Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-19T14:17:15.193Z Has data issue: false hasContentIssue false
  • English
  • Français

Aloe vera increases collagen fibres in extracellular matrix and mRNA expression of peroxiredoxin-6 in bovine ovarian cortical tissues cultured in vitro

Published online by Cambridge University Press:  01 December 2021

Francisco das Chagas Costa ,
Erlândia Márcia Vasconcelos ,
Venância Antônia Nunes Azevedo ,
Ernando Igo Teixeira de Assis ,
Laís Raiane Feitosa Melo Paulino ,
Anderson Weiny Barbalho Silva ,
José Roberto Viana Silva Open the ORCID record for José Roberto Viana Silva [Opens in a new window]  and
Ana Liza Paz Souza Batista
Francisco das Chagas Costa
Affiliation:
Postgraduate Program in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Sobral, CE, Brazil.
Erlândia Márcia Vasconcelos
Affiliation:
Postgraduate Program in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Sobral, CE, Brazil.
Venância Antônia Nunes Azevedo
Affiliation:
Postgraduate Program in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Sobral, CE, Brazil.
Ernando Igo Teixeira de Assis
Affiliation:
Postgraduate Program in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Sobral, CE, Brazil.
Laís Raiane Feitosa Melo Paulino
Affiliation:
Postgraduate Program in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Sobral, CE, Brazil.
Anderson Weiny Barbalho Silva
Affiliation:
Postgraduate Program in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Sobral, CE, Brazil.
José Roberto Viana Silva
Affiliation:
Postgraduate Program in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Sobral, CE, Brazil.
Ana Liza Paz Souza Batista*
Affiliation:
Postgraduate Program in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Sobral, CE, Brazil.
*
Author for correspondence: Ana Liza Paz Souza Batista. Federal University of Ceará, Av. Comandante Maurocélio Rocha Ponte, 100, CEP 62042–280, Sobral, CE, Brazil. Tel: /Fax: +55 88 36118000. E-mail: analizabatista@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

In vitro culture of ovarian tissue containing primordial follicles is an important tool to study the initiation of follicular populations and to develop efficient culture systems to support in vitro follicle growth. Considering that in vitro culture favours oxidative stress, it is very important to supplement culture medium with antioxidant substances such as Aloe vera extract. This study aims to evaluate the effects of different concentrations of Aloe vera on the distribution of collagen fibres in the extracellular matrix, follicular activation, development and survival in bovine ovarian cortical tissues cultured in vitro, as well as on expression of mRNAs for antioxidant enzymes [superoxide dismutase (SOD), catalase (CAT), peroxiredoxin 6 (PRDX6) and glutathione peroxidase 1 (GPX1)]. To this end, ovarian cortical tissues were cultured for 6 days in α-MEM alone or supplemented with different concentrations of Aloe vera extract (1.0, 5.0, 10.0 or 50.0%). After culture, fragments were fixed and processed histologically to evaluate follicular morphology and activation, as well as the extracellular matrix by staining with picrosirius red. The levels of mRNA for SOD, CAT, PRDX6 and GPX1 in cultured ovarian tissues were evaluated by real-time polymerase chain reaction (PCR). Ovarian tissues cultured with 10.0 or 50.0% Aloe vera had higher percentages of collagen fibres than tissues cultured in control medium. A significant increase in developing follicles was observed in ovarian tissues cultured in α-MEM alone or supplemented with 10% Aloe vera when compared with fresh control or tissues cultured with 1.0% Aloe vera. Presence of Aloe vera did not influence the percentage of morphologically normal follicles when compared with control medium. Ovarian tissues cultured with 50.0% Aloe vera had higher percentages of morphologically normal follicles than those cultured with 10.0% Aloe vera. Furthermore, 10% Aloe vera significantly increased mRNA levels for PRDX6. In conclusion, 10.0% Aloe vera improves extracellular matrix distribution in cultured tissues and increases the expression of mRNA for PRDX6 after 6 days in vitro.

Keywords

Aloe veraAntioxidantBovine ovarian folliclesCollagenIn vitro culture
Type
Research Article
Information
Zygote , Volume 30 , Issue 3 , June 2022 , pp. 365 - 372
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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

Adhikari, D, Flohr, G, Gorre, N, Shen, Y, Yang, H, Lundin, E, Lan, Z, Gambello, MJ and Liu, K (2009). Disruption of Tsc2 in oocytes leads to overactivation of the entire pool of primordial follicles. Mol Hum Reprod 15, 765–70.CrossRefGoogle ScholarPubMed
Agarwal, A, Aponte-Mellado, A, Premkumar, BJ, Shaman, A and Gupta, S (2012). The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol 10, 49.CrossRefGoogle ScholarPubMed
Ali, MM, Mahmoud, AM, Le Master, E, Levitan, I and Phillips, SA (2019). Role of matrix metalloproteinases and histone deacetylase in oxidative stress-induced degradation of the endothelial glycocalyx. Am J Physiol Heart Circ Physiol 316, H647–63.CrossRefGoogle ScholarPubMed
Arunakumari, G, Shanmugasundaram, N and Rao, VH (2010). Development of morulae from the oocytes of cultured sheep preantral follicles. Theriogenology 74, 884–94.CrossRefGoogle ScholarPubMed
Bala, S, Chugh, NA, Bansal, SC, Garg, ML and Koul, A (2017). Protective role of Aloe vera against X-ray induced testicular dysfunction. Andrologia 49, 10.1111/and.12697.CrossRefGoogle Scholar
Behmanesh, MA, Najafzadehvarzi, H and Poormoosavi, SM (2018). Protective effect of Aloe vera extract against bisphenol A induced testicular toxicity in Wistar rats. Cell J 20, 278–283.Google ScholarPubMed
Berkholtz, CB, Shea, LD and Woodruff, TK (2006). Extracellular matrix functions in follicle maturation. Semin Reprod Med 24, 262–9.CrossRefGoogle ScholarPubMed
Bizarro-Silva, C, Santos, MM, Gerez, JR, González, SM, Lisboa, LA and Seneda, MM (2018). Influence of follicle-stimulating hormone concentrations on the integrity and development of bovine follicles cultured in vitro . Zygote 26, 417–23.CrossRefGoogle ScholarPubMed
Cesar, V, Jozić, I, Begović, L, Vuković, T, Mlinarić, S, Lepeduš, H, Borović Šunjić, SB and Žarković, N (2018). Cell-type-specific modulation of hydrogen peroxide cytotoxicity and 4-hydroxynonenal binding to human cellular proteins in vitro by antioxidant Aloe vera extract. Antioxidants (Basel) 7, 125.CrossRefGoogle ScholarPubMed
Dupont, J and Scaramuzzi, RJ (2016). Insulin signalling and glucose transport in the ovary and ovarian function during the ovarian cycle. Biochem J 473, 1483–501.CrossRefGoogle ScholarPubMed
Figueiredo, JR and Lima, LF (2017). Artificial ovary technology: applications, state of art, limitations and prospects. Braz J Anim Reprod 41, 248–53.Google Scholar
Fisher, AB, Vasquez-Medina, JP, Dodia, C, Sorokina, EM, Tao, JQ and Feinstein, SI (2018). Peroxiredoxin 6 phospholipid hydroperoxidase activity in the repair of peroxidized cell membranes. Redox Biol 14, 41–6.CrossRefGoogle ScholarPubMed
Franchi, FF, Hernandes, MP, Coalho Ferreira, AL, Vieira de Lima, VA, de Oliveira Mendes, L, Musa de Aquino, A, Scarano, WR and César de Souza Castilho, A (2020). Fractal analysis and histomolecular phenotyping provides insights into extracellular matrix remodeling in the developing bovine fetal ovary. Biochem Biophys Res Commun 523, 823–8.CrossRefGoogle ScholarPubMed
Fu, XH, Chen, CZ, Wang, Y, Peng, YX, Wang, WH, Yuan, B, Gao, Y, Jiang, H and Zhang, JB (2019). COL1A1 affects apoptosis by regulating oxidative stress and autophagy in bovine cumulus cells. Theriogenology 139, 81–9.CrossRefGoogle ScholarPubMed
Gonella-Diaza, AM, Silveira Mesquita, F, Lopes, E, Ribeiro da Silva, K, Cogliati, B, De Francisco Strefezzi, R and Binelli, M (2018). Sex steroids drive the remodeling of oviductal extracellular matrix in cattle. Biol Reprod 99, 590–9.CrossRefGoogle ScholarPubMed
Gouveia, BB, Macedo, TJS, Santos, JMS, Barberino, RS, Menezes, VG, Müller, MC, Almeida, JRGS, Figueiredo, JR and Matos, MHT (2016). Supplemented base medium containing Amburana cearensis associated with FSH improves in vitro development of isolated goat preantral follicles. Theriogenology 86, 1275–84.CrossRefGoogle ScholarPubMed
Gouveia, BB, Barberino, RS, Menezes, VG, Macedo, TJS, Cavalcante, AYP, Gonçalves, RJS, Almeida, JRGS and Matos, MHT (2019). DNA damage and primordial follicle activation after in vitro culture of sheep ovarian cortex in Morus nigra leaf extract. Pesq Vet Bras 39, 85–92.CrossRefGoogle Scholar
Guerreiro, DD, Lima, LFd, Rodrigues, GQ, Carvalho, AdA, Castro, SV, Campello, CC, Pessoa, CdÓ, Gadelha, CRF, Figueiredo, JRd, 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. Microsc Res Tech 79, 773–81.CrossRefGoogle ScholarPubMed
Haritha, K, Ramesh, B and Saralakumari, D (2014). Effect of Aloe vera gel on antioxidant enzymes in streptozotocin-induced cataractogenesis in male and female Wistar rats. J Acute Med 4, 38–44.CrossRefGoogle Scholar
Joseph, B and Raj, SJ (2010). Pharmacognostic and phytochemical properties of Aloe vera Linn – an overview. Int J Pharm Sci Rev Rev Res 4, 106–10.Google Scholar
Kala, M, Shaikh, MV and Nivsarkar, M (2017). Equilibrium between anti-oxidants and reactive oxygen species: a requisite for oocyte development and maturation. Reprod Med Biol 16, 28–35.CrossRefGoogle ScholarPubMed
Kliem, H, Welter, H, Kraetzl, WD, Steffl, M, Meyer, HHD, Schams, D and Berisha, B (2007). Expression and localisation of extracellular matrix degrading proteases and their inhibitors during the oestrous cycle and after induced luteolysis in the bovine corpus luteum. Reproduction 134, 535–47.CrossRefGoogle ScholarPubMed
Lins, TLBG, Cavalcante, AYP, Santos, JMS, Menezes, VG, Barros, VRP, Barberino, RS, Bezerra, MÉS, Macedo, TJS and Matos, MHT (2017). Rutin can replace the use of three other antioxidants in the culture medium, maintaining the viability of sheep isolated secondary follicles. Theriogenology 89, 263–70.CrossRefGoogle ScholarPubMed
Magalhães, DDM, Araujo, VR, Verde, IBL, Matos, MHTd, Silva, RC, Lucci, CM, Báo, SN, Campello, CC and Figueiredo, JRd (2009). Diferentes origens do Hormônio Folículo Estimulante (FSH) influenciam a viabilidade e o desenvolvimento de folículos pré-antrais caprinos. Braz J Vet Res Anim Sci 46, 378–86.CrossRefGoogle Scholar
Magalhães, DM, Fernandes, DD, Mororó, MB, Silva, CM, Rodrigues, GQ, Bruno, JB, Matos, MH, Campello, CC and Figueiredo, JR (2011). Effect of the medium replacement interval on the viability, growth and in vitro maturation of isolated caprine and ovine pre-antral follicles. Reprod Domest Anim 46, 134–40.CrossRefGoogle ScholarPubMed
Mbemya, GT, Cadenas, J, Ribeiro de Sá, NA, Damasceno Guerreiro, D, Donfack, NJ, Alberto Vieira, L, Canafístula de Sousa, FG, Geraldo Alves, B, Lobo, CH, Santos, FW, Lima Pinto, FDC, Loiola Pessoa, OD, Smitz, J, Comizzoli, P, Figueiredo, JR and Rodrigues, APR (2018). Supplementation of in vitro culture medium with FSH to grow follicles and mature oocytes can be replaced by extracts of Justicia insularis . PLoS ONE 13, e0208760.CrossRefGoogle ScholarPubMed
McLaughlin, M, Bromfield, JJ, Albertini, DF and Telfer, EE (2010). Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Mol Hum Reprod 16, 644–53.CrossRefGoogle ScholarPubMed
Muncie, JM and Weaver, VM (2018). The physical and biochemical properties of the extracellular matrix regulate cell fate. Curr Top Dev Biol 130, 1–37.CrossRefGoogle ScholarPubMed
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, 1682–6.CrossRefGoogle ScholarPubMed
Park, CH, Son, HU, Yoo, CY and Lee, SH (2017). Low molecular-weight gel fraction of Aloe vera exhibits gastroprotection by inducing matrix metalloproteinase-9 inhibitory activity in alcohol-induced acute gastric lesion tissues. Pharm Biol 55, 2110–5.CrossRefGoogle ScholarPubMed
Passos, JR, Costa, JJ, da Cunha, EV, Silva, AW, Ribeiro, RP, de Souza, GB, Barroso, PA, Dau, AM, Saraiva, MV, Gonçalves, PB, van den Hurk, R and Silva, JR (2016). Protein and messenger RNA expression of interleukin 1 system members in bovine ovarian follicles and effects of interleukin 1β on primordial follicle activation and survival in vitro . Domest Anim Endocrinol 54, 48–59.CrossRefGoogle ScholarPubMed
Perkins, A, Poole, LB and Karplus, PA (2014). Tuning of peroxiredoxin catalysis for various physiological roles. Biochemistry 53, 7693–705.CrossRefGoogle ScholarPubMed
Quan, J, Elhousiny, M, Johnson, NW and Gao, J (2013). Transforming growth factor-β1 treatment of oral cancer induces epithelial–mesenchymal transition and promotes bone invasion via enhanced activity of osteoclasts. Clin Exp Metastasis 30, 659–70.CrossRefGoogle ScholarPubMed
Rittié, L (2017). Method for picrosirius red-polarization detection of collagen fibers in tissue sections. Methods Mol Biol 1627, 395–407.CrossRefGoogle ScholarPubMed
Sá, NAR, Bruno, JB, Guerreiro, DD, Cadenas, J, Alves, BG, Cibin, FWS, Leal-Cardoso, JH, Gastal, EL and Figueiredo, JR (2018). Anethole reduces oxidative stress and improves in vitro survival and activation of primordial follicles. Braz J Med Biol Res 51, e7129.CrossRefGoogle ScholarPubMed
Saito, M, Tanaka, M, Misawa, E, Yao, R, Nabeshima, K, Yamauchi, K, Abe, F, Yamamoto, Y and Furukawa, F (2016). Oral administration of Aloe vera gel powder prevents UVB-induced decrease in skin elasticity via suppression of overexpression of MMPs in hairless mice. Biosci Biotechnol Biochem 80, 1416–24.CrossRefGoogle ScholarPubMed
Santos, LdPd, Santos, JMdS, Menezes, VG, Barberino, RdS, Gouveia, BB, Cavalcante, AYP, Lins, TLBG, Gonçalves, RJdS, Celestino, JJdH and Matos, MHTd (2017). Blocking the PI3K pathway or the presence of high concentrations of EGF inhibits the spontaneous activation of ovine primordial follicles in vitro. Anim Reprod 14, 1298–306.CrossRefGoogle Scholar
Sharapov, MG, Novoselov, VI and Gudkov, SV (2019). Radioprotective role of peroxiredoxin 6. Antioxidants (Basel) 8, 15.CrossRefGoogle ScholarPubMed
Sholehvar, F, Mehrabani, D, Yaghmaei, P and Vahdati, A (2016). The effect of Aloe vera gel on viability of dental pulp stem cells. Dent Traumatol 32, 390–6.CrossRefGoogle ScholarPubMed
Silva, AWB, Ribeiro, RP, Menezes, VG, Barberino, RS, Passos, JRS, Dau, AMP, Costa, JJN, Melo, LRF, Bezerra, FTG, Donato, MAM, Peixoto, CA, Matos, MHT, Gonçalves, PBD, Van den Hurk, R and Silva, JRV (2017). Expression of TNF-α system members in bovine ovarian follicles and the effects of TNF-α or dexamethasone on preantral follicle survival, development and ultrastructure in vitro . Anim Reprod Sci 182, 56–68.CrossRefGoogle ScholarPubMed
Smith, JD, Bryant, SR, Coupe, LL, Vary, CP, Gotwals, PJ, Koteliansky, VE and Lindner, V (1999). Soluble transforming growth factor-beta type II receptor inhibits negative remodeling, fibroblast transdifferentiation, and intimal lesion formation but not endothelial growth. Circ Res 84, 1212–22.CrossRefGoogle Scholar
Souza, ALP, Lima, GL, Peixoto, GCX, Silva, AM, Oliveira, MF and Silva, AR (2016). Use of Aloe vera–based extender for chilling and freezing collared peccary (Pecari tajacu) semen. Theriogenology 85, 1432–8.CrossRefGoogle ScholarPubMed
Sumi, FA, Sikder, B, Rahman, MM, Lubna, SR, Ulla, A, Hossain, MH, Jahan, IA, Alam, MA and Subhan, N (2019). Phenolic content analysis of Aloe vera gel and evaluation of the effect of Aloe gel supplementation on oxidative stress and fibrosis in isoprenaline-administered cardiac damage in rats. Prev Nutr Food Sci 24, 254–64.CrossRefGoogle ScholarPubMed
Telfer, EE and Zelinski, MB (2013). Ovarian follicle culture: advances and challenges for human and nonhuman primates. Fertil Steril 99, 1523–33.CrossRefGoogle ScholarPubMed
Telfer, EE, McLaughlin, M, Ding, C and Thong, KJ (2008). A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum Reprod 23, 1151–8.CrossRefGoogle ScholarPubMed
Tseng, HS, Wang, YF, Tzeng, YM, Chen, DR, Liao, YF, Chiu, HY and Hsieh, WT (2017). Aloe-emodin enhances tamoxifen cytotoxicity by suppressing Ras/ERK and PI3K/mTOR in breast cancer cells. Am J Chin Med 45, 337–50.CrossRefGoogle ScholarPubMed
Verma, RP and Hansch, C (2007). Matrix metalloproteinases (MMPs): chemical-biological functions and (Q)SARs. Bioorg Med Chem 15, 2223–68.CrossRefGoogle ScholarPubMed
Woodruff, TK and Shea, LD (2007). The role of the extracellular matrix in ovarian follicle development. Reprod Sci 14 Supplement, 6–10.CrossRefGoogle ScholarPubMed
Xing, W, Guo, W, Zou, CH, Fu, TT, Li, XY, Zhu, M, Qi, JH, Song, J, Dong, CH, Li, Z, Xiao, Y, Yuan, PS, Huang, H and Xu, X (2015). Acemannan accelerates cell proliferation and skin wound healing through AKT/mTOR signaling pathway. J Dermatol Sci 79, 101–9.CrossRefGoogle ScholarPubMed
Zha, X, Wu, G, Zhao, X, Zhou, L, Zhang, H, Li, J, Ma, L and Zhang, Y (2015). PRDX6 protects ARPE-19 Cells from Oxidative Damage via PI3K/AKT signaling. Cell Physiol Biochem 36, 2217–28.CrossRefGoogle ScholarPubMed
Zhou, L, Xie, Y, Li, S, Liang, Y, Qiu, Q, Lin, H and Zhang, Q (2017). Rapamycin prevents cyclophosphamide-induced over-activation of primordial follicle pool through PI3K/Akt/mTOR signaling pathway in vivo . J Ovarian Res 10, 56.CrossRefGoogle ScholarPubMed