Cryptochromes in mammals: a magnetoreception misconception?

Zhang, Li; Malkemper, E. Pascal

doi:10.3389/fphys.2023.1250798

Cited by 6 publications

(6 citation statements)

References 129 publications

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“…Xu et al, 2012;Xu et al, 2014;Agliassa et al, 2018). Evidence for cryptochrome mediated physiological responses to applied magnetic fields in plant, Drosophila, as well as in mammalian cell systems has been recently summarized in this Review Series (Kyriacou and Rosato, 2022;Zhang and Malkemper, 2023;Thoradit et al, 2023) although areas of controversy exists in all of these cases (see eg. Bassetto et al, 2023).…”

Section: The Cryptochrome Photocycle and Response To Applied Magnetic...mentioning

confidence: 99%

‘Seeing’ the electromagnetic spectrum: spotlight on the cryptochrome photocycle

Aguida,

Babo,

Baouz

et al. 2024

Front. Plant Sci.

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Cryptochromes are widely dispersed flavoprotein photoreceptors that regulate numerous developmental responses to light in plants, as well as to stress and entrainment of the circadian clock in animals and humans. All cryptochromes are closely related to an ancient family of light-absorbing flavoenzymes known as photolyases, which use light as an energy source for DNA repair but themselves have no light sensing role. Here we review the means by which plant cryptochromes acquired a light sensing function. This transition involved subtle changes within the flavin binding pocket which gave rise to a visual photocycle consisting of light-inducible and dark-reversible flavin redox state transitions. In this photocycle, light first triggers flavin reduction from an initial dark-adapted resting state (FADox). The reduced state is the biologically active or ‘lit’ state, correlating with biological activity. Subsequently, the photoreduced flavin reoxidises back to the dark adapted or ‘resting’ state. Because the rate of reoxidation determines the lifetime of the signaling state, it significantly modulates biological activity. As a consequence of this redox photocycle Crys respond to both the wavelength and the intensity of light, but are in addition regulated by factors such as temperature, oxygen concentration, and cellular metabolites that alter rates of flavin reoxidation even independently of light. Mechanistically, flavin reduction is correlated with conformational change in the protein, which is thought to mediate biological activity through interaction with biological signaling partners. In addition, a second, entirely independent signaling mechanism arises from the cryptochrome photocycle in the form of reactive oxygen species (ROS). These are synthesized during flavin reoxidation, are known mediators of biotic and abiotic stress responses, and have been linked to Cry biological activity in plants and animals. Additional special properties arising from the cryptochrome photocycle include responsivity to electromagnetic fields and their applications in optogenetics. Finally, innovations in methodology such as the use of Nitrogen Vacancy (NV) diamond centers to follow cryptochrome magnetic field sensitivity in vivo are discussed, as well as the potential for a whole new technology of ‘magneto-genetics’ for future applications in synthetic biology and medicine.

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Section: The Cryptochrome Photocycle and Response To Applied Magnetic...mentioning

confidence: 99%

‘Seeing’ the electromagnetic spectrum: spotlight on the cryptochrome photocycle

Aguida,

Babo,

Baouz

et al. 2024

Front. Plant Sci.

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“…Light can also act via the pineal gland, however, to shut down melatonin secretion and aggregate pigment granules [33,34]. Evolutionary analysis suggests that three Crys should be expressed in the amphibian Xenopus laevis: Cry1, Cry2 and Cry4 [30,31]. Here we explore how light coordinates the direct and indirect regulation of pigment synthesis/movement and pigment cell proliferation, and whether light-sensitive Crys participate.…”

Section: Introductionmentioning

confidence: 99%

“…Crys are divided in three groups: i) The type I or the drosophila type Cry (dCry); ii) the type II CRYs (CRY1 and CRY2) found in mammals; and iii) the type IV Cry (Cry4) present in several lineages of Chordata, including fish, amphibians and certain sauropsids [30,31]. The mammalian type II CRYs lack photosensitivity and evolved as light-independent transcription factors that regulate core clock gene expression.…”

Section: Introductionmentioning

confidence: 99%

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Interplay of Light, Melatonin, and Circadian Genes in Skin Pigmentation Regulation

Bertolesi,

Debnath,

Heshami

et al. 2024

Preprint

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Circadian regulation of skin pigmentation is essential for thermoregulation, UV protection, and synchronization of skin cell renewal. This regulation involves both cell-autonomous photic responses and non-cell-autonomous hormonal control, particularly through melatonin produced in a light-sensitive manner. Photosensitive opsins, cryptochromes, and melatonin regulate circadian rhythms in skin pigment cells. We studied light/dark cycles and melatonin coordination in melanin synthesis and cell proliferation of Xenopus laevis melanophores. In vivo, tadpole pigmentation shows robust circadian regulation mainly hormone-driven, in that isolated melanophores respond strongly to melatonin but only slightly to light. Melanophore proliferation is faster in the dark and slower with melatonin compared to a 12/12 light/dark cycle. Expression of circadian core genes (clock, bmal1, per1, per2, per3, cry1, cry2, and cry4) in melatonin-treated cells during the light phase mimics dark phase expression. Individual Cry overexpression did not affect melanisation or cell proliferation, likely due to functional redundancy. Melanin synthesis was inhibited by circadian cycle deregulation through: a) pharmacological inhibition of Cry1 and Cry2 degradation with KL001, b) continuous light or dark conditions, and c) melatonin treatment. Our findings suggest that circadian cycle regulation, rather than proliferative capacity, alters melanisation of melanophores.

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“…[31] The majority of research into the role of RPs in magnetoreception has focused on birds. The RP mechanism could, however, be the same in other animals with magnetic orientation capabilities, as the expression of magneto-sensitive cryptochrome has been shown to occur in the retina of mammals, including humans, [32] although not in insects such as flies. [33] The capacity for magnetic orientation has also been shown to reside in the eyes of different mammals.…”

Section: Introductionmentioning

confidence: 99%

Isotope effects on radical pair performance in cryptochrome: A new hypothesis for the evolution of animal migration

Galván,

Hassasfar,

Adams

et al. 2023

BioEssays

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Mechanisms occurring at the atomic level are now known to drive processes essential for life, as revealed by quantum effects on biochemical reactions. Some macroscopic characteristics of organisms may thus show an atomic imprint, which may be transferred across organisms and affect their evolution. This possibility is considered here for the first time, with the aim of elucidating the appearance of an animal innovation with an unclear evolutionary origin: migratory behaviour. This trait may be mediated by a radical pair (RP) mechanism in the retinal flavoprotein cryptochrome, providing essential magnetic orientation for migration. Isotopes may affect the performance of quantum processes through their nuclear spin. Here, we consider a simple model and then apply the standard open quantum system approach to the spin dynamics of cryptochrome RP. We changed the spin quantum number (I) and g‐factor of hydrogen and nitrogen isotopes to investigate their effect on RP's yield and magnetic sensitivity. Strong differences arose between isotopes with I = 1 and I = 1/2 in their contribution to cryptochrome magnetic sensitivity, particularly regarding Earth's magnetic field strengths (25–65 µT). In most cases, isotopic substitution improved RP's magnetic sensitivity. Migratory behaviour may thus have been favoured in animals with certain isotopic compositions of cryptochrome.

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Cryptochromes in mammals: a magnetoreception misconception?

Cited by 6 publications

References 129 publications

‘Seeing’ the electromagnetic spectrum: spotlight on the cryptochrome photocycle

‘Seeing’ the electromagnetic spectrum: spotlight on the cryptochrome photocycle

Interplay of Light, Melatonin, and Circadian Genes in Skin Pigmentation Regulation

Isotope effects on radical pair performance in cryptochrome: A new hypothesis for the evolution of animal migration

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