Adaptive cell invasion maintains lateral line organ homeostasis in response to environmental changes

Peloggia, Julia; Münch, Daniela; Meneses-Giles, Paloma; Romero‐Carvajal, Andrés; Lush, Mark E.; Lawson, Nathan D.; McClain, Melainia; Pan, Y. Albert; Piotrowski, Tatjana

doi:10.1016/j.devcel.2021.03.027

Cited by 27 publications

(27 citation statements)

References 115 publications

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“…Our analyses have focused on scales and pigmentation, however, zebrafish skin is a fruitful study system for many areas of biology including regeneration and wound healing (Richardson et al, 2016; Cox et al, 2018; Iwasaki et al, 2018; Morris et al, 2018; Pfalzgraff et al, 2018); innate immunity (Lü et al, 2015; Wurster et al, 2021), stem cell regulation (Lee et al, 2014; Chen et al, 2016; Brock et al, 2019), sensory physiology and developmental neuroscience (Rasmussen et al, 2015; Rasmussen et al, 2018; Peloggia et al, 2021), and human disease modeling (Feitosa et al, 2011; Li et al, 2011). Additionally, considerable insight into general mechanisms of development can emerge from comparing developmental mechanisms across species or between organ system.…”

Section: Discussionmentioning

confidence: 99%

Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin

Aman

Saunders

Carr³

et al. 2021

Preprint

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Regulation of neural crest derived pigment cells and dermal cells that form skin appendages is broadly similar across vertebrate taxa. In zebrafish, organized pigment stripes and an array of calcified scales form simultaneously in the skin during post-embryonic development. Understanding mechanisms that regulate stripe patterning and dermal morphogenesis may lead to discovery of fundamental mechanisms that govern development of animal form. To learn about cell types and potential signaling interactions that govern skin patterning and morphogenesis we generated and analyzed single cell transcriptomes of skin with genetic or induced defects in pigmentation and squamation. These data reveal a previously undescribed population of ameloblast-like epidermal cells, suggest hormonal control of epithelial-mesenchymal signaling, clarify the signaling network that governs scale papillae development, and identify the hypodermis as a crucial pigment cell support environment. These analyses provide new insights into the development of skin and pigmentation and highlight the utility of zebrafish for uncovering essential features of post-embryonic development in vertebrates.

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Section: Discussionmentioning

confidence: 99%

Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin

Aman

Saunders

Carr³

et al. 2021

Preprint

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“…Moreover, we identified a small cluster with specific expression of krt5 and many other epithelial cells markers. We also included this cluster in the downstream analyses as we ruled out the possibility of skin cell ( tp63 and krtt1c19e ) and gallbladder cell ( sstr5 ) contamination ( 51 ). To extrapolate the detailed cell embeddings of pancreatic duct and endocrine cells, we manually subselected cells belonging to the endocrine, pancreatic duct, and krt5 + cell clusters (~10,000 cells) and re-ran the analytical pipeline (Fig.…”

Section: Resultsmentioning

confidence: 99%

Decoding pancreatic endocrine cell differentiation and β cell regeneration in zebrafish

Mi,

Liu,

Andersson

2023

Sci. Adv.

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In contrast to mice, zebrafish have an exceptional yet elusive ability to replenish lost β cells in adulthood. Understanding this framework would provide mechanistic insights for β cell regeneration, which may be extrapolated to humans. Here, we characterize a krt4 -expressing ductal cell type, which is distinct from the putative Notch-responsive cells, showing neogenic competence and giving rise to the majority of endocrine cells during postembryonic development. Furthermore, we demonstrate a marked ductal remodeling process featuring a Notch-responsive to krt4 + luminal duct transformation during late development, indicating several origins of krt4 + ductal cells displaying similar transcriptional patterns. Single-cell transcriptomics upon a series of time points during β cell regeneration unveil a previously unrecognized dlb + transitional endocrine precursor cell, distinct regulons, and a differentiation trajectory involving cellular shuffling through differentiation and dedifferentiation dynamics. These results establish a model of zebrafish pancreatic endocrinogenesis and highlight key values of zebrafish for translational studies of β cell regeneration.

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“…We previously showed that decreased salinity and pH lead to the adaptive differentiation of basal stem cells into a pair of Nm ionocytes, which invade lateral line neuromasts 18 . How zebrafish detect environmental changes and activate this adaptive response is still unknown.…”

Section: Identification Of Nm Ionocyte Progenitorsmentioning

confidence: 99%

Environmental and molecular control of tissue-specific ionocyte differentiation in zebrafish

Peloggia,

Lush,

Tsai

et al. 2024

Preprint

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Organisms adjust their physiology to cope with environmental fluctuations and maintain fitness. These adaptations occur via genetic changes over multiple generations or through acclimation, a set of reversible phenotypic changes that confer resilience to the individual. Aquatic organisms are subject to dramatic seasonal fluctuations in water salinity, which can affect the function of lateral line mechanosensory hair cells. To maintain hair cell function when salinity decreases, ion-regulating cells, Neuromast-associated ionocytes (Nm ionocytes), increase in number and invade lateral line neuromasts. How environmental changes trigger this adaptive differentiation of Nm ionocytes and how these cells are specified is still unknown. Here, we identify Nm ionocyte progenitors as foxi3a/foxi3b-expressing skin cells and show that their differentiation is associated with sequential activation of different Notch pathway components, which control ionocyte survival. We demonstrate that new Nm ionocytes are rapidly specified by absolute salinity levels, independently of stress response pathways. We further show that Nm ionocyte differentiation is selectively triggered by depletion of specific ions, such as Ca2+ and Na+/Cl-, but not by low K+ levels, and is independent of media osmolarity. Finally, we demonstrate that hair cell activity plays a role in Nm ionocyte recruitment and that systemic factors are not necessary for Nm ionocyte induction. In summary, we have identified how environmental changes activate a signaling cascade that triggers basal skin cell progenitors to differentiate into Nm ionocytes and invade lateral line organs. This adaptive behavior is an example of physiological plasticity that may prove essential for survival in changing climates.

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Adaptive cell invasion maintains lateral line organ homeostasis in response to environmental changes

Cited by 27 publications

References 115 publications

Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin

Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin

Decoding pancreatic endocrine cell differentiation and β cell regeneration in zebrafish

Environmental and molecular control of tissue-specific ionocyte differentiation in zebrafish

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