AMH/MIS as a contraceptive that protects the ovarian reserve during chemotherapy

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 9, 2017, Pages E1688-E1697

  Kano, Motohiro ^a,b   Sosulski, Amanda E ^a,b   Zhang, LiHua ^a,b   Saatcioglu, Hatice D ^a,b   Wang, Dan ^c   Nagykery, Nicholas ^a,b   Sabatini, Mary E ^a   Gao, Guangping ^c   Donahoe, Patricia K ^a,b   Pépin, David ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

AAV9; AMH; Contraceptive; MIS; Oncofertility

Indexed keywords

CARBOPLATIN; CYCLOPHOSPHAMIDE; DOXORUBICIN; MUELLERIAN INHIBITING FACTOR; ANTINEOPLASTIC AGENT; CONTRACEPTIVE AGENT;

ADENO ASSOCIATED VIRUS 9; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER CHEMOTHERAPY; CELL PROLIFERATION; CHEMOTHERAPY; CONTRACEPTION; CONTROLLED STUDY; EXPERIMENTAL NEOPLASM; FEMALE; GENE THERAPY; GRANULOSA CELL; HAMSTER; HYPERGONADOTROPIC HYPOGONADISM; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; OVARIAN RESERVE; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; PREMATURE OVARIAN FAILURE; PRIORITY JOURNAL; TUMOR GROWTH; UROGENITAL RIDGE; ANIMAL; C57BL MOUSE; DEPENDOPARVOVIRUS; DRUG EFFECTS; MALE; METABOLISM; PROCEDURES; REPRODUCTION;

ANIMALS; ANTI-MULLERIAN HORMONE; ANTINEOPLASTIC AGENTS; CONTRACEPTION; CONTRACEPTIVE AGENTS; DEPENDOVIRUS; FEMALE; GRANULOSA CELLS; MALE; MICE; MICE, INBRED C57BL; OVARIAN FOLLICLE; OVARIAN RESERVE; PRIMARY OVARIAN INSUFFICIENCY; REPRODUCTION;

EID: 85014117016     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1620729114     Document Type: Article

References (66)

1. Baker ML, Metcalfe SA, Hutson JM (1990) Serum levels of Müllerian inhibiting substance in boys from birth to 18 years, as determined by enzyme immunoassay. J Clin Endocrinol Metab 70(1):11-15.
2. Hudson PL, et al. (1990) An immunoassay to detect human müllerian inhibiting substance in males and females during normal development. J Clin Endocrinol Metab 70(1):16-22.
3. Josso N, Legeai L, Forest MG, Chaussain J-L, Brauner R (1990) An enzyme linked immunoassay for anti-müllerian hormone: A new tool for the evaluation of testicular function in infants and children. J Clin Endocrinol Metab 70(1):23-27.
4. Seifer DB, et al. (1993) Gonadotropin-releasing hormone agonist-induced differences in granulosa cell cycle kinetics are associated with alterations in follicular fluid müllerianinhibiting substance and androgen content. J Clin Endocrinol Metab 76(3):711-714.
5. Josso N, Picard JY, Rey R, di Clemente N (2006) Testicular anti-Müllerian hormone: History, genetics, regulation and clinical applications. Pediatr Endocrinol Rev 3(4):347-358.
6. Dewailly D, et al. (2014) The physiology and clinical utility of anti-Mullerian hormone in women. Hum Reprod Update 20(3):370-385.
7. Jost A (1947) Sur les dérivés mülleriens d'embryons de lapin des deux sexes castrés a 21 jours. C R Seances Soc Biol Fil 141(3-4):135.
8. Behringer RR, Finegold MJ, Cate RL (1994) Müllerian-inhibiting substance function during mammalian sexual development. Cell 79(3):415-425.
9. Nilsson EE, Schindler R, Savenkova MI, Skinner MK (2011) Inhibitory actions of Anti- Müllerian Hormone (AMH) on ovarian primordial follicle assembly. PLoS One 6(5):e20087.
10. Hirobe S, He WW, Lee MM, Donahoe PK (1992) Mullerian inhibiting substance messenger ribonucleic acid expression in granulosa and Sertoli cells coincides with their mitotic activity. Endocrinology 131(2):854-862.
11. Teixeira J, et al. (1996) Developmental expression of a candidate Müllerian inhibiting substance type II receptor. Endocrinology 137(1):160-165.
12. Baarends WM, et al. (1994) A novel member of the transmembrane serine/threonine kinase receptor family is specifically expressed in the gonads and in mesenchymal cells adjacent to the Müllerian duct. Development 120(1):189-197.
13. Baarends WM, et al. (1995) Anti-Müllerian hormone and anti-Müllerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology 136(11):4951-4962.
14. di Clemente N, et al. (1994) Cloning, expression, and alternative splicing of the receptor for anti-Müllerian hormone. Mol Endocrinol 8(8):1006-1020.
15. Connolly DC, et al. (2003) Female mice chimeric for expression of the simian virus 40 TAg under control of the MISIIR promoter develop epithelial ovarian cancer. Cancer Res 63(6):1389-1397.
16. Durlinger AL, et al. (1999) Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary. Endocrinology 140(12):5789-5796.
17. Gigli I, Cushman RA, Wahl CM, Fortune JE (2005) Evidence for a role for anti-Mullerian hormone in the suppression of follicle activation inmouse ovaries and bovine ovarian cortex grafted beneath the chick chorioallantoic membrane. Mol Reprod Dev 71(4):480-488.
18. Nilsson E, Rogers N, Skinner MK (2007) Actions of anti-Mullerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition. Reproduction 134(2):209-221.
19. Ragin RC, Donahoe PK, Kenneally MK, Ahmad MF, MacLaughlin DT (1992) Human Müllerian inhibiting substance: Enhanced purification imparts biochemical stability and restores antiproliferative effects. Protein Expr Purif 3(3):236-245.
20. Lorenzo HK, et al. (2002) New approaches for high-yield purification of Müllerian inhibiting substance improve its bioactivity. J Chromatogr B Analyt Technol Biomed Life Sci 766(1):89-98.
21. Pépin D, et al. (2013) An albumin leader sequence coupled with a cleavage site modification enhances the yield of recombinant C-terminal Mullerian Inhibiting Substance. Technology 1(1):63-71.
22. Pépin D, et al. (2015) AAV9 delivering a modified human Mullerian inhibiting substance as a gene therapy in patient-derived xenografts of ovarian cancer. Proc Natl Acad Sci USA 112(32):E4418-E4427.
23. Gupta SK, Malik A, Arukha AP (2015) Ovarian and oocyte targets for development of female contraceptives. Expert Opin Ther Targets 19(11):1433-1446.
24. Pelosi E, Forabosco A, Schlessinger D (2015) Genetics of the ovarian reserve. Front Genet 6:308.
25. Knight PG, Glister C (2006) TGF-β superfamily members and ovarian follicle development. Reproduction 132(2):191-206.
26. Morgan S, Anderson RA, Gourley C, Wallace WH, Spears N (2012) How do chemotherapeutic agents damage the ovary? Hum Reprod Update 18(5):525-535.
27. Hudson MM (2010) Reproductive outcomes for survivors of childhood cancer. Obstet Gynecol 116(5):1171-1183.
28. Green DM, et al. (2009) Ovarian failure and reproductive outcomes after childhood cancer treatment: Results from the Childhood Cancer Survivor Study. J ClinOncol 27(14):2374-2381.
29. El Hachem H, Atallah D, Grynberg M (2014) Fertility preservation in breast cancer patients. Future Oncol 10(10):1767-1777.
30. Woodruff TK (2007) The emergence of a new interdiscipline: Oncofertility. Cancer Treat Res 138:3-11.
31. Jeruss JS, Woodruff TK (2009) Preservation of fertility in patients with cancer. N Engl J Med 360(9):902-911.
32. Lobo RA (2005) Potential options for preservation of fertility in women. N Engl J Med 353(1):64-73.
33. Moore HCF, et al.; POEMS/S0230 Investigators (2015) Goserelin for ovarian protection during breast-cancer adjuvant chemotherapy. N Engl J Med 372(10):923-932.
34. Elgindy E, Sibai H, Abdelghani A, Mostafa M (2015) protecting ovaries during chemotherapy through gonad suppression: A systematic review and meta-analysis. Obstet Gynecol 126(1):187-195.
35. Lambertini M, et al. (2015) Ovarian suppression using luteinizing hormone-releasing hormone agonists during chemotherapy to preserve ovarian function and fertility of breast cancer patients: A meta-analysis of randomized studies. Ann Oncol 26(12):2408-2419.
36. Oktay K, Briggs D, Gosden RG (1997) Ontogeny of follicle-stimulating hormone receptor gene expression in isolated human ovarian follicles. J Clin Endocrinol Metab 82(11):3748-3751.
37. Lee MM, et al. (1997) Measurements of serum müllerian inhibiting substance in the evaluation of children with nonpalpable gonads. N Engl J Med 336(21):1480-1486.
38. GustafsonML, et al. (1992) Müllerian inhibiting substance as a marker for ovarian sexcord tumor. N Engl J Med 326(7):466-471.
39. Cate RL, et al. (1986) Isolation of the bovine and human genes for Müllerian inhibiting substance and expression of the human gene in animal cells. Cell 45(5):685-698.
40. Price JM, Donahoe PK, Ito Y (1979) Involution of the female Mullerian duct of the fetal rat in the organ-culture assay for the detection of Mullerian Inhibiting Substance. Am J Anat 156(2):265-284.
41. Grive KJ, et al. (2016) TAF4b regulates oocyte-specific genes essential for meiosis. PLoS Genet 12(6):e1006128.
42. Nelson JF, Felicio LS, Osterburg HH, Finch CE (1981) Altered profiles of estradiol and progesterone associated with prolonged estrous cycles and persistent vaginal cornification in aging C57BL/6J mice. Biol Reprod 24(4):784-794.
43. Franks LM, Payne J (1970) The influence of age on reproductive capacity in C57BL mice. J Reprod Fertil 21(3):563-565.
44. Jamin SP, Arango NA, Mishina Y, Hanks MC, Behringer RR (2002) Requirement of Bmpr1a for Müllerian duct regression during male sexual development. Nat Genet 32(3):408-410.
45. Xu J, Bishop CV, Lawson MS, Park BS, Xu F (2016) Anti-Müllerian hormone promotes pre-antral follicle growth, but inhibits antral follicle maturation and dominant follicle selection in primates. Hum Reprod 31(7):1522-1530.
46. Schmidt KLT, Kryger-Baggesen N, Byskov AG, Andersen CY (2005) Anti-Müllerian hormone initiates growth of human primordial follicles in vitro.Mol Cell Endocrinol 234(1-2):87-93.
47. Durlinger ALL, et al. (2002) Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 143(3):1076-1084.
48. Cimino I, et al. (2016) Novel role for anti-Müllerian hormone in the regulation of GnRH neuron excitability and hormone secretion. Nat Commun 7:10055.
49. Garrel G, et al. (2016) Anti-Müllerian hormone: A new actor of sexual dimorphism in pituitary gonadotrope activity before puberty. Sci Rep 6:23790.
50. Takahashi M, Koide SS, Donahoe PK (1986) Müllerian inhibiting substance as oocyte meiosis inhibitor. Mol Cell Endocrinol 47(3):225-234.
51. Andersen CY, et al. (2010) Concentrations of AMH and inhibin-B in relation to follicular diameter in normal human small antral follicles. Hum Reprod 25(5):1282-1287.
52. Li J, et al. (2015) Vectored antibody gene delivery mediates long-term contraception. Curr Biol 25(19):R820-R822.
53. Hamy A-S, et al. (2014) Ovarian reserve in breast cancer: Assessment with anti-Müllerian hormone. Reprod Biomed Online 29(5):573-580.
54. Li X, Kang X, Deng Q, Cai J, Wang Z (2013) Combination of a GnRH agonistwith an antagonist prevents flare-up effects and protects primordial ovarian follicles in the rat ovary from cisplatin- induced toxicity: A controlled experimental animal study. Reprod Biol Endocrinol 11:16.
55. Morgan S, Lopes F, Gourley C, Anderson RA, Spears N (2013) Cisplatin and doxorubicin induce distinct mechanisms of ovarian follicle loss; imatinib provides selective protection only against cisplatin. PLoS One 8(7):e70117.
56. Kalich-Philosoph L, et al. (2013) Cyclophosphamide triggers follicle activation and "burnout"; AS101 prevents follicle loss and preserves fertility. Sci Transl Med 5(185):185ra62.
57. van der Kaaij MAE, van Echten-Arends J, Simons AHM, Kluin-Nelemans HC (2010) Fertility preservation after chemotherapy for Hodgkin lymphoma. Hematol Oncol 28(4):168-179.
58. Yuksel A, et al. (2015) The magnitude of gonadotoxicity of chemotherapy drugs on ovarian follicles and granulosa cells varies depending upon the category of the drugs and the type of granulosa cells. Hum Reprod 30(12):2926-2935.
59. McAllister JM, Legro RS, Modi BP, Strauss JF, 3rd (2015) Functional genomics of PCOS: From GWAS to molecular mechanisms. Trends Endocrinol Metab 26(3):118-124.
60. Sullivan SD, Welt C, Sherman S (2011) FMR1 and the continuum of primary ovarian insufficiency. Semin Reprod Med 29(4):299-307.
61. Gavish Z, Peer G, Roness H, Cohen Y, Meirow D (2014) Follicle activation and 'burnout' contribute to post-transplantation follicle loss in ovarian tissue grafts: The effect of graft thickness. Hum Reprod 29(5):989-996.
62. Jensen AK, et al. (2017) Cryopreservation of ovarian tissue for fertility preservation in a large cohort of young girls: Focus on pubertal development. Hum Reprod 32(1):154-164.
63. Committee on Care and Use of Laboratory Animals (2011) Guide for the Care and Use of Laboratory Animals (National Academies Press, Washington, DC), 8th Ed.
64. Pépin D, Paradis F, Perez-Iratxeta C, Picketts DJ, Vanderhyden BC (2013) The imitation switch ATPase Snf2l is required for superovulation and regulates Fgl2 in differentiating mouse granulosa cells. Biol Reprod 88(6):142.
65. Allen E (1922) The oestrous cycle in the mouse. Am J Anat 30(3):297-371.
66. Nagy A (2002) Manipulating the Mouse Embryo: A Laboratory Manual (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY), 3rd Ed.