Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-28T15:09:08.990Z Has data issue: false hasContentIssue false

In vitro culture systems as an alternative for female reproductive toxicology studies

Published online by Cambridge University Press:  15 March 2019

Denise Damasceno Guerreiro*
Affiliation:
Faculdade de Veterinária, Laboratório de Manipulação de Oócitos e Folículos Ovarianos Pré-Antrais (Lamofopa), Universidade Estadual do Ceará, Fortaleza, Ceará, Brasil
Gildas Tetaping Mbemya
Affiliation:
Faculdade de Veterinária, Laboratório de Manipulação de Oócitos e Folículos Ovarianos Pré-Antrais (Lamofopa), Universidade Estadual do Ceará, Fortaleza, Ceará, Brasil
Jamily Bezerra Bruno
Affiliation:
Faculdade de Veterinária, Laboratório de Manipulação de Oócitos e Folículos Ovarianos Pré-Antrais (Lamofopa), Universidade Estadual do Ceará, Fortaleza, Ceará, Brasil
Luciana Rocha Faustino
Affiliation:
Programa de Pós-Graduação em Biotecnologia, Campus Ministro Reis Velloso, Universidade Federal do Piauí, Paranaíba, Piauí, Brasil
José Ricardo de Figueiredo
Affiliation:
Faculdade de Veterinária, Laboratório de Manipulação de Oócitos e Folículos Ovarianos Pré-Antrais (Lamofopa), Universidade Estadual do Ceará, Fortaleza, Ceará, Brasil
Ana Paula Ribeiro Rodrigues
Affiliation:
Faculdade de Veterinária, Laboratório de Manipulação de Oócitos e Folículos Ovarianos Pré-Antrais (Lamofopa), Universidade Estadual do Ceará, Fortaleza, Ceará, Brasil
*
Address for correspondence: Denise Damasceno Guerreiro. Programa de Pós-Graduação em Ciências Veterinárias (PPGCV), Laboratório de Manipulação de Oócitos e Folículos Pré-Antrais (LAMOFOPA), Universidade Estadual do Ceará (UECE), Av. Dr. Silas Munguba, 1700, Campus do Itaperi, Fortaleza – CE – Brasil. CEP: 60 714 903. Tel: +55 85 3101 9852. Fax: +55 85 3101 9840. E-mail: [email protected]

Summary

Studies have shown that daily exposure to different products, whether chemical or natural, can cause irreversible damage to women’s reproductive health. Therefore it is necessary to use tests that evaluate the safety and efficacy of these products. Most reproductive toxicology tests are performed in vivo. However, in recent years, various cell culture methods, including embryonic stem cells and tissues have been developed with the aim of reducing the use of animals in toxicological tests. This is a major advance in the area of toxicology, as these systems have the potential to become a widely used tool compared with in vivo tests routinely used in reproductive biology and toxicology. The present review describes and highlights data on in vitro culture processes used to evaluate reproductive toxicity as an alternative to traditional methods using in vivo tests.

Type
Review Article
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.)

References

Abbott, A (2005) Animal testing: more than a cosmetic change. Nature 10, 438 (7065).Google Scholar
Adler, S, Basketter, D, Creton, S, Pelkonen, O, Van Benthem, J, Zuang, V, Andersen, KE et al (2011) Alternative (non-animal) methods for cosmetics testing: current status and future prospects–2010. Arch Toxicol 85, 367485.Google Scholar
Alves, AM, Chaves, RN, Rocha, RM, Lima, LF, Andrade, PM, Lopes, CA, Souza, CE, Moura, AA, Campello, CC, Báo, SN, Smitz, J and Figueiredo, JR (2013) Dynamic medium containing growth differentiation factor-9 and FSH maintains survival and promotes in vitro growth of caprine preantral follicles after long-term in vitro culture. Reprod Fertil Dev 25, 955965.Google Scholar
American Type, Culture Collection (1994) Catalogue of Cell Lines and Hybrydomas. 8th edn. Rockville: ATCC, 637 pp.Google Scholar
Arunakumari, G, Shanmugasundaram, N and Rao, VH (2010) Development of morulae from the oocytes of cultured sheep preantral follicles. Theriogenology 74, 884894.Google Scholar
Asano, T and Cotruvo, JA (2004) Groundwater recharge with reclaimed municipal wastewater: health and regulatory considerations. Water Res 38 19411951.Google Scholar
Baldassarre, H (2008) Coleta, Conservação e Transferência de Embrião. In: Aisen, EG. Reprodução Ovina e Caprina, 1st edn. São Paulo-SP: Medicina Veterinária, pp. 143152.Google Scholar
Balls, M and Karcher, W (1995) The validation of alternative test methods. ATLA 23, 884886.Google Scholar
Balls, M, Botham, P, Cordier, A, Fumero, S, Kayser, D, Koëter, H, Koundakjian, P, Lindquis, NG, Meyer, O, Pioda, L, Reinhardt, C, Rozemond, H, Smyrniotis, T, Spielmann, H, Van Looy, H, Van Der Venne, MT and Walum, E (1990) Report and recommendations of an international workshop on promotion of the regulatory acceptance of validated non-animal toxicity test procedures. ATLA 18, 339344.Google Scholar
Balls, M, Blaauboer, BJ, Fentem, JH, Bruner, L, Combes, RD, Ekwall, B, Fielder, RJ, Guillouzo, A, Lewis, RW, Lovell, DP, Reinhardt, CA, Repetto, G, Sladowski, D, Spielmann, H and Zucco, F (1995) Practical aspects of the validation of toxicity test procedures. The report and recommendations of ECVAM workshop 5. ATLA 23, 129147.Google Scholar
Balls, M, Van ZelleR, AM and Halder, M (eds) (2000) Progress in the reduction, refinement and replacement of animal experimentation. Amsterdam: Elsevier, 1795 pp.Google Scholar
Beker, VWAB, Gröllers-Mulderij, M, Snel, C, Jeurissen, N, Stierum, R, Wolter-Beek, A (2012) The bovine oocyte in vitro maturation model: a potential tool for reproductive toxicology screening. Reprod Toxicol 34, 251260.Google Scholar
Betteridge, KJ and Rieger, D (1993) Embryo transfer and related techniques in domestic animals, and their implications for human medicine. Hum Reprod 8, 147167.Google Scholar
Bhattacharya, P and Keating, AF (2012) Protective role for ovarian glutathione S-transferase isoform pi during 7,12-dimethylbenz[a]anthracene-induced ovotoxicity. Toxicol Appl Pharmacol 260, 201208.Google Scholar
Blaise, C and Férard, J (eds) (2005) Small‐scale Freshwater Toxicity Investigations. Springer.Google Scholar
Bouwmeester, MC, Ruiter, S, Lommelaars, T, Sippel, J, Hodemaekers, HM, Van den Brandhof, EJ, Pennings, JL, Kamstra, JH, Jelinek, J, Issa, JP, Legler, J and van der Ven, LT (2016) Zebrafish embryos as a screen for DNA methylation modifications after compound exposure. Toxicol Appl Pharmacol 291, 8496.Google Scholar
Bremer, S and Hartung, T (2004) The use of embryonic stem cells for regulatory developmental toxicity testing in vitro – the current status of test developments. Curr Pharmaceut Design 10, 27332747.Google Scholar
Broadhead, CL and Combes, RD (2001) The current status of food additives toxicity testing and the potential for application of the three Rs. Altern Lab Anim 29, 471485.Google Scholar
Burdick, JA, Mason, MN, Hinman, AD, Thorne, K and Anseth, KS (2002) Delivery of osteoinductive growth factors from degradable PEG hydrogels influences osteoblast differentiation and mineralization. J Control Release 63, 5363.Google Scholar
Burton, ABG, York, M and Lawrence, RS (1981) The in vitro assessment of severe eye irritants. Food and Cosmetics Toxicology 19, 471480.Google Scholar
Cain, L, Chatterje, ES and Collins, TJ (1995) In vitro folliculogenesis of rat preantral follicles. Endocrinology 136, 33693377.Google Scholar
Castro, MP (1978) Cultura de células de tecido animal: um esboço histórico. Publ ACIESP, São Paulo, 10, iv.Google Scholar
Cavalcante, AYP, Gouveia, BB, Barberino, RS, Lins, TLBG, Santos, LP, Gonçalves, RJS, Celestino, JJH and Matos, MHT (2015) Kit ligand promotes the transition from primordial to primary follicles after in vitro culture of ovine ovarian tissue. Zygote 24, 578582.Google Scholar
Chamberlain, M and Parish, WE (1990) Hazard and risk based on in vitro test data. Toxicol In Vitro 4(4–5), 694697.Google Scholar
Chamberlain, M, Gad, SC, Gautheron, P and Prinsen, MK (1997) Organotypic models for the assessment/prediction of ocular irritation. Food Chem Toxicol Oxford, 35, 2337.Google Scholar
Chiu, Y-H, Williams, PL, Gillman, MW, Gaskins, AJ, Minguez-Alarcon, L, Souter, I, Toth, TL, Ford, JB, Hauser, R, Chavarro, JE and EARTH, Study Team (2018) Association between pesticide residue intake from consumption of fruits and vegetables and pregnancy outcomes among women undergoing infertility treatment with assisted reproductive technology. JAMA Int Med 178, 1726.Google Scholar
Corrêa, CL, Alonzo, HGA and Trevisan, RMS (2003) Risk assessment. In: Oga, S. Fundamentals of Toxicology 2nd edn. São Paulo: Atheneu. Chapter 16, pp. 6976.Google Scholar
Cortvrindt, R, and Smitz, JEJ (2001) In vitro follicle growth: achievements in mammalian species. Reprod Domest Anim 36, 39.Google Scholar
Cortvrindt, R, Smitz, J and Van Steirteghem, AC (1996) In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepubertal mice in a simplified culture system. Hum Reprod 11, 26562666.Google Scholar
Creton, S, Dewhurst, IC, Earl, LK, Gehen, SC, Guest, RL, Hotchkiss, JA, Indans, I, Woolhiser, MR and Billington, R (2010) Acute toxicity testing of chemicals: opportunities to avoid redundant testing and use alternative approaches. Crit Rev Toxicol 40, 5083.Google Scholar
Cruz, AS (2003) In vitro cytotoxicity test as an alternative to the in vivo Draize test in the evaluation of cosmetic products. Thesis (PhD Production and Pharmaceutical Controls) University of São Paulo, São Paulo.Google Scholar
De Torres, EP Larrauri, AG and Kunh, GR (1997) Ensayos alternativos a la experimentacion animal. Animales de Experimentación 3, 3036.Google Scholar
Devine, PJ, Sipes, IG, Skinner, MK and Hoyer, PB (2002) Characterization of a rat in vitro ovarian culture system to study the ovarian toxicant 4-vinylcyclohexene diepoxide. Toxicol Appl Pharmacol 184, 107115.Google Scholar
Doke, SK and Dhawale, SC (2013) Alternatives to animal testing: a review. Saudi Pharm J 23, 223229.Google Scholar
Eaton, DL and Gilbert, SG (2013) Principles of toxicology. In: Klaassen, CD (ed.). Casarett and Doull’s Toxicology: The Basic Science of Poisons, 8th edn. New York: McGraw-Hill Education, pp. 1348.Google Scholar
Faqi, AS (2012) A critical evaluation of developmental and reproductive toxicology in nonhuman primates. Syst Biol Reprod Med 58, 2332.Google Scholar
Faustino, LR, Rossetto, R, Lima, IM, Silva, CM, Saraiva, MV, Lima, LF, Silva, AW, Donato, MA, Campello, CC, Peixoto, CA, Figueiredo, JR and Rodrigues, AP (2011) Expression of keratinocyte growth factor in goat ovaries and its effects on preantral follicles within cultured ovarian cortex. Reprod Science 18, 12221229.Google Scholar
Ferris, J, Mahboubi, K, Maclusky, N, King, WA and Favetta, L (2016) BPA exposure during in vitro oocyte maturation results in dose-dependent alterations to embryo development rates, apoptosis rate, sex ratio and gene expression. Reprod Toxicol 59,128138.Google Scholar
Figueiredo, JR, Rodrigues, APR, Amorim, CA and Silva, JRV (2008) Manipulação de oócitos inclusos em folículos ovarianos pré-antrais. In: Biotécnicas aplicadas à reprodução animal 2nd edn. São Paulo: Roca, pp. 303327.Google Scholar
Ganesan, S and Keating, AF (2016) Bisphenol a-induced ovotoxicity involves DNA damage induction to which the ovary mounts a protective response indicated by increased expression of proteins involved in dna repair and xenobiotic biotransformation. Toxicol Sci 152, 169180.Google Scholar
Gao, LR, Li, S, Zhang, J, Liang, C, Chen, EN, Zhang, SY, Chuai, M, Bao, YP, Wang, G, and Yang, X (2016) Excess imidacloprid exposure causes the heart tube malformation of chick embryos. J Agric Food Chem 64, 90789088.Google Scholar
Gelboin, HV (1980) Benzo[alpha]pyrene metabolism, activation and carcinogenesis: role and regulation of mixed-function oxidases and related enzymes. Physiol Rev 60, 11071166.Google Scholar
Giridharan, NV (2000) Use of Animals in Scientific Research. New Delhi, India: Indian Council of Medical Research.Google Scholar
Goswami, D and Conway, GS (2005) Premature ovarian failure. Hum Reprod Update 11, 391410.Google Scholar
Guerreiro, DD, Lima, LF, Carvalho, AA, Rodrigues, GQ, Castro, SV Campello, CC, Pessoa, C, Gadelha, CRF, Figueiredo, JR, Bordignon, V and Rodrigues, APR (2016) In situ cultured preantral follicles is a useful model to evaluate the effect of anticancer drugs on caprine folliculogenesis. Micros Res Tech 79, 773781.Google Scholar
Hareng, L, Pellizzer, C, Bremer, S, Schwarz, M and Hartung, T (2005) The integrated project ReProTect: a novel approach in reproductive toxicity hazard assessment. Reprod Toxicol 20, 441452.Google Scholar
Harkness, JE and Wagner, JE (1993) Biologia e cĺinica de coelhos e roedores, 3rd edn. São Paulo: Roca, pp. 1076.Google Scholar
Hart, RJ (2016) Physiological aspects of female fertility: role of the environment, modern lifestyle, and genetics. Physiol Rev 96, 873909.Google Scholar
Hartung, T, Bremer, S, Casati, S, Coecke, S, Corvi, R, Fortaner, S, Gribaldo, L, Halder, M, Hoffmann, S, Roi, AJ Prieto, P, Sabbioni, E, Scott, L, Worth, A and Zuang, V (2004) A modular approach to the ECVAM principles on test validity. Altern Lab Anim 32, 467472.Google Scholar
Hauser, R, Duty, S, Godfrey-Bailey, L and Calafat, AM (2004) Medications as a source of human exposure to phthalates. Environ Health Perspect 112, 751753.Google Scholar
Helke, KL and Swindle, MM (2013) Animal models of toxicology testing: the role of pigs. Expert Opin Drug Metab Toxicol 9, 127139.Google Scholar
Hendriksen, CF (2007) Three Rs achievements in vaccinology. AATEX 14, Special Issue, 575579.Google Scholar
Heudorf, U, Mersch-Sundermann, V and Angerer, J (2007) Phthalates: toxicology and exposure. Int J Hyg Environ Health 210, 623634.Google Scholar
Holmes, AM, Creton, S and Chapman, K (2010) Working in partnership to advance the 3Rs in toxicity testing. Toxicology 267, 1419.Google Scholar
Hoyer, PB and Sipes, IG (1996) Assessment of follicle destruction in chemical-induced ovarian toxicity. Annu Rev Pharmacol Toxicol 36, 307331.Google Scholar
Hu, Q, Guo, F, Zhao, F and Fu, Z (2017) Effects of titanium dioxide nanoparticles exposure on parkinsonism in zebrafish larvae and PC12. Chemosphere 2173, 373379.Google Scholar
Huff, J (2001) Carcinogenicity bioassays of bisphenol A, 4-vinylcyclohexene diepoxide, and 4-vinylcyclohexene. Toxicol Sci 64, 282283.Google Scholar
Husoy, T, Syversen, T and Jenssen, J (1993) Comparisons of four in vitro cytotoxicity tests: the MTT assay, NR assay, uridine incorporation and protein measurements. Toxicol In Vitro Oxford, 7, 149154.Google Scholar
Igawa, Y, Keating, AF, Rajapaksa, KS, Sipes, IG and Hoyer, PB (2009) Evaluation of ovotoxicity induced by 7,12-dimethylbenz[a]anthracene and its 3,4-diol metabolite utilizing a rat in vitro ovarian culture system. Toxicol Appl Pharmacol 234, 361369.Google Scholar
Ikezuki, Y, Tsutsumi, O, Takai, Y, Kamei, Y and Taketani, Y (2002) Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod 17, 28392841.Google Scholar
Jimenez, C, De Azevedo, J, Silveira, R, Penitente-Filho, J, Carrascal-Triana, E, Zolini, A, Araujo, V, Torres, C and Gonçalves, W (2016) Effects of IGF-1 on in vitro culture of bovine preantral follicles are dose-dependent. Reprod Dom Anim 51, 435444.Google Scholar
Keating, AF, Mark, CJ, Sen, N, Sipes, IG and Hoyer, PB (2009) Effect of phosphatidylinositol-3 kinase inhibition on ovotoxicity caused by 4-vinylcyclohexene diepoxide and 7,12-dimethylbenz[a]anthracene in neonatal rat ovaries. Toxicol Appl Pharmacol 241, 127134.Google Scholar
Krysko, DV, Vanden Berghe, T, D’Herde, K, Vandenabeele, P (2008) Apoptosis and necrosis: detection, discrimination and phagocytosis. Methods 44, 205221.Google Scholar
Lande, Y, Fisch, B, Tsur, A, Farhi, J, Prag-Rosenberg, R, Ben-Haroush, A, Kessler-Icekson, G, Zahalka, MA, Ludeman, SM, Abir, R (2017) Short-term exposure of human ovarian follicles to cyclophosphamide metabolites seems to promote follicular activation in vitro . Reprod Biomed Online 34, 104114.Google Scholar
Leiva-Revilla, J, Lima, LF, Castro, SV, Campello, CC, Araújo, VR, Celestino, JJH, Pessoa, ODL, Silveira, ER, Rodrigues, APR and Figueiredo, JR (2016) Fraction of Auxemma oncocalyx and oncocalyxone A affects the in vitro survival and development of caprine preantral follicles enclosed in ovarian cortical tissue. Forsch Komplementmed 23, 307313.Google Scholar
Lenz, WA (1988) A short history of thalidomide embriopathy. Teratology 38, 203215.Google Scholar
Leoni, G, Bogliolo, L, Deiana, G, Berlinguer, F, Rosati, I, Pintus, PP, Ledda, S and Naitana, S (2002) Influence of cadmium exposure on in vitro ovine gamete dysfunction. Reprod Toxicol 16, 371377.Google Scholar
Liang, S, Zhao, MH, Ock, SA, Kim, NH and Cui, XS (2016) Fluoride impairs oocyte maturation and subsequent embryonic development in mice. Environ Toxicol 31,14861495.Google Scholar
Liu, Y, Li, GP, Sessions, BR, Rickords, LF, White, KL and Bunch, TD (2008) Nicotine induces multinuclear formation and causes aberrant embryonic development in bovine. Mol Reprod Dev 75, 801809.Google Scholar
Lopes, F, Smith, R, Anderson, RA and Spears, N (2014) Docetaxel induces moderate ovarian toxicity in mice, primarily affecting granulosa cells of early growing follicles. Mol Hum Reprod 20, 948959.Google Scholar
Lorenzetti, S, Altieri, I, Arabi, S, Balduzzi, D, Bechi, N, Cordelli, E, Galli, C, Ietta, F, Modina, SC, Narciso, L, Pacchierotti, F, Villani, P, Galli, A, Lazzari, G, Luciano, AM, Paulesu, L, Spanò, M and Mantovani, A (2011) Innovative non-animal testing strategies for reproductive toxicology: the contribution of Italian partners within the EU project. ReProTect Annali dell’Istituto Superiore di Sanità 47 (4), 429444.Google Scholar
Luciano, AM, Franciosi, F, Lodde, V, Corban, ID, Lazzari, G, Crotti, G, Galli, C, Pellizzer, C, Bremer, S, Weimer, M and Modina, SC (2010) Transferability and inter-laboratory variability assessment of the in vitro bovine oocyte maturation (IVM) test within ReProTect. Reprod Toxicol 30, 8188.Google Scholar
Madden, JA, Hoyer, PB, Devine, PJ and Keating, AF (2014) Acute 7,12-dimethylbenz[a]anthracene exposure causes differential concentration-dependent follicle depletion and gene expression in neonatal rat ovaries. Toxicol Appl Pharmacol 276, 179187.Google Scholar
Martignoni, M, Groothuis, GMM and De Kante, RR (2006) Species diffeences between mouse, rat, dog, monkey and human CYP‐mediated drug metabolism, inhibition and induction. Expert Opin Drug Metab Toxicol 2, 875894.Google Scholar
McLaughlin, EA and Mciver, SC (2009) Awakening the oocyte: controlling primordial follicle development. Reproduction 137, 111.Google Scholar
Ménézo, YJ and Hérubel, F (2002) Mouse and bovine models for human IVF. Reprod Biomed Online 4, 170175.Google Scholar
Meyer, O (2003) Testing and assessment strategies, including alternative and new approaches. Toxicol Lett 140–141, 2130.Google Scholar
Mlynarcikova, A, Nagyova, E, Fickova, M and Scsuková, S (2009) Effects of selected endocrine disruptors on meiotic maturation, cumulus expansion, synthesis of hyaluronan and progesterone by procine oocyte-cumulus complexes. Toxicol In Vitro 23, 371377.Google Scholar
Muczynski, V, Lecureuil, C, Messiaen, S, Guerquin, M-J, N’Tumba-Byn, T, Moison, D, Hodroj, W, Benjelloun, H, Baijer, J, Livera, G, Frydman, R, Benachi, A, Habert, R and Rouiller-Fabre, V (2012) Cellular and molecular effect of mehp involving lxrα in human fetal testis and ovary. PLoS One 7, e48266.Google Scholar
National Research, Council (USA) Institute for Laboratory Animal Research (2004) The Development of Science-based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop Washington (DC). National Academies Press (USA).Google Scholar
O’Brien, MJ, Pendola, JK and Eppig, JJ (2003) A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol Reprod 68, 16821686.Google Scholar
OECD (2005) Guidance document on the validation and international acceptance of new or updated test methods for hazard assessment. Series on Testing and Assessment No. 34 OECD, Paris.Google Scholar
Pesty, A, Miyara, F, Debey, P, Lefevre, B and Poirot, C (2007) Multiparameter assessment of mouse oogenesis during follicular growth in vitro . Mol Hum Reprod 13, 39.Google Scholar
Postma, JF, de Valk, S, Dubbeldam, M, Maas, JL, Tonkes, M, Schipper, CA and Kater, BJ (2002) Confounding factors in bioassays with freshwater and marine organisms. Ecotoxicol Environ Safety 53, 226237.Google Scholar
Quantin, P, Thélu, A, Catoire, S and Ficheux, H (2015) Perspectives and strategies of alternative methods used in the risk assessment of personal care products. Annales Pharmaceutiques Françaises 73, 422435.Google Scholar
Rajapaksa, KS, Sipes, IG and Hoyer, PB (2007) Involvement of microsomal epoxide hydrolase enzyme in ovotoxicity caused by 7,12-dimethylbenz[a]anthracene. Toxicol Sci 96, 327334.Google Scholar
Richmond, J (2002) Refinement, reduction, and replacement of animal use for regulatory testing: future improvements and implementation within the regulatory framework. ILAR J 43 Suppl(1), S63S68.Google Scholar
Rockett, JC and Kim, SJ (2005) Biomarkers of reproductive toxicity. Cancer Biomark 1, 93108.Google Scholar
Rollin, BE (2003) Toxicology and new social ethics for animals.Toxicol Pathol 31, 128131.Google Scholar
Rose, UM, Hanssen, RG and Kloosterboer, HJ (1999) Development and characterisation of an in vitro ovulation model using mouse ovarian follicles. Biol Reprod 61, 503511.Google Scholar
Roti Roti, EC, Leisman, SK, Abbott, DH, Salih, SM (2012) Acute doxorubicin insult in the mouse ovary is cell-and follicle-type dependente. PLoS One, 7, e42293.Google Scholar
Roti Roti, EC, Ringelstetter, AK, Kropp, J, Abbott, DH, Salih, SM (2014) Bortezomib prevents acute doxorubicin ovarian insult and follicle demise, improving the fertility window and pup birth weight in mice. PLoS One, 9 e108174.Google Scholar
Rusche, B (2003) The 3 Rs and animal welfare-conflict or the way forward. ALTEX 20, 6376.Google Scholar
Russell, WMS and Burch, RL (1992) The Principles of Humane Experimental Technique. London : Methuen and Co. Special edition published by Universities Federation for Animal Welfare (UFAW), 1992.Google Scholar
Saldanha, PH (1994) The tragedy of thalidomide and the advent of experimental teratology. Braz J Genet 17, 449464.Google Scholar
Salih, SM, Ringelstetter, AK, Elsarrag, MZ, Abbott, DH and Roti Roti, EC (2015) Dexrazoxane abrogates acute doxorubicin toxicity in marmoset ovary. Biol Reprod 92, 73.Google Scholar
Santos, BF (2002) Criação e manejo de camundongos. In: Andrade A, Pinto S and Oliveira RS (Org) Animais de laboratório: criacção e experimentação Rio de Janeiro: FIOCRUZ, 2002c pp. 115–8.Google Scholar
Schechtman, LM (2002) Implementation of the 3Rs (Refinement, reduction, and replacement): Validation and regulatory acceptance considerations for alternative toxicological test methods. ILAR J 43 S85S94.Google Scholar
Siddique, S, Sadeau, JC, Foster, WG, Feng, YL and Zhu, J (2014) In vitro exposure to cigarette smoke induces oxidative stress in follicular cells of F1 hybrid mice. J Appl Toxicol 34, 224226.Google Scholar
Smitz, JEJ and Cortvrindt, RG (2002) The earliest stages of folliculogenesis in vitro . Reproduction 123, 185202.Google Scholar
Soares, MA, Costa, JJ, Vasconcelos, GL, Ribeiro, RP, Souza, JC, Silva, AL, Van den Hurk, R and Silva, JR (2017) Effects of frutalin on early follicle morphology, ultrastructure and gene expression in cultured goat ovarian cortical tissue. Histol Histopathol 15, 11882.Google Scholar
Spielmann, H (2009) The way forward in reproductive/developmental toxicity testing. Altern Lab Anim 37, 641656.Google Scholar
Stefansdottir, A, Fowler, PA, Powles-Glove, RN, Anderson, RA and Spears, N (2014) Use of ovary culture techniques in reproductive toxicology. Reprod Toxicol 49, 117135.Google Scholar
Stokes, WS (2002) Humane endpoint for laboratory animals used in regulatory testing. ILAR J 43, S31S38.Google Scholar
Strojny, B, Grodzik, M, Sawosz, E, Winnicka, A, Kurantowicz, N, Jaworski, S, Kutwin, M, Urbańska, K, Hotowy, A, Wierzbicki, M and Chwalibog, A (2016) Diamond nanoparticles modify curcumin activity: in vitro studies on cancer and normal cells and in ovo studies on chicken embryo model. PLoS One 11, e0164637.Google Scholar
Sun, F, Betzendahl, I, Shen, Y, Cortvrindt, R Smitz, J and Eichenlaub-Ritter, U (2004) Pre-antral follicle culture as a novel in vitro assay in reproductive toxicology testing in mammalian oocytes. Mutagenesis 19, 1325.Google Scholar
Toropov, AA, Toropova, AP, Raska, Ijr, Leszczynska, D, Leszczynski, J (2014) Comprehension of drug toxicity: software and databases. Comput Biol Med 45, 2025.Google Scholar
Twu, NF, Srinivasan, R, Chou, CH, Wu, LS and Chiu, CH (2012) Cantharidin and norcantharidin inhibit caprine luteal cell steroidogenesis in vitro . Exp Toxicol Pathol 64(1–2), 3744.Google Scholar
UK Home Office (2014) Annual Statistics of Scientific Procedures on Living Animals Great Britain 2014. Available at: https://www.gov.uk/government/statistics/statistics-of-scientific-procedures-on-living-animals-great-britain-2014 Google Scholar
Vandebriel, RJ and Van Loveren, H (2010) Non-animal sensitization testing: state-of-the-art. Crit Rev Toxicol 40, 389404.Google Scholar
Vrsanska, S, Nagyová, E, Mlynarciková, A, Ficková, M and Kolena, J (2003) Components of cigarette smoke inhibit expansion of oocyte cumulus complexes from porcine follicles. Physiol Res 52, 383387.Google Scholar
Wan, X, Zhu, J, Zhu, Y, Ma, X, Zheng, Y, Wang, F, Liu, Z and Zhang, T (2010) Rat ovarian follicle bioassay reveals adverse effects of cadmium chloride (CdCl2) exposure on follicle development and oocyte maturation. Toxicol Ind Health 26, 609618.Google Scholar
Wilson-Sanders, SE (2011) Invertebrate Models for biomedical research, testing and education. ILAR J 52, 126152.Google Scholar
Žalmanová, T, Hošková, K, Nevoral, J, Adámková, K, KottT, , Šulc, M, Kotíková, Z, Prokešová, S, Jílek, F, Králíčková, M and Petr, J (2017) Bisphenol S negatively affects the meotic maturation of pig oocytes. Sci Rep 7, 485.Google Scholar
Zhang, J and Liu, H (2015) Cytoplasm replacement following germinal vesicle transfer restores meiotic maturation and spindle assembly in meiotically arrested oocytes. Reprod Biomed Online 31, 7178.Google Scholar
Zhang, Q, Ji, C, Yan, L, Lu, M, Lu, C and Zhao, M (2016) The identification of the metabolites of chlorothalonil in zebrafish (Danio rerio) and their embryo toxicity and endocrine effects at environmentally relevant levels. Environ Pollut 218, 815.Google Scholar