Cyclic nucleotide in oocyte In vitro maturation in Assisted Reproductive Technology

In vitro maturation (IVM) is a promising assisted reproductive technology (ART) for human infertility treatment. However, when cumulus oocyte complexes (COCs) are removed from their follicular environment when manipulated in vitro, it can lead to a decrease of intra-oocyte cyclic adenosine 3’, 5’-monophosphare (cAMP) causing spontaneous nuclear maturation and an asynchrony with the oocytes’ cytoplasmic maturation, resulting in poor embryo developmental outcomes. Nuclear and cytoplasmic synchrony is important during oocyte maturation within antral follicles.
It is maintained partially by the actions of c-type natriuretic peptide (CNP) binding with natriuretic peptide receptor 2 (NPR2), supporting high cAMP levels thus holding the oocyte in meiotic arrest. Addition of CNP to pre-IVM media has the capacity of maintaining cAMP levels and thus improve synchrony. Moreover, in women with advanced maternal age, successful IVM of aging oocytes faces significant challenges due to the morphological and cellular changes. Inhibiting initiation of nuclear maturation by cAMP modulator, CNP during pre-IVM period and thus improve oocyte developmental competence regardless of oocyte age.
Article Metrics:
- Romero S, Sanchez F, Lolicato F, Ranst HV and Smitz J. Immature oocytes from unprimed mice become a valuable source from embryo production when using C-type natriuretic peptide as essential component of culture medium. Biology of Reproduction 2016; 95: 1-10
- Wei Q, Zhou C, Yuan M, Miao Y, Zhao X and Ma B. Effect of C-type natriuretic peptide on maturation and developmental competence of immature mouse oocytes in vitro. Reproduction, Fertility and Development 2016; 29:319-324
- Zeng HT, Ren Z, Guzman L, Wang X, Sutton-McDowall ML, Ritter LJ, De Vos M, Smitz J, Thompson JG and Gilchrist RB. Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence. Human Reproduction 2013; 28: 1536-1545
- Edwards RG. Meiosis in ovarian oocytes of adult mammals. Nature 1962; 196:446
- Chian RC, Uzelac PS and Nargund G. In vitro maturation of human immature oocytes for fertility preservation. Fertility Sterility 2013; 99: 1173-1181
- Ellenbogen A, Shavit T and Shalom-Paz E. IVM results are comparable and may have advantages over standard IVF Facts. Views & Visions in Obstetrics, Gynaecology and Reproductive Health 2014; 6: 77-80
- Xu J, Bernuci MP, Lawson MS, Yeoman RR, Fisher TE, Zelinski MB and Stouffer RL. Survival, growth, and maturation of secondary follicles from prepubertal, young, and older adult rhesus monkeys during encapsulated three-dimensional culture: effects of gonadotropins and insulin. Reproduction 2010; 140:685-697
- Child TJ, Philips SJ, Abdul-Jalil AK, Gulekli B and Tan SL. A comparison of in vitro maturation and in vitro fertilization for women with polycystic ovarie.s Obstetrics & Gynaecology 2002; 100: 665-670
- Pincus G and Enzmann EV. The comparative behavior of mammalian eggs in vivo and in vitro: 1. the activation of ovarian eggs. The Journal of Experimental Medicine 1935; 62: 665-675
- Edwards RG. Maturation in vitro of human ovarian oocytes. The Lancet 1965; 2: 926-929
- Zhang M, Su YQ, Sugiura K, Xia G and Epping JJ. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 2010; 330: 366-369
- Lord T, Nixon B, Jones KT and Aitken J. Melatonin prevents post-ovulatory oocyte aging in the mouse and extends the window for optimal fertilization in vitro. Reproduction 2013; 88: 67-76
- Koyama K, Kang SS, Huang W, Yanagawa Y, Takahashi Y and Nagano M. Aging-related changes In Vitro-matured bovine oocytes: oxidative stress, mitochondrial activity and ATP content after nuclear maturation. Journal of Reproduction and Development 2014; 60:136-142
- Walls ML, Hunter T, Ryan JP, Keelan JA, Nathan E and Hart RJ In vitro maturation as an alternative to standard in vitro fertilisaiton for patients diagnosed with polycystic ovaries: a comparative analysis of fresh, frozen and cumulative cycle outcomes. Human Reproduction 2015; 30:88-96
- Maman E, Meirow D, Brengauz M, Raanani H, Dor J and Hourvitz. A Luteal phase oocyte retrieval and in vitro maturation is an optional procedure for urgent fertility preservation. Fertility and Sterility 2011; 95: 64-67
- Liu K and Case A. Advanced Reproductive Age and Fertility. Journal of Obstetrics and Gynaecology 2011; 33:1165-1175
- Hourvitz A, Maman E, Brengauz M, Machtinger R and Dor J. In vitro maturation for patients with repeated in vitro fertilization failure due to ‘oocyte maturation abnormalities. Fertility and Sterility 2010; 92: 496-501
- Cha KY, Koo JJ, Ko JJ, Choi DH, Han SY and Yoon TK. Pregnancy after in vitro fertilization of human follicular oocytes collected from non-stimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertility and Sterility 1991; 55:109-13
- Franks S, McCarthy MI and Hardy K Development of polycystic ovary syndrome: involvement of genetic and environmental factors International. Journal of Andrology 2006; 29: 278-285
- Goodarzi MO, Dumesic DA, Chazenbalk G and Azziz R. Polycystic ovary syndrome: etiology, pathogenesis and diagnosis Nature Reviews Endocronology 2011; 7: 219-231
- Siristatidis CS, Vrachnis N, Creatsa M, Maheshwari A and Bhattacharya S. In vitro maturation in subfertile women with polycystic ovarian syndrome undergoing assisted reproduction (review). Cochrane Database of Systematic Reviews 2013; 10: 1-24
- Trounson A, Wood C and Kausche A. In vitro maturation and the fertilization and developmental competence of oocytes recovered from untreated polycystic ovarian patients Fertility and Sterility 1994; 62: 353-362
- Hassold T, Jacobs PA, Leppert M and Sheldon M Cytogenetic and molecular studies of trisomy. Journal of Medical Genetics 1987; 24: 725-732
- Staessen C, Platteau P, Assche EV, Michiels A, Tournaye H, Camus M, Devroey P, Liebaers I and Steirteghem AV. Comparison of blastocyst transfer with or without preimplantation genetic diagnosis for aneuploidy screening in couples with advanced maternal age: a prospective randomized controlled trial. Human Reproduction 2004; 19: 2849-2858
- Munne S, Alikani M, Tomkin G, Grifo J and Cohen J. Embryo morphology, developmental rates and maternal age are correlated with chromosome abnormalities Fertility and Sterility 1995; 64: 382-391
- Dailey T, Dale B, Cohen J and Munne S. Association between non-disjunction and maternal age in meiosis-II human oocytes detected by FISH analysis. The American Journal of Human Genetics 1996; 59:176-184
- Marquez C, Sanalinas M, Bahce M, Alikani M and Munne S. Chromosome abnormalities in 1255 cleavage-stage human embryos Reproductive BioMedicine Online 2000; 1: 17-26
- Katz-Jaffe MG, Trounson AO & Cram DS. Chromosome 21 mosaic human preimplantation embryos predominantly arise from diploid conceptions Fertility and Sterility 2005; 84: 634-643
- Baart EB, Martini E, Eijkemans MJ, Van Opstal D, Beckers NG, Verhoeff. Milder ovarian stimulation for in-vitro fertilization reduces aneuploidy in the human preimplantation embryo: a randomized controlled trial. Human Reproduction 2007; 22: 980–988
- Hassold T and Chiu D. Maternal age-specific rates of numerical chromosome abnormalities with special reference to trisomy. Human Genetics 1985; 70:11-17
- Hassold T, Hall H and Hunt P The origin of human aneuploidy: where we have been, where we are going. Human Molecular Genetics 2007; 2: R203-R208
- Cross PC and Brinster RL. In vitro development of mouse oocytes. Biology of Reproduction 1970; 3: 298-307
- Le Du A, Kadoch IJ, Bourcigaux N, Doumerc S, Bourrier MC, Chevalier N, Fanchin R, Chian RC, Tachdjian G, Frydman R and Frydman N (2005) In vitro oocyte maturation for the treatment of infertility associated with polycystic ovarian syndrome: the French experience Human reproduction 20 420-424
- Sanchez F, Romero S, Vos MD, Verheyen G and Smitz J. Human cumulus-enclosed germinal vesicle oocytes from early antral follicles reveal heterogeneous cellular and molecular features associated with in vitro maturation capacity. Human Reproduction 2015; 30: 1396-1409
- Romeu A, Muasher SJ, Acosta AA, Veeck LL, Diaz J, Jones GS, Jones HW Jr and Rosenwaks Z. Results of in vitro fertilization attempts in women 40 years of age and older: the Norfolk experience. Fertility and Sterility 1987; 47: 130-136
- Lim AS and Tsakok MF. Age-related decline in fertility: a link to degenerative oocytes? Fertility and Sterility 1997; 68: 265-271
- Henderson SA and Edwards RG. Chiasma frequency and maternal age in mammals. Nature 1968; 218: 22-28
- Tarin JJ, Brines J and Cano A. Long-term effects of delayed parenthood Human Reproduction 1998; 13:2371-2376
- Sher G, Keskintepe L, Keskintepe M, Ginsburg M, Maassarani G, Yakut T, Baltaci V, Kotze D & Unsal E. Oocyte karyotyping by comparative genomic hybridization (correction of hybridization) provides a highly reliable method for selecting “competent” embryos, markedly improving in vitro fertilization outcome: a multiphase study. Fertility and Sterility 2007;87:1033-1040
- Vivarelli E, Conti M, De Felici M and Siracusa G. Meiotic resumption and intracellular cAMP levels in mouse oocytes treated with compounds which act on cAMP metabolism. Cell Differences 1983;12: 271-276
- Törnell J, Billig H and Hillensjo T. Resumption of rat oocyte meiosis is paralleled by a decrease in guanosine 3',5'-cyclic monophosphate (cGMP) and is inhibited by microinjection of cGMP. Acta Physiologica Scandinavica 1990; 139: 511-517
- Li HJ, McDowall ML, Wang X, Sugimura S, Thompson JG and Gilchrist RB. Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions. Human Reproduction 2016; 31: 810-821
- Tsuji T, Kiyosu C, Akiyama K and Kunieda T. CNP/NPR2 signaling maintains oocyte meiotic arrest in early antral follicles and is suppressed by EGFR-mediated signaling in preovulatory follicles. Molecular Reproduction and Development 2012; 79: 795-802
- Zeng HT, Richani D, Sutton-McDowall ML, Ren Z, Smitz J, Stokes Y, Gilchrist RB and Thompson JG. Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocyte. Biology of Reproduction 2014; 91: 1-11
- Bernal-Ulloa SM, Heinzmann J, Herrmann D, Hadeler KG, Aldag P, Winkler S, Pache D, Baulain U, Lucas-Hahn A and Niemann H. Cyclic AMP affects oocyte maturation and embryo development in prepubertal and adult cattle. Plos ONE 2016; 11: e0150264
- Zhang J, Wei Q, Cai J, Zhao X and Ma B. Effect of C-type natriuretic peptide on maturation and developmental competence of goat oocytes matured in vitro. PLoS ONE 2015; 10: e0132318
- Appeltant R, Beek J, Vandenberghe L, Maes D and Soom AV. Increasing the cAMP concentration during in vitro maturation of pig oocytes improves cumulus maturation and subsequent fertilization in vitro. Theriogenology 2015; 83: 344-352
- Kim, E, Geon A. Kim,G, Taweechaipaisankul, A, Ridlo, MR, Lee, SH, Kihae Ra,K, Ahn, C and, Chun, B., Phytanic acid-derived peroxisomal lipid metabolism in porcine oocytes. Theriogenology 2020; 157: 276-285
- Wynn P, Picton HM, Krapez JA, Rutherford AJ, Balen AH and Gosden RG. Pretreatment with follicle stimulating hormone promotes the numbers of human oocytes reaching metaphase II by in-vitro maturation. Human Reproduction 1998; 13: 3132-3138
- Mikkelsen AL, Smith SD, Lindenberg S. In-vitro maturation of human oocytes from regularly menstruating women may be successful without follicle stimulating hormone priming. Human Reproduction 1999; 14: 1847-1851
- Creux H, Monnier P, Son W, Tulandi T and Buckett W. Immature oocyte retrieval and in vitro oocyte maturation at different phases of the menstrual cycle in women with cancer who require urgent gonadotoxic treatment. Fertility Sterility 2017; 107: 198-204
- Zhao JZ, Zhou W, Zhang W, Ge HS, Huang XF and Lin JJ. In vitro maturation and fertilization of oocytes from unstimulated ovaries in infertile women with polycystic ovary syndrome. Fertility and Sterility 2009; 91: 2568-2571
- Ge HS, Huang XF, Zhang W, Zhao JZ, Lin JJ and Zhou W. Exposure to human chorionic gonadotrophin during in vitro maturation does not improve the maturation rate and developmental potential of immature oocytes from patients with polycystic ovary syndrome Fertility and Sterility 2008; 89: 98-103
- Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001; 122: 829-838
- Fortune JE and Eppig JJ. Effects of gonadotropins on steroid secretion by infantile and juvenile mouse ovaries in vitro. Endocrinology 1979; 10:5 760-768
- Cortvrindt R, Smitz J and VanSteirteghem A. Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Human Reproduction 1997; 12: 759-768
- Brower PT and Schultz RM. Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Developmental Biology 1982; 90: 144-153
- Schultz RM, Montgomery RR and Belanoff JR. Regulation of mouse oocyte eiotic maturation: implication of a decrease in oocyte cAMP and protein dephophoryltion in commitment to resume meiosis. Developmental Biology 1983; 97: 264-273
- Salustri A, Ulisse S, Yanagishita M, and Hascall VC. Hyaluronic acid synthesis by mural granulosa cells and cumulus cells in vitro is selectively stimulated by a factor produced by oocytes and by transforming growth factor-b. The Journal of Biological Chemistry 1990; 265: 19517-19523
- Gilchrist RB, Lane M and Thompson JG. Oocyte secreted factors: regulators of cumulus cell function and oocyte quality. Human Reproduction 2008; 14: 159-177
- Hashimoto N and Kishimoto T. Regulation of meiotic metaphase by a cytoplasmic maturation-promoting factor during mouse oocyte maturation. Developmental Biology 1988; 126: 242-252
- Fulka JJ, First NL and Moor RM. Nuclear and cytoplasmic determinants involved in the regulation of mammalian oocyte maturation. Molecular Human Reproduction 1998; 4: 41-49
- Thibault C, Szollosi D and Gerard M. Mammalian oocyte maturation. Reproduction Nutrition Development 1987; 27: 865-896
- Eppig JJ, Schultz RM, O’Brien M and Chesnel F. Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Developmental Biology 1994; 164: 1-9
- Motlik J and Fulka J. Breakdown of the germinal vesicle in pig oocytes in vivo and in vitro. Journal of Experimental Zoology 1976; 198: 155-162
- Rodman TC and Bachvarova R. RNA synthesis in preovulatory mouse oocytes. Journal of Cell Biology 1976; 70: 251
- Erickson BH. Development and senescence of the postnatal bovine ovary. Journal of Animal Science 1966; 25: 800-805
- Kruip TAM, Cran DG, Van Beneden TH, Dieleman SJ. Structural changes in bovine oocytes during final maturation in vivo. Gamete Research 1983; 8 :29-47
- Hyttel P, Callensen H, Greve T. Ultrastructure features of pre-ovulatory oocyte maturation in superovulated cattle. Journal of Reproduction and Fertility 1986; 76: 645-656
- Sirard MA and First NL. In vitro inhibition of oocyte nuclear maturation in the bovine. Biology of Reproduction 1988: 39; 229-234
- Combelles CM, Cekleniak NA, Racowsky C and Albertini DF. Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Human Reproduction 2002; 17: 1006-1016
- Wang JZ, Sui HS, Miao DQ, Liu N, Zhou P, Ge L and Tan JH. Effects of heat stress during in vitro maturation on cytoplasmic versus nuclear components of mouse oocytes. Reproduction 2009; 137: 181-189
- Brevini-Gandolfi T and Gandolfi F. The maternal legacy to the embryo: Cytoplasmic components and their effects on early development . Theriogenology 2001; 55: 1255-1276
- Sirard MA, Richard F, Blondin P and Robert C. Contribution of the oocyte to embryo quality. Theriogenology 2006; 65: 126-136
- Fujiwara T, Nakada K, Shirakawa H and Miyazaki S. Development of inositol trisphosphate-induced calcium release mechanism during maturation of hamster oocytes. Developmental Biology 1993; 156: 69-79
- Liu J, Lu Q, Qian Y, Mao Y and Ding W. Pregnancies and births achieved from in vitro matured oocytes retrieved from poor responders undergoing stimulating in vitro fertilization cycles. Fertility and Sterility 2003; 80: 447-449
- Bai ZD, Liu K and Wang XY. Developmental potential of aged oocyte rescued by nuclear transfer following parthenogenetic activation and in vitro fertilization. Molecular Reproduction and Development 2006; 73: 1448-1453
- Eppig JJ. Regulation of mammalian oocyte maturation. In The Ovary 1993pp 185-208 Eds EY Adashi and PCK Leung. Raven Press, New York
- Kanatsu-Shinohara M, Schultz RM and Kopf GS. Acquisition of meiotic competence in mouse oocytes: absolute amounts of p34cdc2, cyclin B1, cdc25C, and wee1 in meiotically incompetent and competent oocytes. Biology of Reproduction 2000; 63: 1610-1616
- Tsafriri A and Dekel N. Molecular mechanisms in ovulation. In Molecular Biology Female Reproductive System 1994; pp 207-258 Eds JK Findlay. Academic Press, San Diego
- Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J, Movsesian MA,Wang H, KE H, Nikolaev VO and Jaffe LA. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 2009; 136: 1869-1878
- Peng XR, Hsueh AJ, LaPolt PS, Bjersing L and Ny T. Localization of luteinizing hormone receptor messenger ribonucleic acid ex- pression in ovarian cell types during follicle development and ovulation. Endocrinology 1991; 129: 3200-3207
- Eppig JJ, Wigglesworth K, Pendola F and Hirao Y. Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biology of Reproduction 1997; 56: 976-984
- Lonergan P, Monaghan P, Rizos D, Boland MP and Gordon I. Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Molecular Reproduction and Development 1994; 37: 48-53
- Xiao S, Duncan FE, Bai L, Nguyen CT, Shea LD and Woodruff TK. Size-specific follicle selection improves mouse oocyte reproductive outcomes. Reproduction 2015; 150: 183-192
- Gautier J, Norbury C, Lohka M, Nurse P and Maller J. Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene cdc2+. Cell 1988; 54: 433-439
- Labbé JC, Capony JP, Caput D, Cavadore JC, Derancourt J, Kaghad M, Lelias JM, Picard A and Dorée M. MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. The EMBO Journal 1989; 8: 3053-3058
- Hirao Y, Tsuji Y, Miyano T, Okano A, Miyake M, Kato S and Moor RM. Association between p34cdc1 levels and meiotic arrest in pig oocytes during early growth. Zygote 1995; 3: 325-332
- Christmann L, Jung T and Moor RM. MPF components and meiotic competence in growth pig oocytes.. Molecular Reproduction and Development 1994; 38: 85-90
- Heikinheimo O and Gibbons WE. The molecular mechanisms of oocyte maturation and early embryonic development are unveiling new insights into reproductive medicine. Molecular Human Reproduction 1998;4: 745-756
- Vanderhyden BC and Tonary AM (1995) Differential regulation of progesterone and estradiol production by mouse cumulus and mural granulosa cells by a factor(s) secreted by the oocyte Biology of Reproduction 53 1243-1250
- Chen ZQ, Ming TX and Nielsen HI. Maturation arrest of human oocytes at germinal vesicle stage. Journal of Human Reproductive Sciences 2010; 3: 153-157
- Tsutsumi M, Fujiwara R, Nishizawa H, Ito M, Kogo H, Inagaki H, Ohye T, Kato T, Fujii T and Kurahashi H. Age-related decrease of meiotic cohesins in human oocytes. PLoS ONE 2014; 9: e96710
- Horner K, Livera G, Hinckley M, Trinh K, Storm D and Conti M. Rodent oocytes express in active adenylyl cyclase required for meiotic arrest. Developmental Biology 2003; 258: 385-396
- Hinckley M, Vaccari S, Horner K, Chen R and Conti M. The G-protein- coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes. Developmental Biology 2005; 287: 249-261
- Racowsky C. Effect of forskolin on maintenance of meiotic arrest and stimulation of cumulus expansion, progesterone and cyclic AMP production by pig oocyte-cumulus complexes. Journal of Reproduction and Fertility 1985; 74: 9-21
- Vaccari S, Horner K, Mehlmann LM and Conti M. Generation of mouse oocytes defective in cAMP synthesis and degradation: endogenous cyclic AMP is essential for meiotic arrest. Developmental Biology 2008; 316: 124-134
- Vaccari S, Weeks JL 2nd, Hsieh M, Menniti FS and Conti M. Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biology of Reproduction 2009; 81: 595-604
- Norris RP, Freudzon M, Mehlmann LM, Cowan AE, Simon AM, Paul PD and Jaffe LA. Luteinizing hormone causes MAP kinase-dependent phosphorylation and closure of connexin 43 gap junctions in mouse ovarian follicles: one of two paths to meiotic resumption. Development 2008; 135: 3229-3238
- Conti M and Franciosi F. Acquisition of oocyte competence to develop as an embryo: integrated nuclear and cytoplasmic events. Human Reproduction Update 2018; 24: 245-266
- Takahashi T, Igarashi H, Kawagoe J, Amita M, Hara S and Kurachi H. Poor embryo development in mouse oocytes aged in vitro is associated with impaired calcium homeostasis. Biology of Reproduction 2009; 80: 493-502
- Loane M, Morris JK, Addor M, Arriola L, Budd J, Doray B, Garne E, Gatt M, Haeusler M, Khoshnood B, Melve K, Latos-Bielenska A, McDonnell B, Mullaney C, O’Mahony M, Wahrendorf AQ, Rankin J, Rissmann A, Rounding C, Salvador J, Tucker D, Wellesley D, Yevtushok L and Dolk H. Twenty-year trends in the prevalence of down syndrome and other trisomies in Europe: impact of maternal age and preantal screening. European Journal of Human Genetics 2013; 21: 27-33
- Yoon PW, Freeman SB, Sherman SL, Taft LF, Gu F, Pettay D, Flanders WD, Khoury M and Hassold TJ, Advanced maternal age and the risk of Down syndrome characterized by the meiotic stage of chromosomal error: a population-based study The American Journal of Human Genetics 1996; 58:628-633
- Tiwari BS, Belenghi B and Levine A. Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death1 American Society of Plant Biologists 2002;128;1271-1281
- Tripathi A, Khatun S, Pandey AN, Mishra SK, Chaube R, Shrivastav TG and Chaube SK. Intracellular levels of hydrogen peroxide and nitric oxide in oocytes at various stages of meiotic cell cycle and apoptosis. Free Radical Research 2009; 43: 287-294
- Agung B, Otoi T, Wongsrikeao P, Yaniguchi M, Shimizu R, Watari H and Nagai. T. Effect of maturation culture period of oocytes on the sex ratio of in vitro fertilized bovine embryos. Journal of Reproduction and Development 2006; 52: 123-127
- Kikuchi K, Naito K, Noguchi J, Shimada A, Kaneko H, Yamashita M, Aoki F, Tojo H and Yoyoda Y. Maturation/M-phase promoting factor: a regulator of aging in porcine oocytes. Biology of Reproduction 2000; 63: 715-722
- Webb M, Howlett SK, Maro B. Parthenogenesis and cytoskeletal organization in ageing mouse eggs. Journal of Embryology and Experimental Morphology 1986; 9:5 131-145
- Orisaka M, Orisaka S, Jiang JY, Craig J, Wang Y, Kotsuji F and Tsang BK. Growth differentiation factor 9 is antiapoptotic during follicular development from preantral to early antral stage. Molecular Endocrinology 2006; 20: 2456-2468
- Thompson WE, Asselin E, Branch A, Stiles JK, Sutovsky P, Lai L, Im GS, Prather RS, Isom SC, Rucker E and Tsang BK. Regulation of prohibitin expression during follicular development and atresia in the mammalian ovary. Biology of Reproduction 2004; 71: 282-290
Last update: 2021-04-16 20:09:42
Last update: 2021-04-16 20:09:43
The Authors submitting a manuscript do so on the understanding that if accepted for publication, copyright of the article shall be assigned to Journal of Biomedicine and Translational Research Diponegoro University as publisher of the journal.
Copyright encompasses exclusive rights to reproduce and deliver the article in all form and media, including reprints, photographs, microfilms and any other similar reproductions, as well as translations. The reproduction of any part of this journal, its storage in databases and its transmission by any form or media, such as electronic, electrostatic and mechanical copies, photocopies, recordings, magnetic media, etc., will be allowed only with a written permission from Journal of Biomedicine and Translational Research Diponegoro University.
Journal of Biomedicine and Translational Research Diponegoro University, the Editors and the Advisory International Editorial Board make every effort to ensure that no wrong or misleading data, opinions or statements be published in the journal. In any way, the contents of the articles and advertisements published in the Journal of Biomedicine and Translational Research Diponegoro University (JBTR) are sole and exclusive responsibility of their respective authors and advertisers.
The Copyright Transfer Form can be downloaded here: [Copyright Transfer Form JBTR]
The copyright form should be signed originally and send to the Editorial Office in the form of original mail, scanned document or fax :
Journal of Biomedicine and Translational Research Faculty of Medicine, Diponegoro University
Jl. Prof. Soedarto, Kampus UNDIP Tembalang, Semarang, Central Java, Indonesia 50275, Telp.: +62-24-8412311, Fax.: +62-24-8454714
Email: jbtr@fk.undip.ac.id and jbtr@live.undip.ac.id