Pharmacological HIF1 Inhibition Eliminates Downregulation of the Pentose Phosphate Pathway and Prevents Neuronal Apoptosis in Rat Hippocampus Caused by Severe Hypoxia

The pentose phosphate pathway (PPP) of glucose metabolism in the brain serves as a primary source of NADPH which in turn plays a crucial role in multiple cellular processes, including maintenance of redox homeostasis and antioxidant defense. In our model of protective mild hypobaric hypoxia in rats...

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Veröffentlicht in:Journal of molecular neuroscience Jg. 70; H. 5; S. 635 - 646
Hauptverfasser: Vetrovoy, Oleg, Sarieva, Kseniia, Lomert, Ekaterina, Nimiritsky, Peter, Eschenko, Natalia, Galkina, Olga, Lyanguzov, Andrey, Tyulkova, Ekaterina, Rybnikova, Elena
Format: Journal Article
Sprache:Englisch
Veröffentlicht: New York Springer US 01.05.2020
Springer Nature B.V
Schlagworte:
Animals
Antioxidants
Apoptosis
Biomedical and Life Sciences
Biomedicine
Cell Biology
Depletion
Down-Regulation
Glucose
Glucose 6 phosphate dehydrogenase
Glucose metabolism
Glucosephosphate dehydrogenase
Glutathione
Hippocampus
Hippocampus - cytology
Hippocampus - drug effects
Hippocampus - metabolism
Homeostasis
Hypoxia
Hypoxia - drug therapy
Hypoxia - metabolism
Hypoxia-inducible factor 1
Hypoxia-Inducible Factor 1, alpha Subunit - antagonists & inhibitors
Hypoxia-Inducible Factor 1, alpha Subunit - genetics
Hypoxia-Inducible Factor 1, alpha Subunit - metabolism
Hypoxia-inducible factor 1a
Injection
Ischemia
Male
mRNA
NADP
Neurochemistry
Neurology
Neurons - metabolism
Neuroprotection
Neurosciences
Oxidative stress
Pentose
Pentose Phosphate Pathway
Proteomics
Rats
Rats, Wistar
Stimulators
Topotecan
Topotecan - pharmacology
Topotecan - therapeutic use
Pentose phosphate pathway
Oxidative stress
Neuroprotection
Severe hypoxia
Neuronal injury and loss
HIF1
ISSN:0895-8696, 1559-1166, 1559-1166
Online-Zugang:Volltext
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Abstract The pentose phosphate pathway (PPP) of glucose metabolism in the brain serves as a primary source of NADPH which in turn plays a crucial role in multiple cellular processes, including maintenance of redox homeostasis and antioxidant defense. In our model of protective mild hypobaric hypoxia in rats (3MHH), an inverse correlation between hypoxia-inducible factor-1 (HIF1) activity and mRNA levels of glucose-6-phosphate dehydrogenase (G6PD), the key enzyme of PPP, was observed. In the present study, it was demonstrated that severe hypobaric hypoxia (SH) induced short-term upregulation of HIF1 alpha-subunit (HIF1α) in the hippocampal CA1 subfield and decreased the activity of G6PD. The levels of NADPH were also reduced, promoting oxidative stress, triggering apoptosis, and neuronal loss. Injection of a HIF1 inhibitor (HIF1i), topotecan hydrochloride (5 mg/kg, i.p.), before SH prevented the upregulation of HIF1α and normalized G6PD activity. In addition, HIF1i injection caused an increase in NADPH levels, normalization of total glutathione levels and of the cellular redox status as well as suppression of free-radical and apoptotic processes. These results demonstrate a new molecular mechanism of post-hypoxic cerebral pathology development which involves HIF1-dependent PPP depletion and support a recently suggested injurious role of HIF1 activation in the acute phase of cerebral hypoxia/ischemia. Application of PPP stimulators in early post-hypoxic/ischemic period might represent a promising neuroprotective strategy. Graphical abstract HIF1-dependent down-regulation of the pentose phosphate pathway contributes to the hypoxia-induced oxidative stress and neuronal apoptosis in the rat hippocampus
AbstractList The pentose phosphate pathway (PPP) of glucose metabolism in the brain serves as a primary source of NADPH which in turn plays a crucial role in multiple cellular processes, including maintenance of redox homeostasis and antioxidant defense. In our model of protective mild hypobaric hypoxia in rats (3MHH), an inverse correlation between hypoxia-inducible factor-1 (HIF1) activity and mRNA levels of glucose-6-phosphate dehydrogenase (G6PD), the key enzyme of PPP, was observed. In the present study, it was demonstrated that severe hypobaric hypoxia (SH) induced short-term upregulation of HIF1 alpha-subunit (HIF1α) in the hippocampal CA1 subfield and decreased the activity of G6PD. The levels of NADPH were also reduced, promoting oxidative stress, triggering apoptosis, and neuronal loss. Injection of a HIF1 inhibitor (HIF1i), topotecan hydrochloride (5 mg/kg, i.p.), before SH prevented the upregulation of HIF1α and normalized G6PD activity. In addition, HIF1i injection caused an increase in NADPH levels, normalization of total glutathione levels and of the cellular redox status as well as suppression of free-radical and apoptotic processes. These results demonstrate a new molecular mechanism of post-hypoxic cerebral pathology development which involves HIF1-dependent PPP depletion and support a recently suggested injurious role of HIF1 activation in the acute phase of cerebral hypoxia/ischemia. Application of PPP stimulators in early post-hypoxic/ischemic period might represent a promising neuroprotective strategy. Graphical abstract HIF1-dependent down-regulation of the pentose phosphate pathway contributes to the hypoxia-induced oxidative stress and neuronal apoptosis in the rat hippocampus.The pentose phosphate pathway (PPP) of glucose metabolism in the brain serves as a primary source of NADPH which in turn plays a crucial role in multiple cellular processes, including maintenance of redox homeostasis and antioxidant defense. In our model of protective mild hypobaric hypoxia in rats (3MHH), an inverse correlation between hypoxia-inducible factor-1 (HIF1) activity and mRNA levels of glucose-6-phosphate dehydrogenase (G6PD), the key enzyme of PPP, was observed. In the present study, it was demonstrated that severe hypobaric hypoxia (SH) induced short-term upregulation of HIF1 alpha-subunit (HIF1α) in the hippocampal CA1 subfield and decreased the activity of G6PD. The levels of NADPH were also reduced, promoting oxidative stress, triggering apoptosis, and neuronal loss. Injection of a HIF1 inhibitor (HIF1i), topotecan hydrochloride (5 mg/kg, i.p.), before SH prevented the upregulation of HIF1α and normalized G6PD activity. In addition, HIF1i injection caused an increase in NADPH levels, normalization of total glutathione levels and of the cellular redox status as well as suppression of free-radical and apoptotic processes. These results demonstrate a new molecular mechanism of post-hypoxic cerebral pathology development which involves HIF1-dependent PPP depletion and support a recently suggested injurious role of HIF1 activation in the acute phase of cerebral hypoxia/ischemia. Application of PPP stimulators in early post-hypoxic/ischemic period might represent a promising neuroprotective strategy. Graphical abstract HIF1-dependent down-regulation of the pentose phosphate pathway contributes to the hypoxia-induced oxidative stress and neuronal apoptosis in the rat hippocampus.
The pentose phosphate pathway (PPP) of glucose metabolism in the brain serves as a primary source of NADPH which in turn plays a crucial role in multiple cellular processes, including maintenance of redox homeostasis and antioxidant defense. In our model of protective mild hypobaric hypoxia in rats (3MHH), an inverse correlation between hypoxia-inducible factor-1 (HIF1) activity and mRNA levels of glucose-6-phosphate dehydrogenase (G6PD), the key enzyme of PPP, was observed. In the present study, it was demonstrated that severe hypobaric hypoxia (SH) induced short-term upregulation of HIF1 alpha-subunit (HIF1α) in the hippocampal CA1 subfield and decreased the activity of G6PD. The levels of NADPH were also reduced, promoting oxidative stress, triggering apoptosis, and neuronal loss. Injection of a HIF1 inhibitor (HIF1i), topotecan hydrochloride (5 mg/kg, i.p.), before SH prevented the upregulation of HIF1α and normalized G6PD activity. In addition, HIF1i injection caused an increase in NADPH levels, normalization of total glutathione levels and of the cellular redox status as well as suppression of free-radical and apoptotic processes. These results demonstrate a new molecular mechanism of post-hypoxic cerebral pathology development which involves HIF1-dependent PPP depletion and support a recently suggested injurious role of HIF1 activation in the acute phase of cerebral hypoxia/ischemia. Application of PPP stimulators in early post-hypoxic/ischemic period might represent a promising neuroprotective strategy. Graphical abstract HIF1-dependent down-regulation of the pentose phosphate pathway contributes to the hypoxia-induced oxidative stress and neuronal apoptosis in the rat hippocampus.
The pentose phosphate pathway (PPP) of glucose metabolism in the brain serves as a primary source of NADPH which in turn plays a crucial role in multiple cellular processes, including maintenance of redox homeostasis and antioxidant defense. In our model of protective mild hypobaric hypoxia in rats (3MHH), an inverse correlation between hypoxia-inducible factor-1 (HIF1) activity and mRNA levels of glucose-6-phosphate dehydrogenase (G6PD), the key enzyme of PPP, was observed. In the present study, it was demonstrated that severe hypobaric hypoxia (SH) induced short-term upregulation of HIF1 alpha-subunit (HIF1α) in the hippocampal CA1 subfield and decreased the activity of G6PD. The levels of NADPH were also reduced, promoting oxidative stress, triggering apoptosis, and neuronal loss. Injection of a HIF1 inhibitor (HIF1i), topotecan hydrochloride (5 mg/kg, i.p.), before SH prevented the upregulation of HIF1α and normalized G6PD activity. In addition, HIF1i injection caused an increase in NADPH levels, normalization of total glutathione levels and of the cellular redox status as well as suppression of free-radical and apoptotic processes. These results demonstrate a new molecular mechanism of post-hypoxic cerebral pathology development which involves HIF1-dependent PPP depletion and support a recently suggested injurious role of HIF1 activation in the acute phase of cerebral hypoxia/ischemia. Application of PPP stimulators in early post-hypoxic/ischemic period might represent a promising neuroprotective strategy. Graphical abstract HIF1-dependent down-regulation of the pentose phosphate pathway contributes to the hypoxia-induced oxidative stress and neuronal apoptosis in the rat hippocampus
The pentose phosphate pathway (PPP) of glucose metabolism in the brain serves as a primary source of NADPH which in turn plays a crucial role in multiple cellular processes, including maintenance of redox homeostasis and antioxidant defense. In our model of protective mild hypobaric hypoxia in rats (3MHH), an inverse correlation between hypoxia-inducible factor-1 (HIF1) activity and mRNA levels of glucose-6-phosphate dehydrogenase (G6PD), the key enzyme of PPP, was observed. In the present study, it was demonstrated that severe hypobaric hypoxia (SH) induced short-term upregulation of HIF1 alpha-subunit (HIF1α) in the hippocampal CA1 subfield and decreased the activity of G6PD. The levels of NADPH were also reduced, promoting oxidative stress, triggering apoptosis, and neuronal loss. Injection of a HIF1 inhibitor (HIF1i), topotecan hydrochloride (5 mg/kg, i.p.), before SH prevented the upregulation of HIF1α and normalized G6PD activity. In addition, HIF1i injection caused an increase in NADPH levels, normalization of total glutathione levels and of the cellular redox status as well as suppression of free-radical and apoptotic processes. These results demonstrate a new molecular mechanism of post-hypoxic cerebral pathology development which involves HIF1-dependent PPP depletion and support a recently suggested injurious role of HIF1 activation in the acute phase of cerebral hypoxia/ischemia. Application of PPP stimulators in early post-hypoxic/ischemic period might represent a promising neuroprotective strategy.
Author Sarieva, Kseniia
Lomert, Ekaterina
Nimiritsky, Peter
Lyanguzov, Andrey
Tyulkova, Ekaterina
Vetrovoy, Oleg
Eschenko, Natalia
Galkina, Olga
Rybnikova, Elena
Author_xml – sequence: 1
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  orcidid: 0000-0002-1860-5935
  surname: Vetrovoy
  fullname: Vetrovoy, Oleg
  email: vov210292@yandex.ru
  organization: Laboratory of Regulation of Brain Neuron Functions, Pavlov Institute of Physiology, Russian Academy of Sciences, Department of Biochemistry, Faculty of Biology, Saint Petersburg State University
– sequence: 2
  givenname: Kseniia
  surname: Sarieva
  fullname: Sarieva, Kseniia
  organization: Laboratory of Regulation of Brain Neuron Functions, Pavlov Institute of Physiology, Russian Academy of Sciences
– sequence: 3
  givenname: Ekaterina
  surname: Lomert
  fullname: Lomert, Ekaterina
  organization: Laboratory of Cell Biology in Culture, Institute of Cytology, Russian Academy of Sciences
– sequence: 4
  givenname: Peter
  surname: Nimiritsky
  fullname: Nimiritsky, Peter
  organization: Institute for Regenerative Medicine, Medical Research and Education Center, Lomonosov Moscow State University, Faculty of Medicine, Lomonosov Moscow State University
– sequence: 5
  givenname: Natalia
  surname: Eschenko
  fullname: Eschenko, Natalia
  organization: Department of Biochemistry, Faculty of Biology, Saint Petersburg State University
– sequence: 6
  givenname: Olga
  surname: Galkina
  fullname: Galkina, Olga
  organization: Department of Biochemistry, Faculty of Biology, Saint Petersburg State University
– sequence: 7
  givenname: Andrey
  surname: Lyanguzov
  fullname: Lyanguzov, Andrey
  organization: Department of Biochemistry, Faculty of Biology, Saint Petersburg State University
– sequence: 8
  givenname: Ekaterina
  surname: Tyulkova
  fullname: Tyulkova, Ekaterina
  organization: Laboratory of Regulation of Brain Neuron Functions, Pavlov Institute of Physiology, Russian Academy of Sciences
– sequence: 9
  givenname: Elena
  surname: Rybnikova
  fullname: Rybnikova, Elena
  organization: Laboratory of Regulation of Brain Neuron Functions, Pavlov Institute of Physiology, Russian Academy of Sciences
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31865524$$D View this record in MEDLINE/PubMed
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Copyright Springer Science+Business Media, LLC, part of Springer Nature 2019
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ISSN 0895-8696
1559-1166
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Wed Nov 05 01:05:42 EST 2025
Wed Feb 19 02:29:50 EST 2025
Tue Nov 18 21:23:40 EST 2025
Sat Nov 29 04:33:04 EST 2025
Fri Feb 21 02:33:53 EST 2025
IsPeerReviewed true
IsScholarly true
Issue 5
Keywords Pentose phosphate pathway
Oxidative stress
Neuroprotection
Severe hypoxia
Neuronal injury and loss
HIF1
Language English
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Springer Nature B.V
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Snippet The pentose phosphate pathway (PPP) of glucose metabolism in the brain serves as a primary source of NADPH which in turn plays a crucial role in multiple...
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SubjectTerms Animals
Antioxidants
Apoptosis
Biomedical and Life Sciences
Biomedicine
Cell Biology
Depletion
Down-Regulation
Glucose
Glucose 6 phosphate dehydrogenase
Glucose metabolism
Glucosephosphate dehydrogenase
Glutathione
Hippocampus
Hippocampus - cytology
Hippocampus - drug effects
Hippocampus - metabolism
Homeostasis
Hypoxia
Hypoxia - drug therapy
Hypoxia - metabolism
Hypoxia-inducible factor 1
Hypoxia-Inducible Factor 1, alpha Subunit - antagonists & inhibitors
Hypoxia-Inducible Factor 1, alpha Subunit - genetics
Hypoxia-Inducible Factor 1, alpha Subunit - metabolism
Hypoxia-inducible factor 1a
Injection
Ischemia
Male
mRNA
NADP
Neurochemistry
Neurology
Neurons - metabolism
Neuroprotection
Neurosciences
Oxidative stress
Pentose
Pentose Phosphate Pathway
Proteomics
Rats
Rats, Wistar
Stimulators
Topotecan
Topotecan - pharmacology
Topotecan - therapeutic use
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Title Pharmacological HIF1 Inhibition Eliminates Downregulation of the Pentose Phosphate Pathway and Prevents Neuronal Apoptosis in Rat Hippocampus Caused by Severe Hypoxia
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