The myosin interacting-heads motif present in live tarantula muscle explains tetanic and posttetanic phosphorylation mechanisms.
Actin Cytoskeleton
/ chemistry
Animals
Arthropods
/ physiology
Evolution, Molecular
Invertebrates
/ physiology
Models, Molecular
Muscle Contraction
Muscle Relaxation
Muscle, Striated
/ physiology
Myosins
/ chemistry
Phosphorylation
/ physiology
Protein Structure, Secondary
Spiders
/ physiology
Vertebrates
/ physiology
myosin interacting-heads motif
phosphorylation
posttetanic potentiation
skeletal muscle
thick filament activation
Journal
Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876
Informations de publication
Date de publication:
02 06 2020
02 06 2020
Historique:
pubmed:
24
5
2020
medline:
18
8
2020
entrez:
24
5
2020
Statut:
ppublish
Résumé
Striated muscle contraction involves sliding of actin thin filaments along myosin thick filaments, controlled by calcium through thin filament activation. In relaxed muscle, the two heads of myosin interact with each other on the filament surface to form the interacting-heads motif (IHM). A key question is how both heads are released from the surface to approach actin and produce force. We used time-resolved synchrotron X-ray diffraction to study tarantula muscle before and after tetani. The patterns showed that the IHM is present in live relaxed muscle. Tetanic contraction produced only a very small backbone elongation, implying that mechanosensing-proposed in vertebrate muscle-is not of primary importance in tarantula. Rather, thick filament activation results from increases in myosin phosphorylation that release a fraction of heads to produce force, with the remainder staying in the ordered IHM configuration. After the tetanus, the released heads slowly recover toward the resting, helically ordered state. During this time the released heads remain close to actin and can quickly rebind, enhancing the force produced by posttetanic twitches, structurally explaining posttetanic potentiation. Taken together, these results suggest that, in addition to stretch activation in insects, two other mechanisms for thick filament activation have evolved to disrupt the interactions that establish the relaxed helices of IHMs: one in invertebrates, by either regulatory light-chain phosphorylation (as in arthropods) or Ca
Identifiants
pubmed: 32444484
pii: 1921312117
doi: 10.1073/pnas.1921312117
pmc: PMC7275770
doi:
Substances chimiques
Myosins
EC 3.6.4.1
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
11865-11874Subventions
Organisme : NIGMS NIH HHS
ID : P41 GM103622
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL139883
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR072036
Pays : United States
Organisme : NIH HHS
ID : S10 OD018090
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR067279
Pays : United States
Déclaration de conflit d'intérêts
The authors declare no competing interest.
Références
Biochem Biophys Res Commun. 1980 Mar 13;93(1):209-14
pubmed: 6990926
Biochemistry. 2003 Jan 21;42(2):390-401
pubmed: 12525166
Biochem Biophys Res Commun. 1979 Sep 12;90(1):164-70
pubmed: 496969
Int J Mol Sci. 2018 Sep 06;19(9):
pubmed: 30200618
Soc Gen Physiol Ser. 1982;37:29-36
pubmed: 7146950
J Struct Biol. 2016 Jan;193(1):45-54
pubmed: 26592473
Am J Physiol. 1993 May;264(5 Pt 1):C1085-95
pubmed: 8388631
Science. 1977 Aug 12;197(4304):685-7
pubmed: 301660
J Cell Biol. 1983 Jun;96(6):1797-802
pubmed: 6602135
J Biol Chem. 1977 Jul 25;252(14):4752-4
pubmed: 301524
BMC Genomics. 2009 Mar 19;10:117
pubmed: 19298669
J Cell Biol. 1982 Feb;92(2):443-51
pubmed: 7199531
J Muscle Res Cell Motil. 2013 Dec;34(5-6):317-32
pubmed: 24162313
Front Physiol. 2019 Nov 01;10:1359
pubmed: 31736781
Mol Biol Cell. 2008 Aug;19(8):3234-42
pubmed: 18495867
J Mol Biol. 1967 Dec 14;30(2):383-434
pubmed: 5586931
J Struct Biol. 2012 Dec;180(3):469-78
pubmed: 22982253
J Mol Biol. 2004 Sep 24;342(4):1223-36
pubmed: 15351647
J Mol Biol. 2007 Oct 5;372(5):1165-78
pubmed: 17707861
Mol Biosyst. 2015 Aug;11(8):2180-9
pubmed: 26038302
Biology (Basel). 2019 Sep 14;8(3):
pubmed: 31540109
Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4361-6
pubmed: 11287639
Biophys Chem. 1986 Dec 15;25(2):161-8
pubmed: 3493038
Proc Natl Acad Sci U S A. 2008 Feb 19;105(7):2386-90
pubmed: 18252826
Compr Physiol. 2016 Dec 6;7(1):171-212
pubmed: 28135003
Biophys J. 2002 Aug;83(2):1082-97
pubmed: 12124288
J Gen Physiol. 1984 Sep;84(3):321-45
pubmed: 6481333
Biophys J. 2013 Nov 5;105(9):2114-22
pubmed: 24209856
J Mol Biol. 1963 Sep;7:281-308
pubmed: 14064165
J Mol Biol. 1984 Jul 5;176(3):417-20
pubmed: 6611422
J Mol Biol. 2001 Aug 31;311(5):1027-36
pubmed: 11531337
Proc Natl Acad Sci U S A. 2010 Jan 5;107(1):430-5
pubmed: 19966283
Arch Biochem Biophys. 2011 Jun 15;510(2):120-8
pubmed: 21284933
Nature. 2005 Aug 25;436(7054):1195-9
pubmed: 16121187
J Mol Biol. 1985 Aug 5;184(3):429-39
pubmed: 4046022
J Mol Biol. 2011 Nov 18;414(1):44-61
pubmed: 21959262
J Muscle Res Cell Motil. 1991 Jun;12(3):235-41
pubmed: 1874965
Biophys J. 1996 Aug;71(2):898-907
pubmed: 8842229
J Physiol. 1968 Jul;197(2):461-77
pubmed: 5716854
Proc Natl Acad Sci U S A. 2005 Nov 29;102(48):17519-24
pubmed: 16299103
Elife. 2017 Jun 13;6:
pubmed: 28606303
Science. 2012 Sep 7;337(6099):1215-8
pubmed: 22923435
Biophys Rev. 2018 Oct;10(5):1465-1477
pubmed: 28871552
J Mol Biol. 2011 Sep 2;411(5):943-50
pubmed: 21763701
Nature. 2015 Dec 10;528(7581):276-9
pubmed: 26560032
J Mol Biol. 1982 Jul 15;158(4):637-84
pubmed: 6981706
J Muscle Res Cell Motil. 2001;22(1):51-9
pubmed: 11563549
Biochem Biophys Res Commun. 2020 Mar 26;524(1):198-204
pubmed: 31983430
J Mol Biol. 2008 Dec 26;384(4):780-97
pubmed: 18951904
J Cell Biol. 1991 May;113(3):563-72
pubmed: 2016336
Nature. 2012 Jul 12;487(7406):231-4
pubmed: 22763458
Mol Biosyst. 2015 Aug;11(8):2167-79
pubmed: 26038232
Am J Physiol Cell Physiol. 2016 Apr 15;310(8):C692-700
pubmed: 26911280
Proc Natl Acad Sci U S A. 2018 Feb 27;115(9):E1991-E2000
pubmed: 29444861
J Mol Biol. 2016 Mar 27;428(6):1142-1164
pubmed: 26851071
Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):7226-31
pubmed: 10860988
J Mol Biol. 2009 Jan 16;385(2):423-31
pubmed: 18976661
Fed Proc. 1980 Apr;39(5):1552-7
pubmed: 7364051
J Biol Chem. 1981 Sep 10;256(17):9274-8
pubmed: 6114959
Nature. 1975 Oct 16;257(5527):561-4
pubmed: 1165781
Biophys J. 2015 Aug 18;109(4):665-7
pubmed: 26287618
Biophys Rev. 2017 Oct;9(5):461-480
pubmed: 28871556
J Cell Biol. 1987 Sep;105(3):1319-27
pubmed: 2958483
Sci Adv. 2016 Sep 30;2(9):e1600058
pubmed: 27704041
Adv Exp Med Biol. 2007;592:253-64
pubmed: 17278370