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Haitina, Tatjana, DocentORCID iD iconorcid.org/0000-0002-8754-5534
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Publications (10 of 49) Show all publications
Stundl, J., Martik, M. L., Chen, D., Raja, D. A., Franek, R., Pospisilova, A., . . . Bronner, M. E. (2023). Ancient vertebrate dermal armor evolved from trunk neural crest. Proceedings of the National Academy of Sciences of the United States of America, 120(30), Article ID e2221120120.
Open this publication in new window or tab >>Ancient vertebrate dermal armor evolved from trunk neural crest
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2023 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 120, no 30, article id e2221120120Article in journal (Refereed) Published
Abstract [en]

Bone is an evolutionary novelty of vertebrates, likely to have first emerged as part of ancestral dermal armor that consisted of osteogenic and odontogenic components. Whether these early vertebrate structures arose from mesoderm or neural crest cells has been a matter of considerable debate. To examine the developmental origin of the bony part of the dermal armor, we have performed in vivo lineage tracing in the sterlet sturgeon, a representative of nonteleost ray- finned fish that has retained an extensive postcranial dermal skeleton. The results definitively show that sterlet trunk neural crest cells give rise to osteoblasts of the scutes. Transcriptional profiling further reveals neural crest gene signature in sterlet scutes as well as bichir scales. Finally, histological and microCT analyses of ray- finned fish dermal armor show that their scales and scutes are formed by bone, dentin, and hypermineralized covering tissues, in various combinations, that resemble those of the first armored vertebrates. Taken together, our results support a primitive skeletogenic role for the neural crest along the entire body axis, that was later progressively restricted to the cranial region during vertebrate evolution. Thus, the neural crest was a crucial evolutionary innovation driving the origin and diversification of dermal armor along the entire body axis.

Place, publisher, year, edition, pages
Proceedings of the National Academy of Sciences (PNAS), 2023
Keywords
neural crest, vertebrate evolution, scales, sterlet sturgeon, skeleton
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-511895 (URN)10.1073/pnas.2221120120 (DOI)001055246900002 ()37459514 (PubMedID)
Funder
EU, Horizon 2020, 897949Knut and Alice Wallenberg Foundation
Available from: 2023-09-21 Created: 2023-09-21 Last updated: 2023-09-21Bibliographically approved
Leyhr, J., Sanchez, S., Dollman, K. N., Tafforeau, P. & Haitina, T. (2023). Enhanced contrast synchrotron X-ray microtomography for describing skeleton-associated soft tissue defects in zebrafish mutants. Frontiers in Endocrinology, 14, Article ID 1108916.
Open this publication in new window or tab >>Enhanced contrast synchrotron X-ray microtomography for describing skeleton-associated soft tissue defects in zebrafish mutants
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2023 (English)In: Frontiers in Endocrinology, E-ISSN 1664-2392, Vol. 14, article id 1108916Article in journal (Refereed) Published
Abstract [en]

Detailed histological analyses are desirable for zebrafish mutants that are models for human skeletal diseases, but traditional histological techniques are limited to two-dimensional thin sections with orientations highly dependent on careful sample preparation. On the other hand, techniques that provide three-dimensional (3D) datasets including mu CT scanning are typically limited to visualizing the bony skeleton and lack histological resolution. We combined diffusible iodine-based contrast enhancement (DICE) and propagation phase-contrast synchrotron radiation micro-computed tomography (PPC-SR mu CT) to image late larval and juvenile zebrafish, obtaining high-quality 3D virtual histology datasets of the mineralized skeleton and surrounding soft tissues. To demonstrate this technique, we used virtual histological thin sections and 3D segmentation to qualitatively and quantitatively compare wild-type zebrafish and nkx3.2(-/-) mutants to characterize novel soft-tissue phenotypes in the muscles and tendons of the jaw and ligaments of the Weberian apparatus, as well as the sinus perilymphaticus associated with the inner ear. We could observe disrupted fiber organization and tendons of the adductor mandibulae and protractor hyoideus muscles associated with the jaws, and show that despite this, the overall muscle volumes appeared unaffected. Ligaments associated with the malformed Weberian ossicles were mostly absent in nkx3.2(-/-) mutants, and the sinus perilymphaticus was severely constricted or absent as a result of the fused exoccipital and basioccipital elements. These soft-tissue phenotypes have implications for the physiology of nkx3.2(-/-) zebrafish, and demonstrate the promise of DICE-PPC-SR mu CT for histopathological investigations of bone-associated soft tissues in small-fish skeletal disease models and developmental studies more broadly.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2023
Keywords
iodine staining, propagation phase-contrast synchrotron microtomography, virtual histology, zebrafish mutant, 3D segmentation, inner ear, Weberian apparatus, nkx3, 2
National Category
Developmental Biology
Identifiers
urn:nbn:se:uu:diva-500297 (URN)10.3389/fendo.2023.1108916 (DOI)000953634400001 ()36950679 (PubMedID)
Funder
Swedish Research Council, 2022-04988Swedish Research Council, 2019-04595Lars Hierta Memorial Foundation
Available from: 2023-04-25 Created: 2023-04-25 Last updated: 2024-01-17Bibliographically approved
Haitina, T. & Debiais-Thibaud, M. (2023). Evolutionary Genomics of Odontode Tissues (1ed.). In: Dongle Chen (Ed.), Odontodes: The Developmental and Evolutionary Building Blocks of Dentitions (pp. 41). Boca Raton: CRC Press
Open this publication in new window or tab >>Evolutionary Genomics of Odontode Tissues
2023 (English)In: Odontodes: The Developmental and Evolutionary Building Blocks of Dentitions / [ed] Dongle Chen, Boca Raton: CRC Press, 2023, 1, p. 41-Chapter in book (Refereed)
Abstract [en]

Teeth, scales, fin spines, and other odontodes are hot topics in evolutionary biology due to their great variation in number, shape, and anatomical localization in vertebrates as a result of different types of adaptations. Structural adaptation arose through variations in the composition of the enamel/enameloid and dentin layers that build up the mineralized components of teeth and other odontodes. These variations are known from both fossil and extant groups of vertebrates and rely on differences in the proteins secreted by the specialized odontode cells, ameloblasts, and odontoblasts.

In this chapter, we focus on recent genomic and gene expression data to better understand the evolution of gene families engaged in the processes of secretion, mineralization, and maturation of odontode matrices. Our focus will be structural matrix proteins (collagenous and non-collagenous), calcium-interacting proteins necessary for mineralization, and proteins regulating matrix degradation over the course of tissue maturation.

Place, publisher, year, edition, pages
Boca Raton: CRC Press, 2023 Edition: 1
National Category
Developmental Biology Zoology
Identifiers
urn:nbn:se:uu:diva-516268 (URN)9781003439653 (ISBN)
Funder
Swedish Research Council, 2022-04988
Available from: 2023-11-19 Created: 2023-11-19 Last updated: 2024-06-20Bibliographically approved
Leyhr, J., Waldmann, L., Filipek-Górniok, B., Zhang, H., Allalou, A. & Haitina, T. (2022). A novel cis-regulatory element drives early expression of Nkx3.2 in the gnathostome primary jaw joint. eLIFE, 11, Article ID e75749.
Open this publication in new window or tab >>A novel cis-regulatory element drives early expression of Nkx3.2 in the gnathostome primary jaw joint
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2022 (English)In: eLIFE, E-ISSN 2050-084X, Vol. 11, article id e75749Article in journal (Refereed) Published
Abstract [en]

The acquisition of movable jaws was a major event during vertebrate evolution. The role of NK3 homeobox 2 (Nkx3.2) transcription factor in patterning the primary jaw joint of gnathostomes (jawed vertebrates) is well known, however knowledge about its regulatory mechanism is lacking. In this study, we report a proximal enhancer element of Nkx3.2 that is deeply conserved in most gnathostomes but undetectable in the jawless hagfish and lamprey. This enhancer is active in the developing jaw joint region of the zebrafish Danio rerio, and was thus designated as jaw joint regulatory sequence 1 (JRS1). We further show that JRS1 enhancer sequences from a range of gnathostome species, including a chondrichthyan and mammals, have the same activity in the jaw joint as the native zebrafish enhancer, indicating a high degree of functional conservation despite the divergence of cartilaginous and bony fish lineages or the transition of the primary jaw joint into the middle ear of mammals. Finally, we show that deletion of JRS1 from the zebrafish genome using CRISPR/Cas9 results in a significant reduction of early gene expression of nkx3.2 and leads to a transient jaw joint deformation and partial fusion. Emergence of this Nkx3.2 enhancer in early gnathostomes may have contributed to the origin and shaping of the articulating surfaces of vertebrate jaws.

Place, publisher, year, edition, pages
eLife Sciences Publications LtdeLife Sciences Publications, 2022
National Category
Developmental Biology
Identifiers
urn:nbn:se:uu:diva-493106 (URN)10.7554/elife.75749 (DOI)000961591300001 ()36377467 (PubMedID)
Funder
Swedish Research Council, 621-2012-4673Science for Life Laboratory, SciLifeLab, Development Project 2017Science for Life Laboratory, SciLifeLab, Technology Development grant 2018
Available from: 2023-01-12 Created: 2023-01-12 Last updated: 2024-01-15Bibliographically approved
Waldmann, L., Leyhr, J., Zhang, H., Allalou, A., Öhman, C. & Haitina, T. (2022). The Role of Gdf5 in the Development of the Zebrafish Fin Endoskeleton. Developmental Dynamics, 251(9), 1535-1549
Open this publication in new window or tab >>The Role of Gdf5 in the Development of the Zebrafish Fin Endoskeleton
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2022 (English)In: Developmental Dynamics, ISSN 1058-8388, E-ISSN 1097-0177, Vol. 251, no 9, p. 1535-1549Article in journal (Refereed) Published
Abstract [en]

The development of the vertebrate skeleton requires a complex interaction of multiple factors to facilitate correct shaping and positioning of bones and joints. Growth and differentiation factor 5 (Gdf5), a member of the transforming growth factor-beta family (TGF-beta) is involved in patterning appendicular skeletal elements including joints. Expression of gdf5 in zebrafish has been detected within the first pharyngeal arch jaw joint, fin mesenchyme condensations and segmentation zones in median fins, however little is known about the functional role of Gdf5 outside of Amniota. 

We generated CRISPR/Cas9 knockout of gdf5 in zebrafish and analysed the resulting phenotype at different developmental stages. Homozygous gdf5 mutant zebrafish display truncated median fin endoskeletal elements and loss of posterior radials in the pectoral fins. 

These findings are consistent with phenotypes observed in human and mouse appendicular skeleton in response to Gdf5 knockout, suggesting a broadly conserved role for Gdf5 in Osteichthyes.

Place, publisher, year, edition, pages
John Wiley & SonsWiley, 2022
Keywords
gdf5, fin, joints, zebrafish, appendicular skeleton, CRISPR/Cas9 mutant
National Category
Developmental Biology
Identifiers
urn:nbn:se:uu:diva-430383 (URN)10.1002/dvdy.399 (DOI)000678743100001 ()
Funder
Swedish Research Council, 621-2012-4673Science for Life Laboratory, SciLifeLab
Available from: 2021-01-08 Created: 2021-01-08 Last updated: 2024-05-07Bibliographically approved
Leurs, N., Martinand-Mari, C., Venteo, S., Haitina, T. & Debiais-Thibaud, M. (2021). Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates. Frontiers in Genetics, 12, Article ID 620659.
Open this publication in new window or tab >>Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates
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2021 (English)In: Frontiers in Genetics, E-ISSN 1664-8021, Vol. 12, article id 620659Article in journal (Refereed) Published
Abstract [en]

Matrix Gla protein (Mgp) and bone Gla protein (Bgp) are vitamin-K dependent proteins that bind calcium in their gamma-carboxylated versions in mammals. They are recognized as positive (Bgp) or negative (Mgp and Bgp) regulators of biomineralization in a number of tissues, including skeletal tissues of bony vertebrates. The Mgp/Bgp gene family is poorly known in cartilaginous fishes, which precludes the understanding of the evolution of the biomineralization toolkit at the emergence of jawed vertebrates. Here we took advantage of recently released genomic and transcriptomic data in cartilaginous fishes and described the genomic loci and gene expression patterns of the Mgp/Bgp gene family. We identified three genes, Mgp1, Mgp2, and Bgp, in cartilaginous fishes instead of the single previously reported Mgp gene. We describe their genomic loci, resulting in a dynamic evolutionary scenario for this gene family including several events of local (tandem) duplications, but also of translocation events, along jawed vertebrate evolution. We describe the expression patterns of Mgp1, Mgp2, and Bgp in embryonic stages covering organogenesis in the small-spotted catshark Scyliorhinus canicula and present a comparative analysis with Mgp/Bgp family members previously described in bony vertebrates, highlighting ancestral features such as early embryonic, soft tissues, and neuronal expressions, but also derived features of cartilaginous fishes such as expression in fin supporting fibers. Our results support an ancestral function of Mgp in skeletal mineralization and a later derived function of Bgp in skeletal development that may be related to the divergence of bony vertebrates.

Place, publisher, year, edition, pages
Frontiers Media S.A.FRONTIERS MEDIA SA, 2021
Keywords
Gla protein, osteocalcin, shark, skeleton, evo-devo, biomineralization, bglap
National Category
Cancer and Oncology
Identifiers
urn:nbn:se:uu:diva-440901 (URN)10.3389/fgene.2021.620659 (DOI)000631843500001 ()33790944 (PubMedID)
Funder
Swedish Research Council, 621-2012-4673
Available from: 2021-04-28 Created: 2021-04-28 Last updated: 2024-01-15Bibliographically approved
Waldmann, L., Leyhr, J., Zhang, H., Öhman, C., Allalou, A. & Haitina, T. (2021). The broad role of Nkx3.2 in the development of the zebrafish axial skeleton. PLOS ONE, 16(8), Article ID e0255953.
Open this publication in new window or tab >>The broad role of Nkx3.2 in the development of the zebrafish axial skeleton
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2021 (English)In: PLOS ONE, E-ISSN 1932-6203, Vol. 16, no 8, article id e0255953Article in journal (Refereed) Published
Abstract [en]

The transcription factor Nkx3.2 (Bapx1) is an important chondrocyte maturation inhibitor. Previous Nkx3.2 knockdown and overexpression studies in non-mammalian gnathostomes have focused on its role in primary jaw joint development, while the function of this gene in broader skeletal development is not fully described. We generated a mutant allele of nkx3.2 in zebrafish with CRISPR/Cas9 and applied a range of techniques to characterize skeletal phenotypes at developmental stages from larva to adult, revealing loss of the jaw joint, fusions in bones of the occiput, morphological changes in the Weberian apparatus, and the loss or deformation of bony elements derived from basiventral cartilages of the vertebrae. Axial phenotypes are reminiscent of Nkx3.2 knockout in mammals, suggesting that the function of this gene in axial skeletal development is ancestral to osteichthyans. Our results highlight the broad role of nkx3.2 in zebrafish skeletal development and its context-specific functions in different skeletal elements.

Place, publisher, year, edition, pages
Public Library of Science (PLoS)Public Library of Science (PLoS), 2021
National Category
Medical Genetics
Identifiers
urn:nbn:se:uu:diva-455491 (URN)10.1371/journal.pone.0255953 (DOI)000686373300086 ()34411150 (PubMedID)
Funder
Swedish Research Council, 621-2012-4673
Available from: 2021-10-18 Created: 2021-10-18 Last updated: 2024-01-15Bibliographically approved
Ahlberg, P. & Haitina, T. (2020). Chapter 8 Neural Crest in Fossil Vertebrates:: What, If Anything, Can We Know? (1ed.). In: Brian Frank Eames, Daniel Meulemans Medeiros, Igor Adameyko (Ed.), Evolving Neural Crest Cells: (pp. 1-294). Taylor & Francis Group
Open this publication in new window or tab >>Chapter 8 Neural Crest in Fossil Vertebrates:: What, If Anything, Can We Know?
2020 (English)In: Evolving Neural Crest Cells / [ed] Brian Frank Eames, Daniel Meulemans Medeiros, Igor Adameyko, Taylor & Francis Group, 2020, 1, p. 1-294Chapter in book (Refereed)
Place, publisher, year, edition, pages
Taylor & Francis Group, 2020 Edition: 1
National Category
Developmental Biology
Research subject
Biology with specialization in Evolutionary Organismal Biology
Identifiers
urn:nbn:se:uu:diva-429681 (URN)10.1201/b22096 (DOI)9781315209197 (ISBN)
Available from: 2021-01-01 Created: 2021-01-01 Last updated: 2021-10-21Bibliographically approved
Ocampo Daza, D. & Haitina, T. (2020). Reconstruction of the Carbohydrate 6-O Sulfotransferase Gene Family Evolution in Vertebrates Reveals Novel Member, CHST16, Lost in Amniotes. Genome Biology and Evolution, 12(7), 993-1012
Open this publication in new window or tab >>Reconstruction of the Carbohydrate 6-O Sulfotransferase Gene Family Evolution in Vertebrates Reveals Novel Member, CHST16, Lost in Amniotes
2020 (English)In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 12, no 7, p. 993-1012Article in journal (Refereed) Published
Abstract [en]

Glycosaminoglycans are sulfated polysaccharide molecules, essential for many biological processes. The 6-O sulfation of glycosaminoglycans is carried out by carbohydrate 6-O sulfotransferases (C6OSTs), previously named Gal/GalNAc/GlcNAc 6-O sulfotransferases. Here, for the first time, we present a detailed phylogenetic reconstruction, analysis of gene synteny conservation and propose an evolutionary scenario for the C6OST family in major vertebrate groups, including mammals, birds, nonavian reptiles, amphibians, lobe-finned fishes, ray-finned fishes, cartilaginous fishes, and jawless vertebrates. The C6OST gene expansion likely started early in the chordate lineage, giving rise to four ancestral genes after the divergence of tunicates and before the emergence of extant vertebrates. The two rounds of whole-genome duplication in early vertebrate evolution (1R/2R) only contributed two additional C6OST subtype genes, increasing the vertebrate repertoire from four genes to six, divided into two branches. The first branch includes CHST1 and CHST3 as well as a previously unrecognized subtype, CHST16 that was lost in amniotes. The second branch includes CHST2, CHST7, and CHST5. Subsequently, local duplications of CHST5 gave rise to CHST4 in the ancestor of tetrapods, and to CHST6 in the ancestor of primates. The teleost-specific gene duplicates were identified for CHST1, CHST2, and CHST3 and are result of whole-genome duplication (3R) in the teleost lineage. We could also detect multiple, more recent lineage-specific duplicates. Thus, the vertebrate repertoire of C6OST genes has been shaped by gene duplications and gene losses at several stages of vertebrate evolution, with implications for the evolution of skeleton, nervous system, and cell-cell interactions.

Place, publisher, year, edition, pages
OXFORD UNIV PRESS, 2020
Keywords
carbohydrate 6-O sulfotransferases, Gal/GalNAc/GlcNAc 6-O sulfotransferases, whole-genome duplication, vertebrate
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-425247 (URN)10.1093/gbe/evz274 (DOI)000582693800003 ()32652010 (PubMedID)
Funder
Swedish Research Council, 2016-00552Swedish Research Council, 621-2012-4673
Available from: 2020-11-16 Created: 2020-11-16 Last updated: 2020-11-16Bibliographically approved
Zhang, H., Waldmann, L., Manuel, R., Boije, H., Haitina, T. & Allalou, A. (2020). zOPT: an open source optical projection tomography system and methods for rapid 3D zebrafish imaging. Biomedical Optics Express, 11(8), 4290-4305
Open this publication in new window or tab >>zOPT: an open source optical projection tomography system and methods for rapid 3D zebrafish imaging
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2020 (English)In: Biomedical Optics Express, E-ISSN 2156-7085, Vol. 11, no 8, p. 4290-4305Article in journal (Refereed) Published
Abstract [en]

Optical projection tomography (OPT) is a 3D imaging alternative to conventional microscopy which allows imaging of millimeter-sized object with isotropic micrometer resolution. The zebrafish is an established model organism and an important tool used in genetic and chemical screening. The size and optical transparency of the embryo and larva makes them well suited for imaging using OPT. Here, we present an open-source implementation of an OPT platform, built around a customized sample stage, 3D-printed parts and open source algorithms optimized for the system. We developed a versatile automated workflow including a two-step image processing approach for correcting the center of rotation and generating accurate 3D reconstructions. Our results demonstrate high-quality 3D reconstruction using synthetic data as well as real data of live and fixed zebrafish. The presented 3D-printable OPT platform represents a fully open design, low-cost and rapid loading and unloading of samples. Our system offers the opportunity for researchers with different backgrounds to setup and run OPT for large scale experiments, particularly in studies using zebrafish larvae as their key model organism.

Place, publisher, year, edition, pages
The Optical Society, 2020
National Category
Medical Image Processing
Identifiers
urn:nbn:se:uu:diva-419799 (URN)10.1364/BOE.393519 (DOI)000577451600016 ()32923043 (PubMedID)
Funder
Science for Life Laboratory, SciLifeLab
Available from: 2020-09-16 Created: 2020-09-16 Last updated: 2023-02-17Bibliographically approved
Projects
Regulation of Dlx genes in pharyngeal arches [2010-06845_VR]; Uppsala UniversityDevelopment of cranial tendons in the musculoskeletal system of vertebrates [2012-04673_VR]; Uppsala University
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0002-8754-5534

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