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Article

Functional RNA Dynamics Are Progressively Governed by RNA Destabilization during the Adaptation to Chronic Hypoxia

by
Rebekka Bauer
1,
Sofie Patrizia Meyer
1,
Karolina Anna Kloss
2,
Vanesa Maria Guerrero Ruiz
1,
Samira Reuscher
2,
You Zhou
2,
Dominik Christian Fuhrmann
1,3,
Kathi Zarnack
2,*,
Tobias Schmid
1,3,*,† and
Bernhard Brüne
1,3,4,5,†
1
Faculty of Medicine, Institute of Biochemistry I, Goethe-University Frankfurt, 60590 Frankfurt, Germany
2
Faculty of Biological Sciences, Buchmann Institute for Molecular Life Sciences (BMLS), Goethe-University Frankfurt, 60438 Frankfurt, Germany
3
German Cancer Consortium (DKTK), Partner Site Frankfurt, 60590 Frankfurt, Germany
4
Frankfurt Cancer Institute, Goethe-University Frankfurt, 60596 Frankfurt, Germany
5
Fraunhofer Institute for Translational Medicine and Pharmacology, 60596 Frankfurt, Germany
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2022, 23(10), 5824; https://doi.org/10.3390/ijms23105824
Submission received: 6 April 2022 / Revised: 17 May 2022 / Accepted: 20 May 2022 / Published: 22 May 2022
(This article belongs to the Special Issue Molecular Mechanisms of Adaptation to Hypoxia)
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Abstract

Previous studies towards reduced oxygen availability have mostly focused on changes in total mRNA expression, neglecting underlying transcriptional and post-transcriptional events. Therefore, we generated a comprehensive overview of hypoxia-induced changes in total mRNA expression, global de novo transcription, and mRNA stability in monocytic THP-1 cells. Since hypoxic episodes often persist for prolonged periods, we further compared the adaptation to acute and chronic hypoxia. While total mRNA changes correlated well with enhanced transcription during short-term hypoxia, mRNA destabilization gained importance under chronic conditions. Reduced mRNA stability not only added to a compensatory attenuation of immune responses, but also, most notably, to the reduction in nuclear-encoded mRNAs associated with various mitochondrial functions. These changes may prevent the futile production of new mitochondria under conditions where mitochondria cannot exert their full metabolic function and are indeed actively removed by mitophagy. The post-transcriptional mode of regulation might further allow for the rapid recovery of mitochondrial capacities upon reoxygenation. Our results provide a comprehensive resource of functional mRNA expression dynamics and underlying transcriptional and post-transcriptional regulatory principles during the adaptation to hypoxia. Furthermore, we uncover that RNA stability regulation controls mitochondrial functions in the context of hypoxia.
Keywords: hypoxia; monocytes; de novo transcription; RNA stability; SLAM-seq; GRAND-SLAM hypoxia; monocytes; de novo transcription; RNA stability; SLAM-seq; GRAND-SLAM

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MDPI and ACS Style

Bauer, R.; Meyer, S.P.; Kloss, K.A.; Guerrero Ruiz, V.M.; Reuscher, S.; Zhou, Y.; Fuhrmann, D.C.; Zarnack, K.; Schmid, T.; Brüne, B. Functional RNA Dynamics Are Progressively Governed by RNA Destabilization during the Adaptation to Chronic Hypoxia. Int. J. Mol. Sci. 2022, 23, 5824. https://doi.org/10.3390/ijms23105824

AMA Style

Bauer R, Meyer SP, Kloss KA, Guerrero Ruiz VM, Reuscher S, Zhou Y, Fuhrmann DC, Zarnack K, Schmid T, Brüne B. Functional RNA Dynamics Are Progressively Governed by RNA Destabilization during the Adaptation to Chronic Hypoxia. International Journal of Molecular Sciences. 2022; 23(10):5824. https://doi.org/10.3390/ijms23105824

Chicago/Turabian Style

Bauer, Rebekka, Sofie Patrizia Meyer, Karolina Anna Kloss, Vanesa Maria Guerrero Ruiz, Samira Reuscher, You Zhou, Dominik Christian Fuhrmann, Kathi Zarnack, Tobias Schmid, and Bernhard Brüne. 2022. "Functional RNA Dynamics Are Progressively Governed by RNA Destabilization during the Adaptation to Chronic Hypoxia" International Journal of Molecular Sciences 23, no. 10: 5824. https://doi.org/10.3390/ijms23105824

APA Style

Bauer, R., Meyer, S. P., Kloss, K. A., Guerrero Ruiz, V. M., Reuscher, S., Zhou, Y., Fuhrmann, D. C., Zarnack, K., Schmid, T., & Brüne, B. (2022). Functional RNA Dynamics Are Progressively Governed by RNA Destabilization during the Adaptation to Chronic Hypoxia. International Journal of Molecular Sciences, 23(10), 5824. https://doi.org/10.3390/ijms23105824

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