Critical Limb Ischemia Induces Remodeling of Skeletal Muscle Motor Unit, Myonuclear-, and Mitochondrial-Domains.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
02 07 2019
Historique:
received: 25 10 2018
accepted: 20 06 2019
entrez: 4 7 2019
pubmed: 4 7 2019
medline: 23 10 2020
Statut: epublish

Résumé

Critical limb ischemia, the most severe form of peripheral artery disease, leads to extensive damage and alterations to skeletal muscle homeostasis. Although recent research has investigated the tissue-specific responses to ischemia, the role of the muscle stem cell in the regeneration of its niche components within skeletal muscle has been limited. To elucidate the regenerative mechanism of the muscle stem cell in response to ischemic insults, we explored cellular interactions between the vasculature, neural network, and muscle fiber within the muscle stem cell niche. Using a surgical murine hindlimb ischemia model, we first discovered a significant increase in subsynaptic nuclei and remodeling of the neuromuscular junction following ischemia-induced denervation. In addition, ischemic injury causes significant alterations to the myofiber through a muscle stem cell-mediated accumulation of total myonuclei and a concomitant decrease in myonuclear domain size, possibly to enhance the transcriptional and translation output and restore muscle mass. Results also revealed an accumulation of total mitochondrial content per myonucleus in ischemic myofibers to compensate for impaired mitochondrial function and high turnover rate. Taken together, the findings from this study suggest that the muscle stem cell plays a role in motor neuron reinnervation, myonuclear accretion, and mitochondrial biogenesis for skeletal muscle regeneration following ischemic injury.

Identifiants

pubmed: 31266969
doi: 10.1038/s41598-019-45923-4
pii: 10.1038/s41598-019-45923-4
pmc: PMC6606576
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

9551

Subventions

Organisme : NIH HHS
ID : S10 OD016264
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM008433
Pays : United States
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Arthritis and Musculoskeletal and Skin Diseases (NIAMS)
ID : R21AR072287
Pays : International

Références

Exp Cell Res. 2003 Dec 10;291(2):435-50
pubmed: 14644165
Am J Pathol. 1998 Jun;152(6):1667-79
pubmed: 9626071
J Gerontol A Biol Sci Med Sci. 1995 Nov;50 Spec No:91-5
pubmed: 7493226
Nat Protoc. 2017 Aug;12(8):1576-1587
pubmed: 28703790
Arterioscler Thromb Vasc Biol. 2006 Mar;26(3):520-6
pubmed: 16397137
Anat Rec. 1978 Feb;190(2):299-311
pubmed: 629408
Cell. 2006 Jul 14;126(1):177-89
pubmed: 16839885
J Morphol. 1994 Aug;221(2):177-90
pubmed: 7932768
Physiol Rev. 2013 Jan;93(1):23-67
pubmed: 23303905
Neuron. 2001 May;30(2):399-410
pubmed: 11395002
Methods Mol Biol. 2015;1241:23-38
pubmed: 25308485
Ann Anat. 2015 Nov;202:18-27
pubmed: 26340019
J Physiol. 1975 Jun;248(2):285-306
pubmed: 50439
Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3287-92
pubmed: 19966309
EMBO J. 2008 Jan 23;27(2):433-46
pubmed: 18200046
Vasc Health Risk Manag. 2014 Jul 16;10:417-24
pubmed: 25075192
J Cell Biol. 2007 Aug 27;178(5):749-55
pubmed: 17709429
Physiol Rev. 2015 Jul;95(3):809-52
pubmed: 26109340
Cell. 2015 Aug 27;162(5):1127-39
pubmed: 26279190
Cell Stem Cell. 2018 Oct 4;23(4):530-543.e9
pubmed: 30290177
Genes Dev. 2008 Feb 15;22(4):476-88
pubmed: 18281461
FASEB J. 2010 May;24(5):1376-90
pubmed: 20040516
J Cell Biol. 2009 Sep 21;186(6):793-803
pubmed: 19752025
Elife. 2015 Aug 27;4:
pubmed: 26312504
Biochim Biophys Acta. 1995 May 24;1271(1):67-74
pubmed: 7599228
J Vasc Surg. 2017 May;65(5):1504-1514.e11
pubmed: 28024849
Science. 2002 Apr 12;296(5566):349-52
pubmed: 11951046
Arterioscler Thromb Vasc Biol. 2015 Jan;35(1):184-8
pubmed: 25414254
PLoS One. 2012;7(2):e31231
pubmed: 22363587
Circ Res. 2015 Apr 24;116(9):1561-78
pubmed: 25908729
Cell. 2006 Oct 20;127(2):383-95
pubmed: 17055438
Redox Biol. 2014 Feb 23;2:535-62
pubmed: 24634836
Nature. 2009 Apr 23;458(7241):1056-60
pubmed: 19262508
J Biol Chem. 2004 Nov 19;279(47):49064-73
pubmed: 15317809
Curr Protoc Mouse Biol. 2017 Mar 2;7(1):47-54
pubmed: 28252199
J Biol Chem. 2006 Nov 24;281(47):36401-10
pubmed: 17008324
Int J Dev Biol. 1989 Sep;33(3):379-87
pubmed: 2702122
Development. 2012 Aug;139(16):2857-65
pubmed: 22764051
J Vasc Surg. 2003 Oct;38(4):827-32
pubmed: 14560237
Biochem Biophys Res Commun. 1999 Apr 29;258(1):44-9
pubmed: 10222232
Genes Dev. 2005 May 1;19(9):1013-21
pubmed: 15879551
J Physiol. 1960 Feb;150:417-39
pubmed: 13805874
Biochim Biophys Acta. 1999 Feb 9;1410(2):103-23
pubmed: 10076021
EMBO Rep. 2012 Aug;13(8):741-9
pubmed: 22732842
Exp Biol Med (Maywood). 2013 Oct;238(10):1118-26
pubmed: 23996960
Tissue Eng Part C Methods. 2019 Feb;25(2):59-70
pubmed: 30648479
Physiol Rev. 2004 Jan;84(1):209-38
pubmed: 14715915
Mol Cell Endocrinol. 2010 Feb 5;315(1-2):113-20
pubmed: 19804813
Free Radic Biol Med. 2018 Mar;117:180-190
pubmed: 29432799
Physiology (Bethesda). 2015 Nov;30(6):417-27
pubmed: 26525341
J Biol Chem. 2003 Nov 28;278(48):47853-61
pubmed: 14500729
J Biomed Biotechnol. 2010;2010:724914
pubmed: 20467471
Genesis. 2012 Nov;50(11):833-43
pubmed: 22821887
Cell Metab. 2015 Dec 1;22(6):1033-44
pubmed: 26603188
Nucleic Acids Res. 1989 Aug 11;17(15):6167-79
pubmed: 2771643
PLoS One. 2012;7(1):e29082
pubmed: 22235261
Mol Cell. 2015 Nov 19;60(4):685-96
pubmed: 26549682
Cell Death Differ. 2016 Jun;23(6):927-37
pubmed: 26868912
J Appl Physiol (1985). 2013 Feb 15;114(4):490-7
pubmed: 23195625
Genesis. 2012 Jan;50(1):50-8
pubmed: 21898764
Front Physiol. 2015 Nov 18;6:336
pubmed: 26635622
J Biol Chem. 2000 Jan 28;275(4):2733-44
pubmed: 10644737
Mol Ther. 2014 Jul;22(7):1243-1253
pubmed: 24769910
Development. 1992 Mar;114(3):545-53
pubmed: 1618127
Mol Biol Cell. 2009 Aug;20(15):3525-32
pubmed: 19477917
Am J Physiol. 1997 Apr;272(4 Pt 1):C1345-51
pubmed: 9142861
Am J Pathol. 2012 May;180(5):2156-69
pubmed: 22445571
PLoS One. 2016 Jan 25;11(1):e0147198
pubmed: 26807982
EMBO J. 2006 Jul 12;25(13):2966-77
pubmed: 16778770
Proc Natl Acad Sci U S A. 2007 Jul 17;104(29):12017-22
pubmed: 17609368
Am J Physiol Endocrinol Metab. 2002 Apr;282(4):E802-9
pubmed: 11882500
Neuron. 2005 Aug 4;47(3):365-78
pubmed: 16055061
Cell Tissue Res. 1989 Feb;255(2):385-91
pubmed: 2924339
Nat Med. 2009 Jun;15(6):657-64
pubmed: 19483693
Free Radic Biol Med. 2006 Jul 15;41(2):262-9
pubmed: 16814106
Nat Cell Biol. 2014 Oct;16(10):992-1003, 1-15
pubmed: 25241037
Sci Signal. 2014 Jan 28;7(310):ra10
pubmed: 24473195
Stem Cells. 2011 Mar;29(3):486-95
pubmed: 21425411
Neuron. 2000 Oct;28(1):41-51
pubmed: 11086982
Eur J Cancer. 1996 Dec;32A(14):2423-9
pubmed: 9059330
Biochim Biophys Acta. 2011 Jul;1813(7):1286-94
pubmed: 21255616

Auteurs

Mahir Mohiuddin (M)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, GA, 30332, USA.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Nan Hee Lee (NH)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

June Young Moon (JY)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Woojin M Han (WM)

Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
George W. Woodruff School of Mechanical Engineering, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Shannon E Anderson (SE)

Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, GA, 30332, USA.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Jeongmoon J Choi (JJ)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Eunjung Shin (E)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Shadi A Nakhai (SA)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Thu Tran (T)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Berna Aliya (B)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Do Young Kim (DY)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Aimee Gerold (A)

Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, GA, 30332, USA.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Laura M Hansen (LM)

Division of Cardiology, Emory University School of Medicine, Atlanta, GA, 30322, USA.

W Robert Taylor (WR)

Division of Cardiology, Emory University School of Medicine, Atlanta, GA, 30322, USA.

Young C Jang (YC)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA. young.jang@gatech.edu.
Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, GA, 30332, USA. young.jang@gatech.edu.
Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA. young.jang@gatech.edu.

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