The effects of PKCα phosphorylation on the extensibility of titin's PEVK element

Journal of Structural Biology

Volumn 170, Issue 2, 2010, Pages 270-277

  Anderson, Brian R ^a,c   Bogomolovas, Julius ^b   Labeit, Siegfried ^b   Granzier, Henk ^c  

^a University of Arizona   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Passive tension; Post translational modifications; Single molecule mechanics

Indexed keywords

ALANINE; CONNECTIN; PROTEIN KINASE C ALPHA; RECOMBINANT PROTEIN; SERINE; ISOPROTEIN; MUSCLE PROTEIN; PROTEIN KINASE;

ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HEART MUSCLE COMPLIANCE; MOLECULAR MECHANICS; MUTANT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; WILD TYPE; ANIMAL; ATOMIC FORCE MICROSCOPY; CHEMISTRY; CYTOLOGY; ELASTICITY; GENETICS; HEART CONTRACTION; HEART MUSCLE; HUMAN; INSTRUMENTATION; METABOLISM; METHODOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; SITE DIRECTED MUTAGENESIS; SKELETAL MUSCLE;

ANIMALS; ELASTICITY; HUMANS; MICROSCOPY, ATOMIC FORCE; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUTAGENESIS, SITE-DIRECTED; MYOCARDIAL CONTRACTION; MYOCARDIUM; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN KINASE C-ALPHA; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 77951977209     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2010.02.002     Document Type: Article

References (43)

1. Andrew C.D., et al. Effect of phosphorylation on alpha-helix stability as a function of position. Biochemistry 2002, 41(6):1897-1905.
2. Bang M.L., et al. The complete gene sequence of titin, expression of an unusual approximately 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circ. Res. 2001, 89(11):1065-1072.
3. Baumann C.G., et al. Ionic effects on the elasticity of single DNA molecules. Proc. Natl. Acad. Sci. USA 1997, 94(12):6185-6190.
4. Belin R.J., et al. Augmented protein kinase C-alpha-induced myofilament protein phosphorylation contributes to myofilament dysfunction in experimental congestive heart failure. Circ. Res. 2007, 101(2):195-204.
5. Borbely A., et al. Hypophosphorylation of the stiff N2B titin isoform raises cardiomyocyte resting tension in failing human myocardium. Circ. Res. 2009, 104(6):780-786.
6. 2+-sensitive isoforms in the failing human heart. Circulation 1999, 99(3):384-391.
7. Bustamante C., et al. Entropic elasticity of lambda-phage DNA. Science 1994, 265(5178):1599-1600.
8. Forbes J.G., et al. Titin PEVK segment: charge-driven elasticity of the open and flexible polyampholyte. J. Muscle Res. Cell Motil. 2005, 26(6-8):291-301.
9. Freiburg A., et al. Series of exon-skipping events in the elastic spring region of titin as the structural basis for myofibrillar elastic diversity. Circ. Res. 2000, 86(11):1114-1121.
10. Furst D.O., et al. 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, 106(5):1563-1572.
11. Granzier H.L., Labeit S. Titin and its associated proteins: the third myofilament system of the sarcomere. Adv. Protein Chem. 2005, 71:89-119.
12. Granzier H., Labeit S. Structure-function relations of the giant elastic protein titin in striated and smooth muscle cells. Muscle Nerve 2007, 36(6):740-755.
13. Granzier H.L., et al. Truncation of titin's elastic PEVK region leads to cardiomyopathy with diastolic dysfunction. Circ. Res. 2009, 105(6):557-564.
14. Greaser M. Identification of new repeating motifs in titin. Proteins 2001, 43(2):145-149.
15. Gutierrez-Cruz G., Van Heerden A.H., Wang K. Modular motif, structural folds and affinity profiles of the PEVK segment of human fetal skeletal muscle titin. J. Biol. Chem. 2001, 276(10):7442-7449.
16. Hambleton M., et al. Pharmacological- and gene therapy-based inhibition of protein kinase Calpha/beta enhances cardiac contractility and attenuates heart failure. Circulation 2006, 114(6):574-582.
17. Hidalgo C., et al. PKC phosphorylation of titin's PEVK element: a novel and conserved pathway for modulating myocardial stiffness. Circ. Res. 2009, 105(7):631-638. 17 p following 638.
18. Horowits R., et al. A physiological role for titin and nebulin in skeletal muscle. Nature 1986, 323(6084):160-164.
19. Kellermayer M.S., et al. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science 1997, 276(5315):1112-1116.
20. Kellermayer M.S., et al. Mechanical fatigue in repetitively stretched single molecules of titin. Biophys. J. 2001, 80(2):852-863.
21. Kruger M., et al. Protein kinase G modulates human myocardial passive stiffness by phosphorylation of the titin springs. Circ. Res. 2009, 104(1):87-94.
22. Labeit S., Kolmerer B. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science 1995, 270(5234):293-296.
23. Labeit D., et al. Calcium-dependent molecular spring elements in the giant protein titin. Proc. Natl. Acad. Sci. USA 2003, 100(23):13716-13721.
24. Lahmers S., et al. Developmental control of titin isoform expression and passive stiffness in fetal and neonatal myocardium. Circ. Res. 2004, 94(4):505-513.
25. Letunic I., Doerks T., Bork P. SMART 6: recent updates and new developments. Nucleic Acids Res. 2009, 37(Database issue):D229-D232.
26. Li H., et al. Multiple conformations of PEVK proteins detected by single-molecule techniques. Proc. Natl. Acad. Sci. USA 2001, 98(19):10682-10686.
27. Linke W.A., et al. PEVK domain of titin: an entropic spring with actin-binding properties. J. Struct. Biol. 2002, 137(1-2):194-205.
28. Liu Q., et al. Protein kinase C{alpha}, but not PKC{beta} or PKC{gamma}, regulates contractility and heart failure susceptibility: implications for ruboxistaurin as a novel therapeutic approach. Circ. Res. 2009, 105(2):194-200.
29. Ma K., Kan L., Wang K. Polyproline II helix is a key structural motif of the elastic PEVK segment of titin. Biochemistry 2001, 40(12):3427-3438.
30. MacArthur M.W., Thornton J.M. Influence of proline residues on protein conformation. J. Mol. Biol. 1991, 218(2):397-412.
31. Moroz J.D., Nelson P. Torsional directed walks, entropic elasticity, and DNA twist stiffness. Proc. Natl. Acad. Sci. USA 1997, 94(26):14418-14422.
32. Murphy S., Frishman W.H. Protein kinase C in cardiac disease and as a potential therapeutic target. Cardiol. Rev. 2005, 13(1):3-12.
33. Pass J.M., et al. Enhanced PKC beta II translocation and PKC beta II-RACK1 interactions in PKC epsilon-induced heart failure: a role for RACK1. Am. J. Physiol. Heart Circ. Physiol. 2001, 281(6):H2500-H2510.
34. Ping P., et al. Ischemic preconditioning induces selective translocation of protein kinase C isoforms epsilon and eta in the heart of conscious rabbits without subcellular redistribution of total protein kinase C activity. Circ. Res. 1997, 81(3):404-414.
35. Radke M.H., et al. Targeted deletion of titin N2B region leads to diastolic dysfunction and cardiac atrophy. Proc. Natl. Acad. Sci. USA 2007, 104(9):3444-3449.
36. Rief M., et al. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 1997, 276(5315):1109-1112.
37. Schultz J., et al. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA 1998, 95(11):5857-5864.
38. Trombitas K., et al. Extensibility of isoforms of cardiac titin: variation in contour length of molecular subsegments provides a basis for cellular passive stiffness diversity. Biophys. J. 2000, 79(6):3226-3234.
39. Watanabe K., et al. Molecular mechanics of cardiac titin's PEVK and N2B spring elements. J. Biol. Chem. 2002, 277(13):11549-11558.
40. Williamson M.P. The structure and function of proline-rich regions in proteins. Biochem. J. 1994, 297(Pt. 2):249-260.
41. Wu Y., et al. Changes in titin isoform expression in pacing-induced cardiac failure give rise to increased passive muscle stiffness. Circulation 2002, 106(11):1384-1389.
42. Yamasaki R., et al. Protein kinase A phosphorylates titin's cardiac-specific N2B domain and reduces passive tension in rat cardiac myocytes. Circ. Res. 2002, 90(11):1181-1188.
43. Zhu Y., et al. Single molecule force spectroscopy of cardiac titin's N2B element-effects of the molecular chaperone alpha B-crystallin with disease causing mutations. J. Biol. Chem. 2009, 284(20):13914-13923.