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The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization.

Neither the restoration of the centrosome during fertilization nor its reduction during gametogenesis is fully understood, but both are pivotal events in development. During each somatic cell cycle, the chromosomes, cytoplasm, and centrosomes duplicate in interphase, and all three split in two during each cell division. While it has long been recognized that both the sperm and the egg contribute equal haploid genomes during fertilization and that the vast majority of the cytoplasm is contributed by the egg, the relative contributions of the centrosome by each gamete are still in question. This article explores centrosome inheritance patterns and considers nine integral and secondarily derived activities of the centrosome. Boveri once hypothesized that "The ripe egg possesses all of the elements necessary for development save an active division-center. The sperm, on the other hand, possesses such a center but lacks the protoplasmic substratum in which to operate. In this respect the egg and sperm are complementary structures; their union in syngamy thus restores to each the missing element necessary to further development." This article reviews the evidence gathered from 11 experimental strategies used to test this theory. While the majority of these approaches supports the hypothesis that the sperm introduces the centrosome at fertilization, the pattern did not reveal itself as universal, since parthenogenesis occurs in nature and can be induced artificially, since centrosome and centriole form de novo in extracts from unfertilized eggs and since the centrosome is derived from maternal sources during fertilization in some systems--notably, in mice. Models of the centrosome are proposed, along with speculative mechanisms which might lead to the cloaking of the reproducing element of the maternal centrosome during oogenesis and the retention of this structure by the paternal centrosome during spermatogenesis. Proteins essential for microtubule nucleation, like gamma-tubulin, are retained in the cytoplasm during oogenesis, but are largely lost during spermatogenesis. It is further postulated that the restoration of the zygotic centrosome at fertilization requires the attraction of maternal centrosomal components (in particular, gamma-tubulin and the 25S "gamma-some" particle) to the paternal reproducing element; this, along with post-translational modifications (including phosphorylation, disulfide reduction, and calcium ion binding), creates a functional zygote centrosome by blending both maternal and paternal constituents.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Reproductive maternal centrosomes are cast off into polar bodies during maturation division in starfish oocytes.

Animal egg inherits a maternal centrosome from the meiosis-II spindle and sperm can introduce another centrosome at fertilization. It has been believed that in most animals only the sperm centrosome provides the division poles for mitosis in zygotes. This uniparental (paternal) inheritance of the centrosome must depend on the loss of the maternal centrosome. In starfish, suppression of polar body (PB) extrusion is a prerequisite for induction of parthenogenesis (Washitani-Nemoto et al. (1994) Dev. Biol. 163, 293-301), suggesting that the centrosomes cast off into PBs have reproducing capacity. Due to the absence of centriole duplication in meiosis II of starfish oocytes, each centrosome of a meiosis-II spindle has only one single centriole, whereas in meiosis I each has a pair of centrioles (Sluder et al. (1989) Dev. Biol. 131, 567-579; Kato et al. (1990) Dev. Growth Differ. 32, 41-49). Hence, the first PB (PB1) has two centrioles, whereas the second PB (PB2) and the mature egg have only one centriole, respectively. The present study examined the reproductive capacity of PB centrosomes by transplanting them into artificially activated eggs, and then the recipient egg nucleus with the surrounding cytoplasm was removed. A transplanted PB2 centrosome with a single centriole formed a monopolar spindle at the first mitosis, followed by formation of a bipolar spindle in the next mitosis, leading to actual cleavage and subsequent development. This proves the reproducing capacity of the single centriole in the PB2 centrosome. The behavior of the transplanted PB1 centrosome was exactly the same as in the PB2 centrosome, in spite of the difference in the number of centrioles. These results clearly show that four maternal centrioles are heterogeneous in duplicating capacity, during meiosis only one centriole in each of the centrosomes of a meiosis-I spindle pole retains duplicating capacity, the reproductive centrioles are successively cast off into PBs, and finally a mature egg inheriting a nonreproductive centriole alone is formed, and the presence of a single reproductive centriole is sufficient condition for embryonic development in starfish.

Animals↗

Genetic origin of malignant trophoblastic neoplasms analyzed by sequence tag site polymorphic markers.

OBJECTIVE: To study the causative conception of malignant gestational trophoblastic neoplasms (GTNs), we analyzed malignant GTNs by microsatellite PCR markers. METHOD: DNAs extracted from 12 malignant GTNs were subjected to PCR for five different chromosomal locations. RESULT: Of the 7 cases after a complete mole (CM), 5 were derived from androgenesis, but the remaining 2 were from normal fertilization. Of the 5 cases after nonmolar pregnancies, 2 placental site trophoblastic tumors had alleles from both parents. Of the other 3 choriocarcinomas, 1 was from normal fertilization after spontaneous abortion but 2 originated from androgenesis, suggesting that 1 was from a CM prior to the antecedent abortion, transforming after a long interval. CONCLUSION: By combining the previous cases with these, our analysis of 39 cases demonstrated that trophoblastic neoplasms can arise from at least three different modes of origin (androgenesis, normal fertilization, and parthenogenesis), and antecedent pregnancy is not always identical to the causative conception. Placental site trophoblastic tumors might have different machinery for carcinogenesis because of the predominance of paternal and maternal contributions. In addition, a long dormancy of trophoblasts before malignant transformation, especially for those originating from normal fertilization, was also suggested.

Adult↗

Coexistence between cyclical parthenogens, obligate parthenogens, and intermediates in a fluctuating environment

We evaluate the cost of sex in cyclical parthenogens coexisting with obligate parthenogens that produce a few sexuals, a situation found in numerous species. In aphids and cladocera, sex is generally the only way to produce a resistant form; this gives a potential ecological advantage to sex. We focus on the selective factor constituted by variations of the environment, that may be alternatively advantageous to cyclical parthenogens (cold winters in aphids, drought in daphnia) or to obligate parthenogens. Our calculations show that the production of a few sexuals by lineages that are essentially obligate parthenogens has a critical effect on the balance between the different life-cycles, especially when this production is limited to males. This male production by intermediates confers additional fitness to obligate parthenogenesis genes and then sharply increases the cost of sex. Copyright 1998 Academic Press

Journal Article↗

Molecular systematics and evolution of the aphid family Lachnidae.

The aphid family Lachnidae (c. 320 spp.)-sister-group to the economically devastating family Aphididae (c. 3300 spp.)-encompasses a diverse array of associations with hostplants and attendant hymenopterans and of life histories, including potentially long-term parthenogenesis. Most-parsimonious phylogenetic trees were inferred from partial (905-coding-bp) sequences of elongation factor 1alpha (EF-1alpha) and complete (675-bp) sequences of cytochrome oxidase 2 (CO2). The EF-1alpha, CO2, and combined analyses did not conflict with each other. Most tribes and infratribal relationships were robustly supported; intertribal relationships were mostly unresolved in the separate analysis and only weakly supported in the combined analysis. Both genes indicated a close relationship between the genera Nippolachnus and Tuberolachnus, both of which include species with the unusual habit of feeding along the midrib of leaves of Eriobotrya and which are here referred to the tribe Tuberolachnini Mamontova. A sister-group relationship between Tuberolachnini and the putatively ancient asexual tribe Tramini is supported. The combined analysis provides support (albeit weak) for the hypothesis that conifer-feeding is ancestral in Lachninae, which in turn implies that conifer-feeding may be a homologous and uninterrupted habit across disparate families of aphidoids (e.g., Adelgidae, Mindaridae, Drepanosiphidae, and Lachnidae).

Animals↗

The first detection of the insertion sequence ISW1 in the intracellular reproductive parasite Wolbachia.

Wolbachia are maternally inherited intracellular rickettsia-like bacteria known to infect a wide range of arthropods. They are associated with a number of different reproductive phenotypes in their hosts, such as cytoplasmic incompatibility, parthenogenesis, and feminization. We report on a novel insertion sequence (IS), ISW1, which was identified in the region downstream of groEL of a Wolbachia strain, wTai. The 573-bp-long ISW1 sequence is the first IS element observed in this organism, displays significant similarity to IS200, and lacks terminal inverted repeats. There were more than 20 copies of ISW1 on the chromosome of wTai. Sequence analysis of nine distinct ISW1 copies and their flanking regions showed that the copies were identical and suggested that ISW1 has no preference for its insertion sites. Possible roles of ISW1 in the adaptation of Wolbachia to intracellular environments and in various reproductive alterations caused by this bacterium are discussed.

Amino Acid Sequence↗

Wolbachia: intracellular manipulators of mite reproduction.

Cytoplasmically transmitted Wolbachia (alpha-Proteobacteria) are a group of closely related intracellular microorganisms that alter reproduction in arthropods. They are found in a few isopods and are widespread in insects. Wolbachia are implicated as the cause of parthenogenesis in parasitic wasps, feminization in isopods and reproductive (cytoplasmic) incompatibility in many insects. Here we report on the widespread occurrence of Wolbachia in spider mites and predatory mites based on a PCR assay for a 730 bp fragment of the ftsZ gene with primers that are specific for Wolbachia. An additional PCR, using two primer pairs that amplify a 259 bp region of the ftsZ gene that are diagnostic for the two Wolbachia subdivisions A and B, showed that infected mites only carried type B and not type A Wolbachia. The fact that some species tested negative for Wolbachia does not mean that the entire species is uninfected. We found that natural populations of Tetranychus urticae are polymorphic for the infection. The possible effects of Wolbachia on mite reproduction and post-zygotic reproductive isolation are discussed.

Animals↗

Biology of Ixodes (Pholeoixodes) hexagonus under laboratory conditions. Part II. Effect of mating on feeding and fecundity of females.

The effect of mating on the feeding and fecundity of Ixodes (Pholeoixodes) hexagonus females was studied under controlled laboratory conditions of 22-23 degrees C and 98% relative humidity. The feeding period of mated females was 6-15 days and 11-13 days for unmated females. The mean weight of the engorged mated females was 114.84 +/- 45.89 mg, whereas, that of the engorged unmated females was significantly lower (80.61 +/- 28.84 mg). During the initial slow feeding period, the weight of mated females increased 6.6 times. At the end of the blood feeding, they had increased their initial weight 35.5 times. Unmated females never entered the rapid engorgement phase and up to 12 days of feeding period their mean weight did not increase more than 9.2 times. The pre-oviposition periods of mated and unmated females were 6-15 days and 4-12 days, respectively. The mean of the egg production efficiency was 40.26 +/- 12.47% for mated females and 35.68 +/- 12.2% for unmated females. The mean of the mass conversion efficiency was 73.6 +/- 13.7% for mated females and 66.48 +/- 16.55% for unmated females. Sixty per cent of the eggs deposited by mated females hatched whereas only 1% of the eggs deposited by unmated females hatched. These results indicate that I. hexagonus females possess some predisposition for parthenogenesis and only fertility and not fecundity depends on mating.

Animals↗

Behavioral differences among isogenic strains of Drosophila mercatorum.

Mating propensity in eight all-female laboratory lines was measured. The lines are completely isogenic, but each has a different past history. In all cases, mating propensity was significantly lower than in the bisexual controls; in some cases, mating speed was less by a factor of 10. Three of the four lines deriving from the same wild strain are not only different from the parent strain but also different from each other. A highly significant difference exists between two strains recently obtained by selection for parthenogenesis from the same natural population. One strain appears to produce a substance which reduces mating propensity of control females if females from the two strains are reared together in the same vial. As none of the strains was behaviorally selected prior to testing, these behaviors appear to be incidental accompaniments of the very powerful isogenizing effect of the genetic system in these parthenogenetic strains. Indeed, the data show that partial isolation from sexual reproduction can arise wholly by chance. This may have some relevance to theories of species origin which are accompanied by a strong initial founder effect.

Animals↗

Unusual sequences, homologous to 5S RNA, in ribosomal DNA repeats of the nematode Meloidogyne arenaria.

There are sequences homologous to 5S ribosomal RNA in the ribosomal DNA (rDNA) repeats of the plant-parasitic nematode Meloidogyne arenaria. This is surprising, because in all other higher eukaryotes studied to date, the genes for 5S RNA are unlinked to and distinct from a tandem rDNA repeat containing the genes for 18S, 5.8S, and 28S ribosomal RNA. Previously, only prokaryotes and certain "lower eukaryotes" (protozoa and fungi) had been found to have both the larger rRNAs and 5S rRNA represented within a single DNA repeat. This has raised questions on the organization of these repeats in the earliest cell (progenote), and on subsequent evolutionary relationships between pro- and eukaryotes. Evidence is presented for rearrangements and deletions within Meloidogyne rDNA. The unusual life cycles (different levels of ploidy, reproduction by meiotic and mitotic parthenogenesis) of members of this genus might allow rapid fixation of any variants with introduced 5S RNA sequences. The 5S RNA sequences in Meloidogyne rDNA may not be expressed, but their presence raises important questions as to the evolutionary origins and stability of repeat gene families.

Animals↗

The effect of partial zona dissection on the fertilizing capacity of chronically obstructed mouse caput epididymal sperm.

PURPOSE: Having observed that sperm from the chronically obstructed caput epididymis fertilize poorly in vitro, we investigated the effect of partial zona dissection (PZD) on fertilization in a murine model of unilateral proximal epididymal obstruction. Cleavage rates were compared for zona-intact oocytes and PZD oocytes incubated with sperm from the following epididymal segments: the obstructed caput, the contralateral nonobstructed caput, the contralateral cauda, and a sperm-free preparation to control for parthenogenesis. RESULTS: Unilateral epididymal obstruction resulted in significantly higher sperm counts in the obstructed caput compared to the nonobstructed caput, although there was no difference in motility. Cleavage rates for ova incubated with sperm from the obstructed caput and the nonobstructed caput were uniformly poor and did not differ significantly from those for the sperm-free controls. Cauda sperm fertilized significantly better than all other sperm groups (P < 0.05). Partial zona dissection did not improve cleavage rates in any group. CONCLUSION: We conclude that sperm from the chronically obstructed caput epididymis, like sperm from the normal caput, are unable to fertilize ova, and PZD does not enhance this poor fertilizing capacity. Furthermore, the finding that PZD does not improve the fertilizing capacity of the presumably mature cauda sperm in our mouse model suggests that any beneficial effect of PZD may be strain-specific.

Animals↗

Mating for schistosomes.

A mathematical model for schistosomiasis is developed under the hypothesis of promiscuous mating between mature schistosomes. The model is used to study epidemiology, control, and eradication of schistosome infections. Comparisons are made with previously published models that deal with monogamous mating and with parthenogenesis. We find that the two modes of mating give results that are essentially similar. On the other hand, essential differences exist between either mode of mating and the parthenogenetic case. Thus, we conclude that it is not of essential importance to find out if mature schistosomes are monogamous or promiscuous. A second conclusion is that the simplifying assumption of parthenogenetic egg-laying of schistosomes is not acceptable.

Animals↗

The effects of proteasome inhibitor lactacystin on mouse oocyte meiosis and first cleavage.

In order to study the effects of ubiquitin-proteasome pathway (UPP) on mouse oocyte meiosis and cleavage, oocytes undergoing maturation and parthenogenetic activation and 1-cell embryos were treated with lactacystin, a specific inhibitor of proteasome. The results indicated that the rate of GVBD was not influenced by the treatment, but polar body extrusion, parthenogenesis and first cleavage were inhibited. Immunofluorescent staining using anti beta-tubulin antibody indicated that the continuous treatment of lactacystin from GV stage disorganized microtubules and spindle assembly. When metaphase stage oocytes were treated with the drug, the already formed spindle structure was not affected, but the oocytes were arrested at metaphases. The 1-cell embryos were arrested at interphase or metaphase of first mitosis when they were incubated in the drug. Proteasome regulatory subunit PA700 was located in the spindle region, as indicated by immunofluorescence. These results suggest that UPP has effects on the process of oocyte meiosis and early cleavage in many aspects, including normal organization of spindle at prophase and segregation of chromosomes at anaphase for normal meiosis.

Acetylcysteine↗

AFLP-based estimation of 2n gametophytic heterozygosity in two parthenogenetically derived dihaploids of Rosa hybrida L.

Two dihaploid Rosa hybrida L. genotypes, derived through parthenogenesis by using irradiated pollen, were crossed with clonally propagated plants of the diploid species Rosa rugosa Thunb. and Rosa wichuraiana Crép., respectively. Three progeny groups were obtained which contained numerous polyploids, as determined by flow cytometry. Production of fertile 2n female gametes is apparently very common in one of these R. hybrida dihaploid derivatives, whereas the other one is able to produce fertile 2n pollen. Hence, an amplified fragment length polymorphism (AFLP) study was performed on the parental plants and the resulting hybrid offspring in order to estimate (1) the respective genomic parental contributions, and (2) the level of heterozygosity transmitted by the 2n unreduced gametes. Comparison of the levels of transmitted parental heterozygosity revealed that two types of 2n gametes were produced simultaneously, presumably resulting from restitution at the first and at the second meiotic division, respectively.

Journal Article↗

Pramipexole protects against H2O2-induced PC12 cell death.

Pramipexole, a novel non-ergot dopamine (DA) agonist, has been successfully applied to the treatment of Parkinson's disease (PD). Although the specific cause of PD remains unknown, recent studies have provided evidence that oxidative stress plays a role in the parthenogenesis of the disease. In the present study, we examined the effect of pramipexole on hydrogen peroxide (H2O2, 100 microM)-induced PC12 cell death, and the intracellular mechanism of this effect. The 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium (MTT) assay revealed that pretreatment of PC12 cells with pramipexole (1-100 microM) resulted in significant protection against H2O2-induced cell death in a concentration-dependent manner. The protective effect of pramipexole was not affected by pretreatment with the DA receptor antagonists sulpiride, spiperone or domperidone, suggesting that the effect of pramipexole is not mediated by DA receptors. In PC12 cells, pramipexole inhibited H2O2-induced lactate dehydrogenase (LDH) leakage, as well as H2O2-induced cytochrome c release and caspase-3 activation with the resultant apoptosis. It was also observed in PC12 cells that H2O2 stimulated phosphorylation of mitogen-activated protein (MAP) kinases, i.e., extracellular signal-regulated kinase1/2 (ERK1/2), c-Jun NH2-terminal kinase (JNK) and p38 MAP kinase. Pramipexole inhibited H2O2-induced JNK and p38 MAP kinase, but not ERK1/2 phosphorylation. Furthermore, in these cells experiments with a fluorescent probe, 2-[6-(4'-amino)phenoxy-3H-xanthen-3-on-9-yl]benzoic acid, revealed that pramipexole, the JNK inhibitor SP600125 and the p38 MAP kinase inhibitor SB203580 inhibited the generation of H2O2-induced reactive oxygen species. Caspase inhibitors Z-DEVD-FMK and Z-IETD-FMK, as well as SP600125 and SB203580, inhibited H2O2-induced PC12 cell death to a similar extent as pramipexole. These results suggest that pramipexole exerts a protective effect against oxidative stress-induced PC12 cell death in part through an inhibition of JNK and p38 MAP kinase.

Animals↗

Influence of potentially confounding factors on sea urchin porewater toxicity tests.

The influence of potentially confounding factors has been identified as a concern for interpreting sea urchin porewater toxicity test data. The results from >40 sediment-quality assessment surveys using early-life stages of the sea urchin Arbacia punctulata were compiled and examined to determine acceptable ranges of natural variables such as pH, ammonia, and dissolved organic carbon on the fertilization and embryological development endpoints. In addition, laboratory experiments were also conducted with A. punctulata and compared with information from the literature. Pore water with pH as low as 6.9 is an unlikely contributor to toxicity for the fertilization and embryological development tests with A. punctulata. Other species of sea urchin have narrower pH tolerance ranges. Ammonia is rarely a contributing factor in pore water toxicity tests using the fertilization endpoint, but the embryological development endpoint may be influenced by ammonia concentrations commonly found in porewater samples. Therefore, ammonia needs to be considered when interpreting results for the embryological development test. Humic acid does not affect sea urchin fertilization at saturation concentrations, but it could have an effect on the embryological development endpoint at near-saturation concentrations. There was no correlation between sediment total organic carbon concentrations and porewater dissolved organic carbon concentrations. Because of the potential for many varying substances to activate parthenogenesis in sea urchin eggs, it is recommended that a no-sperm control be included with every fertilization test treatment.

Ammonia↗

Wolbachia infections of tephritid fruit flies: molecular evidence for five distinct strains in a single host species.

Endosymbiotic bacteria of the genus Wolbachia are widespread among arthropods and can induce cytoplasmic incompatibility, thelytokous parthenogenesis, male-killing or feminization in their hosts. Here, we report phylogenetic relationships of Wolbachia in tephritid fruit flies based on wsp gene sequences. We also report, for the first time, five distinct strains of Wolbachia in Bactrocera ascita sp. B. Four of the five Wolbachia strains found in this species were in the same groups as those found in other tephritid fruit flies, suggesting possible horizontal transmission of Wolbachia from other fruit flies into B. ascita sp. B. The unreliability of wsp-specific group primers demonstrated in this study suggests that these primers might be useful only for preliminary identification of Wolbachia. Final determination of group affiliation needs to be verified with wsp sequence data.

Amino Acid Sequence↗

Wolbachia replication and host cell division in Aedes albopictus.

Wolbachia pipientis is an obligate intracellular endosymbiont of a range of arthropod species. The microbe is best known for its manipulations of host reproduction that include inducing cytoplasmic incompatibility, parthenogenesis, feminization, and male-killing. Like other vertically transmitted intracellular symbionts, Wolbachia's replication rate must not outpace that of its host cells if it is to remain benign. The mosquito Aedes albopictus is naturally infected both singly and doubly with different strains of Wolbachia pipientis. During diapause in mosquito eggs, no host cell division is believed to occur. Further development is triggered only by subsequent exposure of the egg to water. This study uses diapause in Wolbachia-infected Aedes albopictus eggs to determine whether symbiont replication slows or stops when host cell division ceases or whether it continues at a low but constant rate. We have shown that Wolbachia densities in eggs are greatest during embryonation and then decline throughout diapause, suggesting that Wolbachia replication is dependent on host cell replication.

Aedes↗