Reciprocal regulation of carbon monoxide metabolism and the circadian clock

Klemz, Roman; Reischl, Silke; Wallach, Thomas; Witte, Nicole; Jürchott, Karsten; Klemz, Sabrina; Lang, Veronika; Lorenzen, Stephan; Knauer, Miriam; Heidenreich, Steffi; Xu, Min; Ripperger, Jürgen A.; Schupp, Michael; Stanewsky, Ralf; Kramer, Achim

doi:10.1038/nsmb.3331

Cited by 50 publications

(50 citation statements)

References 66 publications

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“…After initial synchronization to LD cycles, bioluminescence signals from individual pairs of halteres were measured in constant darkness and temperature (DD, 25°C) with 30 min or 1 hr time resolution. In order to determine the period-length of the bioluminescence oscillations, data were detrended and subjected to curve fitting ( Figure 1C, (Klemz et al, 2017)).…”

Section: Resultsmentioning

confidence: 99%

A robust and self-sustained peripheral circadian oscillator reveals differences in temperature compensation properties with central brain clocks

Versteven

Ernst

Stanewsky

2020

Preprint

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Circadian clocks temporally organize physiology and behavior of organisms exposed to the daily changes of light and temperature on our planet, thereby contributing to fitness and health. Circadian clocks and the biological rhythms they control are characterized by three properties. (1) The rhythms are self-sustained in constant conditions with a period of ~ 24 hr,(2), they can be synchronized to the environmental cycles of light and temperature, and (3), they are temperature compensated, meaning they run with the same speed at different temperatures within the physiological range of the organism. Apart from the central clocks located in or near the brain, which regulate the daily activity rhythms of animals, the so-called peripheral clocks are dispersed throughout the body of insects and vertebrates. Based on the three defining properties, it has been difficult to determine if these peripheral clocks are true circadian clocks. We used a set of clock gene -luciferase reporter genes to address this question in Drosophila circadian clocks. We show that self-sustained fly peripheral oscillators over compensate temperature changes, i.e., they slow down with increasing temperature.This over-compensation is not observed in central clock neurons in the fly brain, both in intact flies and in cultured brains, suggesting that neural network properties contribute to temperature compensation. However, an important neuropeptide for synchronizing the circadian neuronal network, the Pigment Dispersing Factor (PDF), is not required for selfsustained and temperature-compensated oscillations in subsets of the central clock neurons.Our findings reveal a fundamental difference between central and peripheral clocks, which likely also applies for vertebrate clocks.

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Section: Resultsmentioning

confidence: 99%

A robust and self-sustained peripheral circadian oscillator reveals differences in temperature compensation properties with central brain clocks

Versteven

Ernst

Stanewsky

2020

Preprint

Self Cite

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“…Sequestration through the formation of heme aggregates such as hemozoin is considered a primary route of heme detoxification in hematophagous organisms (Lara et al, 2005;Otterbein et al, 2000;Toh et al, 2010), thus AgHO likely plays a role in the degradation of the blood heme fraction that escapes heme aggregation. HO may play other roles, however; for instance, in D. melanogaster, DmHO appears to play a role in tissue development (Cui et al, 2008) and regulation of circadian rhythms (Klemz et al, 2017). Mice lacking HO-1 have impaired production of oocytes (Zenclussen et al, 2012) and there is accruing evidence that mammalian HO plays an important role in the female reproductive system, potentially through the influence of CO production on the regulation of metabolic pathways (Němeček et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Characterisation of Anopheles gambiae heme oxygenase and metalloporphyrin feeding suggests a potential role in reproduction

Spencer

Yunta

Lima

et al. 2018

Insect Biochemistry and Molecular Biology

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The mosquito Anopheles gambiae is the principal vector for malaria in sub-Saharan Africa. The ability of A. gambiae to transmit malaria is strictly related to blood feeding and digestion, which releases nutrients for oogenesis, as well as substantial amounts of highly toxic free heme. Heme degradation by heme oxygenase (HO) is a common protective mechanism, and a gene for HO exists in the An. gambiae genome HO (AgHO), although it has yet to be functionally examined. Here, we have cloned and expressed An. gambiae HO (AgHO) in E. coli. Purified recombinant AgHO bound hemin stoichiometrically to form a hemin-enzyme complex similar to other HOs, with a K of 3.9 ± 0.6 μM; comparable to mammalian and bacterial HOs, but 7-fold lower than that of Drosophila melanogaster HO. AgHO also degraded hemin to biliverdin and released CO and iron in the presence of NADPH cytochrome P450 oxidoreductase (CPR). Optimal AgHO activity was observed at 27.5 °C and pH 7.5. To investigate effects of AgHO inhibition, adult female A. gambiae were fed heme analogues Sn- and Zn-protoporphyrins (SnPP and ZnPP), known to inhibit HO. These led to a dose dependent decrease in oviposition. Cu-protoporphyrin (CuPP), which does not inhibit HO had no effect. These results demonstrate that AgHO is a catalytically active HO and that it may play a key role in egg production in mosquitoes. It also presents a potential target for the development of compounds aimed at sterilising mosquitoes for vector control.

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“…Rhythmic time series can be categorized into those showing stationary oscillatory properties and the non-stationary ones where periods, amplitudes and phases change over time. Many currently available tools for the analysis of biological rhythms rely on methods aimed at stationary oscillatory data, using either a standalone software environment such as BRASS (Edwards et al [2010], Locke et al [2005]), ChronoStar (Klemz et al [2017]) and CIRCADA (Cenek et al [2020]) or an online interfaces such as BioDare , Zielinski et al [2014]).…”

Section: Discussionmentioning

confidence: 99%

Optimal time frequency analysis for biological data - pyBOAT

Mönke¹,

Sorgenfrei

Schmal

et al. 2020

Preprint

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Methods for the quantication of rhythmic biological signals have been essential for the discovery of function and design of biological oscillators. Advances in live measurements have allowed recordings of unprecedented resolution revealing a new world of complex heterogeneous oscillations with multiple noisy non-stationary features. However, our understanding of the underlying mechanisms regulating these oscillations has been lagging behind, partially due to the lack of simple tools to reliably quantify these complex non-stationary features. With this challenge in mind, we have developed pyBOAT, a Python-based fully automatic stand-alone software that integrates multiple steps of non-stationary oscillatory time series analysis into an easy-to-use graphical user interface. pyBOAT implements continuous wavelet analysis which is specically designed to reveal time-dependent features. In this work we illustrate the advantages of our tool by analyzing complex non-stationary time-series proles. Our approach integrates data-visualization, optimized sinc-lter detrending, amplitude envelope removal and a subsequent continuous-wavelet based timefrequency analysis. Finally, using analytical considerations and numerical simulations we discuss unexpected pitfalls in commonly used smoothing and detrending operations.

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Reciprocal regulation of carbon monoxide metabolism and the circadian clock

Cited by 50 publications

References 66 publications

A robust and self-sustained peripheral circadian oscillator reveals differences in temperature compensation properties with central brain clocks

A robust and self-sustained peripheral circadian oscillator reveals differences in temperature compensation properties with central brain clocks

Characterisation of Anopheles gambiae heme oxygenase and metalloporphyrin feeding suggests a potential role in reproduction

Optimal time frequency analysis for biological data - pyBOAT

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