Fast-folding α-helices as reversible strain absorbers in the muscle protein myomesin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 34, 2011, Pages 14139-14144

  Berkemeier, Felix ^a   Bertz, Morten ^a,b   Xiao, Senbo ^c,d   Pinotsis, Nikos ^e   Wilmanns, Matthias ^e   Gräter, Frauke ^c,d   Rief, Matthias ^a,f  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b WASEDA UNIVERSITY   (Japan)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^d HEIDELBERG INSTITUTE FOR THEORETICAL STUDIES   (Germany)

^e DESY   (Germany)

^f Munich Center for Integrated Protein Science   (Germany)

Author keywords

Atomic force microscopy; Protein folding

Indexed keywords

DIMER; HOMODIMER; IMMUNOGLOBULIN; MUSCLE PROTEIN; MY12 PROTEIN; MY13 PROTEIN; MYOMESIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; ATOMIC FORCE MICROSCOPY; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE;

BIOMECHANICS; KINETICS; MICROSCOPY, ATOMIC FORCE; MOLECULAR DYNAMICS SIMULATION; MUSCLE PROTEINS; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN UNFOLDING;

EID: 80052140214     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1105734108     Document Type: Article

References (53)

1. Au Y (2004) The muscle ultrastructure: A structural perspective of the sarcomere. Cell Mol Life Sci 61:3016-3033.
2. Gregorio CC, Granzier H, Sorimachi H, Labeit S (1999) Muscle assembly: A titanic achievement? Curr Opin Cell Biol 11:18-25.
3. Li H, et al. (2002) Reverse engineering of the giant muscle protein titin. Nature 418:998-1002. (Pubitemid 34976037)
4. Puchner EM, et al. (2008) Mechanoenzymatics of titin kinase. Proc Natl Acad Sci USA 105:13385-13390.
5. Granzier HL, Labeit S (2005) Titin and its associated proteins: The third myofilament system of the sarcomere. Adv Protein Chem 71:89-119. (Pubitemid 41446927)
6. Grove BK, et al. (1984) A new 185,000-dalton skeletal muscle protein detected by monoclonal antibodies. J Cell Biol 98:518-524. (Pubitemid 14196470)
7. Squire JM, Al-Khayat HA, Knupp C, Luther PK (2005) Molecular architecture in muscle contractile assemblies. Adv Protein Chem 71:17-87. (Pubitemid 41446926)
8. Obermann WM, Plessmann U, Weber K, Fürst DO (1995) Purification and biochemical characterization of myomesin, a myosin-binding and titin-binding protein, from bovine skeletal muscle. Eur J Biochem 233:110-115.
9. Obermann WM, Gautel M, Weber K, Fürst DO (1997) Molecular structure of the sarcomeric M band: Mapping of titin and myosin binding domains in myomesin and the identification of a potential regulatory phosphorylation site in myomesin. EMBO J 16:211-220. (Pubitemid 27049379)
10. Fukuzawa A, et al. (2008) Interactions with titin and myomesin target obscurin and obscurin-like 1 to the M-band: implications for hereditary myopathies. J Cell Sci 121:1841-1851. (Pubitemid 351943377)
11. Lange S, et al. (2005) Dimerisation of myomesin: Implications for the structure of the sarcomeric M-band. J Mol Biol 345:289-298. (Pubitemid 39574851)
12. Potthoff MJ, et al. (2007) Regulation of skeletal muscle sarcomere integrity and postnatal muscle function by Mef2c. Mol Cell Biol 27:8143-8151. (Pubitemid 350234229)
13. Ehler E, Rothen BM, Hämmerle SP, Komiyama M, Perriard JC (1999) Myofibrillogenesis in the developing chicken heart: Assembly of Z-disk, M-line, and the thick filaments. J Cell Sci 112:1529-1539. (Pubitemid 29261315)
14. Agarkova I, Ehler E, Lange S, Schoenauer R, Perriard J-C (2003) M-band: A safeguard for sarcomere stability? J Muscle Res Cell Motil 24:191-203.
15. Agarkova I, Perriard J-C (2005) The M-band: An elastic web that crosslinks thick filaments in the center of the sarcomere. Trends Cell Biol 15:477-485. (Pubitemid 41253467)
16. Bertoncini P, et al. (2005) Study of the mechanical properties of myomesin proteins using dynamic force spectroscopy. J Mol Biol 348:1127-1137. (Pubitemid 40602371)
17. Schoenauer R, et al. (2005) Myomesin is a molecular spring with adaptable elasticity. J Mol Biol 349:367-379. (Pubitemid 40693755)
18. Pinotsis N, Lange S, Perriard J-C, Svergun DI,WilmannsM(2008) Molecular basis of the C-terminal tail-to-tail assembly of the sarcomeric filament protein myomesin. EMBO J 27:253-264.
19. Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276:1109-1112. (Pubitemid 27218118)
20. Schwaiger I, Schleicher M, Noegel AA, Rief M (2005) The folding pathway of a fastfolding immunoglobulin domain revealed by single-molecule mechanical experiments. EMBO Rep 6:46-51. (Pubitemid 41710073)
21. Schwaiger I, Sattler C, Hostetter DR, Rief M (2002) The myosin coiled-coil is a truly elastic protein structure. Nat Mater 1:232-235.
22. Rief M, Pascual J, Saraste M, Gaub HE (1999) Single molecule force spectroscopy of spectrin repeats: Low unfolding forces in helix bundles. J Mol Biol 286:553-561. (Pubitemid 29090169)
23. Li L, Wetzel S, Plückthun A, Fernandez JM (2006) Stepwise unfolding of ankyrin repeats in a single protein revealed by atomic force microscopy. Biophys J 90:L30-32.
24. Marszalek PE, et al. (1999) Mechanical unfolding intermediates in titin modules. Nature 402:100-103.
25. Cao Y, Lam C, Wang M, Li H (2006) Nonmechanical protein can have significant mechanical stability. Angew Chem Int Ed Engl 45:642-645. (Pubitemid 43121465)
26. Puchner EM, Franzen G, Gautel M, Gaub HE (2008) Comparing proteins by their unfolding pattern. Biophys J 95:426-434.
27. Rabiner L, Juang B (1986) An introduction to hidden Markov models. IEEE ASSP Mag 3:4-16.
28. Eddy SR (2004) What is a hidden Markov model? Nat Biotechnol 22:1315-1316.
29. Oberbarnscheidt L, Janissen R, Oesterhelt F (2009) Direct and model free calculation of force-dependent dissociation rates from force spectroscopic data. Biophys J 97:L19-21.
30. Bell GI (1978) Models for the specific adhesion of cells to cells. Science 200:618-627.
31. Evans E, Ritchie K (1997) Dynamic strength of molecular adhesion bonds. Biophys J 72:1541-1555. (Pubitemid 27133095)
32. Schlierf M, Berkemeier F, Rief M (2007) Direct observation of active protein folding using lock-in force spectroscopy. Biophys J 93:3989-3998. (Pubitemid 350223814)
33. Gebhardt JCM, Bornschlögl T, Rief M (2010) Full distance-resolved folding energy landscape of one single protein molecule. Proc Natl Acad Sci USA 107:2013-2018.
34. Bertz M, et al. (2010) Structural and mechanical hierarchies in the alpha-crystallin domain dimer of the hyperthermophilic small heat shock protein Hsp16.5. J Mol Biol 400:1046-1056.
35. Pernigo S, et al. (2010) Structural insight into M-band assembly and mechanics from the titin-obscurin-like-1 complex. Proc Natl Acad Sci USA 107:2908-2913.
36. Eaton WA, Muñoz V, Thompson PA, Chan CK, Hofrichter J (1997) Submillisecond kinetics of protein folding. Curr Opin Struct Biol 7:10-14. (Pubitemid 27092375)
37. Kubelka J, Hofrichter J, Eaton WA (2004) The protein folding "speed limit". Curr Opin Struct Biol 14:76-88.
38. Nunes JM, et al. (2010) A "force buffer" protecting immunoglobulin titin. Angew Chem Int Ed Engl 49:3528-3531.
39. Politou AS, Thomas DJ, Pastore A (1995) The folding and stability of titin immunoglobulin- like modules, with implications for the mechanism of elasticity. Biophys J 69:2601-2610.
40. Carrion-Vazquez M, et al. (1999) Mechanical and chemical unfolding of a single protein: A comparison. Proc Natl Acad Sci USA 96:3694-3699. (Pubitemid 29168972)
41. Huxley HE, Faruqi AR, Kress M, Bordas J, Koch MH (1982) Time-resolved X-ray diffraction studies of the myosin layer-line reflections during muscle contraction. J Mol Biol 158:637-684. (Pubitemid 12044690)
42. LinariM, et al. (2000) Interference fine structure and sarcomere length dependence of the axial X-ray pattern from active single muscle fibers. Proc Natl Acad Sci USA 97:7226-7231.
43. Knappeis GG, Carlsen F (1968) The ultrastructure of the M line in skeletal muscle. J Cell Biol 38:202-211.
44. Luther P, Squire J (1978) Three-dimensional structure of the vertebrate muscle M-region. J Mol Biol 125:313-324. (Pubitemid 9063905)
45. Obermann WM, et al. (1996) The structure of the sarcomeric M band: localization of defined domains of myomesin, M-protein, and the 250-kD carboxy-terminal region of titin by immunoelectron microscopy. J Cell Biol 134:1441-1453. (Pubitemid 26318017)
46. Gautel M (2011) The sarcomeric cytoskeleton: Who picks up the strain? Curr Opin Cell Biol 23:39-46.
47. Linke WA, Fernandez JM (2002) Cardiac titin: molecular basis of elasticity and cellular contribution to elastic and viscous stiffness components in myocardium. J Muscle Res Cell Motil 23:483-497. (Pubitemid 36583666)
48. Bertz M, Wilmanns M, Rief M (2009) The titin-telethonin complex is a directed, superstable molecular bond in the muscle Z-disk. Proc Natl Acad Sci USA 106:13307-13310.
49. Schwaiger I, Kardinal A, Schleicher M, Noegel AA, Rief M (2004) A mechanical unfolding intermediate in an actin-cross-linking protein. Nat Struct Mol Biol 11:81-85. (Pubitemid 38173445)
50. Junker JP, Ziegler F, RiefM(2009) Ligand-dependent equilibrium fluctuations of single calmodulin molecules. Science 323:633-637.
51. Grubmüller H, Heymann B, Tavan P (1996) Ligand binding: Molecular mechanics calculation of the streptavidin-biotin rupture force. Science 271:997-999. (Pubitemid 26066398)
52. Kutzner C, et al. (2007) Speeding up parallel GROMACS on high-latency networks. J Comput Chem 28:2075-2084. (Pubitemid 47153605)
53. Jorgensen WL, Tirado-Rives J (1988) The OPLS [optimized potentials for liquid simulations] potential functions for proteins, energy minimizations for crystals of cyclic peptides and crambin. J Am Chem Soc 110:1657-1666.