The Circadian Clock Protein CRY1 Is a Negative Regulator of HIF-1α

The circadian clock and the hypoxia-signaling pathway are regulated by an integrated interplay of positive and negative feedback limbs that incorporate energy homeostasis and carcinogenesis. We show that the negative circadian regulator CRY1 is also a negative regulator of hypoxia-inducible factor (...

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Published iniScience Vol. 13; pp. 284 - 304
Main Authors Dimova, Elitsa Y., Jakupovic, Mirza, Kubaichuk, Kateryna, Mennerich, Daniela, Chi, Tabughang Franklin, Tamanini, Filippo, Oklejewicz, Małgorzata, Hänig, Jens, Byts, Nadiya, Mäkelä, Kari A., Herzig, Karl-Heinz, Koivunen, Peppi, Chaves, Ines, van der Horst, Gijsbertus, Kietzmann, Thomas
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 29.03.2019
Elsevier
Subjects
Biochemistry
Biological Sciences
Cell Biology
Molecular Biology
Biological Sciences
Biochemistry
Molecular Biology
Cell Biology
Online AccessGet full text
ISSN2589-0042
2589-0042
DOI10.1016/j.isci.2019.02.027

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Abstract The circadian clock and the hypoxia-signaling pathway are regulated by an integrated interplay of positive and negative feedback limbs that incorporate energy homeostasis and carcinogenesis. We show that the negative circadian regulator CRY1 is also a negative regulator of hypoxia-inducible factor (HIF). Mechanistically, CRY1 interacts with the basic-helix-loop-helix domain of HIF-1α via its tail region. Subsequently, CRY1 reduces HIF-1α half-life and binding of HIFs to target gene promoters. This appeared to be CRY1 specific because genetic disruption of CRY1, but not CRY2, affected the hypoxia response. Furthermore, CRY1 deficiency could induce cellular HIF levels, proliferation, and migration, which could be reversed by CRISPR/Cas9- or short hairpin RNA-mediated HIF knockout. Altogether, our study provides a mechanistic explanation for genetic association studies linking a disruption of the circadian clock with hypoxia-associated processes such as carcinogenesis. [Display omitted] •Hypoxia and HIFs affect the circadian rhythm•CRY1 directly interacts with both HIF-1α and HIF-2α•CRY1 inhibits binding of HIFs to its target gene promoters•The CRY1-HIFα interaction has opposite roles on cellular growth and migration Biological Sciences; Biochemistry; Molecular Biology; Cell Biology
AbstractList The circadian clock and the hypoxia-signaling pathway are regulated by an integrated interplay of positive and negative feedback limbs that incorporate energy homeostasis and carcinogenesis. We show that the negative circadian regulator CRY1 is also a negative regulator of hypoxia-inducible factor (HIF). Mechanistically, CRY1 interacts with the basic-helix-loop-helix domain of HIF-1α via its tail region. Subsequently, CRY1 reduces HIF-1α half-life and binding of HIFs to target gene promoters. This appeared to be CRY1 specific because genetic disruption of CRY1, but not CRY2, affected the hypoxia response. Furthermore, CRY1 deficiency could induce cellular HIF levels, proliferation, and migration, which could be reversed by CRISPR/Cas9- or short hairpin RNA-mediated HIF knockout. Altogether, our study provides a mechanistic explanation for genetic association studies linking a disruption of the circadian clock with hypoxia-associated processes such as carcinogenesis. : Biological Sciences; Biochemistry; Molecular Biology; Cell Biology Subject Areas: Biological Sciences, Biochemistry, Molecular Biology, Cell Biology
The circadian clock and the hypoxia-signaling pathway are regulated by an integrated interplay of positive and negative feedback limbs that incorporate energy homeostasis and carcinogenesis. We show that the negative circadian regulator CRY1 is also a negative regulator of hypoxia-inducible factor (HIF). Mechanistically, CRY1 interacts with the basic-helix-loop-helix domain of HIF-1α via its tail region. Subsequently, CRY1 reduces HIF-1α half-life and binding of HIFs to target gene promoters. This appeared to be CRY1 specific because genetic disruption of CRY1, but not CRY2, affected the hypoxia response. Furthermore, CRY1 deficiency could induce cellular HIF levels, proliferation, and migration, which could be reversed by CRISPR/Cas9- or short hairpin RNA-mediated HIF knockout. Altogether, our study provides a mechanistic explanation for genetic association studies linking a disruption of the circadian clock with hypoxia-associated processes such as carcinogenesis. [Display omitted] •Hypoxia and HIFs affect the circadian rhythm•CRY1 directly interacts with both HIF-1α and HIF-2α•CRY1 inhibits binding of HIFs to its target gene promoters•The CRY1-HIFα interaction has opposite roles on cellular growth and migration Biological Sciences; Biochemistry; Molecular Biology; Cell Biology
The circadian clock and the hypoxia-signaling pathway are regulated by an integrated interplay of positive and negative feedback limbs that incorporate energy homeostasis and carcinogenesis. We show that the negative circadian regulator CRY1 is also a negative regulator of hypoxia-inducible factor (HIF). Mechanistically, CRY1 interacts with the basic-helix-loop-helix domain of HIF-1α via its tail region. Subsequently, CRY1 reduces HIF-1α half-life and binding of HIFs to target gene promoters. This appeared to be CRY1 specific because genetic disruption of CRY1, but not CRY2, affected the hypoxia response. Furthermore, CRY1 deficiency could induce cellular HIF levels, proliferation, and migration, which could be reversed by CRISPR/Cas9- or short hairpin RNA-mediated HIF knockout. Altogether, our study provides a mechanistic explanation for genetic association studies linking a disruption of the circadian clock with hypoxia-associated processes such as carcinogenesis. • Hypoxia and HIFs affect the circadian rhythm • CRY1 directly interacts with both HIF-1α and HIF-2α • CRY1 inhibits binding of HIFs to its target gene promoters • The CRY1-HIFα interaction has opposite roles on cellular growth and migration Biological Sciences; Biochemistry; Molecular Biology; Cell Biology
The circadian clock and the hypoxia-signaling pathway are regulated by an integrated interplay of positive and negative feedback limbs that incorporate energy homeostasis and carcinogenesis. We show that the negative circadian regulator CRY1 is also a negative regulator of hypoxia-inducible factor (HIF). Mechanistically, CRY1 interacts with the basic-helix-loop-helix domain of HIF-1α via its tail region. Subsequently, CRY1 reduces HIF-1α half-life and binding of HIFs to target gene promoters. This appeared to be CRY1 specific because genetic disruption of CRY1, but not CRY2, affected the hypoxia response. Furthermore, CRY1 deficiency could induce cellular HIF levels, proliferation, and migration, which could be reversed by CRISPR/Cas9- or short hairpin RNA-mediated HIF knockout. Altogether, our study provides a mechanistic explanation for genetic association studies linking a disruption of the circadian clock with hypoxia-associated processes such as carcinogenesis.The circadian clock and the hypoxia-signaling pathway are regulated by an integrated interplay of positive and negative feedback limbs that incorporate energy homeostasis and carcinogenesis. We show that the negative circadian regulator CRY1 is also a negative regulator of hypoxia-inducible factor (HIF). Mechanistically, CRY1 interacts with the basic-helix-loop-helix domain of HIF-1α via its tail region. Subsequently, CRY1 reduces HIF-1α half-life and binding of HIFs to target gene promoters. This appeared to be CRY1 specific because genetic disruption of CRY1, but not CRY2, affected the hypoxia response. Furthermore, CRY1 deficiency could induce cellular HIF levels, proliferation, and migration, which could be reversed by CRISPR/Cas9- or short hairpin RNA-mediated HIF knockout. Altogether, our study provides a mechanistic explanation for genetic association studies linking a disruption of the circadian clock with hypoxia-associated processes such as carcinogenesis.
The circadian clock and the hypoxia-signaling pathway are regulated by an integrated interplay of positive and negative feedback limbs that incorporate energy homeostasis and carcinogenesis. We show that the negative circadian regulator CRY1 is also a negative regulator of hypoxia-inducible factor (HIF). Mechanistically, CRY1 interacts with the basic-helix-loop-helix domain of HIF-1α via its tail region. Subsequently, CRY1 reduces HIF-1α half-life and binding of HIFs to target gene promoters. This appeared to be CRY1 specific because genetic disruption of CRY1, but not CRY2, affected the hypoxia response. Furthermore, CRY1 deficiency could induce cellular HIF levels, proliferation, and migration, which could be reversed by CRISPR/Cas9- or short hairpin RNA-mediated HIF knockout. Altogether, our study provides a mechanistic explanation for genetic association studies linking a disruption of the circadian clock with hypoxia-associated processes such as carcinogenesis.
Author Koivunen, Peppi
Dimova, Elitsa Y.
Kietzmann, Thomas
Mennerich, Daniela
van der Horst, Gijsbertus
Chaves, Ines
Byts, Nadiya
Kubaichuk, Kateryna
Tamanini, Filippo
Oklejewicz, Małgorzata
Jakupovic, Mirza
Chi, Tabughang Franklin
Herzig, Karl-Heinz
Mäkelä, Kari A.
Hänig, Jens
AuthorAffiliation 1 Faculty of Biochemistry and Molecular Medicine and Biocenter Oulu, University of Oulu, P.O. Box 3000, 90014 Oulu, Finland
2 Department of Biochemistry, University of Kaiserslautern, 67663 Kaiserslautern, Germany
5 Biocenter Oulu, Department of Physiology, University of Oulu, 90014 Oulu, Finland
4 Novartis Pharma GmbH, 97082 Würzburg, Germany
3 Department of Molecular Genetics, Erasmus University Medical Center, Wytemaweg 80, 3015CN Rotterdam, the Netherlands
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30875610$$D View this record in MEDLINE/PubMed
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Keywords Biological Sciences
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Snippet The circadian clock and the hypoxia-signaling pathway are regulated by an integrated interplay of positive and negative feedback limbs that incorporate energy...
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SubjectTerms Biochemistry
Biological Sciences
Cell Biology
Molecular Biology
Title The Circadian Clock Protein CRY1 Is a Negative Regulator of HIF-1α
URI https://dx.doi.org/10.1016/j.isci.2019.02.027
https://www.ncbi.nlm.nih.gov/pubmed/30875610
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