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Article ; Online: Shaping Hox gene activity to generate morphological diversity across vertebrate phylogeny.

Mallo, Moisés

2022 Volume 66, Issue 6, Page(s) 717–726

Abstract: The importance of Hox genes for the development and evolution of the vertebrate axial skeleton and paired appendages has been recognized for already several decades. The steady growth of genomic sequence data from an increasing number of vertebrate ... ...

Abstract	The importance of Hox genes for the development and evolution of the vertebrate axial skeleton and paired appendages has been recognized for already several decades. The steady growth of genomic sequence data from an increasing number of vertebrate species, together with the improvement of methods to analyze genomic structure and interactions, as well as to control gene activity in various species has refined our understanding of Hox gene activity in development and evolution. Here, I will review recent data addressing the influence of Hox regulatory processes in the evolution of the fins and the emergence of the tetrapod limb. In addition, I will discuss the involvement of posterior Hox genes in the control of vertebrate axial extension, focusing on an apparently divergent activity that Hox13 paralog group genes have on the regulation of tail bud development in mouse and zebrafish embryos.
MeSH term(s)	Animals ; Mice ; Genes, Homeobox/genetics ; Zebrafish/genetics
Language	English
Publishing date	2022-07-12
Publishing country	England
Document type	Journal Article
ISSN	1744-1358 ; 0071-1365
ISSN (online)	1744-1358
ISSN	0071-1365
DOI	10.1042/EBC20220050
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Article ; Online: Of Necks, Trunks and Tails

Moisés Mallo

Diversity, Vol 13, Iss 289, p

Axial Skeletal Diversity among Vertebrates

2021 Volume 289

Abstract: The axial skeleton of all vertebrates is composed of individual units known as vertebrae. Each vertebra has individual anatomical attributes, yet they can be classified in five different groups, namely cervical, thoracic, lumbar, sacral and caudal, ... ...

Abstract	The axial skeleton of all vertebrates is composed of individual units known as vertebrae. Each vertebra has individual anatomical attributes, yet they can be classified in five different groups, namely cervical, thoracic, lumbar, sacral and caudal, according to shared characteristics and their association with specific body areas. Variations in vertebral number, size, morphological features and their distribution amongst the different regions of the vertebral column are a major source of the anatomical diversity observed among vertebrates. In this review I will discuss the impact of those variations on the anatomy of different vertebrate species and provide insights into the genetic origin of some remarkable morphological traits that often serve to classify phylogenetic branches or individual species, like the long trunks of snakes or the long necks of giraffes.
Keywords	axial skeleton ; vertebrates ; evolution ; patterning ; body plan ; anatomical diversity ; Biology (General) ; QH301-705.5
Subject code	590
Language	English
Publishing date	2021-06-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
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Article ; Online: The vertebrate tail: a gene playground for evolution.

Mallo, Moisés

Cellular and molecular life sciences : CMLS

2019 Volume 77, Issue 6, Page(s) 1021–1030

Abstract: The tail of all vertebrates, regardless of size and anatomical detail, derive from a post-anal extension of the embryo known as the tail bud. Formation, growth and differentiation of this structure are closely associated with the activity of a group of ... ...

Abstract	The tail of all vertebrates, regardless of size and anatomical detail, derive from a post-anal extension of the embryo known as the tail bud. Formation, growth and differentiation of this structure are closely associated with the activity of a group of cells that derive from the axial progenitors that build the spinal cord and the muscle-skeletal case of the trunk. Gdf11 activity switches the development of these progenitors from a trunk to a tail bud mode by changing the regulatory network that controls their growth and differentiation potential. Recent work in the mouse indicates that the tail bud regulatory network relies on the interconnected activities of the Lin28/let-7 axis and the Hox13 genes. As this network is likely to be conserved in other mammals, it is possible that the final length and anatomical composition of the adult tail result from the balance between the progenitor-promoting and -repressing activities provided by those genes. This balance might also determine the functional characteristics of the adult tail. Particularly relevant is its regeneration potential, intimately linked to the spinal cord. In mammals, known for their complete inability to regenerate the tail, the spinal cord is removed from the embryonic tail at late stages of development through a Hox13-dependent mechanism. In contrast, the tail of salamanders and lizards keep a functional spinal cord that actively guides the tail's regeneration process. I will argue that the distinct molecular networks controlling tail bud development provided a collection of readily accessible gene networks that were co-opted and combined during evolution either to end the active life of those progenitors or to make them generate the wide diversity of tail shapes and sizes observed among vertebrates.
MeSH term(s)	Animals ; Biological Evolution ; Evolution, Molecular ; Gene Expression Regulation, Developmental ; Gene Regulatory Networks ; Humans ; Regeneration ; Tail/embryology ; Tail/metabolism ; Tail/physiology ; Vertebrates
Language	English
Publishing date	2019-09-26
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	1358415-7
ISSN	1420-9071 ; 1420-682X
ISSN (online)	1420-9071
ISSN	1420-682X
DOI	10.1007/s00018-019-03311-1
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Article: Of Necks, Trunks and Tails: Axial Skeletal Diversity among Vertebrates

Mallo, Moisés

Diversity. 2021 June 24, v. 13, no. 7

2021

Abstract	The axial skeleton of all vertebrates is composed of individual units known as vertebrae. Each vertebra has individual anatomical attributes, yet they can be classified in five different groups, namely cervical, thoracic, lumbar, sacral and caudal, according to shared characteristics and their association with specific body areas. Variations in vertebral number, size, morphological features and their distribution amongst the different regions of the vertebral column are a major source of the anatomical diversity observed among vertebrates. In this review I will discuss the impact of those variations on the anatomy of different vertebrate species and provide insights into the genetic origin of some remarkable morphological traits that often serve to classify phylogenetic branches or individual species, like the long trunks of snakes or the long necks of giraffes.
Keywords	phylogeny ; skeleton ; vertebrae
Language	English
Dates of publication	2021-0624
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2518137-3
ISSN	1424-2818
ISSN	1424-2818
DOI	10.3390/d13070289
Database	NAL-Catalogue (AGRICOLA)

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Article: The vertebrate tail: a gene playground for evolution

Mallo, Moisés

Cellular and molecular life sciences. 2020 Mar., v. 77, no. 6

2020

Abstract	The tail of all vertebrates, regardless of size and anatomical detail, derive from a post-anal extension of the embryo known as the tail bud. Formation, growth and differentiation of this structure are closely associated with the activity of a group of cells that derive from the axial progenitors that build the spinal cord and the muscle-skeletal case of the trunk. Gdf11 activity switches the development of these progenitors from a trunk to a tail bud mode by changing the regulatory network that controls their growth and differentiation potential. Recent work in the mouse indicates that the tail bud regulatory network relies on the interconnected activities of the Lin28/let-7 axis and the Hox13 genes. As this network is likely to be conserved in other mammals, it is possible that the final length and anatomical composition of the adult tail result from the balance between the progenitor-promoting and -repressing activities provided by those genes. This balance might also determine the functional characteristics of the adult tail. Particularly relevant is its regeneration potential, intimately linked to the spinal cord. In mammals, known for their complete inability to regenerate the tail, the spinal cord is removed from the embryonic tail at late stages of development through a Hox13-dependent mechanism. In contrast, the tail of salamanders and lizards keep a functional spinal cord that actively guides the tail’s regeneration process. I will argue that the distinct molecular networks controlling tail bud development provided a collection of readily accessible gene networks that were co-opted and combined during evolution either to end the active life of those progenitors or to make them generate the wide diversity of tail shapes and sizes observed among vertebrates.
Keywords	adults ; evolution ; genes ; mice ; spinal cord ; tail
Language	English
Dates of publication	2020-03
Size	p. 1021-1030.
Publishing place	Springer International Publishing
Document type	Article
Note	NAL-AP-2-clean ; Review
ZDB-ID	1358415-7
ISSN	1420-9071 ; 1420-682X
ISSN (online)	1420-9071
ISSN	1420-682X
DOI	10.1007/s00018-019-03311-1
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Article: Reassessing the Role of Hox Genes during Vertebrate Development and Evolution.

Mallo, Moisés

Trends in genetics : TIG

2017 Volume 34, Issue 3, Page(s) 209–217

Abstract: Since their discovery Hox genes have been at the core of the established models explaining the development and evolution of the vertebrate body plan as well as its paired appendages. Recent work brought new light to their role in the patterning processes ...

Abstract	Since their discovery Hox genes have been at the core of the established models explaining the development and evolution of the vertebrate body plan as well as its paired appendages. Recent work brought new light to their role in the patterning processes along the main body axis. These studies show that Hox genes do not control the basic layout of the vertebrate body plan but carry out region-specific patterning instructions loaded on the derivatives of axial progenitors by Hox-independent processes. Furthermore, the finding that Hox clusters are embedded in functional chromatin domains, which critically impacts their expression, has significantly altered our understanding of the mechanisms of Hox gene regulation. This new conceptual framework has broadened our understanding of both limb development and the evolution of vertebrate paired appendages.
MeSH term(s)	Animals ; Body Patterning/genetics ; Evolution, Molecular ; Gene Expression Regulation, Developmental ; Genes, Homeobox/genetics ; Limb Buds/embryology ; Limb Buds/metabolism ; Models, Genetic ; Multigene Family ; Vertebrates/embryology ; Vertebrates/genetics
Language	English
Publishing date	2017-12-18
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	619240-3
ISSN	1362-4555 ; 0168-9525 ; 0168-9479
ISSN (online)	1362-4555
ISSN	0168-9525 ; 0168-9479
DOI	10.1016/j.tig.2017.11.007
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Article ; Online: Revisiting the involvement of signaling gradients in somitogenesis.

Mallo, Moisés

The FEBS journal

2016 Volume 283, Issue 8, Page(s) 1430–1437

Abstract: During embryonic development, formation of individual vertebrae requires that the paraxial mesoderm becomes divided into regular segmental units known as somites. Somites are sequentially formed at the anterior end of the presomitic mesoderm (PSM) ... ...

Abstract	During embryonic development, formation of individual vertebrae requires that the paraxial mesoderm becomes divided into regular segmental units known as somites. Somites are sequentially formed at the anterior end of the presomitic mesoderm (PSM) resulting from functional interactions between the oscillatory activity of signals promoting segmentation and a moving wavefront of tissue competence to those signals, eventually generating a constant flow of new somites at regular intervals. According to the current model for somitogenesis, the wavefront results from the combined activity of two opposing functional gradients in the PSM involving the Fgf, Wnt and retinoic acid (RA) signaling pathways. Here, I use published data to evaluate the wavefront model. A critical analysis of those studies seems to support a role for Wnt signaling, but raise doubts regarding the extent to which Fgf and RA signaling contribute to this process.
MeSH term(s)	Animals ; Humans ; Mesoderm/metabolism ; Morphogenesis ; Signal Transduction ; Somites/physiology
Language	English
Publishing date	2016-04
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2173655-8
ISSN	1742-4658 ; 1742-464X
ISSN (online)	1742-4658
ISSN	1742-464X
DOI	10.1111/febs.13622
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Article ; Online: Regulatory changes associated with the head to trunk developmental transition.

Duarte, Patrícia / Brattig Correia, Rion / Nóvoa, Ana / Mallo, Moisés

BMC biology

2023 Volume 21, Issue 1, Page(s) 170

Abstract: Background: Development of vertebrate embryos is characterized by early formation of the anterior tissues followed by the sequential extension of the axis at their posterior end to build the trunk and tail structures, first by the activity of the ... ...

Abstract	Background: Development of vertebrate embryos is characterized by early formation of the anterior tissues followed by the sequential extension of the axis at their posterior end to build the trunk and tail structures, first by the activity of the primitive streak and then of the tail bud. Embryological, molecular and genetic data indicate that head and trunk development are significantly different, suggesting that the transition into the trunk formation stage involves major changes in regulatory gene networks. Results: We explored those regulatory changes by generating differential interaction networks and chromatin accessibility profiles from the posterior epiblast region of mouse embryos at embryonic day (E)7.5 and E8.5. We observed changes in various cell processes, including several signaling pathways, ubiquitination machinery, ion dynamics and metabolic processes involving lipids that could contribute to the functional switch in the progenitor region of the embryo. We further explored the functional impact of changes observed in Wnt signaling associated processes, revealing a switch in the functional relevance of Wnt molecule palmitoleoylation, essential during gastrulation but becoming differentially required for the control of axial extension and progenitor differentiation processes during trunk formation. We also found substantial changes in chromatin accessibility at the two developmental stages, mostly mapping to intergenic regions and presenting differential footprinting profiles to several key transcription factors, indicating a significant switch in the regulatory elements controlling head or trunk development. Those chromatin changes are largely independent of retinoic acid, despite the key role of this factor in the transition to trunk development. We also tested the functional relevance of potential enhancers identified in the accessibility assays that reproduced the expression profiles of genes involved in the transition. Deletion of these regions by genome editing had limited effect on the expression of those genes, suggesting the existence of redundant enhancers that guarantee robust expression patterns. Conclusions: This work provides a global view of the regulatory changes controlling the switch into the axial extension phase of vertebrate embryonic development. It also revealed mechanisms by which the cellular context influences the activity of regulatory factors, channeling them to implement one of several possible biological outputs.
MeSH term(s)	Transcriptome ; Torso/embryology ; Head/embryology ; Animals ; Mice ; Gene Expression Regulation, Developmental ; Protein Interaction Maps ; Wnt Signaling Pathway ; Chromatin/genetics ; Chromatin/metabolism ; Germ Layers/embryology ; Germ Layers/metabolism ; Transcription Factors/metabolism
Chemical Substances	Chromatin ; Transcription Factors
Language	English
Publishing date	2023-08-08
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2133020-7
ISSN	1741-7007 ; 1741-7007
ISSN (online)	1741-7007
ISSN	1741-7007
DOI	10.1186/s12915-023-01675-2
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Article: Patterning and Morphogenesis From Cells to Organisms: Progress, Common Principles and New Challenges.

Goryachev, Andrew B / Mallo, Moisés

Frontiers in cell and developmental biology

2020 Volume 8, Page(s) 602483

Language	English
Publishing date	2020-11-06
Publishing country	Switzerland
Document type	Editorial
ZDB-ID	2737824-X
ISSN	2296-634X
ISSN	2296-634X
DOI	10.3389/fcell.2020.602483
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Article ; Online: Assessing Myf5 and Lbx1 contribution to carapace development by reproducing their turtle-specific signatures in mouse embryos.

Tekko, Triin / Lozovska, Anastasiia / Nóvoa, Ana / Mallo, Moisés

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

2022 Volume 251, Issue 10, Page(s) 1698–1710

Abstract: Background: The turtle carapace is an evolutionary novelty resulting from changes in the processes that build ribs and their associated muscles in most tetrapod species. Turtle embryos have several unique features that might play a role in this process, ...

Abstract	Background: The turtle carapace is an evolutionary novelty resulting from changes in the processes that build ribs and their associated muscles in most tetrapod species. Turtle embryos have several unique features that might play a role in this process, including the carapacial ridge, a Myf5 gene with shorter coding region that generates an alternative splice variant lacking exon 2, and unusual expression patterns of Lbx1 and HGF. Results: We investigated these turtle-specific expression differences using genetic approaches in mouse embryos. At mid-gestation, mouse embryos producing Myf5 transcripts lacking exon 2 replicated some early properties of turtle somites, but still developed into viable and fertile mice. Extending Lbx1 expression into the hypaxial dermomyotomal lip of trunk somites to mimic the turtle Lbx1 expression pattern, produced fusions in the distal part of the ribs. Conclusions: Turtle-like Myf5 activity might generate a plastic state in developing trunk somites under which they can either enter carapace morphogenetic routes, possibly triggered by signals from the carapacial ridge, or still engage in the development of a standard tetrapod ribcage in the absence of those signals. In addition, trunk Lbx1 expression might play a later role in the formation of the lateral border of the carapace.
MeSH term(s)	Animal Shells ; Animals ; Biological Evolution ; Mice ; Myogenic Regulatory Factor 5/genetics ; Myogenic Regulatory Factor 5/metabolism ; Plastics/metabolism ; Somites ; Turtles/genetics
Chemical Substances	Myf5 protein, mouse ; Myogenic Regulatory Factor 5 ; Plastics
Language	English
Publishing date	2022-06-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1102541-4
ISSN	1097-0177 ; 1058-8388
ISSN (online)	1097-0177
ISSN	1058-8388
DOI	10.1002/dvdy.502
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