Analysis of the targeting sequences of an iron-containing superoxide dismutase (SOD) of the dinoflagellate Lingulodinium polyedrum suggests function in multiple cellular compartments

Archives of Microbiology

Volumn 187, Issue 4, 2007, Pages 281-296

  Bodył, Andrzej ^a   Mackiewicz, Paweł ^a  

^a UNIVERSITY OF WROC AW   (Poland)

Author keywords

Alternative translation; Dinoflagellates; Peridinin plastid; Peroxisome targeting signal; Signal peptide; Superoxide dismutase

Indexed keywords

IRON; MESSENGER RNA; OLIGONUCLEOTIDE; PROTEIN SUBUNIT; SIGNAL PEPTIDE; SUPEROXIDE DISMUTASE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BIOINFORMATICS; CELL COMPARTMENTALIZATION; CELL FUNCTION; CODON; DINOFLAGELLATE; ENZYME LOCALIZATION; IRON CHELATION; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASTID; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; START CODON; STRUCTURE ANALYSIS; TRANSLATION INITIATION;

ANIMALS; BASE SEQUENCE; CELL NUCLEUS; DINOFLAGELLIDA; ELECTROPHORESIS; ISOENZYMES; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PEROXISOMES; PLASTIDS; PROTEIN BIOSYNTHESIS; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

ALGAE; DINOPHYCEAE; LINGULODINIUM POLYEDRUM;

EID: 33947362461     PISSN: 03028933     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00203-006-0194-5     Document Type: Article

References (112)

1. Acker H (2005) The oxygen sensing signal cascade unyder the influence of reactive oxygen species. Philos Trans R Soc Lond B Biol Sci 360:2201-2210
2. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18:298-305
3. Becker T, Qbadou S, Jelic M, Schleiff E (2005) Let's talk about ... chloroplast import. Plant Biol 7:1-14
4. Bender A, van Dooren GG, Ralph SA, McFadden GI, Schneider G (2003) Properties and prediction of mitochondrial transit peptides from Plasmodium falciparum. Mol Biochem Parasitol 132:59-66
5. Bendsten JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783-795
6. Bhasin M, Raghava GP (2004) ESLpred: SVM-based method for subcellular localization of eukaryotic proteins using dipeptide composition and PSI-BLAST. Nucleic Acids Res 32(Web Server issue):W414-W419
7. Blanchard JL, Hicks JS (1999) The non-photosynthetic plastid in malarial parasites and other apicomplexans is derived from outside the green plastid lineage. J Eukaryot Microbiol 46:367-375
8. Blanco E, Parra G, Guigó R (2002) Using geneid to identify genes. In: Baxevanis AD, Davison DB (eds) Current protocols in bioinformatics, vol 1. Wiley, New York (Unit 4.3)
9. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179-194
10. Bodén M, Hawkins J (2005) Prediction of subcellular localization using sequence-biased recurrent networks. Bioinformatics 21:2279-2286
11. Bodył A (2005) Do plastid-related characters support the chromalveolate hypothesis? J Phycol 41:712-719
12. Bodył A, Moszczyński K (2006) Did the peridinin plastid evolve through tertiary endosymbiosis? A hypothesis. Eur J Phycol 41:437-450
13. Bruce BD (2001) The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochim Biophys Acta 1541:2-21
14. Brydges SD, Carruthers VB (2003) Mutation of an unusual mitochondrial targeting sequence of SODB2 produces multiple targeting fates in Toxoplasma gondii. J Cell Sci 116:4675-4685
15. Bueno P, Varela J, Gimenez GG, Del Rio LA (1995) Peroxisomal copper, zinc superoxide dismutase: characterization of the isoenzyme from watermelon cotyledons. Plant Physiol 108:1151-1160
16. Cavalier-Smith T (2003) Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Philos Trans R Soc Lond B Biol Sci 359:109-134
17. Cavener DR (1987) Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res 15:1353-1361
18. Chew O, Rudhe C, Glaser E, Whelan J (2003) Characterization of the targeting signal of dual-targeted pea glutathione reductase. Plant Mol Biol 53:341-356
19. Claros MG, Vincens P (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241:779-786
20. del Rio LA, Corpas FJ, Scandalio LM, Palma JM, Gomez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255-1272
21. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005-1016
22. Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978-984
23. Emanuelsson O, Elofsson A, von Heijne G, Cristobal S (2003) In silico prediction of the peroxisomal proteome in fungi, plants and animals. J Mol Biol 330:443-456
24. Fink RC, Scandalios JG (2002) Molecular evolution and structure-function relationships of the superoxide dismutase gene families in angiosperms and their relationships to other eukaryotic and prokaryotic superoxide dismutases. Arch Biochem Biophys 399:19-36
25. Frolov I, Schlesinger S (1996) Translation of sindbis virus mRNA: analysis of sequences downstream of the initiating AUG codon that enhance translation. J Virol 70:1182-1190
26. Fünfschilling U, Rospert S (1999) Nascent polypeptide-associated complex stimulates protein import into yeast mitochondria. Mol Biol Cell 10:3289-3299
27. George R, Beddoe T, Landl K, Lithgow T (1998) The yeast nascent polypeptide-associated complex initiates protein targeting to mitochondria in vivo. Proc Natl Acad Sci USA 95:2296-2301
28. George R, Walsh P, Beddoe T, Lithgow T (2002) The nascent polypeptide-associated complex (NAC) promotes interaction of ribosomes with the mitochondrial surface in vivo. FEBS Lett 516:213-216
29. Gibbs SP (1978) The chloroplasts of Euglena may have evolved from symbiotic green algae. Can J Bot 56:2883-2889
30. Glaser E, Sjöling S, Tanudji M, Whelan J (1998) Mitochondrial protein import in plants. Signals, sorting, targeting, processing and regulation. Plant Mol Biol 38:311-338
31. Gould SB, Sommer MS, Hadfi K, Zauner S, Kroth PG, Maier U-G (2006) Protein targeting into the complex plastid of cryptophytes. J Mol Evol 62:674-681
32. Gould SG, Keller GA, Subramani S (1987) Identification of a peroxisomal targeting signal at the carboxy terminus of Wrefly luciferase. J Cell Biol 105:2923-2931
33. Gould SJ, Keller GA, Hosken N, Wilkinson J, Subramani S (1989) A conserved tripeptide sorts proteins to peroxisomes. J Cell Biol 108:1657-1664
34. Graham LE, Wilcox LW (2000) Algae. Prentice Hall, UK Guda C, Guda P, Fahy E, Subramaniam S (2004) MITOPRED: a web server for the prediction of mitochondrial proteins. Nucleic Acids Res 32:W372-W374
35. Guda C, Subramaniam S (2005) TARGET: a new method for predicting protein subcellular localization in eukaryotes. Bioinformatics 21:3963-3969
36. Hackett JD, Yoon HS, Soares MB, Bonaldo MF, Casavant TL, Scheetz TE, Nosenko T, Bhattacharya D (2004) Migration of the plastid genome to the the nucleus in a peridinin dinoflagellate. Curr Biol 14:213-218
37. Harper JT, Keeling PJ (2003) Nucleus-encoded, plastid-targeted glyceraldehydes-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol Biol Evol 20:1730-1735
38. Hiller K, Grote G, Scheer M, Münch R, Jahn D (2004) PrediSi: prediction of signal peptides and their cleavage positions. Nucleic Acids Res 32(Web Server issue):W375-W379
39. Hofacker IL (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31:3429-3431
40. Hofmann K, Stoffel W (1993) TMbase - a database of membrane spanning proteins segments. Biol Chem 374:166
41. Horton P, Park KJ, Obayashi T, Nakai K (2006) Protein subcellular localization prediction with WoLF PSORT. In: Jiang T et al. (eds) Proceedings of the 4th Asia-Pacific Bioinformatics Conference (APBC2006). Imperial College Press, Taibei, pp39-48
42. Hua S, Sun Z (2001) Support vector machine approach for protein subcellular localization prediction. Bioinformatics 17:721-728
43. Ishida K (2005) Protein targeting into plastids: a key to understanding the symbiogenetic acquisitions of plastids. J Plant Res 118:237-245
44. Joshi CP, Zhou H, Huang X, Chiang VL (1997) Context sequences of translation initiation codon in plants. Plant Mol Biol 35:993-1001
45. Kaipio K, Kallio J, Pesonen U (2005) Mitochondrial targeting signal in human neuropeptide Y gene. Biochem Biophys Res Commun 35:633-640
46. Käll L, Krogh A, Sonnhammer ELL (2004) A combined trans-membrane topology and signal peptide prediction method. J Mol Biol 338:1027-1036
47. Kilian O, Kroth PG (2005) Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J 41:175-183
48. Koumandou VL, Nisbet RER, Barbrook AC, Howe CJ (2004) Dinoflagellate chloroplasts - where have all the genes gone? Trends Genet 20:261-267
49. Kozak M (1987) An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 15:8125-8132
50. Kozak M (1990) Downstream secondary structure facilitates recognition of initiator codons by eukaryotic ribosomes. Proc Natl Acad Sci USA 87:8301-8305
51. Kozak M (2002) Pushing the limits of the scanning mechanism for initiation of translation. Gene 299:1-34
52. Krogh A (1997) Two methods for improving performance of an HMM and their application for gene finding. Proc Int Conf Intell Syst Mol Biol 5:179-186
53. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567-580
54. Kuroiwa T, Sakaguchi M, Mihara K, Omura T (1991) Systematic analysis of stop-transfer sequence for microsomal membrane. J Biol Chem 266:9251-9255
55. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of protein. J Mol Biol 157:105-132
56. Lao DM, Shimizu T (2001) A method for discriminating a signal peptide and a putative 1st transmembrane segment. In: Valafar F (ed) Proceedings of the 2001 International Conference on Mathematics and Engineering Techniques in Medicine and Biological Sciences (METMBS'01). CSREA Press, USA, pp119-125
57. Leander BS, Keeling PJ (2004) Early evolutionary history of dinoflagellates and apicomplexans (Alveolata) as inferred from HSP90 and actin phylogenies. J Phycol 40:341-350
58. Liu H, Wong L (2003) Data mining tools for biological sequences. J Bioinform Comput Biol 1:139-168
59. Lucattini R, Likic VA, Lithgow T (2004) Bacterial proteins predisposed for targeting to mitochondria. Mol Biol Evol 21:652-658
60. Macasev D, Newbigin E, Whelan J, Lithgow T (2000) How do plant mitochondria avoid importing chloroplast proteins? Components of the import apparatus To20 and Tom22 from Arabidopsis differ from their fungal counterparts. Plant Physiol 123:811-816
61. Manfredini V, Roehrs R, Peralba MC, Henriques JA, Saffi J, Ramos AL, Benfato MS (2004) Glutathione peroxides induction protects Saccharomyces cerevisiae sod1Δsod2Δ double mutants against oxidative damage. Braz J Med Biol Res 37:159-165
62. Martoglio B, Dobberstein B (1998) Signal sequences: more than just greasy peptides. Trends Cell Biol 8:410-415
63. Mathews DH, Disney MD, Childs JL, Schroeder SJ, Zuker M, Turner DH (2004) Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc Natl Acad Sci USA 101:7287-7292
64. McFadden GI, van Dooren GG (2004) Red algal genome affirms a common origin of all plastids. Curr Biol 14:514-516
65. Mukhopadhyay A, Ni L, Weiner H (2004) A co-translational model to explain the in vivo import of proteins into HeLa cell mitochondria. Biochem J 382:385-392
66. Murcha MW, Rudhe C, Elhafez D, Adams KL, Daley DO, Whelan J (2005) Adaptations required for mitochondrial import following mitochondrial to nucleus gene transfer of ribosomal protein S10. Plant Physiol 138:2134-2144
67. Nair R, Rost B (2005) Mimicking cellular sorting improves prediction of subcellular localization. J Mol Biol 348:85-100
68. Nakai K, Horton P (1999) PSORT: a program for detecting the sorting signals of proteins and predicting their subcellular localization. Trends Biochem Sci 24:34-36
69. Nassoury N, Cappadocia M, Morse D (2006) Plastid ultrastructure defines the protein import pathway in dinoflagellates. J Cell Sci 116:2867-2874
70. Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, Eisenhaber F (2003a) Motif refinement of the peroxisomal targeting signal 1 and evaluation of taxon-specific differences. J Mol Biol 328:567-579
71. Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, Eisenhaber F (2003b) Prediction of peroxisomal targeting signal 1 containing proteins from amino acid sequence. J Mol Biol 328:581-592
72. Nielsen H, Krogh A (1998) Prediction of signal peptides and signal anchors by a hidden Markov model. Proc Int Conf Intell Syst Mol Biol 6:122-130
73. Okado-Matsumoto A, Fridovich I (2001) Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J Biol Chem 276:38388-38393
74. Okamoto OK, Robertson DL, Fagan TF, Hastings JW, Colepicolo P (2001) Different regulatory mechanisms modulate the expression of a dinoflagellate iron-superoxide dismutase. J Biol Chem 276:19989-19993
75. Outten CE, Culotta VC (2004) Alternative start sites in the Saccharomyces cerevisiae GLR1 gene are responsible for mitochondrial and cytosolic isoforms of glutathione reductase. J Biol Chem 279:7785-7791
76. Park KJ, Kanehisa M (2003) Prediction of protein subcellular locations by support vector machines using compositions of amino acids and amino acid pairs. Bioinformatics 19:1656-1663
77. Patron NJ, Waller RF, Archibald JM, Keeling PJ (2005) Complex protein targeting to dinoflagellate plastids. J Mol Biol 348:1015-1024
78. Pedersen AG, Nielsen H (1997) Neural network prediction of translation initiation sites in eukaryotes: perspectives for EST and genome analysis. Proc Int Conf Intell Syst Mol Biol 5:226-233
79. Peeters N, Small I (2001) Dual targeting to mitochondria and chloroplasts. Biochim Biophys Acta 1541:54-63
80. Pesole G, Gissi C, Grillo G, Licciulli F, Liuni S, Saccone C (2000) Analysis of oligonucleotide AUG start codon context in eukariotic mRNAs. Gene 261:85-91
81. Petrova V, Drescher D, Kujumdzieva AV, Schmitt MJ (2004) Dual targeting of yeast catalase A to peroxisomes and mitochondria. Biochem J 380:393-400
82. Plewes KA, Barr SD, Gedamu L (2003) Iron superoxide dismutases targeted to the glycosomes of Leishmania chagasi are important for survival. Infect Immun 71:5910-5920
83. Reczko M, Staub E, Fiziev P, Hatzigeorgiou A (2002) Finding signal peptides in human protein sequences using recurrent neural networks. Lect Notes Comput Sci 2452:60-67
84. Reumann S (2004) Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol 135:783-800
85. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276-277
86. Rogozin IB, Kochetov AV, Kondrashov FA, Koonin EV, Milanesi L (2001) Presence of ATG triplets in 5′ untranslated regions of eukaryotic cDNAs correlates with a 'weak' context of the start codon. Bioinformatics 17:890-900
87. Rudhe C, Clifton R, Whelan J, Glaser E (2002) N-terminal domain of the dual-targeted pea glutathione reductase signal peptide controls organellar targeting efficiency. J Mol Biol 324:577-585
88. Rudhe C, Clifton R, Chew O, Zemam K, Richter S, Lamppa G, Whelan J, Glaser E (2004) Processing of the dual targeted precursor protein of glutathione reductase in mitochondria and chloroplasts. J Mol Biol 343:639-647
89. Shalchian-Tabrizi K, Skånseng M, Ronquist F, Klaveness D, Bachvaroff TR, Delwiche CF, Botnen A, Tengs T, Jakobsen KS (2006) Heterotachy processes in rhodophyte-derived secondhand plastid genes: implications for addressing the origin and evolution of dinoflagellate plastids. Mol Biol Evol 23:1504-1515
90. Salamov AA, Nishikawa T, Swindells MB (1998) Assessing protein coding region integrity in cDNA sequencing projects. Bioinformatics 14:384-390
91. Salzberg SL (1997) A method for identifying splice sites and translation start sites in eukaryotic mRNA. Comput Appl Biosci 13:365-376
92. Sarda D, Chua GH, Li KB, Krishnan A (2005) pSLIP: SVM based protein subcellular localization prediction using multiple physicochemical properties. BMC Bioinformatics 6:152
93. Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defences. Braz J Med Biol Res 38:995-1014
94. Schein AI, Kissinger JC, Ungar LH (2001) Chloroplast transit peptide prediction: a peek inside the black box. Nucleic Acids Res 29:E82
95. Schnepf E, Elbrächter M (1999) Dinophyte chloroplasts and phylogeny - a review. Grana 38:81-97
96. Seyler RW Jr, Olson JW, Maier RJ (2001) Superoxide dismutasedeficient mutants of Helicobacter pylori are hypersensitive to oxidative stress and defective in host colonization. Infect Immun 69:4034-4040
97. Sienkiewicz N, Daher W, Dive D, Wrenger C, Viscogliosi E, Wintjens R, Jouin H, Capron M, Müller S, Khalife J (2004) Identification of a mitochondrial superoxide dismutase with an unusual targeting sequence in Plasmodium falciparum. Mol Biochem Parasitol 137:121-132
98. Silva-Filho MC (2003) One ticket for multiple destinations: dual targeting of proteins to distinct subcellular locations. Curr Opin Plant Biol 6:589-595
99. Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581-1590
100. Small I, Wintz H, Akashi K, Mireau H (1998) Two birds with one stone: genes that encode products targeted to two or more compartments. Plant Mol Biol 38:265-277
101. Takahashi K, Maruyama M, Tokuzawa Y, Murakami M, Oda Y, Yoshikane N, Makabe KW, Ichisaka T, Yamanaka S (2005) Evolutionary conserved non-AUG translation initiation in NAT1/p97/DAP5 (EIF4G2). Genomics 85:360-371
102. van Dooren GG, Schwartzbach SD, Osafune T, McFadden GI (2001) Translocation of proteins across the multiple membranes of complex plastids. Biochim Biophys Acta 1541:34-53
103. von Heijne G (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225:487-494
104. Verner K (1993) Co-translational protein import into mitochondria: an alternative view. Trends Biochem Sci 18:366-371
105. Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rolland N, von Heijne G, Grebe M, Bako L, Samuelsson G (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 7:1224-1231
106. Wolfe-Simon F, Grzebyk D, Schofield O, Falkowski PG (2005) The role and evolution of superoxide dismutases in algae. J Phycol 41:453-465
107. Woodruff RC, Phillips JP, Hilliker AJ (2004) Increased spontaneous DNA damage in Cu/Zn superoxide dismutase (SOD1) deficient Drosophila. Genome 47:1029-1035
108. Xie D, Li A, Wang M, Fan Z, Feng H (2005) LOCSVMPSI: a web server for subcellular localization for eukaryotic proteins using SVM and profile of PSI-BLAST. Nucleic Acids Res 33(Web Sever issue):W105-W110
109. Yoon HS, Hackett JD, Van Dolah FM, Nosenko T, Lidie KL, Bhattacharya D (2005) Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol Biol Evol 22:1299-1308
110. Yu CS, Lin CJ, Hwang JK (2004) Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci 13:1402-1406
111. Zhang MQ (1998) Statistical features of human exons and their Xanking regions. Hum Mol Genet 7:919-932
112. Zhang XP, Glaser E (2002) Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends Plant Sci 7:14-21