Trifluoperazine regulation of calmodulin binding to Fas: A computational study

Proteins: Structure, Function and Bioinformatics

Volumn 79, Issue 8, 2011, Pages 2543-2556

  Pan, Di ^a   Yan, Qi ^a   Chen, Yabing ^b,c   Mcdonald, Jay M ^b,c   Song, Yuhua ^a  

^a and Radiation Oncology   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

Binding free energy; CaM antagonist TFP; CaM Fas binding; Conformational and motion analysis; DISC; Molecular dynamics

Indexed keywords

CALMODULIN; FAS ANTIGEN; TRIFLUOPERAZINE;

ALPHA HELIX; ARTICLE; DRUG BINDING; ENZYME REGULATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; SIMULATION;

ANIMALS; ANTIGENS, CD95; CALMODULIN; COMPUTATIONAL BIOLOGY; HUMANS; MICE; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; THERMODYNAMICS; TRIFLUOPERAZINE;

EID: 79960094217     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23081     Document Type: Article

References (84)

1. Nagata S. Apoptosis by death factor. Cell 1997; 88: 355-365.
2. Lee SH, Shin MS, Lee HS, Bae JH, Lee HK, Kim HS, Kim SY, Jang JJ, Joo M, Kang YK, Park WS, Park JY, Oh RR, Han SY, Lee JH, Kim SH, Lee JY, Yoo NJ. Expression of Fas and Fas-related molecules in human hepatocellular carcinoma. Hum Pathol 2001; 32: 250-256.
3. Nambu Y, Hughes SJ, Rehemtulla A, Hamstra D, Orringer MB, Beer DG. Lack of cell surface Fas/APO-1 expression in pulmonary adenocarcinomas. J Clin Investig 1998; 101: 1102-1110.
4. Keane MM, Ettenberg SA, Lowrey GA, Russell EK, Lipkowitz S. Fas expression and function in normal and malignant breast cell lines. Cancer Res 1996; 56: 4791-4798.
5. Weller M, Malipiero U, Rensing-Ehl A, Barr PJ, Fontana A. Fas/APO-1 gene transfer for human malignant glioma. Cancer Res 1995; 55: 2936-2944.
6. Suever JD, Chen Y, McDonald JM, Song Y. Conformation and free energy analyses of the complex of calcium-bound calmodulin and the Fas death domain. Biophys J 2008; 95: 5913-5921.
7. Takakuwa T, Dong Z, Takayama H, Matsuzuka F, Nagata S, Aozasa K. Frequent mutations of Fas gene in thyroid lymphoma. Cancer Res 2001; 61: 1382-1385.
8. Shin MS, Park WS, Kim SY, Kim HS, Kang SJ, Song KY, Park JY, Dong SM, Pi JH, Oh RR, Lee JY, Yoo NJ, Lee SH. Alterations of Fas (Apo-1/CD95) gene in cutaneous malignant melanoma. Am J Pathol 1999; 154: 1785-1791.
9. Maeda T, Yamada Y, Moriuchi R, Sugahara K, Tsuruda K, Joh T, Atogami S, Tsukasaki K, Tomonaga M, Kamihira S. Fas gene mutation in the progression of adult T cell leukemia. J Exp Med 1999; 189: 1063-1071.
10. Watanabe-Fukunaga R, Brannan CI, Copeland NG, Jenkins NA, Nagata S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 1992; 356: 314-317.
11. Fisher GH, Rosenberg FJ, Straus SE, Dale JK, Middleton LA, Lin AY, Strober W, Lenardo MJ, Puck JM. Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell 1995; 81: 935-946.
12. Rieux-Laucat F, Le Deist F, Hivroz C, Roberts I, Debatin K, Fischer A, de Villartay J. Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science 1995; 268: 1347-1349.
13. Puck J, Straus S, Le Deist F, Rieux-Laucat F, Fischer A. Inherited disorders with autoimmune and defective lymphocyte regulation. In: Primary immunodeficiency diseases: a molecular and genetic approach. New York: Oxford University Press; 1999.
14. Bi LL, Pan G, Atkinson TP, Zheng L, Dale JK, Makris C, Reddy V, McDonald JM, Siegel RM, Puck JM, Lenardo MJ, Straus SE. Dominant inhibition of Fas ligand-mediated apoptosis due to a heterozygous mutation associated with autoimmune lymphoproliferative syndrome (ALPS) type Ib. BMC Med Genet 2007; 8: 41.
15. Jhala NC, Vickers SM, Argani P, McDonald JM. Regulators of apoptosis in cholangiocarcinoma. Arch Pathol Lab Med 2005; 129: 481-486.
16. Ahn EY, Pan G, Vickers SM, McDonald JM. IFN-gammaupregulates apoptosis-related molecules and enhances Fas-mediated apoptosis in human cholangiocarcinoma. Int J Cancer 2002; 100: 445-451.
17. Li ZY, Zou SQ. Fas counterattack in cholangiocarcinoma: a mechanism for immune evasion in human hilar cholangiocarcinomas. World J Gastroenterol 2001; 7: 860-863.
18. Shimonishi T, Isse K, Shibata F, Aburatani I, Tsuneyama K, Sabit H, Harada K, Miyazaki K, Nakanuma Y. Up-regulation of fas ligand at early stages and down-regulation of Fas at progressed stages of intrahepatic cholangiocarcinoma reflect evasion from immune surveillance. Hepatology 2000; 32: 761-769.
19. Que FG, Phan VA, Phan VH, Celli A, Batts K, LaRusso NF, Gores GJ. Cholangiocarcinomas express Fas ligand and disable the Fas receptor. Hepatology 1999; 30: 1398-1404.
20. Pan G, Vickers SM, Pickens A, Phillips JO, Ying W, Thompson JA, Siegal GP, McDonald JM. Apoptosis and tumorigenesis in human cholangiocarcinoma cells. Involvement of Fas/APO-1 (CD95) and calmodulin. Am J Pathol 1999; 155: 193-203.
21. Moser MJ, Lee SY, Klevit RE, Davis TN. Ca2+ binding to calmodulin and its role in Schizosaccharomyces pombe as revealed by mutagenesis and NMR spectroscopy. J Biol Chem 1995; 270: 20643-20652.
22. Hait WN, Lazo JS. Calmodulin: a potential target for cancer chemotherapeutic agents. J Clin Oncol 1986; 4: 994-1012.
23. Ito H, Wang JZ, Shimura K. Inhibition of lung metastasis by a calmodulin antagonist. N-(6-aminohexyl)-5-chloro-1-naphthalenesulfonamide (W-7), in mice bearing Lewis lung carcinoma. Anticancer Res 1991; 11: 249-252.
24. Ahn EY, Pan G, Oh JH, Tytler EM, McDonald JM. The combination of calmodulin antagonists and interferon-gamma induces apoptosis through caspase-dependent and -independent pathways in cholangiocarcinoma cells. Am J Pathol 2003; 163: 2053-2063.
25. Chen Y, Pawar P, Pan G, Ma L, Liu H, McDonald JM. Calmodulin binding to the Fas-mediated death-inducing signaling complex in cholangiocarcinoma cells. J Cell Biochem 2008; 103: 788-799.
26. Wu X, Ahn EY, McKenna MA, Yeo H, McDonald JM. Fas binding to calmodulin regulates apoptosis in osteoclasts. J Biol Chem 2005; 280: 29964-29970.
27. Ahn EY, Lim ST, Cook WJ, McDonald JM. Calmodulin binding to the Fas death domain. Regulation by Fas activation. J Biol Chem 2004; 279: 5661-5666.
28. Eldik L, Watterson D. Calmodulin and calcium signal transduction. San Diego: Academic Press; 1998.
29. Ikura M. CALMODULIN TARGET DATABASE.
30. Ganoth A, Friedman R, Nachliel E, Gutman M. A molecular dynamics study and free energy analysis of complexes between the Mlc1p protein and two IQ motif peptides. Biophys J 2006; 91: 2436-2450.
31. Finn BE, Evenas J, Drakenberg T, Waltho JP, Thulin E, Forsen S. Calcium-induced structural changes and domain autonomy in calmodulin. Nat Struct Biol 1995; 2: 777-783.
32. Kretsinger RH, Rudnick SE, Weissman LJ. Crystal structure of calmodulin. J Inorg Biochem 1986; 28: 289-302.
33. Kuboniwa H, Tjandra N, Grzesiek S, Ren H, Klee CB, Bax A. Solution structure of calcium-free calmodulin. Nat Struct Biol 1995; 2: 768-776.
34. Zhang M, Tanaka T, Ikura M. Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nat Struct Biol 1995; 2: 758-767.
35. Seaton BA, Head JF, Engelman DM, Richards FM. Calcium-induced increase in the radius of gyration and maximum dimension of calmodulin measured by small-angle X-ray scattering. Biochemistry 1985; 24: 6740-6743.
36. Heidorn DB, Trewhella J. Comparison of the crystal and solution structures of calmodulin and troponin C. Biochemistry 1988; 27: 909-915.
37. Persechini A, Kretsinger RH. The central helix of calmodulin functions as a flexible tether. J Biol Chem 1988; 263: 12175-12178.
38. Matsushima N, Hayashi N, Jinbo Y, Izumi Y. Ca2+-bound calmodulin forms a compact globular structure on binding four trifluoperazine molecules in solution. Biochem J 347Pt 2000;1: 211-215.
39. Huang B, Eberstadt M, Olejniczak ET, Meadows RP, Fesik SW. NMR structure and mutagenesis of the Fas (APO-1/CD95) death domain. Nature 1996; 384: 638-641.
40. Imtiyaz HZ, Zhang Y, Zhang J. Structural requirements for signal-induced target binding of FADD determined by functional reconstitution of FADD deficiency. J Biol Chem 2005; 280: 31360-31367.
41. Wu X, McKenna MA, Feng X, Nagy TR, McDonald JM. Osteoclast apoptosis: the role of Fas in vivo and in vitro. Endocrinology 2003; 144: 5545-5555.
42. Chen YJ, Xu, N. Jhala, P. Pawar, Z. B. Zhu, L. Ma, C. H. Byon, andJ. M. McDonald. Fas-mediated apoptosis in cholangiocarcinoma cells is enhanced by 3, 3'-diindolylmethane through inhibition of AKT signaling and FLICE-like inhibitory protein. The American journal of pathology 2006; 169: 1833-1842.
43. Cook WJ, Walter LJ, Walter MR. Drug binding by calmodulin: crystal structure of a calmodulin-trifluoperazine complex. Biochemistry 1994; 33: 15259-15265.
44. Vertessy BG, Harmat V, Bocskei Z, Naray-Szabo G, Orosz F, Ovadi J. Simultaneous binding of drugs with different chemical structures to Ca2+-calmodulin: crystallographic and spectroscopic studies. Biochemistry 1998; 37: 15300-15310.
45. Vandonselaar M, Hickie RA, Quail JW, Delbaere LT. Trifluoperazine-induced conformational change in Ca(2+)-calmodulin. Nat Struc Biol 1994; 1: 795-801.
46. Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A. Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 2000; 29: 291-325.
47. Case DA, Cheatham TE, III, Darden T, Gohlke H, Luo R, Merz KMJr, Onufriev A, Simmerling C, Wang B, Woods RJ. The Amber biomolecular simulation programs. J Comput Chem 2005; 26: 1668-1688.
48. Chen R, Weng Z. A novel shape complementarity scoring function for protein-protein docking. Proteins 2003; 51: 397-408.
49. Li L, Chen R, Weng Z. RDOCK: refinement of rigid-body protein docking predictions. Proteins 2003; 53: 693-707.
50. Chen R, Weng Z. Docking unbound proteins using shape complementarity, desolvation, and electrostatics. Proteins 2002; 47: 281-294.
51. Chen R, Tong W, Mintseris J, Li L, Weng Z. ZDOCK predictions for the CAPRI challenge. Proteins 2003; 52: 68-73.
52. Wiehe K, Pierce B, Mintseris J, Tong WW, Anderson R, Chen R, Weng Z. ZDOCK and RDOCK performance in CAPRI rounds 3, 4, and 5. Proteins 2005; 60: 207-213.
53. Yi H, Qiu S, Cao Z, Wu Y, Li W. Molecular basis of inhibitory peptide maurotoxin recognizing Kv1.2 channel explored by ZDOCKand molecular dynamic simulations. Proteins 2008; 70: 844-854.
54. Jin L, Wu Y. Molecular mechanism of the sea anemone toxin ShK recognizing the Kv1.3 channel explored by docking and molecular dynamic simulations. J Chem Inf Model 2007; 47: 1967-1972.
55. Wu Y, Cao Z, Yi H, Jiang D, Mao X, Liu H, Li W. Simulation of the interaction between ScyTx and small conductance calcium-activated potassium channel by docking and MM-PBSA. Biophys J 2004; 87: 105-112.
56. Chen R, Li L, Weng Z. ZDOCK: an initial-stage protein-docking algorithm. Proteins 2003; 52: 80-87.
57. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 1983; 4: 187-217.
58. Wang J, Wang W, Kollman PA, Case DA. Automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model 2006; 25: 247-260.
59. Cieplak P, Cornell WD, Bayly C, Kollman PA. Application of the multimolecule and multiconformational RESP methodology to biopolymers: charge derivation for DNA. RNA, and proteins. Comput Chem 2004; 16: 1357-1377.
60. Zhang W, Hou T, Qiao X, Xu X. Parameters for the generalized born model consistent with RESP atomic partial charge assignment protocol. J Phys Chem B 2003; 107: 9071-9078.
61. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JA, Jr, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA. Gaussian 03. Wallingford, CT: Gaussian, Inc. 2004.
62. Ponder JW, Case DA. Force fields for protein simulations. Adv Protein Chem 2003; 66: 27-85.
63. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983; 79: 926-935.
64. Darden T, York D, Pedersen LG. Particle mesh Ewald: An Nâlog(N) method for Ewald sums in large systems. J Chem Phys 1993; 98: 10089-10092.
65. Li L, Uversky VN, Dunker AK, Meroueh SO. A computational investigation of allostery in the catabolite activator protein. J Am Chem Soc 2007; 129: 15668-15676.
66. Wang W, Lim WA, Jakalian A, Wang J, Wang J, Luo R, Bayly CI, Kollman PA. An analysis of the interactions between the Sem-5 SH3 domain and its ligands using molecular dynamics, free energy calculations, and sequence analysis. J Am Chem Soc 2001; 123: 3986-3994.
67. Kollman PA, Massova I, Reyes C, Kuhn B, Huo S, Chong L, Lee M, Lee T, Duan Y, Wang W, Donini O, Cieplak P, Srinivasan J, Case DA, Cheatham TE, III. 2000. Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc Chem Res 33: 889-897.
68. Brooks B, Karplus M. Harmonic dynamics of proteins: normal modes and fluctuations in bovine pancreatic trypsin inhibitor. Proc Natl Acad Sci U S A 1983; 80: 6571-6575.
69. Go N, Noguti T, Nishikawa T. Dynamics of a small globular protein in terms of low-frequency vibrational modes. Proc Natl Acad Sci U S A 1983; 80: 3696-3700.
70. Levitt M, Sander C, Stern PS. The normal modes of a protein: native bovine pancreatic trypsin inhibitor. Int J Quantum Chem 1983; 24: 181-199.
71. McQuarrie DA. Statistical thermodynamics. New York: Harper & Row; 1973.
72. Efron B, Tibshirani RJ. An introduction to the bootstrap. New York: Chapman & Hall; 1998.
73. Hayward S, Kitao A, Go N. Harmonicity and anharmonicity in protein dynamics: a normal mode analysis and principal component analysis. Proteins 1995; 23: 177-186.
74. Hayward S, Kitao A, Hirata F, Go N. Effect of solvent on collective motions in globular protein. J Mol Biol 1993; 234: 1207-1217.
75. Berendsen HJ, Hayward S. Collective protein dynamics in relation to function. Curr Opin Struct Biol 2000; 10: 165-169.
76. MathWorks T. MATLAB.
77. Allen MP, Tildesley DJ. Computer simulation of liquids. New York: Oxford University Press; 1987.
78. Lee SJ, Song Y, Baker NA. Molecular dynamics simulations of asymmetric NaCl and KCl solutions separated by phosphatidylcholine bilayers: potential drops and structural changes induced by strong Na+-lipid interactions and finite size effects. Biophys J 2008; 94: 3565-3576.
79. Liu Y, Pan D, Bellis SL, Song Y. Effect of altered glycosylation on the structure of the I-like domain of beta1 integrin: a molecular dynamics study. Proteins 2008; 73: 989-1000.
80. Chen AA, Pappu RV. Quantitative characterization of ion pairing and cluster formation in strong 1:1 electrolytes. J Phys Chem 2007; 111: 6469-6478.
81. Bailey NTJ. Statistical methods in biology. New York, NY: Cambridge University Press; 1995.
82. Harmat V, Bocskei Z, Naray-Szabo G, Bata I, Csutor AS, Hermecz I, Aranyi P, Szabo B, Liliom K, Vertessy BG, Ovadi J. A new potent calmodulin antagonist with arylalkylamine structure: crystallographic, spectroscopic and functional studies. J Mol Biol 2000; 297: 747-755.
83. Massom L, Lee H, Jarrett HW. Trifluoperazine binding to porcine brain calmodulin and skeletal muscle troponin C. Biochemistry 1990; 29: 671-681.
84. Scott FL, Stec B, Pop C, Dobaczewska MK, Lee JJ, Monosov, Robinson H, Salvesen GS, Schwarzenbacher R, Riedl SJ. The Fas-FADD death domain complex structure unravels signalling by receptor clustering. Nature 2009; 457: 1019-1022.