A Plasmodium falciparum copper-binding membrane protein with copper transport motifs

Malaria Journal

Volumn 11, Issue , 2012, Pages

  Choveaux, David L ^a   Przyborski, Jude M ^b   Goldring, J P Dean ^a  

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Copper transporter; Malaria; Permeome; PEXEL negative

Indexed keywords

COPPER; COPPER BINDING MEMBRANE PROTEIN; MALTOSE BINDING PROTEIN; MEMBRANE PROTEIN; PEPTIDE ANTIBODY; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CHICKEN; ERYTHROCYTE MEMBRANE; ESCHERICHIA COLI; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOLOCALIZATION; IN VITRO STUDY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PROTEIN LOCALIZATION; SCHIZONT; SEQUENCE ANALYSIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CARRIER PROTEINS; CELL MEMBRANE; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; COPPER; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

EID: 84870058998     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-11-397     Document Type: Article

References (70)

1. WHO, World Malaria Report Geneva: World Health Organization 2011 http://who.int/malaria/world-malaria-report-2011/en/.
2. When is enough enough? The need for a robust pipeline of high-quality antimalarials. Wells TN, Poll EM, Discov Med 2010 9 389 398 20515606
3. Exploiting the therapeutic potential of Plasmodium falciparum solute transporters. Staines HM, Derbyshire ET, Slavic K, Tattersall A, Vial H, Krishna S, Trends Parasitol 2010 26 284 296 10.1016/j.pt.2010.03.004 20392668
4. Membrane transport proteins of the malaria parasite. Martin RE, Ginsburg H, Kirk K, Mol Microbiol 2009 74 519 528 10.1111/j.1365-2958.2009.06863.x 19796339
5. Copper pathways in Plasmodium falciparum infected erythrocytes indicate an efflux role for the copper P-ATPase. Rasoloson D, Shi L, Chong CR, Kafsack BF, Sullivan DJ, Biochem J 2004 381 Pt 3 803 811 15125686 (Pubitemid 39120490)
6. Oxygen toxicity, oxygen radicals, transition metals and disease. Halliwell B, Gutteridge JM, Biochem J 1984 219 1 14 6326753 (Pubitemid 14171443)
7. Mechanisms for copper acquisition, distribution and regulation. Kim BE, Nevitt T, Thiele DJ, Nat Chem Biol 2008 4 176 185 10.1038/nchembio.72 18277979 (Pubitemid 351264130)
8. Human copper homeostasis: a network of interconnected pathways. Lutsenko S, Curr Opin Chem Biol 2010 14 211 217 10.1016/j.cbpa.2010.01.003 20117961
9. Trace elements in human physiology and pathology. Tapiero H, Townsend DM, Tew KD, Copper. Biomed Pharmacother 2003 57 386 398 (Pubitemid 37494714)
10. Structure of the Ctr1 copper trans'PORE'ter reveals novel architecture. Nose Y, Rees EM, Thiele DJ, Trends Biochem Sci 2006 31 604 607 10.1016/j.tibs.2006.09.003 16982196 (Pubitemid 44635262)
11. Drosophila Ctr1A functions as a copper transporter essential for development. Turski ML, Thiele DJ, J Biol Chem 2007 282 24017 24026 10.1074/jbc.M703792200 17573340 (Pubitemid 47328034)
12. Copper transport activity of yeast Ctr1 is down-regulated via its C terminus in response to excess copper. Wu X, Sinani D, Kim H, Lee J, J Biol Chem 2009 284 4112 4122 19088072
13. Plasmodium Genomics Resource http://www.plasmodb.org.
14. Identification of neutralization and diagnostic epitopes on PIM, the polymorphic immunodominant molecule of Theileria parva. Toye P, Nyanjui J, Goddeeris B, Musoke AJ, Infect Immun 1996 64 1832 1838 8613398 (Pubitemid 26129844)
15. The HMMTOP transmembrane topology prediction server. Tusnady GE, Simon I, Bioinformatics 2001 17 849 850 10.1093/bioinformatics/17.9.849 11590105 (Pubitemid 32970487)
16. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Krogh A, Larsson B, von Heijne G, Sonnhammer EL, J Mol Biol 2001 305 567 580 10.1006/jmbi.2000.4315 11152613 (Pubitemid 33032862)
17. Predict7, a program for protein structure prediction. Carmenes RS, Freije JP, Molina MM, Martin JM, Biochem Biophys Res Commun 1989 159 687 693 10.1016/0006-291X(89)90049-1 2539121 (Pubitemid 19089806)
18. Anti-peptide antibodies differentiate between plasmodial lactate dehydrogenases. Hurdayal R, Achilonu I, Choveaux D, Coetzer THT, Goldring JPD, Peptides 2010 31 525 532 10.1016/j.peptides.2010.01.002 20093160
19. A NIMA-related protein kinase is essential for completion of the sexual cycle of malaria parasites. Reininger L, Billker O, Tewari R, Mukhopadhyay A, Fennell C, Dorin-Semblat D, Doerig C, Goldring D, Harmse L, Ranford-Cartwright L, Packer J, Doerig C, J Biol Chem 2005 280 31957 31964 10.1074/jbc.M504523200 15970588 (Pubitemid 41291946)
20. Development of a simple method for the recovery of recombinant proteins from Escherichia coli periplasm. French C, Keshavarz-Moore E, Ward JM, Enzyme Microb Technol 1996 19 332 338 10.1016/S0141-0229(96)00003-8 (Pubitemid 26319491)
21. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Laemmli UK, Nature 1970 227 680 685 10.1038/227680a0 5432063
22. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Towbin H, Staehelin T, Gordon J, Proc Natl Acad Sci USA 1979 76 4350 4354 10.1073/pnas.76.9.4350 388439 (Pubitemid 9256559)
23. Protein quantification methods to determine protein concentration prior to electrophoresis. Goldring JP, Methods Mol Biol 2012 869 29 35 10.1007/978-1-61779-821-4-3 22585474
24. An unusual ERAD-like complex is targeted to the apicoplast of Plasmodium falciparum. Spork S, Hiss JA, Mandel K, Sommer M, Kooij TW, Chu T, Schneider G, Maier UG, Przyborski JM, Eukaryot Cell 2009 8 1134 1145 10.1128/EC.00083-09 19502583
25. Synchronization of Plasmodium falciparum erythrocytic stages in culture. Lambros C, Vanderberg JP, J Parasitol 1979 65 418 420 10.2307/3280287 383936 (Pubitemid 10222999)
26. A quantitative test for copper using bicinchoninic acid. Brenner AJ, Harris ED, Anal Biochem 1995 226 80 84 10.1006/abio.1995.1194 7785783
27. Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Tonkin CJ, van Dooren GG, Spurck TP, Struck NS, Good RT, Handman E, Cowman AF, McFadden GI, Mol Biochem Parasitol 2004 137 13 21 10.1016/j.molbiopara.2004.05. 009 15279947 (Pubitemid 38987938)
28. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S, Science 1996 272 1136 1144 10.1126/science.272.5265.1136 8638158
29. Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome C oxidase. Horng Y-C, Cobine PA, Maxfield AB, Carr HS, Winge DR, J Biol Chem 2004 279 35334 35340 10.1074/jbc.M404747200 15199057 (Pubitemid 39100532)
30. Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. Puig S, Lee J, Lau M, Thiele DJ, J Biol Chem 2002 277 26021 26030 10.1074/jbc.M202547200 11983704 (Pubitemid 34967084)
31. Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. Escalante AA, Ayala FJ, Proc Natl Acad Sci USA 1995 92 5793 5797 10.1073/pnas.92.13.5793 7597031
32. A phylogenetic comparison of gene trees constructed from plastid, mitochondrial and genomic DNA of Plasmodium species. Rathore D, Wahl AM, Sullivan M, McCutchan TF, Mol Biochem Parasitol 2001 114 89 94 10.1016/S0166-6851(01)00241-9 11356517 (Pubitemid 32453218)
33. Three-dimensional structure of the human copper transporter hCTR1. De Feo CJ, Aller SG, Siluvai GS, Blackburn NJ, Unger VM, Proc Natl Acad Sci USA 2009 106 4237 4242 10.1073/pnas.0810286106 19240214
34. Genome-scale protein expression and structural biology of Plasmodium falciparum and related Apicomplexan organisms. Vedadi M, Lew J, Artz J, Amani M, Zhao Y, Dong A, Wasney GA, Gao M, Hills T, Brokx S, Qiu W, Sharma S, Diassiti A, Alam Z, Melone M, Mulichak A, Wernimont A, Bray J, Loppnau P, Plotnikova O, Newberry K, Sundararajan E, Houston S, Walker J, Tempel W, Bochkarev A, Kozieradzki I, Edwards A, Arrowsmith C, Roos D, Kain K, Hui R, Mol Biochem Parasitol 2007 151 100 110 10.1016/j.molbiopara.2006.10.011 17125854 (Pubitemid 44911074)
35. N-terminal domains of human copper-transporting adenosine triphosphatases (the Wilson's and Menkes disease proteins) bind copper selectively in vivo and in vitro with stoichiometry of one copper per metal-binding repeat. Lutsenko S, Petrukhin K, Cooper MJ, Gilliam CT, Kaplan JH, J Biol Chem 1997 272 18939 18944 10.1074/jbc.272.30.18939 9228074 (Pubitemid 27318247)
36. A Mets motif peptide found in copper transport proteins selectively binds Cu(I) with methionine-only coordination. Jiang J, Nadas IA, Kim MA, Franz KJ, Inorg Chem 2005 44 9787 9794 10.1021/ic051180m 16363848
37. Biochemical characterization of the human copper transporter Ctr1. Lee J, Pena MM, Nose Y, Thiele DJ, J Biol Chem 2002 277 4380 4387 10.1074/jbc. M104728200 11734551 (Pubitemid 34968704)
38. Discovery of gene function by expression profiling of the malaria parasite life cycle. Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, De La Vega P, Holder AA, Batalov S, Carucci DJ, Wenzler EA, Science 2003 301 1503 1508 10.1126/science.1087025 12893887 (Pubitemid 37128535)
39. Locating proteins in the cell using TargetP, SignalP and related tools. Emanuelsson O, Brunak S, von Heijne G, Nielsen H, Nat Protoc 2007 2 953 971 10.1038/nprot.2007.131 17446895 (Pubitemid 46745592)
40. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, Roos DS, Cowman AF, McFadden GI, Science 2003 299 705 708 10.1126/science.1078599 12560551 (Pubitemid 36159484)
41. An exported protein of Plasmodium falciparum is synthesized as an integral membrane protein. Gunther K, Tummler M, Arnold HH, Ridley R, Goman M, Scaife JG, Lingelbach K, Mol Biochem Parasitol 1991 46 149 157 10.1016/0166-6851(91)90208-N 1852170
42. A cluster of ring stage-specific genes linked to a locus implicated in cytoadherence in Plasmodium falciparum codes for PEXEL-negative and PEXEL-positive proteins exported into the host cell. Spielmann T, Hawthorne PL, Dixon MW, Hannemann M, Klotz K, Kemp DJ, Klonis N, Tilley L, Trenholme KR, Gardiner DL, Mol Biol Cell 2006 17 3613 3624 10.1091/mbc.E06-04-0291 16760427 (Pubitemid 44156453)
43. Sequence requirements for the export of the Plasmodium falciparum Maurer's clefts protein REX2. Haase S, Herrmann S, Gruring C, Heiber A, Jansen PW, Langer C, Treeck M, Cabrera A, Bruns C, Struck NS, Kono M, Engelberg K, Ruch U, Stunnenberg HG, Gilberger TW, Spielmann T, Mol Microbiol 2009 71 1003 1017 10.1111/j.1365-2958.2008.06582.x 19170882
44. Export of PfSBP1 to the Plasmodium falciparum Maurer's clefts. Saridaki T, Frohlich KS, Braun-Breton C, Lanzer M, Traffic 2009 10 137 152 10.1111/j.1600-0854.2008.00860.x 19054387
45. Eukaryotic CTR copper uptake transporters require two faces of the third transmembrane domain for helix packing, oligomerization, and function. Aller SG, Eng ET, De Feo CJ, Unger VM, J Biol Chem 2004 279 53435 53441 10.1074/jbc.M409421200 15385536 (Pubitemid 40051848)
46. Tryptophan scanning analysis of the membrane domain of CTR-copper transporters. De Feo CJ, Mootien S, Unger VM, J Membr Biol 2010 234 113 123 10.1007/s00232-010-9239-4 20224886
47. A place for thioether chemistry in cellular copper ion recognition and trafficking. Davis AV, O'Halloran TV, Nat Chem Biol 2008 4 148 151 10.1038/nchembio0308-148 18277969 (Pubitemid 351265328)
48. Functional implications of multistage copper binding to the prion protein. Hodak M, Chisnell R, Lu W, Bernholc J, Proc Natl Acad Sci USA 2009 106 11576 11581 10.1073/pnas.0903807106 19561303
49. Escherichia coli mechanisms of copper homeostasis in a changing environment. Rensing C, Grass G, FEMS Microbiol Rev 2003 27 197 213 10.1016/S0168-6445(03)00049-4 12829268 (Pubitemid 36694656)
50. Metalloproteins and metal sensing. Waldron KJ, Rutherford JC, Ford D, Robinson NJ, Nature 2009 460 823 830 10.1038/nature08300 19675642
51. Promiscuity and preferences of metallothioneins: the cell rules. Foster AW, Robinson NJ, BMC Biol 2011 9 25 10.1186/1741-7007-9-25 21527046
52. Plasmodium falciparum heat shock protein 70 is able to suppress the thermosensitivity of an Escherichia coli DnaK mutant strain. Shonhai A, Boshoff A, Blatch GL, Mol Genet Genomics 2005 274 70 78 10.1007/s00438-005-1150-9 15973516 (Pubitemid 41396985)
53. A nutrient-permeable channel on the intraerythrocytic malaria parasite. Desai SA, Krogstad DJ, McCleskey EW, Nature 1993 362 643 646 10.1038/362643a0 7681937 (Pubitemid 23109275)
54. Molecular make-up of the Plasmodium parasitophorous vacuolar membrane. Spielmann T, Montagna GN, Hecht L, Matuschewski K, Int J Med Microbiol 2012 302 179 186 10.1016/j.ijmm.2012.07.011 22898489
55. Chloride (or bicarbonate)-dependent copper uptake through the anion exchanger in human red blood cells. Alda JO, Garay R, Am J Physiol 1990 259 4 Pt 1 570 C576 2221038 (Pubitemid 20340344)
56. Copper-binding proteins in human erythrocytes: searching for potential biomarkers of copper over-exposure. Speisky H, Navarro P, Cherian MG, Jimenez I, BioMetals 2003 16 113 123 10.1023/A:1020724331271 12572671 (Pubitemid 36140222)
57. Fluxes in free and total zinc are essential for progression of intraerythrocytic stages of Plasmodium falciparum. Marvin RG, Wolford JL, Kidd MJ, Murphy S, Ward J, Que EL, Mayer ML, Penner-Hahn JE, Haldar K, O'Halloran TV, Chem Biol 2012 19 731 741 10.1016/j.chembiol.2012.04.013 22726687
58. pfmdr2 confers heavy metal resistance to Plasmodium falciparum. Rosenberg E, Litus I, Schwarzfuchs N, Sinay R, Schlesinger P, Golenser J, Baumeister S, Lingelbach K, Pollack Y, J Biol Chem 2006 281 27039 27045 10.1074/jbc.M601686200 16849328 (Pubitemid 44401732)
59. Occurrence of copper proteins through the three domains of life: a bioinformatic approach. Andreini C, Banci L, Bertini I, Rosato A, J Proteome Res 2008 7 209 216 10.1021/pr070480u 17988086 (Pubitemid 351171133)
60. Malaria parasite transporters as a drug-delivery strategy. Biagini GA, Ward SA, Bray PG, Trends Parasitol 2005 21 299 301 10.1016/j.pt.2005.05.013 15923144 (Pubitemid 40807171)
61. Copper transporters and the cellular pharmacology of the platinum-containing cancer drugs. Howell SB, Safaei R, Larson CA, Sailor MJ, Mol Pharmacol 2010 77 887 894 10.1124/mol.109.063172 20159940
62. Fosmidomycin uptake into Plasmodium and Babesia-infected erythrocytes is facilitated by parasite-induced new permeability pathways. Baumeister S, Wiesner J, Reichenberg A, Hintz M, Bietz S, Harb OS, Roos DS, Kordes M, Friesen J, Matuschewski K, Lingelbach K, Jomaa H, Seeber F, PLoS One 2011 6 19334 10.1371/journal.pone.0019334 21573242
63. Plasmodium falciparum: DNA sequence specificity of cisplatin and cisplatin analogues. Murray V, Campbell HM, Gero AM, Exp Parasitol 2011 128 396 400 10.1016/j.exppara.2011.05.002 21616072
64. The Plasmodium falciparum-infected red blood cell. Tilley L, Dixon MW, Kirk K, Int J Biochem Cell Biol 2011 43 839 842 10.1016/j.biocel.2011.03.012 21458590
65. Antimalarial activity of selected aromatic chelators V. Localization of 59Fe in Plasmodium falciparum in the presence of oxines. Scheibel LW, Rodriguez S, Prog Clin Biol Res 1989 313 119 149 2506579
66. Transition metal complexes of buparvaquone as potent new antimalarial agents. 1. Synthesis, X-ray crystal-structures, electrochemistry and antimalarial activity against Plasmodium falciparum. Gokhale NH, Padhye SB, Croft SL, Kendrick HD, Davies W, Anson CE, Powell AK, J Inorg Biochem 2003 95 249 258 10.1016/S0162-0134(03)00134-X 12818795 (Pubitemid 36773621)
67. Cure with cisplatin (II) or murine malaria infection and in vitro inhibition of a chloroquine-resistant Plasmodium falciparum isolate. Nair L, Bhasin VK, Jpn J Med Sci Biol 1994 47 241 252 7739147
68. Protein export in malaria parasites: do multiple export motifs add up to multiple export pathways? Spielmann T, Gilberger TW, Trends Parasitol 2009 26 6 10 19879191
69. PEXEL-independent trafficking of Plasmodium falciparum SURFIN4.2 to the parasite-infected red blood cell and Maurer's clefts. Alexandre JS, Yahata K, Kawai S, Torii M, Kaneko O, Parasitol Int 2011 60 313 320 10.1016/j.parint.2011. 05.003 21616162
70. Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Boddey JA, Moritz RL, Simpson RJ, Cowman AF, Traffic 2009 10 285 299 10.1111/j.1600-0854.2008.00864.x 19055692