Literature DB >> 17015842

Interdigital webbing retention in bat wings illustrates genetic changes underlying amniote limb diversification.

Scott D Weatherbee1, Richard R Behringer, John J Rasweiler, Lee A Niswander.   

Abstract

Developmentally regulated programmed cell death sculpts the limbs and other embryonic organs in vertebrates. One intriguing example of species-specific differences in apoptotic extent is observed in the tissue between the digits. In chicks and mice, bone morphogenetic proteins (Bmps) trigger apoptosis of the interdigital mesenchyme, leading to freed digits, whereas in ducks, Bmp antagonists inhibit the apoptotic program, resulting in webbed feet. Here, we show that the phyllostomid bat Carollia perspicillata utilizes a distinct mechanism for maintaining interdigit tissue. We find that bat forelimb and hindlimb interdigital tissues express Bmp signaling components but that only bat hindlimbs undergo interdigital apoptosis. Strikingly, the retention of interdigital webbing in the bat forelimb is correlated with a unique pattern of Fgf8 expression in addition to the Bmp inhibitor Gremlin. By using a functional assay, we show that maintenance of interdigit tissue in the bat wing depends on the combined effects of high levels of Fgf signaling and inhibition of Bmp signaling. Our data also indicate that although there is not a conserved mechanism for maintaining interdigit tissue across amniotes, the expression in the bat forelimb interdigits of Gremlin and Fgf8 suggests that these key molecular changes contributed to the evolution of the bat wing.

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Year:  2006        PMID: 17015842      PMCID: PMC1622783          DOI: 10.1073/pnas.0604934103

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  28 in total

Review 1.  Bone morphogenetic proteins regulate interdigital cell death in the avian embryo.

Authors:  R Merino; Y Gañán; D Macias; J Rodríguez-León; J M Hurle
Journal:  Ann N Y Acad Sci       Date:  1999       Impact factor: 5.691

2.  Expression patterns of Fgf-8 during development and limb regeneration of the axolotl.

Authors:  M J Han; J Y An; W S Kim
Journal:  Dev Dyn       Date:  2001-01       Impact factor: 3.780

3.  Development of bat flight: morphologic and molecular evolution of bat wing digits.

Authors:  Karen E Sears; Richard R Behringer; John J Rasweiler; Lee A Niswander
Journal:  Proc Natl Acad Sci U S A       Date:  2006-04-17       Impact factor: 11.205

4.  Function of BMPs in the apical ectoderm of the developing mouse limb.

Authors:  Chi-Kuang Leo Wang; Minoru Omi; Deborah Ferrari; Hsu-Chen Cheng; Gail Lizarraga; Hsian-Jean Chin; William B Upholt; Caroline N Dealy; Robert A Kosher
Journal:  Dev Biol       Date:  2004-05-01       Impact factor: 3.582

5.  A new role for BMP5 during limb development acting through the synergic activation of Smad and MAPK pathways.

Authors:  V Zuzarte-Luís; J A Montero; J Rodriguez-León; R Merino; J C Rodríguez-Rey; J M Hurlé
Journal:  Dev Biol       Date:  2004-08-01       Impact factor: 3.582

6.  Apert syndrome results from localized mutations of FGFR2 and is allelic with Crouzon syndrome.

Authors:  A O Wilkie; S F Slaney; M Oldridge; M D Poole; G J Ashworth; A D Hockley; R D Hayward; D J David; L J Pulleyn; P Rutland
Journal:  Nat Genet       Date:  1995-02       Impact factor: 38.330

7.  Cloning and characterization of an androgen-induced growth factor essential for the androgen-dependent growth of mouse mammary carcinoma cells.

Authors:  A Tanaka; K Miyamoto; N Minamino; M Takeda; B Sato; H Matsuo; K Matsumoto
Journal:  Proc Natl Acad Sci U S A       Date:  1992-10-01       Impact factor: 11.205

8.  Chromosomal localization of seven members of the murine TGF-beta superfamily suggests close linkage to several morphogenetic mutant loci.

Authors:  M E Dickinson; M S Kobrin; C M Silan; D M Kingsley; M J Justice; D A Miller; J D Ceci; L F Lock; A Lee; A M Buchberg
Journal:  Genomics       Date:  1990-03       Impact factor: 5.736

9.  In vivo evidence that BMP signaling is necessary for apoptosis in the mouse limb.

Authors:  Udayan Guha; William A Gomes; Tatsuya Kobayashi; Richard G Pestell; John A Kessler
Journal:  Dev Biol       Date:  2002-09-01       Impact factor: 3.582

10.  The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo.

Authors:  P H Crossley; G R Martin
Journal:  Development       Date:  1995-02       Impact factor: 6.868

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  43 in total

Review 1.  Cortical evolution in mammals: the bane and beauty of phenotypic variability.

Authors:  Leah A Krubitzer; Adele M H Seelke
Journal:  Proc Natl Acad Sci U S A       Date:  2012-06-20       Impact factor: 11.205

Review 2.  Development and embryonic staging in non-model organisms: the case of an afrotherian mammal.

Authors:  Ingmar Werneburg; Athanasia C Tzika; Lionel Hautier; Robert J Asher; Michel C Milinkovitch; Marcelo R Sánchez-Villagra
Journal:  J Anat       Date:  2012-04-27       Impact factor: 2.610

3.  Circumventing the polydactyly 'constraint': the mole's 'thumb'.

Authors:  Christian Mitgutsch; Michael K Richardson; Rafael Jiménez; José E Martin; Peter Kondrashov; Merijn A G de Bakker; Marcelo R Sánchez-Villagra
Journal:  Biol Lett       Date:  2011-07-13       Impact factor: 3.703

4.  Organization of the primary somatosensory cortex and wing representation in the Big Brown Bat, Eptesicus fuscus.

Authors:  M Chadha; C F Moss; S J Sterbing-D'Angelo
Journal:  J Comp Physiol A Neuroethol Sens Neural Behav Physiol       Date:  2010-09-29       Impact factor: 1.836

5.  Between "design" and "bricolage": genetic networks, levels of selection, and adaptive evolution.

Authors:  Adam S Wilkins
Journal:  Proc Natl Acad Sci U S A       Date:  2007-05-09       Impact factor: 11.205

6.  Developmental processes underlying the evolution of a derived foot morphology in salamanders.

Authors:  Martin Jaekel; David B Wake
Journal:  Proc Natl Acad Sci U S A       Date:  2007-12-10       Impact factor: 11.205

7.  Somatosensory substrates of flight control in bats.

Authors:  Kara L Marshall; Mohit Chadha; Laura A deSouza; Susanne J Sterbing-D'Angelo; Cynthia F Moss; Ellen A Lumpkin
Journal:  Cell Rep       Date:  2015-04-30       Impact factor: 9.423

8.  The developmental basis of bat wing muscle.

Authors:  Masayoshi Tokita; Takaaki Abe; Kazuo Suzuki
Journal:  Nat Commun       Date:  2012       Impact factor: 14.919

9.  A second wave of Sonic hedgehog expression during the development of the bat limb.

Authors:  Dorit Hockman; Chris J Cretekos; Mandy K Mason; Richard R Behringer; David S Jacobs; Nicola Illing
Journal:  Proc Natl Acad Sci U S A       Date:  2008-10-28       Impact factor: 11.205

10.  BMP-2 functions independently of SHH signaling and triggers cell condensation and apoptosis in regenerating axolotl limbs.

Authors:  Jean-Charles Guimond; Mathieu Lévesque; Pierre-Luc Michaud; Jérémie Berdugo; Kenneth Finnson; Anie Philip; Stéphane Roy
Journal:  BMC Dev Biol       Date:  2010-02-12       Impact factor: 1.978

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