancer. Crit Rev Eukaryot Gene Expr 1995;5:127-156.
145. Malumbres M. Cyclins and related kinases in cancer cells. J BUON 2007;12 (Suppl 1):S45-52.
146. Vermeulen K, Van Bockstaele DR and Berneman ZN. The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif 2003;36:131-149.
147. Macaluso M, Montanari M, Cinti C and Giordano A. Modulation of cell cycle components by epigenetic and genetic events. Semin Oncol 2005;32:452-457.
148. Salvesen HB, Kumar R, Stefansson I, Angelini S, MacDonald N, Smeds J, Jacobs IJ, Hemminki K, Das S and Akslen LA. Low frequency of BRAF and CDKN2A mutations in endometrial cancer. Int J Cancer 2005;115: 930-934.
149. Maxwell GL, Chandramouli GV, Dainty L, Litzi TJ, Berchuck A, Barrett JC and Risinger JI. Microarray analysis of endometrial carcinomas and mixed mullerian tumors reveals distinct gene expression profiles associated with different histologic types of uterine cancer. Clin Cancer Res 2005;11: 4056-4066.
150. Chiesa-Vottero AG, Malpica A, Deavers MT, Broaddus R, Nuovo GJ and Silva EG. Immunohistochemical overexpression of p16 and p53 in uterine serous carcinoma and ovarian high-grade serous carcinoma. Int J Gynecol Pathol 2007;26:328-333.
151. Reid-Nicholson M, Iyengar P, Hummer AJ, Linkov I, Asher M and Soslow RA. Immunophenotypic diversity of endometrial adenocarcinomas: implications for differential diagnosis. Mod Pathol 2006;19: 1091-1100.
152. Horree N, Heintz AP, Sie-Go DM and van Diest PJ. p16 is consistently expressed in endometrial tubal metaplasia. Cell Oncol 2007;29:37-45.
153. Horree N, van Diest PJ, Sie-Go DM and Heintz AP. The invasive front in endometrial carcinoma: higher proliferation and associated derailment of cell cycle regulators. Hum Pathol 2007;38:1232-1238.
154. Bose I and Ghosh B. The p53-MDM2 network: from oscillations to apoptosis. J Biosci 2007;32:991-997.
155. Zhang Y, Xiong Y and Yarbrough WG. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53
156. Masciullo V, Susini T, Zamparelli A, Bovicelli A, Minimo C, Massi D, Taddei G, Maggiano N, De Iaco P, Ceccaroni M, Bovicelli L, Amunni G, Mancuso S, Scambia G and Giordano A. Frequent loss of expression of the cyclin-dependent kinase inhibitor p27(Kip1) in estrogen-related Endometrial adenocarcinomas. Clin Cancer Res 2003;9: 5332-5338.
157. Schmitz MJ, Hendricks DT, Farley J, Taylor RR, Geradts J, Rose GS and Birrer MJ. p27 and cyclin D1 abnormalities in uterine papillary serous carcinoma. Gynecol Oncol 2000;77: 439-445.
158. Ozkara SK and Corakci A. Significantly decreased P27 expression in endometrial carcinoma compared to complex hyperplasia with atypia (correlation with p53 expression). Pathol Oncol Res 2004;10:89-97.
159. Iida T, Hamano M, Yoshida N, Yonamine K, Hayashi K, Kiguchi K, Ishizuka B, Nishimura Y, Arai T, Kawaguchi M, Hata H, Watanabe J and Kuramoto H. Establishment and characterization of two cell lines (HEC-155, HEC-180) derived from uterine papillary serous adenocarcinoma. Eur J Gynaecol Oncol 2004;25:423-427.
160. Kallakury BV, Ambros RA, Hayner-Buchan AM, Sheehan CE, Malfetano JH and Ross JS. Cell proliferation-associated proteins in endometrial carcinomas, including papillary serous and endometrioid subtypes. Int J Gynecol Pathol 1998;17:320-326.
161. DeBernardo RL, Littell RD, Luo H, Duska LR, Oliva E, Kirley SD, Lynch MP, Zukerberg LR and Rueda BR. Defining the extent of cables loss in endometrial cancer subtypes and its effectiveness as an inhibitor of cell proliferation in malignant endometrial cells in vitro and in vivo. Cancer Biol Ther 2005; 4:103-107.
162. Horree N, van Diest PJ, van der Groep P, Sie-Go DM and Heintz AP. Progressive derailment of cell cycle regulators in endometrial carcinogenesis. J Clin Pathol 2008;61:36-42.
163. Santin AD, Diamandis EP, Bellone S, Marizzoni M, Bandiera E, Palmieri M, Papasakelariou C, Katsaros D, Burnett A and Pecorelli S. Overexpression of kallikrein 10 (hK10) in uterine serous papillary carcinomas. Am J Obstet Gynecol 2006;194:1296-1302.
164. Santin AD, Diamandis EP, Bellone S, Soosaipillai A, Cane S, Palmieri M, Burnett A, Roman JJ and Pecorelli S. Human kallikrein 6: a new potential serum biomarker for uterine serous papillary cancer. Clin Cancer Res 2005;11:3320-3325.
165. Monaghan H, MacWhinnie N and Williams AR. The role of matrix metalloproteinases-2, -7 and -9 and beta-catenin in high grade endometrial carcinoma. Histopathology 2007; 50:348-357.
166. Jeng YM, Chang CC, Hu FC, Chou HY, Kao HL, Wang TH and Hsu HC. RNA-binding protein insulin-like growth factor II mRNA-binding protein 3 expression promotes tumor invasion and predicts early recurrence and poor prognosis in hepatocellular carcinoma. Hepatology 2008; 48: 1118-1127.
167. Li C, Zota V, Woda BA, Rock KL, Fraire AE, Jiang Z, Lu D, Xu B, Dresser K, Lutman CV and Fischer AH. Expression of a novel oncofetal mRNA-binding protein IMP3 in endometrial carcinomas: diagnostic significance and clinicopathologic correlations. Mod Pathol 2007;20:1263-1268.
168. Zheng W, Yi X, Fadare O, Liang SX, Martel M, Schwartz PE and Jiang Z. The oncofetal protein IMP3: a novel biomarker for endometrial serous carcinoma. Am J Surg Pathol 2008;32:304-315.
169. Kelemen LE. The role of folate receptor alpha in cancer development, progression and treatment: cause, consequence or innocent bystander? Int J Cancer 2006;119:243-250.
170. Allard JE, Risinger JI, Morrison C, Young G, Rose GS, Fowler J, Berchuck A and Maxwell GL. Overexpression of folate binding protein is associated with shortened progression-free survival in uterine adenocarcinomas. Gynecol Oncol 2007;107:52-57.
171. Dainty LA, Risinger JI, Morrison C, Chandramouli GV, Bidus MA, Zahn C, Rose GS, Fowler J, Berchuck A and Maxwell GL. Overexpression of folate binding protein and mesothelin are associated with uterine serous carcinoma. Gynecol Oncol 2007; 105:563-570.
172. Memarzadeh S, Kozak KR, Chang L, Natarajan S, Shintaku P, Reddy ST and Farias-Eisner R. Urokinase plasminogen activator receptor: Prognostic biomarker for endometrial cancer. Proc Natl Acad Sci USA 2002;99:10647-10652.