Hostname: page-component-848d4c4894-tn8tq Total loading time: 0 Render date: 2024-06-30T05:54:47.343Z Has data issue: false hasContentIssue false

Effect of aquaporin 3 knockdown by RNA interference on antrum formation in sheep secondary follicles cultured in vitro

Published online by Cambridge University Press:  05 October 2018

Marcela Pinheiro Paz
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Fortaleza-CE, Brazil
Francisca Geovania Canafístula de Sousa
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Fortaleza-CE, Brazil
Benner Geraldo Alves
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Fortaleza-CE, Brazil
Carlos Henrique Lobo
Affiliation:
Laboratory of Reproductive Biology, Animal Science, Federal University of Ceará, Fortaleza, CE, Brazil
Antonia Débora Sales
Affiliation:
Estacio Fic, College & University. Fortaleza, Brazil
Kaio Cesar Simiano Tavares
Affiliation:
Molecular and Developmental Biology Lab, School of Medicine, University of Fortaleza, Fortaleza, CE, Brazil
Naíza Arcângela Ribeiro de Sá
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Fortaleza-CE, Brazil
Denise Damasceno Guerreiro
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Fortaleza-CE, Brazil
Carolina Maside
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Fortaleza-CE, Brazil
Rebeca Magalhães Pedrosa Rocha
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Fortaleza-CE, Brazil
Luciana Relly Bertolini
Affiliation:
Pontifical Catholic University of Rio Grande do Sul, Brazil
Vilceu Bordignon
Affiliation:
Department of Animal Science, McGill University, Ste-Anne-de-Bellevue, QC, Canada
José Ricardo de Figueiredo
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Fortaleza-CE, Brazil
Ana Paula Ribeiro Rodrigues*
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Fortaleza-CE, Brazil
*
Author for correspondence: Ana Paula Ribeiro Rodrigues. Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Fortaleza-CE, Brazil. 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: aprrodriguespapers@gmail.com

Summary

The objectives were to develop an effective protocol for transfection of ovine secondary follicles and to assess the effect of attenuating aquaporin 3 (AQP3) using a small interfering RNA (siRNA-AQP3) on antrum formation and follicular growth in vitro. Various combinations of Lipofectamine® volumes (0.5, 0.75 or 1.0 µl), fluorescent oligonucleotide (BLOCK-iT ™) concentrations (3.18, 27.12 or 36.16 nM) and exposure times (12, 14, 16, 18 or 20 h) were tested. The BLOCK-iT™ was replaced by siRNA-AQP3 in the transfection complex. Ovine secondary follicles were isolated and cultured in vitro for 6 days using standard protocols. Follicles were transfected on day 0 or 3 or on both days (0 and 3) and then cultured for an additional 3 or 6 days. As revealed by the fluorescence signal, the Lipofectamine®/BLOCK-iT™ complex (0.75 µl + 27.12 nM by 12 h of incubation) crossed the basement membrane and granulosa cell and reached the oocytes. In general, the rate of intact follicles was higher and the rate of antrum formation was lower in transfected follicles compared with control follicles. In conclusion, ovine secondary follicles can be successfully transfected during in vitro culture, and siRNA-mediated attenuation of AQP3 gene reduced antrum formation of secondary follicles.

Type
Research Article
Copyright
© Cambridge University Press 2018 

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

Atochina-Vasserman, EN, Biktasova, A, Abramova, E, Cheng, D-S, Polosukhin, VV, Tanjore, H, Takahashi, S, Sonoda, H, Foye, L, Venkov, C, Ryzhov, SV, Novitskiy, S, Shlonimskaya, N, Ikeda, M, Blackwell, TS, Lawson, WE, Gow, AJ, Harris, RC, Dikov, MM Tchekneva, EE (2013) Aquaporin 11 insufficiency modulates kidney susceptibility to oxidative stress. Am J Physiol Renal Physiol 304, 12951307.Google Scholar
Apolloni, LB, Bruno, JB, Alves, BG, Ferreira, ACA, Paes, VM, Moreno, JRC, Aguiar, FLN, Brandão, FZ, Smitz, J, Apgar, G Figueiredo, JR (2016) Accelerated follicle growth during the culture of isolated caprine preantral follicles is detrimental to follicular survival and oocyte meiotic resumption. Theriogenology 86, 15301540.Google Scholar
Bjørkskov, FB, Krabbe, SL, Nurup, CN, Missel, JW, Spulber, M, Bomholt, J, Molbaek, K, Helix-Nielsen, C, Gotfryd, K, Gourdon, P Pedersen, PA (2017) Purification and functional comparison of nine human aquaporins produced in Saccharomyces cerevisiae for the purpose of biophysical characterization. Nat Sci Rep 7, 16899.Google Scholar
Chaves, RN, Martins, FS, Saraiva, MVA, Celestino, JJH, Lopes, CAP, Correia, JC, Lima-Verde, IB, Matos, MHT, Báo, SN, Name, KPO, Campello, CC, Silva, JRV Figueiredo, JR (2008) Chilling ovarian fragments during transportation improve viability and growth of goat preantral follicles cultured in vitro. Reprod Fertil Dev 20, 640647.Google Scholar
Gosden, RG, Hunter, RHF, Telfer, E, Torrance, C Brown, N (1988) Physiological factors underlying the formation of ovarian follicular fluid. J Reprod Fertil 82, 813825.Google Scholar
Hara-Chikuma, M Verkman, AS (2008) Prevention of skin tumorigenesis and impairment of epidermal cell proliferation by targeted aquaporin-3 gene disruption. Mol Cell Biol 28, 328332.Google Scholar
Ishibashi, K Sasaki, S (1997) Aquaporin water channels in mammals. Clin Exp Nephrol 1, 247253.Google Scholar
Lima, IMT, Brito, IR, Rodrigues, GQ, Silva, CMG, Magalhães-Padilha, DM, Lima, LF, Celestino, JJ, Campello, CC, Silva, JR, Figueiredo, JR Rodrigues, AP (2011) Presence of c-kit mRNA in goat ovaries and improvement of in vitro preantral follicle survival and development with kit ligand. Mol Cell Endocrinol 345, 3847.Google Scholar
Livak, KJ Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Method 25, 402408.Google Scholar
Lunardi, FO, Chaves, RN, Lima, LF, Araújo, VR, Brito, IR, Souza, CEA, Donato, MAM, Peixoto, CA, Dinnyes, A, Campello, CC, Figueiredo, JR Rodrigues, APR (2015) Vitrified sheep isolated secondary follicles are able to grow and form antrum after a short period of in vitro culture. Cell Tissue Res 362, 241251.Google Scholar
Luz, VB, Santos, RR, Araújo, VR, Celestino, JJH, Magalhães-Padilha, DM, Chaves, RN, Brito, IR, Silva, TF, Almeida, AP, Campello, CC Figueiredo, JR (2012) The effect of LIF in the absence or presence of FSH on the in vitro development of isolated caprine preantral follicles. Reprod Domest Anim 47, 379384.Google Scholar
Luz, VB, Araújo, VR, Duarte, ABG, Silva, GM, Chaves, RN, Brito, IR, Serafim, MKB, Campello, CC, Feltrin, C, Bertolini, M, Almeida, AP, Santos, RR Figueiredo, JR (2013) Kit ligand and insulin-like growth factor I, affect the in vitro development of ovine preantral follicles. Small Rum Res 115, 99102.Google Scholar
McConnell, NA, Yunus, RS, Gross, SA, Bost, KL, Clemens, MG Hughes, FM Jr (2002) Water permeability of an ovarian antral follicle is predominantly transcellular and mediated by aquaporins. Endocrinology 143, 29052912.Google Scholar
Murai-Hatano, M, Kuwagata, T, Sakurai, J, Nonami, H, Ahamed, A, Nagasuga, K, Matsunami, T, Fukushi, K, Maeshima, M Okada, M (2008) Effect of low root temperature on hydraulic conductivity of rice plants and the possible role of aquaporins. Plant Cell Physiol 49, 12942305.Google Scholar
Pellavio, G, Rui, M, Caliogna, L, Martino, E, Gastaldi, G, Collina, S Laforenza, U (2017) Regulation of aquaporin functional properties mediated by the antioxidant effects of natural compounds. Int J Mol Sci 18, 2665.Google Scholar
Pradel, W, Mai, R, Gedrange, T Lauer, G (2008) Cell passage and composition of culture medium effects proliferation and differentiation of human osteoblast-like cells from facial bone. J Physiol Pharmacol 59(Suppl 5), 4758.Google Scholar
Preston, GM Agree, P (1991) Isolation of the cDNA for erythrocyte integral membrane protein of 28 kD: member of an ancient channel family. Proc Natl Acad Sci USA 88, 1111011114.Google Scholar
Qu, F, Wang, FF, Lu, XE, Dong, MY, Sheng, JZ, Lv, PP, Ding, GL, Shi, BW, Zhang, D Huang, HF (2010) Altered aquaporin expression in women with polycystic ovary syndrome: hyperandrogenism in follicular fluid inhibits aquaporin-9 in granulosa cells through the phosphatidylinositol 3-kinase pathway. Hum Reprod 25, 14411450.Google Scholar
Rodgers, RJ Irving-Rodgers, HF (2010) Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod 82, 10211029.Google Scholar
Sales, AD, Brito, IR, Lima, LF, Lobo, CH, Duarte, ABG, Souza, CEA, Moura, AA, Figueiredo, JR Rodrigues, APR (2014) Expression and localization of aquaporin 3 (AQP3) in folliculogenesis of ewes. Acta Histochem 116, 831837.Google Scholar
Sales, AD, Duarte, ABG, Rodrigues, GQ, Lima, LF, Silva, GM, Carvalho, AA, Brito, IR, Maranguape, RMS, Lobo, CH, Aragão, JAS, Moura, AA, Figueiredo, JR Rodrigues, APR (2015) Steady-state level of mRNA and immunolocalization of AQPs 3, 7 and 9 during in vitro growth of ovine preantral follicles. Theriogenology 84, 110.Google Scholar
Sales, AD, Duarte, AB, Santos, RR, Alves, KA, Lima, LF, Rodrigues, GQ, Brito, IR, Lobo, CH, Bruno, JB, Locatelli, Y, Figueiredo, JR Rodrigues, AP (2016) Modulation of aquaporins 3 and 9 after exposure of ovine ovarian tissue to cryoprotectants followed by in vitro culture. Cell Tissue Res 365, 415424.Google Scholar
Selokar, NL, Saini, M, Agrawal, H, Palta, P, Chauhan, MS, Manik, R Singla, SK (2015) Downregulation of DNA methyltransferase 1 in zona-free cloned buffalo (Bubalus bubalis) embryos by small interfering RNA improves in vitro development but does not alter DNA methylation level. Cell Reprogram 17, 8994.Google Scholar
Silva, JRV, Ferreira, MAL, Costa, SHF, Santos, RR, Carvalho, FAC, Rodrigues, APR, Lucci, CM, Báo, SH Figueiredo, JR (2002) Degeneration rate of preantral follicles in the ovaries of goats. Small Rum Res 43, 203209.Google Scholar
Skowronski, MT, Kwon, TH Nielsen, S (2009) Immunolocalization of aquaporin 1, 5 and 9 in the female pig reproductive system. J Histochem Cytochem 57, 6167.Google Scholar
Skowronski, MT (2010) Distribution and quantitative changes in amounts of aquaporin 1, 5 and 9 in the pig uterus during the estrous cycle and early pregnancy. Reprod Biol Endocrinol 8, 109.Google Scholar
Su, W, Guan, X, Zhang, D, Sun, M, Yang, L, Yi, F, Hao, F, Feng, X Ma, T (2013) Occurrence of multi-oocyte follicles in aquaporin 8-deficient mice. Reprod Biol Endocrinol 10, 88.Google Scholar
Tavares, KCS, Pinho, RM, Carneiro, IS, Aguiar, LH, Calderón, CEM, Martins, LT, Ambrósio, CE, Maga, EA, Bertolini, M, Murray, JD Bertolini, LR (2012) Efficient RNAi-induced protein knockdown in somatic cells using diced or chemically produced small interfering RNAs (siRNA). ASV 40, 1048.Google Scholar
Thoroddsen, A, Dahm-Kahler, P, Lind, AK, Weijdegard, B, Lindenthal, B, Muller, J Brännström, M (2011) The water permeability channels aquaporins 1–4 are differentially expressed in granulosa and theca cells of the preovulatory follicle during precise stages of human ovulation. J Clin Endocrinol Metab 96, 10211028.Google Scholar
Van den Hurk, R, Spek, ER, Hage, WJ, Fair, T, Ralph, JH Schotanus, K (1998) Ultrastructure and viability of isolated bovine preantral follicles. Hum Reprod 4, 833841.Google Scholar
Verkman, AS (2008) Mammalian aquaporins: diverse physiological roles and potential clinical significance. Expert Rev Mol Med 10, e13.Google Scholar
Verkman, AS (2009) Knock-out models reveal new aquaporin functions. Handb Exp Pharmacol 190, 359381.Google Scholar
Verkman, AS (2013) Aquaporins. Curr Biol 23, R52–5.Google Scholar
West-Farrell, ER, Xu, M, Gomberg, MA, Chow, YH, Woodruff, TK Shea, LD (2009) The mouse follicle microenvironment regulates antrum formation and steroid production: alterations in gene expression profiles. Biol Reprod 80, 432439.Google Scholar
Williams, L (2012) The role of aquaporins in the developing ovarian follicle. 203 f Thesis (Doctorate Degree in Philosophy) – University of Nottingham United Kingdon.Google Scholar
Xia, H, Ma, Y, Yu, C, Li, Y, Tang, J, Li, J, Zhao, Y Liu, Y (2014) Aquaporin 3 knockdown suppresses tumour growth and angiogenesis in experimental non-small cell lung cancer. Exp Physiol 99, 974984.Google Scholar
Yang, B, Song, Y, Zhao, D Verkman, AS (2005) Phenotype analysis of aquaporin-8 null mice. AJP – Cell Physiol 288, C1161C1170.Google Scholar