Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-16T21:17:11.831Z Has data issue: false hasContentIssue false
  • English
  • Français

Loss of Arf Guanine Nucleotide Exchange Factor GBF1 Activity Disturbs Organelle Dynamics in Mouse Oocytes

Published online by Cambridge University Press:  22 January 2021

Yuan-Jing Zou ,
Meng-Meng Shan ,
Zhen-Nan Pan ,
Meng-Hao Pan ,
Xiao-Han Li  and
Shao-Chen Sun Open the ORCID record for Shao-Chen Sun [Opens in a new window]
Yuan-Jing Zou
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, China
Meng-Meng Shan
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, China
Zhen-Nan Pan
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, China
Meng-Hao Pan
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, China
Xiao-Han Li
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, China
Shao-Chen Sun*
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, China
*
*Author for correspondence: Shao-Chen Sun, E-mail: [email protected]
Get access

Abstract

GBF1 [Golgi brefeldin A (BFA) resistance factor 1] is a member of the guanine nucleotide exchange factors Arf family. GBF1 localizes at the cis-Golgi and endoplasmic reticulum (ER)-Golgi intermediate compartment where it participates in ER-Golgi traffic by assisting in the recruitment of the coat protein COPI. However, the roles of GBF1 in oocyte meiotic maturation are still unknown. In the present study, we investigated the regulatory functions of GBF1 in mouse oocyte organelle dynamics. In our results, GBF1 was stably expressed during oocyte maturation, and GBF1 localized at the spindle periphery during metaphase I. Inhibiting GBF1 activity led to aberrant accumulation of the Golgi apparatus around the spindle. This may be due to the effects of GBF1 on the localization of GM130, as GBF1 co-localized with GM130 and inhibiting GBF1 induced condensation of GM130. Moreover, the loss of GBF1 activity affected the ER distribution and induced ER stress, as shown by increased GRP78 expression. Mitochondrial localization and functions were affected, as the mitochondrial membrane potential was altered. Taken together, these results suggest that GBF1 has wide-ranging effects on the distribution and functions of Golgi apparatus, ER, and mitochondria as well as normal polar body formation in mouse oocytes.

Keywords

GBF1Golgi apparatusmeiosismitochondriaoocyte
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 27 , Issue 2 , April 2021 , pp. 400 - 408
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the Microscopy Society of America

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

Ackema, KB, Hench, J, Bockler, S, Wang, SC, Sauder, U, Mergentaler, H, Westermann, B, Bard, F, Frank, S & Spang, A (2014). The small GTPase Arf1 modulates mitochondrial morphology and function. EMBO J 33(22), 2659–2675.CrossRefGoogle ScholarPubMed
Ackema, KB, Sauder, U, Solinger, JA & Spang, A (2013). The ArfGEF GBF-1 is required for ER structure, secretion and endocytic transport in C. elegans. PLoS One 8(6), e67076.CrossRefGoogle ScholarPubMed
Citterio, C, Vichi, A, Pacheco-Rodriguez, G, Aponte, AM, Moss, J & Vaughan, M (2008). Unfolded protein response and cell death after depletion of brefeldin A-inhibited guanine nucleotide-exchange protein GBF1. Proc Natl Acad Sci USA 105(8), 2877–2882.CrossRefGoogle ScholarPubMed
Claude, A, Zhao, BP, Kuziemsky, CE, Dahan, S, Berger, SJ, Yan, JP, Armold, AD, Sullivan, EM & Melancon, P (1999). GBF1: A novel Golgi-associated BFA-resistant guanine nucleotide exchange factor that displays specificity for ADP-ribosylation factor 5. J Cell Biol 146(1), 71–84.Google ScholarPubMed
Coticchio, G, Dal Canto, M, Mignini Renzini, M, Guglielmo, MC, Brambillasca, F, Turchi, D, Novara, PV & Fadini, R (2015). Oocyte maturation: Gamete-somatic cells interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization. Hum Reprod Update 21(4), 427–454.CrossRefGoogle ScholarPubMed
Demain, LA, Conway, GS & Newman, WG (2017). Genetics of mitochondrial dysfunction and infertility. Clin Genet 91(2), 199–207.CrossRefGoogle ScholarPubMed
Farhat, R, Ankavay, M, Lebsir, N, Gouttenoire, J, Jackson, CL, Wychowski, C, Moradpour, D, Dubuisson, J, Rouille, Y & Cocquerel, L (2018). Identification of GBF1 as a cellular factor required for hepatitis E virus RNA replication. Cell Microbiol 20, 1.CrossRefGoogle ScholarPubMed
Friedman, JR, Lackner, LL, West, M, DiBenedetto, JR, Nunnari, J & Voeltz, GK (2011). ER tubules mark sites of mitochondrial division. Science 334(6054), 358–362.CrossRefGoogle ScholarPubMed
Gao, Z, Peng, M, Chen, L, Yang, X, Li, H, Shi, R, Wu, G, Cai, L, Song, Q & Li, C (2019). Prion protein protects cancer cells against endoplasmic reticulum stress induced apoptosis. Virol Sin 34(2), 222–234.CrossRefGoogle ScholarPubMed
Garcia-Mata, R, Szul, T, Alvarez, C & Sztul, E (2003). ADP-ribosylation factor/COPI-dependent events at the endoplasmic reticulum-Golgi interface are regulated by the guanine nucleotide exchange factor GBF1. Mol Biol Cell 14(6), 2250–2261.CrossRefGoogle ScholarPubMed
Gilchrist, RB, Lane, M & Thompson, JG (2008). Oocyte-secreted factors: Regulators of cumulus cell function and oocyte quality. Hum Reprod Update 14(2), 159–177.CrossRefGoogle ScholarPubMed
Gillingham, AK & Munro, S (2007). The small G proteins of the Arf family and their regulators. Annu Rev Cell Dev Biol 23, 579–611.CrossRefGoogle ScholarPubMed
Guzel, E, Arlier, S, Guzeloglu-Kayisli, O, Tabak, MS, Ekiz, T, Semerci, N, Larsen, K, Schatz, F, Lockwood, CJ & Kayisli, UA (2017). Endoplasmic reticulum stress and homeostasis in reproductive physiology and pathology. Int J Mol Sci 18(4), 792.CrossRefGoogle ScholarPubMed
He, S, O'Connell, D, Zhang, X, Yang, Y & Liang, C (2014). The intersection of Golgi-ER retrograde and autophagic trafficking. Autophagy 10(1), 180–181.CrossRefGoogle ScholarPubMed
Ignashkova, TI, Gendarme, M, Peschk, K, Eggenweiler, HM, Lindemann, RK & Reiling, JH (2017). Cell survival and protein secretion associated with Golgi integrity in response to Golgi stress-inducing agents. Traffic 18(8), 530–544.CrossRefGoogle ScholarPubMed
Kaczmarek, B, Verbavatz, JM & Jackson, CL (2017). GBF1 and Arf1 function in vesicular trafficking, lipid homoeostasis and organelle dynamics. Biol Cell 109(12), 391–399.CrossRefGoogle ScholarPubMed
Kaufman, RJ (2004). Regulation of mRNA translation by protein folding in the endoplasmic reticulum. Trends Biochem Sci 29(3), 152–158.CrossRefGoogle ScholarPubMed
Kawamoto, K, Yoshida, Y, Tamaki, H, Torii, S, Shinotsuka, C, Yamashina, S & Nakayama, K (2002). GBF1, a guanine nucleotide exchange factor for ADP-ribosylation factors, is localized to the cis-Golgi and involved in membrane association of the COPI coat. Traffic 3(7), 483–495.CrossRefGoogle ScholarPubMed
Kristensen, SG, Pors, SE & Andersen, CY (2017). Improving oocyte quality by transfer of autologous mitochondria from fully grown oocytes. Hum Reprod 32(4), 725–732.Google ScholarPubMed
Latham, KE (2015). Endoplasmic reticulum stress signaling in mammalian oocytes and embryos: Life in balance. Int Rev Cell Mol Biol 316, 227–265.CrossRefGoogle ScholarPubMed
Latham, KE (2016). Stress signaling in mammalian oocytes and embryos: A basis for intervention and improvement of outcomes. Cell Tissue Res 363(1), 159–167.CrossRefGoogle ScholarPubMed
Lee, MC, Miller, EA, Goldberg, J, Orci, L & Schekman, R (2004). Bi-directional protein transport between the ER and Golgi. Annu Rev Cell Dev Biol 20, 87–123.CrossRefGoogle ScholarPubMed
Liu, K, Liu, Y, Xu, Y, Nandakumar, KS, Shen, X, Lin, J, Li, C, He, C & Zhou, C (2019). Regulatory role of Golgi brefeldin A resistance factor-1 in amyloid precursor protein trafficking, cleavage and Abeta formation. J Cell Biochem 120(9), 15604–15615.CrossRefGoogle ScholarPubMed
Lowery, J, Szul, T, Styers, M, Holloway, Z, Oorschot, V, Klumperman, J & Sztul, E (2013). The Sec7 guanine nucleotide exchange factor GBF1 regulates membrane recruitment of BIG1 and BIG2 guanine nucleotide exchange factors to the trans-Golgi network (TGN). J Biol Chem 288(16), 11532–11545.CrossRefGoogle Scholar
Martin, W (2017). Supply and demand of energy in the oocyte and the role of mitochondria. Results Probl Cell Differ 63, 373–387.CrossRefGoogle ScholarPubMed
Moreno, RD, Schatten, G & Ramalho-Santos, J (2002). Golgi apparatus dynamics during mouse oocyte in vitro maturation: Effect of the membrane trafficking inhibitor brefeldin A. Biol Reprod 66(5), 1259–1266.CrossRefGoogle ScholarPubMed
Nakamura, N, Rabouille, C, Watson, R, Nilsson, T, Hui, N, Slusarewicz, P, Kreis, TE & Warren, G (1995). Characterization of a cis-Golgi matrix protein, GM130. J Cell Biol 131(6 Pt 2), 1715–1726.CrossRefGoogle ScholarPubMed
Namgaladze, D, Khodzhaeva, V & Brune, B (2019). ER-mitochondria communication in cells of the innate immune system. Cells 8(9), 1088.CrossRefGoogle ScholarPubMed
Racedo, SE, Rawe, VY & Niemann, H (2012). Dynamic changes of the Golgi apparatus during bovine in vitro oocyte maturation. Reproduction 143(4), 439–447.CrossRefGoogle ScholarPubMed
Reyes, JM & Ross, PJ (2016). Cytoplasmic polyadenylation in mammalian oocyte maturation. Wiley Interdiscip Rev RNA 7(1), 71–89.CrossRefGoogle ScholarPubMed
Saenz, JB, Sun, WJ, Chang, JW, Li, J, Bursulaya, B, Gray, NS & Haslam, DB (2009). Golgicide A reveals essential roles for GBF1 in Golgi assembly and function. Nat Chem Biol 5(3), 157–165.CrossRefGoogle ScholarPubMed
Salonen, RO (1985). Actions of bronchodilator drugs, glucocorticoid, and their combinations on airways in rats and guinea pigs. Acta Pharmacol Toxicol 57(Suppl 3), 1–38.Google ScholarPubMed
Sirard, MA, Richard, F, Blondin, P & Robert, C (2006). Contribution of the oocyte to embryo quality. Theriogenology 65(1), 126–136.CrossRefGoogle ScholarPubMed
Sun, SC & Kim, NH (2013). Molecular mechanisms of asymmetric division in oocytes. Microsc Microanal 19(4), 883–897.CrossRefGoogle ScholarPubMed
Szul, T, Grabski, R, Lyons, S, Morohashi, Y, Shestopal, S, Lowe, M & Sztul, E (2007). Dissecting the role of the ARF guanine nucleotide exchange factor GBF1 in Golgi biogenesis and protein trafficking. J Cell Sci 120(Pt 22), 3929–3940.CrossRefGoogle ScholarPubMed
van der Linden, L, van der Schaar, HM, Lanke, KH, Neyts, J & van Kuppeveld, FJ (2010). Differential effects of the putative GBF1 inhibitors Golgicide A and AG1478 on enterovirus replication. J Virol 84(15), 7535–7542.CrossRefGoogle ScholarPubMed
Walch, L, Pellier, E, Leng, W, Lakisic, G, Gautreau, A, Contremoulins, V, Verbavatz, JM & Jackson, CL (2018). GBF1 and Arf1 interact with miro and regulate mitochondrial positioning within cells. Sci Rep 8(1), 17121.CrossRefGoogle ScholarPubMed
Wilfling, F, Thiam, AR, Olarte, MJ, Wang, J, Beck, R, Gould, TJ, Allgeyer, ES, Pincet, F, Bewersdorf, J, Farese, RV Jr. & Walther, TC (2014). Arf1/COPI machinery acts directly on lipid droplets and enables their connection to the ER for protein targeting. eLife 3, e01607.CrossRefGoogle ScholarPubMed
Yong, H, Oh, HI, Lee, SH, Cheong, HT, Yang, BK & Park, CK (2017). Treatment of epidermal growth factor (EGF) enhances nuclear maturation of porcine oocytes and stimulates expression of ER/Golgi transport proteins. Dev Reprod 21(2), 131–138.CrossRefGoogle ScholarPubMed
Zeghouf, M, Guibert, B, Zeeh, JC & Cherfils, J (2005). Arf, Sec7 and brefeldin A: A model towards the therapeutic inhibition of guanine nucleotide-exchange factors. Biochem Soc Trans 33(Pt 6), 1265–1268.CrossRefGoogle Scholar
Zhang, CH, Wang, ZB, Quan, S, Huang, X, Tong, JS, Ma, JY, Guo, L, Wei, YC, Ouyang, YC, Hou, Y, Xing, FQ & Sun, QY (2011). GM130, a cis-Golgi protein, regulates meiotic spindle assembly and asymmetric division in mouse oocyte. Cell Cycle 10(11), 1861–1870.CrossRefGoogle ScholarPubMed
Zhang, DX, Li, XP, Sun, SC, Shen, XH, Cui, XS & Kim, NH (2010). Involvement of ER-calreticulin-Ca2+ signaling in the regulation of porcine oocyte meiotic maturation and maternal gene expression. Mol Reprod Dev 77(5), 462–471.CrossRefGoogle ScholarPubMed
Zhao, X, Claude, A, Chun, J, Shields, DJ, Presley, JF & Melancon, P (2006). GBF1, a cis-Golgi and VTCs-localized ARF-GEF, is implicated in ER-to-Golgi protein traffic. J Cell Sci 119(Pt 18), 3743–3753.CrossRefGoogle ScholarPubMed
Zhao, X, Lasell, TK & Melancon, P (2002). Localization of large ADP-ribosylation factor-guanine nucleotide exchange factors to different Golgi compartments: Evidence for distinct functions in protein traffic. Mol Biol Cell 13(1), 119–133.CrossRefGoogle ScholarPubMed