Retinoic acid-independent expression of Meis2 during autopod patterning in the developing bat and mouse limb

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dc.contributor.authorMason, Mandy K
dc.contributor.authorHockman, Dorit
dc.contributor.authorCurry, Lyle
dc.contributor.authorCunningham, Thomas J
dc.contributor.authorDuester, Gregg
dc.contributor.authorLogan, Malcolm
dc.contributor.authorJacobs, David S
dc.contributor.authorIlling, Nicola
dc.date.accessioned2021-10-08T07:04:05Z
dc.date.available2021-10-08T07:04:05Z
dc.date.issued2015
dc.description.abstractBackgroundThe bat has strikingly divergent forelimbs (long digits supporting wing membranes) and hindlimbs (short, typically free digits) due to the distinct requirements of both aerial and terrestrial locomotion. During embryonic development, the morphology of the bat forelimb deviates dramatically from the mouse and chick, offering an alternative paradigm for identifying genes that play an important role in limb patterning.ResultsUsing transcriptome analysis of developing Natal long-fingered bat (Miniopterus natalensis) fore- and hindlimbs, we demonstrate that the transcription factor Meis2 has a significantly higher expression in bat forelimb autopods compared to hindlimbs. Validation by reverse transcriptase and quantitative polymerase chain reaction (RT-qPCR) and whole mount in situ hybridisation shows that Meis2, conventionally known as a marker of the early proximal limb bud, is upregulated in the bat forelimb autopod from CS16. Meis2 expression is localised to the expanding interdigital webbing and the membranes linking the wing to the hindlimb and tail. In mice, Meis2 is also expressed in the interdigital region prior to tissue regression. This interdigital Meis2 expression is not activated by retinoic acid (RA) signalling as it is present in the retained interdigital tissue of Rdh10trex/trex mice, which lack RA. Additionally, genes encoding RA-synthesising enzymes, Rdh10 and Aldh1a2, and the RA nuclear receptor RarĪ² are robustly expressed in bat fore- and hindlimb interdigital tissues indicating that the mechanism that retains interdigital tissue in bats also occurs independently of RA signalling.ConclusionsMammalian interdigital Meis2 expression, and upregulation in the interdigital webbing of bat wings, suggests an important role for Meis2 in autopod development. Interdigital Meis2 expression is RA-independent, and retention of interdigital webbing in bat wings is not due to the suppression of RA-induced cell death. Rather, RA signalling may play a role in the thinning (rather than complete loss) of the interdigital tissue in the bat forelimb, while Meis2 may interact with other factors during both bat and mouse autopod development to maintain a pool of interdigital cells that contribute to digit patterning and growth.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0001-y) contains supplementary material, which is available to authorized users.
dc.identifier.apacitationMason, M. K., Hockman, D., Curry, L., Cunningham, T. J., Duester, G., Logan, M., ... Illing, N. (2015). Retinoic acid-independent expression of Meis2 during autopod patterning in the developing bat and mouse limb. <i>EvoDevo</i>, 6(1), 174 - 177. http://hdl.handle.net/11427/34421en_ZA
dc.identifier.chicagocitationMason, Mandy K, Dorit Hockman, Lyle Curry, Thomas J Cunningham, Gregg Duester, Malcolm Logan, David S Jacobs, and Nicola Illing "Retinoic acid-independent expression of Meis2 during autopod patterning in the developing bat and mouse limb." <i>EvoDevo</i> 6, 1. (2015): 174 - 177. http://hdl.handle.net/11427/34421en_ZA
dc.identifier.citationMason, M.K., Hockman, D., Curry, L., Cunningham, T.J., Duester, G., Logan, M., Jacobs, D.S. & Illing, N. et al. 2015. Retinoic acid-independent expression of Meis2 during autopod patterning in the developing bat and mouse limb. <i>EvoDevo.</i> 6(1):174 - 177. http://hdl.handle.net/11427/34421en_ZA
dc.identifier.issn2041-9139
dc.identifier.ris TY - Journal Article AU - Mason, Mandy K AU - Hockman, Dorit AU - Curry, Lyle AU - Cunningham, Thomas J AU - Duester, Gregg AU - Logan, Malcolm AU - Jacobs, David S AU - Illing, Nicola AB - BackgroundThe bat has strikingly divergent forelimbs (long digits supporting wing membranes) and hindlimbs (short, typically free digits) due to the distinct requirements of both aerial and terrestrial locomotion. During embryonic development, the morphology of the bat forelimb deviates dramatically from the mouse and chick, offering an alternative paradigm for identifying genes that play an important role in limb patterning.ResultsUsing transcriptome analysis of developing Natal long-fingered bat (Miniopterus natalensis) fore- and hindlimbs, we demonstrate that the transcription factor Meis2 has a significantly higher expression in bat forelimb autopods compared to hindlimbs. Validation by reverse transcriptase and quantitative polymerase chain reaction (RT-qPCR) and whole mount in situ hybridisation shows that Meis2, conventionally known as a marker of the early proximal limb bud, is upregulated in the bat forelimb autopod from CS16. Meis2 expression is localised to the expanding interdigital webbing and the membranes linking the wing to the hindlimb and tail. In mice, Meis2 is also expressed in the interdigital region prior to tissue regression. This interdigital Meis2 expression is not activated by retinoic acid (RA) signalling as it is present in the retained interdigital tissue of Rdh10trex/trex mice, which lack RA. Additionally, genes encoding RA-synthesising enzymes, Rdh10 and Aldh1a2, and the RA nuclear receptor RarĪ² are robustly expressed in bat fore- and hindlimb interdigital tissues indicating that the mechanism that retains interdigital tissue in bats also occurs independently of RA signalling.ConclusionsMammalian interdigital Meis2 expression, and upregulation in the interdigital webbing of bat wings, suggests an important role for Meis2 in autopod development. Interdigital Meis2 expression is RA-independent, and retention of interdigital webbing in bat wings is not due to the suppression of RA-induced cell death. Rather, RA signalling may play a role in the thinning (rather than complete loss) of the interdigital tissue in the bat forelimb, while Meis2 may interact with other factors during both bat and mouse autopod development to maintain a pool of interdigital cells that contribute to digit patterning and growth.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0001-y) contains supplementary material, which is available to authorized users. DA - 2015 DB - OpenUCT DP - University of Cape Town IS - 1 J1 - EvoDevo LK - https://open.uct.ac.za PY - 2015 SM - 2041-9139 T1 - Retinoic acid-independent expression of Meis2 during autopod patterning in the developing bat and mouse limb TI - Retinoic acid-independent expression of Meis2 during autopod patterning in the developing bat and mouse limb UR - http://hdl.handle.net/11427/34421 ER - en_ZA
dc.identifier.urihttp://hdl.handle.net/11427/34421
dc.identifier.vancouvercitationMason MK, Hockman D, Curry L, Cunningham TJ, Duester G, Logan M, et al. Retinoic acid-independent expression of Meis2 during autopod patterning in the developing bat and mouse limb. EvoDevo. 2015;6(1):174 - 177. http://hdl.handle.net/11427/34421.en_ZA
dc.language.isoeng
dc.publisher.departmentDepartment of Molecular and Cell Biology
dc.publisher.facultyFaculty of Science
dc.sourceEvoDevo
dc.source.journalissue1
dc.source.journalvolume6
dc.source.pagination174 - 177
dc.source.urihttps://dx.doi.org/10.1186/s13227-015-0001-y
dc.subject.otherRarb
dc.subject.otherMeis2
dc.subject.otherMela
dc.subject.otherRdh10
dc.subject.otherTissues
dc.subject.otherExtremities
dc.subject.otherCells
dc.subject.otherWing
dc.subject.otherForelimb
dc.subject.otherMembranes
dc.subject.otherHindlimb
dc.subject.otherTail
dc.subject.otherLimb Buds
dc.subject.otherReceptors, Cytoplasmic and Nuclear
dc.subject.otherEnzymes
dc.subject.otherDNA-Directed RNA Polymerases
dc.subject.otherTretinoin
dc.subject.otherTranscription Factors
dc.subject.otherLocomotion
dc.subject.otherGrowth
dc.subject.otherGenes
dc.subject.otherCell Death
dc.subject.otherGenes, ras
dc.subject.otherEmbryonic Development
dc.subject.otherGene Expression Profiling
dc.subject.otherPolymerase Chain Reaction
dc.subject.otherGallus gallus
dc.titleRetinoic acid-independent expression of Meis2 during autopod patterning in the developing bat and mouse limb
dc.typeJournal Article
uct.type.publicationResearch
uct.type.resourceJournal Article
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