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Article: Growth patterns of caudal fin rays are informed by both external signals from the regenerating organ and remembered identity autonomous to the local tissue.

Autumn, Melody / Hu, Yinan / Zeng, Jenny / McMenamin, Sarah K

bioRxiv : the preprint server for biology

2024

Abstract: Regenerating tissues must remember or interpret their spatial position, using this information to restore original size and patterning. The external skeleton of the zebrafish caudal fin is composed of 18 rays; after any portion of the fin is amputated, ... ...

Abstract	Regenerating tissues must remember or interpret their spatial position, using this information to restore original size and patterning. The external skeleton of the zebrafish caudal fin is composed of 18 rays; after any portion of the fin is amputated, position-dependent regenerative growth restores each ray to its original length. We tested for transcriptional differences during regeneration of proximal versus distal tissues and identified 489 genes that differed in proximodistal expression. Thyroid hormone directs multiple aspects of ray patterning along the proximodistal axis, and we identified 364 transcripts showing a proximodistal expression pattern that was dependent on thyroid hormone context. To test what aspects of ray positional identity are directed by extrinsic cues versus remembered identity autonomous to the tissue itself, we transplanted distal portions of rays to proximal environments and evaluated regeneration within the new location. While neighboring proximal tissue showed robust expression of
Language	English
Publishing date	2024-03-31
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.29.586899
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Article: Dynamics of the Zebrafish Skeleton in Three Dimensions During Juvenile and Adult Development.

Nguyen, Stacy V / Lanni, Dominic / Xu, Yongqi / Michaelson, James S / McMenamin, Sarah K

Frontiers in physiology

2022 Volume 13, Page(s) 875866

Abstract: Zebrafish are a valuable model for normal vertebrate skeletogenesis and the study of myriad bone disorders. Bones grow, ossify and change shape throughout the zebrafish lifetime, and 3D technologies allow us to examine skeletogenic processes in detail ... ...

Abstract	Zebrafish are a valuable model for normal vertebrate skeletogenesis and the study of myriad bone disorders. Bones grow, ossify and change shape throughout the zebrafish lifetime, and 3D technologies allow us to examine skeletogenic processes in detail through late developmental stages. To facilitate analysis of shape, orientation and tissue density of skeletal elements throughout ontogeny and adulthood, we generated a high-resolution skeletal reference dataset of wild-type zebrafish development. Using microCT technology, we produced 3D models of the skeletons of individuals ranging from 12 to 25 mm standard length (SL). We analyzed the dynamics of skeletal density and volume as they increase during juvenile and adult growth. Our resource allows anatomical comparisons between meristic units within an individual-e.g., we show that the vertebral canal width increases posteriorly along the spine. Further, structures may be compared between individuals at different body sizes: we highlight the shape changes that the lower jaw undergoes as fish mature from juvenile to adult. We show that even reproductively mature adult zebrafish (17-25 mm SL) continue to undergo substantial changes in skeletal morphology and composition with continued adult growth. We provide a segmented model of the adult skull and a series of interactive 3D PDFs at a range of key stages. These resources allow changes in the skeleton to be assessed quantitatively and qualitatively through late stages of development, and can serve as anatomical references for both research and education.
Language	English
Publishing date	2022-05-26
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2564217-0
ISSN	1664-042X
ISSN	1664-042X
DOI	10.3389/fphys.2022.875866
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Article ; Online: Thyroid hormone shapes craniofacial bones during postembryonic zebrafish development.

Keer, Stephanie / Storch, Joshua D / Nguyen, Stacy / Prado, Mia / Singh, Rajendra / Hernandez, Luz Patricia / McMenamin, Sarah K

Evolution & development

2022 Volume 24, Issue 1-2, Page(s) 61–76

Abstract: Changing the shape of craniofacial bones can profoundly alter ecological function, and understanding how developmental conditions sculpt skeletal phenotypes can provide insight into evolutionary adaptations. Thyroid hormone (TH) stimulates metamorphosis ... ...

Abstract	Changing the shape of craniofacial bones can profoundly alter ecological function, and understanding how developmental conditions sculpt skeletal phenotypes can provide insight into evolutionary adaptations. Thyroid hormone (TH) stimulates metamorphosis and regulates skeletal morphogenesis across vertebrates. To assess the roles of this hormone in sculpting the craniofacial skeleton of a non-metamorphic vertebrate, we tested zebrafish for developmental periods of TH-induced craniofacial shape change. We analyzed shapes of specific bones that function in prey detection, capture and processing. We quantified these elements from late-larval through adult stages under three developmental TH profiles. Under wild-type conditions, each bone progressively grows allometrically into a mature morphology over the course of postembryonic development. In three of the four bones, TH was required to sculpt an adult shape: hypothyroidism inhibited aspects of shape change, and allowed some components of immature shape to be retained into adulthood. Excess developmental TH stimulated aspects of precocious shape change leading to abnormal morphologies in some bones. Skeletal features with functional importance showed high sensitivities to TH, including the transformator process of the tripus, the mandibular symphysis of the lower jaw, the scutiform lamina of the hyomandibula, and the anterior arm of the pharyngeal jaw. In all, we found that TH is necessary for shaping mature morphology of several essential skeletal elements; this requirement is particularly pronounced during larval development. Altered TH titer leads to abnormal morphologies with likely functional consequences, highlighting the potential of TH and downstream pathways as targets for evolutionary change.
MeSH term(s)	Animals ; Bone and Bones ; Jaw/physiology ; Larva/metabolism ; Thyroid Hormones/metabolism ; Zebrafish
Chemical Substances	Thyroid Hormones
Language	English
Publishing date	2022-03-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2020288-X
ISSN	1525-142X ; 1520-541X
ISSN (online)	1525-142X
ISSN	1520-541X
DOI	10.1111/ede.12399
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Article ; Online: Thyroid hormone regulates proximodistal patterning in fin rays.

Harper, Melody / Hu, Yinan / Donahue, Joan / Acosta, Benjamin / Dievenich Braes, Flora / Nguyen, Stacy / Zeng, Jenny / Barbaro, Julianna / Lee, Hyungwoo / Bui, Hoa / McMenamin, Sarah K

Proceedings of the National Academy of Sciences of the United States of America

2023 Volume 120, Issue 21, Page(s) e2219770120

Abstract: Processes that regulate size and patterning along an axis must be highly integrated to generate robust shapes; relative changes in these processes underlie both congenital disease and evolutionary change. Fin length mutants in zebrafish have provided ... ...

Abstract	Processes that regulate size and patterning along an axis must be highly integrated to generate robust shapes; relative changes in these processes underlie both congenital disease and evolutionary change. Fin length mutants in zebrafish have provided considerable insight into the pathways regulating fin size, yet signals underlying patterning have remained less clear. The bony rays of the fins possess distinct patterning along the proximodistal axis, reflected in the location of ray bifurcations and the lengths of ray segments, which show progressive shortening along the axis. Here, we show that thyroid hormone (TH) regulates aspects of proximodistal patterning of the caudal fin rays, regardless of fin size. TH promotes distal gene expression patterns, coordinating ray bifurcations and segment shortening with skeletal outgrowth along the proximodistal axis. This distalizing role for TH is conserved between development and regeneration, in all fins (paired and medial), and between
MeSH term(s)	Animals ; Zebrafish/physiology ; Zebrafish Proteins/genetics ; Zebrafish Proteins/metabolism ; Thyroid Hormones/genetics ; Animal Fins/physiology ; Regeneration/physiology
Chemical Substances	Zebrafish Proteins ; Thyroid Hormones
Language	English
Publishing date	2023-05-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2219770120
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Article ; Online: Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics.

Galindo, Demi / Sweet, Elly / DeLeon, Zoey / Wagner, Mitchel / DeLeon, Adrian / Carter, Casey / McMenamin, Sarah K / Cooper, W James

Evolution & development

2019 Volume 21, Issue 5, Page(s) 231–246

Abstract: Protrusile jaws are a highly useful innovation that has been linked to extensive diversification in fish feeding ecology. Jaw protrusion can enhance the performance of multiple functions, such as suction production and capturing elusive prey. Identifying ...

Abstract	Protrusile jaws are a highly useful innovation that has been linked to extensive diversification in fish feeding ecology. Jaw protrusion can enhance the performance of multiple functions, such as suction production and capturing elusive prey. Identifying the developmental factors that alter protrusion ability will improve our understanding of fish diversification. In the zebrafish protrusion arises postmetamorphosis. Fish metamorphosis typically includes significant changes in trophic morphology, accompanies a shift in feeding niche and coincides with increased thyroid hormone production. We tested whether thyroid hormone affects the development of zebrafish feeding mechanics. We found that it affected all developmental stages examined, but that effects were most pronounced after metamorphosis. Thyroid hormone levels affected the development of jaw morphology, feeding mechanics, shape variation, and cranial ossification. Adult zebrafish utilize protrusile jaws, but an absence of thyroid hormone impaired development of the premaxillary bone, which is critical to jaw protrusion. Premaxillae from early juvenile zebrafish and hypothyroid adult zebrafish resemble those from adults in the genera Danionella, Devario, and Microdevario that show little to no jaw protrusion. Our findings suggest that evolutionary changes in how the developing skulls of danionin minnows respond to thyroid hormone may have promoted diversification into different feeding niches.
MeSH term(s)	Animals ; Biological Evolution ; Biomechanical Phenomena ; Feeding Behavior ; Jaw/physiology ; Maxillofacial Development/physiology ; Thyroid Hormones/metabolism ; Zebrafish/growth & development ; Zebrafish/physiology
Chemical Substances	Thyroid Hormones
Language	English
Publishing date	2019-08-02
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2020288-X
ISSN	1525-142X ; 1520-541X
ISSN (online)	1525-142X
ISSN	1520-541X
DOI	10.1111/ede.12299
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Article ; Online: Notochord vacuoles absorb compressive bone growth during zebrafish spine formation.

Bagwell, Jennifer / Norman, James / Ellis, Kathryn / Peskin, Brianna / Hwang, James / Ge, Xiaoyan / Nguyen, Stacy V / McMenamin, Sarah K / Stainier, Didier Yr / Bagnat, Michel

eLife

2020 Volume 9

Abstract: The vertebral column or spine assembles around the notochord rod which contains a core made of large vacuolated cells. Each vacuolated cell possesses a single ﬂuid-ﬁlled vacuole, and loss or fragmentation of these vacuoles in zebrafish leads to spine ... ...

Abstract	The vertebral column or spine assembles around the notochord rod which contains a core made of large vacuolated cells. Each vacuolated cell possesses a single ﬂuid-ﬁlled vacuole, and loss or fragmentation of these vacuoles in zebrafish leads to spine kinking. Here, we identified a mutation in the kinase gene
MeSH term(s)	Animals ; Gene Expression Regulation, Developmental ; Mutation ; Notochord/metabolism ; Receptor-Interacting Protein Serine-Threonine Kinases/genetics ; Spine/growth & development ; Vacuoles/metabolism ; Zebrafish/embryology ; Zebrafish Proteins/genetics
Chemical Substances	Zebrafish Proteins ; Receptor-Interacting Protein Serine-Threonine Kinases (EC 2.7.11.1)
Language	English
Publishing date	2020-01-29
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.51221
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Article ; Online: Metamorphosis in teleosts.

McMenamin, Sarah K / Parichy, David M

Current topics in developmental biology

2013 Volume 103, Page(s) 127–165

Abstract: Teleosts are the largest and most diverse group of vertebrates, and many species undergo morphological, physiological, and behavioral transitions, "metamorphoses," as they progress between morphologically divergent life stages. The larval metamorphosis ... ...

Abstract	Teleosts are the largest and most diverse group of vertebrates, and many species undergo morphological, physiological, and behavioral transitions, "metamorphoses," as they progress between morphologically divergent life stages. The larval metamorphosis that generally occurs as teleosts mature from larva to juvenile involves the loss of embryo-specific features, the development of new adult features, major remodeling of different organ systems, and changes in physical proportions and overall phenotype. Yet, in contrast to anuran amphibians, for example, teleost metamorphosis can entail morphological change that is either sudden and profound, or relatively gradual and subtle. Here, we review the definition of metamorphosis in teleosts, the diversity of teleost metamorphic strategies and the transitions they involve, and what is known of their underlying endocrine and genetic bases. We suggest that teleost metamorphosis offers an outstanding opportunity for integrating our understanding of endocrine mechanisms, cellular processes of morphogenesis and differentiation, and the evolution of diverse morphologies and life histories.
MeSH term(s)	Animals ; Biodiversity ; Endocrine System/growth & development ; Fishes/growth & development ; Metamorphosis, Biological ; Morphogenesis
Language	English
Publishing date	2013-01-31
Publishing country	United States
Document type	Journal Article ; Review
ISSN	1557-8933 ; 0070-2153
ISSN (online)	1557-8933
ISSN	0070-2153
DOI	10.1016/B978-0-12-385979-2.00005-8
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Article ; Online: Ancient DNA assessment of tiger salamander population in Yellowstone National Park.

McMenamin, Sarah K / Hadly, Elizabeth A

PloS one

2012 Volume 7, Issue 3, Page(s) e32763

Abstract: Recent data indicates that blotched tiger salamanders (Ambystoma tigrinum melanostictum) in northern regions of Yellowstone National Park are declining due to climate-related habitat changes. In this study, we used ancient and modern mitochondrial ... ...

Abstract	Recent data indicates that blotched tiger salamanders (Ambystoma tigrinum melanostictum) in northern regions of Yellowstone National Park are declining due to climate-related habitat changes. In this study, we used ancient and modern mitochondrial haplotype diversity to model the effective size of this amphibian population through recent geological time and to assess past responses to climatic changes in the region. Using subfossils collected from a cave in northern Yellowstone, we analyzed >700 base pairs of mitochondrial sequence from 16 samples ranging in age from 100 to 3300 years old and found that all shared an identical haplotype. Although mitochondrial diversity was extremely low within the living population, we still were able to detect geographic subdivision within the local area. Using serial coalescent modelling with Bayesian priors from both modern and ancient genetic data we simulated a range of probable population sizes and mutation rates through time. Our simulations suggest that regional mitochondrial diversity has remained relatively constant even through climatic fluctuations of recent millennia.
MeSH term(s)	Ambystoma/genetics ; Analysis of Variance ; Animals ; Base Sequence ; Bayes Theorem ; Computer Simulation ; DNA Primers/genetics ; DNA, Mitochondrial/genetics ; Evolution, Molecular ; Fossils ; Genetic Variation ; Haplotypes/genetics ; Models, Genetic ; Molecular Sequence Data ; Mutation Rate ; Population Density ; Sequence Analysis, DNA ; Wyoming
Chemical Substances	DNA Primers ; DNA, Mitochondrial
Language	English
Publishing date	2012-03-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0032763
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Article ; Online: Anatomical Assessment of the Adult Skeleton of Zebrafish Reared Under Different Thyroid Hormone Profiles.

Keer, Stephanie / Cohen, Karly / May, Catherine / Hu, Yinan / McMenamin, Sarah / Hernandez, Luz Patricia

Anatomical record (Hoboken, N.J. : 2007)

2019 Volume 302, Issue 10, Page(s) 1754–1769

Abstract: Thyroid hormone (TH) directs the growth and maintenance of tissues throughout the body during development and into adulthood, and plays a particularly important role in proper ossification and homeostasis of the skeleton. To better understand the roles ... ...

Abstract	Thyroid hormone (TH) directs the growth and maintenance of tissues throughout the body during development and into adulthood, and plays a particularly important role in proper ossification and homeostasis of the skeleton. To better understand the roles of TH in the skeletogenesis of a vertebrate model, and to define areas of the skeleton that are particularly sensitive to developmental TH, we examined the effects of hypo- and hyperthyroidism on skeletal development in zebrafish. Performing a bone-by-bone anatomical assessment on the entire skeleton of adult fish, we found that TH is required for proper ossification, growth, morphogenesis, and fusion of numerous bones. We showed that the pectoral girdle, dermatocranium, Weberian apparatus, and dentary are particularly sensitive to TH, and that TH affects development of skeletal element regardless of bone type and developmental origin. Indeed, the hormone does not universally promote ossification: we found that developmental TH prevents ectopic ossification in multiple thin bones and within connective tissue of the jaw. In all, we found that TH regulates proper morphogenesis and ossification in the majority of zebrafish bones, and that the requirement for the hormone extends across bone types and developmental profiles. Anat Rec, 302:1754-1769, 2019. © 2019 American Association for Anatomy.
MeSH term(s)	Animals ; Animals, Genetically Modified ; Models, Animal ; Osteogenesis/physiology ; Skeleton/growth & development ; Thyroid Hormones/genetics ; Thyroid Hormones/metabolism ; Zebrafish/growth & development
Chemical Substances	Thyroid Hormones
Language	English
Publishing date	2019-04-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2269667-2
ISSN	1932-8494 ; 1932-8486
ISSN (online)	1932-8494
ISSN	1932-8486
DOI	10.1002/ar.24139
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Article ; Online: Notochord vacuoles absorb compressive bone growth during zebrafish spine formation

Jennifer Bagwell / James Norman / Kathryn Ellis / Brianna Peskin / James Hwang / Xiaoyan Ge / Stacy V Nguyen / Sarah K McMenamin / Didier YR Stainier / Michel Bagnat

eLife, Vol

2020 Volume 9

Abstract	The vertebral column or spine assembles around the notochord rod which contains a core made of large vacuolated cells. Each vacuolated cell possesses a single ﬂuid-ﬁlled vacuole, and loss or fragmentation of these vacuoles in zebrafish leads to spine kinking. Here, we identified a mutation in the kinase gene dstyk that causes fragmentation of notochord vacuoles and a severe congenital scoliosis-like phenotype in zebrafish. Live imaging revealed that Dstyk regulates fusion of membranes with the vacuole. We find that localized disruption of notochord vacuoles causes vertebral malformation and curving of the spine axis at those sites. Accordingly, in dstyk mutants the spine curves increasingly over time as vertebral bone formation compresses the notochord asymmetrically, causing vertebral malformations and kinking of the axis. Together, our data show that notochord vacuoles function as a hydrostatic scaffold that guides symmetrical growth of vertebrae and spine formation.
Keywords	notochord ; vacuolated cells ; vertebra ; scoliosis ; dstyk ; spine ; Medicine ; R ; Science ; Q ; Biology (General) ; QH301-705.5
Language	English
Publishing date	2020-01-01T00:00:00Z
Publisher	eLife Sciences Publications Ltd
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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