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Reproductive toxicity and gender differences induced by cadmium telluride quantum dots in an invertebrate model organism

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ABSTRACT

Sexual glands are key sites affected by nanotoxicity, but there is no sensitive assay for measuring reproductive toxicity in animals. The aim of this study was to investigate the toxic effects of cadmium telluride quantum dots (CdTe-QDs) on gonads in a model organism, Bombyx mori. After dorsal vein injection of 0.32 nmol of CdTe-QDs per individual, the QDs passed through the outer membranes of gonads via the generation of ROS in the membranes of spermatocysts and ovarioles, as well as internal germ cells, thereby inducing early germ cell death or malformations via complex mechanisms related to apoptosis and autophagy through mitochondrial and lysosomal pathways. Histological observations of the gonads and quantitative analyses of germ cell development showed that the reproductive toxicity was characterized by obvious male sensitivity. Exposure to QDs in the early stage of males had severe adverse effects on the quantity and quality of sperm, which was the main reason for the occurrence of unfertilized eggs. Ala- or Gly-conjugated QDs could reduce the nanotoxicity of CdTe-QDs during germ cell development and fertilization of their offspring. The results demonstrate that males are preferable models for evaluating the reproductive toxicity of QDs in combined in vivo/in vitro investigations.

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Effects of QDs on spermateleosis in Bombyx mori.(A) Natural morphology of spermatocysts in the different stages. 1–3 indicate the stages with 64, 128, and 256 primary spermatocytes in spermatocysts, respectively; 4 indicates the spermatocysts during spermiogenesis; 5 indicates the stage of spermatodesms. (B) The culture of male spermatocysts after in vivo exposure to QDs. Cacoplastic morphology of spermatocysts characterized by warping, apoptosis, necrosis, or damaged membranes. 1′–3′ indicate the stages with 64, 128, and 256 cacoplastic primary spermatocytes in spermatocysts, respectively; 4′ indicates the cacoplastic spermatocysts during spermiogenesis process; 5′ indicates the stage of cacoplastic spermatodesms. (C) Spermateleosis was affected by the duration of exposure in vivo. The duration of exposure in vivo was the time until the removal of the testes after exposure to QDs. Fifth instar larvae received vascular injection of 0.32 nmol CdTe QDs, QDs-Ala, or QDs-Gly per larva (10 μL at 32 μM per individual) at 48 h after molting, whereas the control organisms (CK) were injected with the same volume of pure water. Spermatocysts were removed from male larva at 12 h or 24 h after exposure to QDs, and then cultured for 168 h in vitro without QDs. Bars = 100 μm in (A,B), and 200 μm in (C).
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f4: Effects of QDs on spermateleosis in Bombyx mori.(A) Natural morphology of spermatocysts in the different stages. 1–3 indicate the stages with 64, 128, and 256 primary spermatocytes in spermatocysts, respectively; 4 indicates the spermatocysts during spermiogenesis; 5 indicates the stage of spermatodesms. (B) The culture of male spermatocysts after in vivo exposure to QDs. Cacoplastic morphology of spermatocysts characterized by warping, apoptosis, necrosis, or damaged membranes. 1′–3′ indicate the stages with 64, 128, and 256 cacoplastic primary spermatocytes in spermatocysts, respectively; 4′ indicates the cacoplastic spermatocysts during spermiogenesis process; 5′ indicates the stage of cacoplastic spermatodesms. (C) Spermateleosis was affected by the duration of exposure in vivo. The duration of exposure in vivo was the time until the removal of the testes after exposure to QDs. Fifth instar larvae received vascular injection of 0.32 nmol CdTe QDs, QDs-Ala, or QDs-Gly per larva (10 μL at 32 μM per individual) at 48 h after molting, whereas the control organisms (CK) were injected with the same volume of pure water. Spermatocysts were removed from male larva at 12 h or 24 h after exposure to QDs, and then cultured for 168 h in vitro without QDs. Bars = 100 μm in (A,B), and 200 μm in (C).

Mentions: There have been no previous quantitative assessments of the impact of exposure to QDs on animal male germ cell development and a suitable research platform is not available. In order to quantitatively assess the impact of exposure to QDs on the development of silkworm male germ cells, we established an in vitro method for the culture of male spermatocysts after in vivo exposure to QDs in a combined in vivo/in vitro approach. As shown in Fig. 4A, the in vitro-cultured normal spermatocysts could complete the whole in vivo spermatogenesis process from spermatogonia to mature sperms, including primary spermatocytes, spermatocysts during the spermiogenesis process, and the spermatodesms stage.


Reproductive toxicity and gender differences induced by cadmium telluride quantum dots in an invertebrate model organism
Effects of QDs on spermateleosis in Bombyx mori.(A) Natural morphology of spermatocysts in the different stages. 1–3 indicate the stages with 64, 128, and 256 primary spermatocytes in spermatocysts, respectively; 4 indicates the spermatocysts during spermiogenesis; 5 indicates the stage of spermatodesms. (B) The culture of male spermatocysts after in vivo exposure to QDs. Cacoplastic morphology of spermatocysts characterized by warping, apoptosis, necrosis, or damaged membranes. 1′–3′ indicate the stages with 64, 128, and 256 cacoplastic primary spermatocytes in spermatocysts, respectively; 4′ indicates the cacoplastic spermatocysts during spermiogenesis process; 5′ indicates the stage of cacoplastic spermatodesms. (C) Spermateleosis was affected by the duration of exposure in vivo. The duration of exposure in vivo was the time until the removal of the testes after exposure to QDs. Fifth instar larvae received vascular injection of 0.32 nmol CdTe QDs, QDs-Ala, or QDs-Gly per larva (10 μL at 32 μM per individual) at 48 h after molting, whereas the control organisms (CK) were injected with the same volume of pure water. Spermatocysts were removed from male larva at 12 h or 24 h after exposure to QDs, and then cultured for 168 h in vitro without QDs. Bars = 100 μm in (A,B), and 200 μm in (C).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC5037452&req=5

f4: Effects of QDs on spermateleosis in Bombyx mori.(A) Natural morphology of spermatocysts in the different stages. 1–3 indicate the stages with 64, 128, and 256 primary spermatocytes in spermatocysts, respectively; 4 indicates the spermatocysts during spermiogenesis; 5 indicates the stage of spermatodesms. (B) The culture of male spermatocysts after in vivo exposure to QDs. Cacoplastic morphology of spermatocysts characterized by warping, apoptosis, necrosis, or damaged membranes. 1′–3′ indicate the stages with 64, 128, and 256 cacoplastic primary spermatocytes in spermatocysts, respectively; 4′ indicates the cacoplastic spermatocysts during spermiogenesis process; 5′ indicates the stage of cacoplastic spermatodesms. (C) Spermateleosis was affected by the duration of exposure in vivo. The duration of exposure in vivo was the time until the removal of the testes after exposure to QDs. Fifth instar larvae received vascular injection of 0.32 nmol CdTe QDs, QDs-Ala, or QDs-Gly per larva (10 μL at 32 μM per individual) at 48 h after molting, whereas the control organisms (CK) were injected with the same volume of pure water. Spermatocysts were removed from male larva at 12 h or 24 h after exposure to QDs, and then cultured for 168 h in vitro without QDs. Bars = 100 μm in (A,B), and 200 μm in (C).
Mentions: There have been no previous quantitative assessments of the impact of exposure to QDs on animal male germ cell development and a suitable research platform is not available. In order to quantitatively assess the impact of exposure to QDs on the development of silkworm male germ cells, we established an in vitro method for the culture of male spermatocysts after in vivo exposure to QDs in a combined in vivo/in vitro approach. As shown in Fig. 4A, the in vitro-cultured normal spermatocysts could complete the whole in vivo spermatogenesis process from spermatogonia to mature sperms, including primary spermatocytes, spermatocysts during the spermiogenesis process, and the spermatodesms stage.

View Article: PubMed Central - PubMed

ABSTRACT

Sexual glands are key sites affected by nanotoxicity, but there is no sensitive assay for measuring reproductive toxicity in animals. The aim of this study was to investigate the toxic effects of cadmium telluride quantum dots (CdTe-QDs) on gonads in a model organism, Bombyx mori. After dorsal vein injection of 0.32 nmol of CdTe-QDs per individual, the QDs passed through the outer membranes of gonads via the generation of ROS in the membranes of spermatocysts and ovarioles, as well as internal germ cells, thereby inducing early germ cell death or malformations via complex mechanisms related to apoptosis and autophagy through mitochondrial and lysosomal pathways. Histological observations of the gonads and quantitative analyses of germ cell development showed that the reproductive toxicity was characterized by obvious male sensitivity. Exposure to QDs in the early stage of males had severe adverse effects on the quantity and quality of sperm, which was the main reason for the occurrence of unfertilized eggs. Ala- or Gly-conjugated QDs could reduce the nanotoxicity of CdTe-QDs during germ cell development and fertilization of their offspring. The results demonstrate that males are preferable models for evaluating the reproductive toxicity of QDs in combined in vivo/in vitro investigations.

No MeSH data available.


Related in: MedlinePlus