Home LiteratureArticle Details
PMID: 8884600 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Assembly of the cardiac I-band region of titin/connectin: expression of the cardiac-specific regions and their structural relation to the elastic segments.

Journal of muscle research and cell motility ·Vol. 17 ·No. 4 ·1996-08-00 ·Pages 449-61

Gautel M, Lehtonen E, Pietruschka F

Abstract

The giant molecule titin (also called connectin) provides an elastic connection in the I-band between the Z-disk and A-band of striated muscle. This region is assembled in a tissue-specific way by extensive differential splicing events. We have raised monoclonal antibodies against the two N2-line isoforms of titin and demonstrate that both forms of cardiac I-band titin are constitutively co-expressed in atrial and ventricular muscle. In developing mouse embryos, the expression of the cardiac N2-B isoform remains strictly cardiac-specific and is linked to the expression of the ubiquitous N2-A isoform. The mechanical function of the cardiac N2-line region was investigated ultrastructurally. Immunoelectron microscopy reveals that the N2-B region separates two mechanically distinct sections of titin with a hyperextensible segment spanning the distance to the Z-disk. The formation of a plateau in the extension of cardiac titin rules out that Ig-domains can be unfolded as a mechanism of elasticity.

MeSH Terms
Animals Calmodulin-Binding Proteins/metabolism Carrier Proteins/metabolism Connectin Fluorescent Antibody Technique, Indirect Humans Membrane Proteins/metabolism Mice Microscopy, Immunoelectron Muscle Proteins/metabolism Myocardium/metabolism Polymerase Chain Reaction Protein Kinases/metabolism Sarcomeres/metabolism
Chemicals
Calmodulin-Binding Proteins Carrier Proteins Connectin Membrane Proteins Muscle Proteins TTN protein, human Protein Kinases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Gautel M
European Molecular Biology Laboratory, Biological Structures Division, Heidelberg, Germany.
Lehtonen E
Pietruschka F
References (38)
38 references, click to expand
  1. Connectin, an elastic protein from myofibrils.
    J Biochem. 1976 Aug;80(2):405-7 PMID: 1002676
  2. Does titin regulate the length of muscle thick filaments?
    J Mol Biol. 1989 Jan 5;205(1):263-8 PMID: 2926807
  3. Titin: major myofibrillar components of striated muscle.
    Proc Natl Acad Sci U S A. 1979 Aug;76(8):3698-702 PMID: 291034
  4. New elastic protein from muscle.
    Nature. 1976 Jul 1;262(5563):58-60 PMID: 934326
  5. A novel domain sequence of connectin localized at the I band of skeletal muscle sarcomeres: homology to neurofilament subunits.
    Biochem Biophys Res Commun. 1993 Aug 16;194(3):1288-91 PMID: 8352787
  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. Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis.
    Development. 1995 Jan;121(1):37-51 PMID: 7867507
  8. Elastic properties of the titin filament in the Z-line region of vertebrate striated muscle.
    J Muscle Res Cell Motil. 1993 Aug;14(4):416-22 PMID: 8227300
  9. Immunoglobulin-type domains of titin: same fold, different stability?
    Biochemistry. 1994 Apr 19;33(15):4730-7 PMID: 8161531
  10. 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
  11. Connectin, an elastic protein of striated muscle.
    Biophys Chem. 1994 May;50(1-2):73-85 PMID: 8011942
  12. 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
  13. Structure and function of titin and nebulin.
    Curr Opin Cell Biol. 1995 Feb;7(1):32-8 PMID: 7755987
  14. Myogenesis in the mouse embryo: differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly.
    J Cell Biol. 1989 Aug;109(2):517-27 PMID: 2474551
  15. 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
  16. Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments.
    Biophys J. 1995 Mar;68(3):1027-44 PMID: 7756523
  17. The elastic I-band region of titin is assembled in a "modular" fashion by weakly interacting Ig-like domains.
    J Mol Biol. 1996 Feb 2;255(4):604-16 PMID: 8568900
  18. Contractile proteins and myofibrillogenesis.
    Int Rev Cytol. 1993;143:153-89 PMID: 8449663
  19. Cytoskeleton in preimplantation mouse development.
    Cell Differ. 1988 Aug;24(3):165-77 PMID: 3061662
  20. Titins: giant proteins in charge of muscle ultrastructure and elasticity.
    Science. 1995 Oct 13;270(5234):293-6 PMID: 7569978
  21. The structure of proteins; two hydrogen-bonded helical configurations of the polypeptide chain.
    Proc Natl Acad Sci U S A. 1951 Apr;37(4):205-11 PMID: 14816373
  22. Monoclonal antibodies distinguish titins from heart and skeletal muscle.
    J Cell Biol. 1986 Mar;102(3):1099-108 PMID: 3512578
  23. The anatomy of a molecular giant: how the sarcomere cytoskeleton is assembled from immunoglobulin superfamily molecules.
    J Mol Cell Cardiol. 1995 Apr;27(4):951-9 PMID: 7563107
  24. Reversible unfolding of fibronectin type III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin and fibronectin.
    Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):10114-8 PMID: 7937847
  25. Epithelial-mesenchymal interactions regulate the stage-specific expression of a cell surface proteoglycan, syndecan, in the developing kidney.
    Dev Biol. 1989 Aug;134(2):382-91 PMID: 2663574
  26. Immunocytochemical studies using a monoclonal antibody to bovine cardiac titin on intact and extracted myofibrils.
    J Muscle Res Cell Motil. 1985 Jun;6(3):293-312 PMID: 3905857
  27. 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
  28. 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
  29. The mechanically active domain of titin in cardiac muscle.
    Circ Res. 1995 Oct;77(4):856-61 PMID: 7554133
  30. A method to reconstruct myocardial sarcomere lengths and orientations at transmural sites in beating canine hearts.
    Am J Physiol. 1992 Jul;263(1 Pt 2):H293-306 PMID: 1636767
  31. Immunoglobulin-type domains of titin are stabilized by amino-terminal extension.
    FEBS Lett. 1994 Sep 19;352(1):27-31 PMID: 7925935
  32. Towards a molecular understanding of titin.
    EMBO J. 1992 May;11(5):1711-6 PMID: 1582406
  33. The cytoskeleton and associated proteins during cleavage, compaction and blastocyst differentiation in the pig.
    Differentiation. 1993 Aug;54(1):35-45 PMID: 7691669
  34. Elastic filaments in situ in cardiac muscle: deep-etch replica analysis in combination with selective removal of actin and myosin filaments.
    J Cell Biol. 1993 Feb;120(3):711-24 PMID: 8425898
  35. Tertiary structure of an immunoglobulin-like domain from the giant muscle protein titin: a new member of the I set.
    Structure. 1995 Apr 15;3(4):391-401 PMID: 7613868
  36. Connectin, an elastic protein of muscle. Characterization and Function.
    J Biochem. 1977 Aug;82(2):317-37 PMID: 914784
  37. Titin and nebulin: protein rulers in muscle?
    Trends Biochem Sci. 1994 Oct;19(10):405-9 PMID: 7817397
  38. Rigor crossbridge structure in tilted single filament layers and flared-X formations from insect flight muscle.
    J Mol Biol. 1985 Sep 5;185(1):145-76 PMID: 4046036
Article Info
Journal
Journal of muscle research and cell motility
Abbr.
J Muscle Res Cell Motil
ISSN
0142-4319
Published
1996-08-00
Pages
449-61
Language
English
Region
Netherlands
NLM ID
8006298
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com