Hostname: page-component-76d6cb85b7-6jg5l Total loading time: 0 Render date: 2026-07-15T04:23:40.646Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of melatonin on production of reactive oxygen species and developmental competence of bovine oocytes exposed to heat shock and oxidative stress during in vitro maturation

Published online by Cambridge University Press:  07 June 2019

Fernanda de Castro Cavallari ,
Cláudia Lima Verde Leal ,
Roth Zvi  and
Peter J. Hansen Open the ORCID record for Peter J. Hansen [Opens in a new window]
Fernanda de Castro Cavallari
Affiliation:
Department of Veterinary Medicine, Faculty of Animal Science and Food Engineering, University of São Paulo, Pirassununga 13635-900, Brazil Department of Animal Sciences, D. H. Barron Reproductive and Perinatal Biology Research Program and Genetics Institute, University of Florida, Gainesville, Florida 32611-0910, USA
Cláudia Lima Verde Leal
Affiliation:
Department of Veterinary Medicine, Faculty of Animal Science and Food Engineering, University of São Paulo, Pirassununga 13635-900, Brazil
Roth Zvi
Affiliation:
Department of Animal Sciences, Robert H. Smith Faculty of Agricultural, Food & Environment, Hebrew University of Jerusalem, Rehovot 76100, Israel
Peter J. Hansen*
Affiliation:
Department of Animal Sciences, D. H. Barron Reproductive and Perinatal Biology Research Program and Genetics Institute, University of Florida, Gainesville, Florida 32611-0910, USA
*
*Address for correspondence: Peter J. Hansen. Department of Animal Sciences, D. H. Barron Reproductive and Perinatal Biology Research Program and Genetics Institute, University of Florida, Gainesville, Florida 32611-0910, USA. E-mail Hansen@animal.ufl.edu
Get access Rights & Permissions [Opens in a new window]

Summary

Heat shock may disrupt oocyte function by increasing the generation of reactive oxygen species (ROS). We evaluated the capacity of the antioxidant melatonin to protect oocytes using two models of oxidative stress – heat shock and the pro-oxidant menadione. Bovine cumulus–oocyte complexes (COC) were exposed in the presence or absence of 1 µM melatonin to the following treatments during maturation: 38.5°C, 41°C and 38.5°C+5 µM menadione. In the first experiment, COC were matured for 3 h with 5 µM CellROX® and analyzed by epifluorescence microscopy to quantify production of ROS. The intensity of ROS was greater for oocytes exposed to heat shock and menadione than for control oocytes. Melatonin reduced ROS intensity for heat-shocked oocytes and oocytes exposed to menadione, but not for control oocytes. In the second experiment, COC were matured for 22 h. After maturation, oocytes were fertilized and the embryos cultured for 7.5 days. The proportion of oocytes that cleaved after fertilization was lower for oocytes exposed to heat shock and menadione than for control oocytes. Melatonin increased cleavage for heat-shocked oocytes and oocytes exposed to menadione, but not for control oocytes. Melatonin tended to increase the developmental competence of embryos from heat-shocked oocytes but not for embryos from oocytes exposed to menadione or from control oocytes. In conclusion, melatonin reduced production of ROS of maturing oocytes and protected oocytes from deleterious effects of both stresses on competence of the oocyte to cleave after coincubation with sperm. These results suggest that excessive production of ROS compromises oocyte function.

Keywords

EmbryoHeat shockMelatoninMenadioneReactive oxygen species.

Information

Type
Research Article
Information
Zygote , Volume 27 , Issue 3 , June 2019 , pp. 180 - 186
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Ahmed, JA, Dutta, D and Nashiruddullah, N (2016) Comparative efficacy of antioxidant retinol, melatonin, and zinc during in vitro maturation of bovine oocytes under induced heat stress. Turkish J Vet Anim Sci 40, 365–373.Google Scholar
Cebrian-Serrano, A, Salvador, I, Raga, E, Dinnyes, A and Silvestre, MA (2013) Beneficial effect of melatonin on blastocyst in vitro production from heat-stressed bovine oocytes. Reprod Domest Anim 48, 738–746.Google Scholar
Cheuquemán, C, Loren, P, Arias, M, Risopatrón, J, Felmer, R, Álvarez, J, Mogas, T and Sánchez, R (2015) Effects of short-term exposure of mature oocytes to sodium nitroprusside on in vitro embryo production and gene expression in bovine. Theriogenology 84, 1431–1437.Google Scholar
Comporti, M (1989) Three models of free radical-induced cell injury. Chem Biol Interact 72, 1–56.Google Scholar
de Castro e Paula, LA and Hansen, PJ (2007) Interactions between oxygen tension and glucose concentration that modulate actions of heat shock on bovine oocytes during in vitro maturation. Theriogenology 68, 763–770.Google Scholar
Dikmen, S and Hansen, PJ (2009) Is the temperature-humidity index the best indicator of heat stress in lactating dairy cows in a subtropical environment? J Dairy Sci 92, 109–116.Google Scholar
Edwards, JL and Hansen, PJ (1997) Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol Reprod Dev 46, 138–145.Google Scholar
El-Raey, M, Geshi, M, Somfai, T, Kaneda, M, Hirako, M, Abdel-Ghaffar, AE, Sosa, GA, El-Roos, ME and Nagai, T (2011) Evidence of melatonin synthesis in the cumulus oocyte complexes and its role in enhancing oocyte maturation in vitro in cattle. Mol Reprod Dev 78, 250–262.Google Scholar
Farahavar, A, Shahane, AZ, Kohram, H and Vahedi, V (2010) Effect of melatonin on in vitro maturation of bovine oocytes. African J Biotechnol 9, 2579–2583.Google Scholar
Garcia-Ispierto, I, Abdelfatah, A and López-Gatius, F (2013) Melatonin treatment at dry-off improves reproductive performance postpartum in high-producing dairy cows under heat stress conditions. Reprod Domest Anim 48, 577–583.Google Scholar
Hansen, PJ and Fear, JM (2011) Cheating death at the dawn of life: developmental control of apoptotic repression in the preimplantation embryo. Biochem Biophys Res Commun. 413, 155–158.Google Scholar
Hendricks, KE and Hansen, PJ (2010) Consequences for the bovine embryo of being derived from a spermatozoon subjected to oxidative stress. Aust Vet J 88, 307–310.Google Scholar
Ispada, J, Rodrigues, TA, Risolia, PHB, Lima, RS, Gonçalves, DR, Rettori, D, Nichi, M, Feitosa, WB and Paula-Lopes, FF (2018) Astaxanthin counteracts the effects of heat shock on the maturation of bovine oocytes. Reprod Fertil Dev [Epub ahead of print]Google Scholar
Kobayashi, Y, Itoh, MT, Kondo, H, Okuma, Y, Sato, S, Kanishi, Y, Hamada, N, Kiguchi, K and Ishizuka, B (2003) Melatonin binding sites in estrogen receptor-positive cells derived from human endometrial cancer. J Pineal Res 35, 71–74.Google Scholar
Lawrence, JL, Payton, RR, Godkin, JD, Saxton, AM, Schrick, FN and Edwards, JL (2004) Retinol improves development of bovine oocytes compromised by heat stress during maturation. J Dairy Sci 87, 2449–2454.Google Scholar
Li, Y, Zhang, Z, He, C, Zhu, K, Xu, Z, Ma, T, Tao, J. and Liu, G (2015) Melatonin protects porcine oocyte in vitro maturation from heat stress. J Pineal Res 59, 365–375.Google Scholar
Li, Y, Wang, J, Zhang, Z, Yi, J, He, C, Wang, F, Tian, X, Yang, M, Song, Y, He, P and Liu, G (2016) Resveratrol compares with melatonin in improving in vitro porcine oocyte maturation under heat stress. J Anim Sci Biotechnol 7, 33.Google Scholar
Liu, XY, Xu, YT, Shi, Q, Lu, QS, Ma, SR, Xu, XY and Guo, XZ (2013) Alterations of reproductive hormones and receptors of male rats at the winter and summer solstices and the effects of pinealectomy. Neuroendocrinol Lett 34, 143–153.Google Scholar
López-Gatius, F and Hunter, RHF (2019a) Pre-ovulatory follicular cooling correlates positively with the potential for pregnancy in dairy cows: Implications for human IVF. J Gynecol Obstet Hum Reprod [Epub ahead of print]Google Scholar
López-Gatius, F and Hunter, RHF (2019b) Pre-ovulatory follicular temperature in bi-ovular cows. J Reprod Dev 65, 191–194.Google Scholar
Marques, TC, da Silva Santos, EC, Diesel, TO, Leme, LO, Martins, CF, Dode, M, Alves, BG, Costa, F, de Oliveira, EB and Gambarini, ML (2018) Melatonin reduces apoptotic cells, SOD2 and HSPB1 and improves the in vitro production and quality of bovine blastocysts. Reprod Domest Anim 53, 226–236.Google Scholar
Matsuzuka, T, Sakamoto, N, Ozawa, M, Ushitani, A, Hirabayashi, M and Kanai, Y (2005) Alleviation of maternal hyperthermia-induced early embryonic death by administration of melatonin to mice. J Pineal Res 39, 217–223 Google Scholar
Mayo, JC, Sainz, RM, González-Menéndez, P, Hevia, D and Cernuda-Cernuda, R (2017) Melatonin transport into mitochondria. Cell Mol Life Sci 74, 3927–3940.Google Scholar
Meiyu, Q, Liu, D and Roth, Z (2015) IGF-I slightly improves nuclear maturation and cleavage rate of bovine oocytes exposed to acute heat shock in vitro. Zygote 23, 514–524.Google Scholar
Moss, JI, Pontes, E and Hansen, PJ (2009) Insulin-like growth factor-1 protects preimplantation embryos from anti-developmental actions of menadione. Arch Toxicol 83, 1001–1007.Google Scholar
Nabenishi, H, Ohta, H, Nishimoto, T, Morita, T, Ashizawa, K and Tsuzuki, Y (2012) The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress. Zygote 20, 249–259.Google Scholar
Ortega, MS, Rocha-Frigoni, NAS, Mingoti, GZ, Roth, Z and Hansen, PJ (2016) Modification of embryonic resistance to heat shock in cattle by melatonin and genetic variation in HSPA1L. J Dairy Sci 99, 9152–9164.Google Scholar
Ortega, MS, Wohlgemuth, S, Tribulo, P, Siqueira, LG, Cole, JB and Hansen, PJ (2017) A single nucleotide polymorphism in COQ9 affects mitochondrial and ovarian function and fertility in Holstein cows. Biol Reprod 96, 652–663.Google Scholar
Pang, Y, Zhao, S, Sun, Y, Jiang, X, Hao, H, Du, W and Zhu, H. (2018) Protective effects of melatonin on the in vitro developmental competence of bovine oocytes. Anim Sci J. 89, 648–660.Google Scholar
Payton, RR, Rispoli, LA, Nagle, KA, Gondro, C, Saxton, AM, Voy, BH and Edwards, JL (2018) Mitochondrial-related consequences of heat stress exposure during bovine oocyte maturation persist in early embryo development. J Reprod Dev 64, 243–251.Google Scholar
Poon, AM, Liu, ZM, Pang, CS, Brown, GM and Pang, SF (1994) Evidence for a direct action of melatonin on the immune system. Biol Signals 3, 107–117.Google Scholar
Putney, DJ, Drost, M and Thatcher, WW (1988) Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination. Theriogenology 30, 195–209.Google Scholar
Rivera, RM and Hansen, PJ (2001) Development of cultured bovine embryos after exposure to high temperatures in the physiological range. Reproduction 121, 107–115.Google Scholar
Rivera, RM, Dahlgren, GM, De Castro, E Paula, LA, Kennedy, RT and Hansen, PJ (2004) Actions of thermal stress in two-cell bovine embryos: oxygen metabolism, glutathione and ATP content, and the time-course of development. Reproduction 128, 33–42.Google Scholar
Rodrigues, TA, Ispada, J, Risolia, PH, Rodrigues, MT, Lima, RS, Assumpção, ME, Visintin, JA and Paula-Lopes, FF (2016) Thermoprotective effect of insulin-like growth factor 1 on in vitro matured bovine oocyte exposed to heat shock. Theriogenology 86, 2028–2039.Google Scholar
Rodrigues, TA, Tuna, KM, Alli, AA, Tribulo, P, Hansen, PJ, Koh, J and Paula-Lopes, FF (2019) Follicular fluid exosomes act on the bovine oocyte to improve oocyte competence to support development and survival to heat shock. Reprod Fertil Dev 31, 888–897.Google Scholar
Rodrigues-Cunha, MC, Mesquita, LG, Bressan, F, Collado, MD, Balieiro, JC, Schwarz, KR, de Castro, FC, Watanabe, OY, Watanabe, YF, de Alencar Coelho, L and Leal, CL. (2016) Effects of melatonin during IVM in defined medium on oocyte meiosis, oxidative stress, and subsequent embryo development. Theriogenology 86, 1685–1694.Google Scholar
Roth, Z and Hansen, PJ (2004a) Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol Reprod 71, 1898–1906.Google Scholar
Roth, Z and Hansen, PJ (2004b) Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation. Biol Reprod 71, 2072–2078.Google Scholar
Roth, Z and Hansen, PJ (2005) Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129, 235–244.Google Scholar
Sakatani, M, Alvarez, NV, Takahashi, M and Hansen, PJ (2012) Consequences of physiological heat shock beginning at the zygote stage on embryonic development and expression of stress response genes in cattle. J Dairy Sci 95, 3080–3091.Google Scholar
Shah, M, Stebbins, JL, Dewing, A, Qi, J, Pellecchia, M and Ronai, ZA (2009) Inhibition of Siah2 ubiquitin ligase by vitamin K3 (menadione) attenuates hypoxia and MAPK signaling and blocks melanoma tumorigenesis. Pigment Cell Melanoma Res 22, 799–808.Google Scholar
Shi, JM, Tian, XZ, Zhou, GB, Wang, L, Gao, C, Zhu, SE, Zeng, SM, Tian, JH and Liu, GS (2009) Melatonin exists in porcine follicular fluid and improves in vitro maturation and parthenogenetic development of porcine oocytes. J Pineal Res 47, 318–323.Google Scholar
Soto, P, Natzke, RP and Hansen, PJ (2003) Identification of possible mediators of embryonic mortality caused by mastitis: actions of lipopolysaccharide, prostaglandin F2α, and the nitric oxide generator, sodium nitroprusside dihydrate, on oocyte maturation and embryonic development in cattle. Am J Reprod Immunol 50, 263–272.Google Scholar
Soto-Heras, S, Roura, M, Catalá, MG, Menéndez-Blanco, I, Izquierdo, D, Fouladi-Nashta, AA and Paramio, MT (2018) Beneficial effects of melatonin on in vitro embryo production from juvenile goat oocytes. Reprod Fertil Dev 30, 253–261.Google Scholar
Tamura, H, Takasaki, A, Miwa, I, Taniguchi, K, Maekawa, R, Asada, H, Taketani, T, Matsuoka, A, Yamagata, Y, Shimamura, K, Morioka, H, Ishikawa, H, Reiter, RJ and Sugino, N (2008) Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res 44, 280–287.Google Scholar
Tan, DX, Reiter, RJ, Manchester, LC, Yan, MT, El-Sawi, M, Sainz, RM, Mayo, JC, Kohen, R, Allegra, M and Hardeland, R (2002) Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger. Curr Top Med Chem 2, 181–197.Google Scholar
Tian, X, Wang, F, He, C, Zhang, L, Tan, D, Reiter, RJ, Xu, J, Ji, P and Liu, G (2014) Beneficial effects of melatonin on bovine oocytes maturation: a mechanistic approach. J Pineal Res 57, 239–247.Google Scholar
Tian, X, Wang, F, Zhang, L, He, C, Ji, P, Wang, J, Zhang, Z, Lv, D, Abulizi, W, Wang, X, Lian, Z and Liu, G (2017) Beneficial effects of melatonin on the in vitro maturation of sheep oocytes and its relation to melatonin receptors. Int J Mol Sci 18, E834.Google Scholar
Tong, J, Sheng, S, Sun, Y, Li, H, Li, WP, Zhang, C and Chen, ZJ (2017) Melatonin levels in follicular fluid as markers for IVF outcomes and predicting ovarian reserve. Reproduction 153, 443–451.Google Scholar
Yang, M, Tao, J, Chai, M, Wu, H, Wang, J, Li, G, He, C, Xie, L, Ji, P, Dai, Y, Yang, L and Liu, G (2017) Melatonin improves the quality of inferior bovine oocytes and promoted their subsequent IVF embryo development: mechanisms and results. Molecules 22, 2059.Google Scholar
Yazaki, T, Hiradate, Y, Hoshino, Y, Tanemura, K and Sato, E (2013) l-Carnitine improves hydrogen peroxide-induced impairment of nuclear maturation in porcine oocytes. Anim Sci J 84, 395–402.Google Scholar
Zhao, XM, Min, JT, Du, WH, Hao, HS, Liu, Y, Qin, T, Wang, D and Zhu, HB (2015) Melatonin enhances the in vitro maturation and developmental potential of bovine oocytes denuded of the cumulus oophorus. Zygote 23, 525–536.Google Scholar