In Vitro culture of early secondary preantral follicles in hanging drop of ovarian cell-conditioned medium to obtain MII oocytes from outbred deer mice

Tissue Engineering - Part A

Volumn 19, Issue 23-24, 2013, Pages 2626-2637

  Choi, Jung Kyu ^a,b   Agarwal, Pranay ^a,b   He, Xiaoming ^a,b,c  

^a Ohio State University   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOTHERAPY; CONSERVATION; DROPS; RADIATION HAZARDS;

ANIMAL SPECIES; CONVENTIONAL METHODS; ENDANGERED SPECIES; FUNCTIONAL TISSUE; HANGING DROPS; MEDICAL TREATMENT; MICROLITERS; OVARIAN FOLLICLES;

MAMMALS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELL STRUCTURE; CULTURE MEDIUM; CUMULUS CELL; ENZYME CHEMISTRY; EXTRACELLULAR MATRIX; FEMALE; FERTILIZATION IN VITRO; GRANULOSA CELL; HANGING DROP METHOD; IN VITRO OOCYTE MATURATION; MOUSE; NONHUMAN; OOCYTE; OOCYTE MATURATION; OVARY CELL CULTURE; OVARY FOLLICLE; OXYGEN TRANSPORT; PARACRINE SIGNALING; PEROMYSCUS; PRIORITY JOURNAL; STROMA CELL; THECA CELL;

ANIMALS; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; FEMALE; HUMANS; OOCYTES; OVARIAN FOLLICLE; PEROMYSCUS;

EID: 84889779028     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0055     Document Type: Article

References (78)

1. Woodruff, T.K. Making eggs: is it now or later Nat Med 14, 1190, 2008.
2. Barnett, K.R., Schilling, C., Greenfeld, C.R., Tomic, D., and Flaws, J.A. Ovarian follicle development and transgenic mouse models. Hum Reprod Update 12, 537, 2006.
3. Broekmans, F.J., Soules, M.R., and Fauser, B.C. Ovarian aging: mechanisms and clinical consequences. Endocr Rev 30, 465, 2009.
4. Hassold, T., and Hunt, P. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2, 280, 2001.
5. Malizia, B.A., Hacker, M.R., and Penzias, A.S. Cumulative live-birth rates after in vitro fertilization. N Engl J Med 360, 236, 2009.
6. Donnez, J., and Dolmans, M.M. Cryopreservation and transplantation of ovarian tissue. Clin Obstet Gynecol 53, 787, 2010.
7. Andersen, C.Y., Kristensen, S.G., Greve, T., and Schmidt, K.T. Cryopreservation of ovarian tissue for fertility preservation in young female oncological patients. Future Oncol 8, 595, 2012.
8. Jeruss, J.S., and Woodruff, T.K. Preservation of fertility in patients with cancer. N Engl J Med 360, 902, 2009.
9. Jin, M., Yu, Y., and Huang, H. An update on primary ovarian insufficiency. Sci China Life Sci 55, 677, 2012.
10. Goswami, D., and Conway, G.S. Premature ovarian failure. Hum Reprod Update 11, 391, 2005.
11. Santos, R.R., Amorim, C., Cecconi, S., Fassbender, M., Imhof, M., Lornage, J., et al. Cryopreservation of ovarian tissue: an emerging technology for female germline preservation of endangered species and breeds. Anim Reprod Sci 122, 151, 2010.
12. Grynberg, M., Poulain, M., Sebag-Peyrelevade, S., le Parco, S., Fanchin, R., and Frydman, N. Ovarian tissue and follicle transplantation as an option for fertility preservation. Fertil Steril 97, 1260, 2012.
13. Donnez, J., Jadoul, P., Squifflet, J., Van Langendonckt, A., Donnez, O., Van Eyck, A.S., et al. Ovarian tissue cryopreservation and transplantation in cancer patients. Best Pract Res Clin Obstet Gynaecol 24, 87, 2010.
14. Meirow, D., Hardan, I., Dor, J., Fridman, E., Elizur, S., Ra'anani, H., et al. Searching for evidence of disease and malignant cell contamination in ovarian tissue stored from hematologic cancer patients. Hum Reprod 23, 1007, 2008.
15. Shaw, J.M., Bowles, J., Koopman, P., Wood, E.C., and Trounson, A.O. Fresh and cryopreserved ovarian tissue samples from donors with lymphoma transmit the cancer to graft recipients. Hum Reprod 11, 1668, 1996.
16. Eppig, J., and O'Brien, M. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod 54, 197, 1996.
17. Gosden, R.G., Mullan, J., Picton, H.M., Yin, H., and Tan, S.L. Current perspective on primordial follicle cryopreservation and culture for reproductive medicine. Hum Reprod Update 8, 105, 2002.
18. Varghese, A.C., du Plessis, S.S., Falcone, T., and Agarwal, A. Cryopreservation/transplantation of ovarian tissue and in vitro maturation of follicles and oocytes: challenges for fertility preservation. Reprod Biol Endocrinol 6, 47, 2008.
19. Smitz, J., Dolmans, M.M., Donnez, J., Fortune, J.E., Hovatta, O., Jewgenow, K., et al. Current achievements and future research directions in ovarian tissue culture, in vitro follicle development and transplantation: implications for fertility preservation. Hum Reprod Update 16, 395, 2010.
20. Cortvrindt, R.G., and Smitz, J.E. Follicle culture in reproductive toxicology: a tool for in-vitro testing of ovarian function Hum Reprod Update 8, 243, 2002.
21. Trounson, A., and Mohr, L. Human pregnancy following cryopreservation, thawing and transfer of an eight-cell embryo. Nature 305, 707, 1983.
22. Steptoe, P.C., and Edwards, R.G. Birth after the reimplantation of a human embryo. Lancet 2, 366, 1978. (Pubitemid 9007386)
23. Mandelbaum, J., Belaisch-Allart, J., Junca, A.M., Antoine, J.M., Plachot, M., Alvarez, S., et al. Cryopreservation in human assisted reproduction is now routine for embryos but remains a research procedure for oocytes. Hum Reprod 13(Suppl 3), 161, 1998; discussion 75-77.
24. Deepinder, F., and Agarwal, A. Technical and ethical challenges of fertility preservation in young cancer patients. Reprod Biomed Online 16, 784, 2008.
25. Roque, M., Lattes, K., Serra, S., Sola, I., Geber, S., Carreras, R., et al. Fresh embryo transfer versus frozen embryo transfer in in vitro fertilization cycles: a systematic review and metaanalysis. Fertil Steril 99, 156, 2013.
26. Desai, N., Alex, A., AbdelHafez, F., Calabro, A., Goldfarb, J., Fleischman, A., et al. Three-dimensional in vitro follicle growth: overview of culture models, biomaterials, design parameters and future directions. Reprod Biol Endocrinol 8, 119, 2010.
27. Kim, I.W., Gong, S.P., Yoo, C.R., Choi, J.H., Kim, D.Y., and Lim, J.M. Derivation of developmentally competent oocytes by the culture of preantral follicles retrieved from adult ovaries: maturation, blastocyst formation, and embryonic stem cell transformation. Fertil Steril 92, 1716, 2009.
28. Xu, M., Banc, A., Woodruff, T.K., and Shea, L.D. Secondary follicle growth and oocyte maturation by culture in alginate hydrogel following cryopreservation of the ovary or individual follicles. Biotechnol Bioeng 103, 378, 2009.
29. Xu, M., West-Farrell, E.R., Stouffer, R.L., Shea, L.D., Woodruff, T.K., and Zelinski, M.B. Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biol Reprod 81, 587, 2009.
30. Shikanov, A., Xu, M., Woodruff, T.K., and Shea, L.D. Interpenetrating fibrin-alginate matrices for in vitro ovarian follicle development. Biomaterials 30, 5476, 2009.
31. Shikanov, A., Xu, M., Woodruff, T., and Shea, L.Amethod for ovarian follicle encapsulation and culture in a proteolytically degradable 3 dimensional system. J Vis Exp e2695, 2011.
32. Jin, S.Y., Lei, L., Shikanov, A., Shea, L.D., and Woodruff, T.K. A novel two-step strategy for in vitro culture of earlystage ovarian follicles in the mouse. Fertil Steril 93, 2633, 2010.
33. Xu, M., Fazleabas, A.T., Shikanov, A., Jackson, E., Barrett, S.L., Hirshfeld-Cytron, J., et al. In vitro oocyte maturation and preantral follicle culture from the luteal-phase baboon ovary produce mature oocytes. Biol Reprod 84, 689, 2011.
34. Woodruff, T.K., and Shea, L.D. The role of the extracellular matrix in ovarian follicle development. Reprod Sci 14, 6, 2007.
35. Woodruff, T.K., and 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, 2011.
36. Wang, W., Tang, Y., Ni, L., Jongwutiwes, T., Liu, H., and Rosenwaks, Z. A modified protocol for in vitro maturation of mouse oocytes from secondary preantral follicles. Adv Biosci Biotechnol 3, 57, 2012.
37. Liu, J., Van der Elst, J., Van den Broecke, R., and Dhont, M. Live offspring by in vitro fertilization of oocytes from cryopreserved primordial mouse follicles after sequential in vivo transplantation and in vitro maturation. Biol Reprod 64, 171, 2001.
38. Xu, M., Kreeger, P.K., Shea, L.D., and Woodruff, T.K. Tissueengineered follicles produce live, fertile offspring. Tissue Eng 12, 2739, 2006.
39. Eppig, J.J., and Schroeder, A.C. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in-vitro. Biol Reprod 41, 268, 1989.
40. Nayudu, P.L., and Osborn, S.M. Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro. J Reprod Fertil 95, 349, 1992.
41. Roy, S.K., and Treacy, B.J. Isolation and long-term culture of human preantral follicles. Fertil Steril 59, 783, 1993.
42. Oktay, K., Nugent, D., Newton, H., Salha, O., Chatterjee, P., and Gosden, R.G. Isolation and characterization of primordial follicles from fresh and cryopreserved human ovarian tissue. Fertil Steril 67, 481, 1997.
43. Abir, R., Fisch, B., Nitke, S., Okon, E., Raz, A., and Ben Rafael, Z. Morphological study of fully and partially isolated early human follicles. Fertil Steril 75, 141, 2001.
44. Gorman, K.B., Flint, P.L., Esler, D., and Williams, T.D. Ovarian follicle dynamics of female Greater Scaup during egg production. J Field Ornithol 78, 64, 2007.
45. Guimaraes, D.A., de Garcia, S.C., Ferreira, M.A., da Silva Sdo, S., de Albuquerque, N.I., and Le Pendu, Y. Ovarian folliculogenesis in collared peccary, Pecari tajacu (Artiodactyla: Tayassuidae). Rev Biol Trop 60, 437, 2012.
46. Ting, A.Y., Yeoman, R.R., Lawson, M.S., and Zelinski, M.B. In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification. Hum Reprod 26, 2461, 2011.
47. Telfer, E.E., and McLaughlin, M. In vitro development of ovarian follicles. Sem Reprod Med 29, 15, 2011.
48. Hovatta, O., Wright, C., Krausz, T., Hardy, K., and Winston RML. Human primordial, primary and secondary ovarian follicles in long-term culture: effect of partial isolation. Hum Reprod 14, 2519, 1999.
49. Hreinsson, J.G., Scott, J.E., Rasmussen, C., Swahn, M.L., Hsueh AJW, and Hovatta, O. Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J Clin Endocr Metab 87, 316, 2002.
50. Niu, Y., and Liang, S. Genetic differentiation within the inbred C57BL/6J mouse strain. J Zool 278, 42, 2009.
51. Mott, R. A haplotype map for the laboratory mouse. Nat Genet 39, 1054, 2007.
52. Wade, C.M., Kulbokas, E.J., 3rd, Kirby, A.W., Zody, M.C., Mullikin, J.C., Lander, E.S., et al. The mosaic structure of variation in the laboratory mouse genome. Nature 420, 574, 2002.
53. Shorter, K.R., Crossland, J.P., Webb, D., Szalai, G., Felder, M.R., and Vrana, P.B. Peromyscus as a mammalian epigenetic model. Genet Res Int 2012, 179, 2012.
54. Salcedo, T., Geraldes, A., and Nachman, M.W. Nucleotide variation in wild and inbred mice. Genetics 177, 2277, 2007.
55. Klein, M.S., and Markert, C.L. Production of Chimeras in the deer mouse Peromyscus-Maniculatus-Bairdi. J Exp Zool 218, 183, 1981.
56. Joyner, C., Myrick, L., Crossland, J., and Dawson, W. Deer mice as laboratory animals. ILAR J 39, 322, 1998.
57. Veres, M., Duselis, A.R., Graft, A., Pryor, W., Crossland, J., Vrana, P.B., et al. The biology and methodology of assisted reproduction in deer mice (Peromyscus maniculatus). Theriogenology 77, 311, 2012.
58. Duselis, A.R., and Vrana, P.B. Aberrant growth and pattern formation in Peromyscus hybrid placental development. Biol Reprod 83, 988, 2010.
59. Dewey, M.J., and Dawson, W.D. Deer mice: "The Drosophila of North American mammalogy." Genesis 29, 105, 2001.
60. Chappell, M.A., Rezende, E.L., and Hammond, K.A. Age and aerobic performance in deer mice. J Exp Biol 206, 1221, 2003.
61. Choi, J.K., and He, X. In vitro maturation of cumulus-oocyte complexes for efficient isolation of oocytes from outbred deer mice. PLoS One 8, e56158, 2013.
62. Lee, S.T., Choi, M.H., Gong, S.P., Han, J.Y., and Lim, J.M. Establishment of a basic method for manipulating preantral follicles: effects of retrieval method on in vitro growth of preantral follicles and intrafollicular oocytes. Zygote 15, 109, 2007.
63. Gong, S.P., Lee, S.T., Lee, E.J., Kim, D.Y., Lee, G., Chi, S.G., et al. Embryonic stem cell-like cells established by culture of adult ovarian cells in mice. Fertil Steril 93, 2594, 2010.
64. Weigel, A., Schild, D., and Zeug, A. Resolution in the ApoTome and the confocal laser scanning microscope: comparison. J Biomed Opt 14, 014022, 2009.
65. Gines, T.B., and Davidson, M.W. Structured illumination: ZEISS ApoTome. Available at http://zeiss-campus.magnet .fsu.edu/tutorials/opticalsectioning/ apotome/index.html, accessed March 6, 2013.
66. Martin-Coello, J., Gonzalez, R., Crespo, C., Gomendio, M., and Roldan, E.R. Superovulation and in vitro oocyte maturation in three species of mice (Mus musculus, Mus spretus and Mus spicilegus). Theriogenology 70, 1004, 2008.
67. Demeestere, I., Delbaere, A., Gervy, C., Van Den Bergh, M., Devreker, F., and Englert, Y. Effect of preantral follicle isolation technique on in-vitro follicular growth, oocyte maturation and embryo development in mice. Hum Reprod 17, 2152, 2002.
68. Liu, J., Van Der Elst, J., Van Den Broecke, R., Dumortier, F., and Dhont, M. Maturation of mouse primordial follicles by combination of grafting and in vitro culture. Biol Reprod 62, 1218, 2000.
69. Tingen, C.M., Kiesewetter, S.E., Jozefik, J., Thomas, C., Tagler, D., Shea, L., et al. A macrophage and theca cell-enriched stromal cell population influences growth and survival of immature murine follicles in vitro. Reproduction 141, 809, 2011.
70. Tagler, D., Tu, T., Smith, R.M., Anderson, N.R., Tingen, C.M., Woodruff, T.K., et al. Embryonic fibroblasts enable the culture of primary ovarian follicles within alginate hydrogels. Tissue Eng Part A 18, 1229, 2012.
71. Gilchrist, R., Mottershead, D., and Thompson, J. Oocyte maturation and ovulation-an orchestral symphony of signalling. Aust Biochemist 42, 8, 2011.
72. Scaramuzzi, R.J., Baird, D.T., Campbell, B.K., Driancourt, M.A., Dupont, J., Fortune, J.E., et al. Regulation of folliculogenesis and the determination of ovulation rate in ruminants. Reprod Fertil Dev 23, 444, 2011.
73. Murray, A.A., Gosden, R.G., Allison, V., and Spears, N. Effect of androgens on the development of mouse follicles growing in vitro. J Reprod Fertil 113, 27, 1998.
74. Vendola, K.A., Zhou, J., Adesanya, O.O., Weil, S.J., and Bondy, C.A. Androgens stimulate early stages of follicular growth in the primate ovary. J Clin Invest 101, 2622, 1998.
75. Fauser, B.C., Diedrich, K., Bouchard, P., Dominguez, F., Matzuk, M., Franks, S., et al. Contemporary genetic technologies and female reproduction. Hum Reprod Update 17, 829, 2011.
76. Brannstrom, M., and Norman, R.J. Involvement of leukocytes and cytokines in the ovulatory process and corpus luteum function. Hum Reprod 8, 1762, 1993.
77. Terranova, P.F., and Rice, V.M. Review: cytokine involvement in ovarian processes. Am J Reprod Immunol 37, 50, 1997.
78. Wu, R., Van der Hoek, K.H., Ryan, N.K., Norman, R.J., and Robker, R.L. Macrophage contributions to ovarian function. Hum Reprod Update 10, 119, 2004.