Computational Analysis of the MembraneTargeting Domains of Plant-specific PRAF Proteins

Authors: Ewa Wywial, Shaneen M. Singh

Abstract:

The PRAF family of proteins is a plant specific family of proteins with distinct domain architecture and various unique sequence/structure traits. We have carried out an extensive search of the Arabidopsis genome using an automated pipeline and manual methods to verify previously known and identify unknown instances of PRAF proteins, characterize their sequence and build 3D structures of their individual domains. Integrating the sequence, structure and whatever little known experimental details for each of these proteins and their domains, we present a comprehensive characterization of the different domains in these proteins and their variant properties.

Keywords: PRAF proteins, homology modeling, Arabidopsisthaliana

Digital Object Identifier (DOI): doi.org/10.5281/zenodo.1062154

References:

[1] G.C. Briggs, C.F. Mouchel, C.S. Hardtke, Plant Physiol, 140 (2006) 1306.
[2] C.F. Mouchel, G.C. Briggs, C.S. Hardtke, Genes Dev, 18 (2004) 700.
[3] B. Heras, B.K. Drobak, J Exp Bot, 53 (2002) 565.
[4] R.B. Jensen, T. La Cour, J. Albrethsen, M. Nielsen, K. Skriver, Biochem J, 359 (2001) 165.
[5] C.D. Knox, A.E. Belous, J.M. Pierce, A. Wakata, I.B. Nicoud, C.D. Anderson, C.W. Pinson, R.S. Chari, Am J Physiol Gastrointest Liver Physiol, 287 (2004) G533.
[6] P. Garcia, R. Gupta, S. Shah, A.J. Morris, S.A. Rudge, S. Scarlata, V. Petrova, S. McLaughlin, M.J. Rebecchi, Biochemistry, 34 (1995) 16228.
[7] F.M. Flesch, J.W. Yu, M.A. Lemmon, K.N. Burger, Biochem J, 389 (2005) 435.
[8] M.A. Lemmon, K.M. Ferguson, R. O'Brien, P.B. Sigler, J. Schlessinger, Proc Natl Acad Sci U S A, 92 (1995) 10472.
[9] A. Hayakawa, S.J. Hayes, D.C. Lawe, E. Sudharshan, R. Tuft, K. Fogarty, D. Lambright, S. Corvera, J Biol Chem, 279 (2004) 5958.
[10] W. van Leeuwen, L. Okresz, L. Bogre, T. Munnik, Trends Plant Sci, 9 (2004) 378.
[11] B.K. Drobak, B. Heras, Trends Plant Sci, 7 (2002) 132.
[12] M. Lemmon, Biochem Soc Trans. , 32 (2004) 707.
[13] T. Gibson, M. Hyvonen, A. Musacchio, M. Saraste, E. Birney, Trends Biochem Sci. , 19 (1994) 349.
[14] J.M. Kavran, D.E. Klein, A. Lee, M. Falasca, S.J. Isakoff, E.Y. Skolnik, M.A. Lemmon, J Biol Chem, 273 (1998) 30497.
[15] M.A. Lemmon, K.M. Ferguson, Biochem J, 350 (2000) 1.
[16] A. Musacchio, T. Gibson, P. Rice, J. Thompson, M. Saraste, Trends Biochem Sci. , 18 (1993) 343.
[17] A. Petiot, J. Faure, H. Stenmark, J. Gruenberg, J. Cell Biol., 162 (2003) 971.
[18] A.E. Wurmser, J.D. Gary, S.D. Emr, J. Biol. Chem., 274 (1999) 9129.
[19] A. Simonsen, R. Lippe, S. Christoforidis, J.M. Gaullier, A. Brech, J. Callaghan, B.H. Toh, C. Murphy, M. Zerial, H. Stenmark, Nature, 394 (1998) 494.
[20] W. Moore, C. Zhang, P.R. Clarke, Curr Biol, 12 (2002) 1442.
[21] N. Mirkovic, Z. Li, A. Parnassa, D. Murray, Proteins, 66 (2006) 766.
[22] H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I.N. Shindyalov, P.E. Bourne, Nucleic Acids Res, 28 (2000) 235.
[23] H. Berman, K. Henrick, H. Nakamura, Nat Struct Biol, 10 (2003) 980.
[24] M. Kanehisa, Novartis Found Symp, 247 (2002) 91.
[25] M. Kanehisa, S. Goto, M. Hattori, K.F. Aoki-Kinoshita, M. Itoh, S. Kawashima, T. Katayama, M. Araki, M. Hirakawa, Nucl. Acids Res., 34 (2006) D354.
[26] J. Schultz, R.R. Copley, T. Doerks, C.P. Ponting, P. Bork, Nucleic Acids Res, 28 (2000) 231.
[27] J. Schultz, F. Milpetz, P. Bork, C.P. Ponting, PNAS, 95 (1998) 5857.
[28] I. Letunic, R.R. Copley, B. Pils, S. Pinkert, J. Schultz, P. Bork, Nucleic Acids Res, 34 (2006) D257.
[29] A. Bairoch, B. Boeckmann, Nucleic Acids Res, 22 (1994) 3578.
[30] B. Boeckmann, M.C. Blatter, L. Famiglietti, U. Hinz, L. Lane, B. Roechert, A. Bairoch, C R Biol, 328 (2005) 882.
[31] D.A. Benson, I. Karsch-Mizrachi, D.J. Lipman, J. Ostell, D.L. Wheeler, Nucleic Acids Res, 34 (2006) D16.
[32] D.L. Wheeler, T. Barrett, D.A. Benson, S.H. Bryant, K. Canese, V. Chetvernin, D.M. Church, M. DiCuccio, R. Edgar, S. Federhen, L.Y. Geer, W. Helmberg, Y. Kapustin, D.L. Kenton, O. Khovayko, D.J. Lipman, T.L. Madden, D.R. Maglott, J. Ostell, K.D. Pruitt, G.D. Schuler, L.M. Schriml, E. Sequeira, S.T. Sherry, K. Sirotkin, A. Souvorov, G. Starchenko, T.O. Suzek, R. Tatusov, T.A. Tatusova, L. Wagner, E. Yaschenko, Nucleic Acids Res, 34 (2006) D173.
[33] R. Apweiler, A. Bairoch, C.H. Wu, W.C. Barker, B. Boeckmann, S. Ferro, E. Gasteiger, H. Huang, R. Lopez, M. Magrane, M.J. Martin, D.A. Natale, C. O'Donovan, N. Redaschi, L.S. Yeh, Nucleic Acids Res, 32 (2004) D115.
[34] A. Bairoch, R. Apweiler, C.H. Wu, W.C. Barker, B. Boeckmann, S. Ferro, E. Gasteiger, H. Huang, R. Lopez, M. Magrane, M.J. Martin, D.A. Natale, C. O'Donovan, N. Redaschi, L.S. Yeh, Nucleic Acids Res, 33 (2005) D154.
[35] C.H. Wu, R. Apweiler, A. Bairoch, D.A. Natale, W.C. Barker, B. Boeckmann, S. Ferro, E. Gasteiger, H. Huang, R. Lopez, M. Magrane, M.J. Martin, R. Mazumder, C. O'Donovan, N. Redaschi, B. Suzek, Nucleic Acids Res, 34 (2006) D187.
[36] S.F. Altschul, T.L. Madden, A.A. Schaffer, J. Zhang, Z. Zhang, W. Miller, D.J. Lipman, Nucleic Acids Res, 25 (1997) 3389.
[37] A. Bateman, L. Coin, R. Durbin, R.D. Finn, V. Hollich, S. Griffiths- Jones, A. Khanna, M. Marshall, S. Moxon, E.L. Sonnhammer, D.J. Studholme, C. Yeats, S.R. Eddy, Nucleic Acids Res, 32 (2004) D138.
[38] A. Marchler-Bauer, J.B. Anderson, P.F. Cherukuri, C. DeWeese-Scott, L.Y. Geer, M. Gwadz, S. He, D.I. Hurwitz, J.D. Jackson, Z. Ke, C.J. Lanczycki, C.A. Liebert, C. Liu, F. Lu, G.H. Marchler, M. Mullokandov, B.A. Shoemaker, V. Simonyan, J.S. Song, P.A. Thiessen, R.A. Yamashita, J.J. Yin, D. Zhang, S.H. Bryant, Nucleic Acids Res, 33 (2005) D192.
[39] A. Marchler-Bauer, J.B. Anderson, M.K. Derbyshire, C. DeWeese-Scott, N.R. Gonzales, M. Gwadz, L. Hao, S. He, D.I. Hurwitz, J.D. Jackson, Z. Ke, D. Krylov, C.J. Lanczycki, C.A. Liebert, C. Liu, F. Lu, S. Lu, G.H. Marchler, M. Mullokandov, J.S. Song, N. Thanki, R.A. Yamashita, J.J. Yin, D. Zhang, S.H. Bryant, Nucleic Acids Res, 35 (2007) D237.
[40] A. Marchler-Bauer, J.B. Anderson, C. DeWeese-Scott, N.D. Fedorova, L.Y. Geer, S. He, D.I. Hurwitz, J.D. Jackson, A.R. Jacobs, C.J. Lanczycki, C.A. Liebert, C. Liu, T. Madej, G.H. Marchler, R. Mazumder, A.N. Nikolskaya, A.R. Panchenko, B.S. Rao, B.A. Shoemaker, V. Simonyan, J.S. Song, P.A. Thiessen, S. Vasudevan, Y. Wang, R.A. Yamashita, J.J. Yin, S.H. Bryant, Nucleic Acids Res, 31 (2003) 383.
[41] A. Marchler-Bauer, S.H. Bryant, Nucleic Acids Res, 32 (2004) W327.
[42] A. Marchler-Bauer, A.R. Panchenko, B.A. Shoemaker, P.A. Thiessen, L.Y. Geer, S.H. Bryant, Nucleic Acids Res, 30 (2002) 281.
[43] R.L. Tatusov, N.D. Fedorova, J.D. Jackson, A.R. Jacobs, B. Kiryutin, E.V. Koonin, D.M. Krylov, R. Mazumder, S.L. Mekhedov, A.N. Nikolskaya, B.S. Rao, S. Smirnov, A.V. Sverdlov, S. Vasudevan, Y.I. Wolf, J.J. Yin, D.A. Natale, BMC Bioinformatics, 4 (2003) 41.
[44] R.L. Tatusov, E.V. Koonin, D.J. Lipman, Science, 278 (1997) 631.
[45] J.A. Cuff, G.J. Barton, Proteins, 40 (2000) 502.
[46] J.A. Cuff, G.J. Barton, Proteins, 34 (1999) 508.
[47] J.A. Cuff, M.E. Clamp, A.S. Siddiqui, M. Finlay, G.J. Barton, Bioinformatics, 14 (1998) 892.
[48] K. Bryson, L.J. McGuffin, R.L. Marsden, J.J. Ward, J.S. Sodhi, D.T. Jones, Nucleic Acids Res, 33 (2005) W36.
[49] D.T. Jones, J Mol Biol, 292 (1999) 195.
[50] L.J. McGuffin, K. Bryson, D.T. Jones, Bioinformatics, 16 (2000) 404.
[51] B. Rost, Methods Enzymol, 266 (1996) 525.
[52] M. Ouali, R.D. King, Protein Sci, 9 (2000) 1162.
[53] K. Karplus, C. Barrett, R. Hughey, Bioinformatics, 14 (1998) 846.
[54] K. Karplus, S. Katzman, G. Shackleford, M. Koeva, J. Draper, B. Barnes, M. Soriano, R. Hughey, Proteins, 61 Suppl 7 (2005) 135.
[55] K. Karplus, B. Hu, Bioinformatics, 17 (2001) 713.
[56] Y. Guermeur, PhD thesis (1997).
[57] P. Baldi, S. Brunak, P. Frasconi, G. Soda, G. Pollastri, Bioinformatics, 15 (1999) 937.
[58] J. Cheng, A.Z. Randall, M.J. Sweredoski, P. Baldi, Nucleic Acids Res, 33 (2005) W72.
[59] C. Cole, J.D. Barber, G.J. Barton, Nucleic Acids Res, 36 (2008) W197.
[60] O. Dor, Y. Zhou, Proteins, 66 (2007) 838.
[61] B. Wallner, A. Elofsson, Protein Sci, 14 (2005) 1315.
[62] D. Petrey, B. Honig, Mol Cell, 20 (2005) 811.
[63] S.M. Singh, D. Murray, Protein Sci, 12 (2003) 1934.
[64] Z. Xiang, C.S. Soto, B. Honig, Proc Natl Acad Sci U S A, 99 (2002) 7432.
[65] A.A. Canutescu, A.A. Shelenkov, R.L. Dunbrack, Jr., Protein Sci, 12 (2003) 2001.
[66] Z. Xiang, P.J. Steinbach, M.P. Jacobson, R.A. Friesner, B. Honig, Proteins (2007).
[67] Z. Xiang, B. Honig, J Mol Biol, 311 (2001) 421.
[68] M.P. Jacobson, R.A. Friesner, Z. Xiang, B. Honig, J Mol Biol, 320 (2002) 597.
[69] J.L. Sussman, D. Lin, J. Jiang, N.O. Manning, J. Prilusky, O. Ritter, E.E. Abola, Acta Crystallogr D Biol Crystallogr, 54 (1998) 1078.
[70] N.N. Alexandrov, R. Nussinov, R.M. Zimmer, Pac Symp Biocomput (1996) 53.
[71] J. Shi, T.L. Blundell, K. Mizuguchi, J Mol Biol, 310 (2001) 243.
[72] J. Meller, R. Elber, Proteins, 45 (2001) 241.
[73] O. Teodorescu, T. Galor, J. Pillardy, R. Elber, Proteins, 54 (2004) 41.
[74] D. Tobi, R. Elber, Proteins, 41 (2000) 40.
[75] L.A. Kelley, R.M. MacCallum, M.J. Sternberg, J Mol Biol, 299 (2000) 499.
[76] S.F. Altschul, E.V. Koonin, Trends Biochem Sci, 23 (1998) 444.
[77] A.A. Schaffer, L. Aravind, T.L. Madden, S. Shavirin, J.L. Spouge, Y.I. Wolf, E.V. Koonin, S.F. Altschul, Nucleic Acids Res, 29 (2001) 2994.
[78] A.A. Schaffer, Y.I. Wolf, C.P. Ponting, E.V. Koonin, L. Aravind, S.F. Altschul, Bioinformatics, 15 (1999) 1000.
[79] P.A. Bates, L.A. Kelley, R.M. MacCallum, M.J. Sternberg, Proteins, Suppl 5 (2001) 39.
[80] P.A. Bates, M.J. Sternberg, Proteins, Suppl 3 (1999) 47.
[81] B. Contreras-Moreira, P.A. Bates, Bioinformatics, 18 (2002) 1141.
[82] S.C.E. Tosatto, (Submitted).
[83] S.C.E. Tosatto, Journal of Computational Biology, 12 (2005) 1316.
[84] O. Lund, M. Nielsen, C. Lundegaard, P. Worning, Abstract at the CASP5 conference A102 (2002).
[85] K. Nicholas, H. Nicholas, D. Deerfield, EMBNEW.NEWS, 14 (1997).
[86] R. Bonneau, C.E. Strauss, C.A. Rohl, D. Chivian, P. Bradley, L. Malmstrom, T. Robertson, D. Baker, J Mol Biol, 322 (2002) 65.
[87] R. Bonneau, J. Tsai, I. Ruczinski, D. Chivian, C. Rohl, C.E. Strauss, D. Baker, Proteins, Suppl 5 (2001) 119.
[88] D. Chivian, D.E. Kim, L. Malmstrom, P. Bradley, T. Robertson, P. Murphy, C.E. Strauss, R. Bonneau, C.A. Rohl, D. Baker, Proteins, 53 Suppl 6 (2003) 524.
[89] D. Chivian, D.E. Kim, L. Malmstrom, J. Schonbrun, C.A. Rohl, D. Baker, Proteins, 61 Suppl 7 (2005) 157.
[90] D.E. Kim, D. Chivian, D. Baker, Nucl. Acids Res., 32 (2004) W526.
[91] K.T. Simons, C. Kooperberg, E. Huang, D. Baker, J Mol Biol, 268 (1997) 209.
[92] K.T. Simons, I. Ruczinski, C. Kooperberg, B.A. Fox, C. Bystroff, D. Baker, Proteins, 34 (1999) 82.
[93] J. Moult, Curr Opin Struct Biol, 15 (2005) 285.
[94] C. Sander, R. Schneider, Proteins, 9 (1991) 56.
[95] M. Pellegrini-Calace, S. Soro, A. Tramontano, Febs J, 273 (2006) 2977.
[96] A. Fiser, R.K. Do, A. Sali, Protein Sci, 9 (2000) 1753.
[97] M.A. Marti-Renom, A.C. Stuart, A. Fiser, R. Sanchez, F. Melo, A. Sali, Annu Rev Biophys Biomol Struct, 29 (2000) 291.
[98] U. Pieper, N. Eswar, H. Braberg, M.S. Madhusudhan, F.P. Davis, A.C. Stuart, N. Mirkovic, A. Rossi, M.A. Marti-Renom, A. Fiser, B. Webb, D. Greenblatt, C.C. Huang, T.E. Ferrin, A. Sali, Nucleic Acids Res, 32 (2004) D217.
[99] A. Sali, T.L. Blundell, J Mol Biol, 234 (1993) 779.
[100]D. Petrey, Z. Xiang, C.L. Tang, L. Xie, M. Gimpelev, T. Mitros, C.S. Soto, S. Goldsmith-Fischman, A. Kernytsky, A. Schlessinger, I.Y. Koh, E. Alexov, B. Honig, Proteins, 53 Suppl 6 (2003) 430.
[101]J.U. Bowie, R. Luthy, D. Eisenberg, Science, 253 (1991) 164.
[102]D. Eisenberg, R. Luthy, J.U. Bowie, Methods Enzymol, 277 (1997) 396.
[103]R. Luethy, J.U. Bowie, D. Eisenberg, Nature, 356 (1992) 83.
[104]M.J. Sippl, J Comput Aided Mol Des, 7 (1993) 473.
[105]A. Nicholls, K.A. Sharp, B. Honig, Proteins, 11 (1991) 281.
[106]J.C. Gordon, J.B. Myers, T. Folta, V. Shoja, L.S. Heath, A. Onufriev, Nucleic Acids Res, 33 (2005) W368.
[107]J. Myers, G. Grothaus, S. Narayanan, A. Onufriev, Proteins, 63 (2006) 928.
[108]D. Bashford, M. Karplus, Biochemistry, 29 (1990) 10219.
[109]S.G. Jackson, Y. Zhang, R.J. Haslam, M.S. Junop, BMC Struct Biol, 7 (2007) 80.
[110]T.G. Kutateladze, Biochim Biophys Acta, 1761 (2006) 868.
[111]E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, T.E. Ferrin, J Comput Chem, 25 (2004) 1605.
[112]I.D. Kuntz, J.M. Blaney, S.J. Oatley, R. Langridge, T.E. Ferrin, J Mol Biol, 161 (1982) 269.
[113]F.M. Richards, Annu Rev Biophys Bioeng, 6 (1977) 151.
[114]T.E. Ferrin, C.C. Huang, L.E. Jarvis, R. Langridge, J. Mol. Graph., 6 (1988) 13.
[115]B.K. Shoichet, D.L. Bodian, I.D. Kuntz, J. Comp. Chem., 13 (1992) 380.
[116]E.C. Meng, B.K. Shoichet, I.D. Kuntz, J. Comp. Chem., 13 (1992) 505.
[117]V. Sobolev, A. Sorokine, J. Prilusky, E.E. Abola, M. Edelman, Bioinformatics, 15 (1999) 327.
[118]R. Chenna, H. Sugawara, T. Koike, R. Lopez, T.J. Gibson, D.G. Higgins, J.D. Thompson, Nucleic Acids Res, 31 (2003) 3497.
[119]K.M. Ferguson, M.A. Lemmon, J. Schlessinger, P.B. Sigler, Cell, 83 (1995) 1037.
[120]A. Otomo, S. Hadano, T. Okada, H. Mizumura, R. Kunita, H. Nishijima, J. Showguchi-Miyata, Y. Yanagisawa, E. Kohiki, E. Suga, M. Yasuda, H. Osuga, T. Nishimoto, S. Narumiya, J.E. Ikeda, Hum Mol Genet, 12 (2003) 1671.
[121]J.L. Rosa, R.P. Casaroli-Marano, A.J. Buckler, S. Vilaro, M. Barbacid, Embo J, 15 (1996) 4262.
[122]L. Renault, N. Nassar, I. Vetter, J. Becker, C. Klebe, M. Roth, A. Wittinghofer, Nature, 392 (1998) 97.
[123]A. Rodrigues, J. Santiago, S. Rubio, A. Saez, K.S. Osmont, J. Gadea, C.S. Hardtke, P.L. Rodriguez, Plant Physiol., 149 (2009) 1917.