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Semin Reprod Med 2011; 29(1): 024-037
DOI: 10.1055/s-0030-1268701
© Thieme Medical Publishers

The Promise of in Vitro Maturation in Assisted Reproduction and Fertility Preservation

Johan E.J Smitz1 , Jeremy G. Thompson2 , Robert B. Gilchrist2
  • 1Follicle Biology Laboratory, Center for Reproductive Medicine and Medical School, Free University Brussels (VUB), Brussels, Belgium
  • 2Research Centre for Reproductive Health, Robinson Institute, School of Paediatrics and Reproductive Health, The University of Adelaide, Adelaide, Australia
Further Information

Publication History

Publication Date:
04 January 2011 (online)

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ABSTRACT

An innovative approach to in vitro maturation (IVM) for application in infertility treatment and fertility preservation is required to bring this patient-friendly treatment into routine practice. Current approaches to IVM never report more than a 10 to 15% implantation rate per embryo transferred, which is two to three times lower and early pregnancy losses are higher than in conventional in vitro fertilization/intracytoplasmic sperm injection. The cornerstone of such an innovative culture technique is the use of pharmacological compounds that allow synchronization of nuclear and cytoplasmic maturation processes within the oocyte. The rationale of a prolonged oocyte maturation period is to promote a longer interaction between the immature oocyte with adequately conditioned cumulus cells. Successful introduction of a new approach to IVM will reduce the requirement of fertility hormones and will be less invasive to the patient's daily life by reducing the need for monitoring of serum hormone levels and intravaginal ultrasound. The new IVM conditions will reduce a whole range of minor and major complications in assisted reproductive technology and finally will also reduce the total cost for treatment. The minimal invasiveness of this procedure will benefit cancer patients who want to store gonadal tissue before undergoing therapy that devastates subsequent germ-cell competence.

KEYWORDS

Meiosis - in vitro maturation - fertility preservation - PCO - phosphodiesterases - GDF9

REFERENCES

  • 1 Blondin P, Bousquet D, Twagiramungu H, Barnes F, Sirard M A. Manipulation of follicular development to produce developmentally competent bovine oocytes.  Biol Reprod. 2002;  66 (1) 38-43
    CrossrefPubMedGoogle Scholar
  • 2 Cha K Y, Koo J J, Ko J J, Choi D H, Han S Y, Yoon T K. Pregnancy after in vitro fertilization of human follicular oocytes collected from nonstimulated cycles, their culture in vitro and their transfer in a donor oocyte program.  Fertil Steril. 1991;  55 (1) 109-113
    PubMedGoogle Scholar
  • 3 Suikkari A M, Söderström-Anttila V. In-vitro maturation of eggs: is it really useful?.  Best Pract Res Clin Obstet Gynaecol. 2007;  21 (1) 145-155
    CrossrefPubMedGoogle Scholar
  • 4 Mikkelsen A L, Lindenberg S. Benefit of FSH priming of women with PCOS to the in vitro maturation procedure and the outcome: a randomized prospective study.  Reproduction. 2001;  122 (4) 587-592
    CrossrefPubMedGoogle Scholar
  • 5 Söderström-Anttila V, Salokorpi T, Pihlaja M, Serenius-Sirve S, Suikkari A M. Obstetric and perinatal outcome and preliminary results of development of children born after in vitro maturation of oocytes.  Hum Reprod. 2006;  21 (6) 1508-1513
    CrossrefPubMedGoogle Scholar
  • 6 Russell J B, Knezevich K M, Fabian K F, Dickson J A. Unstimulated immature oocyte retrieval: early versus midfollicular endometrial priming.  Fertil Steril. 1997;  67 (4) 616-620
    CrossrefPubMedGoogle Scholar
  • 7 Trounson A, Anderiesz C, Jones G. Maturation of human oocytes in vitro and their developmental competence.  Reproduction. 2001;  121 (1) 51-75
    CrossrefPubMedGoogle Scholar
  • 8 Nogueira D, Staessen C, Van de Velde H, Van Steirteghem A. Nuclear status and cytogenetics of embryos derived from in vitro-matured oocytes.  Fertil Steril. 2000;  74 (2) 295-298
    CrossrefPubMedGoogle Scholar
  • 9 Nogueira D, Albano C, Adriaenssens T et al. Human oocytes reversibly arrested in prophase I by phosphodiesterase type 3 inhibitor in vitro.  Biol Reprod. 2003B;  69 (3) 1042-1052
    CrossrefPubMedGoogle Scholar
  • 10 Son W Y, Chung J T, Herrero B et al. Selection of the optimal day for oocyte retrieval based on the diameter of the dominant follicle in hCG-primed in vitro maturation cycles.  Hum Reprod. 2008;  23 (12) 2680-2685
    CrossrefPubMedGoogle Scholar
  • 11 Trounson A, Wood C, Kausche A. In vitro maturation and the fertilization and developmental competence of oocytes recovered from untreated polycystic ovarian patients.  Fertil Steril. 1994;  62 (2) 353-362
    PubMedGoogle Scholar
  • 12 Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results.  Hum Reprod. 1986;  1 (2) 81-87
    PubMedGoogle Scholar
  • 13 Chikazawa K, Araki S, Tamada T. Morphological and endocrinological studies on follicular development during the human menstrual cycle.  J Clin Endocrinol Metab. 1986;  62 (2) 305-313
    CrossrefPubMedGoogle Scholar
  • 14 McNatty K P, Makris A, DeGrazia C, Osathanondh R, Ryan K J. The production of progesterone, androgens, and estrogens by granulosa cells, thecal tissue, and stromal tissue from human ovaries in vitro.  J Clin Endocrinol Metab. 1979A;  49 (5) 687-699
    CrossrefPubMedGoogle Scholar
  • 15 McNatty K P, Smith D M, Makris A, Osathanondh R, Ryan K J. The microenvironment of the human antral follicle: interrelationships among the steroid levels in antral fluid, the population of granulosa cells, and the status of the oocyte in vivo and in vitro.  J Clin Endocrinol Metab. 1979B;  49 (6) 851-860
    CrossrefPubMedGoogle Scholar
  • 16 Blondin P, Sirard M A. Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes.  Mol Reprod Dev. 1995;  41 (1) 54-62
    CrossrefPubMedGoogle Scholar
  • 17 Irving-Rodgers H F, Morris S, Collett R A et al. Phenotypes of the ovarian follicular basal lamina predict developmental competence of oocytes.  Hum Reprod. 2009;  24 (4) 936-944
    CrossrefPubMedGoogle Scholar
  • 18 Jonard S, Robert Y, Cortet-Rudelli C, Pigny P, Decanter C, Dewailly D. Ultrasound examination of polycystic ovaries: is it worth counting the follicles?.  Hum Reprod. 2003;  18 (3) 598-603
    CrossrefPubMedGoogle Scholar
  • 19 Durinzi K L, Saniga E M, Lanzendorf S E. The relationship between size and maturation in vitro in the unstimulated human oocyte.  Fertil Steril. 1995;  63 (2) 404-406
    PubMedGoogle Scholar
  • 20 Cavilla J L, Kennedy C R, Byskov A G, Hartshorne G M. Human immature oocytes grow during culture for IVM.  Hum Reprod. 2008;  23 (1) 37-45
    PubMedGoogle Scholar
  • 21 Fair T, Hyttel P, Greve T. Bovine oocyte diameter in relation to maturational competence and transcriptional activity.  Mol Reprod Dev. 1995;  42 (4) 437-442
    CrossrefPubMedGoogle Scholar
  • 22 Schipper I, Hop W C, Fauser B C. The follicle-stimulating hormone (FSH) threshold/window concept examined by different interventions with exogenous FSH during the follicular phase of the normal menstrual cycle: duration, rather than magnitude, of FSH increase affects follicle development.  J Clin Endocrinol Metab. 1998;  83 (4) 1292-1298
    CrossrefPubMedGoogle Scholar
  • 23 Schramm R D, Bavister B D. Follicle-stimulating hormone priming of rhesus monkeys enhances meiotic and developmental competence of oocytes matured in vitro.  Biol Reprod. 1994;  51 (5) 904-912
    CrossrefPubMedGoogle Scholar
  • 24 Gilchrist R B, Nayudu P L, Hodges J K. Maturation, fertilization, and development of marmoset monkey oocytes in vitro.  Biol Reprod. 1997;  56 (1) 238-246
    CrossrefPubMedGoogle Scholar
  • 25 Wynn P, Picton H M, Krapez J A, Rutherford A J, Balen A H, Gosden R G. Pretreatment with follicle stimulating hormone promotes the numbers of human oocytes reaching metaphase II by in-vitro maturation.  Hum Reprod. 1998;  13 (11) 3132-3138
    CrossrefPubMedGoogle Scholar
  • 26 Mikkelsen A L, Smith S D, Lindenberg S. In-vitro maturation of human oocytes from regularly menstruating women may be successful without follicle stimulating hormone priming.  Hum Reprod. 1999;  14 (7) 1847-1851
    CrossrefPubMedGoogle Scholar
  • 27 Lin Y H, Hwang J L, Huang L W et al. Combination of FSH priming and hCG priming for in-vitro maturation of human oocytes.  Hum Reprod. 2003;  18 (8) 1632-1636
    CrossrefPubMedGoogle Scholar
  • 28 Child T J, Phillips S J, Abdul-Jalil A K, Gulekli B, Tan S L. A comparison of in vitro maturation and in vitro fertilization for women with polycystic ovaries.  Obstet Gynecol. 2002;  100 (4) 665-670
    CrossrefPubMedGoogle Scholar
  • 29 Fadini R, Dal Canto M B, Mignini Renzini M et al. Effect of different gonadotrophin priming on IVM of oocytes from women with normal ovaries: a prospective randomized study.  Reprod Biomed Online. 2009;  19 (3) 343-351
    CrossrefPubMedGoogle Scholar
  • 30 Oktay K H. Options for preservation of fertility in women.  N Engl J Med. 2005;  353 (13) 1418-1420; author reply 1418–1420
    CrossrefPubMedGoogle Scholar
  • 31 Oktay K, Demirtas E, Son W Y, Lostritto K, Chian R C, Tan S L. In vitro maturation of germinal vesicle oocytes recovered after premature luteinizing hormone surge: description of a novel approach to fertility preservation.  Fertil Steril. 2008;  89 (1) 228, e19-e22
    PubMedGoogle Scholar
  • 32 Chian R C, Gilbert L, Huang J Y et al. Live birth after vitrification of in vitro matured human oocytes.  Fertil Steril. 2009;  91 (2) 372-376
    CrossrefPubMedGoogle Scholar
  • 33 Larsen W J, Wert S E, Brunner G D. A dramatic loss of cumulus cell gap junctions is correlated with germinal vesicle breakdown in rat oocytes.  Dev Biol. 1986;  113 (2) 517-521
    CrossrefPubMedGoogle Scholar
  • 34 Downs S M, Daniel S A, Eppig J J. Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor: evidence for a positive stimulus of somatic cell origin.  J Exp Zool. 1988;  245 (1) 86-96
    CrossrefPubMedGoogle Scholar
  • 35 Sugiura K, Pendola F L, Eppig J J. Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism.  Dev Biol. 2005;  279 (1) 20-30
    CrossrefPubMedGoogle Scholar
  • 36 Banwell K M, Thompson J G. In vitro maturation of mammalian oocytes: outcomes and consequences.  Semin Reprod Med. 2008;  26 (2) 162-174
    Article in Thieme ConnectPubMedGoogle Scholar
  • 37 Leese H J, Barton A M. Production of pyruvate by isolated mouse cumulus cells.  J Exp Zool. 1985;  234 (2) 231-236
    CrossrefPubMedGoogle Scholar
  • 38 Sutton-McDowall M L, Gilchrist R B, Thompson J G. Cumulus expansion and glucose utilisation by bovine cumulus-oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone.  Reproduction. 2004;  128 (3) 313-319
    CrossrefPubMedGoogle Scholar
  • 39 Stokes Y M, Clark A R, Thompson J G. Mathematical modeling of glucose supply toward successful in vitro maturation of mammalian oocytes.  Tissue Eng Part A. 2008;  14 (9) 1539-1547
    CrossrefPubMedGoogle Scholar
  • 40 Marshall S, Bacote V, Traxinger R R. Discovery of a metabolic pathway mediating glucose-induced desensitization of the glucose transport system. Role of hexosamine biosynthesis in the induction of insulin resistance.  J Biol Chem. 1991;  266 (8) 4706-4712
    PubMedGoogle Scholar
  • 41 Eppig J J. Gonadotropin stimulation of the expansion of cumulus oophori isolated from mice: general conditions for expansion in vitro.  J Exp Zool. 1979;  208 (1) 111-120
    CrossrefPubMedGoogle Scholar
  • 42 Salustri A, Yanagishita M, Hascall V C. Synthesis and accumulation of hyaluronic acid and proteoglycans in the mouse cumulus cell-oocyte complex during follicle-stimulating hormone-induced mucification.  J Biol Chem. 1989;  264 (23) 13840-13847
    PubMedGoogle Scholar
  • 43 Gutnisky C, Dalvit G C, Pintos L N, Thompson J G, Beconi M T, Cetica P D. Influence of hyaluronic acid synthesis and cumulus mucification on bovine oocyte in vitro maturation, fertilisation and embryo development.  Reprod Fertil Dev. 2007;  19 (3) 488-497
    CrossrefPubMedGoogle Scholar
  • 44 Rossetti L. Perspective: hexosamines and nutrient sensing.  Endocrinology. 2000;  141 (6) 1922-1925
    CrossrefPubMedGoogle Scholar
  • 45 D'Alessandris C, Andreozzi F, Federici M et al. Increased O-glycosylation of insulin signaling proteins results in their impaired activation and enhanced susceptibility to apoptosis in pancreatic beta-cells.  FASEB J. 2004;  18 (9) 959-961
    PubMedGoogle Scholar
  • 46 Fülöp N, Marchase R B, Chatham J C. Role of protein O-linked N-acetyl-glucosamine in mediating cell function and survival in the cardiovascular system.  Cardiovasc Res. 2007;  73 (2) 288-297
    CrossrefPubMedGoogle Scholar
  • 47 Sutton-McDowall M L, Mitchell M, Cetica P et al. Glucosamine supplementation during in vitro maturation inhibits subsequent embryo development: possible role of the hexosamine pathway as a regulator of developmental competence.  Biol Reprod. 2006;  74 (5) 881-888
    CrossrefPubMedGoogle Scholar
  • 48 Schelbach C J, Kind K L, Lane M, Thompson J G. Mechanisms contributing to the reduced developmental competence of glucosamine-exposed mouse oocytes.  Reprod Fertil Dev. 2010;  22 (5) 771-779
    CrossrefPubMedGoogle Scholar
  • 49 Wells L, Vosseller K, Hart G W. Glycosylation of nucleocytoplasmic proteins: signal transduction and O-GlcNAc.  Science. 2001;  291 (5512) 2376-2378
    CrossrefPubMedGoogle Scholar
  • 50 Wells L, Whelan S A, Hart G W. O-GlcNAc: a regulatory post-translational modification.  Biochem Biophys Res Commun. 2003;  302 (3) 435-441
    CrossrefPubMedGoogle Scholar
  • 51 Zachara N E, Hart G W. O-GlcNAc a sensor of cellular state: the role of nucleocytoplasmic glycosylation in modulating cellular function in response to nutrition and stress.  Biochim Biophys Acta. 2004;  1673 (1–2) 13-28
    CrossrefPubMedGoogle Scholar
  • 52 Sutton M L, Gilchrist R B, Thompson J G. Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity.  Hum Reprod Update. 2003;  9 (1) 35-48
    CrossrefPubMedGoogle Scholar
  • 53 Dumollard R, Carroll J, Duchen M R, Campbell K, Swann K. Mitochondrial function and redox state in mammalian embryos.  Semin Cell Dev Biol. 2009;  20 (3) 346-353
    CrossrefPubMedGoogle Scholar
  • 54 Herrick J R, Brad A M, Krisher R L. Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro.  Reproduction. 2006;  131 (2) 289-298
    CrossrefPubMedGoogle Scholar
  • 55 Urner F, Sakkas D. Involvement of the pentose phosphate pathway and redox regulation in fertilization in the mouse.  Mol Reprod Dev. 2005;  70 (4) 494-503
    CrossrefPubMedGoogle Scholar
  • 56 Downs S M, Humpherson P G, Leese H J. Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway.  Biol Reprod. 1998;  58 (4) 1084-1094
    CrossrefPubMedGoogle Scholar
  • 57 Stojkovic M, Machado S A, Stojkovic P et al. Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture.  Biol Reprod. 2001;  64 (3) 904-909
    CrossrefPubMedGoogle Scholar
  • 58 Eppig J J. The participation of cyclic adenosine monophosphate (cAMP) in the regulation of meiotic maturation of oocytes in the laboratory mouse.  J Reprod Fertil Suppl. 1989;  38 3-8
    PubMedGoogle Scholar
  • 59 Hashimoto S, Minami N, Takakura R, Yamada M, Imai H, Kashima N. Low oxygen tension during in vitro maturation is beneficial for supporting the subsequent development of bovine cumulus-oocyte complexes.  Mol Reprod Dev. 2000;  57 (4) 353-360
    CrossrefPubMedGoogle Scholar
  • 60 Hashimoto S, Minami N, Yamada M, Imai H. Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents.  Mol Reprod Dev. 2000;  56 (4) 520-526
    CrossrefPubMedGoogle Scholar
  • 61 Banwell K M, Lane M, Russell D L, Kind K L, Thompson J G. Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development.  Hum Reprod. 2007;  22 (10) 2768-2775
    CrossrefPubMedGoogle Scholar
  • 62 Preis K A, Seidel Jr G E, Gardner D K. Reduced oxygen concentration improves the developmental competence of mouse oocytes following in vitro maturation.  Mol Reprod Dev. 2007;  74 (7) 893-903
    CrossrefPubMedGoogle Scholar
  • 63 Pinyopummintr T, Bavister B D. Optimum gas atmosphere for in vitro maturation and in vitro fertilization of bovine oocytes.  Theriogenology. 1995;  44 (4) 471-477
    CrossrefPubMedGoogle Scholar
  • 64 Clark A R, Stokes Y M, Lane M, Thompson J G. Mathematical modelling of oxygen concentration in bovine and murine cumulus-oocyte complexes.  Reproduction. 2006;  131 (6) 999-1006
    CrossrefPubMedGoogle Scholar
  • 65 Cetica P D, Pintos L N, Dalvit G C, Beconi M T. Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation.  IUBMB Life. 2001;  51 (1) 57-64
    PubMedGoogle Scholar
  • 66 Tatemoto H, Sakurai N, Muto N. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells.  Biol Reprod. 2000;  63 (3) 805-810
    CrossrefPubMedGoogle Scholar
  • 67 de Matos D G, Furnus C C, Moses D F. Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells.  Biol Reprod. 1997;  57 (6) 1420-1425
    CrossrefPubMedGoogle Scholar
  • 68 de Matos D G, Furnus C C. The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development effect of beta-mercaptoethanol, cysteine and cystine.  Theriogenology. 2000;  53 (3) 761-771
    CrossrefPubMedGoogle Scholar
  • 69 Sutovsky P, Schatten G. Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization.  Biol Reprod. 1997;  56 (6) 1503-1512
    CrossrefPubMedGoogle Scholar
  • 70 Ferguson E M, Leese H J. Triglyceride content of bovine oocytes and early embryos.  J Reprod Fertil. 1999;  116 (2) 373-378
    PubMedGoogle Scholar
  • 71 Ferguson E M, Leese H J. A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development.  Mol Reprod Dev. 2006;  73 (9) 1195-1201
    CrossrefPubMedGoogle Scholar
  • 72 Smitz J, Nogueira D, Vanhoutte L, De Matos D G, Cortvrindt R. Oocyte in vitro maturation. In: Gardner DK, Weissman A, Howles C M, Shoham Z, eds. Textbook of Assisted Reproductive Techniques: Laboratory and Clinical Perspectives. 2nd ed. London, United Kingdom: Martin Dunitz; 2004: 125-161
    Google Scholar
  • 73 Gilchrist R B, Thompson J G. Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro.  Theriogenology. 2007;  67 (1) 6-15
    CrossrefPubMedGoogle Scholar
  • 74 Downs S M, Schroeder A C, Eppig J J. Developmental capacity of mouse oocytes following maintenance of meiotic arrest in vitro.  Gamete Res. 1986;  15 305-316
    CrossrefPubMedGoogle Scholar
  • 75 Sirard M A, First N L. In vitro inhibition of oocyte nuclear maturation in the bovine.  Biol Reprod. 1988;  39 (2) 229-234
    CrossrefPubMedGoogle Scholar
  • 76 Wiersma A, Hirsch B, Tsafriri A et al. Phosphodiesterase 3 inhibitors suppress oocyte maturation and consequent pregnancy without affecting ovulation and cyclicity in rodents.  J Clin Invest. 1998;  102 (3) 532-537
    CrossrefPubMedGoogle Scholar
  • 77 Luciano A M, Pocar P, Milanesi E et al. Effect of different levels of intracellular cAMP on the in vitro maturation of cattle oocytes and their subsequent development following in vitro fertilization.  Mol Reprod Dev. 1999;  54 (1) 86-91
    CrossrefPubMedGoogle Scholar
  • 78 Luciano A M, Modina S, Vassena R, Milanesi E, Lauria A, Gandolfi F. Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte-cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte.  Biol Reprod. 2004;  70 (2) 465-472
    CrossrefPubMedGoogle Scholar
  • 79 Thomas R E, Armstrong D T, Gilchrist R B. Differential effects of specific phosphodiesterase isoenzyme inhibitors on bovine oocyte meiotic maturation.  Dev Biol. 2002;  244 (2) 215-225
    CrossrefPubMedGoogle Scholar
  • 80 Horner K, Livera G, Hinckley M, Trinh K, Storm D, Conti M. Rodent oocytes express an active adenylyl cyclase required for meiotic arrest.  Dev Biol. 2003;  258 (2) 385-396
    CrossrefPubMedGoogle Scholar
  • 81 Vaccari S, Weeks II J L, Hsieh M, Menniti F S, Conti M. Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes.  Biol Reprod. 2009;  81 (3) 595-604
    CrossrefPubMedGoogle Scholar
  • 82 Sirard M A, Bilodeau S. Granulosa cells inhibit the resumption of meiosis in bovine oocytes in vitro.  Biol Reprod. 1990;  43 (5) 777-783
    CrossrefPubMedGoogle Scholar
  • 83 De Loos F A, Zeinstra E, Bevers M M. Follicular wall maintains meiotic arrest in bovine oocytes cultured in vitro.  Mol Reprod Dev. 1994;  39 (2) 162-165
    CrossrefPubMedGoogle Scholar
  • 84 Lonergan P, Khatir H, Carolan C, Mermillod P. Bovine blastocyst production in vitro after inhibition of oocyte meiotic resumption for 24 h.  J Reprod Fertil. 1997;  109 (2) 355-365
    PubMedGoogle Scholar
  • 85 Fulka Jr J, Leibfried-Rutledge M L, First N L. Effect of 6-dimethylaminopurine on germinal vesicle breakdown of bovine oocytes.  Mol Reprod Dev. 1991;  29 (4) 379-384
    CrossrefPubMedGoogle Scholar
  • 86 Mermillod P, Tomanek M, Marchal R, Meijer L. High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 hours in culture by specific inhibition of MPF kinase activity.  Mol Reprod Dev. 2000;  55 (1) 89-95
    CrossrefPubMedGoogle Scholar
  • 87 Kubelka M, Motlík J, Schultz R M, Pavlok A. Butyrolactone I reversibly inhibits meiotic maturation of bovine oocytes without influencing chromosome condensation activity.  Biol Reprod. 2000;  62 (2) 292-302
    CrossrefPubMedGoogle Scholar
  • 88 Lonergan P, Dinnyes A, Fair T, Yang X, Boland M. Bovine oocyte and embryo development following meiotic inhibition with butyrolactone I.  Mol Reprod Dev. 2000;  57 (2) 204-209
    CrossrefPubMedGoogle Scholar
  • 89 Wu G M, Sun Q Y, Mao J et al. High developmental competence of pig oocytes after meiotic inhibition with a specific M-phase promoting factor kinase inhibitor, butyrolactone I.  Biol Reprod. 2002;  67 (1) 170-177
    CrossrefPubMedGoogle Scholar
  • 90 Grupen C G, Fung M, Armstrong D T. Effects of milrinone and butyrolactone-I on porcine oocyte meiotic progression and developmental competence.  Reprod Fertil Dev. 2006;  18 (3) 309-317
    CrossrefPubMedGoogle Scholar
  • 91 Anderiesz C, Fong C Y, Bongso A, Trounson A O. Regulation of human and mouse oocyte maturation in vitro with 6-dimethylaminopurine.  Hum Reprod. 2000;  15 (2) 379-388
    CrossrefPubMedGoogle Scholar
  • 92 Funahashi H, Cantley T C, Day B N. Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization.  Biol Reprod. 1997;  57 (1) 49-53
    CrossrefPubMedGoogle Scholar
  • 93 Bilodeau S, Fortier M A, Sirard M A. Effect of adenylate cyclase stimulation on meiotic resumption and cyclic AMP content of zona-free and cumulus-enclosed bovine oocytes in vitro.  J Reprod Fertil. 1993;  97 (1) 5-11
    PubMedGoogle Scholar
  • 94 Tsafriri A, Chun S Y, Zhang R, Hsueh A J, Conti M. Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors.  Dev Biol. 1996;  178 (2) 393-402
    CrossrefPubMedGoogle Scholar
  • 95 Conti M, Andersen C B, Richard F J, Shitsukawa K, Tsafriri A. Role of cyclic nucleotide phosphodiesterases in resumption of meiosis.  Mol Cell Endocrinol. 1998;  145 (1–2) 9-14
    CrossrefPubMedGoogle Scholar
  • 96 Conti M, Andersen C B, Richard F et al. Role of cyclic nucleotide signaling in oocyte maturation.  Mol Cell Endocrinol. 2002;  187 (1–2) 153-159
    CrossrefPubMedGoogle Scholar
  • 97 Sasseville M, Côté N, Vigneault C, Guillemette C, Richard F J. 3'5′-cyclic adenosine monophosphate-dependent up-regulation of phosphodiesterase type 3A in porcine cumulus cells.  Endocrinology. 2007;  148 (4) 1858-1867
    CrossrefPubMedGoogle Scholar
  • 98 Sasseville M, Albuz F K, Côté N, Guillemette C, Gilchrist R B, Richard F J. Characterization of novel phosphodiesterases in the bovine ovarian follicle.  Biol Reprod. 2009;  81 (2) 415-425
    CrossrefPubMedGoogle Scholar
  • 99 Shitsukawa K, Andersen C B, Richard F J et al. Cloning and characterization of the cyclic guanosine monophosphate-inhibited phosphodiesterase PDE3A expressed in mouse oocyte.  Biol Reprod. 2001;  65 (1) 188-196
    CrossrefPubMedGoogle Scholar
  • 100 Nogueira D, Cortvrindt R, De Matos D G, Vanhoutte L, Smitz J. Effect of phosphodiesterase type 3 inhibitor on developmental competence of immature mouse oocytes in vitro.  Biol Reprod. 2003A;  69 (6) 2045-2052
    CrossrefPubMedGoogle Scholar
  • 101 Thomas R E, Thompson J G, Armstrong D T, Gilchrist R B. Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity.  Biol Reprod. 2004A;  71 (4) 1142-1149
    CrossrefPubMedGoogle Scholar
  • 102 Vanhoutte L, Nogueira D, Dumortier F, De Sutter P. Assessment of a new in vitro maturation system for mouse and human cumulus-enclosed oocytes: three-dimensional prematuration culture in the presence of a phosphodiesterase 3-inhibitor.  Hum Reprod. 2009A;  24 (8) 1946-1959
    CrossrefPubMedGoogle Scholar
  • 103 Thomas R E, Armstrong D T, Gilchrist R B. Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosphate levels.  Biol Reprod. 2004B;  70 (3) 548-556
    PubMedGoogle Scholar
  • 104 Vanhoutte L, De Sutter P, Nogueira D, Gerris J, Dhont M, Van der Elst J. Nuclear and cytoplasmic maturation of in vitro matured human oocytes after temporary nuclear arrest by phosphodiesterase 3-inhibitor.  Hum Reprod. 2007;  22 (5) 1239-1246
    CrossrefPubMedGoogle Scholar
  • 105 Shu Y M, Zeng H T, Ren Z et al. Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes.  Hum Reprod. 2008;  23 (3) 504-513
    CrossrefPubMedGoogle Scholar
  • 106 Vanhoutte L, Nogueira D, De Sutter P. Prematuration of human denuded oocytes in a three-dimensional co-culture system: effects on meiosis progression and developmental competence.  Hum Reprod. 2009B;  24 (3) 658-669
    CrossrefPubMedGoogle Scholar
  • 107 Tanghe S, Van Soom A, Nauwynck H, Coryn M, de Kruif A. Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization.  Mol Reprod Dev. 2002;  61 (3) 414-424
    CrossrefPubMedGoogle Scholar
  • 108 Albertini D F, Barrett S L. Oocyte-somatic cell communication.  Reprod Suppl. 2003;  61 49-54
    PubMedGoogle Scholar
  • 109 Gilchrist R B, Ritter L J, Armstrong D T. Oocyte-somatic cell interactions during follicle development in mammals.  Anim Reprod Sci. 2004;  82–83 431-446
    PubMedGoogle Scholar
  • 110 Hyttel P, Fair T, Callesen H, Greve T. Oocyte growth, capacitation and final maturation in cattle.  Theriogenology. 1997;  47 23-32
    CrossrefPubMedGoogle Scholar
  • 111 Gilchrist R B. Oocyte-cumulus cell interactions regulating oocyte quality.  Acta Scientiae Veterinariae. 2008;  36 S269-S278
    PubMedGoogle Scholar
  • 112 Sirard M A, Desrosier S, Assidi M. In vivo and in vitro effects of FSH on oocyte maturation and developmental competence.  Theriogenology. 2007;  68 (Suppl 1) S71-S76
    CrossrefPubMedGoogle Scholar
  • 113 Eppig J J, Schroeder A C, O'Brien M J. Developmental capacity of mouse oocytes matured in vitro: effects of gonadotrophic stimulation, follicular origin and oocyte size.  J Reprod Fertil. 1992;  95 (1) 119-127
    PubMedGoogle Scholar
  • 114 Izadyar F, Zeinstra E, Bevers M M. Follicle-stimulating hormone and growth hormone act differently on nuclear maturation while both enhance developmental competence of in vitro matured bovine oocytes.  Mol Reprod Dev. 1998;  51 (3) 339-345
    CrossrefPubMedGoogle Scholar
  • 115 Park J Y, Su Y Q, Ariga M, Law E, Jin S L, Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle.  Science. 2004;  303 (5658) 682-684
    CrossrefPubMedGoogle Scholar
  • 116 Ali A, Sirard M A. Protein kinases influence bovine oocyte competence during short-term treatment with recombinant human follicle stimulating hormone.  Reproduction. 2005;  130 (3) 303-310
    CrossrefPubMedGoogle Scholar
  • 117 Eppig J J, Wigglesworth K, Pendola F, Hirao Y. Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells.  Biol Reprod. 1997;  56 (4) 976-984
    CrossrefPubMedGoogle Scholar
  • 118 Li R, Norman R J, Armstrong D T, Gilchrist R B. Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells.  Biol Reprod. 2000;  63 (3) 839-845
    CrossrefPubMedGoogle Scholar
  • 119 Gilchrist R B, Ritter L J, Myllymaa S et al. Molecular basis of oocyte-paracrine signalling that promotes granulosa cell proliferation.  J Cell Sci. 2006;  119 (Pt 18) 3811-3821
    CrossrefPubMedGoogle Scholar
  • 120 Hussein T S, Froiland D A, Amato F, Thompson J G, Gilchrist R B. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins.  J Cell Sci. 2005;  118 (Pt 22) 5257-5268
    CrossrefPubMedGoogle Scholar
  • 121 Vanderhyden B C, Cohen J N, Morley P. Mouse oocytes regulate granulosa cell steroidogenesis.  Endocrinology. 1993;  133 (1) 423-426
    CrossrefPubMedGoogle Scholar
  • 122 Sutton M L, Cetica P D, Beconi M T, Kind K L, Gilchrist R B, Thompson J G. Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes.  Reproduction. 2003A;  126 (1) 27-34
    CrossrefPubMedGoogle Scholar
  • 123 Dragovic R A, Ritter L J, Schulz S J, Amato F, Armstrong D T, Gilchrist R B. Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion.  Endocrinology. 2005;  146 (6) 2798-2806
    CrossrefPubMedGoogle Scholar
  • 124 Gilchrist R B, Lane M, Thompson J G. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality.  Hum Reprod Update. 2008;  14 (2) 159-177
    CrossrefPubMedGoogle Scholar
  • 125 Hussein T S, Thompson J G, Gilchrist R B. Oocyte-secreted factors enhance oocyte developmental competence.  Dev Biol. 2006;  296 (2) 514-521
    CrossrefPubMedGoogle Scholar
  • 126 Yeo C X, Gilchrist R B, Thompson J G, Lane M. Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice.  Hum Reprod. 2008;  23 (1) 67-73
    CrossrefPubMedGoogle Scholar
  • 127 McKenzie L J, Pangas S A, Carson S A et al. Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF.  Hum Reprod. 2004;  19 (12) 2869-2874
    CrossrefPubMedGoogle Scholar
  • 128 Li Q, McKenzie L J, Matzuk M M. Revisiting oocyte-somatic cell interactions: in search of novel intrafollicular predictors and regulators of oocyte developmental competence.  Mol Hum Reprod. 2008;  14 (12) 673-678
    CrossrefPubMedGoogle Scholar
  • 129 Fayad T, Lévesque V, Sirois J, Silversides D W, Lussier J G. Gene expression profiling of differentially expressed genes in granulosa cells of bovine dominant follicles using suppression subtractive hybridization.  Biol Reprod. 2004;  70 (2) 523-533
    CrossrefPubMedGoogle Scholar
  • 130 Diaz F J, Wigglesworth K, Eppig J J. Oocytes are required for the preantral granulosa cell to cumulus cell transition in mice.  Dev Biol. 2007;  305 (1) 300-311
    CrossrefPubMedGoogle Scholar
  • 131 Leoni G G, Bebbere D, Succu S et al. Relations between relative mRNA abundance and developmental competence of ovine oocytes.  Mol Reprod Dev. 2007;  74 (2) 249-257
    CrossrefPubMedGoogle Scholar
  • 132 Feuerstein P, Cadoret V, Dalbies-Tran R, Guerif F, Bidault R, Royere D. Gene expression in human cumulus cells: one approach to oocyte competence.  Hum Reprod. 2007;  22 (12) 3069-3077
    CrossrefPubMedGoogle Scholar
  • 133 van Montfoort A P, Geraedts J P, Dumoulin J C, Stassen A P, Evers J L, Ayoubi T A. Differential gene expression in cumulus cells as a prognostic indicator of embryo viability: a microarray analysis.  Mol Hum Reprod. 2008;  14 (3) 157-168
    CrossrefPubMedGoogle Scholar
  • 134 Hamel M, Dufort I, Robert C et al. Identification of differentially expressed markers in human follicular cells associated with competent oocytes.  Hum Reprod. 2008;  23 (5) 1118-1127
    CrossrefPubMedGoogle Scholar
  • 135 Pavlok A, Lapathitis G, Cech S et al. Simulation of intrafollicular conditions prevents GVBD in bovine oocytes: a better alternative to affect their developmental capacity after two-step culture.  Mol Reprod Dev. 2005;  71 (2) 197-208
    CrossrefPubMedGoogle Scholar
  • 136 Nogueira D, Ron-El R, Friedler S et al. Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development.  Biol Reprod. 2006;  74 (1) 177-184
    CrossrefPubMedGoogle Scholar
  • 137 Shu-Chi M, Jiann-Loung H, Yu-Hung L, Tseng-Chen S, Ming-I L, Tsu-Fuh Y. Growth and development of children conceived by in-vitro maturation of human oocytes.  Early Hum Dev. 2006;  82 (10) 677-682
    CrossrefPubMedGoogle Scholar
  • 138 Eppig J J, O'Brien M J, Wigglesworth K, Nicholson A, Zhang W, King B A. Effect of in vitro maturation of mouse oocytes on the health and lifespan of adult offspring.  Hum Reprod. 2009;  24 (4) 922-928
    CrossrefPubMedGoogle Scholar
  • 139 Baart E B, Martini E, Eijkemans M J et al. Milder ovarian stimulation for in-vitro fertilization reduces aneuploidy in the human preimplantation embryo: a randomized controlled trial.  Hum Reprod. 2007;  22 (4) 980-988
    CrossrefPubMedGoogle Scholar

Johan E.J. SmitzM.D. Ph.D. 

Follicle Biology Laboratory, Center for Reproductive Medicine and Medical School, Free University Brussels (VUB)

Laarbeeklaan 101, 1090 Brussels, Belgium

Email: johan.smitz@uzbrussel.be

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