Molecular mechanisms and biological plausibility underlying the malignant transformation of endometriosis: A critical analysis

Human Reproduction Update

Volumn 12, Issue 1, 2006, Pages 77-89

  Viganó, Paola ^a   Somigliana, Edgardo ^a   Chiodo, Ilda ^a   Abbiati, Annalisa ^a   Vercellini, Paolo ^a  

^a Fondazione Policlinico Mangiagalli Regina Elena   (Italy)

Author keywords

Endometriosis; Malignant transformation of endometriosis; Molecular mechanisms

Indexed keywords

CYTOCHROME P450; DNA; EPOXIDE HYDROLASE; GLUTATHIONE TRANSFERASE; K RAS PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROGESTERONE RECEPTOR; PROTEIN BCL 2; PROTEIN P53;

ALLELE; CANCER GROWTH; CANCER RISK; CARCINOGENESIS; CHROMOSOME ABERRATION; CLEAR CELL CARCINOMA; CLONAL VARIATION; COMPARATIVE GENOMIC HYBRIDIZATION; CYTOGENETICS; DISEASE MODEL; ENDOMETRIOSIS; FLUORESCENCE IN SITU HYBRIDIZATION; GENE DELETION; GENE MUTATION; GENETIC POLYMORPHISM; GENOTYPE; HUMAN; MALIGNANT TRANSFORMATION; MISSENSE MUTATION; MOLECULAR MECHANICS; NONHUMAN; ONCOGENE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TUMOR SUPPRESSOR GENE;

ANIMALS; CHROMOSOME ABERRATIONS; CYTOGENETIC ANALYSIS; ENDOMETRIOSIS; FEMALE; GENES, TUMOR SUPPRESSOR; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; LOSS OF HETEROZYGOSITY; MICE; MUTATION; ONCOGENES; OVARIAN NEOPLASMS; PTEN PHOSPHOHYDROLASE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 29544447489     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmi037     Document Type: Review

References (112)

1. Agoulnik IU, Tong XW, Fischer DC, Korner K, Atkinson NE, Edwards DP, Headon DR, Weigel NL and Kieback DG (2004) A germline variation in the progesterone receptor gene increases transcriptional activity and may modify ovarian cancer risk. J Clin Endocrinol Metab 89,6340-6347.
2. Alderson LM, Castleberg RL, Harsh GR, Louis DN and Henson JW (1995) Human gliomas with wild-type p53 express bc1-2. Cancer Res 55,999-1001.
3. Arvanitis DA, Goumenou AG, Matalliotakis IM, Koumantakis EE and Spandidos DA (2001) Low-penetrance genes are associated with increased susceptibility to endometriosis. Fertil Steril 76,1202-1206.
4. Babu KA, Reddy NG, Deendayal M, Kennedy S and Shivaji S (2005) GSTM1, GSTT1 and CYP1A1 detoxification gene polymorphisms and their relationship with advanced stages of endometriosis in South Indian women. Pharmacogenet Genomics 15,167-172.
5. Baranova H, Canis M, Ivaschenko T, Albuisson E, Bothorishvilli R, Baranov V, Malet P and Bruhat MA (1999) Possible involvement of arylamine N-acetyltransferase 2, glutathione S-transferases M1 and T1 genes in the development of endometriosis. Mol Hum Reprod 5,636-641.
6. Baxter SW, Thomas EJ and Campbell IG (2001) GSTM1 null polymorphism and susceptibility to endometriosis and ovarian cancer. Carcinogenesis 22,63-65.
7. Bayramo H and Duzcan E (2001) Atypical epithelial changes and mutant p53 gene expression in ovarian endometriosis. Pathol Oncol Res 7,33-38.
8. Beliard A, Noel A and Foidart JM (2004) Reduction of apoptosis and proliferation in endometriosis. Fertil Steril 82,80-85.
9. Bergqvist A, Borg A and Ljungberg O (1991) Protooncogenes in endometriotic and endometrial tissue. Ann N Y Acad Sci 626,276-283.
10. Bischoff FZ, Heard M and Simpson JL (2002) Somatic DNA alterations in endometriosis: High frequency of chromosome 17 and p53 loss in late-stage endometriosis. J Reprod Immunol 55,49-64.
11. Bozdogan O, Atasoy P, Erekul S, Bozdogan N and Bayram M (2002) Apoptosis-related proteins and steroid hormone receptors in normal, hyperplastic, and neoplastic endometrium. Int J Gynecol Pathol 21,375-382.
12. Brinton LA, Gridley G, Persson I, Baron J and Bergqvist A (1997) Cancer risk after a hospital discharge diagnosis of endometriosis. Am J Obstet Gynecol 176,572-579.
13. Brinton LA, Lamb EJ, Moghissi KS, Scoccia B, Althuis MD, Mabie JE and Westhoff CL (2004) Ovarian cancer risk associated with varying causes of infertility. Fertil Steril 82,405-414.
14. Brockmoller J, Cascorbi I, Kerb R, Sachse C and Roots I (1998) Polymorphisms in xenobiotic conjugation and disease predisposition. Toxicol Lett 102-103,173-183.
15. Campbell IG and Thomas EJ (2001) Endometriosis: Candidate genes. Hum Reprod Update 7,15-20.
16. Chan WY, Cheung KK, Schorge JO, Huang LW, Welch WR, Bell DA, Berkowitz RS and Mok SC (2000) Bc1-2 and p53 protein expression, apoptosis, and p53 mutation in human epithelial ovarian cancers. Am J Pathol 156,409-417.
17. Cvetkovic D (2003) Early events in ovarian oncogenesis. Reprod Biol Endocrinol 1,68-74.
18. Dangel A, Medchill MT, Davis G, Meloni AM and Sandberg AA (1994) Cytogenetic studies in endometriosis tissue. Cancer Genet Cytogenet 78,172-174.
19. Daniely M, Aviram A, Adams EF, Buchfelder M, Barkai G, Fahlbusch R, Goldman B and Friedman E (1998) Comparative genomic hybridization analysis of nonfunctioning pituitary tumors. J Clin Endocrinol Metab 83,1801-1805.
20. Di Cristofano A and Pandolfi PP (2000) The multiple roles of PTEN in tumor suppression. Cell 100,387-390.
21. Diebold J (1999) Molecular genetics of ovarian carcinomas. Histol Histopathol 14,269-277.
22. Diebold J, Baretton G, Felchner M, Meier W, Dopfer K, Schmidt M and Lohrs U (1996) Bc1-2 expression, p53 accumulation, and apoptosis in ovarian carcinomas. Am J Clin Pathol 105,341-349.
23. Dinulescu DM, Ince TA, Quade BJ, Shafer SA, Crowley D and Jacks T (2005) Role of Kras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat Med 11,63-70.
24. Donaldson CJ, Crapanzano JP, Watson JC, Levine EA and Batzer MA (2002) PROGINS Alu insertion and human genomic diversity. Mutat Res 501,137-141.
25. Fabjani G, Tong D, Czerwenka K, Schuster E, Speiser P, Leodolter S and Zeillinger R (2002) Human progesterone receptor gene polymorphism PROGINS and risk for breast cancer in Austrian women. Breast Cancer Res Treat 72,131-137.
26. Fauvet R, Poncelet C, Hugol D, Lavaur A, Feldmann G and Darai E (2003) Expression of apoptosis-related proteins in endometriomas and benign and malignant ovarian tumours. Virchows Arch 443,38-43.
27. Gogusev J, Bouquet de Joliniere J, Telvi L, Doussau M, du Manoir S, Stojkoski A and Levardon M (1999) Detection of DNA copy number changes in himian endometriosis by comparative genomic hybridization. Hum Genet 105,444-451.
28. Gogusev J, Bouquet de Joliniere J, Telvi L, Doussau M, Stojkoski A and Levardon M (2000) Cellular and genetic constitution of human endometriosis tissues. J Soc Gynecol Investig 7,79-87.
29. Goumenou AG, Arvanitis DA, Matalliotakis IM, Koumantakis EE and Spandidos DA (2001a) Microsatellite DNA assays reveal an allelic imbalance in p16 (Ink4), GALT, p53, and APOA2 loci in patients with endometriosis. Fertil Steril 75,160-165.
30. Goumenou A, Panayiotides I, Matalliotakis I, Vlachonikolis I, Tzardi M and Koumantakis E (2001b) Bc1-2 and Bax expression in human endometriotic and adenomyotic tissues. Eur J Obstet Gynecol Reprod Biol 99,256-260.
31. Goumenou A, Matalliotakis I, Tzardi M, Fragouli YG, Mahutte NG and Arici A (2004) Apoptosis and differential expression of apoptosis-related proteins in endometriotic glandular and stromal cells. J Soc Gynecol Investig 11,318-322.
32. Gurates B and Bulun SE (2003) Endometriosis: The ultimate hormonal disease. Semin Reprod Med 21,125-134.
33. Hadfield RM, Manek S, Weeks DE, Mardon HJ, Barlow DH and Kennedy SH (2001) Linkage and association studies of the relationship between endometriosis and genes encoding the detoxification enzymes GSTM1, GSTT1 and CYP1A1. Mol Hum Reprod 7,1073-1078.
34. Han WC and Weinberg RA (2002) Modelling the molecular circuitry of cancer. Nat Rev 2,321-341.
35. Han AC, Hovenden S, Rosenblum NG and Salazar H (1998) Adenocarcinoma arising in extragonadal endometriosis: An immunohistochemical study. Cancer 83,1163-1169.
36. Holt VL and Weiss NS (2000) Recommendations for the design of epidemiologic studies of endometriosis. Epidemiology 11,654-659.
37. Horiuchi A, Osada R, Nakayama K, Toki T, Nikaido T and Fujii S (1998) Ovarian yolk sac tumor with endometrioid carcinoma arising from endometriosis in a postmenopausal woman, with special reference to expression of alpha-fetoprotein, sex steroid receptors, and p53. Gynecol Oncol 70,295-299.
38. Hsieh YY, Chang CC, Tsai FJ, Lin CC, Chen JM and Tsai CH (2004) Glutathione S-transferase M1 *null genotype but not myeloperoxidase promoter G-463A polymorphism is associated with higher susceptibility to endometriosis. Mol Hum Reprod 10,713-717.
39. Hur SE, Lee JY, Moon HS and Chung HW (2005) Polymorphisms of the genes encoding the GSTM1, GSTT1 and GSTP1 in Korean women: No association with endometriosis. Mol Hum Reprod 11, 15-19.
40. Jacobs IJ, Kohler MF, Wiseman RW, Marks JR, Whitaker R, Kerns BA, Humphrey P, Berchuck A, Ponder BA and Bast RC Jr (1992) Clonal origin of epithelial ovarian carcinoma: Analysis by loss of heterozygosity, p53 mutation, and X-chromosome inactivation. J Natl Cancer Inst 84,1793-1798.
41. Jang SJ and Mao L (2000) Methylation patterns in human androgen receptor gene and clonality analysis. Cancer Res 60,864-866.
42. Jiang X, Hitchcock A, Bryan EJ, Watson RH, Englefield P, Thomas EJ and Campbell IG (1996) Microsatellite analysis of endometriosis reveals loss of heterozygosity at candidate ovarian tumor suppressor gene loci. Cancer Res 56,3534-3539.
43. Jiang X, Morland SJ, Hitchcock A, Thomas EJ and Campbell IG (1998) Allelotyping of endometriosis with adjacent ovarian carcinoma reveals evidence of a common lineage. Cancer Res 58,1707-1712.
44. Jimbo H, Hitomi Y, Yoshikawa H, Yano T, Momoeda M, Sakamoto A, Tsutsumi O, Taketani Y and Esumi H (1997) Evidence for monoclonal expansion of epithelial cells in ovarian endometrial cysts. Am J Pathol 150,1173-1178.
45. Jimbo H, Hitomi Y, Yoshikawa H, Yano T, Momoeda M, Yasugi T, Taketani Y and Esumi H (1999) Clonality analysis of bilateral ovarian endometrial cysts. Fertil Steril 72,1142-1143.
46. Jones RK, Searle RF and Bulmer JN (1998) Apoptosis and bel-2 expression in normal human endometrium, endometriosis and adenomyosis. Hum Reprod 13,3496-3502.
47. Kieback DG, Gause HM, Korner W, Konig R, Runnebaum IB, Mobus VJ, Kreienberg R, Tong XW and Headon DR (1995) A TaqI RLFP in the human progesterone receptor gene is associated with sporadic epithelial ovarian cancer and with breast cancer. J Soc Gynecol Investig 2,137.
48. Korsmeyer SJ (1992) Bc1-2 initiates a new category of oncogenes: regulators of cell death. Blood 80,879-886.
49. Kosugi Y, Elias S, Malinak LR, Nagata J, Isaka K, Takayama M, Simpson JL and Bischoff FZ (1999) Increased heterogeneity of chromosome 17 aneuploidy in endometriosis. Am J Obstet Gynecol 180,792-797.
50. Krajinovic M, Labuda D, Richer C, Karimi S and Sinnett D (1999) Susceptibility to childhood acute lymphoblastic leukemia: Influence of CYP1A1, CYP2D6, GSTM1, and GSTT1 genetic polymorphisms. Blood 93,1496-1501.
51. Kurz C, Temfer CB, Boecskoer S, Unfried G, Nagele F and Hefler LA (2001) The PROGINS progesterone receptor gene polymorphism and idiopathic recurrent miscarriage. J Soc Gynecol Investig 8,295-298.
52. Lancaster JM, Berchuck A, Carney ME, Wiseman R and Taylor JA (1998) Progesterone receptor gene polymorphism and risk for breast and ovarian cancer. Br J Cancer 78,277.
53. Lancaster JM, Wenham RM, Halabi S, Calingaert B, Marks JR, Moorman PG, Bentley RC, Berchuck A and Schildkraut JM (2003) No relationship between ovarian cancer risk and progesterone receptor gene polymorphism in a population-based, case-control study in North Carolina. Cancer Epidemiol Biomarkers Prev 12,226-227.
54. Lattuada D, Somigliana E, Viganó P, Candiani M, Pardi G and Di Blasio AM (2004) Genetics of endometriosis: A role for progesterone receptor gene polymorphism PROGINS? Clin Endocrinol (Oxf) 61,190-194.
55. Lear JT, Smith AG, Strange RC and Fryer AA (2000) Detoxifying enzyme genotypes and susceptibility to cutaneous malignancy. Br J Dermatol 142,8-15.
56. Levy A (2001) Monoclonality of endocrine tumours: What does it mean? Trends Endocrinol Metab 12,301-307.
57. Martini M, Ciccarone M, Garganese G, Maggiore C, Evangelista A, Rahimi S, Zannoni G, Vittori G and Larocca LM (2002) Possible involvement of hMLH1, 16 (INK4a) and PTEN in the malignant transformation of endometriosis. Int J Cancer 102,398-406.
58. Matsuzaki S, Canis M, Murakami T, Dechelotte P, Bruhat MA and Okamura K (2001) Expression of the cyclin-dependent kinase inhibitor p27Kip1 in eutopic endometrium and peritoneal endometriosis. Fertil Steril 75,956-960.
59. Mayr D, Amann G, Siefert C, Diebold J and Anderegg B (2003) Does endometriosis really have premalignant potential? A clonal analysis of laser-microdissected tissue. FASEB J 17,693-695.
60. McKenna NJ, Kieback DG, Carney DN, Fanning M, McLinden J and Headon DR (1995) A germline TaqI restriction fragment length polymorphism in the progesterone receptor gene in ovarian carcinoma. Br J Cancer 71,451-455.
61. Meresman GF, Vighi S, Buquet RA, Contreras-Ortiz O, Tesone M and Rumi LS (2000) Apoptosis and expression of Bc1-2 and Bax in eutopic endometrium from women with endometriosis. Fertil Steril 74,760-766.
62. Mhawech P, Kinkel K, Vlastos G and Pelte MF (2002) Ovarian carcinomas in endometriosis: An immunohistochemical and comparative genomic hybridization study. Int J Gynecol Pathol 21,401-406.
63. Modugno F (2004) Ovarian cancer and polymorphisms in the androgen and progesterone receptor genes: A HuGE review. Am J Epidemiol 159,319-355.
64. Mutter GL, Lin MC, Fitzgerald JT, Kum JB, Baak JP, Lees JA, Weng LP and Eng C (2000) Altered PTEN expression as a diagnostic marker for the earliest endometrial precancers. J Natl Cancer Inst 92,924-930.
65. Myers MP, Stolarov JP, Eng C, Li J, Wang SI, Wigler MH, Parsons R and Tonks NK (1997) P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc Natl Acad Sci USA 94,9052-9057.
66. Nabeshima H, Murakami T, Yoshinaga K, Sato K, Terada Y and Okamura K (2003) Analysis of the clonality of ectopic glands in peritoneal endometriosis using laser microdissection. Fertil Steril 80, 1144-1150.
67. Nakayama K, Toki T, Nikaido T, Zhai Y and Konishi I (2001a) Genetic alterations in microsatellite marker sites among tumor suppressor genes in endometriosis. Gynecol Obstet Invest 51,240-242.
68. Nakayama K, Toki T, Zhai YL, Lu X, Horiuchi A, Nikaido T, Konishi I and Fujii S (2001b) Demonstration of focal p53 expression without genetic alterations in endometriotic lesions. Int J Gynecol Pathol 20,227-231.
69. Ness RB (2003) Endometriosis and ovarian cancer: Thoughts on shared pathophysiology. Am J Obstet Gynecol 189,280-294.
70. Nezhat FR and Kalir T (2002) Comparative immunohistochemical studies of endometriosis lesions and endometriotic cysts. Fertil Steril 78,820-824.
71. Nezhat F, Cohen C, Rahaman J, Gretz H, Cole P and Kalir T (2002) Comparative immunohistochemical studies of bc1-2 and p53 proteins in benign and malignant ovarian endometriotic cysts. Cancer 94,2935-2940.
72. Nilbert M, Pejovic T, Mandahl N, Iosif S, Willen H and Mitelman F (1995) Monoclonal origin of endometriotic cysts. Int J Gynecol Cancer 5,61-63.
73. Noack F, Schmidt H, Buchweitz O, Malik E and Horny HP (2004) Genomic imbalance and onco-protein expression of ovarian endometrioid adenocarcinoma arisen in an endometriotic cyst. Anticancer Res 24,151-154.
74. Obata K and Hoshiai H (2000) Common genetic changes between endometriosis and ovarian cancer. Gynecol Obstet Invest 50,39-43.
75. Obata K, Morland SJ, Watson RH, Hitchcock A, Chenevix-Trench G, Thomas EJ and Campbell IG (1998) Frequent PTEN/MMAC mutations in endometrioid but not serous or mucinous epithelial ovarian tumors. Cancer Res 58,2095-2097.
76. Okuda, T, Otsuka J, Sekizawa A, Saito H, Makino R, Kushima M, Farina A, Kuwano Y and Okai T (2003) p53 mutations and overexpression affect prognosis of ovarian endometrioid cancer but not clear cell cancer. Gynecol Oncol 88,318-325.
77. Pezzella F, Turley H, Kuzu I, Tungekar MF, Dunnill MS, Pierce CB, Harris A, Gatter KC and Mason DY (1993) bc1-2 protein in non-small-cell lung carcinoma. N Engl J Med 329,690-694.
78. Ponder BA, Schmidt GH, Wilkinson MM, Wood MJ, Monk M and Reid A (1985) Derivation of mouse intestinal crypts from single progenitor cells. Nature 313,689-691.
79. Prefumo F, Venturini PL and Fulcheri E (2003) Analysis of p53 and c-erbB-2 expression in ovarian endometrioid carcinomas arising in endometriosis. Int J Gynecol Pathol 22,83-88.
80. Prowse AH, Fakis G, Manek S, Churchman M, Edwards S, Rowan A, Koninckx P, Kennedy S and Tomlinson IP (2005) Allelic loss studies do not provide evidence for the "endometriosis-as-tumor" theory. Fertil Steril 83(Suppl. 1),1134-1143.
81. Reed JC (1994) Bc1-2 and the regulation of programmed cell death. J Cell Biol 124,1-6.
82. Riman T, Persson I and Nilsson S (1998) Hormonal aspects of epithelial ovarian cancer: Review of epidemiological evidence. Clin Endocrinol 49,695-707.
83. Risch H, Marrett LD, Jain M and Howe GR (1996) Difference in risk factors for epithelial ovarian cancer by histologic type. Results of a case-control study. Am J Epidemiol 136,1184-1203.
84. Roy WJ Jr, Watson RH, Hitchcock A, and Campbell IG (1997) Frequent loss of heterozygosity on chromosomes 7 and 9 in benign epithelial ovarian tumours. Oncogene 15,2031-2035.
85. Runnebaum IB, Wang-Gohrke S, Vesprini D, Kreienberg R, Lynch H, Moslehi R, Ghadirian P, Weber B, Godwin AK, Risch H et al. (2001) Progesterone receptor variant increases ovarian cancer risk in BRCA1 and BRCA2 mutation carriers who were never exposed to oral contraceptives. Pharmacogenetics 11,635-638.
86. Saintz de la Cuesta R, Izquierdo M, Canamero M, Granizo JJ and Manzarbeitia F (2004) Increased prevalence of p53 overexpression from typical endometriosis to atypical endometriosis and ovarian cancer associated with endometriosis. Eur J Obstet Gynecol Reprod Biol 113,87-93.
87. Sakurazawa N, Tanaka N, Onda M and Esumi H (2000) Instability of X chromosome methylation in aberrant crypt foci of the human colon. Cancer Res 60,3165-3169.
88. Saretzki G, Hoffmann U, Rohlke P, Psille R, Gaigal T, Keller G, Hofler H, Loning T, Petersen I and Dietel M (1997) Identification of allelic losses in benign, borderline, and invasive epithelial ovarian tumors and correlation with clinical outcome. Cancer 80,1241-1249.
89. Sarmanova J, Benesova K, Gut I, Nedelcheva-Kristensen V, Tynkova L and Soucek P (2001) Genetic polymorphisms of biotransformation enzymes in patients with Hodgkin's and non-Hodgkin's lymphomas. Hum Mol Genet 10,1265-1273.
90. Sato N, Tsunoda H, Nishida M, Morishita Y, Takimoto Y, Kubo, T and Noguchi M (2000) 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 carcinoma and clear cell carcinoma of the ovary. Cancer Res 60,7052-7056.
91. Schneider J, Jimenez E, Rodriguez F and Del Tanago JG (1998) c-myc, c-erb-B2, nm23 and p53 expression in human endometriosis. Oncol Rep 5,49-52.
92. Schuijer M and Berns EM (2003) TP53 and ovarian cancer. Hum Mutat 21,285-291.
93. Shin JC, Ross HL, Elias S, Nguyen DD, Mitchell-Leef D, Simpson JL and Bischoff FZ (1997) Detection of chromosomal aneuploidy in endometriosis by multi-color fluorescence in situ hybridization (FISH). Hum Genet 100,401-406.
94. Sidransky D (1995) Screening for clonal genetic alterations. Eur J Cancer 31A,1127-1129.
95. Signorello LB, Harlow BL, Cramer DW, Spiegelman D and Hill JA (1997) Epidemiologic determinants of endometriosis: A hospital-based case-control study. Ann Epidemiol 7,267-741.
96. Simpson JL, Farideh ZB, Kamat A, Buster JE and Carson SA (2003) Genetics of endometriosis. Obstet Gynecol Clin North Am 30,21-40.
97. Spurdle AB, Webb PM, Purdie DM, Chen X, Green A and Chenevix-Trench G (2001) Polymorphisms at the glutathione S-transferase GSTM1, GSTT1 and GSTP1 loci: Risk of ovarian cancer by histological subtype. Carcinogenesis 22,67-72.
98. Tamura, M, Fukaya T, Murakami T, Uehara S and Yajima A (1998) Analysis of clonality in human endometriotic cysts based on evaluation of X chromosome inactivation in archival formalin-fixed, paraffin-embedded tissue. Lab Invest 78,213-218.
99. Tanaka M, Kyo S, Kanaya T, Yatabe N, Nakamura M, Maida Y, Okabe M and Inoue M (2003) Evidence of the monoclonal composition of human endometrial epithelial glands and mosaic pattern of clonal distribution in luminal epithelium. Am J Pathol 163,295-301.
100. Thomas E and Campbell I (2000a) Evidence that endometriosis behaves in a malignant manner. Gynecol Obstet Invest 50,2-10.
101. Thomas EJ and Campbell IG (2000b) Molecular genetic defects in endometriosis. Gynecol Obstet Invest 50,44-50.
102. Tibiletti MG, Bernasconi B, Furlan D, Riva C, Trubia M, Buraggi G, Franchi M, Bolis P, Mariani A, Frigerio L et al. (1996) Early involvement of 6q in surface epithelial ovarian tumors. Cancer Res 56,4493-4498.
103. Tiltman AJ (1997) Smooth muscle neoplasms of the uterus. Curr Opin Obstet Gynecol 9,48-51.
104. Tong D, Fabjani G, Heinze G, Obermair A, Leodolter S and Zeillinger R (2001) Analysis of the human progesterone receptor gene polymorphism progins in Austrian ovarian carcinoma patients. Int J Cancer 95,394-397.
105. Vercellini P, Parazzini F, Bolis G, Carinelli S, Dindelli M, Vendola N, Luchini L and Crosignani PG (1993) Endometriosis and ovarian cancer. Am J Obstet Gynecol 169,181-182.
106. Vercellini P, Trecca D, Oldani S, Fracchiolla NS, Neri A and Crosignani PG (1994) Analysis of p53 and ras gene mutations in endometriosis. Gynecol Obstet Invest 38,70-71.
107. Vogelstein B, Fearon ER, Hamilton SR, Preisinger AC, Willard HF, Michelson AM, Riggs AD and Orkin SH (1987) Clonal analysis using recombinant DNA probes from the X-chromosome. Cancer Res 47,4806-4813.
108. Watson RH, Neville PJ, Roy WJ Jr, Hitchcock A and Campbell IG (1998) Loss of heterozygosity on chromosomes 7p, 7q, 9p and 11q is an early event in ovarian tumorigenesis. Oncogene 17,207-212.
109. Wieser F, Schneeberger C, Tong D, Tempfer C, Huber JC and Wenzl R (2002) PROGINS receptor gene polymorphism is associated with endometriosis. Fertil Steril 77,309-312.
110. Wu Y, Basir Z, Kajdacsy-Balla A, Strawn E, Macias V, Montgomery K and Guo SW (2003) Resolution of clonal origins for endometriotic lesions using laser capture microdissection and the human androgen receptor (HUMARA) assay. Fertil Steril 79,710-717.
111. Zborovskaya I, Gasparian A, Karseladze A, Elcheva I, Trofimova E, Driouch K, Trassard M, Tatosyan A and Lidereau R (1999) Somatic genetic alterations (LOH) in benign, borderline said invasive ovarian tumours: intratumoral molecular heterogeneity. Int J Cancer 82,822-826.
112. Zondervan KT, Cardon LR and Kennedy SH (2002) What makes a good case-control study? Design issues for complex traits such as endometriosis. Hum Reprod 17,1415-1423.