The<i>Drosophila</i>SUN protein Spag4 cooperates with the coiled-coil protein Yuri Gagarin to maintain association of the basal body and spermatid nucleus

Kracklauer, Martin P; Wiora, Heather M.; Deery, William J.; Chen, Xin; Bolival, Benjamin; Romanowicz, Dwight; Simonette, Rebecca A.; Fuller, Margaret T.; Fischer, Janice A.; Beckingham, Kathy

doi:10.1242/jcs.066589

Cited by 52 publications

(75 citation statements)

References 57 publications

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“…Double mutants for the only two Drosophila KASH domain proteins Msp-300 and Klarsicht were reported previously to have no defects in nuclear morphology or position in early embryogenesis (Technau and Roth, 2008) Flies encode two SUN domain proteins. Only one of them is expressed in embryos and is encoded by two currently independently annotated genes CG3287 and klaroid (Technau and Roth, 2008), while the other SUN domain protein, Spag4 (Sperm-associated antigen 4, previously known as as Giacomo) is expressed specifically in testis (Kracklauer et al, 2010). We thus looked at embryos from parents homozygous for the hypomorphic allele P{EY2g}CG3287 EY03560 , which phenocopies the rough eye phenotype of a deletion comprising both CG3287 and klaroid (see Fig.…”

Section: Cytoplasmic Dynein Bundles Microtubules At the Nementioning

confidence: 99%

Microtubule-induced nuclear envelope fluctuations control chromatin dynamics in Drosophila embryos

et al. 2011

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Nuclear shape is different in stem cells and differentiated cells and reflects important changes in the mechanics of the nuclear envelope (NE). The current framework emphasizes the key role of the nuclear lamina in nuclear mechanics and its alterations in disease. Whether active stress controls nuclear deformations and how this stress interplays with properties of the NE to control NE dynamics is unclear. We address this in the early Drosophila embryo, in which profound changes in NE shape parallel the transcriptional activation of the zygotic genome. We show that microtubule (MT) polymerization events produce the elementary forces necessary for NE dynamics. Moreover, large-scale NE deformations associated with groove formation require concentration of MT polymerization in bundles organized by Dynein. However, MT bundles cannot produce grooves when the farnesylated inner nuclear membrane protein Kugelkern (Kuk) is absent. Although it increases stiffness of the NE, Kuk also stabilizes NE deformations emerging from the collective effect of MT polymerization forces concentrated in bundles. Finally, we report that MT-induced NE deformations control the dynamics of chromatin and its organization at steady state. Thus, the NE is a dynamic organelle, fluctuations of which increase chromatin dynamics. We propose that such mechanical regulation of chromatin dynamics by MTs might be important for gene regulation.

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Section: Cytoplasmic Dynein Bundles Microtubules At the Nementioning

confidence: 99%

Microtubule-induced nuclear envelope fluctuations control chromatin dynamics in Drosophila embryos

et al. 2011

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“…In mammals, KASH domain proteins are divided into the three major groups by association with actin filaments, microtubules, and intermediate filaments (IF) (Roux and Burke, 2007;Razafsky and Hodzic, 2009;Röper et al, 2002;Wilson and Foisner, 2010). In Drosophila, the nesprin-ortholog MSP-300 associated with actin filaments and Klarsicht associated with microtubules are the known KASH domain proteins (Mosley-Bishop et al, 1999;Starr and Han, 2002), and Klaroid and testis specific Spag4 are the known SUN domain proteins (Kracklauer et al, 2007(Kracklauer et al, , 2010. However, KASH domain deleted MSP-300 alleles and klarsicht, spag4 and klaroid null alleles have been reported not to result in lethality (Mosley-Bishop et al, 1999;Kracklauer et al, 2007Kracklauer et al, , 2010Xie and Fischer, 2008;Technau and Roth, 2008).…”

Section: Tablementioning

confidence: 99%

“…In Drosophila, the nesprin-ortholog MSP-300 associated with actin filaments and Klarsicht associated with microtubules are the known KASH domain proteins (Mosley-Bishop et al, 1999;Starr and Han, 2002), and Klaroid and testis specific Spag4 are the known SUN domain proteins (Kracklauer et al, 2007(Kracklauer et al, , 2010. However, KASH domain deleted MSP-300 alleles and klarsicht, spag4 and klaroid null alleles have been reported not to result in lethality (Mosley-Bishop et al, 1999;Kracklauer et al, 2007Kracklauer et al, , 2010Xie and Fischer, 2008;Technau and Roth, 2008). Further, when the distribution of MSP-300 was studied in wild type and LamC LC58 muscles, it was detected in the sarcomere of both as previously described (Volk, 1992).…”

Section: Tablementioning

confidence: 99%

Loss of Drosophila A-type lamin C initially causes tendon abnormality including disintegration of cytoskeleton and nuclear lamina in muscular defects

Uchino

Nonaka

Horigome

et al. 2013

Developmental Biology

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a b s t r a c tLamins are the major components of nuclear envelope architecture, being required for both the structural and informational roles of the nuclei. Mutations of lamins cause a spectrum of diseases in humans, including muscular dystrophy. We report here that the loss of the A-type lamin gene, lamin C in Drosophila resulted in pupal metamorphic lethality caused by tendon defects, matching the characteristics of human A-type lamin revealed by Emery-Dreifuss muscular dystrophy (EDMD). In tendon cells lacking lamin C activity, overall cell morphology was affected and organization of the spectraplakin family cytoskeletal protein Shortstop which is prominently expressed in tendon cells gradually disintegrated, notably around the nucleus and in a manner correlating well with the degradation of musculature. Furthermore, lamin C null mutants were efficiently rescued by restoring lamin C expression to shortstop-expressing cells, which include tendon cells but exclude skeletal muscle cells. Thus the critical function of A-type lamin C proteins in Drosophila musculature is to maintain proper function and morphology of tendon cells.

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“…Both genes are required for recruitment of dynein-dynactin to the nuclear surface; this pool of dynein probably mediates nucleus-basal body and nucleus-Nebenkern attachments, which are defective in both mutants. Genes encoding Spag4 (a SUN protein), Yuri Gagarin (a coiled-coil protein) and GLD2 [a poly(A) polymerase] are required for nucleus-basal body coupling in spermatids, although it is not known whether they interact with ASUN or LIS-1 in this process (Kracklauer et al, 2010;Sartain et al, 2011;Texada et al, 2008). Our studies suggest that Lis-1, but not asun, is required for proper Nebenkern shaping and Nebenkern-basal body association; these functions might be mediated by dynein/microtubules acting at the Nebenkern surface.…”

Section: Research Articlementioning

confidence: 99%

Regulation of dynein localization and centrosome positioning by Lis-1 and asunder during Drosophila spermatogenesis

et al. 2012

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Dynein, a microtubule motor complex, plays crucial roles in cell-cycle progression in many systems. The LIS1 accessory protein directly binds dynein, although its precise role in regulating dynein remains unclear. Mutation of human LIS1 causes lissencephaly, a developmental brain disorder. To gain insight into the in vivo functions of LIS1, we characterized a male-sterile allele of the Drosophila homolog of human LIS1. We found that centrosomes do not properly detach from the cell cortex at the onset of meiosis in most Lis-1 spermatocytes; centrosomes that do break cortical associations fail to attach to the nucleus. In Lis-1 spermatids, we observed loss of attachments between the nucleus, basal body and mitochondria. The localization pattern of LIS-1 protein throughout Drosophila spermatogenesis mirrors that of dynein. We show that dynein recruitment to the nuclear surface and spindle poles is severely reduced in Lis-1 male germ cells. We propose that Lis-1 spermatogenesis phenotypes are due to loss of dynein regulation, as we observed similar phenotypes in flies null for Tctex-1, a dynein light chain. We have previously identified asunder (asun) as another regulator of dynein localization and centrosome positioning during Drosophila spermatogenesis. We now report that Lis-1 is a strong dominant enhancer of asun and that localization of LIS-1 in male germ cells is ASUN dependent. We found that Drosophila LIS-1 and ASUN colocalize and coimmunoprecipitate from transfected cells, suggesting that they function within a common complex. We present a model in which Lis-1 and asun cooperate to regulate dynein localization and centrosome positioning during Drosophila spermatogenesis.

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TheDrosophilaSUN protein Spag4 cooperates with the coiled-coil protein Yuri Gagarin to maintain association of the basal body and spermatid nucleus

Cited by 52 publications

References 57 publications

Microtubule-induced nuclear envelope fluctuations control chromatin dynamics in Drosophila embryos

Microtubule-induced nuclear envelope fluctuations control chromatin dynamics in Drosophila embryos

Loss of Drosophila A-type lamin C initially causes tendon abnormality including disintegration of cytoskeleton and nuclear lamina in muscular defects

Regulation of dynein localization and centrosome positioning by Lis-1 and asunder during Drosophila spermatogenesis

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