The Effect of Preincubation Time and Myo-inositol Supplementation on the Quality of Mouse MII Oocytes

Mohammadi, Fatemeh; Ashrafi, Mahnaz; Zandieh, Zahra; Najafi, Mohammad; Niknafs, Behrooz; Amjadi, Fatemeh Sadat; Haghighi, Maryam

doi:10.18502/jri.v21i4.4330

The Effect of Preincubation Time and Myo-inositol Supplementation on the Quality of Mouse MII Oocytes

Authors

Fatemeh Mohammadi ¹

Mahnaz Ashrafi ²

Zahra Zandieh ²

Mohammad Najafi ³

Behrooz Niknafs ⁴

Fatemeh Sadat Amjadi ⁵

Maryam Haghighi ¹

¹ Student Research Committee, School of Medicine, Iran University of Medical Sciences (IUMS), Tehran, Iran; Anatomy Department, School of Medicine, Iran University of Medical Sciences (IUMS), Tehran, Iran

² Shahid Akbar Abadi Clinical Research Development Unit (ShACRDU), Iran University of Medical Sciences (IUMS), Tehran, Iran; Cellular and Molecular Research Center, Iran University of Medical Sciences (IUMS), Tehran, Iran

³ Biochemistry Department, School of Medicine, Iran University of Medical Sciences (IUMS), Tehran, Iran

⁴ Anatomy Department, School of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran

⁵ Anatomy Department, School of Medicine, Iran University of Medical Sciences (IUMS), Tehran, Iran; Shahid Akbar Abadi Clinical Research Development Unit (ShACRDU), Iran University of Medical Sciences (IUMS), Tehran, Iran

10.18502/jri.v21i4.4330

Abstract

Background: It is demonstrated that optimal preincubation time improves oocyte quality, fertilization potential and developmental rate. This study aimed to evaluate the effect of preincubation time in the simple and myo-inositol supplemented medium on the oocyte quality regarding oxidative stress and mitochondrial alteration. Methods: Cumulus oocyte complexes (COCs) retrieved from superovulated NMRI mice were divided in groups of 0, 4 and 8 hr preincubation time in the simple and 20 mmol/L myo-inositol supplemented media. Intracellular reactive oxygen species (H2O2), glutathione (GSH), mitochondrial membrane potential (MMP), ATP content, and mitochondrial amount were measured and analyzed in experimental groups. One-way ANOVA and Kruskal-Wallis were respectively used for parametric and nonparametric variables. Statistical significance was defined as p<0.05. Results: In comparison to control group, variables including ROS, GSH, mitochondrial amount, fertilization and developmental rates were significantly changed after 4 hr of preincubation in the simple medium, while MMP decreased following 8 hr of preincubation in the simple medium (p˂0.001). Preincubation of oocytes up to 8 hr in the simple medium could not decrease ATP content. For both 4 and 8 hr preincubation times, myo-inositole could decrease H2O2 and increase GSH and MMP levels and consequently could improve fertilization rate compared to oocytes preincubated in the simple culture. Conclusion: It seems that 4 hr or more preincubation time can decrease the oocyte quality and lead to reduced oocyte fertilization and developmental potential. Howevere, myo-inositol may prevent oocyte quality reduction and improve fertilization potential in comparision to the equivalent simple groups.

Keywords

Developmental Rate

Fertilization potential

Mitochondrial alteration

Myo

inositol supplement

Oocyte preincubation time

Oocyte quality

oxidative stress

Irit G, Dekel N. Preparation and evaluation of oocytes for intracytoplasmic sperm injection. In: Gardener DK, Weissman A, Howles C, Shohma Z, editors. Textbook of assisted reproductive techniques: laboratory and clinical perspectives. New York: Taylor and Francis Group; 2016. p. 108-16.

Patrat C, Kaffel A, Delaroche L, Guibert J, Jouannet P, Epelboin S, et al. Optimal timing for oocyte denudation and intracytoplasmic sperm injection. Obstet Gynecol Int. 2012;2012:403531.

Javier GF, Pedro V, Milton Z, Jorge C. High pregnancy and implantation rates can be obtained with preincubation of oocytes before insemination in IVF and ICSI procedures. Health. 2012;4(9);660-6.

Kakade S, Kamat A, Datar S. Optimal timing of oocyte preincubation for intra cytoplasmic sperm injection (ICSI) in IVF treatment. Int J Eng Sci. 2016;5(7):1-6.

Bárcena P, Rodríguez M, Obradors A, Vernaeve V, Vassena R. Should we worry about the clock? relationship between time to ICSI and reproductive outcomes in cycles with fresh and vitrified oocytes. Hum Reprod. 2016;31(6):1182-91.

Ishikawa Y, Inaba M, Matsumoto H, Mizano S, Mori R, Ida M, et al. Influence of the duration between removal of cumulus cells and oocyte retrival on fertilization and embryonic development. Hum Reprod; 2016;31:1-2.

Carvalho M, Mota S, Leal F, Pereira I, Rodrigues C, Aguiar A, et al. The influence of denudation and injection on ICSI outcome-does timing matter? Hum Reprod. 2018;33:102.

Papayannis M, Demarco A, Terrado Gil G, Bisioli C, Serna J, Gomez Pena M, et al. Time intervals from the hCG trigger: analysis of different checkpoints and their impact on embryo development, implantation and pregnancy. Hum Reprod. 2018;33:197.

Gardner DK, Weissman A, Howles CM, Shoham Z. Textbook of assisted reproductive techniques. 5th ed. New York: Taylor and Francis Group; 2016. 423 p.

Karagianni M, Taki E, Moysidou M, Christoforidis N, Chatziparasidou A. From triggering to ICSI: optimal timing between triggering, OPU, denudation and ICSI. Hum Reprod. 2019;34:207.

Hebisha S, Sharaf H, Aziz A. Embryo cleavage rate is enhanced by extending oocyte-cumulus cell contact: a randomized sibling oocyte study. Hum Reprod. 2019;34:236.

Zenzes MT, Belkien L, Bordt J, Kan I, Schneider HP, Nieschlag E. Cytologic investigation of human in vitro fertilization failures. Fertil Steril. 1985;43(6):883-91.

Falcone P, Gambera L, Pisoni M, Lofiego V, De Leo V, Mencaglia L, et al. Correlation between oocyte preincubation time and pregnancy rate after intracytoplasmic sperm injection. Gynecol Endocrinol. 2008;24(6):295-9.

Miao YL, Kikuchi K, Sun QY, Schatten H. Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update. 2009;15(5):573-85.

Takahashi T, Igarashi H, Kawagoe J, Amita M, Hara S, Kurachi H. Poor embryo development in mouse oocytes aged in vitro is associated with impaired calcium homeostasis. Biol Reprod. 2009;80(3):493-502.

Chebotareva T, Taylor J, Mullins JJ, Wilmut I. Rat eggs cannot wait: Spontaneous exit from meiotic metaphase‐II arrest. Mol Reprod Dev. 2011;78(10‐11):795-807.

Prasad S, Tiwari M, Koch B, Chaube SK. Morphological, cellular and molecular changes during postovulatory egg aging in mammals. J Biomed Sci. 2015;22(1):36.

Benkhalifa M, Ferreira YJ, Chahine H, Louanjli N, Miron P, Merviel P, et al. Mitochondria: participation to infertility as source of energy and cause of senescence. Int J Biochem Cell Biol. 2014;55:60-4.

Dumollard R, Carroll J, Duchen MR, Campbell K, Swann K. Mitochondrial function and redox state in mammalian embryos. Semin Cell Dev Biol. 2009;20(3):346-53.

Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction. 2004;128(3):269-80.

Lord T, Aitken RJ. Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction. 2013;146(6):R217-27.

Wilding M, Dale B, Marino M, di Matteo L, Alviggi C, Pisaturo ML, et al. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum Reprod. 2001;16(5):909-17.

Igarashi H, Takahashi T, Abe H, Nakano H, Nakajima O, Nagase S. Poor embryo development in post-ovulatory in vivo-aged mouse oocytes is associated with mitochondrial dysfunction, but mitochondrial transfer from somatic cells is not sufficient for rejuvenation. Hum Reprod. 2016;31(10):2331-8.

Igarashi H, Takahashi T, Takahashi E, Tezuka N, Nakahara K, Takahashi K, et al. Aged mouse oocytes fail to readjust intracellular adenosine triphosphates at fertilization. Biol Reprod. 2005;72(5):1256-61.

Gohil VM, Greenberg ML. Mitochondrial membrane biogenesis: phospholipids and proteins go hand in hand. J Cell Biol. 2009;184(4):469-72.

Marat AL, Haucke V. Phosphatidylinositol 3‐phosphates-at the interface between cell signalling and membrane traffic. EMBO J. 2016;35(6):561-79.

Foskett JK. Inositol trisphosphate receptor Ca2+ release channels in neurological diseases. Pflugers Arch. 2010;460(2):481-94.

Oudit GY, Penninger JM. Cardiac regulation by phosphoinositide 3-kinases and PTEN. Cardiovasc Res. 2009;82(2):250-60.

Santamaria A, Di Benedetto A, Petrella E, Pintaudi B, Corrado F, D’Anna R, et al. Myo-inositol may prevent gestational diabetes onset in overweight women: a randomized, controlled trial. J Matern Fetal Neonatal Med. 2016;29(19):3234-7.

Santamaria A, Giordano D, Corrado F, Pintaudi B, Interdonato M, Vieste GD, et al. One-year effects of myo-inositol supplementation in postmenopausal women with metabolic syndrome. Climacteric. 2012;15(5):490-5.

Iuorno M, Maria J, Jakubowicz M, Daniela J, Baillargeon M, Jean-Patrice, et al. Effects of D-chiro-inositol in lean women with the polycystic ovary syndrome. Endocr Pract. 2002;8(6):417-23.

Jiang WD, Kuang SY, Liu Y, Jiang J, Hu K, Li SH, et al. Effects of myo‐inositol on proliferation, differentiation, oxidative status and antioxidant capacity of carp enterocytes in primary culture. Aquac Nutr. 2013;19(1):45-53.

Mohammadi F, Varanloo N, Nasrabadi MH, Vatannejad A, Amjadi F, Masroor MJ, et al. Supplementation of sperm freezing medium with myoinositol improve human sperm parameters and protects it against DNA fragmentation and apoptosis. Cell Tissue Bank. 2019;20(1):77-86.

Lewin LM, Szeinberg A, Lepkifker E. Gas chromatographic measurement of myo-inositol in human blood, cerebrospinal fluid and seminal fluid. Clin Chim Acta. 1973;45(4):361-8.

Fujiwara T, Nakada K, Shirakawa H, Miyazaki S. Development of inositol trisphosphate-induced calcium release mechanism during maturation of hamster oocytes. Dev Biol. 1993;156(1):69-79.

Chiu TT, Rogers MS, Law EL, Briton-Jones CM, Cheung L, Haines CJ. Follicular fluid and serum concentrations of myo-inositol in patients undergoing IVF: relationship with oocyte quality. Hum Reprod. 2002;17(6):1591-6.

Bevilacqua A, Carlomagno G, Gerli S, Montanino Oliva M, Devroey P, Lanzone A, et al. Results from the international consensus conference on myo-inositol and D-chiro-inositol in obstetrics and gynecology--assisted reproduction technology. Gynecol Endocrinol. 2015;31(6):441-6.

Chiu TTY, Rogers MS, Briton‐Jones C, Haines C. Effects of myo‐inositol on the in‐vitro maturation and subsequent development of mouse oocytes. Hum Reprod. 2003;18(2):408-16.

Huang Y, Yu Y, Gao J, Li R, Zhang C, Zhao H, et al. Impaired oocyte quality induced by dehydroepiandrosterone is partially rescued by metformin treatment. PloS one. 2015;10(3):e0122370.

Yuan B, Liang S, Kwon JW, Jin YX, Park SH, Wang HY, et al. The role of glucose metabolism on porcine oocyte cytoplasmic maturation and its possible mechanisms. PloS one. 2016;11(12):e0168329.

Yao X, Jiang H, Liang S, Shen X, Gao Q, Xu YN, et al. Laminarin enhances the quality of aged pig oocytes by reducing oxidative stress. J Reprod Dev. 2018;64(6):489-94.

Nazmara Z, Salehnia M, HosseinKhani S. Mitochondrial distribution and ATP content of vitrified, in vitro matured mouse oocytes. Avicenna J Med Biotechnol. 2014;6(4):210-7.

Gualtieri R, Iaccarino M, Mollo V, Prisco M, Iaccarino S, Talevi R. Slow cooling of human oocytes: ultrastructural injuries and apoptotic status. Fertil Steril. 2009;91(4):1023-34.

Wesson DE, Elliott SJ. The H2O2-generating enzyme, xanthine oxidase, decreases luminal Ca2+ content of the IP3-sensitive Ca2+ store in vascular endothelial cells. Microcirculation. 1995;2(2):195-203.

Boerjan ML, de Boer P. First cell cycle of zygotes of the mouse derived from oocytes aged postovulation in vivo and fertilized in vivo. Mol Reprod Dev. 1990;25(2):155-63.

Miao Y, Zhou C, Cui Z, Zhang M, ShiYang X, Lu Y, et al. Postovulatory aging causes the deterioration of porcine oocytes via induction of oxidative stress. FASEB J. 2017;32(3):1328-37.

Wu LL, Russell DL, Wong SL, Chen M, Tsai TS, St John JC, et al. Mitochondrial dysfunction in oocytes of obese mothers: transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors. Development. 2015;142(4):681-91.

Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, Amaral A. Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update. 2009;15(5):553-72.

Babayev E, Wang T, Szigeti-Buck K, Lowther K, Taylor HS, Horvath T, et al. Reproductive aging is associated with changes in oocyte mitochondrial dynamics, function, and mtDNA quantity. Maturitas. 2016;93:121-30.