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
N1 - Funding Information:
We thank the Department of Animal Care and Technologies at Arizona State University for assistance in maintaining the lizard colony and Stephen Pratt for statistical consultation. This work was supported by funding from the National Center for Research Resources and the Office of Research Infrastructure Programs (ORIP) grant R21 RR031305 , National Institute of Arthritis, Musculoskeletal, and Skin Diseases grant R21 AR064935 of the National Institutes of Health, Arizona Biomedical Research Commission grant 1113 and Burroughs Wellcome Fund Collaborative Research Travel Grant to KK. XGSA bioinformatic analysis was supported by a Career Development Fellowship ( 1105271 ) from the National Health and Medical Research Council Australia and a Future Leader Fellowship from the National Heart Foundation of Australia 100848 , to JWKH. Computational analysis was supported by allocations from Arizona State University Research Computing. The funding sources listed had no role in the study design, collection, analysis, nor interpretation of the data; in the writing of the paper; nor the decision to submit the article for publication. Authors have no interests to declare. This work has not been published previously, nor is it under consideration for publication elsewhere. This publication has been approved by all authors.
Publisher Copyright:
© 2017 Elsevier Inc.
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.
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U2 - 10.1016/j.ydbio.2017.08.037
DO - 10.1016/j.ydbio.2017.08.037
M3 - Article
C2 - 29291980
AN - SCOPUS:85039778233
VL - 433
SP - 344
EP - 356
JO - Developmental Biology
JF - Developmental Biology
SN - 0012-1606
IS - 2
ER -