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Article ; Online: A novel cis-regulatory element drives early expression of <i>Nkx3.2</i> in the gnathostome primary jaw joint.

Leyhr, Jake / Waldmann, Laura / Filipek-Górniok, Beata / Zhang, Hanqing / Allalou, Amin / Haitina, Tatjana

2022 Volume 11

Abstract: 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 ... ...

Abstract	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.
MeSH term(s)	Animals ; Biological Evolution ; Genome ; Jaw ; Lampreys ; Mammals/genetics ; Regulatory Sequences, Nucleic Acid ; Zebrafish/genetics ; Gene Expression Regulation, Developmental/genetics ; Gene Deletion ; Vertebrates/genetics ; Vertebrates/growth & development
Chemical Substances	nkx3-2 protein, zebrafish
Language	English
Publishing date	2022-11-15
Publishing country	England
Document type	Journal Article ; 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.75749
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Article ; Online: The broad role of Nkx3.2 in the development of the zebrafish axial skeleton.

Waldmann, Laura / Leyhr, Jake / Zhang, Hanqing / Öhman-Mägi, Caroline / Allalou, Amin / Haitina, Tatjana

PloS one

2021 Volume 16, Issue 8, Page(s) e0255953

Abstract: 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 ... ...

Abstract	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.
MeSH term(s)	Animals ; Bone and Bones ; Gene Expression Regulation, Developmental ; Homeodomain Proteins ; Transcription Factors ; Zebrafish
Chemical Substances	Homeodomain Proteins ; Transcription Factors
Language	English
Publishing date	2021-08-19
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.0255953
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Article ; Online: A novel cis-regulatory element drives early expression of Nkx3.2 in the gnathostome primary jaw joint

Jake Leyhr / Laura Waldmann / Beata Filipek-Górniok / Hanqing Zhang / Amin Allalou / Tatjana Haitina

eLife, Vol

2022 Volume 11

Abstract	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.
Keywords	cis-regulatory element ; enhancer deletion ; nkx3.2 ; jaw joint ; gnathostome ; optical projection tomography ; Medicine ; R ; Science ; Q ; Biology (General) ; QH301-705.5
Subject code	570
Language	English
Publishing date	2022-11-01T00:00:00Z
Publisher	eLife Sciences Publications Ltd
Document type	Article ; Online
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Article ; Online: The role of Gdf5 in the development of the zebrafish fin endoskeleton.

Waldmann, Laura / Leyhr, Jake / Zhang, Hanqing / Allalou, Amin / Öhman-Mägi, Caroline / Haitina, Tatjana

Developmental dynamics : an official publication of the American Association of Anatomists

2021 Volume 251, Issue 9, Page(s) 1535–1549

Abstract: Background: The development of the vertebrate limb skeleton requires a complex interaction of multiple factors to facilitate the correct shaping and positioning of bones and joints. Growth and differentiation factor 5 (Gdf5) is involved in patterning ... ...

Abstract	Background: The development of the vertebrate limb skeleton requires a complex interaction of multiple factors to facilitate the correct shaping and positioning of bones and joints. Growth and differentiation factor 5 (Gdf5) is involved in patterning appendicular skeletal elements including joints. Expression of gdf5 in zebrafish has been detected in fin mesenchyme condensations and segmentation zones as well as the jaw joint, however, little is known about the functional role of Gdf5 outside of Amniota. Results: We generated CRISPR/Cas9 knockout of gdf5 in zebrafish and analyzed the resulting phenotype at different developmental stages. Homozygous gdf5 mutant zebrafish displayed changes in segmentation of the endoskeletal disc and, as a consequence, loss of posterior radials in the pectoral fins. Mutant fish also displayed disorganization and reduced length of endoskeletal elements in the median fins, while joints and mineralization seemed unaffected. Conclusions: Our study demonstrates the importance of Gdf5 in the development of the zebrafish pectoral and median fin endoskeleton and reveals that the severity of the effect increases from anterior to posterior elements. Our findings are consistent with phenotypes observed in the human and mouse appendicular skeleton in response to Gdf5 knockout, suggesting a broadly conserved role for Gdf5 in Osteichthyes.
MeSH term(s)	Animal Fins/metabolism ; Animals ; Bone and Bones/metabolism ; Gene Expression Regulation, Developmental ; Growth Differentiation Factor 5/genetics ; Growth Differentiation Factor 5/metabolism ; Mice ; Zebrafish/metabolism ; Zebrafish Proteins/genetics ; Zebrafish Proteins/metabolism
Chemical Substances	Growth Differentiation Factor 5 ; Zebrafish Proteins
Language	English
Publishing date	2021-07-29
Publishing country	United States
Document type	Journal Article
ZDB-ID	1102541-4
ISSN	1097-0177 ; 1058-8388
ISSN (online)	1097-0177
ISSN	1058-8388
DOI	10.1002/dvdy.399
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Article: zOPT: an open source optical projection tomography system and methods for rapid 3D zebrafish imaging.

Zhang, Hanqing / Waldmann, Laura / Manuel, Remy / Boije, Henrik / Haitina, Tatjana / Allalou, Amin

Biomedical optics express

2020 Volume 11, Issue 8, Page(s) 4290–4305

Abstract: 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 ... ...

Abstract	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.
Language	English
Publishing date	2020-07-15
Publishing country	United States
Document type	Journal Article
ZDB-ID	2572216-5
ISSN	2156-7085
ISSN	2156-7085
DOI	10.1364/BOE.393519
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Article ; Online: The broad role of Nkx3.2 in the development of the zebrafish axial skeleton.

Laura Waldmann / Jake Leyhr / Hanqing Zhang / Caroline Öhman-Mägi / Amin Allalou / Tatjana Haitina

PLoS ONE, Vol 16, Iss 8, p e

2021 Volume 0255953

Abstract	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.
Keywords	Medicine ; R ; Science ; Q
Subject code	572
Language	English
Publishing date	2021-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Passive in-vehicle driver breath alcohol detection using advanced sensor signal acquisition and fusion.

Ljungblad, Jonas / Hök, Bertil / Allalou, Amin / Pettersson, Håkan

Traffic injury prevention

2017 Volume 18, Issue sup1, Page(s) S31–S36

Abstract: Objective: The research objective of the present investigation is to demonstrate the present status of passive in-vehicle driver breath alcohol detection and highlight the necessary conditions for large-scale implementation of such a system. Completely ... ...

Abstract	Objective: The research objective of the present investigation is to demonstrate the present status of passive in-vehicle driver breath alcohol detection and highlight the necessary conditions for large-scale implementation of such a system. Completely passive detection has remained a challenge mainly because of the requirements on signal resolution combined with the constraints of vehicle integration. The work is part of the Driver Alcohol Detection System for Safety (DADSS) program aiming at massive deployment of alcohol sensing systems that could potentially save thousands of American lives annually. Method: The work reported here builds on earlier investigations, in which it has been shown that detection of alcohol vapor in the proximity of a human subject may be traced to that subject by means of simultaneous recording of carbon dioxide (CO Results: Improvement of the sensor system with respect to signal resolution including algorithm and software development, and fusion of the sensor and camera signals was successfully implemented and tested before starting the human study. In addition, experimental tests and simulations were performed with the purpose of connecting human subject data with repeatable experimental conditions. The results include occurrence statistics of detected breaths by signal peaks of CO Conclusions: It is concluded that a further important step toward completely passive detection of driver breath alcohol has been taken. If required, the sniffer function with alcohol detection capability can be combined with a subsequent highly accurate breath test to confirm the driver's legal status using the same sensor device. The study is relevant to crash avoidance, in particular driver monitoring systems and driver-vehicle interface design.
MeSH term(s)	Alcoholic Intoxication/diagnosis ; Automobile Driving/statistics & numerical data ; Breath Tests/instrumentation ; Ethanol/isolation & purification ; Humans ; Substance Abuse Detection/methods
Chemical Substances	Ethanol (3K9958V90M)
Language	English
Publishing date	2017-05-29
Publishing country	England
Document type	Journal Article
ZDB-ID	2089818-6
ISSN	1538-957X ; 1538-9588
ISSN (online)	1538-957X
ISSN	1538-9588
DOI	10.1080/15389588.2017.1312688
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Article ; Online: mafba and mafbb differentially regulate lymphatic endothelial cell migration in topographically distinct manners.

Arnold, Hannah / Panara, Virginia / Hußmann, Melina / Filipek-Gorniok, Beata / Skoczylas, Renae / Ranefall, Petter / Gloger, Marleen / Allalou, Amin / Hogan, Benjamin M / Schulte-Merker, Stefan / Koltowska, Katarzyna

Cell reports

2022 Volume 39, Issue 12, Page(s) 110982

Abstract: Lymphangiogenesis, formation of lymphatic vessels from pre-existing vessels, is a dynamic process that requires cell migration. Regardless of location, migrating lymphatic endothelial cell (LEC) progenitors probe their surroundings to form the lymphatic ... ...

Abstract	Lymphangiogenesis, formation of lymphatic vessels from pre-existing vessels, is a dynamic process that requires cell migration. Regardless of location, migrating lymphatic endothelial cell (LEC) progenitors probe their surroundings to form the lymphatic network. Lymphatic-development regulation requires the transcription factor MAFB in different species. Zebrafish Mafba, expressed in LEC progenitors, is essential for their migration in the trunk. However, the transcriptional mechanism that orchestrates LEC migration in different lymphatic endothelial beds remains elusive. Here, we uncover topographically different requirements of the two paralogs, Mafba and Mafbb, for LEC migration. Both mafba and mafbb are necessary for facial lymphatic development, but mafbb is dispensable for trunk lymphatic development. On the molecular level, we demonstrate a regulatory network where Vegfc-Vegfd-SoxF-Mafba-Mafbb is essential in facial lymphangiogenesis. We identify that mafba and mafbb tune the directionality of LEC migration and vessel morphogenesis that is ultimately necessary for lymphatic function.
MeSH term(s)	Animals ; Cell Movement ; Endothelial Cells ; Lymphangiogenesis ; Lymphatic Vessels ; Morphogenesis ; Signal Transduction ; Zebrafish
Language	English
Publishing date	2022-05-31
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2022.110982
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Article ; Online: Chondroitin/dermatan sulfate glycosyltransferase genes are essential for craniofacial development.

Habicher, Judith / Varshney, Gaurav K / Waldmann, Laura / Snitting, Daniel / Allalou, Amin / Zhang, Hanqing / Ghanem, Abdurrahman / Öhman Mägi, Caroline / Dierker, Tabea / Kjellén, Lena / Burgess, Shawn M / Ledin, Johan

PLoS genetics

2022 Volume 18, Issue 2, Page(s) e1010067

Abstract: Chondroitin/dermatan sulfate (CS/DS) proteoglycans are indispensable for animal development and homeostasis but the large number of enzymes involved in their biosynthesis have made CS/DS function a challenging problem to study genetically. In our study, ... ...

Abstract	Chondroitin/dermatan sulfate (CS/DS) proteoglycans are indispensable for animal development and homeostasis but the large number of enzymes involved in their biosynthesis have made CS/DS function a challenging problem to study genetically. In our study, we generated loss-of-function alleles in zebrafish genes encoding CS/DS biosynthetic enzymes and characterized the effect on development in single and double mutants. Homozygous mutants in chsy1, csgalnact1a, csgalnat2, chpfa, ust and chst7, respectively, develop to adults. However, csgalnact1a-/- fish develop distinct craniofacial defects while the chsy1-/- skeletal phenotype is milder and the remaining mutants display no gross morphological abnormalities. These results suggest a high redundancy for the CS/DS biosynthetic enzymes and to further reduce CS/DS biosynthesis we combined mutant alleles. The craniofacial phenotype is further enhanced in csgalnact1a-/-;chsy1-/- adults and csgalnact1a-/-;csgalnact2-/- larvae. While csgalnact1a-/-;csgalnact2-/- was the most affected allele combination in our study, CS/DS is still not completely abolished. Transcriptome analysis of chsy1-/-, csgalnact1a-/- and csgalnact1a-/-;csgalnact2-/- larvae revealed that the expression had changed in a similar way in the three mutant lines but no differential expression was found in any of fifty GAG biosynthesis enzymes identified. Thus, zebrafish larvae do not increase transcription of GAG biosynthesis genes as a consequence of decreased CS/DS biosynthesis. The new zebrafish lines develop phenotypes similar to clinical characteristics of several human congenital disorders making the mutants potentially useful to study disease mechanisms and treatment.
MeSH term(s)	Animals ; Chondroitin Sulfates/metabolism ; Dermatan Sulfate/genetics ; Dermatan Sulfate/metabolism ; Glycosyltransferases/genetics ; Phenotype ; Zebrafish/genetics ; Zebrafish/metabolism
Chemical Substances	Dermatan Sulfate (24967-94-0) ; Chondroitin Sulfates (9007-28-7) ; Glycosyltransferases (EC 2.4.-)
Language	English
Publishing date	2022-02-22
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2186725-2
ISSN	1553-7404 ; 1553-7390
ISSN (online)	1553-7404
ISSN	1553-7390
DOI	10.1371/journal.pgen.1010067
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Article ; Online: (with research data) Automated deep-phenotyping of the vertebrate brain.

Allalou, Amin / Wu, Yuelong / Ghannad-Rezaie, Mostafa / Eimon, Peter M / Yanik, Mehmet Fatih

eLife

2017 Volume 6

Abstract: Here, we describe an automated platform suitable for large-scale deep-phenotyping of zebrafish mutant lines, which uses optical projection tomography to rapidly image brain-specific gene expression patterns in 3D at cellular resolution. Registration ... ...

Abstract	Here, we describe an automated platform suitable for large-scale deep-phenotyping of zebrafish mutant lines, which uses optical projection tomography to rapidly image brain-specific gene expression patterns in 3D at cellular resolution. Registration algorithms and correlation analysis are then used to compare 3D expression patterns, to automatically detect all statistically significant alterations in mutants, and to map them onto a brain atlas. Automated deep-phenotyping of a mutation in the master transcriptional regulator
MeSH term(s)	Animals ; Automation, Laboratory/methods ; Brain/diagnostic imaging ; Brain/physiology ; Brain Mapping/methods ; Gene Expression Profiling/methods ; Mutation ; Phenotype ; Tomography/methods ; Zebrafish/genetics ; Zebrafish/physiology
Language	English
Publishing date	2017-04-13
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.23379
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