Regulation of actin-myosin interaction by conserved periodic sites of tropomyosin

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

Volumn 109, Issue 45, 2012, Pages 18425-18430

  Barua, Bipasha ^a   Winkelmann, Donald A ^a   White, Howard D ^b   Hitchcock DeGregori, Sarah E ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

Actin filament structure; Cell motility; Cytoskeleton; Motility assay; Muscle contraction

Indexed keywords

ACTIN; CALCIUM ION; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; TROPOMYOSIN;

ACTIN FILAMENT; ACTIN MYOSIN INTERACTION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; GENETIC CONSERVATION; LIGHT SCATTERING; MOLECULAR MODEL; MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; REGULATORY MECHANISM; STATIC ELECTRICITY; STEREOSPECIFICITY;

ACTIN CYTOSKELETON; ACTINS; ADENOSINE DIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; FLUORESCENCE; IODOACETAMIDE; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; MYOSINS; PHOSPHATES; PROTEIN BINDING; PROTEIN TRANSPORT; RATS; SCATTERING, RADIATION; TROPOMYOSIN; TROPONIN;

EID: 84868579508     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1212754109     Document Type: Article

References (45)

1. Pollard TD, Cooper JA (2009) Actin, a central player in cell shape and movement. Science 326(5957):1208-1212.
2. Wang CL, Coluccio LM (2010) New insights into the regulation of the actin cytoskeleton by tropomyosin. Int Rev Cell Mol Biol 281:91-128.
3. Gunning P, O 'Neill G, Hardeman E (2008) Tropomyosin-based regulation of the actin cytoskeleton in time and space. Physiol Rev 88(1):1-35.
4. Clayton JE, Sammons MR, Stark BC, Hodges AR, Lord M (2010) Differential regulation of unconventional fission yeast myosins via the actin track. Curr Biol 20(16): 1423-1431.
5. Ostap EM (2008) Tropomyosins as discriminators of myosin function. Adv Exp Med Biol 644:273-282.
6. Fanning AS, Wolenski JS, Mooseker MS, Izant JG (1994) Differential regulation of skeletal muscle myosin-II and brush border myosin-I enzymology and mechanochemistry by bacterially produced tropomyosin isoforms. Cell Motil Cytoskeleton 29 (1):29-45. (Pubitemid 24278004)
7. Lehrer SS, Morris EP (1984) Comparison of the effects of smooth and skeletal tropomyosin on skeletal actomyosin subfragment 1 ATPase. J Biol Chem 259(4):2070-2072. (Pubitemid 14190310)
8. Vibert P, Craig R, Lehman W (1997) Steric-model for activation of muscle thin filaments. J Mol Biol 266(1):8- 14.
9. Milligan RA, Flicker PF (1987) Structural relationships of actin, myosin, and tropomyosin revealed by cryo-electron microscopy. J Cell Biol 105(1):29-39.
10. Behrmann E, et al. (2012) Structure of the rigor actin-tropomyosin-myosin complex. Cell 150(2):327-338.
11. McKillop DF, Geeves MA (1993) Regulation of the interaction between actin and myosin subfragment 1: Evidence for three states of the thin filament. Biophys J 65(2): 693-701. (Pubitemid 23263882)
12. Heeley DH, Belknap B, White HD (2006) Maximal activation of skeletal muscle thin filaments requires both rigor myosin S1 and calcium. J Biol Chem 281(1):668-676. (Pubitemid 43671230)
13. Greene LE, Eisenberg E (1980) Cooperative binding of myosin subfragment-1 to the actin-troponin-tropomyosin complex. Proc Natl Acad Sci USA 77(5):2616- 2620.
14. Lehrer SS, Morris EP (1982) Dual effects of tropomyosin and troponin-tropomyosin on actomyosin subfragment 1 ATPase. J Biol Chem 257(14):8073-8080.
15. Eaton BL (1976) Tropomyosin binding to F-actin induced by myosin heads. Science 192 (4246):1337-1339.
16. Trybus KM, Taylor EW (1980) Kinetic studies of the cooperative binding of subfragment 1 to regulated actin. Proc Natl Acad Sci USA 77(12):7209-7213. (Pubitemid 11189442)
17. Bremel RD, Weber A (1972) Cooperation within actin filament in vertebrate skeletal muscle. Nat New Biol 238(82):97-101.
18. Landis C, Back N, Homsher E, Tobacman LS (1999) Effects of tropomyosin internal deletions on thin filament function. J Biol Chem 274(44):31279-31285.
19. Hitchcock-DeGregori SE, Song Y, Greenfield NJ (2002) Functions of tropomyosin's periodic repeats. Biochemistry 41(50):15036-15044. (Pubitemid 35470683)
20. Kawai M, Lu X, Hitchcock-Degregori SE, Stanton KJ, Wandling MW (2009) Tropomyosin period 3 is essential for enhancement of isometric tension in thin filament-reconstituted bovine myocardium. J Biophys 2009:380967.
21. Oguchi Y, Ishizuka J, Hitchcock-DeGregori SE, Ishiwata S, Kawai M (2011) The role of tropomyosin domains in cooperative activation of the actin-myosin interaction. J Mol Biol 414(5):667-680.
22. Lehman W, et al. (2000) Tropomyosin and actin isoforms modulate the localization of tropomyosin strands on actin filaments. J Mol Biol 302(3):593-606.
23. Barua B, Pamula MC, Hitchcock-DeGregori SE (2011) Evolutionarily conserved surface residues constitute actin binding sites of tropomyosin. Proc Natl Acad Sci USA 108(25): 10150-10155.
24. Fraser ID, Marston SB (1995) In vitro motility analysis of actin-tropomyosin regulation by troponin and calcium. The thin filament is switched as a single cooperative unit. J Biol Chem 270(14):7836-7841.
25. VanBuren P, Palmiter KA, Warshaw DM (1999) Tropomyosin directly modulates actomyosin mechanical performance at the level of a single actin filament. Proc Natl Acad Sci USA 96(22):12488-12493. (Pubitemid 29513529)
26. Nagashima H, Asakura S (1982) Studies on co-operative properties of tropomyosinactin and tropomyosin-troponin-actin complexes by the use of N-ethylmaleimidetreated and untreated species of myosin subfragment 1. J Mol Biol 155(4):409-428. (Pubitemid 12117709)
27. Pemrick S, Weber A (1976) Mechanism of inhibition of relaxation by N-ethylmaleimide treatment of myosin. Biochemistry 15(23):5193-5198.
28. Williams DL, Jr., Greene LE, Eisenberg E (1988) Cooperative turning on of myosin subfragment 1 adenosinetriphosphatase activity by the troponin-tropomyosin-actin complex. Biochemistry 27(18):6987-6993.
29. Gordon AM, Homsher E, Regnier M (2000) Regulation of contraction in striated muscle. Physiol Rev 80(2):853-924. (Pubitemid 30164950)
30. Kad NM, Kim S, Warshaw DM, VanBuren P, Baker JE (2005) Single-myosin crossbridge interactions with actin filaments regulated by troponin-tropomyosin. Proc Natl Acad Sci USA 102(47):16990-16995. (Pubitemid 41692671)
31. Ishii Y, Lehrer SS (1990) Excimer fluorescence of pyrenyliodoacetamide- labeled tropomyosin: A probe of the state of tropomyosin in reconstituted muscle thin filaments. Biochemistry 29(5):1160-1166. (Pubitemid 20053837)
32. Geeves MA, Lehrer SS (1994) Dynamics of the muscle thin filament regulatory switch: The size of the cooperative unit. Biophys J 67(1):273-282. (Pubitemid 24197892)
33. Brown JH, et al. (2005) Structure of the mid-region of tropomyosin: Bending and binding sites for actin. Proc Natl Acad Sci USA 102(52):18878-18883. (Pubitemid 43049535)
34. Nitanai Y, Minakata S, Maeda K, Oda N, Maéda Y (2007) Crystal structures of tropomyosin: Flexible coiled-coil. Adv Exp Med Biol 592:137-151.
35. El-Saleh SC, Thieret R, Johnson P, Potter JD (1984) Modification of Lys-237 on actin by 2,4-pentanedione. Alteration of the interaction of actin with tropomyosin. J Biol Chem 259(17):11014-11021. (Pubitemid 14030185)
36. Gerson JH, Bobkova E, Homsher E, Reisler E (1999) Role of residues 311/312 in actin-tropomyosin interaction. In vitro motility study using yeast actin mutant e311a/r312a. J Biol Chem 274(25):17545-17550.
37. Saeki K, Sutoh K, Wakabayashi T (1996) Tropomyosin-binding site(s) on the Dictyostelium actin surface as identified by site-directed mutagenesis. Biochemistry 35(46): 14465-14472. (Pubitemid 26423705)
38. Szilagyi L, Lu RC (1982) Changes of lysine reactivities of actin in complex with myosin subfragment-1, tropomyosin and troponin. Biochim Biophys Acta 709(2):204-211. (Pubitemid 13156028)
39. Tao T, Lamkin M (1984) Crosslinking of tropomyosin to myosin subfragment-1 in reconstituted rabbit skeletal thin filaments. FEBS Lett 168(1):169-173.
40. Li XE, et al. (2011) Tropomyosin position on F-actin revealed by EM reconstruction and computational chemistry. Biophys J 100(4):1005-1013.
41. McLachlan AD, Stewart M (1976) The 14-fold periodicity in alpha-tropomyosin and the interaction with actin. J Mol Biol 103(2):271-298.
42. Winkelmann DA, Bourdieu L, Ott A, Kinose F, Libchaber A (1995) Flexibility of myosin attachment to surfaces infl uences F-actin motion. Biophys J 68(6):2444-2453.
43. Whitby FG, Phillips GN, Jr. (2000) Crystal structure of tropomyosin at 7 Angstroms resolution. Proteins 38(1):49-59. (Pubitemid 30020602)
44. Greenfield NJ, et al. (2006) Solution NMR structure of the junction between tropomyosin molecules: Implications for actin binding and regulation. J Mol Biol 364(1): 80-96. (Pubitemid 44634526)
45. Pettersen EF, et al. (2004) UCSF Chimera - A visualization system for exploratory research and analysis. J Comput Chem 25(13):1605-1612.