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1.
Toxicology ; 464: 153013, 2021 Dec.
Artigo em Inglês | MEDLINE | ID: mdl-34718031

RESUMO

Patulin is a secondary metabolite mainly secreted by fungi and is the most common mycotoxin found in apples and apple-based products. For the past few years, numerous studies suggested the wide distribution and toxicity of patulin. In this study, we investigated the toxic effect of patulin on mouse oocytes and its possible mechanisms. The results showed that patulin treatment did not affect meiotic resumption, but inhibited oocyte maturation as indicated by failure of first polar body extrusion. Further mechanistic study showed that patulin treatment disturbed normal spindle assembly, chromosome alignment and morphology. We also found increased oxidative stress by testing the level of ROS and decreased mitochondrial membrane potential, indicating mitochondria dysfunction. In summary, our results suggest that patulin treatment causes oocyte meiotic arrest by disturbing normal spindle assembly and chromosome alignment, which may be caused by dysfunctions of mitochondria.

2.
Cell Death Dis ; 12(10): 883, 2021 09 27.
Artigo em Inglês | MEDLINE | ID: mdl-34580275

RESUMO

Protein phosphatase 6 (PP6) is a member of the PP2A-like subfamily, which plays significant roles in numerous fundamental biological activities. We found that PPP6C plays important roles in male germ cells recently. Spermatogenesis is supported by the Sertoli cells in the seminiferous epithelium. In this study, we crossed Ppp6cF/F mice with AMH-Cre mice to gain mutant mice with specific depletion of the Ppp6c gene in the Sertoli cells. We discovered that the PPP6C cKO male mice were absolutely infertile and germ cells were largely lost during spermatogenesis. By combing phosphoproteome with bioinformatics analysis, we showed that the phosphorylation status of ß-catenin at S552 (a marker of adherens junctions) was significantly upregulated in mutant mice. Abnormal ß-catenin accumulation resulted in impaired testicular junction integrity, thus led to abnormal structure and functions of BTB. Taken together, our study reveals a novel function for PPP6C in male germ cell survival and differentiation by regulating the cell-cell communication through dephosphorylating ß-catenin at S552.

3.
Nat Cell Biol ; 23(6): 664-675, 2021 06.
Artigo em Inglês | MEDLINE | ID: mdl-34108658

RESUMO

RNA-binding proteins (RBPs) have essential functions during germline and early embryo development. However, current methods are unable to identify the in vivo targets of a RBP in these low-abundance cells. Here, by coupling RBP-mediated reverse transcription termination with linear amplification of complementary DNA ends and sequencing, we present the LACE-seq method for identifying RBP-regulated RNA networks at or near the single-oocyte level. We determined the binding sites and regulatory mechanisms for several RBPs, including Argonaute 2 (Ago2), Mili, Ddx4 and Ptbp1, in mature mouse oocytes. Unexpectedly, transcriptomics and proteomics analysis of Ago2-/- oocytes revealed that Ago2 interacts with endogenous small interfering RNAs (endo-siRNAs) to repress mRNA translation globally. Furthermore, the Ago2 and endo-siRNA complexes fine-tune the transcriptome by slicing long terminal repeat retrotransposon-derived chimeric transcripts. The precise mapping of RBP-binding sites in low-input cells opens the door to studying the roles of RBPs in embryonic development and reproductive diseases.


Assuntos
Perfilação da Expressão Gênica , Sequenciamento de Nucleotídeos em Larga Escala , Oócitos/metabolismo , Proteínas de Ligação a RNA/metabolismo , Animais , Proteínas Argonauta/genética , Proteínas Argonauta/metabolismo , Sítios de Ligação , RNA Helicases DEAD-box/genética , RNA Helicases DEAD-box/metabolismo , Feminino , Regulação da Expressão Gênica no Desenvolvimento , Células HeLa , Ribonucleoproteínas Nucleares Heterogêneas/genética , Ribonucleoproteínas Nucleares Heterogêneas/metabolismo , Humanos , Células K562 , Camundongos , Camundongos Endogâmicos C57BL , Camundongos Endogâmicos ICR , Camundongos Knockout , Proteína de Ligação a Regiões Ricas em Polipirimidinas/genética , Proteína de Ligação a Regiões Ricas em Polipirimidinas/metabolismo , Ligação Proteica , RNA Mensageiro/genética , RNA Mensageiro/metabolismo , RNA Interferente Pequeno/genética , RNA Interferente Pequeno/metabolismo , Proteínas de Ligação a RNA/genética , RNA-Seq , Transcriptoma
4.
Front Cell Dev Biol ; 9: 647103, 2021.
Artigo em Inglês | MEDLINE | ID: mdl-33842473

RESUMO

There are two important events in oocyte meiotic maturation, the G2/M transition and metaphase I progression. Thousands of proteins participate in regulating oocyte maturation, which highlights the importance of the ubiquitin proteasome system (UPS) in regulating protein synthesis and degradation. Skp1-Cullin-F-box (SCF) complexes, as the best characterized ubiquitin E3 ligases in the UPS, specifically recognize their substrates. F-box proteins, as the variable adaptors of SCF, can bind substrates specifically. Little is known about the functions of the F-box proteins in oocyte maturation. In this study, we found that depletion of FBXO34, an F-box protein, led to failure of oocyte meiotic resumption due to a low activity of MPF, and this phenotype could be rescued by exogenous overexpression of CCNB1. Strikingly, overexpression of FBXO34 promoted germinal vesicle breakdown (GVBD), but caused continuous activation of spindle assembly checkpoint (SAC) and MI arrest of oocytes. Here, we demonstrated that FBXO34 regulated both the G2/M transition and anaphase entry in meiotic oocytes.

5.
J Cell Physiol ; 236(10): 7001-7013, 2021 10.
Artigo em Inglês | MEDLINE | ID: mdl-33724469

RESUMO

Parathyroid hormone-related protein (PTHrP), the main cause of humoral hypercalcemia in malignancies, promotes cell proliferation and delays terminal cell maturation during embryonic development. Our previous study reported that PTHrP plays important roles in blastocyst formation, pluripotency gene expression, and histone acetylation during mouse preimplantation embryonic development. In this study, we further investigated the mechanism of preimplantation embryonic development regulated by PTHrP. Our results showed that Pthrp depletion decreased both the developmental rate of embryos at the cleavage stage and the cell number of morula-stage embryos. Pthrp-depleted embryos had significantly decreased levels of cyclin D1, phospho (p)-AKT (Thr308) and E2F1. However, Pthrp depletion did not cause significant changes in CDK4, ß-catenin or RUNX2 expression. In addition, our results indicated that Pthrp depletion promoted HDAC4 translocation from the cytoplasm to the nucleus in cleavage-stage embryos by stimulating the activity of protein phosphatase 2A (PP2A), which resulted in dephosphorylation of HDAC4. Taken together, these results suggest that PTHrP regulates cleavage division progression and blastocyst formation through the AKT/cyclin D1 pathway and that PTHrP modulates histone acetylation patterns through nuclear translocation of HDAC4 via PP2A-dependent HDAC4 dephosphorylation during preimplantation embryonic development in mice.


Assuntos
Blastocisto/metabolismo , Ciclina D1/metabolismo , Histona Desacetilases/metabolismo , Histonas/metabolismo , Proteína Relacionada ao Hormônio Paratireóideo/metabolismo , Proteínas Proto-Oncogênicas c-akt/metabolismo , Acetilação , Transporte Ativo do Núcleo Celular , Animais , Fator de Transcrição E2F1/genética , Fator de Transcrição E2F1/metabolismo , Desenvolvimento Embrionário , Regulação da Expressão Gênica no Desenvolvimento , Histona Desacetilases/genética , Camundongos , Proteína Relacionada ao Hormônio Paratireóideo/genética , Fosforilação , Proteína Fosfatase 2/metabolismo , Transdução de Sinais
6.
Front Cell Dev Biol ; 9: 638559, 2021.
Artigo em Inglês | MEDLINE | ID: mdl-33718377

RESUMO

Meiosis is essential to the continuity of life in sexually-reproducing organisms through the formation of haploid gametes. Unlike somatic cells, the germ cells undergo two successive rounds of meiotic divisions after a single cycle of DNA replication, resulting in the decrease in ploidy. In humans, errors in meiotic progression can cause infertility and birth defects. Post-translational modifications, such as phosphorylation, ubiquitylation and sumoylation have emerged as important regulatory events in meiosis. There are dynamic equilibrium of protein phosphorylation and protein dephosphorylation in meiotic cell cycle process, regulated by a conservative series of protein kinases and protein phosphatases. Among these protein phosphatases, PP2A, PP4, and PP6 constitute the PP2A-like subfamily within the serine/threonine protein phosphatase family. Herein, we review recent discoveries and explore the role of PP2A-like protein phosphatases during meiotic progression.

7.
J Cell Physiol ; 236(7): 5352-5361, 2021 07.
Artigo em Inglês | MEDLINE | ID: mdl-33586215

RESUMO

In vitro culture of follicles is a promising technology to generate large quantities of mature oocytes and it could offer a novel option of assisted reproductive technologies. Here we described a 2-dimensional follicular serum-free culture system with 3-dimensional effect that can make secondary follicles develop into antral follicles (78.52%), generating developmentally mature oocytes in vitro (66.45%). The oocytes in this serum-free system completed the first meiosis; spindle assembly and chromosome congression in most oocytes matured from follicular culture were normal. However, these oocytes showed significantly lower activation and embryonic development rates, and their ability to produce Ca2+ oscillations was also lower in response to parthenogenetic activation, after which a 2-cell embryonic developmental block occurred. Oocytes matured from follicular culture displayed increased abnormal mitochondrial distribution and increased reactive oxygen species levels when compared to in vivo matured oocytes. These data are important for understanding the reasons for reduced developmental potential of oocytes matured from follicular culture, and for further improving the cultivation system.


Assuntos
Técnicas de Maturação in Vitro de Oócitos/métodos , Oócitos , Folículo Ovariano , Animais , Núcleo Celular , Citoplasma , Feminino , Camundongos , Oócitos/fisiologia
9.
Nat Commun ; 11(1): 6354, 2020 12 11.
Artigo em Inglês | MEDLINE | ID: mdl-33311485

RESUMO

The formation of zygote is the beginning of mammalian life, and dynamic epigenetic modifications are essential for mammalian normal development. H3K27 di-methylation (H3K27me2) and H3K27 tri-methylation (H3K27me3) are marks of facultative heterochromatin which maintains transcriptional repression established during early development in many eukaryotes. However, the mechanism underlying establishment and regulation of epigenetic asymmetry in the zygote remains obscure. Here we show that maternal EZH2 is required for the establishment of H3K27me3 in mouse zygotes. However, combined immunostaining with ULI-NChIP-seq (ultra-low-input micrococcal nuclease-based native ChIP-seq) shows that EZH1 could partially safeguard the role of EZH2 in the formation of H3K27me2. Meanwhile, we identify that EHMT1 is involved in the establishment of H3K27me2, and that H3K27me2 might be an essential prerequisite for the following de novo H3K27me3 modification on the male pronucleus. In this work, we clarify the establishment and regulatory mechanisms of H3K27me2 and H3K27me3 in mouse zygotes.


Assuntos
Genoma , Histona-Lisina N-Metiltransferase/metabolismo , Histonas/metabolismo , Zigoto/metabolismo , Animais , Proteína Potenciadora do Homólogo 2 de Zeste/genética , Proteína Potenciadora do Homólogo 2 de Zeste/metabolismo , Epigenômica , Heterocromatina , Histona-Lisina N-Metiltransferase/genética , Masculino , Metilação , Camundongos , Camundongos Endogâmicos ICR , Camundongos Knockout , Nuclease do Micrococo , Oogênese/fisiologia , Complexo Repressor Polycomb 2/genética , Processamento de Proteína Pós-Traducional
10.
Reprod Toxicol ; 96: 141-149, 2020 Jun 20.
Artigo em Inglês | MEDLINE | ID: mdl-32574675

RESUMO

Cadmium (Cd) is a bioaccumulative heavy metal element with potential toxicity on the female reproductive system, but the exact molecular mechanisms have not yet been clearly defined. In this study, female mice were exposed to 0.5 mg/kg/day of CdCl2 for 60 consecutive days. We found that chronic Cd exposure significantly decreased the fecundity of female mice by affecting oocyte meiotic progression as indicated by disrupted spindle assembly, chromosome alignment and kinetochore-microtubule attachments, consequently resulting in aneuploid oocytes. Further studies showed that the periodic fluctuations of MPF activity and cyclin B1 expression were disturbed in Cd-exposed oocytes probably by affecting the spindle assembly checkpoint protein Bub3. In addition, Cd exposure induced oxidative stress as indicated by an increased level of reactive oxygen species and apoptosis in oocytes, leading to oocyte quality deterioration. Taken together, these data suggest that Cd exposure causes disrupted molecular events of meiotic progression and deterioration of oocyte quality via oxidative stress, leading to decrease of female fertility.

11.
FASEB J ; 34(7): 8990-9002, 2020 07.
Artigo em Inglês | MEDLINE | ID: mdl-32449168

RESUMO

Precise regulation of chromosome segregation during oocyte meiosis is of vital importance to mammalian reproduction. Anaphase promoting complex/cyclosome (APC/C) is reported to play an important role in metaphase-to-anaphase transition. Here we report that cell division cycle 23 (Cdc23, also known as APC8) plays a critical role in regulating the oocyte chromosome separation. Cdc23 localized on the meiotic spindle, and microinjection of Cdc23 siRNA caused decreased ratios of metaphase-to-anaphase transition. Loss of Cdc23 resulted in abnormal spindles, misaligned chromosomes, errors of homologous chromosome segregation, and production of aneuploid oocytes. Further study showed that inactivation of spindle assembly checkpoint and degradation of Cyclin B1 and securin were disturbed after Cdc23 knockdown. Furthermore, we found that inhibiting spindle assembly checkpoint protein Msp1 partly rescued the decreased polar body extrusion and reduced the accumulation of securin in Cdc23 knockdown oocytes. Taken together, our data demonstrate that Cdc23 is required for the chromosome segregation through regulating the spindle assembly checkpoint activity, and cyclin B1 and securin degradation in meiotic mouse oocytes.


Assuntos
Subunidade Apc8 do Ciclossomo-Complexo Promotor de Anáfase/metabolismo , Segregação de Cromossomos , Meiose , Oócitos/fisiologia , Fuso Acromático/fisiologia , Animais , Subunidade Apc8 do Ciclossomo-Complexo Promotor de Anáfase/genética , Proteínas de Ciclo Celular , Feminino , Camundongos , Camundongos Endogâmicos ICR , Oócitos/citologia
12.
Mol Reprod Dev ; 87(5): 550-564, 2020 05.
Artigo em Inglês | MEDLINE | ID: mdl-32215983

RESUMO

BRG1-associated factor 250a (BAF250a) is a component of the SWI/SNF adenosine triphosphate-dependent chromatin remodeling complex, which has been shown to control chromatin structure and transcription. BAF250a was reported to be a key component of the gene regulatory machinery in embryonic stem cells controlling self-renewal, differentiation, and cell lineage decisions. Here we constructed Baf250aF/F ;Gdf9-cre (Baf250aCKO ) mice to specifically delete BAF250a in oocytes to investigate the role of maternal BAF250a in female germ cells and embryo development. Our results showed that BAF250a deletion did not affect folliculogenesis, ovulation, and fertilization, but it caused late embryonic death. RNA sequencing analysis showed that the expression of genes involved in cell proliferation and differentiation, tissue morphogenesis, histone modification, and nucleosome remodeling were perturbed in Baf250aCKO MII oocytes. We showed that covalent histone modifications such as H3K27me3 and H3K27ac were also significantly affected in oocytes, which may reduce oocyte quality and lead to birth defects. In addition, the DNA methylation level of Igf2r, Snrpn, and Peg3 differentially methylated regions was decreased in Baf250aCKO oocytes. Quantitative real-time polymerase chain reaction analysis showed that the relative messenger RNA (mRNA) expression levels of Igf2r and Snrpn were significantly increased. The mRNA expression level of Dnmt1, Dnmt3a, Dnmt3l, and Uhrf1 was decreased, and the protein expression in these genes was also reduced, which might be the cause for impaired imprinting establishment. In conclusion, our results demonstrate that BAF250a plays an important role in oocyte transcription regulation, epigenetic modifications, and embryo development.


Assuntos
Proteínas de Ligação a DNA/genética , Desenvolvimento Embrionário/genética , Epigênese Genética/genética , Oócitos/metabolismo , Fatores de Transcrição/genética , Animais , Diferenciação Celular/genética , Linhagem da Célula/genética , Células Cultivadas , Metilação de DNA/genética , Células-Tronco Embrionárias/metabolismo , Células-Tronco Embrionárias/fisiologia , Feminino , Deleção de Genes , Impressão Genômica , Técnicas de Maturação in Vitro de Oócitos , Camundongos , Camundongos Knockout , Oócitos/fisiologia , Gravidez
13.
Cell Prolif ; 53(1): e12726, 2020 Jan.
Artigo em Inglês | MEDLINE | ID: mdl-31755150

RESUMO

OBJECTIVES: In humans, non-obstructive azoospermia (NOA) is a major cause of male infertility. However, the aetiology of NOA is largely unknown. Previous studies reported that protein CK2ß was abundantly and broadly expressed in spermatogenic cells. Here, we investigate whether protein CK2ß participates in spermatogenesis. MATERIALS AND METHODS: In this study, we separated spermatogenic cells using STA-PUT velocity sedimentation, analysed the expression pattern of protein CK2ß by immunoblotting, specifically deleted Ck2ß gene in early-stage spermatogenic cells by crossing Ck2ßfl mice with Stra8-Cre+ mice and validated the knockout efficiency by quantitative RT-PCR and immunoblotting. The phenotypes of Ck2ßfl/Δ ;SCre+ mice were studied by immunohistochemistry and immunofluorescence. The molecular mechanisms of male germ cell development arrest were elucidated by immunoblotting and TUNEL assay. RESULTS: Ablation of Ck2ß gene triggered excessive germ cell apoptosis, germ cell development arrest, azoospermia and male infertility. Inactivation of Ck2ß gene caused distinctly reduced expression of Ck2α' gene and CK2α' protein. CONCLUSIONS: Ck2ß is a vital gene for germ cell survival and male fertility in mice.


Assuntos
Apoptose/genética , Azoospermia , Caseína Quinase II/deficiência , Células Germinativas , Animais , Azoospermia/enzimologia , Azoospermia/genética , Azoospermia/patologia , Caseína Quinase II/metabolismo , Deleção de Genes , Células Germinativas/enzimologia , Células Germinativas/patologia , Masculino , Camundongos , Camundongos Knockout
14.
Biochem Biophys Res Commun ; 521(1): 265-269, 2020 01 01.
Artigo em Inglês | MEDLINE | ID: mdl-31640856

RESUMO

Before fertilization, ovulated mammalian oocytes are arrested at the metaphase of second meiosis (MII), which is maintained by the so-called cytostatic factor (CSF). It is well known that the continuous synthesis and accumulation of cyclin B is critical for maintaining the CSF-mediated MII arrest. Recent studies by us and others have shown that Ccnb3 is required for the metaphase-to-anaphase transition during the first meiosis of mouse oocytes, but whether Ccnb3 plays a role in MII arrest and exit remains unknown. Here, we showed that the protein level of Ccnb3 gradually decreased during oocyte meiotic maturation, and exogenous expression of Ccnb3 led to release of MII arrest, degradation of securin, separation of sister chromatids, extrusion of the second polar body (PB2), and finally entry into interphase. These phenotypes could be rescued by inhibition of Wee1B or CDK2. Our results indicate that Ccnb3 plays a critical regulatory role in MII arrest and exit in mouse oocytes.


Assuntos
Ciclina B/metabolismo , Meiose/genética , Oócitos/citologia , Oócitos/metabolismo , Animais , Células Cultivadas , Ciclina B/genética , Feminino , Metáfase/genética , Camundongos , Camundongos Endogâmicos ICR , RNA Mensageiro/genética , RNA Mensageiro/metabolismo
15.
Cell Death Differ ; 27(6): 1952-1964, 2020 06.
Artigo em Inglês | MEDLINE | ID: mdl-31819157

RESUMO

Protein phosphatase 6 (PP6) is a member of the PP2A-like subfamily, which plays a critical role in many fundamental cellular processes. We recently reported that PP6 is essential for female fertility. Here, we report that PP6 is involved in meiotic recombination and that germ cell-specific deletion of PP6 by Stra8-Cre causes defective spermatogenesis. The PP6-deficient spermatocytes were arrested at the pachytene stage and defects in DSB repair and crossover formation were observed, indicating that PP6 facilitated meiotic double-stranded breaks (DSB) repair. Further investigations revealed that depletion of PP6 in the germ cells affected chromatin relaxation, which was dependent on MAPK pathway activity, consequently preventing programmed DSB repair factors from being recruited to proper positions on the chromatin. Taken together, our results demonstrate that PP6 has an important role in meiotic recombination and male fertility.


Assuntos
Fosfoproteínas Fosfatases/fisiologia , Espermatócitos , Espermatogênese , Animais , Cromatina/metabolismo , Quebras de DNA de Cadeia Dupla , Reparo do DNA , Masculino , Camundongos , Camundongos Endogâmicos C57BL , Estágio Paquíteno , Espermatócitos/citologia , Espermatócitos/metabolismo
16.
Org Lett ; 21(9): 3131-3135, 2019 05 03.
Artigo em Inglês | MEDLINE | ID: mdl-31013104

RESUMO

A cyclization of propargylic alcohols with tert-butyl nitrite at room temperature in air was achieved using Pd(OAc)2 as catalyst. The first reported 4-oxoisoxazoline N-oxides could be directly accessed from a range of multisubstituted propargylic alcohols in moderate to excellent yields under mild conditions. Density functional theory calculations indicated that the reaction proceeds through a palladium-catalyzed NO2 addition that efficiently generates a ketoxime radical, which eventually produces 4-oxoisoxazoline N-oxide.

17.
Org Lett ; 20(22): 7220-7224, 2018 11 16.
Artigo em Inglês | MEDLINE | ID: mdl-30403485

RESUMO

Eosin Y, a common organo-photocatalyst in visible-light photoredox processes, was found to show excellent catalytic activities for thermal redox reactions under a catalytic amount of Cu(OAc)2. With this catalytic system, vinyl azides and ketene silyl acetals combine to form formal [3 + 2] cycloadducts by α-ester radical addition without light irradiation. This method provides a mild and straightforward paradigm to prepare important synthons of five-membered ene-γ-lactams and bridge ring lactams. It is the first example of an eosin Y-catalyzed redox reaction in the dark.

18.
Chem Commun (Camb) ; 50(100): 15916-9, 2014 Dec 28.
Artigo em Inglês | MEDLINE | ID: mdl-25379881

RESUMO

This communication reports a room temperature visible-light-driven protocol for the C-H difluoromethylenephosphonation of arenes and heteroarenes. Using commercially available diethyl bromodifluoromethyl phosphonate as a precursor of difluoromethyl radical, fac-Ir(ppy)3 as a photosensitizer and a 3 W blue LED as a light source, an array of aromatic compounds containing difluoromethylenephosphonyl groups were prepared directly from the corresponding arenes and heteroarenes in excellent to moderate yields.


Assuntos
Derivados de Benzeno/química , Luz , Organofosfonatos/química , Carbono/química , Catálise , Complexos de Coordenação/química , Hidrogênio/química , Organofosfonatos/síntese química
19.
Ecotoxicol Environ Saf ; 83: 102-7, 2012 Sep.
Artigo em Inglês | MEDLINE | ID: mdl-22770951

RESUMO

The cytotoxicity of alkylmethylimidazolium-based ionic liquids on rat pheochromocytoma (PC12) cells was evaluated by 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay, lactate dehydrogenase release (LDH), and acridine orange staining in the present study. Mitochondrial depolarization, DNA fragmentation, reactive oxygen species (ROS) levels, and caspase-3 activity were also determined. The results showed dose-dependent cytotoxicity of ionic liquids on PC12 cells, and the ionic liquids with longer lateral chains had stronger cytotoxicity. Additionally, we found that exposure to the ionic liquid 1-octyl-3-methylimidazolium bromide ([C(8)mim]Br) provoked cellular LDH release, increased mitochondrial depolarization, induced cellular transmogrification, nuclear shrinkage and DNA fragmentation, and promoted caspase-3 activity and ROS levels in PC12 cells. These results suggest that [C(8)mim]Br may induce PC12 cell apoptosis triggered by excessive ROS and mediated by mitochondrial depolarization and permeability transition. Our result may be helpful for illuminating the cytotoxicity mechanism of alkylmethylimidazolium-based ionic liquids and safely using them in the future.


Assuntos
Apoptose/efeitos dos fármacos , Imidazóis/toxicidade , Líquidos Iônicos/toxicidade , Animais , Boratos/toxicidade , Caspase 3/metabolismo , Forma Celular/efeitos dos fármacos , Fragmentação do DNA/efeitos dos fármacos , Mitocôndrias/efeitos dos fármacos , Células PC12 , Ratos , Espécies Reativas de Oxigênio/metabolismo
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