bims-gamemb 2022-01-09 papers

bims-gamemb

Biomed News

on Gamete and embryo metabolism

Issue of 2022‒01‒09
seven papers selected by
Cameron A. Schmidt
East Carolina University

Phosphoglycerate mutase family member 5 maintains oocyte quality via mitochondrial dynamic rearrangement during aging.
Age-associated changes in cumulus cells and follicular fluid: The local oocyte microenvironment as a determinant of gamete quality.
Cell maturation: Hallmarks, triggers, and manipulation.
Biochemical changes in the cytoplasm of bovine oocytes during the in vitro maturation process: a Raman microscopy study.
TMT-Based Quantitative Proteomic Analysis Reveals the Physiological Regulatory Networks of Embryo Dehydration Protection in Lotus (Nelumbo nucifera).
Loss of PDK1 Induces Meiotic Defects in Oocytes From Diabetic Mice.
Widely targeted metabolome profiling of different colored sesame (Sesamum indicum L.) seeds provides new insight into their antioxidant activities.

Aging Cell. 2022 Jan 07. e13546

Phosphoglycerate mutase family member 5 maintains oocyte quality via mitochondrial dynamic rearrangement during aging.

Chia-Jung Li, Li-Te Lin, Hsiao-Wen Tsai, Zhi-Hong Wen, Kuan-Hao Tsui.

  Decline in ovarian reserve with aging is associated with reduced fertility and the development of metabolic abnormalities. Once mitochondrial homeostasis is imbalanced, it may lead to poor reproductive cell quality and aging. However, Phosphoglycerate translocase 5 (PGAM5), located in the mitochondrial membrane, is associated with necroptosis, apoptosis, and mitophagy, although the underlying mechanisms associated with ovarian aging remain unknown. Therefore, we attempted to uncover whether the high phosphoglycerate mutant enzyme family member 5 (PGAM5) expression is associated with female infertility in cumulus cells, and aims to find out the underlying mechanism of action of PGAM5. We found that PGAM5 is highly expressed and positively associated with aging, and has the potential to help maintain and regulate mitochondrial dynamics and metabolic reprogramming in aging granulosa cells, ovaries of aged female mice, and elderly patients. PGAM5 undergoes activation in the aging group and translocated to the outer membrane of mitochondria, co-regulating DRP1; thereby increasing mitochondrial fission. A significant reduction in the quality of mitochondria in the aging group, a serious imbalance, and a significant reduction in energy, causing metabolism shift toward glycolysis, were also reported. Since PGAM5 is eliminated, the mitochondrial function and metabolism of aging cells are partially reversed. A total of 70 patients undergoing in vitro fertilization (IVF) treatment were recruited in this clinical study. The high expression of PGAM5 in the cumulus cells is negatively correlated with the pregnancy rate of infertile patients. Hence, PGAM5 has immense potential to be used as a diagnostic marker.

Keywords:  PGAM5; cumulus cells; granulosa cells; infertility; mitochondrial dynamics

DOI:  https://doi.org/10.1111/acel.13546
Biol Reprod. 2022 Jan 04. pii: ioab241. [Epub ahead of print]

Age-associated changes in cumulus cells and follicular fluid: The local oocyte microenvironment as a determinant of gamete quality.

Elnur Babayev, Francesca E Duncan.

  The ovary is the first organ to age in humans with functional decline evident already in women in their early thirties. Reproductive aging is characterized by a decrease in oocyte quantity and quality which is associated with an increase in infertility, spontaneous abortions, and birth defects. Reproductive aging also has implications for overall health due to decreased endocrinological output. Understanding the mechanisms underlying reproductive aging has significant societal implications as women globally are delaying childbearing and medical interventions have greatly increased the interval between menopause and total lifespan. Age-related changes inherent to the female gamete are well-characterized and include defects in chromosome and mitochondria structure, function, and regulation. More recently, it has been appreciated that the extra-follicular ovarian environment may have important direct or indirect impacts on the developing gamete, and age-dependent changes include increased fibrosis, inflammation, stiffness, and oxidative damage. The cumulus cells and follicular fluid which directly surround the oocyte during its final growth phase within the antral follicle represent additional critical local microenvironments. Here we systematically review the literature and evaluate the studies that investigated the age-related changes in cumulus cells and follicular fluid. Our findings demonstrate unique genetic, epigenetic, transcriptomic, and proteomic changes with associated metabolomic alterations, redox status imbalance, and increased apoptosis in the local oocyte microenvironment. We propose a model of how these changes interact, which may explain the rapid decline in gamete quality with age. We also review the limitations of published studies and highlight future research frontiers.

Keywords:  angiogenesis; apoptosis; epigenome; extracellular matrix; metabolism; mitochondrial DNA; proteome; reactive oxygen species; telomere; transcriptome

DOI:  https://doi.org/10.1093/biolre/ioab241
Cell. 2021 Dec 30. pii: S0092-8674(21)01450-1. [Epub ahead of print]

Cell maturation: Hallmarks, triggers, and manipulation.

Juan R Alvarez-Dominguez, Douglas A Melton.

  How cells become specialized, or "mature," is important for cell and developmental biology. While maturity is usually deemed a terminal fate, it may be more helpful to consider maturation not as a switch but as a dynamic continuum of adaptive phenotypic states set by genetic and environment programing. The hallmarks of maturity comprise changes in anatomy (form, gene circuitry, and interconnectivity) and physiology (function, rhythms, and proliferation) that confer adaptive behavior. We discuss efforts to harness their chemical (nutrients, oxygen, and growth factors) and physical (mechanical, spatial, and electrical) triggers in vitro and in vivo and how maturation strategies may support disease research and regenerative medicine.

Keywords:  biomaterials; cell maturity; circadian rhythms; directed stem cell differentiation; energy metabolism; machine–tissue interfaces; microfluidic chips; nanotechnology; organoids; tissue anatomy and physiology

DOI:  https://doi.org/10.1016/j.cell.2021.12.012
Vet Res Commun. 2022 Jan 07.

Biochemical changes in the cytoplasm of bovine oocytes during the in vitro maturation process: a Raman microscopy study.

Luis Emanuel Jimenez, Ana Carolina Juárez, Mariela Roldán-Olarte, Rosa María Susana Álvarez.

  The sequence and chronology of the main biochemical changes occurring in the cytoplasm of bovine oocytes during the in vitro maturation process were tracked by Raman microscopy applied to cells previously subjected to enzymatic digestion of the zona pellucida. Specific spectral markers for proteins, lipids and carbohydrates were used to evaluate the developmental status of the ooplasm at four different times. Spectral changes revealed that lipid accumulation was dominant during the first six hours of culture while protein content reached the average levels characteristic of mature oocytes within the last four hours of the maturation process. A time-dependent decrease in carbohydrates was also observed. Finally, the carbohydrate-to-protein (P1037/P1002) ratio proved to be sensitive enough to determine the cytoplasmic maturation state of bovine oocytes and promises to be useful in future research aimed at optimizing culture conditions through the promotion of protein accumulation in the ooplasm.

Keywords:  Bovine ooplasm; Lipids; Macromolecules; Proteins

DOI:  https://doi.org/10.1007/s11259-021-09882-4
Front Plant Sci. 2021 ;12 792057

TMT-Based Quantitative Proteomic Analysis Reveals the Physiological Regulatory Networks of Embryo Dehydration Protection in Lotus (Nelumbo nucifera).

Di Zhang, Tao Liu, Jiangyuan Sheng, Shan Lv, Li Ren.

  Lotus is an aquatic plant that is sensitive to water loss, but its seeds are longevous after seed embryo dehydration and maturation. The great difference between the responses of vegetative organs and seeds to dehydration is related to the special protective mechanism in embryos. In this study, tandem mass tags (TMT)-labeled proteomics and parallel reaction monitoring (PRM) technologies were used to obtain novel insights into the physiological regulatory networks during lotus seed dehydration process. Totally, 60,266 secondary spectra and 32,093 unique peptides were detected. A total of 5,477 proteins and 815 differentially expressed proteins (DEPs) were identified based on TMT data. Of these, 582 DEPs were continuously downregulated and 228 proteins were significantly up-regulated during the whole dehydration process. Bioinformatics and protein-protein interaction network analyses indicated that carbohydrate metabolism (including glycolysis/gluconeogenesis, galactose, starch and sucrose metabolism, pentose phosphate pathway, and cell wall organization), protein processing in ER, DNA repair, and antioxidative events had positive responses to lotus embryo dehydration. On the contrary, energy metabolism (metabolic pathway, photosynthesis, pyruvate metabolism, fatty acid biosynthesis) and secondary metabolism (terpenoid backbone, steroid, flavonoid biosynthesis) gradually become static status during lotus embryo water loss and maturation. Furthermore, non-enzymatic antioxidants and pentose phosphate pathway play major roles in antioxidant protection during dehydration process in lotus embryo. Abscisic acid (ABA) signaling and the accumulation of oligosaccharides, late embryogenesis abundant proteins, and heat shock proteins may be the key factors to ensure the continuous dehydration and storage tolerance of lotus seed embryo. Stress physiology detection showed that H2O2 was the main reactive oxygen species (ROS) component inducing oxidative stress damage, and glutathione and vitamin E acted as the major antioxidant to maintain the REDOX balance of lotus embryo during the dehydration process. These results provide new insights to reveal the physiological regulatory networks of the protective mechanism of embryo dehydration in lotus.

Keywords:  Nelumbo nucifera; TMT proteomics; abiotic stress; dehydration; desiccation tolerance; parallel reaction monitoring; seed embryo

DOI:  https://doi.org/10.3389/fpls.2021.792057
Front Cell Dev Biol. 2021 ;9 793389

Loss of PDK1 Induces Meiotic Defects in Oocytes From Diabetic Mice.

Juan Ge, Na Zhang, Shoubin Tang, Feifei Hu, Xiaojing Hou, Hongzheng Sun, Longsen Han, Qiang Wang.

  Maternal diabetes has been shown to impair oocyte quality; however, the underlying mechanisms remain unclear. Here, using a streptozotocin (STZ)-induced diabetic mouse model, we first detected and reduced expression of pyruvate dehydrogenase kinase 1 (PDK1) in diabetic oocytes, accompanying with the lowered phosphorylation of serine residue 232 on α subunit of the pyruvate dehydrogenase (PDH) complex (Ser232-PDHE1α). Importantly, forced expression of PDK1 not only elevated the phosphorylation level of Ser232-PDHE1α, but also partly prevented the spindle disorganization and chromosome misalignment in oocytes from diabetic mice, with no beneficial effects on metabolic dysfunction. Moreover, a phospho-mimetic S232D-PDHE1α mutant is also capable of ameliorating the maternal diabetes-associated meiotic defects. In sum, our data indicate that PDK1-controlled Ser232-PDHE1α phosphorylation pathway mediates the effects of diabetic environment on oocyte competence.

Keywords:  PDK1; diabetes; meiosis; oocyte; spindle

DOI:  https://doi.org/10.3389/fcell.2021.793389
Food Res Int. 2022 Jan;pii: S0963-9969(21)00750-X. [Epub ahead of print]151 110850

Widely targeted metabolome profiling of different colored sesame (Sesamum indicum L.) seeds provides new insight into their antioxidant activities.

Senouwa Segla Koffi Dossou, Fangtao Xu, Jun You, Rong Zhou, Donghua Li, Linhai Wang.

  Sesame seeds are considered worldwide as a functional food due to their nutritional and therapeutical values. Several physiological functions are being associated with sesame seeds and their derived products. However, the phytochemicals responsible for these various proprieties are not well understood. Thus, to acknowledge the diversity and variability of metabolites in sesame seeds of different colors and reveal key metabolites and pathways contributing to differences in antioxidant activities, black, brown, yellow, and white sesame seeds from 12 varieties were subjected to LC-MS/MS-based widely targeted metabolomics analysis. Totally, 671 metabolites were identified and chemically classified. The metabolic compounds varied significantly with the seed coat color and genotype. Many flavonoids, amino acids, and terpenoids were up-regulated in dark seeds. Sixty key differential metabolites were filtered out. Phenylpropanoid biosynthesis, amino acids biosynthesis, and tyrosine metabolism were the main differently regulated pathways. The DPPH, ABTS, and FRAP assays showed that the antioxidant activities of the seeds increased with the seed coat darkness. Therefore, the pharmacological proprieties of black seeds might be related to their high content of flavonoids and essential amino acids mostly. These findings expand phytochemicals composition information of different colored sesame seeds and provide resources for their comprehensive use and quality improvement.

Keywords:  Antioxidant activity; LC-MS/MS; Metabolome profiling; Seed coat color; Sesame

DOI:  https://doi.org/10.1016/j.foodres.2021.110850