Pathogenesis and malignant transformation of adenomyosis (Review)

Oncology Reports

Volumn 29, Issue 3, 2013, Pages 861-867

  Koike, Natsuki ^a   Tsunemi, Taihei ^a   Uekuri, Chiharu ^a   Akasaka, Juria ^a   Ito, Fuminori ^a   Shigemitsu, Aiko ^a   Kobayashi, Hiroshi ^a  

^a NARA MEDICAL UNIVERSITY   (Japan)

Author keywords

Adenomyosis; Malignant transformation; Pathogenesis

Indexed keywords

ESTROGEN RECEPTOR; NERVE GROWTH FACTOR; PROGESTERONE RECEPTOR;

ADENOMYOSIS; CARCINOGENESIS; ENDOMETRIOID CARCINOMA; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; HUMAN; INTRAUTERINE PRESSURE; MALIGNANT TRANSFORMATION; MAST CELL; METAPLASIA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OVARY CARCINOMA; POSTMENOPAUSE; PRIORITY JOURNAL; REVIEW; STROMA CELL; TUMOR SUPPRESSOR GENE; TUMOR VASCULARIZATION; UTERUS CONTRACTILITY;

ADENOCARCINOMA; ADENOMYOSIS; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; ENDOMETRIAL NEOPLASMS; FEMALE; HUMANS; MYOMETRIUM;

EID: 84872813629     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2012.2184     Document Type: Review

References (73)

1. Ferenczy A: Pathophysiology of adenomyosis. Hum Reprod Update 4: 312-322, 1998. (Pubitemid 28486798)
2. Templeman C, Marshall SF, Ursin G, Horn-Ross PL, Clarke CA, Allen M, Deapen D, Ziogas A, Reynolds P, Cress R, Anton-Culver H, West D, Ross RK and Bernstein L: Adenomyosis and endometriosis in the California Teachers Study. Fertil Steril 90: 415-424, 2008. (Pubitemid 352040696)
3. Lalović N, Cvijanović R, Vladicić ND, Marić R, Jokanović D and Skipina DB: Adenomyomatosis of the gallbladder - case report. Med Pregl 64: 323-326, 2011.
4. Kayahara M, Ohta T, Kitagawa H, Miwa K, Urabe T and Murata T: Adenomyomatosis of the papilla of Vater: a case illustrating diagnostic difficulties. Dig Surg 18: 139-142, 2001. (Pubitemid 32437059)
5. Matsumoto T and Shimada K: A case of gallbladder cancer arising from the Rokitansky-Aschoff sinus. Jpn J Clin Oncol 39: 776, 2009.
6. Krutsay M: Adenomyosis of the common bile duct. Magy Onkol 54: 179-180, 2010 (In Hungarian).
7. Benagiano G, Brosens I and Carrara S: Adenomyosis: new knowledge is generating new treatment strategies. Womens Health 5: 297-311, 2009.
8. Parrott E, Butterworth M, Green A, White IN and Greaves P: Adenomyosis - a result of disordered stromal differentiation. Am J Pathol 159: 623-630, 2001. (Pubitemid 32751092)
9. Mori T, Ohta Y and Nagasawa H: Ultrastructural changes in uterine myometrium of mice with experimentally-induced adenomyosis. Experientia 40: 1385-1387, 1984. (Pubitemid 15179227)
10. Hever A, Roth RB, Hevezi PA, Lee J, Willhite D, White EC, Marin EM, Herrera R, Acosta HM, Acosta AJ and Zlotnik A: Molecular characterization of human adenomyosis. Mol Hum Reprod 12: 737-748, 2006. (Pubitemid 44811652)
11. Barcena de Arellano ML, Gericke J, Reichelt U, Okuducu AF, Ebert AD, Chiantera V, Schneider A and Mechsner S: Immuno-histochemical characterization of endometriosis-associated smooth muscle cells in human peritoneal endometriotic lesions. Hum Reprod 26: 2721-2730, 2011.
12. Mechsner S, Grum B, Gericke C, Loddenkemper C, Dudenhausen JW and Ebert AD: Possible roles of oxytocin receptor and vasopressin-1α receptor in the pathomechanism of dysperistalsis and dysmenorrhea in patients with adenomyosis uteri. Fertil Steril 94: 2541-2546, 2010.
13. Mehasseb MK, Bell SC, Brown L, Pringle JH and Habiba M: Phenotypic characterisation of the inner and outer myometrium in normal and adenomyotic uteri. Gynecol Obstet Invest 71: 217-2 2 4, 2011.
14. Mehasseb MK, Panchal R, Taylor AH, Brown L, Bell SC and Habiba M: Estrogen and progesterone receptor isoform distribution through the menstrual cycle in uteri with and without adenomyosis. Fertil Steril 95: 2228-2235, 2011.
15. Jaffer S, Shynlova O and Lye S: Mammalian target of rapamycin is activated in association with myometrial proliferation during pregnancy. Endocrinology 150: 4672-4680, 2009.
16. Shynlova O, Kwong R and Lye SJ: Mechanical stretch regulates hypertrophic phenotype of the myometrium during pregnancy. Reproduction 139: 247-253, 2010.
17. Treloar SA, Bell TA, Nagle CM, Purdie DM and Green AC: Early menstrual characteristics associated with subsequent diagnosis of endometriosis. Am J Obstet Gynecol 202: 534.e1-6, 2010.
18. Mechsner S, Bartley J, Infanger M, Loddenkemper C, Herbel J and Ebert AD: Clinical management and immunohistochemical analysis of umbilical endometriosis. Arch Gynecol Obstet 280: 235-2 42, 2009.
19. van Kaam KJ, Schouten J P, Nap AW, Dunselman G and Groothuis PG: Fibromuscular differentiation in deeply infiltrating endometriosis is a reaction of resident fibroblasts to the presence of ectopic endometrium. Hum Reprod 23: 2692-2700, 2008.
20. Leyendecker G, Wildt L and Mall G: The pathophysiology of endometriosis and adenomyosis: tissue injury and repair. Arch Gynecol Obstet 280: 529-538, 2009.
21. Walter I, Handler J, Reifinger M and Aurich C: Association of endometriosis in horses with differentiation of periglandular myofibroblasts and changes of extracellular matrix proteins. Reproduction 121: 581-586, 2001. (Pubitemid 32318450)
22. Chen YJ, Li HY, Huang CH, Twu NF, Yen MS, Wang PH, Chou TY, Liu YN, Chao KC and Yang MH: Oestrogen-induced epithelial-mesenchymal transition of endometrial epithelial cells contributes to the development of adenomyosis. J Pathol 222: 261-270, 2010.
23. Zhou S, Yi T, Liu R, Bian C, Qi X, He X, Wang K, Li J, Zhao X, Huang C and Wei Y: Proteomics identification of annexin A2 as a key mediator in the metastasis and proangiogenesis of endo-metrial cells in human adenomyosis. Mol Cell Proteomics 11: M112.017988, 2012.
24. Greaves P and White IN: Experimental adenomyosis. Best Pract Res Clin Obstet Gynaecol 20: 503-510, 2006. (Pubitemid 44688619)
25. Kang S, Li SZ, Wang N, Zhou RM, Wang T, Wang DJ, Li XF, Bui J and Li Y: Association between genetic polymorphisms in flbroblast growth factor (FGF)1 and FGF2 and risk of endome-triosis and adenomyosis in Chinese women. Hum Reprod 25: 1806-1811, 2010.
26. Hinoki A, Kimura K, Higuchi S, Eguchi K, Takaguri A, Ishimaru K, Frank GD, Gerthoffer WT, Sommerville LJ, Autieri MV and Eguchi S: p21-activated kinase 1 participates in vascular remodeling in vitro and in vivo. Hypertension 55: 161-165, 2010.
27. Kim SR, Kim SH, Lee HW, Chae HD, Kim CH and Kang BM: Increased expression of p21-activated kinase in adenomyosis. Fertil Steril 94: 1125-1128, 2010.
28. Meenakshi M and McCluggage WG: Vascular involvement in adenomyosis: report of a large series of a common phenomenon with observations on the pathogenesis of adenomyosis. Int J Gynecol Pathol 29: 117-121, 2010.
29. Sieiński W: Tumor-like intravascular proliferations of the stroma in adenomyosis. Patol Pol 44: 1-4, 1993.
30. Mori A, Zhai YL, Toki T, Nikaido T and Fujii S: Distribution and heterogeneity of mast cells in the human uterus. Hum Reprod 12: 368-372, 1997. (Pubitemid 27129403)
31. Menzies FM, Shepherd MC, Nibbs RJ and Nelson SM: The role of mast cells and their mediators in reproduction, pregnancy and labour. Hum Reprod Update 17: 383-396, 2011.
32. Anaf V, Chapron C, El Nakadi I, De Moor V, Simonart T and Noël JC: Pain, mast cells, and nerves in peritoneal, ovarian, and deep infiltrating endometr iosis. Fertil Steril 86: 1336-1343, 2006. (Pubitemid 44740094)
33. Kusakabe KT, Abe H, Kondo T, Kato K, Okada T and Otsuki Y: DNA microarray analysis in a mouse model for endometriosis and validation of candidate factors with human adenomyosis. J Reprod Immunol 85: 149-160, 2010.
34. Wang F, Wen Z, Li H, Yang Z, Zhao X and Yao X: Human leukocyte antigen-G is expressed by the eutopic and ectopic endometrium of adenomyosis. Fertil Steril 90: 1599-1604, 2008.
35. Choi KC, Leung PC and Jeung EB: Biology and physiology of Calbindin-D9k in female reproductive tissues: involvement of steroids and endocrine disruptors. Reprod Biol Endocrinol 3: 66, 2005.
36. Wang F, Li H, Yang Z, Du X, Cui M and Wen Z: Expression of interleukin-10 in patients with adenomyosis. Fertil Steril 91: 1681-1685, 2009.
37. Kang S, Zhao X, Xing H, Wang N, Zhou R, Chen S, Li W, Zhao J, Duan Y, Sun D and Li Y: Polymorphisms in the matrix metallopro-teinase-2 and tissue inhibitor of metalloproteinase-2 and the risk of human adenomyosis. Environ Mol Mutagen 49: 226-231, 2008. (Pubitemid 351499913)
38. Chen YJ, Li HY, Chang YL, Yuan CC, Tai LK, Lu KH, Chang CM and Chiou SH: Suppression of migratory/invasive ability and induction of apoptosis in adenomyosis-derived mesenchymal stem cells by cyclooxygenase-2 inhibitors. Fertil Steril 94: 1972-1979, 2010.
39. Kang R, Zeh HJ, Lotze MT and Tang D: The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 18: 571-580, 2011.
40. Ren Y, Mu L, Ding X and Zheng W: Decreased expression of Beclin 1 in eutopic endometrium of women with adenomyosis. Arch Gynecol Obstet 282: 401-406, 2010.
41. Liu X, Nie J and Guo SW: Elevated immunoreactivity against class I histone deacetylases in adenomyosis. Gynecol Obstet Invest 74: 50-55, 2012.
42. Suire RA, Goodman DG, Valerio MG, Fredrickson TN, Strandberg JD, Levitt MH, Lingeman CH, Harshbarger JC and Dawe CJ: Female reproductive system. In: Pathology of Laboratory Animals. Vol. 2. Benirschke K, Garner FM and Jones TC (eds). Springer-Verlag, New York, NY, pp1051-1262 1978.
43. Oehler MK, Greschik H, Fischer DC, Tong X, Schuele R and Kieback DG: Functional characterization of somatic point mutations of the human estrogen receptor alpha (hERalpha) in adenomyosis uteri. Mol Hum Reprod 10: 853-860, 2004. (Pubitemid 40045308)
44. Mehasseb MK, Bell SC and Habiba MA: The effects of tamoxifen and estradiol on myometrial differentiation and organization during early uterine development in the CD1 mouse. Reproduction 138: 341-350, 2009.
45. Green AR, Styles JA, Parrott EL, Gray D, Edwards RE, Smith AG, Gant TW, Greaves P, Al-Azzawi F and White IN: Neonatal tamoxifen treatment of mice leads to adenomyosis but not uterine cancer. Exp Toxicol Pathol 56: 255-263, 2005. (Pubitemid 40312750)
46. Li Y, Zhang SF, Zou SE, Xia X and Bao L: Accumulation of nerve growth factor and its receptors in the uterus and dorsal root ganglia in a mouse model of adenomyosis. Reprod Biol Endocrinol 9: 30, 2011.
47. Sampson JA: Endometrial carcinoma of the ovary arising in endo-metrial tissue of that organ. Arch Surg 10: 1-72, 1925.
48. Motohara K, Tashiro H, Ohtake H, Saito F, Ohba T and Katabuchi H: Endometrioid adenocarcinoma arising in adeno-myosis: elucidation by periodic magnetic resonance imaging evaluations. Int J Clin Oncol 13: 266-270, 2008. (Pubitemid 351871886)
49. Kumar D and Anderson W: Malignancy in endometriosis interna. J Obstet Gynaecol Br Emp 65: 435-437, 1958.
50. Colman HI and Rosenthal AH: Carcinoma developing in areas of adenomyosis. Obset Gynecol 14: 342-348, 1959.
51. Ismiil ND, Rasty G, Ghorab Z, Nofech-Mozes S, Bernardini M, Thomas G, Ackerman I, Covens A and Khalifa MA: Adenomyosis is associated with myometrial invasion by FIGO 1 endometrial adenocarcinoma. Int J Gynecol Pathol 26: 278-283, 2007. (Pubitemid 46986063)
52. Kucera E, Hejda V, Dankovcik R, Valha P, Dudas M and Feyereisl J: Malignant changes in adenomyosis in patients with endometrioid adenocarcinoma. Eur J Gynaecol Oncol 32: 182-184, 2011.
53. Hernandez E and Woodruff JD: Endometrial adenocarcinoma arising in adenomyosis. Am J Obstet Gynecol 138: 827-832, 1980. (Pubitemid 11199022)
54. Kazandi M, Zeybek B, Terek MC, Zekioglu O, Ozdemir N and Oztekin K: Grade 2 endometrioid adenocarcinoma arising from adenomyosis of the uterus: report of a case. Eur J Gynaecol Oncol 31: 719-721, 2010.
55. Rolly F: Über einen Fall von Adenomyoma Uteri, Übergang in Karzinom und Metastasenbildung. Virchows Arch 150: 555, 1897 (In German).
56. Abushahin N, Zhang T, Chiang S, Zhang X, Hatch K and Zheng W: Serous endometrial intraepithelial carcinoma arising in adenomyosis: a report of 5 cases. Int J Gynecol Pathol 30: 271-281, 2011.
57. Puppa G, Shozu M, Perin T, Nomura K, Gloghini A, Campagnutta E and Canzonieri V: Small primary adenocarcinoma in adeno-myosis with nodal metastasis: a case report. BMC Cancer 7: 103, 2007.
58. Takeuchi K, Yamanaka Y, Hamana S, Ohara N and Maruo T: Invasive adenocarcinoma arising from uterine adenomyosis involving the rectosigmoid colon. Int J Gynecol Cancer 14: 1004-1006, 2004. (Pubitemid 39238190)
59. Izadi-Mood N, Samadi N, Sarmadi S and Eftekhar Z: Papillary serous carcinoma arising from adenomyosis presenting as intramural leiomyoma. Arch Iran Med 10: 2582-2560, 2007.
60. Hirabayashi K, Yasuda M, Kajiwara H, Nakamura N, Sato S, Nishijima Y, Mikami M and Osamura RY: Clear cell adeno-carcinoma arising from adenomyosis. Int J Gynecol Pathol 28: 262-266, 2009.
61. Jha P, Ansari C, Coakley F V, Wang ZJ, Yeh BM, Rabban J and Poder L: Case report: imaging of Mullerian adenosarcoma arising in adenomyosis. Clin Radiol 64: 645-648, 2009.
62. Ohta Y, Hamatani S, Suzuki T, Ikeda K, Kiyokawa K, Shiokawa A, Kushima M and Ota H: Clear cell adenocarcinoma arising from a giant cystic adenomyosis: a case report with immunohistochemical analysis of laminin-5 gamma2 chain and p53 overexpression. Pathol Res Pract 204: 677-682, 2008.
63. Couto D, Mota F, Silva T and de Oliveira C: Adenocarcinoma arising in adenomyosis: report of an unusual case. Acta Obstet Gynecol Scand 83: 406-408, 2004. (Pubitemid 38406825)
64. Woodruff JD, Erozan YS and Genadry R: Adenocarcinoma arising in adenomyosis detected by atypical cytology. Obstet Gynecol 67: 145-148, 1986. (Pubitemid 16174319)
65. Koshiyama M, Suzuki A, Ozawa M, Fujita K, Sakakibara A, Kawamura M, Takahashi S, Fujii H, Hirano T, Okagaki A, Nagano T and Ban C: Adenocarcinomas arising from uterine adenomyosis: a report of four cases. Int J Gynecol Pathol 21: 2392-2345, 2002.
66. Kuwashima Y, Uehara T, Kishi K, Tajima H, Shiromizu K, Matsuzawa M and Takayama S: Intramural adenocarcinoma of the uterus, arisen from adenomyosis uteri, showing unique histologic appearances. Report of two cases. Eur J Gynaecol Oncol 15: 418-423, 1994. (Pubitemid 24361198)
67. Rubod C, Narducci F, Delattre C, Decocq J, Verbert A and Delahousse G: Endometrioid adenocarcinoma arising from adenomyosis. A case report and literature review. J Gynecol Obstet Biol Reprod 33: 140-144, 2004. (Pubitemid 38453735)
68. Takai N, Akizuki S, Nasu K, Etoh Y and Miyakawa I: Endometrioid adenocarcinoma arising from adenomyosis. Gynecol Obstet Invest 48: 141-144, 1999. (Pubitemid 29397128)
69. Heo SH, Lee KH, Kim JW and Jeong YY: Unusual manifestation of endometrioid adenocarcinoma arising from subserosal cystic adenomyosis of the uterus: emphasis on MRI and positron emission tomography CT findings. Br J Radiol 84: e210-212, 2011.
70. Boes AS, Tousseyn T, Vandenput I, Timmerman D, Vergote I, Moerman P and Amant F: Pitfall in the diagnosis of endometrial cancer: case report of an endometrioid adenocarcinoma arising from uterine adenomyosis. Eur J Gynaecol Oncol 32: 431-434, 2011.
71. Ink4 and GALT loci. Int J Mol Med 6: 667-671, 2000.
72. Jones RK, Searle RF and Bulmer JN: Apoptosis and bcl-2 expression in normal human endometrium, endometriosis and adenomyosis. Hum Reprod 13: 3496-3502, 1998. (Pubitemid 29002647)
73. Jichan Nie, Xishi Liu and Guo SW: Promoter hypermethylation of progesterone receptor isoform B (PR-B) in adenomyosis and its rectification by a histone deacetylase inhibitor and a demeth-ylation agent. Reprod Sci 17: 995-1005, 2010.