Natural history of ABC systems: Not only transporters

Essays in Biochemistry

Volumn 50, Issue 1, 2011, Pages 19-42

  Dassa, Elie ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA;

ABC TRANSPORTER;

EVOLUTION; GENETICS; PHYLOGENY; PHYSIOLOGY; REVIEW;

ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL EVOLUTION; PHYLOGENY;

EID: 84856303726     PISSN: 00711365     EISSN: None     Source Type: Journal    
DOI: 10.1042/BSE0500019     Document Type: Article

References (90)

1. Finn, R.D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J.E., Gavin, O.L., Gunasekaran, P., Ceric, G., Forslund, K. et al. (2010) The Pfam protein families database. Nucleic Acids Res. 38, D211-D222
2. Oswald, C., Holland, I.B. and Schmitt, L. (2006) The motor domains of ABC-transporters: what can structures tell us? Naunyn Schmiedeberg's Arch. Pharmacol. 372, 385-399
3. Rees, D.C., Johnson, E. and Lewinson, O. (2009) ABC transporters: the power to change. Nat. Rev. Mol. Cell Biol. 10, 218-227
4. Ye, J.Q., Osborne, A.R., Groll, M. and Rapoport, T.A. (2004) RecA-like motor ATPases: lessons from structures. Biochim. Biophys. Acta 1659, 1-18
5. Davidson, A.L., Dassa, E., Orelle, C. and Chen, J. (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317-364
6. Annilo, T., Chen, Z.Q., Shulenin, S., Costantino, J., Thomas, L., Lou, H., Stefanov, S. and Dean, M. (2006) Evolution of the vertebrate ABC gene family: analysis of gene birth and death. Genomics 88, 1-11
7. Dean, M. and Allikmets, R. (2001) Complete characterization of the human ABC gene family. J. Bioenerg. Biomembr. 33, 475-479
8. Hughes, A.L. (1994) Evolution of the ATP-binding-cassette transmembrane transporters of ver-tebrates. Mol. Biol. Evol. 11, 899-910
9. Li, G., Zhang, Q.J., Ji, Z.L. and Wang, Y.Q. (2007) Origin and evolution of vertebrate ABCA genes: a story from Amphioxus. Gene 405, 88-95
10. Garcia, O., Bouige, P., Forestier, C. and Dassa, E. (2004) Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems. J. Mol. Biol. 343, 249-265
11. Dean, M. and Annilo, T. (2005) Evolution of the ATP-binding cassette (ABC) transporter super-family in vertebrates. Annu. Rev. Genomics Hum. Genet. 6, 123-142
12. Verrier, P.J., Bird, D., Buria, B., Dassa, E., Forestier, C., Geisler, M., Klein, M., Kolukisaoglu, U., Lee, Y., Martinoia, E. et al. (2008) Plant ABC proteins: a unified nomenclature and updated inven-tory. Trends Plant Sci. 13, 151-159
13. Saurin, W., Hofnung, M. and Dassa, E. (1999) Getting in or out: early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. J. Mol. Evol. 48, 22-41
14. Dassa, E. and Bouige, P. (2001) The ABC of ABCs: a phylogenetic and functional classification of ABC systems in living organisms. Res. Microbiol. 152, 211-229
15. Bouige, P., Laurent, D., Piloyan, L. and Dassa, E. (2002) Phylogenetic and functional classification of ATP-binding cassette (ABC) systems. Curr. Protein Pept. Sci. 3, 541-559
16. Fuellen, G., Spitzer, M., Cullen, P. and Lorkowski, S. (2005) Correspondence of function and phy-logeny of ABC proteins based on an automated analysis of 20 model protein data sets. Proteins 61, 888-899
17. Aller, S.G., Yu, J., Ward, A., Weng, Y., Chittaboina, S., Zhuo, R.P., Harrell, P.M., Trinh, Y.T., Zhang, Q.H., Urbatsch, I.L. and Chang, G. (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323, 1718-1722
18. Oldham, M.L., Khare, D., Quiocho, F.A., Davidson, A.L. and Chen, J. (2007) Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450, 515-521
19. Wang, B., Dukarevich, M., Sun, E.I., Yen, M.R. and Saier, M.H. (2009) Membrane porters of ATP-binding cassette transport systems are polyphyletic. J. Membr. Biol. 231, 1-10
20. 2. Nat. Cell Biol. 10, 1217-1223
21. Brem, D., Pelludat, C., Rakin, A., Jacobi, C.A. and Heesemann, J. (2001) Functional analysis of yersiniabactin transport genes of Yersinia enterocolitica. Microbiology 147, 1115-1127
22. Fetherston, J.D., Bertolino, V.J. and Perry, R.D. (1999) YbtP and YbtQ: two ABC transporters required for iron uptake in Yersinia pestis. Mol. Microbiol. 32, 289-299
23. Rodriguez, G.M. and Smith, I. (2006) Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J. Bacteriol. 188, 424-430
24. Heather, Z., Holden, M.T. G., Steward, K.F., Parkhill, J., Song, L.J., Challis, G.L., Robinson, C., Davis-Poynter, N. and Waller, A.S. (2008) A novel streptococcal integrative conjugative element involved in iron acquisition. Mol. Microbiol. 70, 1274-1292
25. Goosen, N. and Moolenaar, G.F. (2008) Repair of UV damage in bacteria. DNA Repair 7, 353-379
26. Pakotiprapha, D., Inuzuka, Y., Bowman, B.R., Moolenaar, G.F., Goosen, N., Jeruzalmi, D. and Verdinel, G.L. (2008) Crystal structure of Bacillus stearothermophilus UvrA provides insight into ATP-modulated dimerization, UvrB interaction, and DNA binding. Mol. Cell 29, 122-133
27. Croteau, D.L., DellaVecchia, M.J., Perera, L. and Van Houten, B. (2008) Cooperative damage recognition by UvrA and UvrB: identification of UvrA residues that mediate DNA binding. DNA Repair 7, 392-404
28. Lomovskaya, N., Hong, S.K., Kim, S.U., Fonstein, L., Furuya, K. and Hutchinson, R.C. (1996) The Streptomyces peucetius drrC gene encodes a UvrA-like protein involved in daunorubicin resistance and production. J. Bacteriol. 178, 3238-3245
29. Ylihonko, K., Tuikkanen, J., Jussila, S., Cong, L. and Mantsala, P. (1996) A gene cluster involved in nogalamycin biosynthesis from Streptomyces nogalater: sequence analysis and complementation of early-block mutations in the anthracycline pathway. Mol. Gen. Genet. 251, 113-120
30. Timmins, J., Gordon, E., Caria, S., Leonard, G., Acajjaoui, S., Kuo, M.S., Monchois, V. and McSweeney, S. (2009) Structural and mutational analyses of Deinococcus radiodurans UvrA2 provide insight into DNA binding and damage recognition by UvrAs. Structure 17, 547-558
31. Anand, M., Balar, B., Ulloque, R., Gross, S.R. and Kinzy, T.G. (2006) Domain and nucleotide dependence of the interaction between Saccharomyces cerevisiae translation elongation factors 3 and 1A. J. Biol. Chem. 281, 32318-32326
32. Kurata, S., Nielsen, K.H., Mitchell, S.F., Lorsch, J.R., Kaji, A. and Kaji, H. (2010) Ribosome recycling step in yeast cytoplasmic protein synthesis is catalyzed by eEF3 and ATP. Proc. Natl. Acad. Sci. U.S.A. 107, 10854-10859
33. Andersen, C.B.F., Becker, T., Blau, M., Anand, M., Halic, M., Balar, B., Mielke, T., Boesen, T., Pedersen, J.S., Spahn, C.M.T. et al. (2006) Structure of eEF3 and the mechanism of transfer RNA release from the E-site. Nature 443, 663-668
34. Kerr, I.D. (2004) Sequence analysis of twin ATP binding cassette proteins involved in translational control, antibiotic resistance, and ribonuclease L inhibition. Biochem. Biophys. Res. Commun. 315, 166-173
35. Hinnebusch, A.G. (2005) Translational regulation of GCN4 and the general amino acid control of yeast. Annu. Rev. Microbiol. 59, 407-450
36. Murat, D., Goncalves, L. and Dassa, E. (2008) Deletion of the Escherichia coli uup gene encoding a protein of the ATP binding cassette superfamily affects bacterial competitiveness. Res. Microbiol. 159, 671-677
37. Murat, D., Bance, P., Callebaut, I. and Dassa, E. (2006) ATP hydrolysis is essential for the function of the Uup ATP-binding cassette ATPase in precise excision of transposons. J. Biol. Chem. 281, 6850-6859
38. Kerr, I.D., Reynolds, E.D. and Cove, J.H. (2005) ABC proteins and antibiotic drug resistance: is it all about transport? Biochem. Soc. Trans. 33, 1000-1002
39. Bisbal, C., Silhol, M., Laubenthal, H., Kaluza, T., Carnac, G., Milligan, L., Le Roy, F. and Salehzada, T. (2000) The 2'-5' oligoadenylate/RNase L/RNase L inhibitor pathway regulates both MyoD mRNA stability and muscle cell differentiation. Mol. Cell. Biol. 20, 4959-4969
40. Dong, J.S., Lai, R., Nielsen, K., Fekete, C.A., Qiu, H.F. and Hinnebusch, A.G. (2004) The essential ATP-binding cassette protein RLI1 functions in translation by promoting preinitiation complex assembly. J. Biol. Chem. 279, 42157-42168
41. Yarunin, A., Panse, V.G., Petfalski, E., Dez, C., Tollervey, D. and Hurt, E.C. (2005) Functional link between ribosome formation and biogenesis of iron-sulfur proteins. EMBO J. 24, 580-588
42. Chen, Z.Q., Dong, J.S., Ishimura, A., Daar, I., Hinnebusch, A.G. and Dean, M. (2006) The essential vertebrate ABCE1 protein interacts with eukaryotic initiation factors. J. Biol. Chem. 281, 7452-7457
43. Kispal, G., Sipos, K., Lange, H., Fekete, Z., Bedekovics, T., Janaky, T., Bassler, J., Netz, D.J.A., Balk, J., Rotte, C. and Lill, R. (2005) Biogenesis of cytosolic ribosomes requires the essential iron-sulphur protein Rli1p and mitochondria. EMBO J. 24, 589-598
44. Khoshnevis, S., Gross, T., Rotte, C., Baierlein, C., Ficner, R. and Krebber, H. (2010) The iron- sulphur protein RNase L inhibitor functions in translation termination. EMBO Rep. 11, 214-219
45. Pisarev, A.V., Skabkin, M.A., Pisareva, V.P., Skabkina, O.V., Rakotondrafara, A.M., Hentze, M.W., Hellen, C.U.T. and Pestova, T.V. (2010) The role of ABCE1 in eukaryotic posttermination ribosomal recycling. Mol. Cell 37, 196-210
46. Karcher, A., Schele, A. and Hopfner, K.P. (2008) X-ray structure of the complete ABC enzyme ABCE1 from Pyrococcus abyssi. J. Biol. Chem. 283, 7962-7971
47. Karcher, A., Buttner, K., Martens, B., Jansen, R.P. and Hopfner, K.P. (2005) X-ray structure of RLI, an essential twin cassette ABC ATPase involved in ribosome biogenesis and HIV capsid assembly. Structure 13, 649-659
48. Barthelme, D., Scheele, U., Dinkelaker, S., Janoschka, A., MacMillan, F., Albers, S.V., Driessen, A.J.M., Stagni, M.S., Bill, E., Meyer-Klaucke, W. et al. (2007) Structural organization of essential iron-sulfur clusters in the evolutionarily highly conserved ATP-binding cassette protein ABCE1. J. Biol. Chem. 282, 14598-14607
49. Albrecht, C. and Viturro, E. (2007) The ABCA subfamily: gene and protein structures, functions and associated hereditary diseases. Pflügers Arch. 453, 581-589
50. Dassa, E. (2007) Periplasmic ABC transporters. In The Periplasm (Ehrmann, M., ed.), pp. 287-303, ASM Press, Washington DC
51. Oldham, M.L., Davidson, A.L. and Chen, J. (2008) Structural insights into ABC transporter mechanism. Curr. Opin. Struct. Biol. 18, 726-733
52. Kim, K., Lee, S., Lee, K. and Lim, D. (1998) Isolation and characterization of toluene-sensitive mutants from the toluene-resistant bacterium Pseudomonas putida GM73. J. Bacteriol. 180, 3692-3696
53. Hong, M., Gleason, Y., Wyckoff, E.E. and Payne, S.M. (1998) Identification of two Shigella flexneri chromosomal loci involved in intercellular spreading. Infect. Immun. 66, 4700-4710
54. Malinverni, J.C. and Silhavy, T.J. (2009) An ABC transport system that maintains lipid asymmetry in the Gram-negative outer membrane. Proc. Natl. Acad. Sci. U.S.A. 106, 8009-8014
55. Mohn, W.W., van der Geize, R., Stewart, G.R., Okamoto, S., Liu, J., Dijkhuizen, L. and Eltis, L.D. (2008) The actinobacterial Mce4 locus encodes a steroid transporter. J. Biol. Chem. 283, 35368-35374
56. Pandey, A.K. and Sassetti, C.M. (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc. Natl. Acad. Sci. U.S.A. 105, 4376-4380
57. Benning, C. (2009) Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu. Rev. Cell Dev. Biol. 25, 71-91
58. Rodionov, D.A., Hebbeln, P., Gelfand, M.S. and Eitinger, T. (2006) Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters. J. Bacteriol. 188, 317-327
59. Hebbeln, P., Rodionov, D.A., Alfandega, A. and Eitinger, T. (2007) Biotin uptake in prokaryotes by solute transporters with an optional ATP-binding cassette-containing module. Proc. Natl. Acad. Sci. U.S.A. 104, 2909-2914
60. Rodionov, D.A., Vitreschak, A.G., Mironov, A.A. and Gelfand, M.S. (2002) Comparative genomics of thiamin biosynthesis in procaryotes: new genes and regulatory mechanisms. J. Biol. Chem. 277, 48949-48959
61. Rodionov, D.A., Hebbeln, P., Eudes, A., ter Beek, J., Rodionova, I.A., Erkens, G.B., Slotboom, D.J., Gelfand, M.S., Osterman, A.L., Hanson, A.D. and Eitinger, T. (2009) A novel class of modular transporters for vitamins in prokaryotes. J. Bacteriol. 191, 42-51
62. Eitinger, T., Rodionov, D.A., Grote, M. and Schneider, E. (2011) Canonical and ECF-type ATP-binding cassette importers in prokaryotes: diversity in modular organization and cellular functions. FEMS Microbiol. Rev. 35, 3-67
63. Hirano, T. (2005) SMC proteins and chromosome mechanics: from bacteria to humans. Philos. Trans. R. Soc. London Ser. B 360, 507-514
64. Graumann, P.L. and Knust, T. (2009) Dynamics of the bacterial SMC complex and SMC-like proteins involved in DNA repair. Chromosome Res. 17, 265-275
65. Cobbe, N. and Heck, M.M.S. (2004) The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol. Biol. Evol. 21, 332-347
66. Nasmyth, K. and Haering, C.H. (2005) The structure and function of SMC and Kleisin complexes. Annu. Rev. Biochem. 74, 595-648
67. De Piccoli, G., Torres-Rosell, J. and Aragon, L. (2009) The unnamed complex: what do we know about Smc5-Smc6? Chromosome Res. 17, 251-263
68. Haering, C.H., Lowe, J., Hochwagen, A. and Nasmyth, K. (2002) Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 9, 773-788
69. Hirano, T. (2002) The ABCs of SMC proteins: two-armed ATPases for chromosome condensation, cohesion, and repair. Genes Dev. 16, 399-414
70. Lim, J.H. and Oh, B.H. (2009) Structural and functional similarities between two bacterial chromosome compacting machineries. Biochem. Biophys. Res. Commun. 386, 415-419
71. Cui, Y., Petrushenko, Z.M. and Rybenkov, V.V. (2008) MukB acts as a macromolecular clamp in DNA condensation. Nat. Struct. Mol. Biol. 15, 411-418
72. Petrushenko, Z.M., Cui, Y., She, W. and Rybenkov, V.V. (2010) Mechanics of DNA bridging by bacterial condensin MukBEF in vitro and in singulo. EMBO J. 29, 1126-1135
73. Lowe, J., Cordell, S.C. and van den Ent, F. (2001) Crystal structure of the SMC head domain: an ABC ATPase with 900 residues antiparallel coiled-coil inserted. J. Mol. Biol. 306, 25-35
74. Borde, V. and Cobb, J. (2009) Double functions for the Mre11 complex during DNA double-strand break repair and replication. Int. J. Biochem. Cell Biol. 41, 1249-1253
75. Williams, R.S., Williams, J.S. and Tainer, J.A. (2007) Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template. Biochem. Cell Biol. 85, 509-520
76. Waltes, R., Kalb, R., Gatei, M., Kijas, A.W., Stumm, M., Sobeck, A., Wieland, B., Varon, R., Lerenthal, Y., Lavin, M.F. et al. (2009) Human RAD50 deficiency in a Nijmegen breakage syndrome-like disorder. Am. J. Hum. Genet. 84, 605-616
77. Kinoshita, E., van der Linden, E., Sanchez, H. and Wyman, C. (2009) RAD50, an SMC family member with multiple roles in DNA break repair: how does ATP affect function? Chromosome Res. 17, 277-288
78. Hopfner, K.P., Karcher, A., Shin, D.S., Craig, L., Arthur, L.M., Carney, J.P. and Tainer, J.A. (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101, 789-800
79. Eykelenboom, J.K., Blackwood, J.K., Okely, E. and Leach, D.R.F. (2008) SbcCD causes a double-strand break at a DNA palindrome in the Escherichia coli chromosome. Mol. Cell. 29, 644-651
80. Cromie, G.A. and Leach, D.R. (2001) Recombinational repair of chromosomal DNA double-strand breaks generated by a restriction endonuclease. Mol. Microbiol. 41, 873-883
81. Bzymek, M. and Lovett, S.T. (2001) Evidence for two mechanisms of palindrome-stimulated deletion in Escherichia coli: single-strand annealing and replication slipped mispairing. Genetics 158, 527-540
82. Mascarenhas, J., Sanchez, H., Tadesse, S., Kidane, D., Krisnamurthy, M., Alonso, J.C. and Graumann, P.L. (2006) Bacillus subtilis SbcC protein plays an important role in DNA inter-strand cross-link repair. BMC Mol. Biol. 7, 20
83. Cobbe, N. and Heck, M.M. (2000) SMCs in the world of chromosome biology: from prokaryotes to higher eukaryotes. J. Struct. Biol. 129, 123-143
84. Connelly, J.C. and Leach, D.R. F. (2002) Tethering on the brink: the evolutionarily conserved Mre11-Rad50 complex. Trends Biochem. Sci. 27, 410-418
85. Cobbe, N. and Heck, M.M. (2004) The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol. Biol. Evol. 21, 332-347
86. Michel, B., Boubakri, H., Baharoglu, Z., LeMasson, M. and Lestini, R. (2007) Recombination proteins and rescue of arrested replication forks. DNA Repair 6, 967-980
87. Koroleva, O., Makharashvili, N., Courcelle, C.T., Courcelle, J. and Korolev, S. (2007) Structural conservation of RecF and Rad50: implications for DNA recognition and RecF function. EMBO J. 26, 867-877
88. Lamers, M.H., Perrakis, A., Enzlin, J.H., Winterwerp, H.H.K., de Wind, N. and Sixma, T.K. (2000) The crystal structure of DNA mismatch repair protein MutS binding to a G·T mismatch. Nature 407, 711-717
89. Obmolova, G., Ban, C., Hsieh, P. and Yang, W. (2000) Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 407, 703-710
90. Junop, M.S., Obmolova, G., Rausch, K., Hsieh, P. and Yang, W. (2001) Composite active site of an ABC ATPase: MutS uses ATP to verify mismatch recognition and authorize DNA repair. Mol. Cell 7, 1-12