Effect of resveratrol on the in vitro maturation of ovine (Ovis aries) oocytes and the subsequent development of handmade cloned embryos

José Luis Martínez-Ibarra, Eugenia Adriana Espinoza-Mendoza, Raymundo Rangel-Santos, Demetrio Alonso Ambriz-García, María Del Carmen Navarro-Maldonado

Abstract


Veterinaria México OA
ISSN: 2448-6760

Cite this as:

  • Martínez-Ibarra JL, Espinoza-Mendoza EA, Rangel-Santos R, Ambriz-García DA, Navarro-Maldonado MDC. Effect of resveratrol on the in vitro maturation of ovine (Ovis aries) oocytes and the subsequent development of handmade cloned embryos. Veterinaria México OA. 2018;5(4).  doi:10.22201/fmvz.24486760e.2018.4.491

The effect of resveratrol on the in vitro maturation (IVM) of ovine (Ovis aries) oocytes and the development of handmade cloned embryos was evaluated. The nuclear maturation and reactive oxygen species (ROS) levels in the oocytes, as well as the early development and morphological cloned embryo quality, were evaluated under different resveratrol concentrations (0, 0.5, 2 and 5 μM). After IVM, no significant difference was observed in the maturation rate of oocytes treated with 0.5 μM (81.3 %) and 2 μM (72 %) resveratrol compared to that of the control group (0 μM) (74.2 %), but the rate significantly decreased at 5 μM (56 %) (p < 0.05). When the oocyte ROS levels were determined, no significant differences among the groups were observed (p > 0.05). For cloned embryo development, the embryos obtained from the oocytes treated with 0.5 μM resveratrol showed higher (p < 0.05) compacted morula rates (10.7 %) compared to the embryos obtained from the oocytes treated with 0, 2 and 5 μM (6.2, 0 and 0 %, respectively). Regarding embryo morphological quality, the embryos from the oocytes treated with 0.5 μM resveratrol showed a lower rate of poor quality morulae (4.7 %) in comparison to those treated with 0, 2 and 5 μM (23.8, 23.3 and 33.3 %, respectively) (p < 0.05). In conclusion, resveratrol showed no significant improvement on the IVM or ROS levels in domestic ovine oocytes. However, treatment with 0.5 μM resveratrol during IVM improved embryo quality and promoted morulae compaction of Ovis aries handmade cloned embryos.

Figure 3. Different developmental stages of the HMC sheep embryos cultured in the WOW system. Cleaved embryos (a-d), 8‒16 blastomere embryos (e-h), morulae (i-l) and compact morulae (m-p) (200X).


Keywords


Resvertarol; Ovis aries; In vitro maturation; Reactive oxigen species; Embryo development; Handmade cloning

Full Text:

PDF

References


Folch J, Cocero MJ, Chesné P, Alabart JL, Domínguez V, Cognié Y, et al. First birth of an animal from an extinct subspecies (Capra pyrenaica pyrenaica) by cloning. Theriogenology. 2009;71:1026‒34. doi: 10.1016/j.theriogenology.2008.11.005.

Bren L. Cloning: revolution or evolution in animal production. FDA Consum. 2003;37:28‒33.

Meissner A, Jaenisch R. Mammalian nuclear transfer. Dev Dyn. 2006;235:2460‒9. doi: 10.1002/dvdy.20915.

Lanza RP, Cibelli JB, Diaz F, Moraes CT, Farin PW, Farin CE, et al. Cloning of an endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning. 2000;2:79‒90. doi: 10.1089/152045500436104.

Loi P, Ptak G, Barboni B, Fulka J, Cappai P, Clinton M. Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nat Biotechnol. 2001;19:962‒4. doi: 10.1038/nbt1001-962.

Shi D, Lu F, Wei Y, Cui K, Yang S, Wei J, et al. Buffalos (Bubalus bubalis) cloned by nuclear transfer of somatic cells. Biol Reprod. 2007;77:285‒91. doi: 10.1095/biolreprod.107.060210.

Kim MK, Jang G, Oh HJ, Yuda F, Kim HJ, Hwang WS, et al. Endangered wolves cloned from adult somatic cells. Cloning Stem Cells. 2007;9:130‒7. doi: 10.1089/clo.2006.0034.

Wani NA, Wernery U, Hassan FA, Wernery R, Skidmore JA. Production of the first cloned camel by somatic cell nuclear transfer. Biol Reprod. 2010;82:373‒9. doi: 10.1095/biolreprod.109.081083.

Vajta G, Lewis IM, Hyttel P, Thouas GA, Trounson AO. Somatic cell cloning without micromanipulators. Cloning. 2001;3:89‒95. doi: 10.1089/15204550152475590.

Du Y, Kragh PM, Zhang Y, Li J, Schmidt M, Bogh IB. Piglets born from handmade cloning, an innovative cloning method without micromanipulation. Theriogenology. 2007;68:1104‒10. doi: 10.1016/j.theriogenology.2007.07.021.

Taylor-Robinson AW, Walton S, Vajta G. Production of a healthy farm-born calf by modified somatic cell nuclear transfer. Int J Livest Res. 2014;4:99‒104. doi: 10.5455/ijlr.20140301122524.

Zhang P, Liu P, Dou H, Chen L, Chen L, Lin L, et al. Handmade cloned transgenic sheep rich in Omega-3 fatty acids. PloS ONE. 2013;8:e55941. doi: 10.1371/journal.pone.0055941.

Oback B. Climbing mount efficiency–small steps, not giant leaps towards higher cloning success in farm animals. Reprod Domest Anim. 2008;43(Suppl 2):407‒16. doi: 10.1111/j.1439-0531.2008.01192.x.

Han YM, Kang YK, Koo DB, Lee KK. Nuclear reprogramming of cloned embryos produced in vitro. Theriogenology. 2003;59:33‒44. doi: 10.1016/S0093-691X(02)01271-2.

Camargo LS, Viana JH, Sa WF, Ferreira AM, Ramos AA. Factors influencing in vitro embryo production. Anim Reprod. 2006;3:19‒28.

Combelles CM, Gupta S, Agarwal A. Could oxidative stress influence the in-vitro maturation of oocytes? Reprod Biomed Online. 2009;18:864‒80. doi: 10.1016/S1472-6483(10)60038-7.

You J, Kim J, Lim J, Lee E. Anthocyanin stimulates in vitro development of cloned pig embryos by increasing the intracellular glutathione level and inhibiting reactive oxygen species. Theriogenology. 2010;74:777‒85. doi: 10.1016/j.theriogenology.2010.04.002.

Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol. 2003;552:335‒44. doi: 10.1113/jphysiol.2003.049478.

De Matos DG, Furnus CC. The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development: effect of β-mercaptoethanol, cysteine and cystine. Theriogenology. 2000;53:761‒71. doi: 10.1016/S0093-691X(99)00278-2.

Tao Y, Chen H, Tian NN, Huo DT, Li G, Zhang YH, et al. Effects of l‐Ascorbic acid, α‐Tocopherol and co‐culture on in vitro developmental potential of porcine cumulus cells free oocytes. Reprod Dom Anim. 2010;45:19‒25. doi: 10.1111/j.1439-0531.2008.01129.x.

Kwak SS, Cheong SA, Jeon Y, Lee E, Choi KC, Jeung EB, et al. The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization. Theriogenology. 2012;78:86‒101. doi: 10.1016/j.theriogenology.2012.01.024.

Wang F, Tian X, Zhang L, He C, Ji P, Li Y, et al. Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization. Fertil Steril. 2014;101:577‒86. doi: 10.1016/j.fertnstert.2013.10.041.

Mukherjee A, Malik H, Saha AP, Dubey A, Singhal DK, Boateng S, et al. Resveratrol treatment during goat oocytes maturation enhances developmental competence of parthenogenetic and hand-made cloned blastocysts by modulating intracellular glutathione level and embryonic gene expression. J Assist Reprod Genet. 2014;31:229‒39. doi: 10.1007/s10815-013-0116-9.

Gambini J, López-Grueso R, Olaso-González G, Inglés M, Abdelazid K, El Alami M, et al. Resveratrol: distribución, propiedades y perspectivas. Rev Esp Geriatr Gerontol. 2013;48:79‒88. doi: 10.1016/j.regg.2012.04.007.

Itami N, Shirasuna K, Kuwayama T, Iwata H. Resveratrol improves the quality of pig oocytes derived from early antral follicles through sirtuin 1 activation. Theriogenology. 2015;83:1360‒7. doi: 10.1016/j.theriogenology.2015.01.029.

Robledo-Verduzco JM, Herrera-Camacho J, Cajero-Juárez M, Navarro-Maldonado MC, García-Valladares A. Evaluación de dos medios de maduración in vitro para la producción de embriones ovinos. Trop Subtrop Agroecosyt. 2009;10:95‒9.

Kakkassery MP, Vijayakumaran V, Sreekumaran T. Effect of cumulus oocyte complex morphology on in vitro maturation of bovine oocytes. J Vet Anim Sci. 2010;41:12‒7.

Navarro-Maldonado MDC, Hernández-Martínez S, Martínez-Ibarra J, Vázquez-Avedaño R, Ambríz-García DA, Rangel-Santos R, et al. Clonación de embriones de Ovis aries utilizando fibroblastos criopreservados durante 14 meses. R Iberoam Cienc. 2016;3:45‒53.

Rienzi L, Balaban B, Ebner T, Mandelbaum J. The oocyte. Hum Reprod. 2012;27(Suppl 1):i2‒i21. doi: 10.1093/humrep/des200.

Vajta G, Bartels P, Joubert J, De la Rey M, Treadwell R, Callesen H. Production of a healthy calf by somatic cell nuclear transfer without micromanipulators and carbon dioxide incubators using the Handmade Cloning (HMC) and the Submarine Incubation System (SIS). Theriogenology. 2004;62:1465‒72. doi: 10.1016/j.theriogenology.2004.02.010.

Stringfellow DA, Seidel SM. Manual of the International Embryo Transfer Society: a procedural guide and general information for the use of embryo transfer technology, emphasizing sanitary precautions. 2a ed. Savoy, IL: International Embryo Transfer Society; 1990.

Tennen RI, Michishita-Kioi E, Chua KF. Finding a target for resveratrol. Cell. 2012;148:387‒9. doi: 10.1016/j.cell.2012.01.032.

Tarazona A, López A, Olivera-Ángel M. La competencia del ovocito: ¿qué, cómo y cuándo? Acta Biol Colomb. 2010;15:3‒18.

Nagafuchi A, Shirayoshi Y, Okazaki K, Yasuda K, Takeichi M. Transformation of cell adhesión properties by exogenously introduced E-cadherin cDNA. Nature. 1987;329:341‒3. doi: 10.1038/32934la0.

Watson AJ, Westhusin ME, DeSousa PA, Betts DH, Barcroft LC. Gene expression regulating blastocyst formation. Theriogenology. 1999;51:117‒33.

Qing J, Xuan L, Zhifen H, Lihong Z, Hua S, Linlin Y, et al. Resveratrol suppresses epithelial-to-mesenchymal transition in colorectal cancer through TGF-ß1/Smads signaling pathway mediated Snail/E-cadherin expression. BMC Cancer. 2015;15:97. doi 10.1186/s12885-015-1119-y.

Halstead P, Collins P, Isaakidou V. Sorting the sheep from the goats: morphological distinctions between the mandibles and mandibular teeth of adult Ovis and Capra. J Archaeol Sci. 2002;29:545‒53. doi: 10.1006/jasc.2001.0777.

Hamatani T, Carter MG, Sharov AA, Ko MS. Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell. 2004;6:117‒31. doi: 10.1016/S1534-5807(03)00373-3.




DOI: http://dx.doi.org/10.22201/fmvz.24486760e.2018.4.491

Refbacks

  • There are currently no refbacks.