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The dynamic pattern of PLIN3 in pig oocytes and cumulus cells during in vitro maturation

Published online by Cambridge University Press:  13 December 2017

Mingzhu Xu ,
Yaqiong Zeng ,
Daming Chi ,
Linan Si ,
Xiao Qu  and
Juan Li
Mingzhu Xu
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing Weigang No. 1, Jiangsu Province 210095, People's Republic of China
Yaqiong Zeng
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing Weigang No. 1, Jiangsu Province 210095, People's Republic of China
Daming Chi
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing Weigang No. 1, Jiangsu Province 210095, People's Republic of China
Linan Si
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing Weigang No. 1, Jiangsu Province 210095, People's Republic of China
Xiao Qu
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing Weigang No. 1, Jiangsu Province 210095, People's Republic of China
Juan Li*
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing Weigang No. 1, Jiangsu Province 210095, People's Republic of China
*
All correspondence to: College of Animal Science and Technology, Nanjing Agricultural University, Nanjing Weigang No. 1, Jiangsu Province 210095, People's Republic of China. Tel: +86 18994049308. Fax: +86 025 84395314. E-mail: juanli@njau.edu.cn
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Summary

Lipid droplets (LDs) are the main energy resource for porcine preimplantation embryonic development. PLIN3 has been implicated in LD formation and regulation. Therefore, this study aimed to detect the dynamic pattern of PLIN3 in pig oocytes and cumulus cells (CC) during in vitro maturation (IVM), and to determine the relationship between PLIN3 and LD content. IVM with cumulus-enclosed oocytes (CEO), cumulus-denuded oocytes (DO) and the CCs denuded from the corresponding oocytes (DCC) was performed in porcine follicular fluid (PFF) or PFF-free optimized medium. DO and the DCC were cultured together under the same conditions as described above, while the DO was named DTO and the DCC was named DTCC in this group. Firstly, our results revealed LDs distributed widely in oocytes and CC, while the PLIN3 protein coated these LDs and spread out ubiquitously in the cytoplasm. Secondly, not only the mRNA level but also at protein level of PLIN3 in immature naked oocytes (IO) was higher than that in matured CEO, DO and DTO. Although PLIN3 was expressed at lower levels in CC from immature oocytes (ICC), the protein level of PLIN3 was comparably higher in the ECC and DCC groups. The triglyceride (TG) content in CEO and DO was significantly less abundant compared with that in IO. Therefore, our results indicated that co-culturing of oocytes and CC might affect PLIN3 expression levels in CC but not in oocytes. Lipid accumulation in pig oocytes during maturation might be affected by PLIN3 cross-talk between oocytes and CC.

Keywords

Cumulus cellsLipid dropletOocytesPigPLIN3
Type
Research Article
Information
Zygote , Volume 26 , Issue 1 , February 2018 , pp. 40 - 49
Copyright
Copyright © Cambridge University Press 2017 

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References

Aardema, H., Vos, P.L.A.M., Lolicato, F., Roelen, B.A.J., Knijn, H.M., Vaandrager, A.B., Helms, J.B. & Gadella, B.M. (2011). Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol. Reprod. 85, 62–9.CrossRefGoogle ScholarPubMed
Auclair, S., Uzbekov, R., Elis, S., Sanchez, L., Kireev, I., Lardic, L., Dalbies-Tran, R. & Uzbekova, S. (2013). Absence of cumulus cells during in vitro maturation affects lipid metabolism in bovine oocytes. Am. J. Physiol. Endocrinol. Metab. 304, E599–613.Google Scholar
Bickel, P.E., Tansey, J.T. & Welte, M.A. (2009). PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1791, 419–40.Google Scholar
Bijttebier, J., Van, S.A., Meyer, E., Mateusen, B. & Maes, D. (2008). Preovulatory follicular fluid during in vitro maturation decreases polyspermic fertilization of cumulus-intact porcine oocytes in vitro maturation of porcine oocytes. Theriogenology 70, 715–24.Google Scholar
Blanchettemackie, E.J., Dwyer, N.K., Barber, T., Coxey, R.A., Takeda, T., Rondinone, C.M., Theodorakis, J.L., Greenberg, A.S. & Londos, C. (1995). Perilipin is located on the surface-layer of intracellular lipid droplets in adipocytes. J. Lipid Res. 36, 1211–26.Google Scholar
Brasaemle, D.L., Barber, T., Wolins, N.E., Serrero, G., Blanchette Mackie, E.J. & Londos, C. (1997). Adipose differentiation-related protein is an ubiquitously expressed lipid storage droplet-associated protein. J. Lipid Res. 38, 2249–63.Google Scholar
Buccione, R., Schroeder, A.C. &, Eppig, J.J. (1990). Interactions between somatic-cells and germ-cells throughout mammalian oogenesis. Biol. Reprod. 43, 543–7.CrossRefGoogle ScholarPubMed
Bulankina, A.V., Deggerich, A., Wenzel, D., Mutenda, K., Wittmann, J.G., Rudolph, M.G., Burger, K.N.J. & Honing, S. (2009). TIP47 functions in the biogenesis of lipid droplets. J. Cell Biol. 185, 641–55.Google Scholar
Camera, E., Dahlhoff, M., Ludovici, M., Zouboulis, C.C. & Schneider, M.R. (2014). Perilipin 3 modulates specific lipogenic pathways in SZ95 sebocytes. Exp. Dermatol. 23, 759–61.CrossRefGoogle ScholarPubMed
Cetica, P., Pintos, L., Dalvit, G. & Beconi, M. (2002). Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro . Reproduction 124, 675–81.Google Scholar
Covington, J.D., Bajpeyi, S., Moro, C., Tchoukalova, Y.D., Ebenezer, P.J., Burk, D.H., Ravussin, E. & Redman, L.M. (2015). Potential effects of aerobic exercise on the expression of perilipin 3 in the adipose tissue of women with polycystic ovary syndrome: a pilot study. Eur. J. Endocrinol. 172, 47–58.Google Scholar
Dahlhoff, M., Fröhlich, T., Arnold, G.J., Müller, U., Leonhardt, H., Zouboulis, C.C. & Schneider, M.R. (2015). Characterization of the sebocyte lipid droplet proteome reveals novel potential regulators of sebaceous lipogenesis. Exp. Cell Res. 332, 146–55.CrossRefGoogle ScholarPubMed
de Loos, F., van Maurik, P., van Beneden, T. & Kruip, T.A. (1992). Structural aspects of bovine oocyte maturation in vitro . Mol. Reprod. Dev. 31, 208–14.Google Scholar
Diaz, E. & Pfeffer, S.R. (1998). TIP47: A cargo selection device for mannose 6-phosphate receptor trafficking. Cell 93, 433–43.Google Scholar
Dichlberger, A., Schlager, S., Lappalainen, J., Kakela, R., Hattula, K., Butcher, S.J., Schneider, W.J. & Kovanen, P.T. (2011). Lipid body formation during maturation of human mast cells. J. Lipid Res. 52, 2198–208.Google Scholar
Greenberg, A.S., Egan, JJ., Wek, S.A., Moos, M.C. Jr, Londos, C. & Kimmel, A.R. (1993). Isolation of cDNAs for perilipins A and B: sequence and expression of lipid droplet-associated proteins of adipocytes. Biochemistry 90, 12035–9.Google Scholar
Ferguson, E.M. & Leese, H.J. (1999). Triglyceride content of bovine oocytes and early embryos. J. Reprod. Fertil. 116, 373–8.Google Scholar
Ferguson, E.M. & Leese, H.J. (2006). A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo. Dev. Mol. Reprod. Dev. 73, 1195–201.Google Scholar
Geshi, M., Takenouchi, N., Yamauchi, N. & Nagai, T. (2000). Effects of sodium pyruvate in nonserum maturation medium on maturation, fertilization, and subsequent Dev. of bovine oocytes with or without cumulus cells. Biol. Reprod. 63, 1730–4.Google Scholar
Gilchrist, R.B. & Thompson, J.G. (2007). Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro . Theriogenology 67, 6–15.CrossRefGoogle ScholarPubMed
Greenberg, A.S., Egan, J.J., Wek, S.A., Garty, N.B., Blanchettemackie, E.J. & Londos, C. (1991). Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets. J. Biol. Chem. 266, 11341–6.Google Scholar
Homa, S.T., Racowsky, C. & McGaughey, R.W. (1986). Lipid analysis of immature pig oocytes. J. Reprod. Fertil. 77, 425–34.Google Scholar
Hyttel, P., Callesen, H. & Greve, T. (1986). Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J. Reprod. Fertil. 76, 645–56.CrossRefGoogle ScholarPubMed
Kim, J.Y., Kinoshita, M., Ohnishi, M. & Fukui, Y. (2001). Lipid and fatty acid analysis of fresh and frozen–thawed immature and in vitro matured bovine oocytes. Reproduction 122, 131–8.Google Scholar
Loewenstein, J.E. & Cohen, A.I. (1964). Dry mass, lipid content and protein content of the intact and zona-free mouse ovum. J. Embryol. Exp. Morphol. 12, 113–21.Google Scholar
Lolicato, F., Brouwers, J.F., van de Lest, C.H.A., Wubbolts, R., Aardema, H., Priore, P., Roelen, B.A.J., Helms, J.B. & Gadella, B.M. (2015). The cumulus cell layer protects the bovine maturing oocyte against fatty acid-induced lipotoxicity. Biol. Reprod. 92, 16.Google Scholar
Ouandaogo, Z.G., Haouzi, D., Assou, S., Dechaud, H., Kadoch, I.J., De Vos, J. & Hamamah, S. (2011). Human cumulus cells molecular signature in relation to oocyte nuclear maturity stage. PLoS One 6, e27179.CrossRefGoogle ScholarPubMed
McEvoy, T.G., Coull, G.D., Broadbent, P.J., Hutchinson, J.S. & Speake, B.K. (2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod.Fig Fertil. 118, 163–70.Google Scholar
Murphy, D.J. (2001). The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Progr. Lipid Res. 40, 325–438.CrossRefGoogle ScholarPubMed
Prates, E.G., Marques, C.C., Baptista, M.C., Vasques, M.I., Carolino, N., Horta, A.E, Charneca, R., Nunes, J.T. & Pereira, R.M. (2013). Fat area and lipid droplet morphology of porcine oocytes during in vitro maturation with trans-10, cis-12 conjugated linoleic acid (t10, c12 CLA). and forskolin. Animal 7, 602–9.Google Scholar
Prates, E.G., Nunes, J.T. & Pereira, R.M. (2014). A role of lipid metabolism during cumulus–oocyte complex maturation: impact of lipid modulators to improve embryo production. Mediators Inflamm. 2014, 692067.Google Scholar
Sastre, D., da Costa, N.N., de Sa, A.L.A., Conceicao, S.D.B., Chiaratti, M.R., Adona, P.R., Guemra, S., Meirelles, F.V., Santos, S.D.D., Sena, L., Ohashi, O.M., dos Santos, E.J.M. & Miranda, M.D. (2014). Expression of PLIN2 and PLIN3 during oocyte maturation and early embryo development in cattle. Theriogenology 81, 326–31.CrossRefGoogle ScholarPubMed
Schweiger, M. & Zechner, R. (2015). Breaking the barrier-chaperone-mediated autophagy of perilipins regulates the lipolytic degradation of fat. Cell Metab. 22, 60–1.Google Scholar
Skinner, J.R., Shew, T.M., Schwartz, D.M., Tzekov, A., Lepus, C.M., Abumrad, N.A. & Wolins, N.E. (2009). Diacylglycerol enrichment of endoplasmic reticulum or lipid droplets recruits perilipin 3/TIP47 during lipid storage and mobilization. J. Biol. Chem. 284, 30941–8.Google Scholar
Straub, B.K. (2015). Lipid droplet-associated proteins. Importance in steatosis, steatohepatitis and hepatocarcinogenesis. Pathologe 36, 146–52.Google Scholar
Sturmey, R.G. & Leese, H.J. (2003). Energy metabolism in pig oocytes and early embryos. Reproduction 126, 197–204.Google Scholar
Sturmey, R.G., O'Toole, P.J. & Leese, H.J. (2006). Fluorescence resonance energy transfer analysis of mitochondrial: lipid association in the porcine oocyte. Reproduction 132, 829–37.Google Scholar
Su, Y.Q., Sugiura, K., Wigglesworth, K., O'Brien, M.J., Affourtit, J.P., Pangas, S.A., Matzuk, M.M. & Eppig, J.J. (2008). Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 135, 111–21.Google Scholar
Sutton, M.L., Gilchrist, R.B. & Thompson, J.G. (2003). Effect of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity. Hum. Reprod. 9, 35–48.Google Scholar
Tanghe, S., Van Soom, A., Nauwynck, H., Coryn, M. & De Kruif, A. (2002). Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol. Reprod. Dev. 61, 414–24.Google Scholar
Tatemoto, H., Sakurai, N. & Muto, N. (2000). Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol. Reprod. 63, 805–10.Google Scholar
Thompson, J.G., Lane, M. & Gilchrist, R.B. (2007). Metabolism of the bovine cumulus–oocyte complex and influence on subsequent developmental competence. Soc. Reprod. Fertil. Suppl. 64, 179–90.Google Scholar
Walther, T.C. & Farese, R.V. Jr. (2009). The life of lipid droplets. Biochim. Biophys. Acta 1791, 459–66.Google Scholar
Wolins, N.E., Rubin, D. & Brasaemle, D.L. (2001). TIP47 associates with lipid droplets. J. Biol. Chem. 276, 5101–8.CrossRefGoogle ScholarPubMed
Wolins, N.E., Skinner, J.R., Schoenfish, M.J., Tzekov, A., Bensch, K.G. & Bickel, P.E. (2003). Adipocyte protein S3–12 coats nascent lipid droplets. J. Biol. Chem. 278, 37713–21.Google Scholar
Wolins, N.E., Quaynor, B.K., Skinner, J.R., Schoenfish, M.J., Tzekov, A. & Bickel, P. (2005). S3–12, adipophilin, and TIP47 package lipid in adipocytes. J. Biol. Chem. 280, 19146–55.Google Scholar
Wolins, N.E., Brasaemle, D.L. & Bickel, P.E. (2006). A proposed model of fat packaging by exchangeable lipid droplet proteins. FEBS Lett. 580, 5484–91.Google Scholar
Yang, X., Dunning, K.R., Wu, L.L.Y., Hickey, T.E., Norman, R.J., Russell, D.L., Liang, X.Y. & Robker, R.L. (2010). Identification of Perilipin-2 as a lipid droplet protein regulated in oocytes during maturation. Reprod. Fertil. Dev. 22, 1262–71.Google Scholar