The Dual Functional Reflecting Iris of the Zebrafish

Gur, Dvir; Nicolas, Jan-David; Brumfeld, Vlad; Bar-Elli, Omri; Oron, Dan; Levkowitz, Gil

doi:10.1002/advs.201800338

Cited by 40 publications

(44 citation statements)

References 27 publications

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“…To map the structural organization of iridophores across the entire skin pattern, we used synchrotron-based micro X-ray diffraction, which allows large areas to be scanned while still providing information on orientations and anisotropy of crystal arrays at the level of a single cell. In this system, high angular distribution diffractions having a full-ring signal are indicative of crystal orientations that vary (i.e., disordered), whereas low angular distribution diffractions having a punctuated-ring signal are indicative of crystals that are consistently oriented (i.e., ordered ) 15 . Dorso-ventral line scanning across the flank of the fish demonstrated there were consistent differences in structural organization of stripe vs. interstripe regions ( Fig.…”

Section: Resultsmentioning

confidence: 99%

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In situdifferentiation of iridophore crystallotypes underlies zebrafish stripe patterning

Gur

Bain

Johnson

et al. 2020

Preprint

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22Skin color patterns are ubiquitous in nature, evolve rapidly, and impact social 23 behavior 1 , predator avoidance 2 , and protection from ultraviolet irradiation 3 . A 24 leading model system for vertebrate skin patterning is the zebrafish 4-7 ; its 25 alternating blue stripes and yellow interstripes depend on guanine crystal-26 containing cells called iridophores that reflect light. It was suggested that the 27 zebrafish's alternating color pattern arises from a single type of iridophore 28 migrating differentially to stripes and interstripes 7-9 . When we tracked iridophores, 29 however, we found they did not migrate between stripes and interstripes but 30 instead differentiated and proliferated in place based on their micro-environment. 31RNA seq analysis further revealed stripe and interstripe iridophores had different 32 transcriptomic states, while cryogenic scanning electron microscopy and micro-33 X-ray diffraction showed they had different guanine crystal organizations and 34 responsiveness to norepinephrine, all indicating that stripe and interstripe 35 iridophores are different cell types. Based on these results, we present a new 36 model of skin patterning in zebrafish in which distinct iridophore crystallotypes 37 containing specialized, physiologically responsive, subcellular organelles arise in 38 stripe and interstripe zones by in situ differentiation. In this model, pattern 39 phenotype depends not only on interactions among pigment cells that affect their 40 arrangements, but also on factors that specify subcellular organization and 41 physiological responsiveness of specialized organelles. 42 43 Introduction 1 Biological patterning is ubiquitous in nature, but mechanisms underlying its 2 establishment and maintenance have been well-documented in only a few instances that 3 are unlikely to represent the full spectrum of pattern-forming systems 6,10 . Indeed, 4 patterning can arise in response to graded positional information or by self-organization 5 of interacting cells, and it can require alternative specification of cell-types from a 6 common progenitor or sorting-out of cells that are heterogeneous already. Elucidating 7 the mechanisms required to pattern cells in diverse tissues and organs is fundamental to 8 understanding development and how phenotypes evolve.9The alternating dark (blue) and light (yellow) pigmented stripe pattern of adult 10 zebrafish Danio rerio (Fig. 1a) is a useful model for dissecting patterning 11 mechanisms 4,5,7,11,12 . Cells within the dark stripes include black pigment-containing 12 melanophores; cells in the light stripes (known as "interstripes") include orange-pigment 13 containing xanthophores; and both dark stripes and light interstripes contain specialized 14 cells called iridophores 13,14 . Iridophores are the major players for skin pattern 15 establishment and reiteration in zebrafish. They behave as reflective cells, exhibiting 16 angular-dependent changes in hue-iridescence-owing to membrane-bound reflecting 17 platelets of crystalline guanine 14-16...

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Section: Resultsmentioning

confidence: 99%

“…4a ). Specifically, based on their (012) and (002) diffraction planes 15,35 , crystal plates in iridophores of the stripe zone were well oriented (i.e., ordered) ( Figs. 4a , panels 1 and 3), whereas those in the interstripe zone were non-aligned (i.e., disordered) ( Figs.…”

Section: Resultsmentioning

confidence: 99%

In situdifferentiation of iridophore crystallotypes underlies zebrafish stripe patterning

Gur

Bain

Johnson

et al. 2020

Preprint

Self Cite

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“…S5 A ). Moreover, both cell types lacked the angular-dependent change of hues—iridescence—of iridophores, which results from stacked arrangements of crystalline guanine reflecting platelets within membrane-bound organelles (5, 28, 29) (Fig. 3 A ).…”

Section: Resultsmentioning

confidence: 99%

Fate plasticity and reprogramming in genetically distinct populations of Danio leucophores

Lewis

Saunders

Larson

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Understanding genetic and cellular bases of adult form remains a fundamental goal at the intersection of developmental and evolutionary biology. The skin pigment cells of vertebrates, derived from embryonic neural crest, are a useful system for elucidating mechanisms of fate specification, pattern formation, and how particular phenotypes impact organismal behavior and ecology. In a survey of Danio fishes, including the zebrafish Danio rerio, we identified two populations of white pigment cells—leucophores—one of which arises by transdifferentiation of adult melanophores and another of which develops from a yellow–orange xanthophore or xanthophore-like progenitor. Single-cell transcriptomic, mutational, chemical, and ultrastructural analyses of zebrafish leucophores revealed cell-type–specific chemical compositions, organelle configurations, and genetic requirements. At the organismal level, we identified distinct physiological responses of leucophores during environmental background matching, and we showed that leucophore complement influences behavior. Together, our studies reveal independently arisen pigment cell types and mechanisms of fate acquisition in zebrafish and illustrate how concerted analyses across hierarchical levels can provide insights into phenotypes and their evolution.

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“…For cryo-SEM, adult zebrafish hypophyses were dissected and fixed in 4% PFA and were then submitted to Cryo-SEM imaging as described in (Gur et al, 2018). In short, dissected pituitaries were cryo-immobilized in a high-pressure freezing device (HPM10; Bal-Tec).…”

Section: Image Acquisitionmentioning

confidence: 99%

Fenestrae-associated protein Plvap regulates the rate of blood-borne proteins passage into the hypophysis

Gordon

Blechman

Shimoni

et al. 2019

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To maintain body homeostasis, endocrine systems must detect and integrate a multitude of blood-borne peripheral signals. This is mediated by specialized permeable pores in the endothelial membrane, dubbed fenestrae. Plasmalemma vesicles-associated protein (Plvap) is located in the fenestral diaphragm and is thought play a role in the selective passage of proteins through the fenestrae. However, this suggested function has yet to be demonstrated directly.Here, we studied the development of fenestrated capillaries in a major neuroendocrine interface between the blood and brain, namely the hypophysis. Using a transgenic permeability biosensor to visualize the vascular excretion of a genetically tagged plasma protein (DBP-EGFP), we show that the developmental acquisition of vascular permeability is associated with differential expression of zebrafish plvap orthologs in the hypophysis versus brain.Ultrastructural analysis of the hypophyseal vasculature revealed that plvapb mutants display deficiencies in fenestral and stomatal diaphragms as well as increased density of fenestrae, but not of caveolae. Measurements of DBP-EGFP dynamics in live plvapb mutant larvae provided a direct proof that Plvap limits the rate of blood-borne protein passage through fenestrated endothelia. Overall, we present the regulatory role of Plvap in the development of blood-borne protein detection machinery in a major neuroendocrine interface between the brain and the general circulation.

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The Dual Functional Reflecting Iris of the Zebrafish

Cited by 40 publications

References 27 publications

In situdifferentiation of iridophore crystallotypes underlies zebrafish stripe patterning

In situdifferentiation of iridophore crystallotypes underlies zebrafish stripe patterning

Fate plasticity and reprogramming in genetically distinct populations of Danio leucophores

Fenestrae-associated protein Plvap regulates the rate of blood-borne proteins passage into the hypophysis

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