Eye development and photoreceptor differentiation in the cephalopod <i>Doryteuthis pealeii</i>

Koenig, Kristen M.; Sun, Peter D.; Meyer, Eli; Gross, Jeffrey M.

doi:10.1242/dev.134254

Cited by 31 publications

(79 citation statements)

References 111 publications

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“…This enrichment of repressive chromatin through long-range chromatin association may be linked to numerous previous observations of overall attenuation of the transcription rate at the conclusion of terminal differentiation in adipogenesis and other differentiation paradigms (Fig. 5E) [45][46][47][48][49]. This ensuing decrease in gene transcription is subtle, relative to the robust induction of cell type-specific genes during differentiation.…”

Section: Discussionsupporting

confidence: 70%

Hierarchical role for transcription factors and chromatin structure in genome organization along adipogenesis

et al. 2017

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The three dimensional folding of mammalian genomes is cell-type specific and difficult to alter suggesting that it is an important component of gene regulation. However, given the multitude of chromatin associating factors, the mechanisms driving the co-localization of active chromosomal domains and the role of this organization in regulating the transcription program in adipocytes are not clear. Analysis of genome-wide chromosomal associations revealed cell type-specific spatial clustering of adipogenic genes in 3T3-L1 cells. Time course analysis demonstrated that the adipogenic "hub", sampled by PPARγ and Lpin1, undergoes orchestrated reorganization during adipogenesis. Coupling the dynamics of genome architecture with multiple chromatin datasets indicated that among all the transcription factors tested, RXR is central to genome reorganization at the beginning of adipogenesis. Interestingly, at the end of differentiation, the adipogenic hub was shifted to an H3K27me3 repressive environment in conjunction with attenuation of gene transcription. We propose a stage-specific hierarchy for the activity of transcription factors contributing to the establishment of an adipogenic genome architecture that brings together the adipogenic genetic program. In addition, the repositioning of this network in a H3K27me3-rich environment at the end of differentiation may contribute to the stabilization of gene transcription levels and reduce the developmental plasticity of these specialized cells.

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Section: Discussionsupporting

confidence: 70%

Hierarchical role for transcription factors and chromatin structure in genome organization along adipogenesis

et al. 2017

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“…The two segments are limited by a basement membrane. The development of the eye has been described in Sepiella japonica , in Sepioteuthis australis , in Loligo vulgaris , and recently in Doryteuthis pealeii (Marthy, 1973 ; Yamamoto, 1985 ; Bozzano et al, 2009 ; Koenig et al, 2016 ). The iris and cornea derive from two layers (respectively inner and outer) of ectodermal and mesodermal tissues growing around the optic vesicle (Lemaire and Richard, 1978 ; Tomarev et al, 1997 ); the circular lens is produced by lentigenic cells (West et al, 1995 ), and the retina, is formed during invagination of the primary optic vesicle (Lemaire, 1971 ; Lemaire and Richard, 1978 ).…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, it has been shown that pax6 is an upstream regulator in the RDGN in Drosophila (Czerny et al, 1999 ). Besides this network, otx (Orthodenticle homeobox 2) and Notch play a key role in photoreceptor cell differentiation and retinal organization (for review see Boyl et al, 2001 ; Buresi et al, 2012 ; Koenig et al, 2016 ). In fine , photoreception is allowed by the presence of pigments of the opsin family, present in all groups whatever the structure of the photoreceptor cells (Gehring, 2002 ).…”

Section: Introductionmentioning

confidence: 99%

“…The development of the cephalopod eye is investigated in numerous molecular and genomic studies (Tomarev et al, 1997 ; Hartmann et al, 2003 ; Bozzano et al, 2009 ; Ogura et al, 2013 ; Peyer et al, 2014 ; Yoshida et al, 2014 ; Koenig et al, 2016 ). To complete the behavioral approaches and to understand mechanisms of eye maturation and visual function appearance, we have chosen to explore the molecular pathways underlying the developmental processes in an evolutionary perspective in S. officinalis.…”

Section: Introductionmentioning

confidence: 99%

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Eye Development in Sepia officinalis Embryo: What the Uncommon Gene Expression Profiles Tell Us about Eye Evolution

et al. 2017

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In metazoans, there is a remarkable diversity of photosensitive structures; their shapes, physiology, optical properties, and development are different. To approach the evolution of photosensitive structures and visual function, cephalopods are particularly interesting organisms due to their most highly centralized nervous system and their camerular eyes which constitute a convergence with those of vertebrates. The eye morphogenesis in numerous metazoans is controlled mainly by a conserved Retinal Determination Gene Network (RDGN) including pax, six, eya, and dac playing also key developmental roles in non-retinal structures and tissues of vertebrates and Drosophila. Here we have identified and explored the role of Sof-dac, Sof-six1/2, Sof-eya in eye morphogenesis, and nervous structures controlling the visual function in Sepia officinalis. We compare that with the already shown expressions in eye development of Sof-otx and Sof-pax genes. Rhodopsin is the pigment responsible for light sensitivity in metazoan, which correlate to correlate visual function and eye development. We studied Sof-rhodopsin expression during retina differentiation. By in situ hybridization, we show that (1) all of the RDGN genes, including Sof-pax6, are expressed in the eye area during the early developmental stages but they are not expressed in the retina, unlike Sof-otx, which could have a role in retina differentiation; (2) Sof-rhodopsin is expressed in the retina just before vision gets functional, from stage 23 to hatching. Our results evidence a role of Sof-six1/2, Sof-eya, and Sof-dac in eye development. However, the gene network involved in the retinal photoreceptor differentiation remains to be determined. Moreover, for the first time, Sof-rhodopsin expression is shown in the embryonic retina of cuttlefish suggesting the evolutionary conservation of the role of rhodopsin in visual phototransduction within metazoans. These findings are correlated with the physiological and behavioral observations suggesting that S. officinalis is able to react to light stimuli from stage 25 of organogenesis on, as soon as the first retinal pigments appear.

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“…Additionally, their adaptation to a wide range of marine environments is associated with a suite of morphological novelties that have evolved across the subclass such as light and adhesive organs, accessory nidamental glands, sucker ring teeth, toxin producing salivary glands, among others ( Figure ). Cephalopods have thus been the target of several research areas such as behavioral biology, phylogeography, development, neurobiology, and, more recently, genomics . They provide a fruitful, yet almost entirely unexplored model system to study the role of genomic innovations shaping morphology, development, and behavior.…”

Section: Introductionmentioning

confidence: 99%

Coupled Genomic Evolutionary Histories as Signatures of Organismal Innovations in Cephalopods

et al. 2019

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How genomic innovation translates into organismal organization remains largely unanswered. Possessing the largest invertebrate nervous system, in conjunction with many species-specific organs, coleoid cephalopods (octopuses, squids, cuttlefishes) provide exciting model systems to investigate how organismal novelties evolve. However, dissecting these processes requires novel approaches that enable deeper interrogation of genome evolution. Here, the existence of specific sets of genomic co-evolutionary signatures between expanded gene families, genome reorganization, and novel genes is posited. It is reasoned that their co-evolution has contributed to the complex organization of cephalopod nervous systems and the emergence of ecologically unique organs. In the course of reviewing this field, how the first cephalopod genomic studies have begun to shed light on the molecular underpinnings of morphological novelty is illustrated and their impact on directing future research is described. It is argued that the application and evolutionary profiling of evolutionary signatures from these studies will help identify and dissect the organismal principles of cephalopod innovations. By providing specific examples, the implications of this approach both within and beyond cephalopod biology are discussed.

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Eye development and photoreceptor differentiation in the cephalopod Doryteuthis pealeii

Cited by 31 publications

References 111 publications

Hierarchical role for transcription factors and chromatin structure in genome organization along adipogenesis

Hierarchical role for transcription factors and chromatin structure in genome organization along adipogenesis

Eye Development in Sepia officinalis Embryo: What the Uncommon Gene Expression Profiles Tell Us about Eye Evolution

Coupled Genomic Evolutionary Histories as Signatures of Organismal Innovations in Cephalopods

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