Dynamic features of carboxy cytoglobin distal mutants investigated by molecular dynamics simulations
Tóm tắt
Cytoglobin (Cgb) is a member of hemoprotein family with roles in NO metabolism, fibrosis, and tumourigenesis. Similar to other hemoproteins, Cgb structure and functions are markedly influenced by distal key residues. The sixth ligand His81 (E7) is crucial to exogenous ligand binding, heme pocket conformation, and physiological roles of this protein. However, the effects of other key residues on heme pocket and protein biological functions are not well known. In this work, a molecular dynamics (MD) simulation study of two single mutants in CO-ligated Cgb (L46FCgbCO and L46VCgbCO) and two double mutants (L46FH81QCgbCO and L46VH81QCgbCO) was conducted to explore the effects of the key distal residues Leu46(B10) and His81(E7) on Cgb structure and functions. Results indicated that the distal mutation of B10 and E7 affected CgbCO dynamic properties on loop region fluctuation, internal cavity rearrangement, and heme motion. The distal conformation change was reflected by the distal key residues Gln62 (CD3) and Arg84(E10). The hydrogen bond between heme propionates with CD3 or E10 residues were evidently influenced by B10/E7 mutation. Furthermore, heme pocket rearrangement was also observed based on the distal pocket volume and occurrence rate of inner cavities. The mutual effects of B10 and E7 residues on protein conformational rearrangement and other dynamic features were expressed in current MD studies of CgbCO and its distal mutants, suggesting their crucial role in heme pocket stabilization, ligand binding, and Cgb biological functions. The mutation of distal B10 and E7 residues affects the dynamic features of carboxy cytoglobin.
Từ khóa
Tài liệu tham khảo
Burmester T, Ebner B, Weich B, Hankeln T (2002) Mol Biol Evol 19:416–421
Kawada N, Kristensen DB, Asahina K, Nakatani K, Minamiyama Y, Seki S, Yoshizato K (2001) J Biol Chem 276:47744–47745
Oleksiewicz U, Liloglou T, Field JK, Xinarianos G (2011) Cell Mol Life Sci 68:3869–3883
Trent JT, Hargrove MS (2002) J Biol Chem 277:19538–19545
Gardner AM, Cook MR, Gardner PR (2010) J Biol Chem 285:23850–23857
Li H, Hemann C, Abdelghany TM, El-Mahdy MA, Zweier JL (2012) J Biol Chem 287:36623–36633
Sawai H, Makino M, Mizutani Y, Ohta T, Sugimoto H, Uno T, Kawada N, Yoshizato K, Kitagawa T, Shiro Y (2005) Biochemistry 44:13257–13265
Hankeln T, Ebner B, Fuchs C, Gerlach F, Haberkamp M, Laufs TL, Roesner A, Schmidt M, Weich B, Wystub S, Saaler-Reinhardt S, Reuss S, Bolognesi M, De Sanctis D, Marden MC, Kiger L, Moens L, Dewilde S, Nevo E, Avivi A, Weber RE, Fago A, Burmester T (2005) J Inorg Biochem 99:110–119
Lv Y, Wang Q, Diao Y, Xu R (2008) Curr Gene Ther 8:287–294
Shivapurkar N, Stastny V, Okumura N, Girard L, Xie Y, Prinsen C, Thunnissen FB, Wistuba II, Czerniak B, Frenkel E, Roth JA, Liloglou T, Xinarianos G, Field JK, Minna JD, Gazdar AF (2008) Cancer Res 68:7448–7456
Xu R, Harrison PM, Chen M, Li L, Tsui TY, Fung PC, Cheung PT, Wang G, Li H, Diao Y, Krissansen GW, Xu S, Farzaneh F (2006) Mol Ther 13:1093–1100
Thuy LTT, Matsumoto Y, Thuy TTV, Hai H, Suoh M, Urahara Y, Motoyama H, Fujii H, Tamori A, Kubo S, Takemura S, Morita T, Yoshizato K, Kawada N (2015) Am J Pathol 185:1045–1060
Burmester T, Hankeln T (2014) Acta Physiol 211:501–514
Oleksiewicz U, Liloglou T, Tasopoulou KM, Daskoulido N, Bryan J, Gosney JR, Field JK, Xinarianos G (2013) Hum Mol Genet 22:3207–3217
Makino M, Sawai H, Shiro Y, Sugimoto H (2011) Proteins 79:1143–1153
Pesce A, Bolognesi M, Bocedi A, Ascenzi P, Dewilde S, Moens L, Hankeln T, Burmester T (2002) EMBO Rep 3:1146–1151
de Sanctis D, Dewilde S, Pesce A, Moens L, Ascenzi P, Hankeln T, Burmester T, Bolognesi M (2004) J Mol Biol 336:917–927
Smagghe BJ, Sarath G, Ross E, Hilbert JL, Hargrove MS (2006) Biochemistry 45:561–570
Gabba M, Abbruzzetti S, Spyrakis F, Forti F, Bruno S, Mozzarelli A, Luque FJ, Viappiani C, Cozzini P, Nardini M, Germani F, Bolognesi M, Moens L, Dewilde S (2013) PLoS ONE 8:e49770
Ioanitescu AI, Van Doorslaer S, Dewilde S, Endeward B, Moens L (2007) Mol Phys 105:2073–2086
Witmer JR, University IS (2007) Role of Leu(B10) in cytoglobin and comparison of direct and indirect measurements of hexacoordinate hemoglobin ligand affinity. Iowa: Iowa State University
Arredondo-Peter R, Hargrove MS, Moran JF, Sarath G, Klucas RV (1998) Plant Physiol 118:1121–1125
Smagghe BJ, Kundu S, Hoy JA, Halder P, Weiland TR, Savage A, Venugopal A, Goodman M, Premer S, Hargrove MS (2006) Biochemistry 45:9735–9745
Srajer V, Ren Z, Teng TY, Schmidt M, Ursby T, Bourgeois D, Pradervand C, Schildkamp W, Wulff M, Moffat K (2001) Biochemistry 40:13802–13815
Anselmi M, Di Nola A, Amadei A (2011) Proteins 79:867–879
Sparacino-Watkins C, Ragireddy V, Gladwin M, Tejero J (2014) Nitric Oxide 42:141
Bondarenko V, Dewilde S, Moens L, La Mar GN (2006) J Am Chem Soc 128:12988–12999
Halder P, Trent JT, Hargrove MS (2007) Proteins 66:172–182
Moschetti T, Mueller U, Schulze J, Brunori M, Vallone B (2009) Biophys J 97:1700–1708
Weiland TR, Kundu S, Trent JT, Hoy JA, Hargrove MS (2004) J Am Chem Soc 126:11930–11935
Anselmi M, Brunori M, Vallone B, Di Nola A (2008) Biophys J 95:4157–4162
Anselmi M, Di Nola A, Amadei A (2008) Biophys J 94:4277–4281
Olson JS, Mathews AJ, Rohlfs RJ, Springer BA, Egeberg KD, Sligar SG, Tame J, Renaud JP, Nagai K (1988) Nature 336:265–266
Olson JS, Phillips GN Jr (1996) J Biol Chem 271:17593–17596
Gardner PR, Gardner AM, Martin LA, Salzman AL (1998) Proc Natl Acad Sci USA 95:10378–10383
Wittenberg JB, Bolognesi M, Wittenberg BA, Guertin M (2002) J Biol Chem 277:871–874
Nishimura R, Matsumoto D, Shibata T, Yanagisawa S, Ogura T, Tai H, Matsuo T, Hirota S, Neya S, Suzuki A, Yamamoto Y (2014) Inorg Chem 53:9156–9165
Grunwald EW, Richards MP (2006) J Agric Food Chem 54:4452–4460
Lin Y, Shu X, Du K, Nie C, Wen G (2014) Comput Biol Chem 52:60–65
Bossa C, Anselmi M, Roccatano D, Amadei A, Vallone B, Brunori M, Di Nola A (2004) Biophys J 86:3855–3862
Bret C, Roth M, Norager S, Hatchikian EC, Field MJ (2002) Biophys J 83:3049–3065
Ceccarelli M, Ruggerone P, Anedda R, Fais A, Era B, Sollaino MC, Corda M, Casu M (2006) Biophys J 91:3529–3541
Elber R, Karplus M (1987) Science 235:318–321
Hummer G, Schotte F, Anfinrud PA (2004) Proc Natl Acad Sci USA 101:15330–15334
Park H, Lee S, Suh J (2005) J Am Chem Soc 127:13634–13642
Scorciapino MA, Robertazzi A, Casu M, Ruggerone P, Ceccarelli M (2009) J Am Chem Soc 131:11825–11832
Furlan S, Penna GL, Banci L, Mealli C (2007) J Phys Chem B 111:1157–1164
La Penna G, Furlan S, Banci L (2007) J Biol Inorg Chem 12:180–193
Giachetti A, La Penna GL, Perico A, Banci L (2004) Biophys J 87:498–512
Banci L, Gori-Savellini G, Turano P (1997) Eur J Biochem 249:716–723
Anselmi M, Brunori M, Vallone B, Di Nola A (2007) Biophys J 93:434–441
Danielsson J, Meuwly M (2008) J Chem Theory Comput 4:1083–1093
Mouawad L, Marechal JD, Perahia D (2005) Biochim Biophys Acta 1724:385–393
Nadra AD, Marti MA, Pesce A, Bolognesi M, Estrin DA (2008) Proteins 71:695–705
Orlowski S, Nowak W (2007) J Mol Model 13:715–723
Xu J, Yin G, Du W (2011) Proteins 79:191–202
Xu J, Yin G, Huang F, Wang B, Du W (2010) J Mol Model 16:759–770
Zhao C, Zhang B, Du W (2013) J Biol Inorg Chem 18:947–955
SYBYL 7.3, Tripos Software Inc, El Cerrito, CA, USA
Case DA, Dardern TA, Cheatham TE, Simmerling CL, Wang J, Duke RE, Luo R, Merz KM, Pearlman DA, Crowley M, Walker RC, Zhang W, Wang B, Hayik S, Roitberg A, Seabra G, Wong KF, Paesani F, Wu X, Brozell S, Tsui V, Gohlke H, Yang L, Tan C, Mongan J, Hornak V, Cui G, Beroza P, Mathews DH, Schafmeister C, Ross WS, Kollman PA (2006) AMBER 9. University of California, San Francisco
Giammona DA (1984) An examination of conformational flexibility in porphyrins and bulky-ligand binding in myoglobin. Ph. D. Thesis. University of California: Davis, CA
Adcock SA, McCammon JA (2006) Chem Rev 106:1589–1615
Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR (1984) J Chem Phys 81:3684–3690
Laskowski RA (1995) J Mol Graph 13:323–330
Zhang B, Xu J, Li Y, Du W, Fang W (2011) J Inorg Biochem 105:949–956
Oobatake M, Ooi T (1993) Prog Biophys Mol Biol 59:237–284
Singh H, Ahmad S (2009) BMC Struct Biol 9 doi:10.1186/1472-6807-9-25
Tsodikov OV, Record MT, Sergeev YV (2002) J Comput Chem 23:600–609
Lechauve C, Chauvierre C, Dewilde S, Moens L, Green BN, Marden MC, Celier C, Kiger L (2010) FEBS J 277:2696–2704
Mompean M, Gonzalez C, Lomba E, Laurents DV (2014) J Phys Chem B 118:7312–7316
de Sanctis D, Dewilde S, Pesce A, Moens L, Ascenzi P, Hankeln T, Burmester T, Bolognesi M (2004) Biochem Biophys Res Commun 316:1217–1221
Kim H, Park H (2004) Proteins 54:557–562
Ioanitescu AI, Van Doorslaer S, Dewilde S, Endeward B, Moens L (2007) Mol Phys 105:2073–2086
Du J, Li W, Li L, Wen G, Lin Y, Tan X (2015) Chemistryopen 4:97–105
Sugimoto H, Makino M, Sawai H, Kawada N, Yoshizato K, Shiro Y (2004) J Mol Biol 339:873–885
Pietra F (2013) Chem Biodiversity 10:86–95
Zhao X, Vyas K, Nguyen BD, Rajarathnam K, La Mar GN, Li T, Phillips GN Jr, Eich RF, Olson JS, Ling J, Bocian DF (1995) J Biol Chem 270:20763–20774
Arcon JP, Rosi P, Petruk AA, Marti MA, Estrin DA (2015) J Phys Chem B 119:1802–1813
Tetreau C, Blouquit Y, Novikov E, Quiniou E, Lavalette D (2004) Biophys J 86:435–447
Nishihara Y, Sakakura M, Kimura Y, Terazima M (2004) J Am Chem Soc 128:11877–11888
Maragliano L, Cottone G, Ciccotti G, Vanden-Eijnden E (2009) J Am Chem Soc 132:1010–1017
Laberge M, Yonetani T (2007) IUBMB Life 59:528–534
Astudillo L, Bernad S, Derrien V, Sebban P, Miksovska J (2013) J Inorg Biochem 129:23–29
Vallone B, Nienhaus K, Matthes A, Brunori M, Nienhaus GU (2004) Proc Natl Acad Sci USA 101:17351–17356
Alayash AI, Ryan BAB, Eich RF, Olson JS, Cashon RE (1999) J Biol Chem 274:2029–2037