Daily rhythmicity of high affinity copper transport

Perea-García, Ana; Sanz, Ana Gimeno; Moreno, J.; Andrés-Bordería, Amparo; Mayo, Sonia; Davis, Amanda M; Huijser, Peter; Davis, Seth J; Peñarrubia, Lola

doi:10.1080/15592324.2016.1140291

Cited by 8 publications

(6 citation statements)

References 23 publications

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“…The relationship between trace metals, circadian rhythms, and metabolism is still largely uninvestigated, but several studies in plants demonstrate rhythms in copper and iron homeostasis and how they pertain to circadian activity and metabolism (Andres‐Colas et al., ; Penarrubia et al., ; Perea‐Garcia, Sanz, et al., ; Tissot et al., ). As Cu plays a role in iron homeostasis, it is noteworthy that a circadian rhythm in iron levels in the midbrain of mice has been reported (Unger et al., , ), and there is growing evidence of evolutionarily conserved, circadian control of iron homeostasis and vice‐versa (Ben‐Shlomo et al., ; Botebol et al., ; Cao, Li, Jin, & Hu, ; Dean, Allen, O'Donnell, & Earley, ; Mandilaras & Missirlis, ; Marelja, Leimkuhler, & Missirlis, ; Okazaki et al., ; Robles et al., ; Saha et al., ; Simcox et al., ; Tissot et al., ; Zhang et al., ).…”

Section: Discussionmentioning

confidence: 99%

“…Cu is essential for normal COX function, and hence oxidative phosphorylation, and the TTFL clock may coordinate Cu homeostasis to ensure timely cellular Cu import and/or delivery to mitochondrial proteins. Interestingly, in Arabidopsis thaliana , clock proteins have been shown to regulate the expression of Cu import and export proteins such that cytosolic Cu may exhibit a circadian oscillation (Penarrubia et al., ; Perea‐Garcia, Andres‐Borderia, et al., ; Perea‐Garcia, Sanz, et al., ). On the other hand, unanticipated changes in cytosolic and mitochondrial Cu levels may induce responses that feedback on TTFL clock function.…”

Section: Introductionmentioning

confidence: 99%

“…On the other hand, unanticipated changes in cytosolic and mitochondrial Cu levels may induce responses that feedback on TTFL clock function. In Arabidopsis , a Cu‐metabolism relationship has been shown to affect circadian output and growth (Andres‐Colas, Perea‐Garcia, Puig, & Penarrubia, ; Perea‐Garcia, Andres‐Borderia, et al., ; Perea‐Garcia, Sanz, et al., ). Similarly, exposure to Cu has been shown to affect circadian gene expression in zebrafish (Doria et al., ; Vicario‐Pares et al., ).…”

Section: Introductionmentioning

confidence: 99%

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Copper in the suprachiasmatic circadian clock: A possible link between multiple circadian oscillators

Yamada

Prosser

2018

Eur J of Neuroscience

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The mammalian circadian clock in the suprachiasmatic nucleus (SCN) is very robust, able to coordinate our daily physiological and behavioral rhythms with exquisite accuracy. Simultaneously, the SCN clock is highly sensitive to environmental timing cues such as the solar cycle. This duality of resiliency and sensitivity may be sustained in part by a complex intertwining of three cellular oscillators: transcription/translation, metabolic/redox, and membrane excitability. We suggest here that one of the links connecting these oscillators may be forged from copper (Cu). Cellular Cu levels are highly regulated in the brain and peripherally, and Cu affects cellular metabolism, redox state, cell signaling, and transcription. We have shown that both Cu chelation and application induce nighttime phase shifts of the SCN clock in vitro and that these treatments affect glutamate, N‐methyl‐D‐aspartate receptor, and associated signaling processes differently. More recently we found that Cu induces mitogen‐activated protein kinase‐dependent phase shifts, while the mechanisms by which Cu removal induces phase shifts remain unclear. Lastly, we have found that two Cu transporters are expressed in the SCN, and that one of these transporters (ATP7A) exhibits a day/night rhythm. Our results suggest that Cu homeostasis is tightly regulated in the SCN, and that changes in Cu levels may serve as a time cue for the circadian clock. We discuss these findings in light of the existing literature and current models of multiple coupled circadian oscillators in the SCN.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Copper in the suprachiasmatic circadian clock: A possible link between multiple circadian oscillators

Yamada

Prosser

2018

Eur J of Neuroscience

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“…Reports investigating the roles of calcium, copper, iron, zinc and magnesium ions illustrate the critical nutritional role of several metals and the homeostatic relations between them [25,26,50]. Indeed the increased concentration of several of these metals causes alterations in signalling, and it is known that the uptake and transport of all of these ions are themselves subject to circadian regulation [6,46,47,51]. Another area of concern regards the contamination of soils [42].…”

Section: Environmental Contextmentioning

confidence: 99%

Multiple metals influence distinct properties of the Arabidopsis circadian clock

Hargreaves

Oakenfull

Davis

et al. 2021

Preprint

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Circadian rhythms coordinate endogenous events with external signals, and are essential to biological function. When environmental contaminants affect these rhythms, the organism may experience fitness consequences such as reduced growth or increased susceptibility to pathogens. In their natural environment plants may be exposed to a wide range of industrial and agricultural pollutants. Here, we investigate how the addition of various metal salts to the environment can impact plant-circadian rhythms, via the promoter:luciferase system. The consequences of these environmental changes were found to be varied and complex. Therefore, in addition to Fourier-based analyses, we apply novel wavelet-based spectral hypothesis testing and clustering methodologies to organize and understand the data. We are able to classify broad sets of responses to environmental contaminants, including pollutants which increase, or decrease, the period, or which induce a lack of precision or disrupt any meaningful periodicity. The methods are general, and may be applied to discover common responses and hidden structures within a wide range of biological time series data.

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“…It has been suggested that the SPL7-mediated auto-regulatory effect of Cu on pmCOPT expression could establish a feedback loop responsible for cyclic expression, peaking at dawn ( Andrés-Colás et al, 2010 ; Peñarrubia et al, 2010 ). Deregulated Cu + uptake in COPT-overexpressing plants causes abnormal development in the absence of environmental cycles ( Andrés-Colás et al, 2010 ; Perea-García et al, 2016a , b ). Furthermore, the observed interaction between SPL7 and ELONGATED HYPOCOTYL5 (HY5) underscores a connection between Cu homeostasis and light ( Zhang et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

Expression of the Intracellular COPT3-Mediated Cu Transport Is Temporally Regulated by the TCP16 Transcription Factor

et al. 2018

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Copper is an essential element in plants. When scarce, copper is acquired from extracellular environment or remobilized from intracellular sites, through members of the high affinity copper transporters family COPT located at the plasma membrane and internal membrane, respectively. Here, we show that COPT3 is an intracellular copper transporter, located at a compartment of the secretory pathway, that is mainly expressed in pollen grains and vascular bundles. Contrary to the COPT1 plasma membrane member, the expression of the internal COPT3 membrane transporter was higher at 12 h than at 0 h of a neutral photoperiod day under copper deficiency. The screening of a library of conditionally overexpressed transcription factors implicated members of the TCP family in the COPT3 differential temporal expression pattern. Particularly, in vitro, TCP16 was found to bind to the COPT3 promoter and down-regulated its expression. Accordingly, TCP16 was mainly expressed at 0 h under copper deficiency and induced at 12 h by copper excess. Moreover, TCP16 overexpression resulted in increased sensitivity to copper deficiency, whereas the tcp16 mutant was sensitive to copper excess. Both copper content and the expression of particular copper status markers were altered in plants with modified levels of TCP16. Consistent with TCP16 affecting pollen development, the lack of COPT3 function led to altered pollen morphology. Furthermore, analysis of copt3 and COPT3 overexpressing plants revealed that COPT3 function exerted a negative effect on TCP16 expression. Taken together, these results suggest a differential daily regulation of copper uptake depending on the external and internal copper pools, in which TCP16 inhibits copper remobilization at dawn through repression of intracellular transporters.

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Daily rhythmicity of high affinity copper transport

Cited by 8 publications

References 23 publications

Copper in the suprachiasmatic circadian clock: A possible link between multiple circadian oscillators

Copper in the suprachiasmatic circadian clock: A possible link between multiple circadian oscillators

Multiple metals influence distinct properties of the Arabidopsis circadian clock

Expression of the Intracellular COPT3-Mediated Cu Transport Is Temporally Regulated by the TCP16 Transcription Factor

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