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1.
Sci Rep ; 14(1): 8263, 2024 04 09.
Article in English | MEDLINE | ID: mdl-38594333

ABSTRACT

Oocytes of both vertebrates and invertebrates often contain an intricate organelle assemblage, termed the Balbiani body (Bb). It has previously been suggested that this assemblage is involved in the delivery of organelles and macromolecules to the germ plasm, formation of oocyte reserve materials, and transfer of mitochondria to the next generation. To gain further insight into the function of the Bb, we performed a series of analyses and experiments, including computer-aided 3-dimensional reconstructions, detection of DNA (mtDNA) synthesis as well as immunolocalization studies. We showed that in orthopteran Meconema meridionale, the Bb comprises a network of mitochondria and perinuclear nuage aggregations. As oogenesis progresses, the network expands filling almost entire ooplasm, then partitions into several smaller entities, termed micro-networks, and ultimately into individual mitochondria. As in somatic cells, this process involves microfilaments and elements of endoplasmic reticulum. We showed also that at least some of the individual mitochondria are surrounded by phagophores and eliminated via mitophagy. These findings support the idea that the Bb is implicated in the multiplication and selective elimination of (defective) mitochondria and therefore may participate in the transfer of undamaged (healthy) mitochondria to the next generation.


Subject(s)
Oocytes , Orthoptera , Animals , Oocytes/metabolism , Oogenesis/genetics , Mitochondria/genetics , Insecta , Endoplasmic Reticulum
2.
Theriogenology ; 217: 25-36, 2024 Mar 15.
Article in English | MEDLINE | ID: mdl-38241912

ABSTRACT

Telocytes represent a relatively recently discovered population of interstitial cells with a unique morphological structure that distinguishes them from other neighboring cells. Through their long protrusions extending from the cell body, telocytes create microenvironments via tissue compartmentalization and create homo- and hetero-cellular junctions. These establish a three-dimensional network enabling the maintenance of interstitial compartment homeostasis through regulation of extracellular matrix organization and activity, structural support, paracrine and juxtracrine communication, immunomodulation, immune surveillance, cell survival, and apoptosis. The presence of telocytes has also been confirmed in testicular interstitial tissue of many species of animals. The objective of this review is to summarize recent findings on telocytes in the male gonad, on which conclusions have been deduced that indicate the involvement of telocytes in maintaining the cytoarchitecture of the testicular interstitial tissue, in the processes of spermatogenesis and steroidogenesis, and photoperiod-mediated changes in the testes in seasonally reproductive animals.


Subject(s)
Telocytes , Testis , Male , Animals , Leydig Cells
3.
Results Probl Cell Differ ; 71: 47-63, 2024.
Article in English | MEDLINE | ID: mdl-37996672

ABSTRACT

Syncytia are common in the animal and plant kingdoms both under normal and pathological conditions. They form through cell fusion or division of a founder cell without cytokinesis. A particular type of syncytia occurs in invertebrate and vertebrate gametogenesis when the founder cell divides several times with partial cytokinesis producing a cyst (nest) of germ line cells connected by cytoplasmic bridges. The ultimate destiny of the cyst's cells differs between animal groups. Either all cells of the cyst become the gametes or some cells endoreplicate or polyploidize to become the nurse cells (trophocytes). Although many types of syncytia are permanent, the germ cell syncytium is temporary, and eventually, it separates into individual gametes. In this chapter, we give an overview of syncytium types and focus on the germline and somatic cell syncytia in various groups of insects. We also describe the multinuclear giant cells, which form through repetitive nuclear divisions and cytoplasm hypertrophy, but without cell fusion, and the accessory nuclei, which bud off the oocyte nucleus, migrate to its cortex and become included in the early embryonic syncytium.


Subject(s)
Cysts , Germ Cells , Animals , Cysts/metabolism , Germ Cells/metabolism , Giant Cells , Insecta , Oocytes
4.
Endocrine ; 80(2): 448-458, 2023 05.
Article in English | MEDLINE | ID: mdl-36658296

ABSTRACT

PURPOSE: Ovarian cancer is characterized by recurrent peritoneal and distant metastasis. To survive in a non-adherent state, floating ovarian cancer spheroids develop mechanisms to resist anoikis. Moreover, ascitic fluid from ovarian cancer patients contains high levels of visfatin with anti-apoptotic properties. However, the mechanism by which visfatin induces anoikis resistance in ovarian cancer spheroids remains unknown. Here, we aimed to assess wheather visfatin which possess anti-apoptotic properties can induce resistance of anoikis in ovarian cancer spheroids. METHODS: Visfatin synthesis were examined using a commercial human visfatin ELISA Kit. Spheroid were exposed to visfatin and cell viability and caspase 3/7 activity were measured using CellTiter-Glo 3D cell viability assay and Caspase-Glo® 3/7 Assay System. mRNA and protein expression were analyzed by Real-time PCR and Western Blot analysis, respectively. Analysis of mitochondrial activity was estimated by JC-1 staining. RESULTS: First, our results suggested higher expression and secretion of visfatin by epithelial than by granulosa ovarian cells, and in non-cancer tissues versus cancer tissues. Interestingly, visfatin increased the proliferation/apoptosis ratio in ovarian cancer spheroids. Specifically, both the intrinsic and extrinsic pathways of anoikis were regulated by visfatin. Moreover, the effect of the visfatin inhibitor (FK866) was opposite to that of visfatin. Furthermore, both NAMPT and FK866 affected mitochondrial activity in ovarian cancer cells. CONCLUSION: In conclusion, visfatin acts as an anti-apoptotic factor by regulating mitochondrial activity, leading to anoikis resistance in ovarian cancer spheroids. The finding suggest visfatin as a potential novel therapeutic target for the treatment of ovarian carcinoma with peritoneal dissemination.


Subject(s)
Anoikis , Nicotinamide Phosphoribosyltransferase , Ovarian Neoplasms , Female , Humans , Cell Line, Tumor , Nicotinamide Phosphoribosyltransferase/metabolism , Ovarian Neoplasms/metabolism , Ovarian Neoplasms/pathology
5.
Reprod Fertil Dev ; 35(3): 294-305, 2023 Jan.
Article in English | MEDLINE | ID: mdl-36403477

ABSTRACT

CONTEXT: The destruction of granulosa cells (GCs), the main functional cell type in the ovary, prevents steroid hormone production, which in turn may damage oocytes, resulting in ovarian failure. The accumulation of a number of persistent organic pollutants (POPs) in the ovarian follicular fluid (FF) has been documented, which raises serious questions regarding their impact on female fertility. AIMS: We aimed to determine whether a mixture of POPs reflecting the profile found in FF influences mouse GCs or oocyte function and viability. METHODS: A mixture of POPs, comprising perfluorooctanoate, perfluorooctane sulfonate, 2,2-dichlorodiphenyldichloroethylene, polychlorinated biphenyl 153, and hexachlorobenzene, was used. In addition to using the exact concentration of POPs previously measured in human FF, we tested two other mixtures, one with10-fold lower and another with 10-fold higher concentrations of each POP. KEY RESULTS: Steroidogenesis was disrupted in GCs by the POP mixture, as demonstrated by lower oestradiol and progesterone secretion and greater lipid droplet accumulation. Furthermore, the POP mixture reduced GC viability and increased apoptosis, assessed using caspase-3 activity. The POP mixture significantly increased the number of oocytes that successfully progressed to the second meiotic metaphase and the oocyte reactive oxygen species (ROS) concentration. CONCLUSIONS: Thus, a mixture of POPs that are typically present in human FF has detrimental effects on ovarian function: it reduces the viability of GCs, and increases the oocyte concentrations of ROS. IMPLICATIONS: These results indicate that chronic exposure to POPs adversely affects female reproductive health.


Subject(s)
Environmental Pollutants , Persistent Organic Pollutants , Female , Animals , Humans , Mice , Reactive Oxygen Species/metabolism , Persistent Organic Pollutants/metabolism , Granulosa Cells/metabolism , Oocytes/metabolism , Environmental Pollutants/toxicity
6.
Zoology (Jena) ; 155: 126051, 2022 12.
Article in English | MEDLINE | ID: mdl-36108419

ABSTRACT

Balbiani bodies (Bbs) are female germline-specific organelle assemblages usually composed of mitochondria, Golgi complexes, elements of endoplasmic reticulum and accumulations of fine granular material, termed the nuage. Here we present results of morphological and ultrastructural analysis of the Bb of four bush crickets nested in four subfamilies of the family Tettigonidae. This study has revealed that Bbs of closely related species (belonging to the defined evolutionary line) are morphologically rather different. In two species (Meconema meridionale and Pholidoptera griseoaptera) the Bb has the form of a hollow hemisphere that covers a part of the germinal vesicle surface. In contrast, the Bb of Conocephalus fuscus and Leptophyes albovittata is less distinct and surrounds the whole or the majority of the germinal vesicle surface. Aside from this difference, the Bbs of all four studied species are built of identical sets of organelles and, most importantly, share one significant feature: close association of mitochondria and nuage accumulations. We show additionally that mitochondria remaining in direct contact with the nuage are characterized by distinct morphologies e.g. elongated, dumbbell shaped or bifurcated. In the light of our results and literature survey, the ancestral function of the Bb is discussed.


Subject(s)
Gryllidae , Animals , Oocytes/metabolism , Organelles/metabolism , Organelles/ultrastructure , Germ Cells , Mitochondria/ultrastructure , Oogenesis
7.
Sci Rep ; 11(1): 13772, 2021 07 02.
Article in English | MEDLINE | ID: mdl-34215832

ABSTRACT

Our present knowledge on interrelation between morphology/ultrastructure of mitochondria of the Leydig cell and its steroidogenic function is far from satisfactory and needs additional studies. Here, we analyzed the effects of blockade of androgen receptor, triggered by exposure to flutamide, on the expression of steroidogenic proteins (1) and ultrastructure of Leydig cells' constituents (2). We demonstrated that increase in the expression level of steroidogenic (StAR, CYP11A1, 3ß-HSD, and CYP19A1) proteins (and respective mRNAs) in rat testicular tissue as well as elevation of intratesticular sex steroid hormone (testosterone and estradiol) levels observed in treated animals correspond well to morphological alterations of the Leydig cell ultrastructure. Most importantly, up-regulation of steroidogenic proteins' expression apparently correlates with considerable multiplication of Leydig cell mitochondria and subsequent formation of local mitochondrial networks. Interestingly, we showed also that the above-mentioned processes were associated with elevated transcription of Drp1 and Mfn2 genes, encoding proteins implicated in mitochondrial dynamics. Collectively, our studies emphasize the importance of mitochondrial homeostasis to the steroidogenic function of Leydig cells.


Subject(s)
Aromatase/genetics , Cholesterol Side-Chain Cleavage Enzyme/genetics , Hydroxysteroid Dehydrogenases/genetics , Receptors, Androgen/genetics , Animals , Flutamide/pharmacology , Gene Expression Regulation, Developmental , Gonadal Steroid Hormones/biosynthesis , Gonadal Steroid Hormones/genetics , Leydig Cells/drug effects , Leydig Cells/metabolism , Luteinizing Hormone/biosynthesis , Luteinizing Hormone/metabolism , Male , Mitochondria/drug effects , Mitochondria/genetics , Mitochondria/ultrastructure , Rats , Receptors, Androgen/metabolism , Steroids/biosynthesis , Steroids/metabolism , Testis/growth & development , Testis/metabolism , Testosterone/biosynthesis , Testosterone/metabolism
8.
Reprod Toxicol ; 104: 114-124, 2021 09.
Article in English | MEDLINE | ID: mdl-34311058

ABSTRACT

Disruption of granulosa cells (GCs), the main functional cells in the ovary, is associated with impaired female fertility. Epidemiological studies demonstrated that women have detectable levels of organic pollutants (e.g., perfluorooctanoate, perfluorooctane sulfonate, 2,2-dichlorodiphenyldichloroethylene, polychlorinated biphenyl 153, and hexachlorobenzene) in their follicular fluid (FF), and thus these compounds may directly affect the function of GCs in the ovary. Considering that humans are exposed to multiple pollutants simultaneously, we elucidated the effects of a mixture of endocrine-disrupting chemicals (EDCs) on human granulosa HGrC1 cells. The EDC mixture directly increased progesterone secretion by upregulating 3ß-hydroxysteroid dehydrogenase (3ßHSD) expression. Furthermore, the EDC mixture increased activity of mitochondria, which are the central sites for steroid hormone biosynthesis, and the ATP content. Unexpectedly, the EDC mixture reduced glucose transporter 4 (GLUT4) expression and perturbed glucose uptake; however, this did not affect the glycolytic rate. Moreover, inhibition of GLUT1 by STF-31 did not alter the effects of the EDC mixture on steroid secretion but decreased basal estradiol secretion. Taken together, our results demonstrate that the mixture of EDCs present in FF can alter the functions of human GCs by disrupting steroidogenesis and may thus adversely affect female reproductive health. This study highlights that the EDC mixture elicits its effects by targeting mitochondria and increases mitochondrial network formation, mitochondrial activity, and expression of 3ßHSD, which is associated with the inner mitochondrial membrane.


Subject(s)
Follicular Fluid/metabolism , Persistent Organic Pollutants/metabolism , Progesterone/metabolism , Endocrine Disruptors/metabolism , Estradiol/metabolism , Female , Follicular Fluid/chemistry , Granulosa Cells/drug effects , Humans , Luteinization/drug effects , Mitochondria/drug effects , Ovarian Neoplasms , Persistent Organic Pollutants/toxicity , Steroids/metabolism , Up-Regulation/drug effects
9.
Postepy Biochem ; 67(4)2021 12 31.
Article in Polish | MEDLINE | ID: mdl-35107964

ABSTRACT

The Balbiani body is an organelle assemblage (termed sometimes a super-organelle) characteristic for the developing oocytes of almost all investigated animal species. In the vast majority of species, this complex resides next to the germinal vesicle and comprises such organelles as mitochondria, elements of endoplasmic reticulum, Golgi complexes as well as accumulations of nuage material. Comparative analyses have shown that the Balbiani bodies, even in closely related organisms, are often morphologically different. The differences concern not only the composition of this assemblage but also mutual relations between its components. So far, it has been found that the Balbiani body is implicated in several cellular processes undergoing in female germline cells. Most importantly this organelle complex is responsible for the delivery and localization of certain macromolecules and organelles to specific regions of the ooplasm (oocyte cytoplasm), as well as in the transfer of mitochondria to the zygote, i.e. to the next generation. Moreover, it has been shown recently that at least in some species the Balbiani body participates in the elimination of nonfunctional, damaged mitochondria from the developing oocytes and egg cells.


Subject(s)
Invertebrates , Oocytes , Animals , Endoplasmic Reticulum , Morphogenesis , Vertebrates
10.
J Morphol ; 281(9): 1142-1151, 2020 09.
Article in English | MEDLINE | ID: mdl-32767591

ABSTRACT

Balbiani body (Bb) is a female germline specific organelle complex. Although the morphology and morphogenesis of the Bb have been analyzed in numerous vertebrate and invertebrate species, the role and ultimate fate of this organelle assemblage are still under debate. As a result, various functions have been attributed to the Bb in given animal lineages or even species. Our analyses showed that in the bush cricket, Metrioptera brachyptera, the Bb is an elaborate and highly dynamic structure positioned at one side of the oocyte nucleus. It forms in early previtellogenic oocytes and consists of two compartments: perinuclear and cytoplasmic. In the cytoplasmic compartment, characteristic complexes of nuage and polymorphous mitochondria are present. Computer-aided 3D reconstructions revealed that mitochondria clustered around neighboring nuage accumulations remain in a physical contact and form an extensive, though dispersed network. As oogenesis progresses, nuage/mitochondria complexes are partitioned into progressively smaller entities that become separated from each other. Concurrently, the mitochondrial network splits into small individual mitochondria populating the whole ooplasm. Immunohistochemical analysis showed that the latter process involves dynamin-related protein 1 (Drp1). Collectively, our findings suggest that in basal insect species, the Bb might be responsible for the selection as well as multiplication of the oocyte mitochondria.


Subject(s)
Chromosomal Puffs/physiology , Germ Cells/metabolism , Insecta/anatomy & histology , Mitochondria/metabolism , Morphogenesis , Animals , Female , Imaging, Three-Dimensional , Immunohistochemistry , Mitochondria/ultrastructure , Oocytes/cytology , Oocytes/ultrastructure , Ovary/anatomy & histology , Vitellogenesis
11.
Reprod Toxicol ; 95: 1-10, 2020 08.
Article in English | MEDLINE | ID: mdl-32418891

ABSTRACT

Using JEG-3 and BeWo cells, we examined the effect of "real life" mixtures of polycyclic aromatic hydrocarbons (PAHs), at doses reported in maternal blood (Mix I) and in placental tissue (Mix II), on human chorionic gonadotropin (hCG), placental lactogen (hPL) and placental growth factor (hPLGF) secretion, protein expression and immunolocalization. Additionally, the action of PAH mixtures on basal and hormone-stimulated matrix metalloproteinase-2 (MMP-2), MMP-9 and vascular endothelial growth factor (VEGF) protein expression was evaluated. Under basal conditions, the PAH mixtures increased hCG and decreased hPLGF levels in both cell lines, while hPL expression was stimulated in JEG-3 and inhibited in BeWo. There was no effect on the MMP-2/MMP-9 ratio or VEGF expression. In hormone-stimulated cells, PAH mixtures changed the MMP-2/MMP-9 ratio in JEG-3 cells in favor of MMP-9, while in BeWo MMP-2 was favored. The effect on VEGF expression was cell specific and dependent on the mixture. In hCG-treated cells, only Mix II inhibited VEGF expression in JEG-3 cells. Neither PAH mixtures affected this protein in BeWo cells. In hPL-treated cells, Mix I had a stimulatory effect in JEG-3 cells, while Mix II exerted an inhibitory effect in BeWo cells. In hPLGF-treated cells, Mix II decreased in JEG-3 cells, but in BeWo cells, both mixtures increased VEGF expression. Considering that the evaluated protein hormones play crucial roles in angiogenesis and neovascularization in the placenta, "real life" PAH mixtures by disrupting protein hormones levels, the MMP-2/MMP-9 ratio and VEGF expression can lead to insufficiency and many pregnancy-related disorders.


Subject(s)
Placenta/cytology , Polycyclic Aromatic Hydrocarbons/toxicity , Cell Line , Chorionic Gonadotropin/metabolism , Female , Humans , Matrix Metalloproteinase 2/metabolism , Matrix Metalloproteinase 9/metabolism , Placenta Growth Factor/metabolism , Placental Lactogen/metabolism , Pregnancy , Vascular Endothelial Growth Factor A/metabolism
12.
Int J Mol Sci ; 21(10)2020 May 21.
Article in English | MEDLINE | ID: mdl-32455738

ABSTRACT

Although epidemiological studies from the last years report an increase in the incidences of Leydig cell tumors (previously thought to be a rare disease), the biochemical characteristics of that tumor important for understanding its etiology, diagnosis, and therapy still remains not completely characterized. Our prior studies reported G-protein coupled estrogen receptor signaling and estrogen level disturbances in Leydig cell tumors. In addition, we found that expressions of multi-level-acting lipid balance- and steroidogenesis-controlling proteins including peroxisome proliferator-activated receptor are altered in this tumor. In order to get deeper into the other molecular mechanisms that regulate lipid homeostasis in the Leydig cell tumor, here we investigate the presence and expression of newly-described hormones responsible for lipid homeostasis balancing (leptin and adiponectin), together with expression of estrogen synthase (aromatase). Samples of Leydig cell tumors (n = 20) were obtained from patients (31-45 years old) and used for light and transmission electron microscopic, western blotting, and immunohistochemical analyses. In addition, body mass index (BMI) was calculated. In tumor mass, abundant lipid accumulation in Leydig cells and various alterations of Leydig cell shape, as well as the presence of adipocyte-like cells, were observed. Marked lipid content and various lipid droplet size, especially in obese patients, may indicate alterations in lipid homeostasis, lipid processing, and steroidogenic organelle function in response to interstitial tissue pathological changes. We revealed significantly increased expression of leptin, adiponectin and their receptors, as well as aromatase in Leydig cell tumors in comparison to control. The majority of patients (n = 13) were overweight as indicated by their BMI. Moreover, a significant increase in expression of phospholipase C (PLC), and kinases Raf, ERK which are part of adipokine transductional pathways, was demonstrated. These data expand our previous findings suggesting that in human Leydig cell tumors, estrogen level and signaling, together with lipid status, are related to each other. Increased BMI may contribute to certain biochemical characteristics and function of the Leydig cell in infertile patients with a tumor. In addition, altered adipokine-estrogen microenvironment can have an effect on proliferation, growth, and metastasis of tumor cells. We report here various targets (receptors, enzymes, hormones) controlling lipid balance and estrogen action in Leydig cell tumors indicating their possible usefulness for diagnostics and therapy.


Subject(s)
Adiponectin/metabolism , Aromatase/metabolism , Carcinogenesis/metabolism , Leptin/metabolism , Leydig Cell Tumor/metabolism , Adult , Carcinogenesis/ultrastructure , Humans , Leydig Cell Tumor/ultrastructure , Leydig Cells/metabolism , Leydig Cells/ultrastructure , Lipid Droplets/metabolism , Male , Signal Transduction
13.
Int J Mol Med ; 45(3): 691-702, 2020 Mar.
Article in English | MEDLINE | ID: mdl-31922236

ABSTRACT

Placentation requires the production of numerous growth factors, hormones and transcription factors. Many of them, like the adipose tissue­derived leptin or adiponectin, have been identified in the placenta and their role has been established in the proliferation and subsequent development of the placenta. Apelin is another adipokine known for proliferative effects in different cell types. PCR, immunoblotting and immunocytochemistry were used to study mRNA and protein expression of apelin and its receptor (APJ) in syncytiotrophoblast (BeWo) and cytotrophoblast (JEG­3) cells as well in immunohistochemistry in human normal placenta slides. The effect of apelin on cell proliferation study was investigated by alamarBlue® and Cell Counting Kit­8 assays, the cell cycle by the flow cytometry method and the protein expression of cyclins and phosphorylation level of extracellular signal­regulated kinases (ERK)1/2, phosphatidylinositol 3'­kinase/protein kinase B (Akt), signal transducer and activator of transcription 3 (Stat3) and 5'­monophosphate­activated protein kinase (AMPKα) were studied by western blotting. Apelin was increased in JEG­3 compared with in BeWo cells, while APJ was the same in both placenta cell lines. Immunocytochemical analyses revealed high cytoplasmic and/or membrane apelin localisation in JEG­3, while BeWo cells exhibited markedly weaker apelin signal in the cytoplasm. Apelin increased cell proliferation as well as the percentage of cells in the G2/M phase of the cell cycle, cyclin proteins and the expression of all kinases mentioned above. In conclusion, apelin by promotion of trophoblast cell proliferation by APJ and ERK1/2, Stat3 and AMPKα signalling could be a new important adipokine in the regulation of early placental development.


Subject(s)
Apelin Receptors/metabolism , Apelin/metabolism , Cell Proliferation/physiology , Placenta/metabolism , Signal Transduction/physiology , Apelin/analysis , Apelin/genetics , Apelin Receptors/analysis , Apelin Receptors/genetics , Cell Cycle/physiology , Female , Humans , Placenta/chemistry , Pregnancy , Trophoblasts/metabolism
14.
Genes (Basel) ; 11(1)2020 01 16.
Article in English | MEDLINE | ID: mdl-31963356

ABSTRACT

The most important role of mitochondria is to supply cells with metabolic energy in the form of adenosine triphosphate (ATP). As synthesis of ATP molecules is accompanied by the generation of reactive oxygen species (ROS), mitochondrial DNA (mtDNA) is highly vulnerable to impairment and, consequently, accumulation of deleterious mutations. In most animals, mitochondria are transmitted to the next generation maternally, i.e., exclusively from female germline cells (oocytes and eggs). It has been suggested, in this context, that a specialized mechanism must operate in the developing oocytes enabling escape from the impairment and subsequent transmission of accurate (devoid of mutations) mtDNA from one generation to the next. Literature survey suggest that two distinct and irreplaceable pathways of mitochondria transmission may be operational in various animal lineages. In some taxa, the mitochondria are apparently selected: functional mitochondria with high inner membrane potential are transferred to the cells of the embryo, whereas those with low membrane potential (overloaded with mutations in mtDNA) are eliminated by mitophagy. In other species, the respiratory activity of germline mitochondria is suppressed and ROS production alleviated leading to the same final effect, i.e., transmission of undamaged mitochondria to offspring, via an entirely different route.


Subject(s)
DNA, Mitochondrial , Mitochondria , Mitophagy , Mutation , Oocytes/metabolism , Oogenesis , Animals , DNA, Mitochondrial/genetics , DNA, Mitochondrial/metabolism , Female , Mitochondria/genetics , Mitochondria/metabolism
15.
J Morphol ; 281(1): 47-54, 2020 01.
Article in English | MEDLINE | ID: mdl-31710388

ABSTRACT

Representatives of the highly specialized earwig family Hemimeridae are epizoic and viviparous. Their embryos develop inside terminal ovarian follicles (termed also embryonic follicles) and rely solely on nutrients transferred from mother tissues. In this report, we present results of ultrastructural and histochemical studies of the initial stage of Hemimerus talpoides development. Our results show that the follicular cells surrounding fully grown oocyte of Hemimerus do not degenerate after initiation of embryogenesis, but transform and gradually form the wall of the incubation chamber in which the embryo develops. We also show that amniotic cells of the early embryo remain in direct contact with transformed follicular cells. In the region of contact, short outgrowths of the amniotic cells associate with irregular surface specializations of the transformed follicular cells. We suggest that extended "postfertilization" activity of hemimerid follicular cells represents an adaptation to viviparity and matrotrophy in this insect lineage.


Subject(s)
Embryonic Development , Epithelium/embryology , Insecta/embryology , Morphogenesis , Ovarian Follicle/growth & development , Viviparity, Nonmammalian , Animals , Embryo, Nonmammalian/anatomy & histology , Embryo, Nonmammalian/ultrastructure , Epithelium/ultrastructure , Female , Insecta/ultrastructure , Ovarian Follicle/ultrastructure
16.
Sci Rep ; 9(1): 16090, 2019 11 06.
Article in English | MEDLINE | ID: mdl-31695096

ABSTRACT

Although pregenital abdominal outgrowths occur only rarely in pterygote insects, they are interesting from the evolutionary viewpoint because of their potential homology to wings. Our previous studies of early development of an epizoic dermapteran, Arixenia esau revealed that abdominal segments of the advanced embryos and larvae, growing inside a mother's uterus, are equipped with paired serial outgrowths. Here, we focus on the origin and functioning of these outgrowths. We demonstrate that they bud from the lateral parts of the abdominal nota, persist till the end of intrauterine development, and remain in contact with the uterus wall. We also show that the bundles of muscle fibers associated with the abdominal outgrowths may facilitate flow of the haemolymph from the outgrowths' lumen to the larval body cavity. Following completion of the intrauterine development, abdominal outgrowths are shed together with the larval cuticle during the first molt after the larva birth. Using immunohistochemical and biochemical approaches, we demonstrate that the Arixenia abdominal outgrowths represent an evolutionary novelty, presumably related to intrauterine development, and suggest that they are not related to serial wing homologs.


Subject(s)
Biological Evolution , Neoptera/growth & development , Abdomen/growth & development , Animals , Female , Larva/genetics , Larva/growth & development , Male , Neoptera/genetics , Wings, Animal/growth & development
17.
Results Probl Cell Differ ; 68: 455-475, 2019.
Article in English | MEDLINE | ID: mdl-31598867

ABSTRACT

Nutritional modes operating during embryonic/larval development of viviparous species range from "pure" lecitothrophy in which embryos rely solely on reserve materials (yolk spheres, lipid droplets, and glycogen particles) accumulated in the egg cytoplasm to matrotrophy in which embryos are continuously supplied with nutrients from a parental organism. Interestingly, a wide spectrum of diverse "mixed" modes employed in the embryo nourishment have also been described among viviparous species. Here, we summarize results of histochemical, ultrastructural, and biochemical analyses of reproductive systems as well as developing embryos of two closely related viviparous species of earwigs (Dermaptera), Hemimerus talpoides and Arixenia esau. These analyses clearly indicate that morphological as well as physiological modifications (adaptations) supporting viviparity and matrotrophy in Hemimerus and Arixenia, with the exception of a complex biphasic respiration, are markedly different. Most importantly, Hemimerus embryos complete their development inside terminal (largest) ovarian follicles, whereas Arixenia embryos, after initial developmental stages, are transferred to highly modified lateral oviducts, that is the uterus, where they develop until the release (birth) of larvae. The obtained results strongly suggest that viviparity in hemimerids and arixeniids had evolved independently and might therefore serve as an example of evolutionary parallelism as well as remarkable functional plasticity of insect reproduction and embryonic development.


Subject(s)
Biological Evolution , Embryonic Development , Neoptera/embryology , Neoptera/physiology , Ovarian Follicle/physiology , Oviducts/physiology , Reproduction/physiology , Viviparity, Nonmammalian/physiology , Animals , Female , Larva , Neoptera/anatomy & histology
18.
Protoplasma ; 256(6): 1573-1584, 2019 Nov.
Article in English | MEDLINE | ID: mdl-31218520

ABSTRACT

Earwigs (Dermaptera) use different strategies to increase their reproductive success. Most species lay eggs; however, viviparity of the matrotrophic type has been reported in two groups: Hemimeridae and Arixeniidae. In Arixeniidae, offspring develop in two separate places: inside an ovary (the intraovarian phase) and within a uterus (the intrauterine phase). Both morphological and physiological aspects of viviparity in Arixeniidae have begun to be unraveled only recently. Here, we characterize how the first instar larvae of Arixenia esau, developing inside the mother's reproductive system, manage respiration and gas exchange. Using modern light and electron microscopy techniques as well as immunological approach, we provide a detailed account of the maternal and larval tissue interactions during the intrauterine development. We demonstrate that respiration in the Arixenia first instar larvae relies on the extensive tracheal system of the mother as well as a respiratory pigment (hemocyanin) present within the body cavity of the larvae. Our results indicate that the larval fat body tissue is the likely place of the hemocyanin synthesis. Our study shows that characteristic cone-shaped lobes of the outgrowths located on the larval abdomen are a part of a placenta-like organ and mediate the gas exchange between the maternal and larval organisms. Based on the obtained results, we propose that Arixenia esau evolved a unique biphasic system supporting respiration of the first instar larvae during their development inside the mother's reproductive tract.


Subject(s)
Insecta/physiology , Animals , Viviparity, Nonmammalian
19.
Curr Opin Insect Sci ; 31: 1-7, 2019 02.
Article in English | MEDLINE | ID: mdl-31109662

ABSTRACT

Besides reserve materials (yolk spheres, lipid droplets), ribosomes and various mRNA species, insect oocytes contain large easily morphologically recognizable organelle assemblages: the Balbiani body and the oosome (pole plasm). These assemblages are implicated in the transfer of oocyte components (mitochondria, polar granules) to the embryo that is to offspring. Here, we review present knowledge of morphology, morphogenesis, molecular composition and function/s of these assemblages. We discuss also the morphogenesis and presumed function of unconventional organelle assemblages, dormant stacks of endoplasmic reticulum, recently described in the oocytes and early embryos of a viviparous dermapteran, Hemimerus talpoides.


Subject(s)
Insecta/embryology , Oocytes/cytology , Organelles , Animals , Endoplasmic Reticulum , Neoptera/cytology , Oocytes/growth & development
20.
Arthropod Struct Dev ; 49: 62-69, 2019 Mar.
Article in English | MEDLINE | ID: mdl-30445116

ABSTRACT

The embryos and first instar larvae of the epizoic earwig, Arixenia esau, develop sequentially in two different compartments of the female reproductive system, that is ovarian follicles and the lateral oviducts (the uterus). Here we show that the second (intrauterine) phase of development consists of three physiologically disparate stages: early embryos (before dorsal closure, surrounded by an egg envelope), late embryos (after dorsal closure, surrounded by an egg envelope) and the first instar larvae (after "hatching" from an egg envelope). Early and late embryos float in the fluid filling the uterus, whereas the first instar larvae develop attached to the uterus wall. Our analyses revealed also that in Arixenia serial multilobed outgrowths develop on dorso-lateral aspects of all abdominal segments. At the onset of the third developmental stage and after liberation from an egg envelope, these outgrowths (or more precisely their lobes) adhere to the epithelium lining the uterus, forming a series of small contact sites, where the mother and embryo tissues are separated only by a thin, presumably permeable, embryonic cuticle. We suggest that all these contact sites collectively constitute a dispersed placenta-like organ involved in the nourishment of the embryo.


Subject(s)
Morphogenesis , Neoptera/growth & development , Abdomen/anatomy & histology , Abdomen/growth & development , Animals , Embryo, Nonmammalian/embryology , Embryonic Development , Female , Larva/anatomy & histology , Larva/growth & development , Larva/ultrastructure , Microscopy, Electron, Scanning , Neoptera/anatomy & histology , Neoptera/embryology , Neoptera/ultrastructure
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