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Glycogen and glucose metabolism are essential for early embryonic development of the red flour beetle Tribolium castaneum.

Fraga A, Ribeiro L, Lobato M, Santos V, Silva JR, Gomes H, da Cunha Moraes JL, de Souza Menezes J, de Oliveira CJ, Campos E, da Fonseca RN - PLoS ONE (2013)

Bottom Line: In oviparous insects the egg becomes an isolated system after egg laying with all energy conversion taking place during embryogenesis.Expression analysis via in situ hybridization shows that both genes are expressed only in the embryonic tissue, suggesting that embryonic and extra-embryonic cells display different metabolic activities. dsRNA adult female injection (parental RNAi) of both genes lead a reduction in egg laying and to embryonic lethality.Morphological analysis via DAPI stainings indicates that early development is impaired in Tc-GSK-3 and Tc-HexA1 RNAi embryos.

View Article: PubMed Central - PubMed

Affiliation: Laboratório Integrado de Bioquímica Hatisaburo Masuda (LIBHM), Núcleo de Pesquisas Ecológicas e Sócioambientais de Macaé (NUPEM), Universidade Federal do Rio de Janeiro (UFRJCampus Macaé), Rio de Janeiro, Brazil.

ABSTRACT
Control of energy metabolism is an essential process for life. In insects, egg formation (oogenesis) and embryogenesis is dependent on stored molecules deposited by the mother or transcribed later by the zygote. In oviparous insects the egg becomes an isolated system after egg laying with all energy conversion taking place during embryogenesis. Previous studies in a few vector species showed a strong correlation of key morphogenetic events and changes in glucose metabolism. Here, we investigate glycogen and glucose metabolism in the red flour beetle Tribolium castaneum, an insect amenable to functional genomic studies. To examine the role of the key enzymes on glycogen and glucose regulation we cloned and analyzed the function of glycogen synthase kinase 3 (GSK-3) and hexokinase (HexA) genes during T. castaneum embryogenesis. Expression analysis via in situ hybridization shows that both genes are expressed only in the embryonic tissue, suggesting that embryonic and extra-embryonic cells display different metabolic activities. dsRNA adult female injection (parental RNAi) of both genes lead a reduction in egg laying and to embryonic lethality. Morphological analysis via DAPI stainings indicates that early development is impaired in Tc-GSK-3 and Tc-HexA1 RNAi embryos. Importantly, glycogen levels are upregulated after Tc-GSK-3 RNAi and glucose levels are upregulated after Tc-HexA1 RNAi, indicating that both genes control metabolism during embryogenesis and oogenesis, respectively. Altogether our results show that T. castaneum embryogenesis depends on the proper control of glucose and glycogen.

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Simplified view of the metabolic pathways investigated in this study.Glycogen Synthase Kinase-3 (GSK-3-blue) is not only involved in glycogen synthase (GS) regulation, but also acts as a downstream component of the Wnt signaling pathway (e.g.[60]). Glycogen Phosphorylase (GP) breaks up glycogen into glucose subunits. Hexokinase (Hex-red) is involved in producing Glucose-6-P from glucose, acting as an important enzyme of the glycolytic pathway. Other Glucose-6-P possible roles in different metabolic pathways are omitted for simplicity.
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pone-0065125-g001: Simplified view of the metabolic pathways investigated in this study.Glycogen Synthase Kinase-3 (GSK-3-blue) is not only involved in glycogen synthase (GS) regulation, but also acts as a downstream component of the Wnt signaling pathway (e.g.[60]). Glycogen Phosphorylase (GP) breaks up glycogen into glucose subunits. Hexokinase (Hex-red) is involved in producing Glucose-6-P from glucose, acting as an important enzyme of the glycolytic pathway. Other Glucose-6-P possible roles in different metabolic pathways are omitted for simplicity.

Mentions: A simplified model of energy utilization of glycogen mobilization into the glycolytic pathway (Figure 1) shows that glycogen storage is mobilized into the glycolytic pathway due to the action of Glycogen Phosphorylase (GP), while its synthesis is due to Glycogen Synthase (GS), whose activity is regulated by glycogen synthase kinase-3 (GSK-3) (reviewed in [10]). GSK-3 is not only involved in metabolic reactions but also acts as an essential kinase of the Wnt pathway [11], [12], which plays an essential role during embryogenesis. Recently, GSK-3 was also shown to be involved in the integration of the Wnt and BMP/Smad1 pathways [13], [14], [15]. Thus, GSK-3 is an important “hub” linking important signaling pathways during embryogenesis to metabolic reactions.


Glycogen and glucose metabolism are essential for early embryonic development of the red flour beetle Tribolium castaneum.

Fraga A, Ribeiro L, Lobato M, Santos V, Silva JR, Gomes H, da Cunha Moraes JL, de Souza Menezes J, de Oliveira CJ, Campos E, da Fonseca RN - PLoS ONE (2013)

Simplified view of the metabolic pathways investigated in this study.Glycogen Synthase Kinase-3 (GSK-3-blue) is not only involved in glycogen synthase (GS) regulation, but also acts as a downstream component of the Wnt signaling pathway (e.g.[60]). Glycogen Phosphorylase (GP) breaks up glycogen into glucose subunits. Hexokinase (Hex-red) is involved in producing Glucose-6-P from glucose, acting as an important enzyme of the glycolytic pathway. Other Glucose-6-P possible roles in different metabolic pathways are omitted for simplicity.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3672164&req=5

pone-0065125-g001: Simplified view of the metabolic pathways investigated in this study.Glycogen Synthase Kinase-3 (GSK-3-blue) is not only involved in glycogen synthase (GS) regulation, but also acts as a downstream component of the Wnt signaling pathway (e.g.[60]). Glycogen Phosphorylase (GP) breaks up glycogen into glucose subunits. Hexokinase (Hex-red) is involved in producing Glucose-6-P from glucose, acting as an important enzyme of the glycolytic pathway. Other Glucose-6-P possible roles in different metabolic pathways are omitted for simplicity.
Mentions: A simplified model of energy utilization of glycogen mobilization into the glycolytic pathway (Figure 1) shows that glycogen storage is mobilized into the glycolytic pathway due to the action of Glycogen Phosphorylase (GP), while its synthesis is due to Glycogen Synthase (GS), whose activity is regulated by glycogen synthase kinase-3 (GSK-3) (reviewed in [10]). GSK-3 is not only involved in metabolic reactions but also acts as an essential kinase of the Wnt pathway [11], [12], which plays an essential role during embryogenesis. Recently, GSK-3 was also shown to be involved in the integration of the Wnt and BMP/Smad1 pathways [13], [14], [15]. Thus, GSK-3 is an important “hub” linking important signaling pathways during embryogenesis to metabolic reactions.

Bottom Line: In oviparous insects the egg becomes an isolated system after egg laying with all energy conversion taking place during embryogenesis.Expression analysis via in situ hybridization shows that both genes are expressed only in the embryonic tissue, suggesting that embryonic and extra-embryonic cells display different metabolic activities. dsRNA adult female injection (parental RNAi) of both genes lead a reduction in egg laying and to embryonic lethality.Morphological analysis via DAPI stainings indicates that early development is impaired in Tc-GSK-3 and Tc-HexA1 RNAi embryos.

View Article: PubMed Central - PubMed

Affiliation: Laboratório Integrado de Bioquímica Hatisaburo Masuda (LIBHM), Núcleo de Pesquisas Ecológicas e Sócioambientais de Macaé (NUPEM), Universidade Federal do Rio de Janeiro (UFRJCampus Macaé), Rio de Janeiro, Brazil.

ABSTRACT
Control of energy metabolism is an essential process for life. In insects, egg formation (oogenesis) and embryogenesis is dependent on stored molecules deposited by the mother or transcribed later by the zygote. In oviparous insects the egg becomes an isolated system after egg laying with all energy conversion taking place during embryogenesis. Previous studies in a few vector species showed a strong correlation of key morphogenetic events and changes in glucose metabolism. Here, we investigate glycogen and glucose metabolism in the red flour beetle Tribolium castaneum, an insect amenable to functional genomic studies. To examine the role of the key enzymes on glycogen and glucose regulation we cloned and analyzed the function of glycogen synthase kinase 3 (GSK-3) and hexokinase (HexA) genes during T. castaneum embryogenesis. Expression analysis via in situ hybridization shows that both genes are expressed only in the embryonic tissue, suggesting that embryonic and extra-embryonic cells display different metabolic activities. dsRNA adult female injection (parental RNAi) of both genes lead a reduction in egg laying and to embryonic lethality. Morphological analysis via DAPI stainings indicates that early development is impaired in Tc-GSK-3 and Tc-HexA1 RNAi embryos. Importantly, glycogen levels are upregulated after Tc-GSK-3 RNAi and glucose levels are upregulated after Tc-HexA1 RNAi, indicating that both genes control metabolism during embryogenesis and oogenesis, respectively. Altogether our results show that T. castaneum embryogenesis depends on the proper control of glucose and glycogen.

Show MeSH