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Incorporation of arginine, glutamine or leucine in culture medium accelerates in vitro activation of primordial follicles in 1-day-old mouse ovary

Published online by Cambridge University Press:  02 June 2020

Parimah Alborzi ,
Mohammad Jafari Atrabi ,
Vahid Akbarinejad ,
Ramezan Khanbabaei  and
Rouhollah Fathi Open the ORCID record for Rouhollah Fathi [Opens in a new window]
Parimah Alborzi
Affiliation:
Department of Embryology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
Mohammad Jafari Atrabi
Affiliation:
Department of Embryology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
Vahid Akbarinejad
Affiliation:
Department of Theriogenology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
Ramezan Khanbabaei
Affiliation:
Department of Biology, Qaemshahr Branch, Islamic Azad University, Qaemshahr, Iran
Rouhollah Fathi*
Affiliation:
Department of Embryology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
*
Author for correspondence: Rouhollah Fathi. Department of Embryology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran. E-mail: [email protected]
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Summary

In vitro activation of primordial follicles provides cancer patients subjected to oncotherapy with a safe therapeutic strategy for fertility preservation, however a successful protocol for activation of primordial follicles in prepubertal patients has not yet been defined comprehensively. There is evidence that amino acids such as leucine, arginine and glutamine could stimulate the mammalian target of rapamycin (mTOR) pathway, which plays a pivotal role in primordial follicle activation. Nevertheless, there has been no report that elucidates the effect of these amino acids on in vitro development of ovarian follicles. Therefore, the present study was conducted to evaluate the effects of these amino acids and their combination on the formation and activation of primordial follicles in 1-day-old murine ovaries during an 11-day culture period. The experimental groups consisted of base medium (BM), base medium + arginine (ARG), base medium + glutamine (GLU), base medium + leucine (LEU) and base medium + a combination of arginine, glutamine and leucine (AGL). The proportions of different stages of ovarian follicles and gene expression of regulatory factors were assessed using histology and quantitative real-time PCR on days 5 and 11 of culture. The proportion of transitional and primary follicles was greater in all amino acid-treated groups compared with the BM group (P < 0.05). Moreover, leucine resulted in elevated expression of Gdf9 and Bmp15, and glutamine augmented the expression of Pi3k on day 11 of culture. In conclusion, the present study showed that inclusion of leucine, glutamine, arginine or their combination in the culture medium for murine ovarian tissue could accelerate the activation of primordial follicles and alter the expression of the corresponding factors.

Keywords

Amino acidsMouseOvaryPrimordial follicle activation
Type
Research Article
Information
Zygote , Volume 28 , Issue 5 , October 2020 , pp. 409 - 416
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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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
Adhikari, D, Risal, S, Liu, K and Shen, Y (2013). Pharmacological inhibition of mTORC1 prevents over-activation of the primordial follicle pool in response to elevated PI3K signaling. PLoS One 8, e53810.CrossRefGoogle ScholarPubMed
Amorim, CA and Shikanov, A (2016). The artificial ovary: current status and future perspectives. Future Oncol 12, 2323–32.CrossRefGoogle ScholarPubMed
Atrabi, MJ, Akbarinejad, V, Khanbabaee, R, Dalman, A, Andrade Amorim, C, Najar-Asl, M, Valojerdi, MR and Fathi, R (2019). Formation and activation induction of primordial follicles using granulosa and cumulus cells conditioned media. J Cell Physiol 234, 10148–56.CrossRefGoogle ScholarPubMed
Bockstaele, L, Tsepelidis, S, Dechene, J, Englert, Y and Demeestere, I (2012). Safety of ovarian tissue autotransplantation for cancer patients. Obstet Gynecol Int 2012, 495142.CrossRefGoogle ScholarPubMed
Chantranupong, L, Scaria, SM, Saxton, RA, Gygi, MP, Shen, K, Wyant, GA, Wang, T, Harper, JW, Gygi, SP and Sabatini, DM (2016). The CASTOR proteins are arginine sensors for the mTORC1 pathway. Cell 165, 153–64.CrossRefGoogle ScholarPubMed
Chen, X-Y, Xia, H-X, Guan, H-Y, Li, B and Zhang, W (2016). Follicle loss and apoptosis in cyclophosphamide-treated mice: what’s the matter? Int J Mol Sci 17, 836.CrossRefGoogle ScholarPubMed
Chen, Y, Breen, K and Pepling, ME (2009). Estrogen can signal through multiple pathways to regulate oocyte cyst breakdown and primordial follicle assembly in the neonatal mouse ovary. J Endocrinol 202, 407–17.CrossRefGoogle ScholarPubMed
Cheng, Y, Kim, J, Li, XX and Hsueh, AJ (2015). Promotion of ovarian follicle growth following mTOR activation: synergistic effects of AKT stimulators. PLoS One 10, e0117769.CrossRefGoogle ScholarPubMed
Dong, J, Albertini, DF, Nishimori, K, Kumar, TR, Lu, N and Matzuk, MM (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531.CrossRefGoogle ScholarPubMed
Durán, RV, Oppliger, W, Robitaille, AM, Heiserich, L, Skendaj, R, Gottlieb, E and Hall, MN (2012). Glutaminolysis activates Rag-mTORC1 signaling. Mol Cell 47, 349–58.CrossRefGoogle ScholarPubMed
El-Mestrah, M, Castle, PE, Borossa, G and Kan, FW (2002). Subcellular distribution of ZP1, ZP2, and ZP3 glycoproteins during folliculogenesis and demonstration of their topographical disposition within the zona matrix of mouse ovarian oocytes. Biol Reprod 66, 866–76.CrossRefGoogle ScholarPubMed
Fingar, DC and Blenis, J (2004). Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 23, 3151.CrossRefGoogle ScholarPubMed
Gilchrist, RB, Lane, M and Thompson, JG (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update 14, 159–77.CrossRefGoogle ScholarPubMed
Goldman, KN, Chenette, D, Arju, R, Duncan, FE, Keefe, DL, Grifo, JA and Schneider, RJ (2017). mTORC1/2 inhibition preserves ovarian function and fertility during genotoxic chemotherapy. Proc Natl Acad Sci USA 114, 3186–91.CrossRefGoogle ScholarPubMed
Hayashi, M, McGee, E, Min, G, Klein, C, Rose, UM, Duin, MV and Hsueh, AJ (1999). Recombinant growth differentiation factor-9 (GDF-9). enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 140, 1236–44.CrossRefGoogle ScholarPubMed
Herbst, RS, Baas, P, Kim, D-W, Felip, E, Pérez-Gracia, JL, Han, J-Y, Molina, J, Kim, J-H, Arvis, CD and Ahn, M-J (2016). Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet 387, 1540–50.CrossRefGoogle ScholarPubMed
Huang, Q, Cheung, AP, Zhang, Y, Huang, H-F, Auersperg, N and Leung, PC (2009). Effects of growth differentiation factor 9 on cell cycle regulators and ERK42/44 in human granulosa cell proliferation. Am J Physiol Endocrinol Metab 296, E1344–53.CrossRefGoogle ScholarPubMed
Hussein, MR (2005). Apoptosis in the ovary: molecular mechanisms. Hum Reprod Update 11, 162–78.CrossRefGoogle ScholarPubMed
Jeruss, JS and Woodruff, TK (2009). Preservation of fertility in patients with cancer. New Engl J Med 360, 902–11.CrossRefGoogle ScholarPubMed
Jewell, JL, Kim, YC, Russell, RC, Yu, F-X, Park, HW, Plouffe, SW, Tagliabracci, VS and Guan, K-L (2015). Metabolism. Differential regulation of mTORC1 by leucine and glutamine. Science 347, 194–8.CrossRefGoogle ScholarPubMed
John, GB, Gallardo, TD, Shirley, LJ and Castrillon, DH (2008). Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol 321, 197–204.CrossRefGoogle ScholarPubMed
Kim, JY (2012). Control of ovarian primordial follicle activation. Clin Exp Reprod Med 39, 10–14.CrossRefGoogle ScholarPubMed
Laplante, M and Sabatini, DM (2009). mTOR signaling at a glance. J Cell Sci 122, 3589–94.CrossRefGoogle ScholarPubMed
Li, N, Lee, B, Liu, R-J, Banasr, M, Dwyer, JM, Iwata, M, Li, X-Y, Aghajanian, G and Duman, RS (2010). mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 329, 959–64.CrossRefGoogle ScholarPubMed
Litscher, ES, Williams, Z and Wassarman, PM (2009). Zona pellucida glycoprotein ZP3 and fertilization in mammals. Mol Reprod Dev 76, 933–41.CrossRefGoogle ScholarPubMed
Luyckx, V, Scalercio, S, Jadoul, P, Amorim, CA, Soares, M, Donnez, J and Dolmans, M-M (2013). Evaluation of cryopreserved ovarian tissue from prepubertal patients after long-term xenografting and exogenous stimulation. Fertil Steril 100, 1350–1357. e1353.CrossRefGoogle ScholarPubMed
Ma, X, Han, M, Li, D, Hu, S, Gilbreath, KR, Bazer, FW and Wu, G (2017). L-Arginine promotes protein synthesis and cell growth in brown adipocyte precursor cells via the mTOR signal pathway. Amino Acids 49, 957–64.CrossRefGoogle ScholarPubMed
McLaughlin, M, Albertini, D, Wallace, W, Anderson, R and Telfer, E (2018). Metaphase II oocytes from human unilaminar follicles grown in a multi-step culture system. Mol Hum Reprod 24, 135–42.CrossRefGoogle Scholar
McNatty, KP, Juengel, JL, Reader, KL, Lun, S, Myllymaa, S, Lawrence, SB, Western, A, Meerasahib, MF, Mottershead, DG and Groome, NP (2005). Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function. Reproduction 129, 473–80.CrossRefGoogle ScholarPubMed
Memmott, RM and Dennis, PA (2009). Akt-dependent and-independent mechanisms of mTOR regulation in cancer. Cell Signal 21, 656–64.CrossRefGoogle ScholarPubMed
Molina, JR, Barton, DL and Loprinzi, CL (2005). Chemotherapy-induced ovarian failure. Drug Safety 28, 401–16.CrossRefGoogle ScholarPubMed
Mottershead, DG, Ritter, LJ and Gilchrist, RB (2011). Signalling pathways mediating specific synergistic interactions between GDF9 and BMP15. Mol Hum Reprod 18, 121–8.CrossRefGoogle ScholarPubMed
Nakajo, T, Yamatsuji, T, Ban, H, Shigemitsu, K, Haisa, M, Motoki, T, Noma, K, Nobuhisa, T, Matsuoka, J and Gunduz, M (2004). Glutamine is a key regulator for amino acid-controlled cell growth through the mTOR signaling pathway in rat intestinal epithelial cells. Biochem Biophys Res Commun 326, 174–80.CrossRefGoogle Scholar
Nilsson, EE and Skinner, MK (2002). Growth and differentiation factor-9 stimulates progression of early primary but not primordial rat ovarian follicle development. Biol Reprod 67, 1018–24.CrossRefGoogle Scholar
Otsuka, F, McTavish, KJ and Shimasaki, S (2011). Integral role of GDF-9 and BMP-15 in ovarian function. Mol Reprod Dev 78, 9–21.CrossRefGoogle ScholarPubMed
Otsuka, F, Yao, Z, Lee, T-H, Yamamoto, S, Erickson, GF and Shimasaki, S (2000). Bone morphogenetic protein-15: identification of target cells and biological functions. J Biol Chem 275, 39523–8.CrossRefGoogle ScholarPubMed
Perez-Andujar, A, Newhauser, W, Taddei, P, Mahajan, A and Howell, R (2013). The predicted relative risk of premature ovarian failure for three radiotherapy modalities in a girl receiving craniospinal irradiation. Phys Med Biol 58, 3107.CrossRefGoogle Scholar
Saxton, RA and Sabatini, DM (2017). mTOR signaling in growth, metabolism, and disease. Cell 168, 960–76.CrossRefGoogle ScholarPubMed
Saxton, RA, Chantranupong, L, Knockenhauer, KE, Schwartz, TU and Sabatini, DM (2016a). Mechanism of arginine sensing by CASTOR1 upstream of mTORC1. Nature 536, 229.CrossRefGoogle ScholarPubMed
Saxton, RA, Knockenhauer, KE, Wolfson, RL, Chantranupong, L, Pacold, ME, Wang, T, Schwartz, TU and Sabatini, DM (2016b). Structural basis for leucine sensing by the Sestrin2-mTORC1 pathway. Science 351, 53–8.CrossRefGoogle ScholarPubMed
Shamji, AF, Nghiem, P and Schreiber, SL (2003). Integration of growth factor and nutrient signaling: implications for cancer biology. Mol Cell 12, 271–80.CrossRefGoogle ScholarPubMed
Sun, X, Su, Y, He, Y, Zhang, J, Liu, W, Zhang, H, Hou, Z, Liu, J and Li, J (2015). New strategy for in vitro activation of primordial follicles with mTOR and PI3K stimulators. Cell Cycle 14, 721–31.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
Tingen, CM, Bristol-Gould, SK, Kiesewetter, SE, Wellington, JT, Shea, L and Woodruff, TK (2009). Prepubertal primordial follicle loss in mice is not due to classical apoptotic pathways. Biol Reprod 81, 16–25.CrossRefGoogle Scholar
Tong, Y, Li, F, Lu, Y, Cao, Y, Gao, J and Liu, J (2013). Rapamycin-sensitive mTORC1 signaling is involved in physiological primordial follicle activation in mouse ovary. Mol Reprod Dev 80, 1018–34.CrossRefGoogle ScholarPubMed
Vitt, U, Hayashi, M, Klein, C and Hsueh, A (2000). Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol Reprod 62, 370–7.CrossRefGoogle ScholarPubMed
Wassarman, P, Jovine, L and Litscher, E (2004). Mouse zona pellucida genes and glycoproteins. Cytogenet Genome Res 105, 228–34.CrossRefGoogle ScholarPubMed
Wolfson, RL, Chantranupong, L, Saxton, RA, Shen, K, Scaria, SM, Cantor, JR and Sabatini, DM (2016). Sestrin2 is a leucine sensor for the mTORC1 pathway. Science 351, 43–8.CrossRefGoogle ScholarPubMed
Xiao, S, Zhang, J, Romero, MM, Smith, KN, Shea, LD and Woodruff, TK (2015). In vitro follicle growth supports human oocyte meiotic maturation. Sci Rep 5, 17323.CrossRefGoogle ScholarPubMed
Yan, C, Wang, P, DeMayo, J, DeMayo, FJ, Elvin, JA, Carino, C, Prasad, SV, Skinner, SS, Dunbar, BS and Dube, JL (2001). Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol 15, 854–66.CrossRefGoogle ScholarPubMed
Yao, K, Yin, Y-L, Chu, W, Liu, Z, Deng, D, Li, T, Huang, R, Zhang, J, Tan, B and Wang, W (2008). Dietary arginine supplementation increases mTOR signaling activity in skeletal muscle of neonatal pigs. J Nutr 138, 867–72.CrossRefGoogle ScholarPubMed
Zhang, H and Liu, K (2015). Cellular and molecular regulation of the activation of mammalian primordial follicles: somatic cells initiate follicle activation in adulthood. Hum Reprod Update 21, 779–86.CrossRefGoogle ScholarPubMed
Zhang, H, Risal, S, Gorre, N, Busayavalasa, K, Li, X, Shen, Y, Bosbach, B, Brännström, M and Liu, K (2014). Somatic cells initiate primordial follicle activation and govern the development of dormant oocytes in mice. Curr Biol 24, 2501–8.CrossRefGoogle ScholarPubMed
Zhao, Y, Zhang, Y, Li, J, Zheng, N, Xu, X, Yang, J, Xia, G and Zhang, M (2018). MAPK3/1 participates in the activation of primordial follicles through mTORC1-KITL signaling. J Cell Physiol 233, 226–37.CrossRefGoogle ScholarPubMed
Zhou, S, Yan, W, Shen, W, Cheng, J, Xi, Y, Yuan, S, Fu, F, Ding, T, Luo, A and Wang, S (2018). Low expression of SEMA 6C accelerates the primordial follicle activation in the neonatal mouse ovary. J Cell Mol Med 22, 486–96.CrossRefGoogle Scholar