Mitochondrial network configuration influences sarcomere and myosin filament structure in striated muscles.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
13 10 2022
13 10 2022
Historique:
received:
18
01
2022
accepted:
28
09
2022
entrez:
13
10
2022
pubmed:
14
10
2022
medline:
18
10
2022
Statut:
epublish
Résumé
Sustained muscle contraction occurs through interactions between actin and myosin filaments within sarcomeres and requires a constant supply of adenosine triphosphate (ATP) from nearby mitochondria. However, it remains unclear how different physical configurations between sarcomeres and mitochondria alter the energetic support for contractile function. Here, we show that sarcomere cross-sectional area (CSA) varies along its length in a cell type-dependent manner where the reduction in Z-disk CSA relative to the sarcomere center is closely coordinated with mitochondrial network configuration in flies, mice, and humans. Further, we find myosin filaments near the sarcomere periphery are curved relative to interior filaments with greater curvature for filaments near mitochondria compared to sarcoplasmic reticulum. Finally, we demonstrate variable myosin filament lattice spacing between filament ends and filament centers in a cell type-dependent manner. These data suggest both sarcomere structure and myofilament interactions are influenced by the location and orientation of mitochondria within muscle cells.
Identifiants
pubmed: 36229433
doi: 10.1038/s41467-022-33678-y
pii: 10.1038/s41467-022-33678-y
pmc: PMC9561657
doi:
Substances chimiques
Actins
0
Adenosine Triphosphate
8L70Q75FXE
Myosins
EC 3.6.4.1
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
6058Subventions
Organisme : Intramural NIH HHS
ID : ZIA HL006221
Pays : United States
Informations de copyright
© 2022. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.
Références
J Exp Biol. 2020 May 4;223(Pt 9):
pubmed: 32205362
J Physiol. 1997 Jun 15;501 ( Pt 3):573-88
pubmed: 9218218
Am J Physiol Cell Physiol. 2004 Oct;287(4):C817-33
pubmed: 15355853
Nat Commun. 2018 Nov 30;9(1):5111
pubmed: 30504768
J Gen Physiol. 2016 Dec;148(6):459-488
pubmed: 27864330
Cell Rep. 2021 Oct 19;37(3):109846
pubmed: 34686324
Nat Commun. 2022 May 13;13(1):2661
pubmed: 35562354
Development. 1997 Sep;124(17):3333-41
pubmed: 9310328
Physiol Rev. 1998 Apr;78(2):359-91
pubmed: 9562033
J Struct Biol. 2019 Jul 1;207(1):1-11
pubmed: 30914296
Proc Natl Acad Sci U S A. 2018 Oct 9;115(41):10369-10374
pubmed: 30249654
J Cell Biol. 1972 Mar;52(3):626-38
pubmed: 5009524
Cardiovasc Res. 2020 Feb 1;116(2):260-261
pubmed: 31688919
Biochem J. 2003 May 1;371(Pt 3):811-21
pubmed: 12558500
J Muscle Res Cell Motil. 1992 Feb;13(1):100-5
pubmed: 1556165
J Physiol. 1977 Jul;269(2):255-72
pubmed: 302331
Wiley Interdiscip Rev Syst Biol Med. 2020 Jan;12(1):e1462
pubmed: 31407867
Cell Metab. 2017 May 2;25(5):1186-1193.e4
pubmed: 28467934
J Med Chem. 2016 Dec 8;59(23):10411-10434
pubmed: 27560192
Elife. 2021 Jun 14;10:
pubmed: 34121660
PLoS Comput Biol. 2010 Dec 02;6(12):e1001018
pubmed: 21152002
PLoS Biol. 2004 Oct;2(10):e348
pubmed: 15486583
Int Rev Cytol. 1993;143:63-152
pubmed: 8449665
Arch Biochem Biophys. 1987 May 15;255(1):80-8
pubmed: 3592671
Biochim Biophys Acta. 1978 Mar 13;501(3):349-69
pubmed: 629958
Biology (Basel). 2014 Dec 03;3(4):846-65
pubmed: 25478994
Biophys J. 1993 Jan;64(1):187-96
pubmed: 7679296
Nat Chem. 2020 Feb;12(2):165-172
pubmed: 31792385
J Cell Sci. 1971 Jul;9(1):123-37
pubmed: 5565058
PLoS Comput Biol. 2012;8(11):e1002770
pubmed: 23166482
Am J Physiol. 1975 Apr;228(4):1029-33
pubmed: 165725
J Exp Biol. 2021 Oct 1;224(19):
pubmed: 34581401
J Muscle Res Cell Motil. 1998 Oct;19(7):811-23
pubmed: 9836152
J Cell Physiol. 1983 Mar;114(3):346-64
pubmed: 6601109
J Appl Physiol (1985). 2001 Mar;90(3):1158-64
pubmed: 11181631
Nature. 1954 May 22;173(4412):971-3
pubmed: 13165697
G3 (Bethesda). 2017 Oct 5;7(10):3521-3531
pubmed: 28866639
Nat Commun. 2022 Nov 4;13(1):6622
pubmed: 36333356
J Physiol. 2020 Nov;598(22):5165-5182
pubmed: 32818298
Biophys J. 1993 Jan;64(1):197-210
pubmed: 7679297
J Biol Chem. 1987 Jul 5;262(19):9109-14
pubmed: 3597408
J Exp Biol. 2003 Dec;206(Pt 24):4385-91
pubmed: 14610025
Free Radic Biol Med. 2020 May 20;152:767-775
pubmed: 31972341
Nature. 1954 May 22;173(4412):973-6
pubmed: 13165698
Methods. 2012 Jan;56(1):69-77
pubmed: 22079350
J Cell Sci. 1970 Jan;6(1):257-76
pubmed: 4907041
Cytoskeleton (Hoboken). 2014 Sep;71(9):513-29
pubmed: 25145272
Anat Rec (Hoboken). 2019 Jan;302(1):146-152
pubmed: 30302911
Front Physiol. 2020 Nov 11;11:541040
pubmed: 33262702
Biophys J. 2021 Sep 21;120(18):4079-4090
pubmed: 34384761
J Mol Cell Cardiol. 1983 Jul;15(7):413-20
pubmed: 6620393
Proc Natl Acad Sci U S A. 1989 Mar;86(5):1583-7
pubmed: 2922400
Dev Cell. 2012 Sep 11;23(3):664-73
pubmed: 22975331
Acta Anat (Basel). 1981;109(4):332-8
pubmed: 7027725
Proc Biol Sci. 2013 Sep 07;280(1766):20130697
pubmed: 23843386
Methods. 2012 Jan;56(1):78-86
pubmed: 22037247
Bone. 2010 Dec;47(6):1076-9
pubmed: 20817052
Bioinformatics. 2016 Nov 15;32(22):3532-3534
pubmed: 27412086
Am J Physiol Cell Physiol. 2020 Nov 1;319(5):C858-C876
pubmed: 32783659
J Struct Biol. 2012 Jan;177(1):135-44
pubmed: 21907807
Am J Anat. 1983 Feb;166(2):209-22
pubmed: 6601453
PLoS Comput Biol. 2007 Jul;3(7):e115
pubmed: 17630823
Mol Biol Cell. 2021 Mar 15;32(6):470-474
pubmed: 33476183
Nature. 2015 Jul 30;523(7562):617-20
pubmed: 26223627
Nature. 2011 Nov 16;479(7373):406-9
pubmed: 22094701
Dev Biol. 2021 Jan 1;469:12-25
pubmed: 32980309
J Biophys Biochem Cytol. 1957 Mar 25;3(2):269-300
pubmed: 13438910
Rev Physiol Biochem Pharmacol. 1990;116:1-76
pubmed: 2149884
J Morphol. 1977 Aug;153(2):307-16
pubmed: 142843
Cell. 2021 Apr 15;184(8):2135-2150.e13
pubmed: 33765442
Free Radic Biol Med. 2012 Jul 15;53(2):260-70
pubmed: 22580337
R Soc Open Sci. 2021 Mar 3;8(3):201784
pubmed: 33959340
Curr Opin Struct Biol. 1997 Apr;7(2):247-57
pubmed: 9094325
Dev Cell. 2001 Dec;1(6):829-39
pubmed: 11740944
J Pharmacol Exp Ther. 2017 Dec;363(3):303-313
pubmed: 28935700
J Mol Biol. 1985 Sep 5;185(1):211-4
pubmed: 4046039
Physiol Rev. 2021 Oct 1;101(4):1561-1607
pubmed: 33733879
J Anat. 1973 Jan;114(Pt 1):1-6
pubmed: 4577028
J Exp Biol. 1998;201(3):299-307
pubmed: 9427665
Calcif Tissue Int. 2015 Mar;96(3):183-95
pubmed: 25294644
J Muscle Res Cell Motil. 1990 Jun;11(3):203-15
pubmed: 2119393
Biophys J. 2011 Mar 16;100(6):1499-508
pubmed: 21402032
Physiol Rev. 2011 Oct;91(4):1447-531
pubmed: 22013216
Pflugers Arch. 1973 Nov 28;344(3):217-32
pubmed: 4797912
J Physiol. 1987 Apr;385:661-75
pubmed: 3309266
Proc Natl Acad Sci U S A. 2021 Apr 27;118(17):
pubmed: 33888578
Nat Commun. 2021 Apr 7;12(1):2091
pubmed: 33828099
Wellcome Open Res. 2021 Feb 22;6:37
pubmed: 33954267
J Appl Physiol (1985). 2013 Sep;115(6):785-93
pubmed: 23788574
J Appl Physiol (1985). 1994 Feb;76(2):974-8
pubmed: 8175613
Acta Physiol Scand. 1976 Oct;98(2):143-56
pubmed: 1086583
Annu Rev Pathol. 2010;5:297-348
pubmed: 20078222
Cell Rep. 2017 Apr 18;19(3):487-496
pubmed: 28423313
Nat Commun. 2016 Oct 31;7:13281
pubmed: 27796302
Nat Commun. 2020 Jul 24;11(1):3722
pubmed: 32709902
Arch Biochem Biophys. 1981 Jul;209(2):539-54
pubmed: 7294809
Am J Physiol. 1986 Sep;251(3 Pt 1):C395-402
pubmed: 3752235
Comp Biochem Physiol B Biochem Mol Biol. 1998 May;120(1):35-40
pubmed: 9787776
J Exp Biol. 2020 Mar 25;223(Pt 6):
pubmed: 32098882
Proc Natl Acad Sci U S A. 2021 Apr 20;118(16):
pubmed: 33850019
PLoS One. 2011;6(7):e21985
pubmed: 21779362
J Exp Biol. 2019 Nov 29;222(Pt 23):
pubmed: 31784473
J Cell Sci. 1970 Mar;6(2):593-603
pubmed: 4911694
J Muscle Res Cell Motil. 1983 Feb;4(1):25-53
pubmed: 6841591
Cells. 2020 Jul 09;9(7):
pubmed: 32660165
Dev Biol. 2003 Aug 15;260(2):391-403
pubmed: 12921740
Biophys J. 1987 Jul;52(1):127-31
pubmed: 3607220