Maelstrom coordinates microtubule organization during <i>Drosophila</i> oogenesis through interaction with components of the MTOC

Sato, Kaoru; Nishida, Kazumichi M.; Shibuya, Aoi; Siomi, Mikiko C.; Siomi, Haruhiko

doi:10.1101/gad.174110.111

Cited by 103 publications

(141 citation statements)

References 88 publications

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“…Interestingly, loss of Maelstrom (Mael), a high-mobility group box protein that regulates microtubule organization leads to egg chambers with cell division defects but also results in an encapsulation defect with misplaced oocytes that is similar to the one observed in nost;;cip4 double mutants (Sato et al, 2011). Mael forms a complex with the components of the microtubuleorganizing center (MTOC) -including centrosomin and c-tubulin, which seems to be required not only for early oocyte determination but also egg chamber packing and oocyte positioning in the germarium.…”

Section: Discussionmentioning

confidence: 99%

Cooperative functions of the two F-BAR proteins Cip4 and Nostrin in regulating E-cadherin in epithelial morphogenesis

Zobel

Brinkmann

Koch

et al. 2014

Journal of Cell Science

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There was an error published in J. Cell Sci. 128, 499-515.On p. 507 of this article, the legend of Fig. 6 contained an incomplete description of panel B.The correct sentence should read: (B) Wild type stage 4 egg chamber stained for Armadillo and E-cadherin; arrowhead indicates apical E-cadherin localization in follicle cells. We apologise to the readers for any confusion that this error might have caused.

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Section: Discussionmentioning

confidence: 99%

Cooperative functions of the two F-BAR proteins Cip4 and Nostrin in regulating E-cadherin in epithelial morphogenesis

Zobel

Brinkmann

Koch

et al. 2014

Journal of Cell Science

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“…Imaging was with a Leica TCS-SP2 confocal microscope. Mouse anti-α-tubulin DM1A staining of ovaries is described by Sato et al (Sato et al, 2011) and EB1 staining by Sanghavi et al (Sanghavi et al, 2012).…”

Section: Immunostainingmentioning

confidence: 99%

Clathrin heavy chain plays multiple roles in polarizing the Drosophila oocyte downstream of Bic-D

et al. 2014

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Bicaudal-D (Bic-D), Egalitarian (Egl), microtubules and their motors form a transport machinery that localizes a remarkable diversity of mRNAs to specific cellular regions during oogenesis and embryogenesis. Bic-D family proteins also promote dynein-dependent transport of Golgi vesicles, lipid droplets, synaptic vesicles and nuclei. However, the transport of these different cargoes is still poorly understood. We searched for novel proteins that either mediate Bic-Ddependent transport processes or are transported by them. Clathrin heavy chain (Chc) co-immunopurifies with Bic-D in embryos and ovaries, and a fraction of Chc colocalizes with Bic-D. Both proteins control posterior patterning of the Drosophila oocyte and endocytosis. Although the role of Chc in endocytosis is well established, our results show that Bic-D is also needed for the elevated endocytic activity at the posterior of the oocyte. Apart from affecting endocytosis indirectly by its role in osk mRNA localization, Bic-D is also required to transport Chc mRNA into the oocyte and for transport and proper localization of Chc protein to the oocyte cortex, pointing to an additional, more direct role of Bic-D in the endocytic pathway. Furthermore, similar to Bic-D, Chc also contributes to proper localization of osk mRNA and to oocyte growth. However, in contrast to other endocytic components and factors of the endocytic recycling pathway, such as Rabenosyn-5 (Rbsn-5) and Rab11, Chc is needed during early stages of oogenesis (from stage 6 onwards) to localize osk mRNA correctly. Moreover, we also uncovered a novel, presumably endocytosis-independent, role of Chc in the establishment of microtubule polarity in stage 6 oocytes.

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“…Rabbit anti P-MAD (anti-phosphorylated Smad1, PS1) used at 1:3500 was given to us by N. Yakoby (Rutgers University, Camden, NJ, USA) (Persson et al, 1998;Niepielko et al, 2011). Monoclonal mouse antiMael (1:200), anti-Armi (1:200) and anti-Piwi (1:500) were a gift from M. C. Siomi (University of Tokyo, Tokyo, Japan) (Saito et al, 2006;Sato et al, 2011). Polyclonal rabbit anti-Aub (1:2000); anti-AGO3 (1:250) and antiPiwi (1:500) were from T. Schupbach (Princeton University, Princeton, NJ, USA) and G. Hannon (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA) (Brennecke et al, 2007).…”

Section: Antibodies and Microscopymentioning

confidence: 99%

“…Co-immunoprecipitation with monoclonal mouse anti-Mael and anti-Piwi antibody (Saito et al, 2006;Sato et al, 2011) was performed in the presence of RNase inhibitor RNaseOUT (Invitrogen) as previously described (Brennecke et al, 2007). Ovaries from 50 young flies (<20 hours old) were used for each experiment.…”

Section: Co-immunoprecipitationmentioning

confidence: 99%

Zfrp8/PDCD2is required in ovarian stem cells and interacts with the piRNA pathway machinery

2014

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The maintenance of stem cells is central to generating diverse cell populations in many tissues throughout the life of an animal. Elucidating the mechanisms involved in how stem cells are formed and maintained is crucial to understanding both normal developmental processes and the growth of many cancers. Previously, we showed that Zfrp8/PDCD2 is essential for the maintenance of Drosophila hematopoietic stem cells. Here, we show that Zfrp8/PDCD2 is also required in both germline and follicle stem cells in the Drosophila ovary. Expression of human PDCD2 fully rescues the Zfrp8 phenotype, underlining the functional conservation of Zfrp8/PDCD2. The piRNA pathway is essential in early oogenesis, and we find that nuclear localization of Zfrp8 in germline stem cells and their offspring is regulated by some piRNA pathway genes. We also show that Zfrp8 forms a complex with the piRNA pathway protein Maelstrom and controls the accumulation of Maelstrom in the nuage. Furthermore, Zfrp8 regulates the activity of specific transposable elements also controlled by Maelstrom and Piwi. Our results suggest that Zfrp8/PDCD2 is not an integral member of the piRNA pathway, but has an overlapping function, possibly competing with Maelstrom and Piwi. KEY WORDS: Somatic stem cells, Germline stem cells, piRNA pathway, Drosophila INTRODUCTIONGene expression in multicellular organisms is regulated at many levels. Complex transcriptional control is followed by processing, transport and translation of all mRNAs. Small RNAs function in all of these steps by guiding the regulatory protein complexes to specific RNA and DNA targets. One class of small RNAs is the repeat-associated small interfering RNAs (rasi-RNAs) or, more commonly, Piwi-interacting RNAs (piRNAs) (Saito et al., 2006;Vagin et al., 2006; Brennecke et al., 2007). These 23-31 nt small RNAs are produced by Dicer-independent mechanisms and associate with Piwi family Argonaute (AGO) proteins. Both RNAs and protein components of the piRNA pathway are most abundantly expressed in the gonads of all animals, but recent studies suggest that the pathway may similarly function in other somatic stem and progenitor cells (reviewed by Juliano et al., 2011;Siddiqi and Matushansky, 2012;Mani and Juliano, 2013;Peng and Lin, 2013).Much of the progress in understanding piRNA pathway mechanisms comes from Drosophila ovaries, where piRNAs suppress the activity of transposable elements (TEs) and protect genome integrity during germ stem cell (GSC) differentiation and oocyte development (reviewed by Siomi et al., 2011;Guzzardo et al., 2013;Peng and Lin, 2013). Different sets of TEs are active in the ovarian germline and surrounding somatic cells and are regulated by piRNA mechanisms that partially overlap (Malone et al., 2009). The pathway used in the somatic cells is called the primary piRNA processing pathway. The primary single-stranded RNAs are transcribed from piRNA clusters and exported into the cytoplasm. Their maturation requires the RNA helicase Armitage (Armi) (Klattenhoff et al., 2007...

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Maelstrom coordinates microtubule organization during Drosophila oogenesis through interaction with components of the MTOC

Cited by 103 publications

References 88 publications

Cooperative functions of the two F-BAR proteins Cip4 and Nostrin in regulating E-cadherin in epithelial morphogenesis

Cooperative functions of the two F-BAR proteins Cip4 and Nostrin in regulating E-cadherin in epithelial morphogenesis

Clathrin heavy chain plays multiple roles in polarizing the Drosophila oocyte downstream of Bic-D

Zfrp8/PDCD2is required in ovarian stem cells and interacts with the piRNA pathway machinery

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