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Journal ArticleDOI

Evolution of photosensory pineal organs in new light: the fate of neuroendocrine photoreceptors

29 Oct 2003-Philosophical Transactions of the Royal Society B (The Royal Society)-Vol. 358, Iss: 1438, pp 1679-1700
TL;DR: A new hypothesis of pineal evolution is proposed, in which the old notion 'gradual regression within the sensory cell line' should be replaced with 'changes in fate restriction within the neural lineage of the pineal field'.
Abstract: Pineal evolution is envisaged as a gradual transformation of pinealocytes (a gradual regression of pinealocyte sensory capacity within a particular cell line), the so-called sensory cell line of the pineal organ. In most non-mammals the pineal organ is a directly photosensory organ, while the pineal organ of mammals (epiphysis cerebri) is a non-sensory neuroendocrine organ under photoperiod control. The phylogenetic transformation of the pineal organ is reflected in the morphology and physiology of the main parenchymal cell type, the pinealocyte. In anamniotes, pinealocytes with retinal cone photoreceptor-like characteristics predominate, whereas in sauropsids so-called rudimentary photoreceptors predominate. These have well-developed secretory characteristics, and have been interpreted as intermediaries between the anamniote pineal photoreceptors and the mammalian non-sensory pinealocytes. We have re-examined the original studies on which the gradual transformation hypothesis of pineal evolution is based, and found that the evidence for this model of pineal evolution is ambiguous. In the light of recent advances in the understanding of neural development mechanisms, we propose a new hypothesis of pineal evolution, in which the old notion 'gradual regression within the sensory cell line' should be replaced with 'changes in fate restriction within the neural lineage of the pineal field'.

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Citations
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Journal ArticleDOI
TL;DR: A wide range of findings are reviewed that capture glimpses of the gradations that appear to have occurred during eye evolution, and a scenario for the unseen steps that have led to the emergence of the vertebrate eye is provided.
Abstract: Charles Darwin appreciated the conceptual difficulty in accepting that an organ as wonderful as the vertebrate eye could have evolved through natural selection. He reasoned that if appropriate gradations could be found that were useful to the animal and were inherited, then the apparent difficulty would be overcome. Here, we review a wide range of findings that capture glimpses of the gradations that appear to have occurred during eye evolution, and provide a scenario for the unseen steps that have led to the emergence of the vertebrate eye.

441 citations

Journal ArticleDOI
TL;DR: How manipulation of the photic cues impact on fish circannual clock and annual cycle of reproduction, and how this can be used for aquaculture purposes is discussed.

386 citations

Journal ArticleDOI
TL;DR: A remnant silhouette of premortem dynamics within the hormone’s biosynthesis pathway can be constructed and protein‐protein interactions and nucleo‐cytoplasmic protein shuttling indicate furthermore a novel twist in the molecular dynamics in the cells of this neuroendocrine brain structure.
Abstract: The human pineal gland is a neuroendocrine transducer that forms an integral part of the brain. Through the nocturnally elevated synthesis and release of the neurohormone melatonin, the pineal gland encodes and disseminates information on circadian time, thus coupling the outside world to the biochemical and physiological internal demands of the body. Approaches to better understand molecular details behind the rhythmic signalling in the human pineal gland are limited but implicitly warranted, as human chronobiological dysfunctions are often associated with alterations in melatonin synthesis. Current knowledge on melatonin synthesis in the human pineal gland is based on minimally invasive analyses, and by the comparison of signalling events between different vertebrate species, with emphasis put on data acquired in sheep and other primates. Together with investigations using autoptic pineal tissue, a remnant silhouette of premortem dynamics within the hormone's biosynthesis pathway can be constructed. The detected biochemical scenario behind the generation of dynamics in melatonin synthesis positions the human pineal gland surprisingly isolated. In this neuroendocrine brain structure, protein-protein interactions and nucleo-cytoplasmic protein shuttling indicate furthermore a novel twist in the molecular dynamics in the cells of this neuroendocrine brain structure. These findings have to be seen in the light that an impaired melatonin synthesis is observed in elderly and/or demented patients, in individuals affected by Alzheimer's disease, Smith-Magenis syndrome, autism spectrum disorder and sleep phase disorders. Already, recent advances in understanding signalling dynamics in the human pineal gland have significantly helped to counteract chronobiological dysfunctions through a proper restoration of the nocturnal melatonin surge.

354 citations


Cites background from "Evolution of photosensory pineal or..."

  • ...Owing to a developmental re-programming [8, 62], lateral eyes function as inputs for the discrimination of shape and colour of objects....

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  • ...This is not surprising from a phylogenetic standpoint, as the eyes share their diencephalic origin with the pineal gland [8, 62]....

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  • ...In anamniotes, like fish and amphibians, pinealocytes with retinal cone photoreceptor-like properties predominate, while in sauropsids, like reptiles and birds, photoreceptor properties are reduced [62]....

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Journal ArticleDOI
TL;DR: Evidence is reviewed from a wide range of studies relevant to the evolution of vertebrate photoreceptors and phototransduction, in order to permit the synthesis of a scenario for the major steps that occurred during the Evolution of cones, rods and the vertebrate retina.

316 citations


Cites background from "Evolution of photosensory pineal or..."

  • ...The following description for Eptatretus species is based largely on the reports of Holmberg (1971, 1977), Fernholm and Holmberg (1975) and Locket and Jorgensen (1998)....

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  • ...The following description for Eptatretus species is based largely on the reports of Holmberg (1971, 1977), Fernholm and Holmberg (1975) and Locket and Jorgensen (1998). General features of the hagfish eye....

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Journal ArticleDOI
TL;DR: This review aims to bring together the current knowledge on the photic control of reproduction mainly focusing on seasonal temperate fish species and shape the current working hypotheses supported by recent findings obtained in teleosts or based on knowledge gathered in mammalian and avian species.
Abstract: Seasonality is an important adaptive trait in temperate fish species as it entrains or regulates most physiological events such as reproductive cycle, growth profile, locomotor activity and key life-stage transitions. Photoperiod is undoubtedly one of the most predictable environmental signals that can be used by most living organisms including fishes in temperate areas. This said, however, understanding of how such a simple signal can dictate the time of gonadal recruitment and spawning, for example, is a complex task. Over the past few decades, many scientists attempted to unravel the roots of photoperiodic signalling in teleosts by investigating the role of melatonin in reproduction, but without great success. In fact, the hormone melatonin is recognized as the biological time-keeping hormone in fishes mainly due to the fact that it reflects the seasonal variation in daylength across the whole animal kingdom rather than the existence of direct evidences of its role in the entrainment of reproduction in fishes. Recently, however, some new studies clearly suggested that melatonin interacts with the reproductive cascade at a number of key steps such as through the dopaminergic system in the brain or the synchronization of the final oocyte maturation in the gonad. Interestingly, in the past few years, additional pathways have become apparent in the search for a fish photoneuroendocrine system including the clock-gene network and kisspeptin signalling and although research on these topics are still in their infancy, it is moving at great pace. This review thus aims to bring together the current knowledge on the photic control of reproduction mainly focusing on seasonal temperate fish species and shape the current working hypotheses supported by recent findings obtained in teleosts or based on knowledge gathered in mammalian and avian species. Four of the main potential regulatory systems (light perception, melatonin, clock genes and kisspeptin) in fish reproduction are reviewed.

248 citations

References
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Journal ArticleDOI
25 Feb 2000-Science
TL;DR: Before the full potential of neural stem cells can be realized, the authors need to learn what controls their proliferation, as well as the various pathways of differentiation available to their daughter cells.
Abstract: Neural stem cells exist not only in the developing mammalian nervous system but also in the adult nervous system of all mammalian organisms, including humans. Neural stem cells can also be derived from more primitive embryonic stem cells. The location of the adult stem cells and the brain regions to which their progeny migrate in order to differentiate remain unresolved, although the number of viable locations is limited in the adult. The mechanisms that regulate endogenous stem cells are poorly understood. Potential uses of stem cells in repair include transplantation to repair missing cells and the activation of endogenous cells to provide "self-repair. " Before the full potential of neural stem cells can be realized, we need to learn what controls their proliferation, as well as the various pathways of differentiation available to their daughter cells.

4,608 citations

Journal ArticleDOI
08 Feb 2002-Science
TL;DR: It is shown that retinal ganglion cells innervating the SCN are intrinsically photosensitive, and depolarized in response to light even when all synaptic input from rods and cones was blocked.
Abstract: Light synchronizes mammalian circadian rhythms with environmental time by modulating retinal input to the circadian pacemaker-the suprachiasmatic nucleus (SCN) of the hypothalamus. Such photic entrainment requires neither rods nor cones, the only known retinal photoreceptors. Here, we show that retinal ganglion cells innervating the SCN are intrinsically photosensitive. Unlike other ganglion cells, they depolarized in response to light even when all synaptic input from rods and cones was blocked. The sensitivity, spectral tuning, and slow kinetics of this light response matched those of the photic entrainment mechanism, suggesting that these ganglion cells may be the primary photoreceptors for this system.

3,052 citations

Journal ArticleDOI
08 Feb 2002-Science
TL;DR: It is shown that melanopsin is present in cell bodies, dendrites, and proximal axonal segments of a subset of rat RGCs, most likely the visual pigment of phototransducing R GCs that set the circadian clock and initiate other non–image-forming visual functions.
Abstract: The primary circadian pacemaker, in the suprachiasmatic nucleus (SCN) of the mammalian brain, is photoentrained by light signals from the eyes through the retinohypothalamic tract. Retinal rod and cone cells are not required for photoentrainment. Recent evidence suggests that the entraining photoreceptors are retinal ganglion cells (RGCs) that project to the SCN. The visual pigment for this photoreceptor may be melanopsin, an opsin-like protein whose coding messenger RNA is found in a subset of mammalian RGCs. By cloning rat melanopsin and generating specific antibodies, we show that melanopsin is present in cell bodies, dendrites, and proximal axonal segments of a subset of rat RGCs. In mice heterozygous for tau-lacZ targeted to the melanopsin gene locus, beta-galactosidase-positive RGC axons projected to the SCN and other brain nuclei involved in circadian photoentrainment or the pupillary light reflex. Rat RGCs that exhibited intrinsic photosensitivity invariably expressed melanopsin. Hence, melanopsin is most likely the visual pigment of phototransducing RGCs that set the circadian clock and initiate other non-image-forming visual functions.

2,359 citations