Class VI Unconventional Myosin is Required for Spermatogenesis in<i>Drosophila</i>

Hicks, Jennifer L.; Deng, Wu-Min; Rogat, Aaron D.; Miller, Ken; Bownes, Mary

doi:10.1091/mbc.10.12.4341

Cited by 105 publications

(119 citation statements)

References 23 publications

(28 reference statements)

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“…In regard to sperm individualization, the testes of 19 lncRNA KO mutants, including CR42858 −/− and CR43282 −/− , exhibited defects in coordinated actin cone movement, resulting in poorly aligned or lagging ICs. Similar phenotypes have been reported for the mutants in the genes encoding the testis-specific proteasome subunit Prosα6T, myosin VI, myosin V, and dynein (Hicks et al 1999;Li et al 2004;Mermall et al 2005;Zhong and Belote 2007). It remains to be determined whether these lncRNAs are directly functional in late spermatogenesis or instead play a role in the early spermatogenesis that is only manifest in the late stage.…”

Section: Discussionsupporting

confidence: 58%

Critical roles of long noncoding RNAs in Drosophila spermatogenesis

et al. 2016

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Long noncoding RNAs (lncRNAs), a recently discovered class of cellular RNAs, play important roles in the regulation of many cellular developmental processes. Although lncRNAs have been systematically identified in various systems, most of them have not been functionally characterized in vivo in animal models. In this study, we identified 128 testis-specific Drosophila lncRNAs and knocked out 105 of them using an optimized three-component CRISPR/Cas9 system. Among the lncRNA knockouts, 33 (31%) exhibited a partial or complete loss of male fertility, accompanied by visual developmental defects in late spermatogenesis. In addition, six knockouts were fully or partially rescued by transgenes in a trans configuration, indicating that those lncRNAs primarily work in trans. Furthermore, gene expression profiles for five lncRNA mutants revealed that testis-specific lncRNAs regulate global gene expression, orchestrating late male germ cell differentiation. Compared with coding genes, the testis-specific lncRNAs evolved much faster. Moreover, lncRNAs of greater functional importance exhibited higher sequence conservation, suggesting that they are under constant evolutionary selection. Collectively, our results reveal critical functions of rapidly evolving testis-specific lncRNAs in late Drosophila spermatogenesis.

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Section: Discussionsupporting

confidence: 58%

Critical roles of long noncoding RNAs in Drosophila spermatogenesis

et al. 2016

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“…The latter process involves the formation of a complex machinery bringing together cytoskeleton and membrane remodelling. The only proteins identi¢ed so far as being crucial in this process are myosin VI [13], actin and the coat protein clathrin [37]. This evidence indicates that endocytosis and membrane recycling form an important step during sperm individualisation and provide further support for the proposal that myosin VI works as an endocytic motor.…”

Section: Myosin VI As An Endocytic Motor In Di¡erentiationmentioning

confidence: 68%

Myosin VI, a new force in clathrin mediated endocytosis

2001

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The integrity of the actin cytoskeleton and associated motor proteins are essential for the efficient functioning of clathrin mediated endocytosis at least in polarised cells. Myosin VI, the only motor protein so far identified that moves towards the minus end of actin filaments, is the first motor protein to be shown to associate with clathrin coated pits/vesicles at the plasma membrane and to modulate clathrin mediated endocytosis. Recent kinetic studies suggest that myosin VI may move processively along actin filaments providing clues about its functions in the cell. The possible role(s) of myosin VI in the sequential steps involved in receptor mediated endocytosis are discussed. ß

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“…Although, a later study showed that the F-actin assembly occurs throughout the cone (Noguchi and Miller, 2003). The F-actin cone bundles appeared disrupted in myosin VI homozygous testes (Hicks et al, 1999) and genetic interaction studies showed that myosin VI (jar 1 ) and dynamin (shi ts1 ) could act in parallel pathways to maintain the F-actin levels in these cones (Rogat and Miller, 2002). Because the plasma membrane is not endocytosed at the investment cone, the role of dynamin in this organelle could be limited to F-actin assembly.…”

Section: Introductionmentioning

confidence: 96%

Dynein Light Chain 1 Regulates Dynamin-mediated F-Actin Assembly during Sperm Individualization inDrosophila

Ghosh-Roy

Desai

Ray

2005

MBoC

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Toward the end of spermiogenesis, spermatid nuclei are compacted and the clonally related spermatids individualize to become mature and active sperm. Studies in Drosophila showed that caudal end-directed movement of a microfilamentrich structure, called investment cone, expels the cytoplasmic contents of individual spermatids. F-actin dynamics plays an important role in this process. Here we report that the dynein light chain 1 (DLC1) of Drosophila is involved in two separate cellular processes during sperm individualization. It is enriched around spermatid nuclei during postelongation stages and plays an important role in the dynein-dynactin-dependent rostral retention of the nuclei during this period. In addition, DDLC1 colocalizes with dynamin along investment cones and regulates F-actin assembly at this organelle by retaining dynamin along the cones. Interestingly, we found that this process does not require the other subunits of cytoplasmic dynein-dynactin complex. Altogether, these observations suggest that DLC1 could independently regulate multiple cellular functions and established a novel role of this protein in F-actin assembly in Drosophila. INTRODUCTIONSperm elongation and maturation involves complex choreography of a range of different cytoskeletal events leading to a large-scale alteration of cell shape and bulk membrane movement. One of the unique features of sperm differentiation is the clearing of cytoplasmic contents of spermatids after elongation, which also separates them as individual sperm. It is a key step to form mature and active sperm. Morphogenetic changes associated with sperm individualization have been studied in detail in Drosophila (reviewed by Lindsley and Tokuyasu, 1980). It involves compaction of the nuclei, formation of the microfilament rich investment cones around the nucleus, and extrusion of cytoplasmic contents of each spermatid by a caudal end-directed movement of the investment cone. In comparison, the molecular mechanisms underlying these processes are not so well understood.F-actin and Lamin are the two known cytoskeleton components of investment cone, also known as F-actin cone (Fabrizio et al., 1998;Arama et al., 2003). Pharmacological treatments of isolated cysts established that F-actin dynamics plays a critical role in membrane extraction and F-actin cone movement and that both these processes are microtubule independent (Noguchi and Miller, 2003). F-actin-associated proteins, such as capping protein, cortactin, Arp2/3 complex, and myosin VI, are enriched at the leading edges of F-actin cones, whereas dynamin is localized throughout (Rogat and Miller, 2002), indicating that F-actin assembly would be initiated at the leading edges. Although, a later study showed that the F-actin assembly occurs throughout the cone (Noguchi and Miller, 2003). The F-actin cone bundles appeared disrupted in myosin VI homozygous testes (Hicks et al., 1999) and genetic interaction studies showed that myosin VI (jar 1 ) and dynamin (shi ts1 ) could act in parallel pathways to maintain t...

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Class VI Unconventional Myosin is Required for Spermatogenesis inDrosophila

Cited by 105 publications

References 23 publications

Critical roles of long noncoding RNAs in Drosophila spermatogenesis

Critical roles of long noncoding RNAs in Drosophila spermatogenesis

Myosin VI, a new force in clathrin mediated endocytosis

Dynein Light Chain 1 Regulates Dynamin-mediated F-Actin Assembly during Sperm Individualization inDrosophila

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