Kinetic analysis of the interactions between Troponin C (TnC) and Troponin I (TnI) binding peptides: Evidence for separate binding sites for the 'structural' N-terminus and the 'regulatory' C-terminus of TnI on TnC

Journal of Molecular Recognition

Volumn 16, Issue 1, 2003, Pages 37-53

  Tripet, Brian ^a   De Crescenzo, Gregory ^b   Grothe, Suzanne ^b   O'Connor McCourt, Maureen ^b   Hodges, Robert S ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Muscle regulation; Surface plasmon resonance; Troponin C; Troponin I

Indexed keywords

ANIMALS; BINDING SITES; CALCIUM; MAGNESIUM; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RABBITS; SPECTROMETRY, FLUORESCENCE; SURFACE PLASMON RESONANCE; TROPONIN C; TROPONIN I;

EID: 12244269333     PISSN: 09523499     EISSN: None     Source Type: Journal    
DOI: 10.1002/jmr.606     Document Type: Article

References (66)

1. Chong PC, Asselbergs PJ, Hodges RS. 1983. Inhibition of rabbit skeletal muscle acto-S1 ATPase by troponin T. FEBS Lett. 153: 372-376.
2. Dalgarno D, Grand R, Levine B, Moir A, Scott G, Perry S. 1982. Interaction between troponin I and troponin C. FEBS Lett. 150: 54-58.
3. De Crescenzo G, Grothe S, Lortie R, Debanne MT, O'Connor-McCourt M. 2000. Real-time kinetic studies on the interaction of transforming growth factor alpha with the epidermal growth factor receptor extracellular domain reveal a conformational change model. Biochemistry 39: 9466-9476.
4. De Crescenzo G, Grothe S, Zwaagstra J, Tsang M, O'Connor-McCourt MD. 2001. Real-time monitoring of the interactions of transforming growth factor- beta (TGF-beta) isoforms with latency-associated protein and the ectodomains of the TGF-beta type II and III receptors reveals different kinetic models and stoichiometries of binding. J. Biol. Chem. 276: 29632-29643.
5. Ding XL, Akella AB, Su H, Gulati J. 1994. The role of glycine (residue 89) in the central helix of EF-hand protein troponin-C exposed following amino-terminal alpha-helix deletion. Protein Sci. 3: 2089-2096.
6. Drabikowski W, Dalgarno DC, Levine BA, Gergely J, Grabarek Z, Leavis PC. 1985. Solution conformation of the C-terminal domain of skeletal troponin C. Cation, trifluoperazine and troponin I binding effects. Eur. J. Biochem. 151: 17-28.
7. Farah CS, Reinach FC. 1995. The troponin complex and regulation of muscle contraction. Faseb J. 9: 755-767.
8. Farah CS, Miyamoto CA, Ramos CH, da Silva AC, Quaggio RB, Fujimori K, Smillie LB, Reinach FC. 1994. Structural and regulatory functions of the NH2- and COOH-terminal regions of skeletal muscle troponin I. J. Biol. Chem. 269: 5230-5240.
9. Gagne SM, Tsuda S, Li MX, Smillie LB, Sykes BD. 1995. Structures of the troponin C regulatory domains in the apo and calcium- saturated states. Nat. Struct. Biol. 2: 784-789.
10. Grabarek Z, Drabikowski W, Leavis PC, Rosenfeld SS, Gergely J. 1981. Proteolytic fragments of troponin C. Interactions with the other troponin subunits and biological activity. J. Biol. Chem. 256: 13121-13127.
11. Herzberg O, James MN. 1985. Structure of the calcium regulatory muscle protein troponin-C at 2.8 A resolution. Nature 313: 653-659.
12. 2+-switch in the calmodulin superfamily. Structure 5: 1695-1711.
13. 2+ and subunit interactions on surface accessibility of cysteine residues in cardiac troponin. Biochemistry 27: 5891-5898.
14. Jha PK, Mao C, Sarkar S. 1996. Photo-cross-linking of rabbit skeletal troponin I deletion mutants with troponin C and its thiol mutants: the inhibitory region enhances binding of troponin I fragments to troponin C. Biochemistry 35: 11026-11035.
15. Johnsson B, Lofas S, Lindquist G. 1991. Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors. Anal. Biochem. 198: 268-277.
16. Kobayashi T, Tao T, Grabarek Z, Gergely J, Collins JH. 1991. Cross-linking of residue 57 in the regulatory domain of a mutant rabbit skeletal muscle troponin C to the inhibitory region of troponin I. J. Biol. Chem. 266: 13746-13751.
17. Kobayashi T, Tao T, Gergely J, Collins JH. 1994. Structure of the troponin complex. Implications of photocross-linking of troponin I to troponin C thiol mutants. J. Biol. Chem. 269: 5725-5729.
18. Kobayashi T, Leavis PC, Collins JH. 1996. Interaction of a troponin I inhibitory peptide with both domains of troponin C. Biochim. Biophys. Acta 1294: 25-30.
19. 2+-dependent interaction of the inhibitory region of troponin I with acidic residues in the N-terminal domain of troponin C. Biochim. Biophys. Acta. 1430: 214-221.
20. Kobayashi T, Zhao X, Wade R, Collins JH. 1999b. Involvement of conserved, acidic residues in the N-terminal domain of troponin C in calcium-dependent regulation. Biochemistry 38: 5386-5391.
21. Kretsinger RH, Nockolds CE. 1973. Carp muscle calcium-binding protein. II. Structure determination and general description. J. Biol. Chem. 248: 3313-3326.
22. Lan J, Albaugh S, Steiner RF. 1989. Interactions of troponin I and its inhibitory fragment (residues 104-115) with troponin C and calmodulin. Biochemistry 28: 7380-7385.
23. Leavis PC, Gowell E, Tao T. 1984. Fluorescence lifetime and acrylamide quenching studies of the interactions between troponin subunits. Biochemistry 23: 4156-4161.
24. Leszyk J, Collins JH, Leavis PC, Tao T. 1987. Cross-linking of rabbit skeletal muscle troponin with the photoactive reagent 4-maleimidobenzophenone: identification of residues in troponin I that are close to cysteine-98 of troponin C. Biochemistry 26: 7042-7047.
25. Leszyk J, Collins JH, Leavis PC, Tao T. 1988. Cross-linking of rabbit skeletal muscle troponin subunits: labeling of cysteine-98 of troponin C with 4-maleimidobenzophenone and analysis of products formed in the binary complex with troponin T and the ternary complex with troponins I and T. Biochemistry 27: 6983-6987.
26. Leszyk J, Grabarek Z, Gergely J, Collins JH. 1990. Characterization of zero-length cross-links between rabbit skeletal muscle troponin C and troponin I: evidence for direct interaction between the inhibitory region of troponin I and the NH2-terminal, regulatory domain of troponin C. Biochemistry 29: 299-304.
27. Leszyk J, Tao T, Nuwaysir LM, Gergely J. 1998. Identification of the photocrosslinking sites in troponin-I with 4-maleimidobenzophenone labelled mutant troponin-Cs having single cysteines at positions 158 and 21. J. Muscle Res. Cell Motil. 19: 479-490.
28. Li MX, Spyracopoulos L, Sykes BD. 1999. Binding of cardiac troponin-1147-163 induces a structural opening in human cardiac troponin-C. Biochemistry 38: 8289-8298.
29. Luo Y, Wu JL, Gergely J, Tao T. 1998. Localization of Cys133 of rabbit skeletal troponin-I with respect to troponin-C by resonance energy transfer. Biophys. J. 74: 3111-3119.
30. Luo Y, Leszyk J, Qian Y, Gergely J, Tao T. 1999. Residues 48 and 82 at the N-terminal hydrophobic pocket of rabbit skeletal muscle troponin-C photo-cross-link to Met121 of troponin-I. Biochemistry 38: 6678-6688.
31. Luo Y, Leszyk J, Li B, Gergely J, Tao T. 2000a. Proximity relationships between residue 6 of troponin I and residues in troponin C: further evidence for extended conformation of troponin C in the troponin complex. Biochemistry 39: 15306-15315.
32. Luo Y, Wu JL, Li B, Langsetmo K, Gergely J, Tao T. 2000b. Photocrosslinking of benzophenone-labeled single cysteine troponin I mutants to other thin filament proteins. J. Mol. Biol. 296: 899-910.
33. McKay RT, Tripet BP, Hodges RS, Sykes BD. 1997. Interaction of the second binding region of troponin I with the regulatory domain of skeletal muscle troponin C as determined by NMR spectroscopy. J. Biol. Chem. 272: 28494-28500.
34. McKay RT, Tripet BP, Pearlstone JR, Smillie LB, Sykes BD. 1999. Defining the region of troponin-I that binds to troponin-C. Biochemistry 38: 5478-5489.
35. 2+ binding and subsequent interactions with regions 1-40 and 96-115 of troponin I. Biochemistry 39: 2902-2911.
36. Ngai SM, Hodges RS. 1992. Biologically important interactions between synthetic peptides of the N- terminal region of troponin I and troponin C. J. Biol. Chem. 267: 15715-15720.
37. Ngai SM, Hodges RS. 2001a. Characterization of the biologically important interaction between troponin C and the N-terminal region of troponin I. J. Cell Biochem. 83: 99-110.
38. Ngai SM, Hodges RS. 2001b. Structural and functional studies on Troponin I and Troponin C interactions. J. Cell Biochem. 83: 33-46.
39. Ngai SM, Sonnichsen FD, Hodges RS. 1994. Photochemical cross-linking between native rabbit skeletal troponin C and benzoylbenzoyl-troponin I inhibitory peptide, residues 104-115. J. Biol. Chem. 269: 2165-2172.
40. Pearlstone JR, Sykes BD, Smillie LB. 1997. Interactions of structural C and regulatory N domains of troponin C with repeated sequence motifs in troponin I. Biochemistry 36: 7601-7606.
41. Perry SV. 1999. Troponin I: inhibitor or facilitator. Mol. Cell Biochem. 190: 9-32.
42. Potter JD, Gergely J. 1975. The calcium and magnesium binding sites on troponin and their role in the regulation of myofibrillar adenosine triphosphatase. J. Biol. Chem. 250: 4628-4633.
43. 2+ regulation of muscle contraction. J. Biol. Chem. 270: 2557-2562.
44. Ramakrishnan S, Hitchcock-DeGregori SE. 1995. Investigation of the structural requirements of the troponin C central helix for function. Biochemistry 34: 16789-16796.
45. Sheng Z, Strauss WL, Francois JM, Potter JD. 1990. Evidence that both Ca(2+)-specific sites of skeletal muscle TnC are required for full activity. J. Biol. Chem. 265: 21554-21560.
46. Sheng Z, Pan BS, Miller TE, Potter JD. 1992. Isolation, expression, and mutation of a rabbit skeletal muscle cDNA clone for troponin I. The role of the NH2 terminus of fast skeletal muscle troponin I in its biological activity. J. Biol. Chem. 267: 25407-25413.
47. Slupsky CM, Sykes BD. 1995. NMR solution structure of calcium-saturated skeletal muscle troponin C. Biochemistry 34: 15953-15964.
48. 1H NMR study of a ternary peptide complex that mimics the interaction between troponin C and troponin I. Protein Sci. 1: 1595-1603.
49. Sorenson MM, da Silva AC, Gouveia CS, Sousa VP, Oshima W, Ferro JA, Reinach FC. 1995. Concerted action of the high affinity calcium binding sites in skeletal muscle troponin C. J. Biol. Chem. 270: 9770-9777.
50. Strynadka NC, Cherney M, Sielecki AR, Li MX, Smillie LB, James MN. 1997. Structural details of a calcium-induced molecular switch: X-ray crystallographic analysis of the calcium-saturated N-terminal domain of troponin C at 1.75 A resolution. J. Mol. Biol. 273: 238-255.
51. Sundaralingam M, Bergstrom R, Strasburg G, Rao ST, Roy-Chowdhury P, Greaser M, Wang BC. 1985. Molecular structure of troponin C from chicken skeletal muscle at 3-angstrom resolution. Science 227: 945-948.
52. Swenson CA, Fredricksen RS. 1992. Interaction of troponin C and troponin C fragments with troponin I and the troponin I inhibitory peptide. Biochemistry 31: 3420-3429.
53. Syska H, Wilkinson JM, Grand RJ, Perry SV. 1976. The relationship between biological activity and primary structure of troponin I from white skeletal muscle of the rabbit. Biochem. J. 153: 375-387.
54. 2+ binding sites of troponin C in the regulation of skeletal muscle contraction. J. Biol. Chem. 271: 8381-8386.
55. Talbot JA, Hodges RS. 1981. Synthetic studies on the inhibitory region of rabbit skeletal troponin I. Relationship of amino acid sequence to biological activity. J. Biol. Chem. 256: 2798-2802.
56. 2+ dependence of the distance between Cys-98 of troponin C and Cys- 133 of troponin I in the ternary troponin complex. Resonance energy transfer measurements. Biochemistry 28: 5902-5908.
57. Tobacman LS. 1996. Thin filament-mediated regulation of cardiac contraction. A. Rev. Physiol. 58: 447-481.
58. 2+-dependent regulation of muscle contraction. J. Mol. Biol. 271: 728-750.
59. Tripet B, DeCrescenzo G, Grothe S, O'Connor-McCourt M, Hodges RS. 2002. Kinetic analysis of the interactions between troponin C and the C-terminal troponin I regulatory region and validation of a new peptide delivery/capture system used for surface plasmon resonance. J. Mol. Biol. 323: 345-362.
60. Tsuda S, Aimoto S, Hikichi K. 1992. 1H-NMR study of Ca(2+)-and Mg(2+)-dependent interaction between troponin C and troponin I inhibitory peptide (96-116). J. Biochem. (Tokyo) 112: 665-670.
61. Van Eyk JE, Hodges RS. 1988. The biological importance of each amino acid residue of the troponin I inhibitory sequence 104-115 in the interaction with troponin C and tropomyosin-actin. J. Biol. Chem. 263: 1726-1732.
62. Van Eyk JE, Strauss JD, Hodges RS, Ruegg JC. 1993. A synthetic peptide mimics troponin I function in the calcium-dependent regulation of muscle contraction. FEBS Lett. 323: 223-228.
63. 2+ sensitivity of the acto-S1-TM ATPase activity of the thin filament. J. Biol. Chem. 272: 10529-10537.
64. Vassylyev DG, Takeda S, Wakatsuki S, Maeda K, Maeda Y. 1998. Crystal structure of troponin C in complex with troponin I fragment at 2.3-A resolution. Proc. Natl Acad. Sci. USA 95: 4847-4852.
65. Wang ZY, Sarkar S, Gergely J, Tao T. 1990. Ca2(+)-dependent interactions between the C-helix of troponin-C and troponin-I. Photocross-linking and fluorescence studies using a recombinant troponin-C. J. Biol. Chem. 265: 4953-4957.
66. Weeks RA, Perry SV. 1978. Characterization of a region of the primary sequence of troponin C involved in calcium ion-dependent interaction with troponin I. Biochem. J. 173: 449-457.