Outer dense fibre protein 2 (ODF2) is a self-interacting centrosomal protein with affinity for microtubules

Donkor, Fatima; Mönnich, Maren; Czirr, Eva; Hollemann, Thomas; Hoyer‐Fender, Sigrid

doi:10.1242/jcs.01303

Cited by 75 publications

(70 citation statements)

References 48 publications

(78 reference statements)

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“…3). These proteins are associated with the development of sperm tails, where they provide elasticity and protection from shear [41]. Interestingly, up-regulation of opsins was also observed in males with respect to androchrome and infuscans female morphs (Fig.…”

Section: Resultsmentioning

confidence: 99%

Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression

2016

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BackgroundSexual dimorphism occurs widely across the animal kingdom and has profound effects on evolutionary trajectories. Here, we investigate sex-specific gene expression in Ischnura elegans (Odonata: dragonflies and damselflies), a species with pronounced sexual differences including a female-limited colour polymorphism with two female-like gynochrome morphs and one male-mimicking, androchrome morph. Whole-organism transcriptome profiling and sex-biased gene expression analysis was conducted on adults of both sexes (pooling all females as well as separating the three morphs) to gain insights into genes and pathways potentially associated with sexual development and sexual conflict.ResultsThe de novo transcriptome assembly was of high quality and completeness (54 k transcripts; 99.6% CEGMA score; 55% annotated). We identified transcripts of several relevant pathways, including transcripts involved in sex determination, hormone biosynthesis, pigmentation and innate immune signalling. A total of 1,683 genes were differentially expressed (DE) between males and all females (1,173 were female-biased; 510 male-biased). The DE genes were associated with sex-specific physiological and reproductive processes, olfaction, pigmentation (ommochrome and melanin), hormone (ecdysone) biosynthesis and innate immunity signalling pathways. Comparisons between males and each female morph category showed that the gynochromes differed more from males than the androchrome morph.ConclusionsThis is the first study to characterize sex-biased gene expression in odonates, one of the most ancient extant insect orders. Comparison between I. elegans sexes revealed expression differences in several genes related to sexual differences in behaviour and development as well as morphology. The differential expression of several olfactory genes suggests interesting sexual components in the detection of odours, pheromones and environmental volatiles. Up-regulation of pigmentation pathways in females indicates a prominent role of ommochrome pigments in the formation of the genetically controlled female colour polymorphism. Finally, the female-biased expression of several immunity genes suggests a stronger immune response in females, possibly related to the high levels of male mating harassment and recurrent matings in this species, both of which have been shown to injure females and expose them to sexually transmitted diseases and toxins contained in seminal fluids.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3334-6) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression

2016

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“…ODF2, Hexokinase, and Aldolase C Outer dense fiber protein 2 (ODF2) is a major component of the cytoskeletal structure of the sperm tail and is associated, albeit indirectly, with microtubules [67]. Hexokinase binds ATP in an actin fold-like structural motif to phosphorylate glucose, and it has been localized in the acrosome, midpiece, and tail of human spermatozoa [68,69].…”

Section: Rhoa-interacting Proteins In Bovine Spermatozoamentioning

confidence: 99%

Identification and Characterization of RHOA-Interacting Proteins in Bovine Spermatozoa1

Fiedler¹,

Bajpai²,

Carr³

2008

Biology of Reproduction

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In somatic cells, RHOA mediates actin dynamics through a GNA13-mediated signaling cascade involving RHO kinase (ROCK), LIM kinase (LIMK), and cofilin. RHOA can be negatively regulated by protein kinase A (PRKA), and it interacts with members of the A-kinase anchoring (AKAP) family via intermediary proteins. In spermatozoa, actin polymerization precedes the acrosome reaction, which is necessary for normal fertility. The present study was undertaken to determine whether the GNA13-mediated RHOA signaling pathway may be involved in acrosome reaction in bovine caudal sperm, and whether AKAPs may be involved in its targeting and regulation. GNA13, RHOA, ROCK2, LIMK2, and cofilin were all detected by Western blot in bovine caudal sperm. Overlay, immunoprecipitation, and subsequent mass spectrometry analysis identified several RHOA-interacting proteins, including proacrosin, angiotensin-converting enzyme, tubulin, aldolase C, and AKAP4. Using overlay and pulldown techniques, we demonstrate that phosphorylation of AKAP3 increases its interaction with the RHOA-interacting proteins PRKAR2 (the type II regulatory subunit of PRKA, formerly RII) and ropporin (ROPN1, a PRKAR2-like protein, or R2D2). Varying calcium concentrations in pulldown assays did not significantly alter binding to R2D2 proteins. These data suggest that the actin-regulating GNA13-mediated RHOA-ROCK-LIMK-cofilin pathway is present in bovine spermatozoa, that RHOA interacts with proteins involved in capacitation and the acrosome reaction, and that RHOA signaling in sperm may be targeted by AKAPs. Finally, AKAP3 binding to PRKAR2 and ROPN1 is regulated by phosphorylation in vitro.

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“…ODF2 is a putative coiled coil protein containing two leucine zippers that mediate interaction with ODF1, another major component of the outer dense fibers (Donkor et al, 2004;Shao et al, 1997). A critical function of Odf2 is implied by strong sequence conservation (Petersen et al, 1999): for example, the amino acid sequences of human and mouse ODF2 share greater than 97% homology.…”

Section: Introductionmentioning

confidence: 99%

“…However, in a recent publication, monoclonal antibodies directed against purified chicken centrosomes have identified ODF2 protein as a widespread centrosomal component (Nakagawa et al, 2001). Further studies have also suggested that ODF2 protein at the centrosome is able to associate both with itself and with microtubules (Donkor et al, 2004). Furthermore, an Odf2 gene targeted knockout mouse F9 cell line has recently been described, in which a critical role for ODF2 at the centrosome for the generation of primary cilia was revealed (Ishikawa et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

A gene trap knockout of the abundant sperm tail protein, outer dense fiber 2, results in preimplantation lethality

Salmon

Pera

2006

Genesis

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SummaryOuter dense fiber 2 (Odf2) is highly expressed in the testis where it encodes a major component of the outer dense fibers of the sperm flagellum. Furthermore, ODF2 protein has recently been identified as a wide-spread centrosomal protein. While the expression of Odf2 highlighted a potential role for this gene in male germ cell development and centrosome function, the in vivo function of Odf2 was not known. We have generated Odf2 knockout mice using an Odf2 gene trapped embryonic stem cell (ESC) line. Insertion of a gene trap vector into exon 9 resulted in a gene that encodes a severely truncated protein lacking a large portion of its predicted coil forming domains as well as both leucine zipper motifs that are required for protein-protein interactions with ODF1, another major component of the outer dense fibers. Although wild-type and heterozygous mice were recovered, no mice homozygous for the Odf2 gene trap insertion were recovered in an extended breeding program. Furthermore, no homozygous embryos were found at the blastocyst stage of embryonic development, implying a critical pre-implantation role for Odf2. We show that Odf2 is expressed widely in adults and is also expressed in the blastocyst stage of preimplantation development. These findings are in contrast with early studies reporting Odf2 expression as testis specific and suggest that embryonic Odf2 expression plays a critical role during preimplantation development in mice.

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Outer dense fibre protein 2 (ODF2) is a self-interacting centrosomal protein with affinity for microtubules

Cited by 75 publications

References 48 publications

Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression

Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression

Identification and Characterization of RHOA-Interacting Proteins in Bovine Spermatozoa1

A gene trap knockout of the abundant sperm tail protein, outer dense fiber 2, results in preimplantation lethality

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