Primordial Follicle Transplantation within Designer Biomaterial Grafts Produce Live Births in a Mouse Infertility Model

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Kniazeva, E ^a,d   Hardy, A N ^b   Boukaidi, S A ^c   Woodruff, T K ^d   Jeruss, J S ^d,e   Shea, L D ^a,d,e  

^a Northwestern University   (United States)

^b FOX CHASE CANCER CENTER   (United States)

^c CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

^d NORTHWESTERN UNIVERSITY   (United States)

^e UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIAL;

ANIMAL; DISEASE MODEL; FEMALE; HUMAN; INFERTILITY, FEMALE; LIVE BIRTH; MOUSE; OVARY FOLLICLE; PATHOLOGY; PREGNANCY; PREVENTION AND CONTROL; PRIMARY OVARIAN INSUFFICIENCY; TRANSPLANTATION; TUMOR RECURRENCE;

ANIMALS; BIOCOMPATIBLE MATERIALS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INFERTILITY, FEMALE; LIVE BIRTH; MICE; NEOPLASM RECURRENCE, LOCAL; OVARIAN FOLLICLE; PREGNANCY; PRIMARY OVARIAN INSUFFICIENCY; TRANSPLANTS;

EID: 84949185772     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17709     Document Type: Article

References (67)

1. Jeruss, J. S. & Woodruff, T. K. Preservation of fertility in patients with cancer. N Engl J Med 360, 902-911 (2009).
2. Shapira, M., Raanani, H., Cohen, Y. & Meirow, D. Fertility preservation in young females with hematological malignancies. Acta Haematol 132, 400-413 (2014).
3. Partridge, A. H. et al. Web-based survey of fertility issues in young women with breast cancer. J Clin Oncol 22, 4174-4183 (2004).
4. Loscalzo, M. & Clark, K. L. The psychosocial context of cancer-related infertility. Cancer Treat Res 138, 180-190 (2007).
5. Jung, M. et al. The clinical outcome of chemotherapy-induced amenorrhea in premenopausal young patients with breast cancer with long-term follow-up. Ann Surg Oncol 17, 3259-3268 (2010).
6. Oktem, O. & Oktay, K. A novel ovarian xenografting model to characterize the impact of chemotherapy agents on human primordial follicle reserve. Cancer Res 67, 10159-10162 (2007).
7. Kim, S. et al. Rescue of platinum-damaged oocytes from programmed cell death through inactivation of the p53 family signaling network. Cell Death Differ 20, 987-997 (2013).
8. Mahajan, N. Fertility preservation in female cancer patients: An overview. J Hum Reprod Sci 8, 3-13 (2015).
9. Blumenfeld, Z. & Evron, A. Preserving fertility when choosing chemotherapy regimens-the role of gonadotropin-releasing hormone agonists. Expert Opin Pharmacother 16, 1-12 (2015).
10. Kerr, J. et al. The primordial follicle reserve is not renewed after chemical or γ -irradiation mediated depletion. Reproduction 143, 469-476 (2012).
11. Nakayama, K., Milbourne, A., Schover, L. R., Champlin, R. E. & Ueno, N. T. Gonadal failure after treatment of hematologic malignancies: from recognition to management for health-care providers. Nat Clin Pract Oncol 5, 78-89 (2008).
12. Redig, A. J., Brannigan, R., Stryker, S. J., Woodruff, T. K. & Jeruss, J. S. Incorporating fertility preservation into the care of young oncology patients. Cancer 117, 4-10 (2011).
13. Irtan, S., Orbach D., Helfre S. & Sarnacki, S. Ovarian transposition in prepubescent and adolescent girls with cancer. Lancet Oncol 14, e601-e608 (2013).
14. Noyes, N., Knopman, J. M., Long, K., Coletta, J. M. & Abu-Rustum, N. R. Fertility considerations in the management of gynecologic malignancies. Gynecol Oncol 120, 326-333 (2011).
15. Wallace, W. H., Thomson, A. B., Saran, F. & Kelsey, T. W. Predicting age of ovarian failure after radiation to a field that includes the ovaries. Int J Radiat Oncol Biol Phys 62, 738-744 (2005).
16. Wallace, W. H., Thomson, A. B. & Kelsey, T. W. The radiosensitivity of the human oocyte. Hum Reprod 18, 117-121 (2003).
17. Hulvat, M. C. & Jeruss, J. S. Maintaining fertility in young women with breast cancer. Curr Treat Options Oncol 10, 308-317 (2009).
18. Knight, S. et al. An approach to fertility preservation in prepubertal and postpubertal females: A critical review of current literature. Pediatr Blood Cancer 62, 935-939 (2015).
19. ISFP Practice Committee et al. Recommendations for fertility preservation in patients with lymphoma, leukemia, and breast cancer. J Assist Reprod Genet 29, 465-468 (2012).
20. Schmidt, K. T., Andersen, C. Y. & ISFP Practice Committee. Recommendations for fertility preservation in patients with lymphomas. J Assist Reprod Genet 29, 473-477 (2012).
21. Jadoul, P., Kim, S. S. & ISFP Practice Committee. Fertility considerations in young women with hematological malignancies. J Assist Reprod Genet 29, 479-487 (2012).
22. Klemp, J. & Kim, S. S. & ISFP Practice Committee. Fertility preservation in young women with breast cancer. J Assist Reprod Genet 29, 469-472 (2012).
23. Bockstaele, L., Tsepelidis, S., Dechene, J., Englert, Y. & Demeestere, I. Safety of ovarian tissue autotransplantation for cancer patients. Obstet Gynecol Int 2012, 495142 (2012).
24. Lee, D. M. et al. Live birth after ovarian tissue transplant. Nature 428, 137-138 (2004).
25. Donnez, J. et al. Pregnancy and live birth after autotransplantation of frozen-thawed ovarian tissue in a patient with metastatic disease undergoing chemotherapy and hematopoietic stem cell transplantation. Fertil Steril 95, 1787 e1781-1784 (2011).
26. Ernst, E., Bergholdt, S., Jorgensen, J. S. & Andersen, C. Y. The first woman to give birth to two children following transplantation of frozen/thawed ovarian tissue. Hum Reprod 25, 1280-1281 (2010).
27. Silber, S. J. et al. A series of monozygotic twins discordant for ovarian failure: ovary transplantation (cortical versus microvascular) and cryopreservation. Hum Reprod 23, 1531-1537 (2008).
28. Donnez, J. et al. Restoration of ovarian activity and pregnancy after transplantation of cryopreserved ovarian tissue: a review of 60 cases of reimplantation. Fertil Steril 99, 1503-1513 (2013).
29. Donnez, J. & Dolmans, M. M. Transplantation of ovarian tissue. Best Pract Res Clin Obstet Gynaecol 28, 1188-1197 (2014).
30. Macklon, K. T., Jensen, A. K., Loft, A., Ernst, E. & Andersen, C. Y. Treatment history and outcome of 24 deliveries worldwide after autotransplantation of cryopreserved ovarian tissue, including two new Danish deliveries years after autotransplantation. J Assist Reprod Genet 31, 1557-1564 (2014).
31. Donnez J. et al. Fertility preservation for age-related fertility decline. Lancet 385, 506-507 (2015).
32. Demeestere, I. et al. Live birth after autograft of ovarian tissue cryopreserved during childhood. Hum Reprod 30, 2107-2109 (2015).
33. Donnez, J. & Dolmans, M. M. Ovarian cortex transplantation: 60 reported live births brings the success and worldwide expansion of the technique towards routine clinical practice. J Assist Reprod Genet 32, 1167-1170 (2015).
34. Dolmans, M. M. et al. Reimplantation of cryopreserved ovarian tissue from patients with acute lymphoblastic leukemia is potentially unsafe. Blood 116, 2908-2914 (2010).
35. Shaw, J. M., Bowles, J., Koopman, P., Wood, E. C. & Trounson, A. O. Fresh and cryopreserved ovarian tissue samples from donors with lymphoma transmit the cancer to graft recipients. Hum Reprod 11, 1668-1673 (1996).
36. Xu, M., Kreeger, P. K., Shea, L. D. & Woodruff, T. K. Tissue-engineered follicles produce live, fertile offspring. Tissue Eng 12, 2739-2746 (2006).
37. Shikanov, A., Xu, M., Woodruff, T. K. & Shea, L. D. Interpenetrating fibrin-alginate matrices for in vitro ovarian follicle development. Biomaterials 30, 5476-5485 (2009).
38. Shikanov, A. et al. Fibrin encapsulation and vascular endothelial growth factor delivery promotes ovarian graft survival in mice. Tissue Eng Part A 17, 3095-3104 (2011).
39. Xu, M. et al. In vitro grown human ovarian follicles from cancer patients support oocyte growth. Hum Reprod 24, 2531-2540 (2009).
40. Xu, J. et al. Fibrin promotes development and function of macaque primary follicles during encapsulated three-dimensional culture. Hum Reprod 28, 2187-2200 (2013).
41. Rodrigues, J. K., Navarro, P. A., Zelinski, M. B., Stouffer, R. L. & Xu, J. Direct actions of androgens on the survival, growth and secretion of steroids and anti-Müllerian hormone by individual macaque follicles during three-dimensional culture. Hum Reprod 30, 664-674 (2015).
42. Amorim, C. A., Van Langendonckt, A., David, A., Dolmans, M. M. & Donnez, J. Survival of human pre-antral follicles after cryopreservation of ovarian tissue, follicular isolation and in vitro culture in a calcium alginate matrix. Hum Reprod 24, 92-99 (2009).
43. Kerr, J. B. et al. Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply. Reproduction 132, 95-109 (2006).
44. Smith, R. M. et al. Fibrin-mediated delivery of an ovarian follicle pool in a mouse model of infertility. Tissue Eng Part A 20, 3021-3030 (2014).
45. Bristol-Gould, S. K. et al. Fate of the initial follicle pool: empirical and mathematical evidence supporting its sufficiency for adult fertility. Dev Biol 298, 149-154 (2006).
46. Luyckx, V. et al. Is transplantation of cryopreserved ovarian tissue from patients with advanced-stage breast cancer safe? A pilot study. J Assist Reprod Genet 30, 1289-1299 (2013).
47. Smith, R. M., Woodruff, T. K. & Shea, L. D. Designing follicle-environment interactions with biomaterials. Cancer Treat Res 156, 11-24 (2010).
48. Laronda, M. et al. Alginate encapsulation supports the growth and differentiation of human primordial follicles within ovarian cortical tissue. J Assist Reprod Genet 31, 1013-1028 (2014).
49. Tagler, D. et al. Promoting extracellular matrix remodeling via ascorbic acid enhances the survival of primary ovarian follicles encapsulated in alginate hydrogels. Biotechnol Bioeng 111, 1417-1429 (2014).
50. Tagler, D., Makanji, Y., Anderson, N. R., Woodruff, T. K. & Shea, L. D. Supplemented α MEM/F12-based medium enables the survival and growth of primary ovarian follicles encapsulated in alginate hydrogels. Biotechnol Bioeng 110, 3258-3268 (2013).
51. Hornick, J. E., Duncan, F. E., Shea, L. D. & Woodruff, T. K. Isolated primate primordial follicles require a rigid physical environment to survive and grow in vitro. Hum Reprod 27, 1801-1810 (2012).
52. Woodruff, T. K. & Shea, L. D. A new hypothesis regarding ovarian follicle development: ovarian rigidity as a regulator of selection and health. J Assist Reprod Genet 28, 3-6 (2011).
53. Jin, S. et al. Markers of growth and development in primate primordial follicles are preserved after slow cryopreservation. Fertil Steril 93, 2627-2632 (2010).
54. Jin, S. Y., Lei, L., Shikanov, A., Shea, L. D. & Woodruff, T. K. A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse. Fertil Steril 93, 2633-2639 (2010).
55. Shea, L. D., Woodruff, T. K. & Shikanov, A. Bioengineering the ovarian follicle microenvironment. Annu Rev Biomed Eng 16, 29-52 (2014).
56. Carroll, J. & Gosden, R. G. Transplantation of frozen-thawed mouse primordial follicles. Human Reprod 8, 1163-1167 (1993).
57. Luyckx, V. et al. A new step toward the artificial ovary: survival and proliferation of isolated murine follicles after autologous transplantation in a fibrin scaffold. Fertil Steril 101, 1149-1156 (2014).
58. Dolmans, M. M., Luyckx, V., Donnez, J., Andersen, C. Y. & Greve, T. Risk of transferring malignant cells with transplanted frozen-thawed ovarian tissue. Fertil Steril 99, 1514-1522 (2013).
59. Cummings, C. L., Gawlitta, D., Nerem, R. M. & Stegemann, J. Properties of engineered vascular constructs made from collagen, fibrin, and collagen-fibrin mixtures. Biomaterials 25, 3699-3706 (2004).
60. Roness, H., Gavish, Z., Cohen, Y. & Meirow, D. Ovarian follicle burnout: a universal phenomenon? Cell Cycle 12, 3245-3246 (2013).
61. Gavish, Z., Peer, G., Roness, H., Cohen, Y. & Meirow, D. Follicle activation and 'burn-out' contribute to post-transplantation follicle loss in ovarian tissue grafts: the effect of graft thickness. Hum Reprod 29, 989-996 (2014).
62. Meirow, D. et al. Cortical fibrosis and blood-vessels damage in human ovaries exposed to chemotherapy. Potential mechanisms of ovarian injury. Hum Reprod 22, 1626-1633 (2007).
63. Abir, R. et al. Ovarian minimal residual disease in chronic myeloid leukaemia. Reprod Biomed Online 28, 255-260 (2014).
64. Rosendahl, M., Greve, T. & Andersen, C. Y. The safety of transplanting cryopreserved ovarian tissue in cancer patients: a review of the literature. J Assist Reprod Genet 30, 11-24 (2013).
65. Schröder, C. P. et al. An in vitro model for purging of tumour cells from ovarian tissue. Hum Reprod 19, 1069-1075 (2004).
66. Soares, M. et al. Evaluation of a human ovarian follicle isolation technique to obtain disease-free follicle suspensions before safely grafting to cancer patients. Fertil Steril 104, 672-680 (2015).
67. Yoneda, T., Williams, P. J., Hiraga, T., Niewolna, M. & Nishimura, R. A bone-seeking clone exhibits different biological properties from the MDA-MB-231 parental human breast cancer cells and a brain-seeking clone in vivo and in vitro. J Bone Miner Res 16, 1486-1495 (2001).