| Reproductive Biology and Endocrinology | |
| The hormonal composition of follicular fluid and its implications for ovarian cancer pathogenesis | |
| Ronny Drapkin1  Megan M Emori1  | |
| [1] Department of Medical Oncology, Dana Farber Cancer Institute, Harvard Medical School, 450 Brookline Avenue, Boston, MA 02115, USA | |
| 关键词: Hormones; Ovarian cancer; Follicular fluid; | |
| Others : 1149547 DOI : 10.1186/1477-7827-12-60 |
|
| received in 2014-05-09, accepted in 2014-06-27, 发布年份 2014 | |
PDF
|
|
【 摘 要 】
Ovulation has long been associated with an increased risk in ovarian cancer, yet the underlying molecular mechanisms remain obscure. Two aspects of ovulation have been linked to ovarian cancer pathogenesis. The first is the impact of repetitive tissue injury and repair that occurs with each ovulatory event. The second is the release of follicular fluid that accompanies the follicular rupture and its effect on the ovarian and fallopian tube epithelial cells. Hormones are an important component of follicular fluid, which transiently bathes the ovarian surface and fallopian tube epithelium during ovulation. Much work has been done exploring the role of hormones in fertility, but some, such as estrogen, have also been implicated in the pathogenesis of ovarian and other cancers. Understanding the role of hormones within follicular fluid, as well as how they are altered in disorders which increase ovarian cancer risk, will enhance our ability to assess risk and develop preventative strategies. This review provides an in depth discussion of the logistics of using and studying follicular fluid in ovarian cancer research, and discusses the fluctuations in follicular fluid hormone levels during normal physiological processes versus conditions that increase ovarian cancer risk.
【 授权许可】
2014 Emori and Drapkin; licensee BioMed Central Ltd.
【 预 览 】
| Files | Size | Format | View |
|---|---|---|---|
| 20150405081536988.pdf | 669KB | ||
| Figure 1. | 107KB | Image |
【 图 表 】
Figure 1.
【 参考文献 】
- [1]Vaughan S, Coward JI, Bast RC, Berchuck A, Berek JS, Brenton JD, Coukos G, Crum CC, Drapkin R, Etemadmoghadam D, Friedlander M, Gabra H, Kaye SB, Lord CJ, Lengyel E, Levine DA, McNeish IA, Menon U, Mills GB, Nephew KP, Oza AM, Sood AK, Stronach EA, Walczak H, Bowtell DD, Balkwill FR: Rethinking ovarian cancer: recommendations for improving outcomes. Nat Rev Cancer 2011, 11:719-725.
- [2]Kurman RJ, Shih IM: The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol 2010, 34:433-443.
- [3]Karst AM, Drapkin R: Ovarian cancer pathogenesis: a model in evolution. J Oncol 2010, 2010:932371.
- [4]Fathalla MF: Incessant ovulation- a factor in ovarian neoplasia? Lancet 1971, 2:163.
- [5]Cramer DW, Welch WR: Determinants of ovarian cancer risk. II. Inferences regarding pathogenesis. J Natl Cancer Inst 1983, 71:717-721.
- [6]Levanon K, Crum C, Drapkin R: New insights into the pathogenesis of serous ovarian cancer and its clinical impact. J Clin Oncol 2008, 26:5284-5293.
- [7]Mandai M, Yamaguchi K, Matsumura N, Baba T, Konishi I: Ovarian cancer in endometriosis: molecular biology, pathology, and clinical management. Int J Clin Oncol 2009, 14:383-391.
- [8]Vercellini P, Crosignani P, Somigliana E, Vigano P, Buggio L, Bolis G, Fedele L: The ‘incessant menstruation’ hypothesis: a mechanistic ovarian cancer model with implications for prevention. Hum Reprod 2011, 26:2262-2273.
- [9]Backman S, Kollara A, Haw R, Stein L, Brown T: Glucocorticoid-induced reversal of interleukin-1β-stimulated inflammatory gene expression in human oviductal cells. PLoS One 2014, 9:e97997.
- [10]Lau A, Kollara A, St John E, Tone AA, Virtanen C, Greenblatt E, King W, Brown T: Altered expression of inflammation-associated genes in oviductal cells following follicular fluid exposure: implications for ovarian carcinogenesis. Exp Biol Med 2014, 239:24-32.
- [11]McCartney CR, Eagleson CA, Marshall JC: Regulation of gonadotropin secretion: implications for polycystic ovary syndrome. Semin Reprod Med 2002, 20:317-326.
- [12]Yancik R, Ries LG, Yates JW: Ovarian cancer in the elderly: an analysis of surveillance, epidemiology, and end results program data. Am J Obstet Gynecol 1986, 154:639-647.
- [13]Bächler M, Menshykau D, De Geyter C, Iber D: Species-specific differences in follicular antral sizes result from diffusion-based limitations on the thickness of the granulosa cell layer. Mol Hum Reprod 2014, 20:208-221.
- [14]Auersperg N: Ovarian surface epithelium as a source of ovarian cancers: unwarranted speculation or evidence-based hypothesis? Gynecol Oncol 2013, 130:246-251.
- [15]Bahar-Shany K, Brand H, Sapoznik S, Jacob-Hirsch J, Yung Y, Korach J, Perri T, Cohen Y, Hourvitz A, Levanon K: Exposure of fallopian tube epithelium to follicular fluid mimics carcinogenic changes in precursor lesions of serous papillary carcinoma. Gynecol Oncol 2014, 132:322-327.
- [16]Jiang JY, Macchiarelli G, Miyabayashi K, Sato E: Follicular microvasculature in the porcine ovary. Cell Tissue Res 2002, 310:93-101.
- [17]Carson R, Findlay J, Mattner P, Brown B: Relative levels of thecal blood flow in atretic and non-atretic ovarian follicles of the conscious sheep. Aust J Exp Biol Med Sci 1986, 64:381-387.
- [18]Rodgers RJ, Irving-Rodgers HF: Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod 2010, 82:1021-1029.
- [19]Shalgi R, Kracier P, Rimon A, Pinto M, Soferman N: Proteins of human follicular fluid: the blood-follicle barrier. Fertil Steril 1973, 48:109-118.
- [20]Garzo VG, Dorrington JH: Aromatase activity in human granulosa cells during follicular development and the modulation by follicle-stimulating hormone and insulin. Am J Obstet Gynecol 1984, 148:657-662.
- [21]De los Santos MJ, Garcia-Laez V, Beltran D, Labarta E, Zuzuarregui JL, Alama P, Gamiz P, Crespo J, Bosch E, Pellicer A: The follicular hormonal profile in low-responder patients undergoing unstimulated cycles: is it hypoandrogenic? Hum Reprod 2013, 28:224-229.
- [22]Jana SK, Babu KN, Chattopadhyay R, Chakravarty B, Chaudhury K: Upper control limit of reactive oxygen species in follicular fluid beyond which viable embryo formation is not favorable. Reprod Toxicol 2010, 29:447-451.
- [23]Agarwal A, Saleh RA, Bedaiwy MA: Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil and Steril 2003, 79:829-843.
- [24]King SM, Hilliard TS, Wu LY, Jaffe RC, Fazleabas AT, Burdette JE: The impact of ovulation on fallopian tube epithelial cells: evaluating three hypotheses connecting ovulation and serous ovarian cancer. Endocr Relat Cancer 2011, 18:627-642.
- [25]Ghoneim IM, Waheed MM, El-Bahr SM, Alhaider AK, Al-Eknah MM: Comparison of some biochemical and hormonal constituents of oversized follicles and preovulatory follicles in camels (Camelus dromedarius). Theriogenology 2013, 79:647-652.
- [26]Walsh SW, Matthews D, Browne JA, Forde N, Crowe MA, Mihm M, Diskin M, Evans AC: Acute dietary restriction in heifers alters expression of genes regulating exposure and response to gonadotropins and IGF in dominant follicles. Anim Reprod Sci 2012, 133:43-51.
- [27]Johnson PA, Giles JR: The hen as a model of ovarian cancer. Nat Rev Canc 2013, 13:432-436.
- [28]Drummond AE: The role of steroids in follicular growth. Reprod Biol Endocrinol 2006, 4:16.
- [29]Gougeon A: Human ovarian follicular development: from activation of resting follicles to preovulatory maturation. Ann Endocrinol (Paris) 2010, 71:132-143.
- [30]Feigelson HS, Henderson BE: Estrogens and breast cancer. Carcinogenesis 1996, 17:2279-2284.
- [31]Cavalieri E, Frenkel K, Liehr JG, Rogan E, Roy D: Estrogens as endogenous genotoxic agents- DNA adducts and mutations. J Natl Cancer Inst Monogr 2000, 27:75-94.
- [32]Liehr JG: Is estradiol a genotoxic mutagenic carcinogen? Endocr Rev 2000, 21:40-54.
- [33]De Resende LO, Vireque AA, Santana LF, Moreno DA, De Sa Rosa e Silva AC, Ferriani RA, Scrideli CA, Reis RM: Single-cell expression analysis of BMP15 and GDF9 in mature oocytes and BMPR2 in cumulus cells of women with polycystic ovary syndrome undergoing controlled ovarian hyperstimulation. J Assist Reprod Genet 2012, 29:1057-1065.
- [34]Du YB, Gao MZ, Shi Y, Sun ZG, Wang J: Endocrine and inflammatory factors and endometriosis-associated infertility in assisted reproduction techniques. Arch Gynecol Obstet 2013, 287:123-130.
- [35]Pacella L, Zander-Fox DL, Armstrong DT, Lane M: Women with reduced ovarian reserve or advanced maternal age have an altered follicular environment. Fertil and Steril 2012, 98:986-994.
- [36]Sherman BM, West JH, Korenman SG: The menopausal transition: analysis of LH, FSH, estradiol, and progesterone concentrations during menstrual cycles of older women. J Clin Endocrinol Metab 1976, 42:629-636.
- [37]De los Santos MJ, Garcia-Laez V, Beltran-Torregrosa D, Horcajadas JA, Martinez-Conejero JA, Esteban FJ, Pellicer A, Labarta E: Hormonal and molecular characterization of follicular fluid, cumulus cells and oocytes from pre-ovulatory follicles in stimulated and unstimulated cycles. Hum Reprod 2012, 27:1596-1605.
- [38]Lydon JP, DeMAyo FJ, Funk CR, Mani SK, Hughes AR, Montgomery CA, Shyamala G, Conneely OM, O’Malley BW: Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 1995, 9:2266-2278.
- [39]Kastner P, Krust A, Turcotte B, Stropp U, Tora L, Gronemyer H, Chambon P: Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J 1990, 9:1603-1614.
- [40]Kim JJ, Kurita T, Bulun SE: Progesterone action in endometrial cancer, endometriosis, uterine fibroids, and breast cancer. Endocr Rev 2013, 34:130-162.
- [41]Faber MT, Jensen A, Frederiksen K, Glud E, Hogdall E, Hogdall C, Blaakaer J, Kjaer SK: Oral contraceptive use and impact of cumulative intake of estrogen and progestin on risk of ovarian cancer. Cancer Causes Control 2013, 24:2197-2206.
- [42]Hu YC, Wang PH, Yeh S, Wang RS, Xie C, Xu Q, Zhou X, Chao HT, Tsai MY, Chang C: Subfertility and defective folliculogenesis in female mice lacking androgen receptor. Proc Natl Acad Sci U S A 2003, 101:1209-1214.
- [43]Lyon MF, Glenister PH: Reduced reproductive performance in androgen-resistant Tfm/Tfm female mice. Proc R Soc Lond B Biol Sci 1979, 208:1-12.
- [44]Hillier SG, Tetsuka M: Role of androgens in follicle maturation and atresia. Baillieres Clin Obstet Gynaecol 1997, 11:249-260.
- [45]Hillier SG: Current concepts of the roles of follicle stimulating hormone and luteinizing hormone in folliculogenesis. Hum Reprod 1994, 9:188-191.
- [46]Danilovich N, Babu PS, Xing W, Gerdes M, Krishnamurthy H, Sairam MR: Estrogen deficiency, obesity, and skeletal abnormalities in follicle-stimulating hormone receptor knockout (FORKO) female mice. Endocrinology 2000, 141:4295-4308.
- [47]Sherman BM, Korenman SG: Hormonal characteristics of the human menstrual cycle throughout reproductive life. J Clin Investig 1975, 55:699-706.
- [48]Slovis BH, Check JH: Younger women with diminished oocyte reserve are not more prone to meiosis errors leading to spontaneous abortion than their age peers with normal oocyte reserve. Clin Exp Obstet Gynecol 2013, 40:29-32.
- [49]Chakrabarti J: Serum leptin level in women with polycystic ovary syndrome: correlation with adiposity, insulin, and circulating testosterone. Ann Med Health Sci Res 2013, 3:191-196.
- [50]Siraj A, Desestret V, Antoine M, Fromont G, Huerre M, Sanson M, Camparo P, Pichon C, Planeix F, Gonin J, Radu A, Ghinea N: Expression of follicle-stimulating hormone receptor by the vascular endothelium in tumor metastases. BMC Cancer 2013, 13:246.
- [51]Tao X, Zhao N, Jin H, Zhang Z, Liu Y, Wu J, Bast RC, Yu Y, Feng Y: FSH enhances the proliferation of ovarian cancer cells by activating transient receptor potential channel C3. Endocr Rel Cancer 2013, 20:415-429.
- [52]Mak VC, Siu MK, Wong OG, Chan KK, Ngan HY, Cheung AN: Dysregulated stemness-related genes in gynecological malignancies. Histol Histopathol 2012, 27:1121-1130.
- [53]Zhang Z, Zhu Y, Lai Y, Wu X, Feng Z, Yu Y, Bast RC, Wan X, Xi X, Feng Y: Follicle-stimulating hormone inhibits apoptosis in ovarian cancer cells by regulating the OCT4 stem cell signaling pathway. Int J Oncol 2013, 43:1194-1204.
- [54]Visser JA, De Jong FH, Laven JS, Themmen AP: Anti-mullerian hormone: a new marker for ovarian function. Reproduction 2006, 131:1-9.
- [55]Carlsson IB, Scott JE, Visser JA, Ritvos O, Themmen AP, Hovatta O: Anti-mullerian hormone inhibits initiation of growth of human primordial ovarian follicles in vitro. Hum Reprod 2006, 21:2223-2227.
- [56]Durlinger AL, Gruijters MJ, Kramer P, Karels B, Kumar TR, Matzuk MM, Rose UM, De Jong FH, Uilenbroek JT, Grootegoed JA: Anti-mullerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology 2001, 142:4891-4899.
- [57]Kelsey TW, Wright P, Nelson SM, Anderson RA, Wallace WH: A validated model of serum anti-mullerian hormone from conception to menopause. PLoS One 2011, 6:e22024.
- [58]Jeppesen JV, Anderson RA, Kelsey TW, Christiansen SL, Kristensen SG, Jayaprakasan K, Raine-Fenning N, Campbell BK, Yding Andersen C: Which follicles make the most anti-mullerian hormone in humans? Evidence for an abrupt decline in AMH production at the time of follicle selection. Mol Hum Reprod 2013, 19:519-527.
- [59]Fanchin R, Schonauer LM, Righini C, Frydman N, Frydman R, Taieb J: Serum anti-mullerian hormone dynamics during controlled ovarian hyperstimulation. Hum Reprod 2003, 18:328-332.
- [60]Durlinger AL, Kramer P, Karels B, De Jong FH, Uilenbroek JT, Grootegoed JA, Themmen AP: Control of primordial follicle recruitment by anti-müllerian hormone in the mouse ovary. Endocrinology 1999, 140(12):5789-5796.
- [61]Anckaert E, Smitz J, Schiettecatte J, Klein BM, Arce JC: The value of anti-Mullerian hormone measurement in the long GnRH agonist protocol: association with ovarian response and gonadotropin-dose adjustments. Hum Reprod 2012, 27:1829-1839.
- [62]Geerts I, Vergote I, Neven P, Billen J: The role of inhibins B and antimullerian hormone for diagnosis and follow-up of granulosa cell tumors. Int J Gynecol Canc 2009, 19:847-855.
- [63]Walentowicz P, Sadlecki P, Krintus M, Sypniewska G, Mankowska-Cyl A, Grabiec M, Walentowicz-Sadlecka M: Serum anti-mullerian hormone levels in patients with epithelial ovarian cancer. Int J Endocrinol 2013, 2013:517239.
- [64]Fevold HL, Hisaw FL, Leonard SL: The gonad stimulating and the luteinizing hormones of the anterior lobe of the hypophesis. Am J Physiol 1931, 97:291-301.
- [65]Baird DT, Swanston IA, McNeilly AS: Relationship between LH, FSH, and prolactin concentration and the secretion of androgens and estrogens by the preovulatory follicle in the ewe. Biol Reprod 1981, 24:1013-1025.
- [66]Ma X, Dong Y, Matzuk MM, Kumar TR: Targeted disruption of luteinizing hormone β-subunit leads to hypogonadism, defects in gonadal steroidogenesis, and infertility. Proc Natl Acad Sci U S A 2004, 101:17294-17299.
- [67]Chada M, Prusa R, Bronsky J, Pechova M, Kotaska K, Lisa L: Inhibin B, follicle stimulating hormone, luteinizing hormone, and estradiol and their relationship to the regulation of follicle development in girls during childhood and puberty. Physiol Res 2003, 52:341-346.
- [68]Brodowska A, Laszczynska M, Brodowski J, Masiuk M, Starczewski A: Analysis of pituitary gonadotropin concentration in blood serum and immunolocalization and immunoexpression of follicle stimulating hormone and luteinising hormone receptors in ovaries of postmenopausal women. Histol Histopathol 2012, 27:241-248.
- [69]Liao H, Zhou Q, Gu Y, Duan T, Feng Y: Luteinizing hormone facilitates angiogenesis in ovarian epithelial tumor cells and metformin inhibits the effect through mTOR signaling pathway. Oncol Rep 2012, 27:1873-1878.
- [70]Zhang Z, Liao H, Chen X, Zheng Y, Liu Y, Tao X, Gu C, Dong L, Duan T, Yang Y, Liu X, Feng Y: Luteinizing hormone upregulates survivin and inhibits apoptosis in ovarian epithelial tumors. Eur J Obstet Gynecol Repod Biol 2011, 155:69-74.
- [71]Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, Garber J, Birch C, Mou H, Gordon RW, Cramer DW, McKeon FD, Crum CP: A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol 2007, 211:26-35.
- [72]Sjoquist K, Martyn J, Edmondson R, Friedlander M: The role of hormonal therapy in gynecological cancers-current status and future directions. Int J Gynecol Cancer 2011, 21:1328-1333.
- [73]Chumsri S, Howes T, Bao T, Sabnis G, Brodie A: Aromatase, aromatase inhibitors, and breast cancer. J Steroid Biochem Mol Biol 2011, 125:13-22.
- [74]Martinez-Delgado B, Yanowsky K, Inglada-Perez L, de la Hoya M, Caldes T, Vega A, Blanco A, Martin T, Gonzalez-Sarmiento R, Blasco M, Robledo M, Urioste M, Song H, Pharoah P, Benitez J: Shorter telomere length is associated with increased ovarian cancer risk in both familial and sporatic cases. J Med Genet 2012, 49:341-344.
- [75]Murakami J, Nagai N, Ohama K, Tahara H, Ide T: Telomerase activity in ovarian tumors. Cancer 1997, 80:1085-1092.
PDF