Folliculogenesis is not fully inhibited during GnRH analogues treatment in mice challenging their efficiency to preserve the ovarian reserve during chemotherapy in this model

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Horicks, Florence ^a   Van Den Steen, Géraldine ^a   Houben, Sarah ^a   Englert, Yvon ^a,b   Demeestere, Isabelle ^a,b  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b ERASME HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CETRORELIX; CYCLOPHOSPHAMIDE; FOLLITROPIN; TRIPTORELIN; ANTINEOPLASTIC AGENT; GONADORELIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG ACTIVITY; DRUG EFFICACY; ESTRUS CYCLE; FEMALE; FOLLITROPIN RELEASE; GRANULOSA CELL; IMMUNOHISTOCHEMISTRY; MORPHOLOGY; MOUSE; NONHUMAN; OOCYTE; OVARIAN PRESERVATION; OVARIAN RESERVE; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; TUNEL ASSAY; VAGINA SMEAR; ANALOGS AND DERIVATIVES; ANIMAL; ANIMAL MODEL; C57BL MOUSE; CBA MOUSE; CYTOLOGY; DRUG EFFECTS;

ANIMALS; ANTINEOPLASTIC AGENTS; CYCLOPHOSPHAMIDE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GONADOTROPIN-RELEASING HORMONE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MODELS, ANIMAL; OVARIAN FOLLICLE; OVARIAN RESERVE;

EID: 84943338825     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137164     Document Type: Article

References (49)

1. De Vos M, Devroey P, Fauser BC. Primary ovarian insufficiency. Lancet. 2010;376(9744):911-21. doi: 10.1016/S0140-6736 (10) 60355-8 PMID: 20708256.
2. Razzano A, Revelli A, Delle Piane L, Salvagno F, Casano S, Randaccio S, et al. Fertility preservation program before ovarotoxic oncostatic treatments: role of the psychological support in managing emotional aspects. Gynecol Endocrinol. 2014;30(11):822-4. doi: 10.3109/09513590.2014.944153 PMID: 25054374.
3. Meirow D. Reproduction post-chemotherapy in young cancer patients. Mol Cell Endocrinol. 2000;169(1-2):123-31. PMID: 11155944.
4. Loren AW, Mangu PB, Beck LN, Brennan L, Magdalinski AJ, Partridge AH, et al. Fertility preservation for patients with cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2013;31(19):2500-10. doi: 10.1200/JCO.2013.49.2678 PMID: 23715580.
5. Oktem O, Oktay K. A novel ovarian xenografting model to characterize the impact of chemotherapy agents on human primordial follicle reserve. Cancer Res. 2007;67(21):10159-62. doi: 10.1158/0008-5472. CAN-07-2042 PMID: 17974956.
6. Meirow D, Biederman H, Anderson RA, Wallace WH. Toxicity of chemotherapy and radiation on female reproduction. Clinical obstetrics and gynecology. 2010;53(4):727-39. doi: 10.1097/GRF. 0b013e3181f96b54 PMID: 21048440.
7. Roness H, Gavish Z, Cohen Y, Meirow D. Ovarian follicle burnout: a universal phenomenon? Cell Cycle. 2013;12(20):3245-6. doi: 10.4161/cc.26358 PMID: 24036538; PubMed Central PMCID: PMC3885633.
8. Kalich-Philosoph L, Roness H, Carmely A, Fishel-Bartal M, Ligumsky H, Paglin S, et al. Cyclophosphamide triggers follicle activation and "burnout"; AS101 prevents follicle loss and preserves fertility. Sci Transl Med. 2013;5(185):185ra62. doi: 10.1126/scitranslmed.3005402 PMID: 23677591.
9. Demeestere I, Moffa F, Peccatori F, Poirot C, Shalom-Paz E. Multiple approaches for individualized fertility protective therapy in cancer patients. Obstet Gynecol Int. 2012;2012:961232. doi: 10.1155/2012/961232 PMID: 22253632; PubMed Central PMCID: PMC3255296.
10. Hayden C. GnRH analogues: applications in assisted reproductive techniques. European journal of endocrinology/European Federation of Endocrine Societies. 2008;159 Suppl 1:S17-25. doi: 10.1530/EJE-08-0354 PMID: 18849304.
11. Kiesel LA, Rody A, Greb RR, Szilagyi A. Clinical use of GnRH analogues. Clinical endocrinology. 2002;56(6):677-87. PMID: 12072036.
12. Meirow D, Assad G, Dor J, Rabinovici J. The GnRH antagonist cetrorelix reduces cyclophosphamideinduced ovarian follicular destruction in mice. Human reproduction. 2004;19(6):1294-9. doi: 10.1093/humrep/deh257 PMID: 15117898.
13. Tan SJ, Yeh YC, Shang WJ, Wu GJ, Liu JY, Chen CH. Protective effect of a gonadotropin-releasing hormone analogue on chemotherapeutic agent-induced ovarian gonadotoxicity: a mouse model. Eur J Obstet Gynecol Reprod Biol. 2010;149(2):182-5. doi: 10.1016/j.ejogrb.2009.12.028 PMID: 20074846.
14. Ataya KM, McKanna JA, Weintraub AM, Clark MR, Le Maire WJ. A luteinizing hormone-releasing hormone agonist for the prevention of chemotherapy-induced ovarian follicular loss in rats. Cancer Res. 1985;45(8):3651-6. PMID: 3926307.
15. Bokser L, Szende B, Schally AV. Protective effects of D-Trp6-luteinising hormone-releasing hormone microcapsules against cyclophosphamide-induced gonadotoxicity in female rats. Br J Cancer. 1990;61(6):861-5. PMID: 2142603; PubMed Central PMCID: PMC1971695.
16. Matsuo G, Ushijima K, Shinagawa A, Takahashi S, Fujiyoshi N, Takemoto S, et al. GnRH agonist acts as ovarian protection in chemotherapy induced gonadotoxicity: an experiment using a rat model. Kurume Med J. 2007;54(1-2):25-9. PMID: 18332593.
17. Lemos CN, Reis FM, Pena GN, Silveira LC, Camargos AF. Assessment of fertility protection and ovarian reserve with GnRH antagonist in rats undergoing chemotherapy with cyclophosphamide. Reprod Biol Endocrinol. 2010;8:51. doi: 10.1186/1477-7827-8-51 PMID: 20482803; PubMed Central PMCID: PMC2885402.
18. Zhao XJ, Huang YH, Yu YC, Xin XY. GnRH antagonist cetrorelix inhibits mitochondria-dependent apoptosis triggered by chemotherapy in granulosa cells of rats. Gynecol Oncol. 2010;118(1):69-75. doi: 10.1016/j.ygyno. 2010.03.021 PMID: 20417958.
19. Ataya K, Rao LV, Lawrence E, Kimmel R. Luteinizing hormone-releasing hormone agonist inhibits cyclophosphamide-induced ovarian follicular depletion in rhesus monkeys. Biology of reproduction. 1995;52(2):365-72. PMID: 7711205.
20. Montz FJ, Wolff AJ, Gambone JC. Gonadal protection and fecundity rates in cyclophosphamide-treated rats. Cancer Res. 1991;51(8):2124-6. PMID: 1901240.
21. Detti L, Uhlmann RA, Zhang J, Diamond MP, Saed GM, Fletcher NM, et al. Goserelin fosters bone elongation but does not prevent ovarian damage in cyclophosphamide-treated prepubertal mice. Fertil Steril. 2014;101(4):1157-64 e1. doi: 10.1016/j.fertnstert.2013.12.028 PMID: 24462062.
22. Danforth DR, Arbogast LK, Friedman CI. Acute depletion of murine primordial follicle reserve by gonadotropinreleasing hormone antagonists. Fertil Steril. 2005;83(5):1333-8. doi: 10.1016/j.fertnstert.2004. 12.030 PMID: 15866565.
23. Turner NH, Partridge A, Sanna G, Di Leo A, Biganzoli L. Utility of gonadotropin-releasing hormone agonists for fertility preservation in young breast cancer patients: the benefit remains uncertain. Ann Oncol. 2013;24(9):2224-35. doi: 10.1093/annonc/mdt196 PMID: 23709175.
24. Del Mastro L, Ceppi M, Poggio F, Bighin C, Peccatori F, Demeestere I, et al. Gonadotropin-releasing hormone analogues for the prevention of chemotherapy-induced premature ovarian failure in cancer women: systematic review and meta-analysis of randomized trials. Cancer Treat Rev. 2014;40(5):675-83. doi: 10.1016/j.ctrv. 2013.12.001 PMID: 24360817.
25. Moore HC, Unger JM, Phillips KA, Boyle F, Hitre E, Porter D, et al. Goserelin for ovarian protection during breast-cancer adjuvant chemotherapy. The New England journal of medicine. 2015;372(10):923-32. doi: 10.1056/NEJMoa1413204 PMID: 25738668.
26. Chapman RM, Sutcliffe SB. Protection of ovarian function by oral contraceptives in women receiving chemotherapy for Hodgkin's disease. Blood. 1981;58(4):849-51. PMID: 7272513.
27. Glode LM, Robinson J, Gould SF. Protection from cyclophosphamide-induced testicular damage with an analogue of gonadotropin-releasing hormone. Lancet. 1981;1(8230):1132-4. PMID: 6112490.
28. Horvath JE, Bajo AM, Schally AV, Kovacs M, Herbert F, Groot K. Effects of long-term treatment with the luteinizing hormone-releasing hormone (LHRH) agonist Decapeptyl and the LHRH antagonist Cetrorelix on the levels of pituitary LHRH receptors and their mRNA expression in rats. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(23):15048-53. doi: 10.1073/pnas.232579499 PMID: 12409615; PubMed Central PMCID: PMC137542.
29. Kovacs M, Schally AV. Comparison of mechanisms of action of luteinizing hormone-releasing hormone (LHRH) antagonist cetrorelix and LHRH agonist triptorelin on the gene expression of pituitary LHRH receptors in rats. Proceedings of the National Academy of Sciences of the United States of America. 2001;98(21):12197-202. doi: 10.1073/pnas.211442598 PMID: 11593037; PubMed Central PMCID: PMC59791.
30. Byers SL, Wiles MV, Dunn SL, Taft RA. Mouse estrous cycle identification tool and images. PloS one. 2012;7(4):e35538. doi: 10.1371/journal.pone.0035538 PMID: 22514749; PubMed Central PMCID: PMC3325956.
31. Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocrine reviews. 1996;17(2):121-55. doi: 10.1210/edrv-17-2-121 PMID: 8706629.
32. Van Casteren JI, Schoonen WG, Kloosterboer HJ. Development of time-resolved immunofluorometric assays for rat follicle-stimulating hormone and luteinizing hormone and application on sera of cycling rats. Biology of reproduction. 2000;62(4):886-94. PMID: 10727257.
33. Browne HN, Moon KS, Mumford SL, Schisterman EF, Decherney AH, Segars JH, et al. Is anti-Mullerian hormone a marker of acute cyclophosphamide-induced ovarian follicular destruction in mice pretreated with cetrorelix? Fertil Steril. 2011;96(1):180-6 e2. doi: 10.1016/j.fertnstert.2011.04.008 PMID: 21550044; PubMed Central PMCID: PMC3129384.
34. Ezoe K, Murata N, Yabuuchi A, Okuno T, Kobayashi T, Kato O, et al. Long-term adverse effects of cyclophosphamide on follicular growth and angiogenesis in mouse ovaries. Reprod Biol. 2014;14(3):238-42. doi: 10.1016/j.repbio.2014.04.007 PMID: 25152523.
35. Desmeules P, Devine PJ. Characterizing the ovotoxicity of cyclophosphamide metabolites on cultured mouse ovaries. Toxicol Sci. 2006;90(2):500-9. doi: 10.1093/toxsci/kfj086 PMID: 16381661.
36. Morgan S, Lopes F, Gourley C, Anderson RA, Spears N. Cisplatin and doxorubicin induce distinct mechanisms of ovarian follicle loss; imatinib provides selective protection only against cisplatin. PloS one. 2013;8(7):e70117. doi: 10.1371/journal.pone.0070117 PMID: 23922929; PubMed Central PMCID: PMC3726485.
37. Roti Roti EC, Leisman SK, Abbott DH, Salih SM. Acute doxorubicin insult in the mouse ovary is celland follicle-type dependent. PloS one. 2012;7(8):e42293. doi: 10.1371/journal.pone.0042293 PMID: 22876313; PubMed Central PMCID: PMC3410926.
38. Kerr JB, Hutt KJ, Michalak EM, Cook M, Vandenberg CJ, Liew SH, et al. DNA damage-induced primordial follicle oocyte apoptosis and loss of fertility require TAp63-mediated induction of Puma and Noxa. Mol Cell. 2012;48(3):343-52. doi: 10.1016/j.molcel.2012.08.017 PMID: 23000175; PubMed Central PMCID: PMC3496022.
39. Hutt K. Protecting female fertility during anti-cancer treatment. Talk World Congress of Reproductive Biology. 2014.
40. Demeestere I, Brice P, Peccatori FA, Kentos A, Gaillard I, Zachee P, et al. Gonadotropin-releasing hormone agonist for the prevention of chemotherapy-induced ovarian failure in patients with lymphoma: 1-year follow-up of a prospective randomized trial. J Clin Oncol. 2013;31(7):903-9. doi: 10.1200/JCO. 2012.42.8185 PMID: 23129737.
41. Decanter C, Peigne M, Mailliez A, Morschhauser F, Dassonneville A, Dewailly D, et al. Toward a better follow-up of ovarian recovery in young women after chemotherapy with a hypersensitive antimullerian hormone assay. Fertil Steril. 2014;102(2):483-7. doi: 10.1016/j.fertnstert.2014.05.014 PMID: 24951363.
42. Sobinoff AP, Nixon B, Roman SD, McLaughlin EA. Staying alive: PI3K pathway promotes primordial follicle activation and survival in response to 3MC-induced ovotoxicity. Toxicol Sci. 2012;128(1):258-71. doi: 10.1093/toxsci/kfs137 PMID: 22505044.
43. Hasky N, Uri-Belapolsky S, Goldberg K, Miller I, Grossman H, Stemmer SM, et al. Gonadotrophinreleasing hormone agonists for fertility preservation: unraveling the enigma? Human reproduction. 2015. doi: 10.1093/humrep/dev037 PMID: 25796551.
44. Couzinet B, Lahlou N, Thomas G, Thalabard JC, Bouchard P, Roger M, et al. Effects of gonadotrophin releasing hormone antagonist and agonist on the pulsatile release of gonadotrophins and alpha-subunit in postmenopausal women. Clinical endocrinology. 1991;34(6):477-83. PMID: 1716186.
45. Matikainen T, Ding YQ, Vergara M, Huhtaniemi I, Couzinet B, Schaison G. Differing responses of plasma bioactive and immunoreactive follicle-stimulating hormone and luteinizing hormone to gonadotropinreleasing hormone antagonist and agonist treatments in postmenopausal women. J Clin Endocrinol Metab. 1992;75(3):820-5. doi: 10.1210/jcem.75.3.1517372 PMID: 1517372.
46. Sharpe KL, Bertero MC, Lyon BP, Muse KN, Vernon MW. Follicular atresia and infertility in rats treated with a gonadotropin-releasing hormone antagonist. Endocrinology. 1990;127(1):25-31. doi: 10.1210/endo-127-1-25 PMID: 2113868.
47. Gosden RG, Wade JC, Fraser HM, Sandow J, Faddy MJ. Impact of congenital or experimental hypogonadotrophism on the radiation sensitivity of the mouse ovary. Human reproduction. 1997;12(11):2483-8. PMID: 9436690.
48. Singh P, Krishna A. Effects of GnRH agonist treatment on steroidogenesis and folliculogenesis in the ovary of cyclic mice. J Ovarian Res. 2010;3:26. doi: 10.1186/1757-2215-3-26 PMID: 21083942; PubMed Central PMCID: PMC2998501.
49. Huang YH, Zhao XJ, Zhang QH, Xin XY. The GnRH antagonist reduces chemotherapy-induced ovarian damage in rats by suppressing the apoptosis. Gynecol Oncol. 2009;112(2):409-14. doi: 10.1016/j. ygyno. 2008.09.044 PMID: 19038435.