DNA Topoisomerase IIα contributes to the early steps of adipogenesis in 3T3-L1 cells
DNA topoisomerases (Topo) are multifunctional enzymes resolving DNA topological problems such as those arising during DNA replication, transcription and mitosis. Mammalian cells express 2 class II isoforms, Topoisomerases IIα (Topo IIα) and IIβ (Topo IIβ), which have similar enzymatic properties but...
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Published in | Cellular signalling Vol. 28; no. 10; pp. 1593 - 1603 |
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Format | Journal Article |
Language | English |
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01.10.2016
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Abstract | DNA topoisomerases (Topo) are multifunctional enzymes resolving DNA topological problems such as those arising during DNA replication, transcription and mitosis. Mammalian cells express 2 class II isoforms, Topoisomerases IIα (Topo IIα) and IIβ (Topo IIβ), which have similar enzymatic properties but are differently expressed, in dividing and pluripotent cells, and in post-mitotic and differentiated cells respectively. Pre-adipocytes re-enter the cell cycle prior to committing to their differentiation and we hypothesised that Topo II could contribute to these processes. We show that Topo IIα expression in 3T3-L1 cells is induced within 16h after the initiation of the differentiation programme, peaks at 24h and rapidly declines thereafter. In contrast Topo IIβ was present both in pre-adipocytes and throughout differentiation. Inhibition of PI3K with LY294002, known to prevent adipocyte differentiation, consistently reduced the expression of Topo IIα, whereas a clear effect on Topo IIβ was not apparent. In addition, inhibition of mTOR with rapamycin also reduced the protein levels of Topo IIα. Using specific class IA PI3K catalytic subunit inhibitors, we show that p110α inhibition with A66 has the greatest reduction of Topo IIα expression and of differentiation, as measured by triglyceride storage. The timing of Topo IIα expression coincides with the mitotic clonal expansion (MCE) phase of differentiation and inhibition of Topo II with ICRF-187 during this stage decreased PPARγ1 and 2 protein levels and triglyceride storage, whereas inhibition later on has little impact. Moreover, the addition of ICRF-187 had no effect on the incorporation of EdU during S-phase at day 1 but lowered the relative cell numbers on day 2. ICRF-187 also induced an increase in the centri/pericentromeric heterochromatin localisation of Topo IIα, indicating a role for Topo IIα at these locations during MCE. In summary, we present evidence that Topo IIα plays an important role in adipogenesis during MCE and in a PI3K/mTOR-dependent manner. Considering that Topoisomerases II are targets in cancer chemotherapy, our results highlight that treatment of cancer with Topo II inhibitors may alter metabolic processes in the adipose tissue. |
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AbstractList | DNA topoisomerases (Topo) are multifunctional enzymes resolving DNA topological problems such as those arising during DNA replication, transcription and mitosis. Mammalian cells express 2 class II isoforms, Topoisomerases IIα (Topo IIα) and IIβ (Topo IIβ), which have similar enzymatic properties but are differently expressed, in dividing and pluripotent cells, and in post-mitotic and differentiated cells respectively. Pre-adipocytes re-enter the cell cycle prior to committing to their differentiation and we hypothesised that Topo II could contribute to these processes. We show that Topo IIα expression in 3T3-L1 cells is induced within 16h after the initiation of the differentiation programme, peaks at 24h and rapidly declines thereafter. In contrast Topo IIβ was present both in pre-adipocytes and throughout differentiation. Inhibition of PI3K with LY294002, known to prevent adipocyte differentiation, consistently reduced the expression of Topo IIα, whereas a clear effect on Topo IIβ was not apparent. In addition, inhibition of mTOR with rapamycin also reduced the protein levels of Topo IIα. Using specific class IA PI3K catalytic subunit inhibitors, we show that p110α inhibition with A66 has the greatest reduction of Topo IIα expression and of differentiation, as measured by triglyceride storage. The timing of Topo IIα expression coincides with the mitotic clonal expansion (MCE) phase of differentiation and inhibition of Topo II with ICRF-187 during this stage decreased PPARγ1 and 2 protein levels and triglyceride storage, whereas inhibition later on has little impact. Moreover, the addition of ICRF-187 had no effect on the incorporation of EdU during S-phase at day 1 but lowered the relative cell numbers on day 2. ICRF-187 also induced an increase in the centri/pericentromeric heterochromatin localisation of Topo IIα, indicating a role for Topo IIα at these locations during MCE. In summary, we present evidence that Topo IIα plays an important role in adipogenesis during MCE and in a PI3K/mTOR-dependent manner. Considering that Topoisomerases II are targets in cancer chemotherapy, our results highlight that treatment of cancer with Topo II inhibitors may alter metabolic processes in the adipose tissue. DNA topoisomerases (Topo) are multifunctional enzymes resolving DNA topological problems such as those arising during DNA replication, transcription and mitosis. Mammalian cells express 2 class II isoforms, Topoisomerases II alpha (Topo II alpha ) and II beta (Topo II beta ), which have similar enzymatic properties but are differently expressed, in dividing and pluripotent cells, and in post-mitotic and differentiated cells respectively. Pre-adipocytes re-enter the cell cycle prior to committing to their differentiation and we hypothesised that Topo II could contribute to these processes. We show that Topo II alpha expression in 3T3-L1 cells is induced within 16 h after the initiation of the differentiation programme, peaks at 24 h and rapidly declines thereafter. In contrast Topo II beta was present both in pre-adipocytes and throughout differentiation. Inhibition of PI3K with LY294002, known to prevent adipocyte differentiation, consistently reduced the expression of Topo II alpha , whereas a clear effect on Topo II beta was not apparent. In addition, inhibition of mTOR with rapamycin also reduced the protein levels of Topo II alpha . Using specific class IA PI3K catalytic subunit inhibitors, we show that p110 alpha inhibition with A66 has the greatest reduction of Topo II alpha expression and of differentiation, as measured by triglyceride storage. The timing of Topo II alpha expression coincides with the mitotic clonal expansion (MCE) phase of differentiation and inhibition of Topo II with ICRF-187 during this stage decreased PPAR gamma 1 and 2 protein levels and triglyceride storage, whereas inhibition later on has little impact. Moreover, the addition of ICRF-187 had no effect on the incorporation of EdU during S-phase at day 1 but lowered the relative cell numbers on day 2. ICRF-187 also induced an increase in the centri/pericentromeric heterochromatin localisation of Topo II alpha , indicating a role for Topo II alpha at these locations during MCE. In summary, we present evidence that Topo II alpha plays an important role in adipogenesis during MCE and in a PI3K/mTOR-dependent manner. Considering that Topoisomerases II are targets in cancer chemotherapy, our results highlight that treatment of cancer with Topo II inhibitors may alter metabolic processes in the adipose tissue. |
Author | Lewis, Aurélia E Jacobsen, Rhîan G Mazloumi Gavgani, Fatemeh Mellgren, Gunnar |
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Keywords | DNA Topoisomerase II Class I PI3K PPARγ Adipogenesis |
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SubjectTerms | 3T3-L1 Cells Adipocytes - cytology Adipocytes - metabolism Adipogenesis Animals Biocatalysis Cell Proliferation Centris Clone Cells DNA - biosynthesis DNA Topoisomerases, Type II - metabolism Isoenzymes - metabolism Mice Mitosis Phosphatidylinositol 3-Kinases - metabolism PPAR gamma - metabolism TOR Serine-Threonine Kinases - metabolism Up-Regulation |
Title | DNA Topoisomerase IIα contributes to the early steps of adipogenesis in 3T3-L1 cells |
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