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PMID: 9653138 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Nature of PEVK-titin elasticity in skeletal muscle.

Linke WA, Ivemeyer M, Mundel P, Stockmeier MR, Kolmerer B

Abstract

A unique sequence within the giant titin molecule, the PEVK domain, has been suggested to greatly contribute to passive force development of relaxed skeletal muscle during stretch. To explore the nature of PEVK elasticity, we used titin-specific antibodies to stain both ends of the PEVK region in rat psoas myofibrils and determined the region's force-extension relation by combining immunofluorescence and immunoelectron microscopy with isolated myofibril mechanics. We then tried to fit the results with recent models of polymer elasticity. The PEVK segment elongated substantially at sarcomere lengths above 2.4 micro(m) and reached its estimated contour length at approximately 3.5 micro(m). In immunofluorescently labeled sarcomeres stretched and released repeatedly above 3 micro(m), reversible PEVK lengthening could be readily visualized. At extensions near the contour length, the average force per titin molecule was calculated to be approximately 45 pN. Attempts to fit the force-extension curve of the PEVK segment with a standard wormlike chain model of entropic elasticity were successful only for low to moderate extensions. In contrast, the experimental data also could be correctly fitted at high extensions with a modified wormlike chain model that incorporates enthalpic elasticity. Enthalpic contributions are likely to arise from electrostatic stiffening, as evidenced by the ionic-strength dependency of titin-based myofibril stiffness; at high stretch, hydrophobic effects also might become relevant. Thus, at physiological muscle lengths, the PEVK region does not function as a pure entropic spring. Rather, PEVK elasticity may have both entropic and enthalpic origins characterizable by a polymer persistence length and a stretch modulus.

MeSH Terms
Animals Connectin Elasticity Fluorescent Antibody Technique Male Microscopy, Immunoelectron Muscle Proteins/chemistry Muscle, Skeletal/chemistry Protein Kinases/chemistry Rats Rats, Wistar Stress, Mechanical
Chemicals
Connectin Muscle Proteins Protein Kinases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Linke W A
Institute of Physiology II, University of Heidelberg, Im Neuenheimer Feld 326, D-69120 Heidelberg, Germany. wolfgang.linke@urz.uni.heidelberg.de
Ivemeyer M
Mundel P
Stockmeier M R
Kolmerer B
References (34)
34 references, click to expand
  1. Connectin, an elastic protein of muscle. Characterization and Function.
    J Biochem. 1977 Aug;82(2):317-37 PMID: 914784
  2. Characterization of beta-connectin (titin 2) from striated muscle by dynamic light scattering.
    Biophys J. 1993 Nov;65(5):1906-15 PMID: 8298020
  3. A physiological role for titin and nebulin in skeletal muscle.
    Nature. 1986 Sep 11-17;323(6084):160-4 PMID: 3755803
  4. The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line.
    J Cell Biol. 1988 May;106(5):1563-72 PMID: 2453516
  5. Does titin regulate the length of muscle thick filaments?
    J Mol Biol. 1989 Jan 5;205(1):263-8 PMID: 2926807
  6. Extensible and less-extensible domains of connectin filaments in stretched vertebrate skeletal muscle sarcomeres as detected by immunofluorescence and immunoelectron microscopy using monoclonal antibodies.
    J Biochem. 1988 Oct;104(4):504-8 PMID: 3071530
  7. Passive tension and stiffness of vertebrate skeletal and insect flight muscles: the contribution of weak cross-bridges and elastic filaments.
    Biophys J. 1993 Nov;65(5):2141-59 PMID: 8298040
  8. Connectin, an elastic protein of striated muscle.
    Biophys Chem. 1994 May;50(1-2):73-85 PMID: 8011942
  9. Entropic elasticity of lambda-phage DNA.
    Science. 1994 Sep 9;265(5178):1599-600 PMID: 8079175
  10. Titin and nebulin: protein rulers in muscle?
    Trends Biochem Sci. 1994 Oct;19(10):405-9 PMID: 7817397
  11. Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments.
    Biophys J. 1995 Mar;68(3):1027-44 PMID: 7756523
  12. Titins: giant proteins in charge of muscle ultrastructure and elasticity.
    Science. 1995 Oct 13;270(5234):293-6 PMID: 7569978
  13. A molecular map of titin/connectin elasticity reveals two different mechanisms acting in series.
    FEBS Lett. 1996 Apr 29;385(1-2):11-4 PMID: 8641453
  14. Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules.
    Science. 1996 Feb 9;271(5250):795-9 PMID: 8628994
  15. Towards a molecular understanding of the elasticity of titin.
    J Mol Biol. 1996 Aug 9;261(1):62-71 PMID: 8760502
  16. Elastic filaments in situ in striated muscle revealed by selective removal of thin filaments with plasma gelsolin.
    Adv Biophys. 1996;33:41-52 PMID: 8922101
  17. The giant protein titin. Emerging roles in physiology and pathophysiology.
    Circ Res. 1997 Feb;80(2):290-4 PMID: 9012751
  18. Direct visualization of extensibility in isolated titin molecules.
    J Mol Biol. 1997 Jan 17;265(2):100-6 PMID: 9020973
  19. Stretching DNA with optical tweezers.
    Biophys J. 1997 Mar;72(3):1335-46 PMID: 9138579
  20. Connectin/titin, giant elastic protein of muscle.
    FASEB J. 1997 Apr;11(5):341-5 PMID: 9141500
  21. Reversible unfolding of individual titin immunoglobulin domains by AFM.
    Science. 1997 May 16;276(5315):1109-12 PMID: 9148804
  22. Folding-unfolding transitions in single titin molecules characterized with laser tweezers.
    Science. 1997 May 16;276(5315):1112-6 PMID: 9148805
  23. Elasticity and unfolding of single molecules of the giant muscle protein titin.
    Nature. 1997 May 15;387(6630):308-12 PMID: 9153398
  24. Stretching single protein molecules: titin is a weird spring.
    Science. 1997 May 16;276(5315):1090-2 PMID: 9173540
  25. Actin-titin interaction in cardiac myofibrils: probing a physiological role.
    Biophys J. 1997 Aug;73(2):905-19 PMID: 9251807
  26. Basis of passive tension and stiffness in isolated rabbit myofibrils.
    Am J Physiol. 1997 Jul;273(1 Pt 1):C266-76 PMID: 9252465
  27. A survey of in situ sarcomere extension in mouse skeletal muscle.
    J Muscle Res Cell Motil. 1997 Aug;18(4):465-72 PMID: 9276339
  28. Titin extensibility in situ: entropic elasticity of permanently folded and permanently unfolded molecular segments.
    J Cell Biol. 1998 Feb 23;140(4):853-9 PMID: 9472037
  29. Characterizing titin's I-band Ig domain region as an entropic spring.
    J Cell Sci. 1998 Jun;111 ( Pt 11):1567-74 PMID: 9580564
  30. Use of poly(vinylpyrrolidone) and poly(vinyl alcohol) for cryoultramicrotomy.
    Histochem J. 1989 Mar;21(3):163-71 PMID: 2722561
  31. Podocytes in glomerulus of rat kidney express a characteristic 44 KD protein.
    J Histochem Cytochem. 1991 Aug;39(8):1047-56 PMID: 1856454
  32. Regulation of skeletal muscle stiffness and elasticity by titin isoforms: a test of the segmental extension model of resting tension.
    Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7101-5 PMID: 1714586
  33. Nature and origin of gap filaments in striated muscle.
    J Cell Sci. 1991 Dec;100 ( Pt 4):809-14 PMID: 1726102
  34. Titin: major myofibrillar components of striated muscle.
    Proc Natl Acad Sci U S A. 1979 Aug;76(8):3698-702 PMID: 291034
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1998-07-07
Pages
8052-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC20927
Subset
IM
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