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Biochemical Society Transactions Aug 2018Two classes of dynein power long-distance cargo transport in different cellular contexts. Cytoplasmic dynein-1 is responsible for the majority of transport toward... (Review)
Review
Two classes of dynein power long-distance cargo transport in different cellular contexts. Cytoplasmic dynein-1 is responsible for the majority of transport toward microtubule minus ends in the cell interior. Dynein-2, also known as intraflagellar transport dynein, moves cargoes along the axoneme of eukaryotic cilia and flagella. Both dyneins operate as large ATP-driven motor complexes, whose dysfunction is associated with a group of human disorders. But how similar are their mechanisms of action and regulation? To examine this question, this review focuses on recent advances in dynein-1 and -2 research, and probes to what extent the emerging principles of dynein-1 transport could apply to or differ from those of the less well-understood dynein-2 mechanoenzyme.
Topics: Adenosine Triphosphate; Axoneme; Cilia; Cytoplasm; Dyneins; Protein Transport
PubMed: 30065109
DOI: 10.1042/BST20170568 -
Cytoskeleton (Hoboken, N.J.) Aug 2018Ciliary and flagellar motility is caused by the ensemble action of inner and outer dynein arm motors acting on axonemal doublet microtubules. The switch point or...
Ciliary and flagellar motility is caused by the ensemble action of inner and outer dynein arm motors acting on axonemal doublet microtubules. The switch point or switching hypothesis, for which much experimental and computational evidence exists, requires that dyneins on only one side of the axoneme are actively working during bending, and that this active motor region propagate along the axonemal length. Generation of a reverse bend results from switching active sliding to the opposite side of the axoneme. However, the mechanochemical states of individual dynein arms within both straight and curved regions and how these change during beating has until now eluded experimental observation. Recently, Lin and Nicastro used high-resolution cryo-electron tomography to determine the power stroke state of dyneins along flagella of sea urchin sperm that were rapidly frozen while actively beating. The results reveal that axonemal dyneins are generally in a pre-power stroke conformation that is thought to yield a force-balanced state in straight regions; inhibition of this conformational state and microtubule release on specific doublets may then lead to a force imbalance across the axoneme allowing for microtubule sliding and consequently the initiation and formation of a ciliary bend. Propagation of this inhibitory signal from base-to-tip and switching the microtubule doublet subsets that are inhibited is proposed to result in oscillatory motion.
Topics: Animals; Axonemal Dyneins; Axoneme; Cilia; Dyneins; Flagella; Male; Microtubules
PubMed: 30176122
DOI: 10.1002/cm.21483 -
Arthropod Structure & Development Mar 2019The ultrastructure of the complex organisation of the spermatozoa in Harmonia axyridis and Adalia decempunctata (Coccinellidae) was studied, with particular emphasis on...
The ultrastructure of the complex organisation of the spermatozoa in Harmonia axyridis and Adalia decempunctata (Coccinellidae) was studied, with particular emphasis on the origin of the anterior shifting of the axonemal structure, which becomes parallel to the nucleus in the sperm flagellum. In studying the spermiogenesis, a centriolar remodelling was observed with the long centriole, present in the early spermatids, transformed in the spermatozoa into an exceptionally long and narrowed basal body (about 0.16 × 3.5-4.0 μm long) displaying a 9 + 0 microtubular pattern in the proximal part and a 9 + 2 pattern in the following part; this is a characteristic not observed in any other pterygotan insect. The sperm also have a very long acrosome surrounded by a dense layer of material extending along the whole basal body. These two uncommon features were discussed in the light of sperm movement.
Topics: Animals; Axoneme; Coleoptera; Fluorescent Antibody Technique; Male; Microscopy, Electron, Transmission; Species Specificity; Spermatogenesis; Spermatozoa
PubMed: 30445115
DOI: 10.1016/j.asd.2018.11.004 -
Biochemistry Nov 2013When Chlamydomonas cells resorb their flagella, seven polypeptides become asymmetrically dimethylated (aDMA) on arginine residues. Tandem mass spectrometry has...
When Chlamydomonas cells resorb their flagella, seven polypeptides become asymmetrically dimethylated (aDMA) on arginine residues. Tandem mass spectrometry has identified these as radial spoke proteins 1, 2, 5, and 6; tektin, a structural component of the outer doublets; and flagellar-associated protein 172 (FAP172) (coiled-coil domain containing protein 40 (CCDC40)) and FAP250 (CCDC65), which are associated with inner arm dynein and the nexin-dynein regulatory complex. The enzyme protein arginine methyl transferase 1 (PRMT1), which generates aDMA residues, is a component of the flagellar matrix; antibodies to PRMT1 label full-length flagella in a punctate pattern along the length of the axoneme. During resorption, PRMT1 localization becomes enhanced at the flagellar tip, which is the site of the net disassembly of the flagellar axoneme, and gel shift assays indicate PRMT1 is phosphorylated under resorbing conditions. These data are consistent with a model in which a resorption signal activates one or more protein kinases, resulting in the up-regulation of the components of a protein methylation pathway resident in flagella. Methylation results in axonemal instability and/or enhances the interaction of axonemal polypeptides with intraflagellar transport particles, which then move disassembled components to the cell body for degradation or recycling.
Topics: Algal Proteins; Arginine; Axoneme; Chlamydomonas; Cytoskeletal Proteins; Electrophoretic Mobility Shift Assay; Flagella; Metamorphosis, Biological; Methylation; Microtubule Proteins; Molecular Weight; Peptide Mapping; Plant Proteins; Protein Isoforms; Protein Processing, Post-Translational; Protein Stability; Protein Transport; Protein-Arginine N-Methyltransferases; Protozoan Proteins; Up-Regulation
PubMed: 24152136
DOI: 10.1021/bi4011623 -
Current Topics in Developmental Biology 2011The cilia and flagella of eukaryotic cells are complex filamentous organelles that undulate rapidly and produce propulsive force against the fluids that surround the... (Review)
Review
The cilia and flagella of eukaryotic cells are complex filamentous organelles that undulate rapidly and produce propulsive force against the fluids that surround the living cell. They provide a number of important functions in the life cycle of higher organisms including humans. A flagellum propels the spermatozoa to the site of fertilization and cilia move the egg through the oviduct to the uterus and have a role in left-right asymmetry in the developing embryo and contribute to normal brain morphology. The geometric clutch hypothesis is a mechanistic explanation of how the repetitive bending of cilia and flagella is generated. This chapter recounts the events leading to the development of the geometric clutch hypothesis, explores the conceptual framework of the hypothesis as it relates to properties of the axoneme, and considers the experimental support for the existence of such a mechanism in real cilia and flagella.
Topics: Axoneme; Biomechanical Phenomena; Cilia; Dyneins; Flagella; Models, Biological
PubMed: 21501747
DOI: 10.1016/B978-0-12-385065-2.00001-3 -
Scientific Reports Sep 2019Monozoic caryophyllidean cestodes, intestinal parasites of cyprinid fishes, represent a group of tapeworms with an unclear evolutionary history. As spermatology may...
Monozoic caryophyllidean cestodes, intestinal parasites of cyprinid fishes, represent a group of tapeworms with an unclear evolutionary history. As spermatology may provide phylogenetically important data, the spermiogenesis and ultrastructure of the mature spermatozoon have been investigated using an integrative approach combining transmission electron microscopy, cytochemistry and electron tomography in Khawia rossittensis (Szidat, 1937). The process of spermatid formation is accompanied by the presence of ultrastructural characters not described in traditional models of spermiogenesis, e.g., apical electron-dense material, the two striated roots situated unusually opposite each other, branching of typical striated roots, an intercentriolar body comprising five electron-dense and four electron-lucent layers, rotation of both free flagella and flagellar buds to the median cytoplasmic process at 90°, and a complete proximodistal fusion. The synchronous rotation of both flagellar buds and growing free flagella is an evolutionarily linked pattern favouring the hypothesis that the Caryophyllidea are not ancestral but are secondarily derived from polyzoic forms. Electron tomography analysis has revealed a unique feature of two helicoidal tubular structures in the central electron-dense core of the axoneme of mature spermatozoon. These data provide new insights into the architecture of the 9 + '1' axoneme, which is shared by male gametes of all trepaxonematan Platyhelminthes.
Topics: Animals; Axoneme; Cestoda; Cyprinidae; Microscopy, Electron; Spermatogenesis
PubMed: 31501467
DOI: 10.1038/s41598-019-49312-9 -
The Journal of Biological Chemistry May 2015Anterograde intraflagellar transport (IFT) employing kinesin-2 molecular motors has been implicated in trafficking of photoreceptor outer segment proteins. We generated...
Anterograde intraflagellar transport (IFT) employing kinesin-2 molecular motors has been implicated in trafficking of photoreceptor outer segment proteins. We generated embryonic retina-specific (prefix "emb") and adult tamoxifen-induced (prefix "tam") deletions of KIF3a and IFT88 in adult mice to study photoreceptor ciliogenesis and protein trafficking. In (emb)Kif3a(-/-) and in (emb)Ift88(-/-) mice, basal bodies failed to extend transition zones (connecting cilia) with outer segments, and visual pigments mistrafficked. In contrast, (tam)Kif3a(-/-) and (tam)Ift88(-/-) photoreceptor axonemes disintegrated slowly post-induction, starting distally, but rhodopsin and cone pigments trafficked normally for more than 2 weeks, a time interval during which the outer segment is completely renewed. The results demonstrate that visual pigments transport to the retinal outer segment despite removal of KIF3 and IFT88, and KIF3-mediated anterograde IFT is responsible for photoreceptor transition zone and axoneme formation.
Topics: Animals; Axoneme; Basal Bodies; Kinesins; Mice; Mice, Knockout; Protein Transport; Retinal Cone Photoreceptor Cells; Rhodopsin; Tumor Suppressor Proteins
PubMed: 25825494
DOI: 10.1074/jbc.M115.638437 -
Signal Transduction and Targeted Therapy Jan 2023
Topics: Male; Humans; Animals; Mice; Dyneins; Microtubule-Associated Proteins; Cytoskeleton; Axoneme; Spermatogenesis
PubMed: 36627292
DOI: 10.1038/s41392-022-01293-4 -
Reproduction (Cambridge, England) Sep 2008After a long period of spermatogenesis (several weeks to months), marine fish spermatozoa are delivered at male spawning in seawater (SW) at the same time as ova. In... (Review)
Review
After a long period of spermatogenesis (several weeks to months), marine fish spermatozoa are delivered at male spawning in seawater (SW) at the same time as ova. In some fish species, as the ova micropyle closes quickly after release, these minute unicells, the spermatozoa, have to accomplish their task of reaching the micropyle within a very brief period (several seconds to minutes), for delivery of the haploid male genetic information to the ova. To achieve this goal, their high-performance motile equipment, the flagellum, must fully activate immediately on contact with the SW and then propel the sperm cell at an unusually high initial velocity. The cost of such 'hyperactivity' is a very rapid consumption of intracellular ATP that outstrips the supply. The spermatozoa become rapidly exhausted because mitochondria cannot compensate for this very fast flagellar energy consumption. Therefore, any spermatozoon ends up with two possibilities: either becoming exhausted and immotile or reaching the egg micropyle within its very short period of forward motility (in the range of tens of seconds) before micropyle closure in relation to both contact of SW and cortical reaction. The aim of the present review is to present step by step the successive events occurring in marine fish spermatozoa from activation until their full arrest of motility. The present knowledge of activation mechanisms is summarized, as well as a description of the motility parameters characterizing the motility period. As a complement, in vitro results on axonemal motility obtained after demembranation of flagella bring further understanding. The description of the sperm energetic content (ATP and other high energy compounds) and its evolution during the swimming period is also discussed. A general model aiming to explain all the successive cellular events occurring immediately after the activation is presented. This model is proposed as a guideline for understanding the events governing the sperm lifespan in the marine fish species that reproduce through external fertilization.
Topics: Adenosine Triphosphate; Animals; Axoneme; Energy Metabolism; Fishes; Male; Models, Biological; Seawater; Sperm Motility; Sperm Tail; Spermatozoa
PubMed: 18524881
DOI: 10.1530/REP-07-0522 -
Cytoskeleton (Hoboken, N.J.) May 2014The Ephemeroptera sperm axoneme is devoid of outer dynein arms (ODA) and exhibits a pronounced modification of the central pair complex (CPC), which is substituted by...
The Ephemeroptera sperm axoneme is devoid of outer dynein arms (ODA) and exhibits a pronounced modification of the central pair complex (CPC), which is substituted by the central sheath (CS): a tubular element of unknown molecular composition. We performed a detailed ultrastructural analysis of sperm axonemes in the genera Cloeon and Ecdyonurus using quick-freeze, deep-etch electron microscopy, showing that the loss of the conventional CPC is not only concomitant with the loss of ODA, but also with a substantial modification in the longitudinal distribution of both radial spokes (RS) and inner dynein arms (IDA). Such structures are no longer distributed following the alternation of different repeats as in the 9 + 2 axoneme, but instead share a 32 nm longitudinal repeat: a multiple of the 8 nm repeat observed along the CS wall. Differently from the conventional CPC, the CS and the surrounding RS possess a ninefold symmetry, coherently with the three-dimensional pattern of motility observed in Cloeon free spermatozoa. Biochemical analyses revealed that ultrastructural modifications are concomitant with a reduced complexity of the IDA heavy chain complement. We propose that these structural and molecular modifications might be related to the relief from the evolutionary constraints imposed by the CPC on the basal 9 + 9 + 2 axoneme and could also represent the minimal set compatible with flagellar beating and progressive motility mechanically regulated as suggested by the geometric clutch hypothesis. © 2014 Wiley Periodicals, Inc.
Topics: Animals; Axoneme; Dyneins; Ephemeroptera; Male; Microscopy, Electron, Transmission; Spermatozoa
PubMed: 24668829
DOI: 10.1002/cm.21175