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Expression of XNOA 36 in the mitochondrial cloud of Xenopus laevis oocytes

Published online by Cambridge University Press:  15 April 2011

M.C. Vaccaro ,
M. Wilding ,
B. Dale ,
C. Campanella  and
R. Carotenuto
M.C. Vaccaro
Affiliation:
Department of Structural and Functional Biology, University of Naples ‘Federico II’, Italy.
M. Wilding
Affiliation:
Centre for Assisted Fertilization, Clinica Villa del Sole, Naples, Italy.
B. Dale
Affiliation:
Centre for Assisted Fertilization, Clinica Villa del Sole, Naples, Italy.
C. Campanella
Affiliation:
Department of Structural and Functional Biology, University of Naples ‘Federico II’, Italy.
R. Carotenuto*
Affiliation:
Department of Structural and Functional Biology. University of Naples Federico II. Complesso Universitario Monte Sant'Angelo, Via Cinthia, I-80126, Napoli, Italy.
*
All correspondence to: Rosa Carotenuto, Department of Structural and Functional Biology. University of Naples Federico II. Complesso Universitario Monte Sant'Angelo, Via Cinthia, I-80126, Napoli, Italy. Tel: +39 081 679195. Fax: +39 081 679233. e-mail: rosa.carotenuto@unina.it
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Summary

In Xenopus laevis oocytes a mitochondrial cloud (MC) is found between the nucleus and the plasma membrane at stages I–II of oogenesis. The MC contains RNAs that are transported to the future vegetal pole at stage II of oogenesis. In particular, germinal plasm mRNAs are found in the Message Transport Organiser (METRO) region, the MC region opposite to the nucleus. At stages II–III, a second pathway transports Vg1 and VegT mRNAs to the area where the MC content merges with the vegetal cortex. Microtubules become polarized at the sites of migration of Vg1 and VegT mRNAs through an unknown signalling mechanism. In early meiotic stages, the centrioles are almost completely lost with their remnants being dispersed into the cytoplasm and the MC, which may contain a MTOC to be used in the later localization pathway of the mRNAs. In mammals, XNOA 36 encodes a member of a highly conserved protein family and localises to the nucleolus or in the centromeres. In the Xenopus late stage I oocyte, XNOA 36 mRNA is transiently segregated in one half of the oocyte, anchored by a cytoskeletal network that contains spectrin. Here we found that XNOA 36 transcript also localises to the nucleoli and in the METRO region. XNOA 36 protein immunolocalization, using an antibody employed for the library immunoscreening that depicted XNOA 36 expression colonies, labels the migrating MC, the cytoplasm of stage I oocytes and in particular the vegetal cortex facing the MC. The possible role of XNOA 36 in mRNA anchoring to the vegetal cortex or in participating in early microtubule reorganization is discussed.

Keywords

CytoskeletonMicrotubulesMitochondrial cloudOocyteXenopus laevis
Type
Research Article
Information
Zygote , Volume 20 , Issue 3 , August 2012 , pp. 237 - 242
Copyright
Copyright © Cambridge University Press 2011

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References

Alarcon, V.B. & Elinson, R.P. (2001). RNA anchoring in the vegetal cortex of the Xenopus oocyte. J. Cell Sci. 114, 1731–41.CrossRefGoogle ScholarPubMed
Bolivar, J., Diaz, I., Iglesias, C. & Valdivia, M. (1999). Molecular cloning of a zinc finger autoantigen transiently associated with interphase nucleolus and mitotic centromeres and midbodies. J. Biol. Chem. 274, 36456–64.CrossRefGoogle ScholarPubMed
Chang, P., Torres, J., Lewis, R.A., Mowry, K.L., Houliston, E. & King, M.L. (2004). Localization of RNAs to the mitochondrial cloud in Xenopus laevis oocytes through entrapment and association with endoplasmic reticulum. Mol. Biol. 15, 4669–81.Google Scholar
de Melo, I.S., Iglesias, C., Benítez-Rondán, A., Medina, F., Martínez-Barberá, J.P. & Bolívar, J. (2009). NOA36/ZNF330 is a conserved cystein-rich protein with proapoptotic activity in human cells. Biochim. Biophys. Acta. 12, 1876–85.CrossRefGoogle Scholar
Dumont, J.N. (1972). Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J. Morph. 136, 153–80.CrossRefGoogle ScholarPubMed
Gard, D.L. (1995). Axis formation during amphibian oogenesis: revaluating the role of the cytoskeleton. Curr. Top. Dev. Biol. 30, 215–52.Google Scholar
Gard, D.L. (1999). Confocal microscopy and 3-D reconstruction of the cytoskeleton of Xenopus oocytes. Micro. Res. Tech. 44, 388–414.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Gard, D.L., Cha, B.-J. & King, E. (1997). The organization and animal–vegetal asymmetry of cytokeratin filaments in stage VI Xenopus oocytes is dependent upon F-actin and microtubules. Dev. Biol. 184, 95–114.CrossRefGoogle ScholarPubMed
Heasman, J., Quarmby, J. & Wylie, C.C. (1984). The mitochondrial cloud of Xenopus oocytes: the source of germinal granule material. Dev. Biol. 105, 458–69.CrossRefGoogle ScholarPubMed
Houston, D.W. & King, M.L. (2000). Germ plasm and molecular determinants of germ cell fate. In: Current Topics in Developmental Biology (eds Peterson, R. & Schatten, G.) pp. 155–182. New York: Academic Press.Google Scholar
King, M.L., Messit, T.J. & Mowry, K.L. (2005). Putting RNAs in the right place at the right time: RNA localization in the frog oocyte. Biol. Cell. 97, 19–33.CrossRefGoogle Scholar
Kloc, M., & Etkin, L.D. (1998). Apparent continuity between the messenger transport organizer and late RNA localization pathways during oogenesis in Xenopus. Mech. Dev. 73, 95–106.CrossRefGoogle ScholarPubMed
Kloc, M., Larabell, C. & Ettkin, L.D. (1996). Elaboration of the messenger transport organiser pathway for localisation of RNA to the vegetal cortex of Xenopus oocytes. Dev. Biol. 180, 119–30.CrossRefGoogle Scholar
Kloc, M., Bilinski, S., Dougherty, M.T., Brey, E.M. & Ettkin, L.D. (2004). Formation, architecture and polarity of female germline cyst in Xenopus. Dev. Biol. 266, 43–61.CrossRefGoogle ScholarPubMed
Klymkowsky, M.W., Maynell, L.A. & Polson, A.G. (1987). Polar asymmetry in the organization of the cortical cytokeratin system of Xenopus laevis oocytes and embryos. Development 100, 543–57.CrossRefGoogle ScholarPubMed
Kress, T.L., Yoon, Y.J. & Mowry, K.L. (2004). Nuclear RNP complex assembly initiates cytoplasmic RNA localization. J. Cell Biol. 165, 203–11.CrossRefGoogle ScholarPubMed
Ku, M. & Melton, D.A. (1993). Xwnt11: a maternally expressed wnt gene. Development 119, 1161–73.CrossRefGoogle ScholarPubMed
MacArthur, H., Houston, D.W., Bubunenko, M., Mosquera, L. & King, M.L. (2000). DEADSouth is a germ plasm specific DEAD-box RNA helicase in Xenopus related to eIF4A. Mech. Dev. 95, 291–5.CrossRefGoogle ScholarPubMed
Mosquera, L., Forristall, C., Zhou, Y. & King, M.L. (1993). An mRNA localized to the vegetal cortex encodes a protein with a nanos-like zinc finger domain. Development 117, 377–86.CrossRefGoogle Scholar
Neuman-Silberberg, F.S. & Schüpbach, T. (1996). The Drosophila TGF-alpha-like protein Gurken: expression and cellular localization during Drosophila oogenesis. Mech. Dev. 59, 105–13.CrossRefGoogle ScholarPubMed
Nilson, T.L.A. & Schüpbach, T. (1999). EGF receptor signaling in Drosophila oogenesis. Curr. Top. Dev. Biol. 44, 203–43.CrossRefGoogle ScholarPubMed
Roth, S. (2003). The origin of dorsoventral polarity in Drosophila. Phil. Trans. R. Soc. Lond. B Biol. Sci. 358, 1317–29.CrossRefGoogle ScholarPubMed
Schüpbach, T. & Wieschaus, E. (1986). Germline autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila. Dev. Biol. 113, 443–8.CrossRefGoogle ScholarPubMed
Tao, Q., Yokota, C., Puck, H., Kofron, M., Birsoy, B., Yan, D., Asashima, M., Wylie, C.C. & Heasman, J. (2005). Maternal Wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos. Cell 120, 857–71.CrossRefGoogle ScholarPubMed
Thomsen, G.H. & Melton, D.A. (1993). Processed Vg1 protein is an axial mesoderm inducer in Xenopus. Cell 74, 433–41.CrossRefGoogle ScholarPubMed
Vaccaro, M.C, De Santo, M.G, Caputo, M., Just, M., Tian, J.D., Gong, H., Lennarz, W.J. & Campanella, C. (2001). Primary structure and developmental expression of DP ZP2, a vitelline envelope glycoprotein homolog to ZP2, in Discoglossus pictus, one of the oldest living anuran species. Mol. Rep. Dev. 59, 133–43.CrossRefGoogle ScholarPubMed
Vaccaro, M.C., Gigliotti, S., Graziani, F., Carotenuto, R., De Angelis, C., Tussellino, M. & Campanella., C. (2010). A transient asymmetry of XNOA 36 mRNA and associated spectrin network bisects stage I oocytes along the future A/V axis in Xenopus laevis. Eur. J. Cell Biol. 89, 525–36.CrossRefGoogle Scholar
Yisraeli, J.K., Sokol, S. & Melton, D.A. (1990). A two-step model for the localization of maternal mRNA in Xenopus oocytes: involvement of microtubules and microfilaments in the translocation and anchoring of Vg1 mRNA. Development 108, 289–98.CrossRefGoogle ScholarPubMed
Wilding, M., Carotenuto, R., Infante, V., Dale, B., Marino, M., Di Matteo, L., Campanella, C. (2001). Confocal analysis of the activity of mitochondria contained within the ‘mitochondrial cloud’ during oogenesis of Xenopus laevis. Zygote 9, 347–52.CrossRefGoogle ScholarPubMed
Zhang, J., Houston, D. W., King, M. L., Payne, C., Wylie, C. & Heasman, L. (1998). The role of maternal VegT in establishing the primary germ layers in Xenopus embryos. Cell 94, 515–24.CrossRefGoogle ScholarPubMed