Comparative analysis of ear-hole closure identifies epimorphic regeneration as a discrete trait in mammals

Thomas R. Gawriluk; Jennifer Simkin; Katherine L. Thompson; Shishir K. Biswas; Zak Clare-Salzler; John M. Kimani; Stephen G. Kiama; Jeramiah J. Smith; Vanessa O. Ezenwa; Ashley W. Seifert

doi:10.1038/ncomms11164

Comparative analysis of ear-hole closure identifies epimorphic regeneration as a discrete trait in mammals

Thomas R. Gawriluk
, Jennifer Simkin
, Katherine L. Thompson
, Shishir K. Biswas
, Zak Clare-Salzler
, John M. Kimani
, Stephen G. Kiama
, Jeramiah J. Smith
, Vanessa O. Ezenwa
, Ashley W. Seifert

Producción científica: Article › revisión exhaustiva

137 Citas (Scopus)

Resumen

Why mammals have poor regenerative ability has remained a long-standing question in biology. In regenerating vertebrates, injury can induce a process known as epimorphic regeneration to replace damaged structures. Using a 4-mm ear punch assay across multiple mammalian species, here we show that several Acomys spp. (spiny mice) and Oryctolagus cuniculus completely regenerate tissue, whereas other rodents including MRL/MpJ 'healer' mice heal similar injuries by scarring. We demonstrate ear-hole closure is independent of ear size, and closure rate can be modelled with a cubic function. Cellular and genetic analyses reveal that injury induces blastema formation in Acomys cahirinus. Despite cell cycle re-entry in Mus musculus and A. cahirinus, efficient cell cycle progression and proliferation only occurs in spiny mice. Together, our data unite blastema-mediated regeneration in spiny mice with regeneration in other vertebrates such as salamanders, newts and zebrafish, where all healthy adults regenerate in response to injury.

Idioma original	English
Número de artículo	11164
Publicación	Nature Communications
Volumen	7
DOI	https://doi.org/10.1038/ncomms11164
Estado	Published - abr 25 2016

Nota bibliográfica

Funding Information:
We thank Matt Snider, Zara Ashraf, Malik Guidry, John Ewoi and Stanley Marete for help with live-trapping, animal care and data collection. We thank Tiberius for reliable transport and Edward Scott for the gift of MRL/MpJ mice. We also thank Peter Jessel for kindly allowing us access to his property and for fruitful discussions. Funding for this work was provided by the National Science Foundation (NSF) and the Office for International Science and Engineering (OISE) to A.W.S. (IOS-1353713) and V.O.E. (IOS-1353857). Additional funding was provided to A.W.S. by the University of Kentucky.

Financiación

We thank Matt Snider, Zara Ashraf, Malik Guidry, John Ewoi and Stanley Marete for help with live-trapping, animal care and data collection. We thank Tiberius for reliable transport and Edward Scott for the gift of MRL/MpJ mice. We also thank Peter Jessel for kindly allowing us access to his property and for fruitful discussions. Funding for this work was provided by the National Science Foundation (NSF) and the Office for International Science and Engineering (OISE) to A.W.S. (IOS-1353713) and V.O.E. (IOS-1353857). Additional funding was provided to A.W.S. by the University of Kentucky.

Financiadores	Número del financiador
University of Kentucky
National Science Foundation Arctic Social Science Program	1353713, IOS-1353857
Office of International Science and Engineering	IOS-1353713, IOS-1353857

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General
General Physics and Astronomy

Acceder al documento

10.1038/ncomms11164

Otros archivos y enlaces

Citar esto

@article{d6cebdecbb0341119c717685608db797,

title = "Comparative analysis of ear-hole closure identifies epimorphic regeneration as a discrete trait in mammals",

abstract = "Why mammals have poor regenerative ability has remained a long-standing question in biology. In regenerating vertebrates, injury can induce a process known as epimorphic regeneration to replace damaged structures. Using a 4-mm ear punch assay across multiple mammalian species, here we show that several Acomys spp. (spiny mice) and Oryctolagus cuniculus completely regenerate tissue, whereas other rodents including MRL/MpJ 'healer' mice heal similar injuries by scarring. We demonstrate ear-hole closure is independent of ear size, and closure rate can be modelled with a cubic function. Cellular and genetic analyses reveal that injury induces blastema formation in Acomys cahirinus. Despite cell cycle re-entry in Mus musculus and A. cahirinus, efficient cell cycle progression and proliferation only occurs in spiny mice. Together, our data unite blastema-mediated regeneration in spiny mice with regeneration in other vertebrates such as salamanders, newts and zebrafish, where all healthy adults regenerate in response to injury.",

author = "Gawriluk, \{Thomas R.\} and Jennifer Simkin and Thompson, \{Katherine L.\} and Biswas, \{Shishir K.\} and Zak Clare-Salzler and Kimani, \{John M.\} and Kiama, \{Stephen G.\} and Smith, \{Jeramiah J.\} and Ezenwa, \{Vanessa O.\} and Seifert, \{Ashley W.\}",

note = "Funding Information: We thank Matt Snider, Zara Ashraf, Malik Guidry, John Ewoi and Stanley Marete for help with live-trapping, animal care and data collection. We thank Tiberius for reliable transport and Edward Scott for the gift of MRL/MpJ mice. We also thank Peter Jessel for kindly allowing us access to his property and for fruitful discussions. Funding for this work was provided by the National Science Foundation (NSF) and the Office for International Science and Engineering (OISE) to A.W.S. (IOS-1353713) and V.O.E. (IOS-1353857). Additional funding was provided to A.W.S. by the University of Kentucky.",

year = "2016",

month = apr,

day = "25",

doi = "10.1038/ncomms11164",

language = "English",

volume = "7",

}

TY - JOUR

T1 - Comparative analysis of ear-hole closure identifies epimorphic regeneration as a discrete trait in mammals

AU - Gawriluk, Thomas R.

AU - Simkin, Jennifer

AU - Thompson, Katherine L.

AU - Biswas, Shishir K.

AU - Clare-Salzler, Zak

AU - Kimani, John M.

AU - Kiama, Stephen G.

AU - Smith, Jeramiah J.

AU - Ezenwa, Vanessa O.

AU - Seifert, Ashley W.

N1 - Funding Information: We thank Matt Snider, Zara Ashraf, Malik Guidry, John Ewoi and Stanley Marete for help with live-trapping, animal care and data collection. We thank Tiberius for reliable transport and Edward Scott for the gift of MRL/MpJ mice. We also thank Peter Jessel for kindly allowing us access to his property and for fruitful discussions. Funding for this work was provided by the National Science Foundation (NSF) and the Office for International Science and Engineering (OISE) to A.W.S. (IOS-1353713) and V.O.E. (IOS-1353857). Additional funding was provided to A.W.S. by the University of Kentucky.

PY - 2016/4/25

Y1 - 2016/4/25

N2 - Why mammals have poor regenerative ability has remained a long-standing question in biology. In regenerating vertebrates, injury can induce a process known as epimorphic regeneration to replace damaged structures. Using a 4-mm ear punch assay across multiple mammalian species, here we show that several Acomys spp. (spiny mice) and Oryctolagus cuniculus completely regenerate tissue, whereas other rodents including MRL/MpJ 'healer' mice heal similar injuries by scarring. We demonstrate ear-hole closure is independent of ear size, and closure rate can be modelled with a cubic function. Cellular and genetic analyses reveal that injury induces blastema formation in Acomys cahirinus. Despite cell cycle re-entry in Mus musculus and A. cahirinus, efficient cell cycle progression and proliferation only occurs in spiny mice. Together, our data unite blastema-mediated regeneration in spiny mice with regeneration in other vertebrates such as salamanders, newts and zebrafish, where all healthy adults regenerate in response to injury.

AB - Why mammals have poor regenerative ability has remained a long-standing question in biology. In regenerating vertebrates, injury can induce a process known as epimorphic regeneration to replace damaged structures. Using a 4-mm ear punch assay across multiple mammalian species, here we show that several Acomys spp. (spiny mice) and Oryctolagus cuniculus completely regenerate tissue, whereas other rodents including MRL/MpJ 'healer' mice heal similar injuries by scarring. We demonstrate ear-hole closure is independent of ear size, and closure rate can be modelled with a cubic function. Cellular and genetic analyses reveal that injury induces blastema formation in Acomys cahirinus. Despite cell cycle re-entry in Mus musculus and A. cahirinus, efficient cell cycle progression and proliferation only occurs in spiny mice. Together, our data unite blastema-mediated regeneration in spiny mice with regeneration in other vertebrates such as salamanders, newts and zebrafish, where all healthy adults regenerate in response to injury.

UR - https://www.scopus.com/pages/publications/84964659738

UR - https://www.scopus.com/pages/publications/84964659738#tab=citedBy

U2 - 10.1038/ncomms11164

DO - 10.1038/ncomms11164

M3 - Article

C2 - 27109826

AN - SCOPUS:84964659738

SN - 2041-1723

VL - 7

JO - Nature Communications

JF - Nature Communications

M1 - 11164

ER -

Comparative analysis of ear-hole closure identifies epimorphic regeneration as a discrete trait in mammals

Resumen

Nota bibliográfica

Financiación

ASJC Scopus subject areas

Acceder al documento

Otros archivos y enlaces

Huella

Citar esto