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Article ; Online: The limb dorsoventral axis: Lmx1b's role in development, pathology, evolution, and regeneration.

Castilla-Ibeas, Alejandro / Zdral, Sofía / Oberg, Kerby C / Ros, Marian A

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

2024

Abstract: The limb anatomy displays well-defined dorsal and ventral compartments, housing extensor, and flexor muscles, which play a crucial role in facilitating limb locomotion and manipulation. Despite its importance, the study of limb dorsoventral patterning ... ...

Abstract	The limb anatomy displays well-defined dorsal and ventral compartments, housing extensor, and flexor muscles, which play a crucial role in facilitating limb locomotion and manipulation. Despite its importance, the study of limb dorsoventral patterning has been relatively neglected compared to the other two axes leaving many crucial questions about the genes and developmental processes implicated unanswered. This review offers a thorough overview of the current understanding of limb dorsoventral patterning, synthesizing classical literature with recent research. It covers the specification of dorsal fate in the limb mesoderm and its subsequent translation into dorsal morphologies-a process directed by the transcription factor Lmx1b. We also discuss the potential role of dorsoventral patterning in the evolution of paired appendages and delve into the involvement of LMX1B in Nail-Patella syndrome, discussing the molecular and genetic aspects underlying this condition. Finally, the potential role of dorsoventral polarity in digit tip regeneration, a prominent instance of multi-tissue regeneration in mammals is also considered. We anticipate that this review will renew interest in a process that is critical to limb function and evolutionary adaptations but has nonetheless been overlooked.
Language	English
Publishing date	2024-01-30
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	1102541-4
ISSN	1097-0177 ; 1058-8388
ISSN (online)	1097-0177
ISSN	1058-8388
DOI	10.1002/dvdy.695
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Article ; Online: HOX13 proteins: the molecular switcher in Hoxd bimodal regulation.

Ros, Marian A

Genes & development

2016 Volume 30, Issue 10, Page(s) 1135–1137

Abstract: The striking correlation between the genomic arrangement of Hox genes and their temporal and spatial pattern of expression during embryonic development has been a source of fascination since its discovery. This correspondence has been used as a ... ...

Abstract	The striking correlation between the genomic arrangement of Hox genes and their temporal and spatial pattern of expression during embryonic development has been a source of fascination since its discovery. This correspondence has been used as a privileged example in the investigation of the connection between genomic architecture and function. In this issue of Genes & Development, Beccari and colleagues (pp. 1172-1186) make a big step forward in understanding Hox gene regulation during limb development by showing the pivotal role of HOXA13 and HOXD13 proteins in the transition from a proximal to a distal type of Hoxd transcriptional regulation.
MeSH term(s)	Embryonic Development ; Extremities/embryology ; Gene Expression Regulation, Developmental ; Genes, Homeobox ; Homeodomain Proteins/genetics ; Transcription Factors/genetics
Chemical Substances	Homeodomain Proteins ; Transcription Factors
Language	English
Publishing date	2016--15
Publishing country	United States
Document type	Journal Article ; Comment
ZDB-ID	806684-x
ISSN	1549-5477 ; 0890-9369
ISSN (online)	1549-5477
ISSN	0890-9369
DOI	10.1101/gad.283598.116
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Article ; Online: Ectoderm-mesoderm crosstalk in the embryonic limb: The role of fibroblast growth factor signaling.

Mariani, Francesca V / Fernandez-Teran, Marian / Ros, Maria A

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

2017 Volume 246, Issue 4, Page(s) 208–216

Abstract: In this commentary we focus on the function of FGFs during limb development and morphogenesis. Our goal is to understand, interpret and, when possible, reconcile the interesting findings and conflicting results that remain unexplained. For example, the ... ...

Abstract	In this commentary we focus on the function of FGFs during limb development and morphogenesis. Our goal is to understand, interpret and, when possible, reconcile the interesting findings and conflicting results that remain unexplained. For example, the cell death pattern observed after surgical removal of the AER versus genetic removal of the AER-Fgfs is strikingly different and the field is at an impasse with regard to an explanation. We also discuss the idea that AER function may involve signaling components in addition to the AER-FGFs and that signaling from the non-AER ectoderm may also have a significant contribution. We hope that a re-evaluation of current studies and a discussion of outstanding questions will motivate new experiments, especially considering the availability of new technologies, that will fuel further progress toward understanding the intricate ectoderm-to-mesoderm crosstalk during limb development. Developmental Dynamics 246:208-216, 2017. © 2016 Wiley Periodicals, Inc.
MeSH term(s)	Animals ; Chick Embryo ; Ectoderm/embryology ; Extremities/embryology ; Fibroblast Growth Factors/metabolism ; Fibroblast Growth Factors/physiology ; Mesoderm/enzymology ; Mice ; Receptor Cross-Talk ; Signal Transduction
Chemical Substances	Fibroblast Growth Factors (62031-54-3)
Language	English
Publishing date	2017-02-06
Publishing country	United States
Document type	Journal Article ; Review ; 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.24480
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Article ; Online: Evidence that the limb bud ectoderm is required for survival of the underlying mesoderm.

Fernandez-Teran, Marian / Ros, Maria A / Mariani, Francesca V

Developmental biology

2013 Volume 381, Issue 2, Page(s) 341–352

Abstract: The limb forms from a bud of mesoderm encased in a hull of ectoderm that grows out from the flank of the embryo. Coordinated signaling between the limb mesoderm and ectoderm is critical for normal limb outgrowth and patterning. The apical ectodermal ... ...

Abstract	The limb forms from a bud of mesoderm encased in a hull of ectoderm that grows out from the flank of the embryo. Coordinated signaling between the limb mesoderm and ectoderm is critical for normal limb outgrowth and patterning. The apical ectodermal ridge (AER), found at the distal tip, is a rich source of signaling molecules and has been proposed to specify distal structures and maintain the survival of cells in the underlying distal mesoderm. The dorsal and ventral non-AER ectoderm is also a source of signaling molecules and is important for dorsal-ventral patterning of the limb bud. Here we determine if this ectoderm provides cell survival signals by surgically removing the dorsal or ventral ectoderm during early chicken limb bud development and assaying for programmed cell death. We find that, similar to the AER, removal of the dorsal or ventral non-AER ectoderm results in massive cell death in the underlying mesoderm. In addition, although a re-epithelialization occurs, we find perturbations in the timing of Shh expression and, for the case of the dorsal ectoderm removal, defects in soft tissue and skeletal development along the proximal-distal axis. Furthermore, ectoderm substitution experiments show that the survival signal produced by the dorsal limb ectoderm is specific. Thus, our results argue that the non-AER ectoderm, like the AER, provides a specific survival signal to the underlying mesoderm that is necessary for normal limb development and conclusions drawn from experiments in which the non-AER ectoderm is removed, need to take into consideration this observation.
MeSH term(s)	Animals ; Animals, Genetically Modified/growth & development ; Animals, Genetically Modified/metabolism ; Body Patterning ; Cell Death ; Cell Survival ; Chick Embryo ; Chickens/growth & development ; Chickens/metabolism ; Ectoderm/cytology ; Ectoderm/metabolism ; Fibroblast Growth Factor 8/genetics ; Fibroblast Growth Factor 8/metabolism ; Gene Expression Regulation, Developmental ; Hedgehog Proteins/genetics ; Hedgehog Proteins/metabolism ; Limb Buds/cytology ; Limb Buds/embryology ; Limb Buds/metabolism ; Mesoderm/cytology ; Mesoderm/metabolism ; Time Factors ; Wings, Animal/embryology
Chemical Substances	Hedgehog Proteins ; Fibroblast Growth Factor 8 (148997-75-5)
Language	English
Publishing date	2013-07-09
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2013.06.032
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Article ; Online: An intrinsic cell cycle timer terminates limb bud outgrowth.

Pickering, Joseph / Rich, Constance A / Stainton, Holly / Aceituno, Cristina / Chinnaiya, Kavitha / Saiz-Lopez, Patricia / Ros, Marian A / Towers, Matthew

eLife

2018 Volume 7

Abstract: The longstanding view of how proliferative outgrowth terminates following the patterning phase of limb development involves the breakdown of reciprocal extrinsic signalling between the distal mesenchyme and the overlying epithelium (e-m signalling). ... ...

Abstract	The longstanding view of how proliferative outgrowth terminates following the patterning phase of limb development involves the breakdown of reciprocal extrinsic signalling between the distal mesenchyme and the overlying epithelium (e-m signalling). However, by grafting distal mesenchyme cells from late stage chick wing buds to the epithelial environment of younger wing buds, we show that this mechanism is not required. RNA sequencing reveals that distal mesenchyme cells complete proliferative outgrowth by an intrinsic cell cycle timer in the presence of e-m signalling. In this process, e-m signalling is required permissively to allow the intrinsic cell cycle timer to run its course. We provide evidence that a temporal switch from BMP antagonism to BMP signalling controls the intrinsic cell cycle timer during limb outgrowth. Our findings have general implications for other patterning systems in which extrinsic signals and intrinsic timers are integrated.
MeSH term(s)	Animals ; Cell Cycle/genetics ; Cell Proliferation/genetics ; Chickens ; Epithelium/growth & development ; Extremities/growth & development ; Gene Expression Regulation, Developmental ; Limb Buds/growth & development ; Limb Buds/metabolism ; Mesoderm/growth & development ; Organogenesis/genetics ; Sequence Analysis, RNA ; Signal Transduction/genetics
Language	English
Publishing date	2018-09-03
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.37429
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Article ; Online: An intrinsic cell cycle timer terminates limb bud outgrowth

Joseph Pickering / Constance A Rich / Holly Stainton / Cristina Aceituno / Kavitha Chinnaiya / Patricia Saiz-Lopez / Marian A Ros / Matthew Towers

eLife, Vol

2018 Volume 7

Abstract	The longstanding view of how proliferative outgrowth terminates following the patterning phase of limb development involves the breakdown of reciprocal extrinsic signalling between the distal mesenchyme and the overlying epithelium (e-m signalling). However, by grafting distal mesenchyme cells from late stage chick wing buds to the epithelial environment of younger wing buds, we show that this mechanism is not required. RNA sequencing reveals that distal mesenchyme cells complete proliferative outgrowth by an intrinsic cell cycle timer in the presence of e-m signalling. In this process, e-m signalling is required permissively to allow the intrinsic cell cycle timer to run its course. We provide evidence that a temporal switch from BMP antagonism to BMP signalling controls the intrinsic cell cycle timer during limb outgrowth. Our findings have general implications for other patterning systems in which extrinsic signals and intrinsic timers are integrated.
Keywords	limb ; timing ; growth ; Medicine ; R ; Science ; Q ; Biology (General) ; QH301-705.5
Language	English
Publishing date	2018-09-01T00:00:00Z
Publisher	eLife Sciences Publications Ltd
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Direct reprogramming of non-limb fibroblasts to cells with properties of limb progenitors.

Atsuta, Yuji / Lee, ChangHee / Rodrigues, Alan R / Colle, Charlotte / Tomizawa, Reiko R / Lujan, Ernesto G / Tschopp, Patrick / Galan, Laura / Zhu, Meng / Gorham, Joshua M / Vannier, Jean-Pierre / Seidman, Christine E / Seidman, Jonathan G / Ros, Marian A / Pourquié, Olivier / Tabin, Clifford J

Developmental cell

2024 Volume 59, Issue 3, Page(s) 415–430.e8

Abstract: The early limb bud consists of mesenchymal limb progenitors derived from the lateral plate mesoderm (LPM). The LPM also gives rise to the mesodermal components of the flank and neck. However, the cells at these other levels cannot produce the variety of ... ...

Abstract	The early limb bud consists of mesenchymal limb progenitors derived from the lateral plate mesoderm (LPM). The LPM also gives rise to the mesodermal components of the flank and neck. However, the cells at these other levels cannot produce the variety of cell types found in the limb. Taking advantage of a direct reprogramming approach, we find a set of factors (Prdm16, Zbtb16, and Lin28a) normally expressed in the early limb bud and capable of imparting limb progenitor-like properties to mouse non-limb fibroblasts. The reprogrammed cells show similar gene expression profiles and can differentiate into similar cell types as endogenous limb progenitors. The further addition of Lin41 potentiates the proliferation of the reprogrammed cells. These results suggest that these same four factors may play pivotal roles in the specification of endogenous limb progenitors.
MeSH term(s)	Mice ; Animals ; Extremities ; Proteins/metabolism ; Fibroblasts ; Mesoderm/metabolism ; Limb Buds
Chemical Substances	Proteins
Language	English
Publishing date	2024-02-04
Publishing country	United States
Document type	Journal Article
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2023.12.010
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Article ; Online: Failure of digit tip regeneration in the absence of Lmx1b suggests Lmx1b functions disparate from dorsoventral polarity.

Castilla-Ibeas, Alejandro / Zdral, Sofía / Galán, Laura / Haro, Endika / Allou, Lila / Campa, Víctor M / Icardo, Jose M / Mundlos, Stefan / Oberg, Kerby C / Ros, Marian A

Cell reports

2023 Volume 42, Issue 1, Page(s) 111975

Abstract: Mammalian digit tip regeneration is linked to the presence of nail tissue, but a nail-explicit model is missing. Here, we report that nail-less double-ventral digits of ΔLARM1/2 mutants that lack limb-specific Lmx1b enhancers fail to regenerate. To ... ...

Abstract	Mammalian digit tip regeneration is linked to the presence of nail tissue, but a nail-explicit model is missing. Here, we report that nail-less double-ventral digits of ΔLARM1/2 mutants that lack limb-specific Lmx1b enhancers fail to regenerate. To separate the nail's effect from the lack of dorsoventral (DV) polarity, we also interrogate double-dorsal double-nail digits and show that they regenerate. Thus, DV polarity is not a prerequisite for regeneration, and the nail requirement is supported. Transcriptomic comparison between wild-type and non-regenerative ΔLARM1/2 mutant blastemas reveals differential upregulation of vascularization and connective tissue functional signatures in wild type versus upregulation of inflammation in the mutant. These results, together with the finding of Lmx1b expression in the postnatal dorsal dermis underneath the nail and uniformly in the regenerative blastema, open the possibility of additional Lmx1b roles in digit tip regeneration, in addition to the indirect effect of mediating the formation of the nail.
MeSH term(s)	Animals ; Extremities ; Gene Expression Profiling ; Mammals ; Transcriptome ; LIM-Homeodomain Proteins/metabolism
Chemical Substances	LIM homeobox transcription factor 1 beta ; LIM-Homeodomain Proteins
Language	English
Publishing date	2023-01-14
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.2022.111975
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Article ; Online: Personal autonomy and self-determination are crucial for professionalism in healthcare.

Organ, Jason M / Smith, Heather F / Trainor, Paul A / Allen, Kari / Balta, Joy Y / Beresheim, Amy C / Brewer-Deluce, Danielle / Brown, Kirsten M / Burrows, Anne M / Byers, Kelsey T / Byram, Jessica N / Cale, Andrew S / Carroll, Melissa A / Champney, Thomas / Cornwall, Jon / Dayal, Manisha R / DeLeon, Valerie B / Dunnwald, Martine / Ferrigno, Christopher /

Finn, Gabrielle M / Fox, Glenn M / Geller, Pamela L / Guttmann, Geoffrey D / Harper, Noah / Harrell, Kelly M / Hartstone-Rose, Adam / Hildebrandt, Sabine / Hortsch, Michael / Jackson, Jon / Johnson, Laura E / Lohman Bonfiglio, Chelsea M / McCumber, Travis L / Menegaz, Rachel A / Mussell, Jason C / O'Loughlin, Valerie D / Otobo, Tarimobo M / Oyedele, Olusegun / Pascoe, Michael A / Person, Dianne / Reidenberg, Joy S / Robinson, Rhiannon E / Rogers, Kem A / Ros, Marian A / Ross, Callum F / Sanders, Kat A / Schmitt, Brandi / Schoenwolf, Gary C / Smith, Theodore C / Smith, Timothy D / Sumner, D Rick / Taylor, Andrea B / Taylor, Meredith J / Teaford, Mark F / Topp, Kimberly S / Willmore, Katherine E / Wisco, Jonathan J / Yang, Jian / Zumwalt, Ann C

Anatomical sciences education

2023 Volume 16, Issue 4, Page(s) 571–573

MeSH term(s)	Humans ; Personal Autonomy ; Professionalism ; Anatomy/education ; Physicians ; Attitude of Health Personnel
Language	English
Publishing date	2023-05-09
Publishing country	United States
Document type	Editorial
ZDB-ID	2483491-9
ISSN	1935-9780 ; 1935-9772
ISSN (online)	1935-9780
ISSN	1935-9772
DOI	10.1002/ase.2278
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Article ; Online: Time-sequenced transcriptomes of developing distal mouse limb buds: A comparative tissue layer analysis.

Fernandez-Guerrero, Marc / Zdral, Sofia / Castilla-Ibeas, Alejandro / Lopez-Delisle, Lucille / Duboule, Denis / Ros, Marian A

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

2021 Volume 251, Issue 9, Page(s) 1550–1575

Abstract: Background: The development of the amniote limb has been an important model system to study patterning mechanisms and morphogenesis. For proper growth and patterning, it requires the interaction between the distal sub-apical mesenchyme and the apical ... ...

Abstract	Background: The development of the amniote limb has been an important model system to study patterning mechanisms and morphogenesis. For proper growth and patterning, it requires the interaction between the distal sub-apical mesenchyme and the apical ectodermal ridge (AER) that involve the separate implementation of coordinated and tissue-specific genetic programs. Results: Here, we produce and analyze the transcriptomes of both distal limb mesenchymal progenitors and the overlying ectodermal cells, following time-coursed dissections that cover from limb bud initiation to fully patterned limbs. The comparison of transcriptomes within each layer as well as between layers over time, allowed the identification of specific transcriptional signatures for each of the developmental stages. Special attention was given to the identification of genes whose transcription dynamics suggest a previously unnoticed role in the context of limb development and also to signaling pathways enriched between layers. Conclusion: We interpret the transcriptomic data in light of the known development pattern and we conclude that a major transcriptional transition occurs in distal limb buds between E9.5 and E10.5, coincident with the switch from an early phase continuation of the signature of trunk progenitors, related to the initial proximo distal specification, to a late intrinsic phase of development.
MeSH term(s)	Animals ; Ectoderm/metabolism ; Extremities ; Gene Expression Regulation, Developmental ; Limb Buds/metabolism ; Mesoderm ; Mice ; Signal Transduction ; Transcriptome
Language	English
Publishing date	2021-07-17
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.394
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