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PMID: 2808523 Published · ppublish English Journal Article

Elastic behavior of connectin filaments during thick filament movement in activated skeletal muscle.

The Journal of cell biology ·Vol. 109 ·No. 5 ·1989-11-00 ·Pages 2169-76

Horowits R, Maruyama K, Podolsky RJ

Abstract

Connectin (also called titin) is a huge, striated muscle protein that binds to thick filaments and links them to the Z-disc. Using an mAb that binds to connectin in the I-band region of the molecule, we studied the behavior of connectin in both relaxed and activated skinned rabbit psoas fibers by immunoelectron microscopy. In relaxed fibers, antibody binding is visualized as two extra striations per sarcomere arranged symmetrically about the M-line. These striations move away from both the nearest Z-disc and the thick filaments when the sarcomere is stretched, confirming the elastic behavior of connectin within the I-band of relaxed sarcomeres as previously observed by several investigators. When the fiber is activated, thick filaments in sarcomeres shorter than 2.8 microns tend to move from the center to the side of the sarcomere. This translocation of thick filaments within the sarcomere is accompanied by movement of the antibody label in the same direction. In that half-sarcomere in which the thick filaments move away from the Z-disc, the spacings between the Z-disc and the antibody and between the antibody and the thick filaments both increase. Conversely, on the side of the sarcomere in which the thick filaments move nearer to the Z-line, these spacings decrease. Regardless of whether I-band spacing is varied by stretch of a relaxed sarcomere or by active sliding of thick filaments within a sarcomere of constant length, the spacings between the Z-line and the antibody and between the antibody and the thick filaments increase with I-band length identically. These results indicate that the connectin filaments remain bound to the thick filaments in active fibers, and that the elastic properties of connectin are unaltered by calcium ions and cross-bridge activity.

MeSH Terms
Actin Cytoskeleton/drug effects,physiology,ultrastructure Animals Antibodies, Monoclonal Calcium/pharmacology Connectin Cytoskeleton/physiology Elasticity Electrophoresis, Polyacrylamide Gel Immunoblotting In Vitro Techniques Membrane Proteins/physiology Microscopy, Electron Muscle Contraction Muscle Proteins/analysis,physiology Muscles/physiology,ultrastructure Myofibrils/physiology Protein Kinases Rabbits Sarcomeres/physiology,ultrastructure
Chemicals
Antibodies, Monoclonal Connectin Membrane Proteins Muscle Proteins Protein Kinases Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Horowits R
National Institute of Arthritis and Musculoskeletal and Skin Diseases, Bethesda, Maryland 20892.
Maruyama K
Podolsky R J
References (21)
21 references, click to expand
  1. Does titin regulate the length of muscle thick filaments?
    J Mol Biol. 1989 Jan 5;205(1):263-8 PMID: 2926807
  2. Titin: major myofibrillar components of striated muscle.
    Proc Natl Acad Sci U S A. 1979 Aug;76(8):3698-702 PMID: 291034
  3. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane.
    Biochemistry. 1971 Jun 22;10(13):2606-17 PMID: 4326772
  4. Giant polypeptides of skeletal muscle titin: sedimentation equilibrium in guanidine hydrochloride.
    Biochem Biophys Res Commun. 1988 Feb 15;150(3):1155-61 PMID: 3342063
  5. Molecular size and shape of beta-connectin, an elastic protein of striated muscle.
    J Biochem. 1984 May;95(5):1423-33 PMID: 6746614
  6. Connectin filaments link thick filaments and Z lines in frog skeletal muscle as revealed by immunoelectron microscopy.
    J Cell Biol. 1985 Dec;101(6):2167-72 PMID: 3905821
  7. Sarcomere-associated cytoskeletal lattices in striated muscle. Review and hypothesis.
    Cell Muscle Motil. 1985;6:315-69 PMID: 3888377
  8. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  9. The positional stability of thick filaments in activated skeletal muscle depends on sarcomere length: evidence for the role of titin filaments.
    J Cell Biol. 1987 Nov;105(5):2217-23 PMID: 3680378
  10. Control of sarcomere length in skinned muscle fibres of Rana temporaria during mechanical transients.
    J Physiol. 1984 May;350:497-518 PMID: 6611404
  11. 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
  12. Thick filament movement and isometric tension in activated skeletal muscle.
    Biophys J. 1988 Jul;54(1):165-71 PMID: 3416026
  13. A physiological role for titin and nebulin in skeletal muscle.
    Nature. 1986 Sep 11-17;323(6084):160-4 PMID: 3755803
  14. Monoclonal antibodies distinguish titins from heart and skeletal muscle.
    J Cell Biol. 1986 Mar;102(3):1099-108 PMID: 3512578
  15. Human skeletal muscle: properties of the "chemically skinned%" fiber.
    Science. 1975 Mar 21;187(4181):1075-6 PMID: 17799688
  16. FILAMENT LENGTHS IN STRIATED MUSCLE.
    J Cell Biol. 1963 Nov;19:369-90 PMID: 14086763
  17. 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
  18. Purification and properties of native titin.
    J Mol Biol. 1984 Dec 5;180(2):331-56 PMID: 6512859
  19. Electron microscope studies of thick filaments from vertebrate skeletal muscle.
    J Mol Biol. 1979 Jun 15;131(1):133-6 PMID: 490643
  20. Myofibrillar interaction of blot immunoaffinity-purified antibodies against native titin as studied by direct immunofluorescence and immunogold staining.
    Eur J Cell Biol. 1986 Apr;40(2):176-84 PMID: 3519219
  21. Connectin, an elastic protein of muscle. Characterization and Function.
    J Biochem. 1977 Aug;82(2):317-37 PMID: 914784
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1989-11-00
Pages
2169-76
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2115863
Subset
IM
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