Bridging the muscle genome to phenome across multiple biological scales.


Journal

The Journal of experimental biology
ISSN: 1477-9145
Titre abrégé: J Exp Biol
Pays: England
ID NLM: 0243705

Informations de publication

Date de publication:
01 04 2022
Historique:
received: 05 10 2021
accepted: 08 03 2022
pubmed: 16 3 2022
medline: 15 4 2022
entrez: 15 3 2022
Statut: ppublish

Résumé

Muscle is highly hierarchically organized, with functions shaped by genetically controlled expression of protein ensembles with different isoform profiles at the sarcomere scale. However, it remains unclear how isoform profiles shape whole-muscle performance. We compared two mouse hindlimb muscles, the slow, relatively parallel-fibered soleus and the faster, more pennate-fibered tibialis anterior (TA), across scales: from gene regulation, isoform expression and translation speed, to force-length-velocity-power for intact muscles. Expression of myosin heavy-chain (MHC) isoforms directly corresponded with contraction velocity. The fast-twitch TA with fast MHC isoforms had faster unloaded velocities (actin sliding velocity, Vactin; peak fiber velocity, Vmax) than the slow-twitch soleus. For the soleus, Vactin was biased towards Vactin for purely slow MHC I, despite this muscle's even fast and slow MHC isoform composition. Our multi-scale results clearly identified a consistent and significant dampening in fiber shortening velocities for both muscles, underscoring an indirect correlation between Vactin and fiber Vmax that may be influenced by differences in fiber architecture, along with internal loading due to both passive and active effects. These influences correlate with the increased peak force and power in the slightly more pennate TA, leading to a broader length range of near-optimal force production. Conversely, a greater force-velocity curvature in the near-parallel fibered soleus highlights the fine-tuning by molecular-scale influences including myosin heavy and light chain expression along with whole-muscle characteristics. Our results demonstrate that the individual gene, protein and whole-fiber characteristics do not directly reflect overall muscle performance but that intricate fine-tuning across scales shapes specialized muscle function.

Identifiants

pubmed: 35288729
pii: 274716
doi: 10.1242/jeb.243630
pmc: PMC9080751
pii:
doi:

Substances chimiques

Protein Isoforms 0
Myosin Heavy Chains EC 3.6.4.1
Myosins EC 3.6.4.1

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

Subventions

Organisme : University of Massachusetts, Lowell
Organisme : American Heart Association
ID : 20PRE35120307
Organisme : University of Massachusetts Lowell
ID : R50180000038587

Informations de copyright

© 2022. Published by The Company of Biologists Ltd.

Déclaration de conflit d'intérêts

Competing interests The authors declare no competing or financial interests.

Références

Muscle Nerve. 2000 Nov;23(11):1647-66
pubmed: 11054744
Anal Biochem. 1996 Jan 1;233(1):31-5
pubmed: 8789143
Comp Biochem Physiol B. 1993 Nov;106(3):463-75
pubmed: 8281747
J Physiol. 1949 Dec;110(3-4):249-80
pubmed: 15406429
J Physiol. 2018 Apr 15;596(8):1467-1483
pubmed: 29455454
J Exp Biol. 1998 Feb;201(Pt 3):309-16
pubmed: 9503642
Biophys J. 1997 Apr;72(4):1767-79
pubmed: 9083681
J Physiol. 1964 Sep;173:74-95
pubmed: 14205033
J Morphol. 1994 Aug;221(2):177-90
pubmed: 7932768
Biophys J. 1995 Mar;68(3):1027-44
pubmed: 7756523
J Physiol. 1991 Jun;437:655-72
pubmed: 1890654
J Biol Chem. 1971 Aug 10;246(15):4866-71
pubmed: 4254541
J Appl Physiol (1985). 1999 May;86(5):1445-57
pubmed: 10233103
J Muscle Res Cell Motil. 1994 Oct;15(5):517-34
pubmed: 7860700
J Physiol. 2003 Feb 1;546(Pt 3):677-89
pubmed: 12562996
J Physiol. 1989 Sep;416:245-54
pubmed: 2607450
Proc Biol Sci. 2014 Apr 02;281(1783):20140002
pubmed: 24695429
Nature. 1954 May 22;173(4412):971-3
pubmed: 13165697
Arch Biochem Biophys. 2015 Aug 15;580:14-21
pubmed: 26116789
J Exp Biol. 2001 Dec;204(Pt 24):4237-48
pubmed: 11815648
J Exp Biol. 1995 Feb;198(Pt 2):491-502
pubmed: 7699317
J Exp Biol. 2016 Jan;219(Pt 2):276-84
pubmed: 26792340
J Gen Physiol. 2005 Nov;126(5):461-80
pubmed: 16230467
J Physiol. 1965 May;178:252-69
pubmed: 14298118
J Cell Biol. 1998 Feb 23;140(4):853-9
pubmed: 9472037
J Muscle Res Cell Motil. 1994 Feb;15(1):11-9
pubmed: 8182105
Nature. 1954 May 22;173(4412):973-6
pubmed: 13165698
Dev Biol. 2016 Feb 1;410(1):1-13
pubmed: 26708096
J Exp Biol. 1997 Nov;200(Pt 22):2907-12
pubmed: 9344980
J Gen Physiol. 1967 Jul;50(6):Suppl:197-218
pubmed: 4227924
Prog Biophys Biophys Chem. 1957;7:255-318
pubmed: 13485191
Am J Physiol Cell Physiol. 2019 Jun 1;316(6):C844-C861
pubmed: 30865518
Exp Physiol. 1992 Sep;77(5):757-60
pubmed: 1418957
Front Physiol. 2016 May 25;7:187
pubmed: 27252660
J Exp Biol. 2012 Jan 15;215(Pt 2):324-30
pubmed: 22189776
J Biomech. 2011 Jan 4;44(1):109-15
pubmed: 20889156
Exp Gerontol. 2005 Dec;40(12):966-75
pubmed: 16243468
Magn Reson Med. 2005 Jun;53(6):1333-40
pubmed: 15906281
J Exp Biol. 2020 Oct 7;223(Pt 19):
pubmed: 32737211
J Vis Exp. 2013 Feb 09;(72):
pubmed: 23426237
J Appl Physiol (1985). 1994 Aug;77(2):493-501
pubmed: 8002492
BMC Genomics. 2020 Nov 19;21(1):808
pubmed: 33213377
Prog Biophys Mol Biol. 2000;73(2-4):195-262
pubmed: 10958931
J Cell Biochem. 2012 Apr;113(4):1265-73
pubmed: 22105831
Proc Biol Sci. 2012 Mar 22;279(1731):1108-13
pubmed: 21957134
Exp Cell Res. 2010 Nov 1;316(18):3093-9
pubmed: 20580710
BMC Genomics. 2009 Aug 07;10:365
pubmed: 19660143
Microsc Res Tech. 2000 Sep 15;50(6):500-9
pubmed: 10998639
Biol Cell. 2003 Sep;95(6):399-406
pubmed: 14519557
J Physiol. 1999 Oct 15;520 Pt 2:463-71
pubmed: 10523415
J Mol Biol. 1996 Aug 9;261(1):62-71
pubmed: 8760502
Arch Biochem Biophys. 2014 Dec 15;564:89-99
pubmed: 25241052
PLoS One. 2016 Apr 26;11(4):e0147669
pubmed: 27115354
Circ Res. 2000 Jun 9;86(11):1114-21
pubmed: 10850961
Biophys J. 2014 Dec 16;107(12):L41-L44
pubmed: 25517169
Elife. 2018 May 29;7:
pubmed: 29809149
Philos Trans R Soc Lond B Biol Sci. 2011 May 27;366(1570):1466-76
pubmed: 21502118
Physiol Rev. 2011 Oct;91(4):1447-531
pubmed: 22013216
J Physiol. 1989 Jun;413:379-97
pubmed: 2600856
Front Physiol. 2020 May 19;11:495
pubmed: 32508678
Annu Rev Physiol. 2018 Feb 10;80:327-351
pubmed: 29433413
J Exp Biol. 1997 Dec;200(Pt 24):3119-31
pubmed: 9364020
J Biol Chem. 2001 Dec 7;276(49):45902-8
pubmed: 11590173
Curr Protoc Hum Genet. 2015 Oct 06;87:11.16.1-11.16.14
pubmed: 26439713
J Appl Physiol (1985). 2021 Apr 1;130(4):941-951
pubmed: 33411643
Biophys J. 2020 Jan 21;118(2):303-312
pubmed: 31882250
J Gen Physiol. 2021 Jul 5;153(7):
pubmed: 34014247
Am J Physiol Regul Integr Comp Physiol. 2009 Aug;297(2):R265-74
pubmed: 19458282
Exp Physiol. 2012 Jul;97(7):873-81
pubmed: 22467761
Exp Gerontol. 2021 Dec;156:111618
pubmed: 34737004
Proc Natl Acad Sci U S A. 2017 Sep 26;114(39):E8147-E8154
pubmed: 28900011
Biochemistry. 2004 Nov 30;43(47):15058-65
pubmed: 15554713
J Physiol. 1988 Oct;404:71-82
pubmed: 3253447
J Muscle Res Cell Motil. 1986 Oct;7(5):387-404
pubmed: 3540004
Proc Natl Acad Sci U S A. 2010 Oct 5;107(40):17403-8
pubmed: 20855589
Integr Comp Biol. 2022 Feb 5;61(6):2066-2074
pubmed: 34259855
Muscle Nerve. 2013 Apr;47(4):588-90
pubmed: 23381871
J Exp Biol. 2009 Aug;212(Pt 16):2511-9
pubmed: 19648394
Science. 1971 Nov 12;174(4010):709-12
pubmed: 4107849
Nature. 1965 May 15;206(985):718-9
pubmed: 5832859

Auteurs

SaiLavanyaa Sundar (S)

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01854, USA.
UMass Movement Center, University of Massachusetts, Lowell, MA 01854, USA.

Barbora Rimkus (B)

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01854, USA.
UMass Movement Center, University of Massachusetts, Lowell, MA 01854, USA.

Prabath S Meemaduma (PS)

UMass Movement Center, University of Massachusetts, Lowell, MA 01854, USA.
Department of Chemistry, University of Massachusetts, Lowell, MA 01854, USA.

Samuel deLap (S)

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01854, USA.
UMass Movement Center, University of Massachusetts, Lowell, MA 01854, USA.

Nicholas LaFave (N)

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01854, USA.
UMass Movement Center, University of Massachusetts, Lowell, MA 01854, USA.

Alice W Racca (AW)

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01854, USA.
UMass Movement Center, University of Massachusetts, Lowell, MA 01854, USA.

Pabodha Hettige (P)

UMass Movement Center, University of Massachusetts, Lowell, MA 01854, USA.
Department of Chemistry, University of Massachusetts, Lowell, MA 01854, USA.

Jeffrey Moore (J)

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01854, USA.
UMass Movement Center, University of Massachusetts, Lowell, MA 01854, USA.

Matthew Gage (M)

UMass Movement Center, University of Massachusetts, Lowell, MA 01854, USA.
Department of Chemistry, University of Massachusetts, Lowell, MA 01854, USA.

Andrea Shehaj (A)

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01854, USA.
UMass Movement Center, University of Massachusetts, Lowell, MA 01854, USA.

Nicolai Konow (N)

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01854, USA.
UMass Movement Center, University of Massachusetts, Lowell, MA 01854, USA.

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