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Circadian Regulation and Clock-Controlled Mechanisms of Glycerophospholipid Metabolism from Neuronal Cells and Tissues to Fibroblasts

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Abstract

Along evolution, living organisms developed a precise timekeeping system, circadian clocks, to adapt life to the 24-h light/dark cycle and temporally regulate physiology and behavior. The transcriptional molecular circadian clock and metabolic/redox oscillator conforming these clocks are present in organs, tissues, and even in individual cells, where they exert circadian control over cellular metabolism. Disruption of the molecular clock may cause metabolic disorders and higher cancer risk. The synthesis and degradation of glycerophospholipids (GPLs) is one of the most highly regulated metabolisms across the 24-h cycle in terms of total lipid content and enzyme expression and activity in the nervous system and individual cells. Lipids play a plethora of roles (membrane biogenesis, energy sourcing, signaling, and the regulation of protein-chromatin interaction, among others), making control of their metabolism a vital checkpoint in the cellular organization of physiology. An increasing body of evidence clearly demonstrates an orchestrated and sequential series of events occurring in GPL metabolism across the 24-h day in diverse retinal cell layers, immortalized fibroblasts, and glioma cells. Moreover, the clock gene Per1 and other circadian-related genes are tightly involved in the regulation of GPL synthesis in quiescent cells. However, under proliferation, the metabolic oscillator continues to control GPL metabolism of brain cancer cells even after molecular circadian clock disruption, reflecting the crucial role of the temporal metabolism organization in cell preservation. The aim of this review is to examine the control exerted by circadian clocks over GPL metabolism, their synthesizing enzyme expression and activities in normal and tumorous cells of the nervous system and in immortalized fibroblasts.

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Abbreviations

AA:

Arachidonic acid

ACC:

Acetyl-CoA carboxylase

AMPK:

Adenosine monophosphate-regulated kinase

BMAL1:

Aryl hydrocarbon receptor translocator-like protein 1

cAMP:

Cyclic adenosine monophosphate

CCG:

Clock-controlled genes

CCT:

CTP:phosphocholine cytidylyltransferase

CET:

CTP:ethanolamine cytidylyltransferase

CG:

Clock genes

ChoK:

Choline kinase

CLOCK:

Circadian locomotor output cycles kaput

CNS:

Central nervous system (CNS)

CPT:

CDP‐choline:1,2‐diacylglycerol cholinephosphotransferase

CREB:

CAMP response elements and protein-CRE binding

CRY:

Cryptochrome

DAG:

Diacylglycerol

DD:

Constant darkness

DEX:

Dexamethasone

DGL:

Diacylglycerol lipase

DHA:

Docosahexaenoic acid (DHA, 22:6n-3)

DHAP:

Dihydroxyacetone phosphate

EK:

Ethanolamine kinase

EPT:

1,2‐Diacylglycerol ethanolaminephosphotransferase

ER:

Endoplasmic reticulum;

FA:

Fatty acid

G3P:

Glycerol-3-phosphate

GBM:

Glioblastoma multiforme

GCL:

Ganglion cell layer

GPAT:

G3P acyltransferase;

GPL:

Glycerophospholipids

GR:

Glucocorticoid receptors

GRE:

Glucocorticoid response elements

HIF1 α:

Hypoxia-inducible factor 1α

INL:

Inner nuclear layer cells

iPLA2:

Calcium-independent phospholipase A2

L/D:

Light dark cycle

LD:

Lipid droplet

LL:

Constant light

LPA:

Lysophosphatidic acid

LPAAT:

Lysophosphatidic acid acyltransferase

LPCAT:

Lysophosphatidylcholine acyltransferase

LPEAT:

Lysophosphatidylethanolamine acyltransferase

LPIAT:

Lysophosphatidylinositol acyltransferase

LPLAT:

Lysophospholipid acyltransferase

NAD+ :

Nicotinamide adenine dinucleotide

NPAS2:

PAS domain-containing protein 2

NR:

Nuclear receptor

ONL:

Outer plexiform layer

OS:

Outer segments

PA:

Phosphatidic acid

PAP:

Phosphatidate phosphohydrolase

PAP-2:

Phosphate phosphatase

PARP-1:

Poly (ADP-ribose) polymerase 1;

PC:

Phosphatidylcholine

PE:

Phosphatidylethanolamine

PEMT:

Phosphatidylethanolamine methyl transferase

PER:

Period

PGC-1α:

Peroxisome proliferator-activated receptor gamma coactivator1-alpha

PI:

Phosphatidylinositol

PLA2:

Phospholipases A2

PPAR:

Peroxisome proliferator-activated receptor

PPRE:

PPAR regulatory element

PRX:

Peroxiredoxin

PS:

Phosphatidylserine

ROR:

Retinoic acid receptor-related orphan receptor

RORE:

Retinoic acid receptor-related orphan receptor response element

ROS:

Reactive oxygen species

SCN:

Suprachiasmatic nuclei

SIRT1:

NAD+ -dependent deacetylase

SPM:

Sphingomyelin

SRE:

Serum response element

SREBP:

Sterol regulatory element-binding protein

SRF:

Serum response factor

TAG:

Triacylglycerol

TTFL:

Transcriptional–translational feedback loop

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Acknowledgements

This work has been supported by Agencia Nacional de Promoción Científica y Técnica (FONCyT, PICT 2016-0187, PICT 2017-631, PICT 2017-0224), Consejo Nacional de Investigaciones Científicas y Tecnológicas de la República Argentina (CONICET) (PIP 2014, PIP 2017), Secretaría de Ciencia y Tecnología de la Universidad Nacional de Córdoba (SeCyT-UNC, Consolidar 2018-2022), and Secretaría de Ciencia y Tecnología de la Universidad Nacional del Sur (PGI-UNS 24B292).

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  1. CIQUIBIC-CONICET, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Córdoba, 5000, Argentina

    Mario E. Guido, Natalia M. Monjes & Paula M. Wagner

  2. Departamento de Química Biológica “Ranwel Caputto”, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Córdoba, 5000, Argentina

    Mario E. Guido, Natalia M. Monjes & Paula M. Wagner

  3. INIBIBB-UNS-CONICET, Departamento de Biología, Bioquímica y Farmacia, UNS, Bahía Blanca, Argentina

    Gabriela A. Salvador

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  4. Gabriela A. Salvador
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All authors (MEG, NMM, PMW, and GAS) contributed to the first draft of the manuscript, performed the literature search and data analysis, and critically revised the work. The illustrations were made by PMW and NMM and final edition by NMM. The Table 1 was made by PMW. The last version was revised by MEG, and all authors commented on previous versions of the manuscript and read and approved the final version.

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Correspondence to Mario E. Guido.

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Natalia M. Monjes and Paula M. Wagner contributed equally to this work.

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Guido, M.E., Monjes, N.M., Wagner, P.M. et al. Circadian Regulation and Clock-Controlled Mechanisms of Glycerophospholipid Metabolism from Neuronal Cells and Tissues to Fibroblasts. Mol Neurobiol 59, 326–353 (2022). https://doi.org/10.1007/s12035-021-02595-4

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