The initiation of spermiogenesis in the nematode Caenorhabditis elegans

Ward, Samuel; Hogan, Eileen; Nelson, Gregory A.

doi:10.1016/0012-1606(83)90336-6

Cited by 136 publications

(143 citation statements)

References 19 publications

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“…Mating activates male sperm to form a lamellipodium (10). We revealed the same two modes of movement in vivo as observed for extruded, pronase-activated cells, i.e., crawling cells and active, but stationary cells, indicating that this latter behavior was physiologically relevant (Movie S2).…”

Section: Resultssupporting

confidence: 75%

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Membrane tension regulates motility by controlling lamellipodium organization

Batchelder

Hollopeter

Campillo

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

135

114

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Many cell movements proceed via a crawling mechanism, where polymerization of the cytoskeletal protein actin pushes out the leading edge membrane. In this model, membrane tension has been seen as an impediment to filament growth and cell motility. Here we use a simple model of cell motility, the Caenorhabditis elegans sperm cell, to test how membrane tension affects movement and cytoskeleton dynamics. To enable these analyses, we create transgenic worm strains carrying sperm with a fluorescently labeled cytoskeleton. Via osmotic shock and deoxycholate treatments, we relax or tense the cell membrane and quantify apparent membrane tension changes by the membrane tether technique. Surprisingly, we find that membrane tension reduction is correlated with a decrease in cell displacement speed, whereas an increase in membrane tension enhances motility. We further demonstrate that apparent polymerization rates follow the same trends. We observe that membrane tension reduction leads to an unorganized, rough lamellipodium, composed of short filaments angled away from the direction of movement. On the other hand, an increase in tension reduces lateral membrane protrusions in the lamellipodium, and filaments are longer and more oriented toward the direction of movement. Overall we propose that membrane tension optimizes motility by streamlining polymerization in the direction of movement, thus adding a layer of complexity to our current understanding of how membrane tension enters into the motility equation. I n crawling cells, motility is mainly driven by actin polymerization, which forms filaments beneath the leading edge cell membrane to make protrusions (1). In this scenario, polymerization is inhibited by the presence of the cell membrane, and membrane tension is thus commonly seen as an impediment to cell motility (2). Experiments show that lamellipodial extension rate is indeed inversely correlated with membrane tension (3), but steady-state, whole cell translocation has not been studied. Here we use a simplified system of crawling cell motility, the Caenorhabditis elegans sperm cell, in order to address the question of how membrane tension affects whole cell translocation. The sperm cell contains only cytoskeleton, mitochondria, and nuclear material and is incapable of de novo protein synthesis or classical exo-and endocytosis, thus representing a useful model for exploring the interplay between membrane tension and cell motility. The sperm cell translocates by adhering to the substrate and emitting a dynamic lamellipodia, in a manner that is morphologically similar to actomyosin containing motile cells, despite the fact that the movement of sperm cells is powered by the dynamics of the major sperm protein (MSP) cytoskeleton in the absence of actin and known molecular motors (4, 5).The production of fluorescently labeled actin in living cells was a watershed in the understanding of how actin structures assemble, flow, and disassemble to produce cell motility. However, due to efficient gene silencing mechanisms in th...

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Section: Resultssupporting

confidence: 75%

“…1A). When extruded from male worms and activated by pronase digestion to form lamellipodia (10), strains carrying the spe-11 promotor gave sperm cells with fluorescent lamellipodia that were mottled in appearance, whereas fluorescence was dim and diffuse in the cell body (Fig. 1B).…”

Section: Resultsmentioning

confidence: 99%

Membrane tension regulates motility by controlling lamellipodium organization

Batchelder

Hollopeter

Campillo

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

135

114

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“…In hermaphrodites, spermiogenesis occurs in the spermatheca, and in males, it occurs when sperm mixes with seminal fluid during ejaculation into the hermaphrodite during copulation (20). Sperm activation appears to involve cation in-http://bmbreports.org BMB reports flux, pH elevation, and intracellular Ca 2+ release (20)(21)(22)(23)(24). Mature sperm must crawl towards the spermatheca and maintain their position in the reproductive tract while eggs are ovulated into the spermatheca.…”

Section: Elegans As a Model Organismmentioning

confidence: 99%

“…In spermatids, SPE-38 is found in sperm vesicles called the membranous organelles (MOs) (36). The MOs fuse with the plasma membrane during spermiogenesis, and, upon fusion, SPE-38 is released to the cell surface and then redistributed to the pseudopod, resulting in a similar localization pattern as that of SPE-9 (22,(36)(37)(38).…”

Section: Fertilizationmentioning

confidence: 99%

Fertilization and the oocyte-to-embryo transition in C. elegans

Marcello¹,

Singson²

2010

BMB Reports

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Fertilization is a complex process comprised of numerous steps. During fertilization, two highly specialized and differentiated cells (sperm and egg) fuse and subsequently trigger the development of an embryo from a quiescent, arrested oocyte. Molecular interactions between the sperm and egg are necessary for regulating the developmental potential of an oocyte, and precise coordination and regulation of gene expression and protein function are critical for proper embryonic development. The nematode Caenorhabditis elegans has emerged as a valuable model system for identifying genes involved in fertilization and the oocyte-to-embryo transition as well as for understanding the molecular mechanisms that govern these processes. In this review, we will address current knowledge of the molecular underpinnings of gamete interactions during fertilization and the oocyte-to-embryo transition in C. elegans. We will also compare our knowledge of these processes in C. elegans to what is known about similar processes in mammalian, specifically mouse, model systems. [BMB reports 2010; 43(6): 389-399]

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“…Nematode spermatids can be activated in Ca 2+ -free medium (Movie S2) (Ward et al, 1983;Washington and Ward, 2006), indicating that the [Ca 2+ ] i increase might be caused by Ca 2+ release from intracellular store. Ca 2+ oscillations are primarily regulated by IP 3 R (Berridge, 2007), which can be activated by inositol (1,4,5)-trisphosphate (IP 3 ) generated through cleavage of phosphatidylinositol 4,5-bisphosphate (PIP 2 ) by PLC in a variety of cell types (Berridge, 2007).…”

Section: Introductionmentioning

confidence: 99%

Cytosolic Ca2+ as a multifunctional modulator is required for spermiogenesis inAscaris suum

et al. 2013

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The dynamic polar polymers actin fi laments and microtubules are usually employed to provide the structural basis for establishing cell polarity in most eukaryotic cells. Radially round and immotile spermatids from nematodes contain almost no actin or tubulin, but still have the ability to break symmetry to extend a pseudopod and initiate the acquisition of motility powered by the dynamics of cytoskeleton composed of major sperm protein (MSP) during spermiogenesis (sperm activation). However, the signal transduction mechanism of nematode sperm activation and motility acquisition remains poorly understood. Here we show that Ca 2+ oscillations induced by the Ca 2+ release from intracellular Ca 2+ store through inositol (1,4,5)-trisphosphate receptor are required for Ascaris suum sperm activation. The chelation of cytosolic Ca 2+ suppresses the generation of a functional pseudopod, and this suppression can be relieved by introducing exogenous Ca 2+ into sperm cells. Ca 2+ promotes MSP-based sperm motility by increasing mitochondrial membrane potential and thus the energy supply required for MSP cytoskeleton assembly. On the other hand, Ca 2+ promotes MSP disassembly by activating Ca 2+ /calmodulin-dependent serine/threonine protein phosphatase calcineurin. In addition, Ca 2+ /camodulin activity is required for the fusion of sperm-specifi c membranous organelle with the plasma membrane, a regulated exocytosis required for sperm motility. Thus, Ca 2+ plays multifunctional roles during sperm activation in Ascaris suum.

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The initiation of spermiogenesis in the nematode Caenorhabditis elegans

Cited by 136 publications

References 19 publications

Membrane tension regulates motility by controlling lamellipodium organization

Membrane tension regulates motility by controlling lamellipodium organization

Fertilization and the oocyte-to-embryo transition in C. elegans

Cytosolic Ca2+ as a multifunctional modulator is required for spermiogenesis inAscaris suum

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