Hypoxia limits mouse follicle growth in vitro
J. M. Connolly A C , M. T. Kane A , L. R. Quinlan A , P. Dockery B and A. C. Hynes A
+ Author Affiliations
- Author Affiliations
A Physiology, National University of Ireland Galway, University Road, Galway, Ireland.
B Anatomy, National University of Ireland Galway, University Road, Galway, Ireland.
C Corresponding author. Email: ailish.hynes@nuigalway.ie
Reproduction, Fertility and Development 28(10) 1570-1579 https://doi.org/10.1071/RD14471
Submitted: 26 November 2014 Accepted: 5 March 2015 Published: 13 April 2015
Abstract
Ovarian follicle culture is useful for elucidation of factors involved in the regulation of follicular function. We examined the effects of gas phase oxygen concentration, an oil overlay, serum type and medium supplementation with FSH, insulin–transferrin–selenium (ITS) and l-ascorbic acid on cultured preantral mouse follicle growth in a spherical, non-attached follicle culture system. Follicle growth in 5% oxygen was significantly (P < 0.01) inferior to growth in 20% oxygen in terms of follicle diameter. This was likely due to hypoxia, as evidenced by significantly (P < 0.05) increased follicle secretion of vascular endothelial growth factor (VEGF), a marker of cell hypoxia. Follicular growth was not (P > 0.05) affected by an oil overlay, ITS supplementation or serum type. Culture in medium with 5% mouse serum, 1 IU mL–1 FSH, 25 μg mL–1 l-ascorbic acid and 20% oxygen without an oil overlay supported the growth of follicles to a maximum diameter of 380 μm in 6 days. Compared with mature preovulatory mouse follicles in vivo that often have diameters >500 μm within the same time frame, in vitro-grown follicles clearly exhibit limited growth. Thus, adequate oxygenation is an essential factor in the process of optimising follicle growth.
Additional keywords: culture system, development, growth, oxygen, preantral, VEGF.
References
Adam, A. A. G., Takahashi, Y., Katagiri, S., and Nagano, M. (2004). In vitro culture of mouse preantral follicles using membrane inserts and developmental competence of in vitro ovulated oocytes. J. Reprod. Dev. 50, 579–586.| In vitro culture of mouse preantral follicles using membrane inserts and developmental competence of in vitro ovulated oocytes.Crossref | GoogleScholarGoogle Scholar |
Bishonga, C., Takahashi, Y., Katagiri, S., Nagano, M., and Ishikawa, A. (2001). In vitro growth of mouse ovarian preantral follicles and the capacity of their oocytes to develop to the blastocyst stage. J. Vet. Med. Sci. 63, 619–624.
| In vitro growth of mouse ovarian preantral follicles and the capacity of their oocytes to develop to the blastocyst stage.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fit1Kgsw%3D%3D&md5=f0db89419dc1500e4a32ed41f9506258CAS | 11459007PubMed |
Boland, N. I., and Gosden, R. G. (1994). Effects of epidermal growth factor on the growth and differentiation of cultured mouse ovarian follicles. J. Reprod. Fertil. 101, 369–374.
| Effects of epidermal growth factor on the growth and differentiation of cultured mouse ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlvFKlu7Y%3D&md5=06928aca1e713273e354942478ac8f0cCAS | 7932371PubMed |
Boland, N. I., Humpherson, P. G., Leese, H. J., and Gosden, R. G. (1993). Pattern of lactate production and steroidogenesis during growth and maturation of mouse ovarian follicles in vitro. Biol. Reprod. 48, 798–806.
| Pattern of lactate production and steroidogenesis during growth and maturation of mouse ovarian follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1enuro%3D&md5=f8b1778131fbced295722922fd2e93e5CAS | 8485244PubMed |
Boland, N. I., Humpherson, P. G., Leese, H. J., and Gosden, R. G. (1994). Characterization of follicular energy metabolism. Hum. Reprod. 9, 604–609.
| 1:STN:280:DyaK2czitFGhsg%3D%3D&md5=b2c0d96fe8e895c60ccf25c691f6e544CAS | 8046010PubMed |
Braw-Tal, R., and Yossefi, S. (1997). Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. J. Reprod. Fertil. 109, 165–171.
| Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhs1Gls7w%3D&md5=2783625474f798791a4996acab26849cCAS | 9068428PubMed |
Byskov, A. G. (1969). Ultrastructural studies on the preovulatory follicle in the mouse ovary. Z. Zellforsch. Mikrosk. Anat. 100, 285–299.
| Ultrastructural studies on the preovulatory follicle in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3c%2FlslOrsA%3D%3D&md5=d2e1489a9fe3ca9a9917e036cb323e96CAS | 5358093PubMed |
Cecconi, S., Barboni, B., Coccia, M., and Mattioli, M. (1999). In vitro development of sheep preantral follicles. Biol. Reprod. 60, 594–601.
| In vitro development of sheep preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsFekt7g%3D&md5=02e7c69f4b12b1a9946451ac5ee5572dCAS | 10026104PubMed |
Cortvrindt, R., Hu, Y., and Smitz, J. (1998). Recombinant luteinizing hormone as a survival and differentiation factor increases oocyte maturation in recombinant follicle stimulating hormone supplemented mouse preantral follicle culture. Hum. Reprod. 13, 1292–1302.
| Recombinant luteinizing hormone as a survival and differentiation factor increases oocyte maturation in recombinant follicle stimulating hormone supplemented mouse preantral follicle culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktF2htbs%3D&md5=623e970233a5154dbe4c4ce2224251cbCAS | 9647562PubMed |
Demeestere, I., Delbaere, A., Gervy, C., Van den Bergh, M., Devreker, F., and Englert, Y. (2002). Effect of preantral follicle isolation technique on in vitro follicular growth, oocyte maturation and embryo development in mice. Hum. Reprod. 17, 2152–2159.
| Effect of preantral follicle isolation technique on in vitro follicular growth, oocyte maturation and embryo development in mice.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38vgt1arsw%3D%3D&md5=b0935e71ffc89738a4b88541bf2a5f3bCAS | 12151451PubMed |
Eppig, J. J., and O’Brien, M. (1996). Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod. 54, 197–207.
| Development in vitro of mouse oocytes from primordial follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtVSisLjO&md5=f9f45ebc57f714300a2f7181e4eab4acCAS | 8838017PubMed |
Eppig, J. J., and Wigglesworth, K. (1995). Factors affecting the developmental competence of mouse oocytes grown in vitro: oxygen concentration. Mol. Reprod. Dev. 42, 447–456.
| Factors affecting the developmental competence of mouse oocytes grown in vitro: oxygen concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpvVGisbw%3D&md5=a3ba0e301b3d34aeca09e8fc0b70f467CAS | 8607975PubMed |
Fortune, J. E. (2003). The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim. Reprod. Sci. 78, 135–163.
| The early stages of follicular development: activation of primordial follicles and growth of preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksF2gsbc%3D&md5=1534b04d788e70a1663eb9af61b59c25CAS | 12818642PubMed |
Freshney, I. (2001). Application of cell cultures to toxicology. Cell Biol. Toxicol. 17, 213–230.
| Application of cell cultures to toxicology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksF2lsA%3D%3D&md5=e790ea6220503a080061882f6da32cccCAS | 11768591PubMed |
Friedman, C. I., Danforth, D. R., Herbosa-Encarnacion, C., Arbogast, L., Alak, B. M., and Seifer, D. B. (1997). Follicular fluid vascular endothelial growth factor concentrations are elevated in women of advanced reproductive age undergoing ovulation induction. Fertil. Steril. 68, 607–612.
| Follicular fluid vascular endothelial growth factor concentrations are elevated in women of advanced reproductive age undergoing ovulation induction.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FgtVyjtw%3D%3D&md5=c580ac26c6fddbb59f55150c7a8ef6cdCAS | 9341598PubMed |
Gook, D. A., Edgar, D. H., Lewis, K., Sheedy, J. R., and Gardner, D. K. (2014). Impact of oxygen concentration on adult murine pre-antral follicle development in vitro and the corresponding metabolic profile. Mol. Hum. Reprod. 20, 31–41.
| Impact of oxygen concentration on adult murine pre-antral follicle development in vitro and the corresponding metabolic profile.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1GqsQ%3D%3D&md5=5b5eecb35f1cf66ab05b9201e8c77caeCAS | 24013158PubMed |
Gstraunthaler, G., Seppi, T., and Pfaller, W. (1999). Impact of culture conditions, culture media volumes, and glucose content on metabolic properties of renal epithelial cell cultures. Are renal cells in tissue culture hypoxic? Cell. Physiol. Biochem. 9, 150–172.
| Impact of culture conditions, culture media volumes, and glucose content on metabolic properties of renal epithelial cell cultures. Are renal cells in tissue culture hypoxic?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtVOiurw%3D&md5=31b4e66709dc76c2843225106f46f66cCAS | 10494029PubMed |
Guarnaccia, M. M., Takami, M., Jones, E. E., Preston, S. L., and Behrman, H. R. (2000). Luteinizing hormone depletes ascorbic acid in preovulatory follicles. Fertil. Steril. 74, 959–963.
| Luteinizing hormone depletes ascorbic acid in preovulatory follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FktlSjsw%3D%3D&md5=063b42e17108cdc6807e8041560d8989CAS | 11056240PubMed |
Halliwell, B., and Gutteridge, J. M. C. (Eds) (1985). Protection against oxygen radicals in biological systems: the superoxide theory of oxygen toxicity. In: ‘Free Radicals in Biology and medicine’. pp. 1–18. ( Oxford University Press: Oxford, UK.)
Hartshorne, G. M. (1997). In vitro culture of ovarian follicles. Rev. Reprod. 2, 94–104.
| In vitro culture of ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktV2nur0%3D&md5=76f6949d1ed2cfc9a7c7b915fcae860eCAS | 9414471PubMed |
Hartshorne, G. M., Sargent, I. L., and Barlow, D. H. (1994). Meiotic progression of mouse oocytes throughout follicle growth and ovulation in vitro. Hum. Reprod. 9, 352–359.
| 1:STN:280:DyaK2c3pvFOlug%3D%3D&md5=0792bd4c112ca637d57a7733031bec85CAS | 8027296PubMed |
Hovatta, O., Silye, R., Abir, R., Krausz, T., and Winston, R. M. (1997). Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture. Hum. Reprod. 12, 1032–1036.
| Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szjsl2qsg%3D%3D&md5=53187709d6a5ff410dafffde60f7e4c0CAS | 9194661PubMed |
Hu, Y., Betzendahl, I., Cortvrindt, R., Smitz, J., and Eichenlaub-Ritter, U. (2001). Effects of low O2 and ageing on spindles and chromosomes in mouse oocytes from pre-antral follicle culture. Hum. Reprod. 16, 737–748.
| Effects of low O2 and ageing on spindles and chromosomes in mouse oocytes from pre-antral follicle culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSisro%3D&md5=361115ac01d3fb74c70c84ac17b29eaeCAS | 11278227PubMed |
Hulshof, S. C., Figueiredo, J. R., Beckers, J. F., Bevers, M. M., van der Donk, J. A., and Van den Hurk, R. (1995). Effects of foetal bovine serum, FSH and 17beta-estradiol on the culture of bovine preantral follicles. Theriogenology 44, 217–226.
| Effects of foetal bovine serum, FSH and 17beta-estradiol on the culture of bovine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt12ksbw%3D&md5=fe5bba7ddd92f15df9ede91f22954c53CAS | 16727721PubMed |
Kątska-Książkiewicz, L. K. (2006). Recent achievements in in vitro culture and preservation of ovarian follicles in mammals. Reprod. Biol. 6, 3–16.
Kreeger, P. K., Deck, J. W., Woodruff, T. K., and Shea, L. D. (2006). The in vitro regulation of ovarian follicle development using alginate–extracellular matrix gels Biomaterials 27, 714–723.
| The in vitro regulation of ovarian follicle development using alginate–extracellular matrix gelsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFakur3E&md5=889f107095a7064ef7d28f7688e9eea0CAS | 16076485PubMed |
Liu, J., Van der Elst, J., Van den Broecke, R., and Dhont, M. (2001). Live offspring by in vitro fertilisation of oocytes from cryopreserved primordial mouse follicles after sequential in vivo transplantation and in vitro maturation. Biol. Reprod. 64, 171–178.
| Live offspring by in vitro fertilisation of oocytes from cryopreserved primordial mouse follicles after sequential in vivo transplantation and in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFCltw%3D%3D&md5=ed93fe4186f5ba425c05740f05bf06bfCAS | 11133672PubMed |
Metzen, E., Wolff, M., Fandrey, J., and Jelkmann, W. (1995). Pericellular Po2 and O2 consumption in monolayer cell cultures. Respir. Physiol. 100, 101–106.
| Pericellular Po2 and O2 consumption in monolayer cell cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmt1Kqsr4%3D&md5=26e0bb8f486fe8039a1c831e0de51fb4CAS | 7624611PubMed |
Mizunuma, H., Liu, X., Andoh, K., Abe, Y., Kobayashi, J., Yamada, K., Yokota, H., Ibuki, Y., and Hasegawa, Y. (1999). Activin from secondary follicles causes small preantral follicles to remain dormant at the resting stage. Endocrinology 140, 37–42.
| Activin from secondary follicles causes small preantral follicles to remain dormant at the resting stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtFWgsw%3D%3D&md5=6137a87143d5ed33e92d0f04fcc98c90CAS | 9886804PubMed |
Morbeck, D. E., Khan, Z., Barnidge, D. R., and Walker, D. L. (2010). Washing mineral oil reduces contaminants and embryotoxicity. Fertil. Steril. 94, 2747–2752.
| Washing mineral oil reduces contaminants and embryotoxicity.Crossref | GoogleScholarGoogle Scholar | 20452587PubMed |
Murray, A. A., Gosden, R. G., Allison, V., and Spears, N. (1998). Effect of androgens on the development of mouse follicles growing in vitro. J. Reprod. Fertil. 113, 27–33.
| Effect of androgens on the development of mouse follicles growing in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsVSgtb8%3D&md5=e9eeb19170ed0a4c03b50e1f91e8be4aCAS | 9713373PubMed |
Murray, A. A., Molinek, M. D., Baker, S. J., Kojima, F. N., Smith, M. F., Hillier, S. G., and Spears, N. (2001). Role of ascorbic acid in promoting follicle integrity and survival in intact mouse ovarian follicles in vitro. Reproduction 121, 89–96.
| Role of ascorbic acid in promoting follicle integrity and survival in intact mouse ovarian follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslarsw%3D%3D&md5=b7222d6bd18d9db2c87de7f2a37a8ceaCAS | 11226031PubMed |
Nayudu, P. L., and Osborn, S. M. (1992). Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro. J. Reprod. Fertil. 95, 349–362.
| Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlt1Cqurs%3D&md5=bd1089619356c99b2c9f14d8e560616eCAS | 1517993PubMed |
Nayudu, P. L., Fehrenbach, A., Kiesel, P., Vitt, U. A., Pancharatna, K., and Osborn, S. (2001). Progress toward understanding follicle development in vitro: appearances are not deceiving. Arch. Med. Res. 32, 587–594.
| Progress toward understanding follicle development in vitro: appearances are not deceiving.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltVentg%3D%3D&md5=cdbf25aa0084a84214c317cf04be8977CAS | 11750734PubMed |
Neeman, M., Abramovitch, R., Schiffenbauer, Y. S., and Tempel, C. (1997). Regulation of angiogenesis by hypoxic stress: from solid tumours to the ovarian follicle. Int. J. Exp. Pathol. 78, 57–70.
| Regulation of angiogenesis by hypoxic stress: from solid tumours to the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szksl2isQ%3D%3D&md5=6f8c8fd1f186969767f09ce2c4c9b74eCAS | 9203980PubMed |
O’Brien, M. J., Pendola, J. K., and Eppig, J. J. (2003). A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol. Reprod. 68, 1682–1686.
| A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt12ltrY%3D&md5=95fc0c8093009d4fa593e22bfd7c7015CAS | 12606400PubMed |
Picton, H. M., and Gosden, R. G. (2000). In vitro growth of human primordial follicles from frozen-banked ovarian tissue. Mol. Cell. Endocrinol. 166, 27–35.
| In vitro growth of human primordial follicles from frozen-banked ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtlGktL4%3D&md5=b91fcb675726cea2c603f7202898aba4CAS | 10989205PubMed |
Picton, H. M., Harris, S. E., Muruvi, W., and Chambers, E. L. (2008). The in vitro growth and maturation of follicles. Reproduction 136, 703–715.
| The in vitro growth and maturation of follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXns1CktA%3D%3D&md5=3169c95f5e75bc1097a0ba5494e96129CAS | 19074213PubMed |
Porter, R. K., and Brand, M. D. (1995). Cellular oxygen consumption depends on body mass. Am. J. Physiol. 269, R226–R228.
| 1:CAS:528:DyaK2MXnt1Grs7w%3D&md5=dcec97d17f6d4cddd01042ba80508110CAS | 7631898PubMed |
Rose, U. M., Hanssen, R. G., and Kloosterboer, H. J. (1999). Development and characterisation of an in vitro ovulation model using mouse ovarian follicles. Biol. Reprod. 61, 503–511.
| Development and characterisation of an in vitro ovulation model using mouse ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslKqt7g%3D&md5=9c0ba312716ecf1b9d70baad9a9c7940CAS | 10411533PubMed |
Rowghani, N. M., Heise, M. K., McKeel, D., McGee, E. A., Koepsel, R. R., and Russell, A. J. (2004). Maintenance of morphology and growth of ovarian follicles in suspension culture. Tissue Eng. 10, 545–552.
| Maintenance of morphology and growth of ovarian follicles in suspension culture.Crossref | GoogleScholarGoogle Scholar | 15165471PubMed |
Segers, I., Adriaenssens, T., Coucke, W., Cortvrindt, R., and Smitz, J. (2008). Timing of nuclear maturation and postovulatory aging in oocytes of in vitro-grown mouse follicles with or without oil overlay. Biol. Reprod. 78, 859–868.
| Timing of nuclear maturation and postovulatory aging in oocytes of in vitro-grown mouse follicles with or without oil overlay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltVOnsr0%3D&md5=91ab7d076f1e3d43d4795903fe4a72a4CAS | 18184922PubMed |
Semenza, G. L. (1999). Regulation of mammalian oxygen homeostasis by hypoxia-inducible factor 1. Annu. Rev. Cell Dev. Biol. 15, 551–578.
| Regulation of mammalian oxygen homeostasis by hypoxia-inducible factor 1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtVSnu70%3D&md5=18e83283945b69e4011bb3bf9397a14cCAS | 10611972PubMed |
Shaw, J., and Trounson, A. (1997). Oncological implications in the replacement of ovarian tissue. Hum. Reprod. 12, 403–405.
| Oncological implications in the replacement of ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3nslSgsA%3D%3D&md5=7f478dc1113fad625cc7705544586be6CAS | 9130725PubMed |
Smitz, J. E., and Cortvrindt, R. G. (2002). The earliest stages of folliculogenesis in vitro. Reproduction 123, 185–202.
| The earliest stages of folliculogenesis in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsFChsbo%3D&md5=121ce6a1ac691809214cba1afaa0cb70CAS | 11866686PubMed |
Smitz, J., Cortvrindt, R., and Van Steirteghem, A. C. (1996). Normal oxygen atmosphere is essential for the solitary long-term culture of early preantral mouse follicles. Mol. Reprod. Dev. 45, 466–475.
| Normal oxygen atmosphere is essential for the solitary long-term culture of early preantral mouse follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsVWgs7g%3D&md5=eac048080aa7bcd94f17e2f64c106c81CAS | 8956285PubMed |
Spears, N., Boland, N. I., Murray, A. A., and Gosden, R. G. (1994). Mouse oocytes derived from in vitro grown primary ovarian follicles are fertile. Hum. Reprod. 9, 527–532.
| 1:STN:280:DyaK2c3nsVymsQ%3D%3D&md5=e564661099e092d99119731c7c9ff269CAS | 8006146PubMed |
Spears, N., de Bruin, J. P., and Gosden, R. G. (1996). The establishment of follicular dominance in co-cultured mouse ovarian follicles. J. Reprod. Fertil. 106, 1–6.
| The establishment of follicular dominance in co-cultured mouse ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtVCnsg%3D%3D&md5=948c508b488ad153979f385de1c61d65CAS | 8667332PubMed |
Spears, N., Murray, A. A., Allison, V., Boland, N. I., and Gosden, R. G. (1998). Role of gonadotrophins and ovarian steroids in the development of mouse follicles in vitro. J. Reprod. Fertil. 113, 19–26.
| Role of gonadotrophins and ovarian steroids in the development of mouse follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsVSgtLc%3D&md5=09d484893c660a1bf8d940b1a0ba79fcCAS | 9713372PubMed |
Stein, W. D. (1990). Chapter 2: Simple diffusion of nonelectrolytes and ions. In: ‘Channels, Carriers, and Pumps: An Introduction to Membrane Transport’. pp. 29–35. (Harcourt Brace Jovanovich: San Diego.)
Stouffer, R. L., Martínez-Chequer, J. C., Molskness, T. A., Xu, F., and Hazzard, T. M. (2001). Regulation and action of angiogenic factors in the primate ovary. Arch. Med. Res. 32, 567–575.
| Regulation and action of angiogenic factors in the primate ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltVensA%3D%3D&md5=eb79fe7140e249f809c53e3c4f9cb064CAS | 11750732PubMed |
Taylor, W. G., and Camalier, R. F. (1982). Modulation of epithelial cell proliferation in culture by dissolved oxygen. J. Cell. Physiol. 111, 21–27.
| Modulation of epithelial cell proliferation in culture by dissolved oxygen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL383hsVansg%3D%3D&md5=a96a73d1a3dfdf8689070507de43d8efCAS | 6806304PubMed |
Telfer, E. E., and Zelinski, M. B. (2013). Ovarian follicle culture: advances and challenges for human and nonhuman primates. Fertil. Steril. 99, 1523–1533.
| Ovarian follicle culture: advances and challenges for human and nonhuman primates.Crossref | GoogleScholarGoogle Scholar | 23635350PubMed |
Telfer, E. E., McLaughlin, M., Ding, C., and Joo Thong, K. (2008). A two-step serum free culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum. Reprod. 23, 1151–1158.
| A two-step serum free culture system supports development of human oocytes from primordial follicles in the presence of activin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1ags7o%3D&md5=9bf84c253156fe836d703ef8231cc87aCAS | 18326514PubMed |
Thomas, F. H., Leask, R., Srsen, V., Riley, S. C., Spears, N., and Telfer, E. E. (2001). Effect of ascorbic acid on health and morphology of bovine preantral follicles during long-term culture. Reproduction 122, 487–495.
| Effect of ascorbic acid on health and morphology of bovine preantral follicles during long-term culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntVGktr4%3D&md5=b91c84b168b2275283e7cbb7ad0abb28CAS | 11597314PubMed |
Vitt, U. A., Kloosterboer, H. J., Rose, U. M., Mulders, J. W., Kiesel, P. S., Bete, S., and Naydu, P. L. (1998). Isoforms of human recombinant follicle-stimulating hormone: comparison of effects murine follicle development in vitro. Biol. Reprod. 59, 854–861.
| Isoforms of human recombinant follicle-stimulating hormone: comparison of effects murine follicle development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsVGrsbo%3D&md5=d68612502585ef73eded7e0423f2a704CAS | 9746735PubMed |
Vitt, U. A., Naydu, P. L., Rose, U. M., and Kloosterboer, H. J. (2001). Embryonic development after follicle culture is influenced by follicle-stimulating hormone isoelectric point range. Biol. Reprod. 65, 1542–1547.
| Embryonic development after follicle culture is influenced by follicle-stimulating hormone isoelectric point range.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVersLo%3D&md5=866bc432180cf3206124c88249acafebCAS | 11673273PubMed |
Wandji, S. A., Eppig, J. J., and Fortune, J. E. (1996). FSH and growth factors affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles. Theriogenology 45, 817–832.
| FSH and growth factors affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XisV2qs7c%3D&md5=e09c8d6de8f5a424bc08a10a8ab1b7b7CAS | 16727844PubMed |
Wandji, S. A., Srsen, V., Nathanielsz, P. W., Eppig, J. J., and Fortune, J. E. (1997). Initiation of growth of baboon primordial follicles in vitro. Hum. Reprod. 12, 1993–2001.
| Initiation of growth of baboon primordial follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FivVenuw%3D%3D&md5=f62289be3b2c6744c25e31d57c80b819CAS | 9363719PubMed |
West, E. R., Zelinski, M. B., Kondapalli, L. A., Gracia, C., Chang, J., Coutifaris, C., Critser, J., Stouffer, R., Shea, L. D., and Woodruff, T. K. (2009). Preserving female fertility following cancer treatment: current options and future possibilities. Pediatr. Blood Cancer 53, 289–295.
| Preserving female fertility following cancer treatment: current options and future possibilities.Crossref | GoogleScholarGoogle Scholar | 19301373PubMed |
Wolff, M., Fandrey, J., and Jelkmann, W. (1993). Microelectrode measurements of pericellular Po2 in erythropoietin-producing human hepatoma cell cultures. Am. J. Physiol. 265, C1266–C1270.
| 1:CAS:528:DyaK2cXltFSrtg%3D%3D&md5=ee5afd5e430bc89fdd6876ee1e1ea29eCAS | 8238479PubMed |
Wright, C. S., Hovatta, O., Margara, R., Trew, G., Winston, R. M., Franks, S., and Hardy, K. (1999). Effects of follicle-stimulating hormone and serum substitution on the in-vitro growth of human ovarian follicles. Hum. Reprod. 14, 1555–1562.
| Effects of follicle-stimulating hormone and serum substitution on the in-vitro growth of human ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktFGhtL4%3D&md5=af7ac9295467530f833c7a20ab22ac90CAS | 10357975PubMed |
Wycherley, G., Downey, D., Kane, M. T., and Hynes, A. C. (2004). A novel follicle culture system markedly increases follicle volume, cell number and oestradiol secretion. Reproduction 127, 669–677.
| A novel follicle culture system markedly increases follicle volume, cell number and oestradiol secretion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1Ohu7w%3D&md5=9b71d0ce3710ebd2318e92e1b459ae0fCAS | 15175503PubMed |
Wycherley, G., Kane, M. T., and Hynes, A. C. (2005). Oxidative phosphorylation and the tricarboxylic acid cycle are essential for normal development of mouse ovarian follicles. Hum. Reprod. 20, 2757–2763.
| Oxidative phosphorylation and the tricarboxylic acid cycle are essential for normal development of mouse ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVelsLbL&md5=681d3355ad1eaab1a4724c85e5c70abcCAS | 16006477PubMed |
Xu, M., Kreeger, P. K., Shea, L. D., and Woodruff, T. K. (2006). Tissue-engineered follicles produce live, fertile offspring. Tissue Eng. 12, 2739–2746.
| Tissue-engineered follicles produce live, fertile offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFSht7fF&md5=9cd68bde5ac7c7a3618a577c10b34d04CAS | 17518643PubMed |
Xu, M., West-Farrell, E. R., Stouffer, R. L., Shea, L. D., Woodruff, T. K., and Zelinski, M. B. (2009a). Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biol. Reprod. 81, 587–594.
| Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVChu7zL&md5=4ec29cddf24c70ab65caddde15eb5a43CAS | 19474063PubMed |
Xu, M., Barrett, S. L., West-Farrell, E., Kondapalli, L. A., Kiesewetter, S. E., Shea, L. D., and Woodruff, T. K. (2009b). In vitro grown human ovarian follicles from cancer patients support oocyte growth. Hum. Reprod. 24, 2531–2540.
| In vitro grown human ovarian follicles from cancer patients support oocyte growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOqurnE&md5=bc4f763d864bafd71f008a0c9a93a30dCAS | 19597190PubMed |
Xu, J., Lawson, M. S., Yeoman, R. R., Zelinski, M. B., and Stouffer, R. L. (2011). Secondary follicle growth and oocyte maturation during encapsulated three-dimensional culture in rhesus monkeys: effects of gonadotrophins, oxygen and fetuin. Hum. Reprod. 26, 1061–1072.
| Secondary follicle growth and oocyte maturation during encapsulated three-dimensional culture in rhesus monkeys: effects of gonadotrophins, oxygen and fetuin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltleht7c%3D&md5=079644d6b143d701fa424c9617780799CAS | 21362681PubMed |
Xu, J., Lawson, M. S., Yeoman, R. R., Molskness, T. A., Ting, A. Y., Stouffer, R. L., and Zelinski, M. B. (2013). Fibrin promotes development and function of macaque primary follicles during encapsulated three-dimensional culture. Hum. Reprod. 28, 2187–2200.
| Fibrin promotes development and function of macaque primary follicles during encapsulated three-dimensional culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFOgtrrL&md5=ff478c1ee21aad4ed3765fd4cce60176CAS | 23608357PubMed |
