bims-gamemb Biomed News
on Gamete and embryo metabolism
Issue of 2022–02–20
twelve papers selected by
Cameron A. Schmidt, East Carolina University
  1. Role of Granulosa Cells in the Aging Ovarian Landscape: A Focus on Mitochondrial and Metabolic Function.
  2. Impact of L-carnitine supplementation on the in vitro developmental competence and cryotolerance of buffalo embryos.
  3. Aldose Reductase B1 in Pig Sperm Is Related to Their Function and Fertilizing Ability.
  4. Mitochondrial DNA content reduction in the most fertile spermatozoa is accompanied by increased mitochondrial DNA rearrangement.
  5. Early seed development requires the A-type ATP-binding cassette protein ABCA10.
  6. Ras-related proteins (Rab) play significant roles in sperm motility and capacitation status.
  7. The stallion spermatozoa: A valuable model to help understand the interplay between metabolism and redox (de)regulation in sperm cells.
  8. Female fertility: The role of mitochondrial protease LONP1 in oocyte development and survival.
  9. The Non-Gastric H+/K+ ATPase (ATP12A) Is Expressed in Mammalian Spermatozoa.
  10. All for one - changes in mitochondrial morphology and activity during syncytial oogenesis.
  11. Lactate Activates Germline and Cleavage Embryo Genes in Mouse Embryonic Stem Cells.
  12. Did doubly uniparental inheritance (DUI) of mtDNA originate as a cytoplasmic male sterility (CMS) system?
  1. Front Physiol. 2021 ;12 800739
    Role of Granulosa Cells in the Aging Ovarian Landscape: A Focus on Mitochondrial and Metabolic Function.
    Hannah C Alberico, Dori C Woods.
      Mitochondria are at the intersection of aging and fertility, with research efforts centered largely on the role that these specialized organelles play in the relatively rapid decline in oocyte quality that occurs as females approach reproductive senescence. In addition to various roles in oocyte maturation, fertilization, and embryogenesis, mitochondria are critical to granulosa cell function. Herein, we provide a review of the literature pertaining to the role of mitochondria in granulosa cell function, with emphasis on how mitochondrial aging in granulosa cells may impact reproduction in female mammals.
    Keywords:  granulosa cells; mitochondria; oocytes; ovarian aging; reproduction
    DOI:  https://doi.org/10.3389/fphys.2021.800739
  2. Vet World. 2021 Dec;14(12): 3164-3169
    Impact of L-carnitine supplementation on the in vitro developmental competence and cryotolerance of buffalo embryos.
    Mohamed M M El-Sokary, Al-Shimaa Al-H H El-Naby, Amal R Abd El Hameed, Karima Gh M Mahmoud, T H Scholkamy.
       Background and Aim: Despite many trials, buffalo embryos have poor cryosurvivability because of their high lipid content. L-carnitine was found to be a lipid-reducing agent when added to oocyte and embryo culture media. The study aimed to determine the most effective concentration of L-carnitine to improve the oocyte developmental competence and cryotolerance of buffalo embryos.
    Materials and Methods: In vitro maturation and embryo culture media were supplemented with four concentrations of L-carnitine: 0 (control), 0.25, 0.5, and 1 mM. Good-quality embryos on 7 days were vitrified using mixtures of dimethyl sulfoxide and ethylene glycol at two concentrations (3.5 and 7 M).
    Results: The result showed that the cleavage and morula rates were significantly (p<0.05) higher in the 0.5 mM group. Blastocyst rates were significantly (p<0.05) higher at both 0.5 and 1 mM. The rates of viable embryos directly after thawing were significantly (p<0.05) increased in the 0.5 mM group. No significant difference was found in embryos cultured for 24 h after warming among all the groups.
    Conclusion: The addition of L-carnitine at a concentration of 0.5 mM to the culture media improves the oocyte developmental competence and cryotolerance of buffalo embryos directly after warming but not after 24 h of culture. Nevertheless, further studies must identify how L-carnitine exerts its beneficial micromechanisms.
    Keywords:  L-carnitine; antioxidant; buffalo embryos; cryotolerance
    DOI:  https://doi.org/10.14202/vetworld.2021.3164-3169
  3. Front Endocrinol (Lausanne). 2022 ;13 773249
    Aldose Reductase B1 in Pig Sperm Is Related to Their Function and Fertilizing Ability.
    Yentel Mateo-Otero, Jordi Ribas-Maynou, Ariadna Delgado-Bermúdez, Marc Llavanera, Sandra Recuero, Isabel Barranco, Marc Yeste.
      Aldose reductase B1 (AKR1B1) has been reported to participate in the modulation of male and female reproductive physiology in several mammalian species. In spite of this, whether or not AKR1B1 could be related to sperm quality, functionality and fertilizing ability is yet to be elucidated. The present study, therefore, aimed to investigate: i) the presence of AKR1B1 in epididymal and ejaculated sperm; ii) the relationship between the AKR1B1 present in sperm and the physiology of the male gamete; iii) the liaison between the relative content of AKR1B1 in sperm and their ability to withstand preservation for 72 h; and iv) the potential link between sperm AKR1B1 and in vitro fertility outcomes. Immunoblotting revealed that AKR1B1 is present in both epididymal and ejaculated sperm with a similar relative content. Moreover, the relative levels of AKR1B1 in sperm (36 kDa band) were found to be negatively related to several kinematic parameters and intracellular calcium levels, and positively to the percentage of sperm with distal cytoplasmic droplets after storage. Finally, AKR1B1 amounts in sperm (36 kDa band) were negatively associated to fertilization rate at two days post-fertilization and embryo development at six days post-fertilization. The results of the present work suggest that AKR1B1 in sperm is probably acquired during maturation rather than at ejaculation and could play a role in that process. Moreover, AKR1B1 seems to be related to the sperm resilience to preservation and to their fertilizing capacity, as lower levels of the 36 kDa band (putative inactive form of this protein) result in better reproductive outcomes.
    Keywords:  AKR1B1; aldose reductase B1; ejaculated sperm; epididymal maturation; in vitro fertilization (IVF); sperm physiology
    DOI:  https://doi.org/10.3389/fendo.2022.773249
  4. Hum Reprod. 2022 Feb 12. pii: deac024. [Epub ahead of print]
    Mitochondrial DNA content reduction in the most fertile spermatozoa is accompanied by increased mitochondrial DNA rearrangement.
    M Boguenet, V Desquiret-Dumas, D Goudenège, C Bris, L Boucret, O Blanchet, V Procaccio, P E Bouet, P Reynier, P May-Panloup.
       STUDY QUESTION: Is there an association between male fertility and spermatozoa mitochondrial DNA (mtDNA) copy number and genome rearrangements?
    SUMMARY ANSWER: Normal spermatozoa not only have a lower mtDNA copy number but also more DNA rearrangements than spermatozoa of men with severe oligoasthenospermia (SOA).
    WHAT IS KNOWN ALREADY: While there is a consensus that mtDNA content is decreased in the most fertile spermatozoa, the role of mtDNA sequence alteration in male infertility is unclear. High-throughput sequencing, which allows an exhaustive analysis of mtDNA rearrangements and mutations, could be helpful in this context, but has yet to be used.
    STUDY DESIGN, SIZE, DURATION: This is an observational study of semen samples obtained from 44 men undergoing ART at an academic infertility centre in France, from October 2018 to November 2020. The men were classified into two groups: 20 men in the SOA group and 24 men with normal semen parameters in the control group.
    PARTICIPANTS/MATERIALS, SETTING, METHODS: For each patient and control, mtDNA was isolated from sperm fractions from the 40% and 90% layers of the density gradient. The average mtDNA content of each sample was assessed using digital PCR. Deep sequencing was performed using next-generation sequencing. Signal processing and base calling were performed via the embedded pre-processing pipeline, the variants were analysed using an in-house workflow and a dedicated tool, based on soft-clipping, was used to study large mtDNA rearrangements. The distribution and the type of rearrangements and variants were compared between patients with SOA and controls on one hand, and between the 40% and 90% gradient layers, on the other hand.
    MAIN RESULTS AND THE ROLE OF CHANCE: The mtDNA content of spermatozoa in the SOA group was significantly higher than in the control group (P < 0.0001). Moreover, mtDNA content was significantly higher in spermatozoa from the 40% layer (the most fertile spermatozoa) compared to the 90% layer, both in the SOA (P = 0.02) and the control group (P < 0.0001). The frequency of large mtDNA deletions and duplications was significantly higher in the control group (P = 0.002). Most of these rearrangements are potentially related to DNA breaks and their number was reduced by the removal of the linear mtDNA from the samples. Heteroplasmic variants were found more frequently in the SOA group (P = 0.05) and in the 40% layer (P = 0.03), but none had any obvious functional consequence.
    LIMITATIONS, REASONS FOR CAUTION: Our findings are novel and significant but should be verified in larger cohorts and other types of male infertility.
    WIDER IMPLICATIONS OF THE FINDINGS: Our findings suggest that sperm mtDNA rearrangements are not necessarily associated with mitochondrial dysfunction and male infertility. Instead, they seem to be concomitant with the process of mtDNA content reduction in the most potentially fertile spermatozoa. Furthermore, they refute the hypothesis that, in the case of mtDNA alteration, a compensatory mechanism allows an increase in mtDNA copy number to rectify the energy deficit. The increased frequency of mtDNA rearrangements in the most fertile spermatozoa is a novel result that offers new insight into the relation between sperm quality and mtDNA.
    STUDY FUNDING/COMPETING INTEREST(S): This work was supported by Angers University Hospital (grant AOI CHU Angers 2018), Angers University and the French national research centres INSERM and CNRS. There are no competing interests.
    TRIAL REGISTRATION NUMBER: N/A.
    Keywords:  copy number; digital PCR; male infertility; mitochondrial DNA; next-generation sequencing; oligoasthenospermia; rearrangements; spermatozoa
    DOI:  https://doi.org/10.1093/humrep/deac024
  5. Plant Physiol. 2022 Feb 15. pii: kiac062. [Epub ahead of print]
    Early seed development requires the A-type ATP-binding cassette protein ABCA10.
    Seungjun Shin, Chayanee Chairattanawat, Yasuyo Yamaoka, Qianying Yang, Youngsook Lee, Jae-Ung Hwang.
      A-type ATP-binding cassette (ABCA) proteins transport lipids and lipid-based molecules in humans, and their malfunction is associated with various inherited diseases. Although plant genomes encode many ABCA transporters, their molecular and physiological functions remain largely unknown. Seeds are rapidly developing organs that rely on the biosynthesis and transport of large quantities of lipids to generate new membranes and storage lipids. In this study, we characterized the Arabidopsis (Arabidopsis thaliana) ABCA10 transporter, which is selectively expressed in female gametophytes and early developing seeds. By 3 days after flowering (DAF), seeds from the abca10 loss-of-function mutant exhibited a smaller chalazal endosperm than those of the wild type. By 4 DAF, their endosperm nuclei occupied a smaller area than those of the wild type. The endosperm nuclei of the mutants also failed to distribute evenly inside the seed coat and stayed aggregated instead, possibly due to inadequate expansion of abca10 endosperm. This endosperm defect might have retarded abca10 embryo development. At 7 DAF, a substantial portion of abca10 embryos remained at the globular or earlier developmental stages, whereas wild-type embryos were at the torpedo or later stages. ABCA10 is likely involved in lipid metabolism, as ABCA10 overexpression induced the overaccumulation of triacylglycerol but did not change the carbohydrate or protein contents in seeds. In agreement, ABCA10 localized to the endoplasmic reticulum (ER), the major site of lipid biosynthesis. Our results reveal that ABCA10 plays an essential role in early seed development, possibly by transporting substrates for lipid metabolism to the ER.
    DOI:  https://doi.org/10.1093/plphys/kiac062
  6. Reprod Biol. 2022 Feb 15. pii: S1642-431X(22)00016-X. [Epub ahead of print]22(2): 100617
    Ras-related proteins (Rab) play significant roles in sperm motility and capacitation status.
    Jeong-Won Bae, Jun Koo Yi, Eun-Ju Jeong, Woo-Jin Lee, Ju-Mi Hwang, Dae-Hyun Kim, Jae Jung Ha, Woo-Sung Kwon.
      Rab proteins are widely known for their involvement in establishing Golgi apparatus and controlling Golgi trafficking in eukaryotic cells. Specifically, Rab proteins play significant roles in acrosome formation and exocytosis. Furthermore, mechanisms involved in the regulation of Rab proteins during capacitation have been identified. However, there has been no direct evaluation to assess the correlation between Rab proteins and sperm function. Consequently, this study was designed to analyze the correlation between Rab proteins and sperm functions. Individually, we analyzed the sperm motility patterns, motion kinematics, capacitation status, and Rab protein expression levels of sperm samples from 31 boars before and after capacitation. As a result, we discovered that Rab3A, Rab5, Rab11, Rab14, and Rab27A correlated with various sperm motility patterns, motion kinematics before capacitation. Rab3A, Rab5, Rab11, Rab14, and Rab34 correlated with various sperm motility patterns, motion kinematics after capacitation. Moreover, Rab4 and Rab34 were associated with capacitation status before capacitation, and Rab3A, 25, and 27A correlated with capacitation status after capacitation. This is the first study to analyze the correlation between Rab proteins and sperm functions. Collectively, our results indicate that specific sperm motility and kinematics, as well as the structural condition of the sperm head and capacitation status, regulate individual Rab protein. Therefore, we expect that the current findings will be used to identify the etiology of idiopathic male infertility patients and to diagnose male fertility and that Rab proteins will be employed as biomarkers to predict and analyze male fertility.
    Keywords:  Capacitation; Correlation; Motion kinematics; Rab proteins; Sperm motility
    DOI:  https://doi.org/10.1016/j.repbio.2022.100617
  7. Antioxid Redox Signal. 2022 Feb 18.
    The stallion spermatozoa: A valuable model to help understand the interplay between metabolism and redox (de)regulation in sperm cells.
    Fernando J Peña, Cristian O'Flaherty, Jose M Ortiz Rodríguez, Francisco E Martin Cano, Gemma L Gaitskell-Phillips, Maria C Gil, Cristina Ortega-Ferrusola.
      Proper functionality of the spermatozoa depends on the tight regulation of their redox status, at the same time these cells are very energy demanding, and in the energetic metabolism, reactive oxygen species (ROS) are continuously produced, mainly in the electron transport chain, but also in the Krebs Cycle and during the beta oxidation of fatty acids. Additionally, in the glycolysis, elimination of phosphate groups from the trioses phosphates glyceraldehyde 3-phosphate and dihydroxyacetone phosphate originates as byproducts glyoxal (G) and methylglyoxal (MG); these products are 2-oxoaldehydes and due to their adjacent carbonyl groups are strong electrophiles that react rapidly and spontaneously with nucleophiles of proteins, lipids and DNA, forming advanced glycation end products (AGEs). This mechanism is behind subfertility in diabetic patients; in the animal breeding industry, commercial extenders for stallion semen contain a supraphysiological concentration of glucose that promote the production of methylglyoxal, constituting a potential model of interest. Increasing our knowledge on sperm metabolism and its interactions with redox regulation, may improve current sperm technologies in use and shall provide new clues to the understanding of male factor infertility.
    DOI:  https://doi.org/10.1089/ars.2021.0092
  8. EBioMedicine. 2022 Feb 15. pii: S2352-3964(22)00065-2. [Epub ahead of print]77 103881
    Female fertility: The role of mitochondrial protease LONP1 in oocyte development and survival.
    Lu Mu, Hua Zhang.
      
    DOI:  https://doi.org/10.1016/j.ebiom.2022.103881
  9. Int J Mol Sci. 2022 Jan 19. pii: 1048. [Epub ahead of print]23(3):
    The Non-Gastric H+/K+ ATPase (ATP12A) Is Expressed in Mammalian Spermatozoa.
    Maria Favia, Andrea Gerbino, Elisabetta Notario, Vincenzo Tragni, Maria Noemi Sgobba, Maria Elena Dell'Aquila, Ciro Leonardo Pierri, Lorenzo Guerra, Elena Ciani.
      H+/K+ ATPase Type 2 is an heteromeric membrane protein involved in cation transmembrane transport and consists of two subunits: a specific α subunit (ATP12A) and a non-specific β subunit. The aim of this study was to demonstrate the presence and establish the localization of ATP12A in spermatozoa from Bubalus bubalis, Bos taurus and Ovis aries. Immunoblotting revealed, in all three species, a major band (100 kDa) corresponding to the expected molecular mass. The ATP12A immunolocalization pattern showed, consistently in the three species, a strong signal at the acrosome. These results, described here for the first time in spermatozoa, are consistent with those observed for the β1 subunit of Na+/K+ ATPase, suggesting that the latter may assemble with the α subunit to produce a functional ATP12A dimer in sperm cells. The above scenario appeared to be nicely supported by 3D comparative modeling and interaction energy calculations. The expression of ATP12A during different stages of bovine sperm maturation progressively increased, moving from epididymis to deferent ducts. Based on overall results, we hypothesize that ATP12A may play a role in acrosome reactions. Further studies will be required in order to address the functional role of this target protein in sperm physiology.
    Keywords:  3D molecular modelling; Bos taurus; Bubalus bubalis; H+/K+ ATPase; Ovis aries; Western blot; immunofluorescence; in silico sequence analysis; spermatozoa
    DOI:  https://doi.org/10.3390/ijms23031048
  10. Biol Reprod. 2022 Feb 14. pii: ioac035. [Epub ahead of print]
    All for one - changes in mitochondrial morphology and activity during syncytial oogenesis.
    Anna Z Urbisz, Łukasz Chajec, Karol Małota, Sebastian Student, Marta K Sawadro, Małgorzata A Śliwińska, Piotr Świątek.
      The syncytial groups of germ cells (germ-line cysts) forming in ovaries of clitellate annelids are an attractive model to study mitochondrial stage-specific changes. Using transmission electron microscopy, serial block-face scanning electron microscopy, and fluorescent microscopy, we analyzed the mitochondria distribution and morphology and the state of membrane potential in female cysts in Enchytraeus albidus. We visualized in 3D at the ultrastructural level mitochondria in cysts at successive stages: 2-celled, 4-celled, 16-celled cysts, and cyst in advanced oogenesis. We found that mitochondria form extensive aggregates - they are fused and connected into large and branched mitochondrial networks. The most extensive networks are formed with up to 10,000 fused mitochondria, whereas individual organelles represent up to 2% of the total mitochondrial volume. We classify such morphology of mitochondria as a dynamic hyperfusion state, and suggest that it can maintain their high activity and intensifies the process of cellular respiration within the syncytial cysts. We found some individual mitochondria undergoing degradation, which implies that damaged mitochondria are removed from networks for their final elimination. As it was shown that growing oocytes possess less active mitochondria than the nurse cells, it suggests that the high activity of mitochondria in the nurse cells and their dynamic hyperfusion state serve the needs of the growing oocyte. Additionally, we measured by calorimetry the total antioxidant capacity of germ-line cysts in comparison to somatic tissue, and it suggests that antioxidative defense systems, together with mitochondrial networks, can effectively protect germ-line mitochondria from damage.
    Keywords:  fusionfissionnurse celloocytegerm-line cyst
    DOI:  https://doi.org/10.1093/biolre/ioac035
  11. Cells. 2022 Feb 04. pii: 548. [Epub ahead of print]11(3):
    Lactate Activates Germline and Cleavage Embryo Genes in Mouse Embryonic Stem Cells.
    Qing Tian, Li-Quan Zhou.
      Lactate was recently found to mediate histone lysine lactylation and facilitate polarization of M1 macrophages, indicating its role in metabolic regulation of gene expression. During somatic cell reprogramming, lactate promotes histone lactylation of pluripotency genes and improves reprogramming efficiency. However, the function of lactate in cell fate control in embryonic stem cells (ESCs) remains elusive. In this study, we revealed that lactate supplementation activated germline genes in mouse ESCs. Lactate also induced global upregulation of cleavage embryo genes, such as members of the Zscan4 gene family. Further exploration demonstrated that lactate stimulated H3K18 lactylation accumulation on germline and cleavage embryo genes, which in turn promoted transcriptional elongation. Our findings indicated that lactate supplementation expanded the transcriptional network in mouse ESCs.
    Keywords:  cell fate; germline gene; histone lactylation; lactate; zygotic genome activation
    DOI:  https://doi.org/10.3390/cells11030548
  12. Bioessays. 2022 Feb 16. e2100283
    Did doubly uniparental inheritance (DUI) of mtDNA originate as a cytoplasmic male sterility (CMS) system?
    Sophie Breton, Donald T Stewart, Julie Brémaud, Justin C Havird, Chase H Smith, Walter R Hoeh.
      Animal and plant species exhibit an astonishing diversity of sexual systems, including environmental and genetic determinants of sex, with the latter including genetic material in the mitochondrial genome. In several hermaphroditic plants for example, sex is determined by an interaction between mitochondrial cytoplasmic male sterility (CMS) genes and nuclear restorer genes. Specifically, CMS involves aberrant mitochondrial genes that prevent pollen development and specific nuclear genes that restore it, leading to a mixture of female (male-sterile) and hermaphroditic individuals in the population (gynodioecy). Such a mitochondrial-nuclear sex determination system is thought to be rare outside plants. Here, we present one possible case of CMS in animals. We hypothesize that the only exception to the strict maternal mtDNA inheritance in animals, the doubly uniparental inheritance (DUI) system in bivalves, might have originated as a mitochondrial-nuclear sex-determination system. We document and explore similarities that exist between DUI and CMS, and we propose various ways to test our hypothesis.
    Keywords:  bivalves; mitochondria; mitonuclear interactions; plants; sex determination
    DOI:  https://doi.org/10.1002/bies.202100283
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