Identification of satellite cells from anole lizard skeletal muscle and demonstration of expanded musculoskeletal potential

Joanna Palade, Djordje Djordjevic, Elizabeth D. Hutchins, Rajani M. George, John A. Cornelius, Jeffery Rawls, Joshua W.K. Ho, Kenro Kusumi, Norma Wilson-Rawls

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

The lizards are evolutionarily the closest vertebrates to humans that demonstrate the ability to regenerate entire appendages containing cartilage, muscle, skin, and nervous tissue. We previously isolated PAX7-positive cells from muscle of the green anole lizard, Anolis carolinensis, that can differentiate into multinucleated myotubes and express the muscle structural protein, myosin heavy chain. Studying gene expression in these satellite/progenitor cell populations from A. carolinensis can provide insight into the mechanisms regulating tissue regeneration. We generated a transcriptome from proliferating lizard myoprogenitor cells and compared them to transcriptomes from the mouse and human tissues from the ENCODE project using XGSA, a statistical method for cross-species gene set analysis. These analyses determined that the lizard progenitor cell transcriptome was most similar to mammalian satellite cells. Further examination of specific GO categories of genes demonstrated that among genes with the highest level of expression in lizard satellite cells were an increased number of genetic regulators of chondrogenesis, as compared to mouse satellite cells. In micromass culture, lizard PAX7-positive cells formed Alcian blue and collagen 2a1 positive nodules, without the addition of exogenous morphogens, unlike their mouse counterparts. Subsequent quantitative RT-PCR confirmed up-regulation of expression of chondrogenic regulatory genes in lizard cells, including bmp2, sox9, runx2, and cartilage specific structural genes, aggrecan and collagen 2a1. Taken together, these data suggest that tail regeneration in lizards involves significant alterations in gene regulation with expanded musculoskeletal potency.

Original languageEnglish (US)
Pages (from-to)344-356
Number of pages13
JournalDevelopmental Biology
Volume433
Issue number2
DOIs
StatePublished - Jan 15 2018

Fingerprint

Lizards
Skeletal Muscle
Transcriptome
Genes
Cartilage
Regeneration
Collagen
Stem Cells
Aggrecans
Chondrogenesis
Nerve Tissue
Alcian Blue
Myosin Heavy Chains
Muscle Proteins
Skeletal Muscle Fibers
Regulator Genes
Muscle Cells
Vertebrates
Tail
Up-Regulation

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology
  • Cell Biology

Cite this

Identification of satellite cells from anole lizard skeletal muscle and demonstration of expanded musculoskeletal potential. / Palade, Joanna; Djordjevic, Djordje; Hutchins, Elizabeth D.; George, Rajani M.; Cornelius, John A.; Rawls, Jeffery; Ho, Joshua W.K.; Kusumi, Kenro; Wilson-Rawls, Norma.

In: Developmental Biology, Vol. 433, No. 2, 15.01.2018, p. 344-356.

Research output: Contribution to journalArticle

Palade, Joanna ; Djordjevic, Djordje ; Hutchins, Elizabeth D. ; George, Rajani M. ; Cornelius, John A. ; Rawls, Jeffery ; Ho, Joshua W.K. ; Kusumi, Kenro ; Wilson-Rawls, Norma. / Identification of satellite cells from anole lizard skeletal muscle and demonstration of expanded musculoskeletal potential. In: Developmental Biology. 2018 ; Vol. 433, No. 2. pp. 344-356.
@article{107899e054d043a4b8608647c0808a3f,
title = "Identification of satellite cells from anole lizard skeletal muscle and demonstration of expanded musculoskeletal potential",
abstract = "The lizards are evolutionarily the closest vertebrates to humans that demonstrate the ability to regenerate entire appendages containing cartilage, muscle, skin, and nervous tissue. We previously isolated PAX7-positive cells from muscle of the green anole lizard, Anolis carolinensis, that can differentiate into multinucleated myotubes and express the muscle structural protein, myosin heavy chain. Studying gene expression in these satellite/progenitor cell populations from A. carolinensis can provide insight into the mechanisms regulating tissue regeneration. We generated a transcriptome from proliferating lizard myoprogenitor cells and compared them to transcriptomes from the mouse and human tissues from the ENCODE project using XGSA, a statistical method for cross-species gene set analysis. These analyses determined that the lizard progenitor cell transcriptome was most similar to mammalian satellite cells. Further examination of specific GO categories of genes demonstrated that among genes with the highest level of expression in lizard satellite cells were an increased number of genetic regulators of chondrogenesis, as compared to mouse satellite cells. In micromass culture, lizard PAX7-positive cells formed Alcian blue and collagen 2a1 positive nodules, without the addition of exogenous morphogens, unlike their mouse counterparts. Subsequent quantitative RT-PCR confirmed up-regulation of expression of chondrogenic regulatory genes in lizard cells, including bmp2, sox9, runx2, and cartilage specific structural genes, aggrecan and collagen 2a1. Taken together, these data suggest that tail regeneration in lizards involves significant alterations in gene regulation with expanded musculoskeletal potency.",
author = "Joanna Palade and Djordje Djordjevic and Hutchins, {Elizabeth D.} and George, {Rajani M.} and Cornelius, {John A.} and Jeffery Rawls and Ho, {Joshua W.K.} and Kenro Kusumi and Norma Wilson-Rawls",
year = "2018",
month = "1",
day = "15",
doi = "10.1016/j.ydbio.2017.08.037",
language = "English (US)",
volume = "433",
pages = "344--356",
journal = "Developmental Biology",
issn = "0012-1606",
publisher = "Academic Press Inc.",
number = "2",

}

TY - JOUR

T1 - Identification of satellite cells from anole lizard skeletal muscle and demonstration of expanded musculoskeletal potential

AU - Palade, Joanna

AU - Djordjevic, Djordje

AU - Hutchins, Elizabeth D.

AU - George, Rajani M.

AU - Cornelius, John A.

AU - Rawls, Jeffery

AU - Ho, Joshua W.K.

AU - Kusumi, Kenro

AU - Wilson-Rawls, Norma

PY - 2018/1/15

Y1 - 2018/1/15

N2 - The lizards are evolutionarily the closest vertebrates to humans that demonstrate the ability to regenerate entire appendages containing cartilage, muscle, skin, and nervous tissue. We previously isolated PAX7-positive cells from muscle of the green anole lizard, Anolis carolinensis, that can differentiate into multinucleated myotubes and express the muscle structural protein, myosin heavy chain. Studying gene expression in these satellite/progenitor cell populations from A. carolinensis can provide insight into the mechanisms regulating tissue regeneration. We generated a transcriptome from proliferating lizard myoprogenitor cells and compared them to transcriptomes from the mouse and human tissues from the ENCODE project using XGSA, a statistical method for cross-species gene set analysis. These analyses determined that the lizard progenitor cell transcriptome was most similar to mammalian satellite cells. Further examination of specific GO categories of genes demonstrated that among genes with the highest level of expression in lizard satellite cells were an increased number of genetic regulators of chondrogenesis, as compared to mouse satellite cells. In micromass culture, lizard PAX7-positive cells formed Alcian blue and collagen 2a1 positive nodules, without the addition of exogenous morphogens, unlike their mouse counterparts. Subsequent quantitative RT-PCR confirmed up-regulation of expression of chondrogenic regulatory genes in lizard cells, including bmp2, sox9, runx2, and cartilage specific structural genes, aggrecan and collagen 2a1. Taken together, these data suggest that tail regeneration in lizards involves significant alterations in gene regulation with expanded musculoskeletal potency.

AB - The lizards are evolutionarily the closest vertebrates to humans that demonstrate the ability to regenerate entire appendages containing cartilage, muscle, skin, and nervous tissue. We previously isolated PAX7-positive cells from muscle of the green anole lizard, Anolis carolinensis, that can differentiate into multinucleated myotubes and express the muscle structural protein, myosin heavy chain. Studying gene expression in these satellite/progenitor cell populations from A. carolinensis can provide insight into the mechanisms regulating tissue regeneration. We generated a transcriptome from proliferating lizard myoprogenitor cells and compared them to transcriptomes from the mouse and human tissues from the ENCODE project using XGSA, a statistical method for cross-species gene set analysis. These analyses determined that the lizard progenitor cell transcriptome was most similar to mammalian satellite cells. Further examination of specific GO categories of genes demonstrated that among genes with the highest level of expression in lizard satellite cells were an increased number of genetic regulators of chondrogenesis, as compared to mouse satellite cells. In micromass culture, lizard PAX7-positive cells formed Alcian blue and collagen 2a1 positive nodules, without the addition of exogenous morphogens, unlike their mouse counterparts. Subsequent quantitative RT-PCR confirmed up-regulation of expression of chondrogenic regulatory genes in lizard cells, including bmp2, sox9, runx2, and cartilage specific structural genes, aggrecan and collagen 2a1. Taken together, these data suggest that tail regeneration in lizards involves significant alterations in gene regulation with expanded musculoskeletal potency.

UR - http://www.scopus.com/inward/record.url?scp=85039778233&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85039778233&partnerID=8YFLogxK

U2 - 10.1016/j.ydbio.2017.08.037

DO - 10.1016/j.ydbio.2017.08.037

M3 - Article

VL - 433

SP - 344

EP - 356

JO - Developmental Biology

JF - Developmental Biology

SN - 0012-1606

IS - 2

ER -