Inteins, valuable genetic elements in molecular biology and biotechnology

Applied Microbiology and Biotechnology

Volumn 87, Issue 2, 2010, Pages 479-489

  Elleuche, Skander ^a   Pöggeler, Stefanie ^b  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b HAMBURG UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Cyclic proteins; Intein; Protein purification; Protein splicing; Selenoproteins

Indexed keywords

BIOCHEMISTRY; BIOTECHNOLOGY; MOLECULAR BIOLOGY; MOLECULAR STRUCTURE; PURIFICATION; RNA; SYNTHESIS (CHEMICAL);

CATALYTIC ACTIVITY; CATALYTIC RESIDUE; COFACTORS; ENGINEERING APPLICATIONS; EXTEINS; FLANKING SEQUENCE; FUNCTIONAL PROTEINS; GENETIC ELEMENTS; HOST PROTEINS; INTEINS; INTRAMOLECULAR REACTIONS; N-AND C-TERMINAL DOMAINS; PEPTIDE BONDS; PRE-MRNA; PROTEIN PURIFICATION; PROTEIN-SPLICING; SELENOPROTEINS; SELF-EXCISION; VIRAL PROTEINS;

PROTEINS;

INTEIN; SELENOPROTEIN; BACTERIAL PROTEIN;

BIOTECHNOLOGY; CATALYSIS; ENZYME ACTIVITY; GENETIC ENGINEERING; MOLECULAR ECOLOGY; PEPTIDE; PROTEIN;

BIOTECHNOLOGY; CATALYSIS; MOLECULAR BIOLOGY; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SHORT SURVEY; CHEMISTRY; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE;

BACTERIAL PROTEINS; BIOTECHNOLOGY; CATALYSIS; INTEINS; MOLECULAR BIOLOGY; PROTEIN SPLICING; PROTEIN STRUCTURE, TERTIARY;

EID: 77953043452     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-010-2628-x     Document Type: Short Survey

References (103)

1. Amitai G, Callahan BP, Stanger MJ, Belfort G, Belfort M (2009) Modulation of intein activity by its neighboring extein substrates. Proc Natl Acad Sci U S A 106:11005-11010
2. Arnér ES, Sarioglu H, Lottspeich F, Holmgren A, Bock A (1999) High-level expression in Escherichia coli of selenocysteine-containing rat thioredoxin reductase utilizing gene fusions with engineered bacterial-type SECIS elements and co-expression with the selA, selB and selC genes. J Mol Biol 292:1003-1016
3. Arnér ES, Cheng Q, Donald HJ (2009) Method for producing selenoproteins. World Intellectual Property Organization (WIPO), United Nations
4. Arnold U (2009) Incorporation of non-natural modules into proteins: structural features beyond the genetic code. Biotechnol Lett 31:1129-1139
5. Banki MR, Gerngross TU, Wood DW (2005) Novel and economical purification of recombinant proteins: intein-mediated protein purification using in vivo polyhydroxybutyrate (PHB) matrix association. Protein Sci 14:1387-1395
6. Bastings MM, van Baal I, Meijer EW, Merkx M (2008) One-step refolding and purification of disulfide-containing proteins with a C-terminal MESNA thioester. BMC Biotechnol 8:76
7. Belfort M, Derbyshire V, Stoddard BL, Wood DW (2005) Homing endonucleases and inteins. Springer, Berlin Heidelberg New York
8. Billich A, Zocher R (1987) Enzymatic synthesis of cyclosporin A. J Biol Chem 262:17258-17259
9. Caspi J, Amitai G, Belenkiy O, Pietrokovski S (2003) Distribution of split DnaE inteins in cyanobacteria. Mol Microbiol 50:1569-1577
10. Charalambous A, Andreou M, Skourides PA (2009) Intein-mediated site-specific conjugation of Quantum Dots to proteins in vivo. J Nanobiotechnology 7:9
11. Cheriyan M, Perler FB (2009) Protein splicing: a versatile tool for drug discovery. Adv Drug Deliv Rev 61:899-907
12. Chevalier BS, Stoddard BL (2001) Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility. Nucl Acids Res 29:3757-3774
13. Choi JI, Lee SY, Han K (1998) Cloning of the Alcaligenes latus polyhydroxyalkanoate biosynthesis genes and use of these genes for enhanced production of Poly(3-hydroxybutyrate) in Escherichia coli. Appl Environ Microbiol 64:4897-4903
14. Choi JJ, Nam KH, Min B, Kim SJ, Söll D, Kwon ST (2006) Protein trans-splicing and characterization of a split family B-type DNA polymerase from the hyperthermophilic archaeal parasite Nanoarchaeum equitans. J Mol Biol 356:1093-1106
15. Chong S, Xu MQ (1997) Protein splicing of the Saccharomyces cerevisiae VMA intein without the endonuclease motifs. J Biol Chem 272:15587-155890
16. Chong S, Xu MQ (2005) Harnessing inteins for protein purification and characterization. In: Belfort M, Derbyshire V, Stoddard BL, Wood DW (eds) Homing endonucleases and inteins, vol. 16. Springer, Berlin Heidelberg New York, pp. 273-292
17. Chong S, Mersha FB, Comb DG, Scott ME, Landry D, Vence LM, Perler FB, Benner J, Kucera RB, Hirvonen CA, Pelletier JJ, Paulus H, Xu MQ (1997) Single-column purification of free recombinant proteins using a self-cleavable affinity tag derived from a protein splicing element. Gene 192:271-281
18. Craik DJ (2006) Chemistry. Seamless proteins tie up their loose ends. Science 311:1563-1564
19. Craik DJ, Daly NL, Bond T, Waine C (1999) Plant cyclotides: a unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J Mol Biol 294:1327-1336
20. Dassa B, Amitai G, Caspi J, Schueler-Furman O, Pietrokovski S (2007) Trans protein splicing of cyanobacterial split inteins in endogenous and exogenous combinations. Biochemistry 46:322-330
21. Dassa B, London N, Stoddard BL, Schueler-Furman O, Pietrokovski S (2009) Fractured genes: a novel genomic arrangement involving new split inteins and a new homing endonuclease family. Nucl Acids Res 37:2560-2573
22. Dawson PE, Kent SB (2000) Synthesis of native proteins by chemical ligation. Annu Rev Biochem 69:923-960
23. Derbyshire V, Wood DW, Wu W, Dansereau JT, Dalgaard JZ, Belfort M (1997) Genetic definition of a protein-splicing domain: functional mini-inteins support structure predictions and a model for intein evolution. Proc Natl Acad Sci U S A 94:11466-11471
24. Ding Y, Xu MQ, Ghosh I, Chen X, Ferrandon S, Lesage G, Rao Z (2003) Crystal structure of a mini-intein reveals a conserved catalytic module involved in side chain cyclization of asparagine during protein splicing. J Biol Chem 278:39133-39142
25. Douglas SE, Penny SL (1999) The plastid genome of the cryptophyte alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae. J Mol Evol 48:236-344
26. Driscoll DM, Copeland PR (2003) Mechanism and regulation of selenoprotein synthesis. Ann Rev Nutr 23:17-40
27. Elleuche S, Pöggeler S (2007) Trans-splicing of an artificially split fungal mini-intein. Biochem Biophys Res Commun 355:830-834
28. Elleuche S, Pöggeler S (2009) Inteins - selfish elements in fungal genomes. In: Anke T, Weber D (eds) The mycota XV. Physiology and genetics. Selected basic and applied aspects. Springer, Berlin Heidelberg New York, pp. 41-61
29. Elleuche S, Nolting N, Pöggeler S (2006) Protein splicing of PRP8 mini-inteins from species of the genus Penicillium. Appl Microbiol Biotechnol 72:959-967
30. Evans TC Jr, Xu MQ (1999) Intein-mediated protein ligation: harnessing nature's escape artists. Biopolymers 51:333-342
31. Evans TC Jr, Benner J, Xu MQ (1999) The cyclization and polymerization of bacterially expressed proteins using modified self-splicing inteins. J Biol Chem 274:18359-18363
32. Floss DM, Schallau K, Rose-John S, Conrad U, Scheller J (2009) Elastin-like polypeptides revolutionize recombinant protein expression and their biomedical application. Trends Biotechnol 28:37-45
33. Fong BA, Wu WY, Wood DW (2009) Optimization of ELP-intein mediated protein purification by salt substitution. Protein Expr Purif 66:198-202
34. Fong BA, Wu WY, Wood DW (2010) The potential role of self-cleaving purification tags in commercial-scale processes. Trends Biotechnol 28:272-279
35. Ge X, Yang DS, Trabbic-Carlson K, Kim B, Chilkoti A, Filipe CD (2005) Self-cleavable stimulus responsive tags for protein purification without chromatography. J Am Chem Soc 127:11228-11229
36. Georgiou G, Jeong KJ (2005) Proteins from PHB granules. Protein Sci 14:1385-1386
37. Gillies AR, Hsii JF, Oak S, Wood DW (2008) Rapid cloning and purification of proteins: gateway vectors for protein purification by self-cleaving tags. Biotechnol Bioeng 101:229-240
38. Gillies AR, Mahmoud RB, Wood DW (2009) PHB-intein-mediated protein purification strategy. Methods Mol Biol 498:173-183
39. Gogarten JP, Senejani AG, Zhaxybayeva O, Olendzenski L, Hilario E (2002) Inteins: structure, function, and evolution. Annu Rev Microbiol 56:263-287
40. Hall TM, Porter JA, Young KE, Koonin EV, Beachy PA, Leahy DJ (1997) Crystal structure of a Hedgehog autoprocessing domain: homology between Hedgehog and self-splicing proteins. Cell 91:85-97
41. Hirata R, Ohsumk Y, Nakano A, Kawasaki H, Suzuki K, Anraku Y (1990) Molecular structure of a gene, VMA1, encoding the catalytic subunit of H(+)-translocating adenosine triphosphatase from vacuolar membranes of Saccharomyces cerevisiae. J Biol Chem 265:6726-6733
42. Hondal RJ (2009) Using chemical approaches to study selenoproteins-focus on thioredoxin reductases. Biochim Biophys Acta 1790:1501-1512
43. Johnson MA, Southworth MW, Herrmann T, Brace L, Perler FB, Wüthrich K (2007) NMR structure of a KlbA intein precursor from Methanococcus jannaschii. Protein Sci 16:1316-1328
44. Kane PM, Yamashiro CT, Wolczyk DF, Neff N, Goebl M, Stevens TH (1990) Protein splicing converts the yeast TFP1 gene product to the 69-kD subunit of the vacuolar H(+)-adenosine triphosphatase. Science 250:651-657
45. Klabunde T, Sharma S, Telenti A, Jacobs WRJ, Sacchettini JC (1998) Crystal structure of GyrA intein from Mycobacterium xenopi reveals structural basis of protein splicing. Nat Struct Biol 5:31-36
46. Koonin EV (1995) A protein splice-junction motif in hedgehog family proteins. Trends Biochem Sci 20:141-142
47. Liu XQ (2000) Protein-splicing intein: genetic mobility, origin, and evolution. Ann Rev Genet 34:61-76
48. Liu XQ, Yang J (2003) Split dnaE genes encoding multiple novel inteins in Trichodesmium erythraeum. J Biol Chem 278:26315-26318
49. Liu XQ, Yang J, Meng Q (2003) Four inteins and three group II introns encoded in a bacterial ribonucleotide reductase gene. J Biol Chem 278:46828-46831
50. Liu JR, Duan CH, Zhao X, Tzen JT, Cheng KJ, Pai CK (2008) Cloning of a rumen fungal xylanase gene and purification of the recombinant enzyme via artificial oil bodies. Appl Microbiol Biotechnol 79:225-233
51. Luo J, Hall BD (2007) A multistep process gave rise to RNA polymerase IV of land plants. J Mol Evol 64:101-112
52. Mathys S, Evans TC, Chute IC, Wu H, Chong S, Benner J, Liu XQ, Xu MQ (1999) Characterization of a self-splicing mini-intein and its conversion into autocatalytic N- and C-terminal cleavage elements: facile production of protein building blocks for protein ligation. Gene 231:1-13
53. Meyer DE, Chilkoti A (1999) Purification of recombinant proteins by fusion with thermally-responsive polypeptides. Nat Biotechnol 17:1112-1115
54. Mills KV, Lew BM, Jiang S, Paulus H (1998) Protein splicing in trans by purified N- and C-terminal fragments of the Mycobacterium tuberculosis RecA intein. Proc Natl Acad Sci USA 95:3543-3548
55. Mootz HD, Muir TW (2002) Protein splicing triggered by a small molecule. J Am Chem Soc 124:9044-9045
56. Muir TW, Sondhi D, Cole PA (1998) Expressed protein ligation: a general method for protein engineering. Proc Natl Acad Sci U S A 95:6705-6710
57. Noren CJ, Wang J, Perler FB (2000) Dissecting the chemistry of protein splicing and its applications. Angew Chem Int Ed Engl 39:450-466
58. Oeemig JS, Aranko AS, Djupsjobacka J, Heinamaki K, Iwai H (2009) Solution structure of DnaE intein from Nostoc punctiforme: structural basis for the design of a new split intein suitable for site-specific chemical modification. FEBS Lett 583:1451-1456
59. Ozawa T, Umezawa Y (2005) Inteins for split-protein reconstitutions and their applications. In: Belfort M, Derbyshire V, Stoddard BL, Wood DW (eds) Homing endonucleases and inteins, vol. 16. Springer, Berlin Heidelberg New York, pp. 307-323
60. Ozawa T, Sako Y, Sato M, Kitamura T, Umezawa Y (2003) A genetic approach to identifying mitochondrial proteins. Nat Biotechnol 21:287-293
61. Ozawa T, Nishitani K, Sako Y, Umezawa Y (2005) A high-throughput screening of genes that encode proteins transported into the endoplasmic reticulum in mammalian cells. Nucleic Acids Res 33:e34
62. Paulus H (2000) Protein splicing and related forms of protein autoprocessing. Annu Rev Biochem 69:447-496
63. Perler FB (1998) Protein splicing of inteins and hedgehog autoproteolysis: structure, function, and evolution. Cell 92:1-4
64. Perler FB (2002) InBase: the Intein Database. Nucl Acids Res 30:383-384
65. Perler FB, Davis EO, Dean GE, Gimble FS, Jack WE, Neff N, Noren CJ, Thorner J, Belfort M (1994) Protein splicing elements: inteins and exteins - a definition of terms and recommended nomenclature. Nucl Acids Res 22:1125-1127
66. Perler FB, Olsen GJ, Adam E (1997) Compilation and analysis of intein sequences. Nucl Acids Res 25:1087-1093
67. Pietrokovski S (1994) Conserved sequence features of inteins (protein introns) and their use in identifying new inteins and related proteins. Protein Sci 3:2340-2350
68. Pietrokovski S (1998) Identification of a virus intein and a possible variation in the protein-splicing reaction. Curr Biol 8:R634-R635
69. Poulter RT, Goodwin TJ, Butler MI (2007) The nuclear-encoded inteins of fungi. Fungal Genet Biol 44:153-179
70. Saleh L, Perler FB (2006) Protein splicing in cis and in trans. Chem Rec 6:183-193
71. Sancheti H, Camarero JA (2009) "Splicing up" drug discovery. Cell-based expression and screening of genetically-encoded libraries of backbone-cyclized polypeptides. Adv Drug Deliv Rev 61:908-917
72. Scott CP, Abel-Santos E, Wall M, Wahnon DC, Benkovic SJ (1999) Production of cyclic peptides and proteins in vivo. Proc Natl Acad Sci USA 96:13638-13643
73. Severinov K, Muir TW (1998) Expressed protein ligation, a novel method for studying protein-protein interactions in transcription. J Biol Chem 273:16205-16209
74. Seyedsayamdost MR, Yee CS, Stubbe J (2007) Site-specific incorporation of fluorotyrosines into the R2 subunit of E. coli ribonucleotide reductase by expressed protein ligation. Nat Protoc 2:1225-1235
75. Sharma SS, Chong S, Harcum SW (2006) Intein-mediated protein purification of fusion proteins expressed under high-cell density conditions in E. coli. J Biotechnol 125:48-56
76. Shen Y, Ai HX, Song R, Liang ZN, Li JF, Zhang SQ (2010) Expression and purification of moricin CM4 and human beta-defensins 4 in Escherichia coli using a new technology. Microbiol Res in press
77. Shingledecker K, Jiang SQ, Paulus H (1998) Molecular dissection of the Mycobacterium tuberculosis RecA intein: design of a minimal intein and of a trans-splicing system involving two intein fragments. Gene 207:187-195
78. Singleton SF, Simonette RA, Sharma NC, Roca AI (2002) Intein-mediated affinity-fusion purification of the Escherichia coli RecA protein. Protein Expr Purif 26:476-488
79. Southworth MW, Adam E, Panne D, Byer R, Kautz R, Perler FB (1998) Control of protein splicing by intein fragment reassembly EMBO J 17:918-926
80. Southworth MW, Benner J, Perler FB (2000) An alternative protein splicing mechanism for inteins lacking an N-terminal nucleo-phile. EMBO J 19:5019-5026
81. Srinivasa Babu K, Muthukumaran T, Antony A, Prem Singh Samuel SD, Balamurali M, Murugan V, Meenakshisundaram S (2009) Single step intein-mediated purification of hGMCSF expressed in salt-inducible E. coli. Biotechnol Lett 31:659-664
82. Starokadomskyy PL (2007) Protein splicing. Mol Biol (Mosk) 41:314-330
83. Sun W, Yang J, Liu XQ (2004) Synthetic two-piece and three-piece split inteins for protein trans-splicing. J Biol Chem 279:35281-35286
84. Sun P, Ye S, Ferrandon S, Evans TC, Xu MQ, Rao Z (2005) Crystal structures of an intein from the split dnaE gene of Synechocystis sp. PCC6803 reveal the catalytic model without the penultimate histidine and the mechanism of zinc Ion inhibition of protein splicing. J Mol Biol 353:1093-1105
85. Tavassoli A, Benkovic SJ (2007) Split-intein mediated circular ligation used in the synthesis of cyclic peptide libraries in E. coli. Nat Protoc 2:1126-1133
86. Tavassoli A, Naumann TA, Benkovic SJ (2005) Production of cyclic proteins and peptides. In: Belfort M, Derbyshire V, Stoddard BL, Wood DW (eds) Homing endonucleases and inteins, vol. 16. Springer, Berlin Heidelberg New York, pp. 293-305
87. Terpe K (2003) Overview of tag protein fusions: from molecular and biochemical fundamentals to commercial systems. Appl Microbiol Biotechnol 60:523-533
88. Thali M (1995) Cyclosporins: immunosuppressive drugs with anti-HIV-1 activity. Mol Med Today 1:287-291
89. Tori K, Dassa B, Johnson MA, Southworth MW, Brace LE, Ishino Y, Pietrokovski S, Perler FB (2010) Splicing of the mycobacteriophage Bethlehem DnaB intein: identification of a new mechanistic class of inteins that contain an obligate block F nucleophile. J Biol Chem 285:2515-2526
90. Turmel M, Brouard J-S, Gagnon C, Otis C, Lemieux C (2008) Deep division in the Chlorophyceae (Chlorophyta) revealed by chloroplast phylogenomic analyses. J Phycol 44:739-750
91. Van Roey P, Pereira B, Li Z, Hiraga K, Belfort M, Derbyshire V (2007) Crystallographic and mutational studies of Mycobacterium tuberculosis recA mini-inteins suggest a pivotal role for a highly conserved aspartate residue. J Mol Biol 367:162-173
92. Wang S, Liu XQ (1997) Identification of an unusual intein in chloroplast ClpP protease of Chlamydomonas eugametos. J Biol Chem 272:11869-11873
93. Waugh DS (2005) Making the most of affinity tags. Trends Biotechnol 23:316-320
94. Weber G, Schörgendorfer K, Schneider-Scherzer E, Leitner E (1994) The peptide synthetase catalyzing cyclosporine production in Tolypocladium niveum is encoded by a giant 45.8-kilobase open reading frame. Curr Genet 26:120-125
95. Wieczorek R, Pries A, Steinbüchel A, Mayer F (1995) Analysis of a 24-kilodalton protein associated with the polyhydroxyalka-noic acid granules in Alcaligenes eutrophus. J Bacteriol 177:2425-2435
96. Wood DW, Wu W, Belfort G, Derbyshire V, Belfort M (1999) A genetic system yields self-cleaving inteins for bioseparations. Nat Biotechnol 17:889-892
97. Wood DW, Harcum SW, Belfort G (2005) Industrial applications of intein technology. In: Belfort M, Derbyshire V, Stoddard BL, Wood DW (eds) Homing endonucleases and inteins, vol. 16. Springer, Berlin Heidelberg New York, pp. 345-364
98. Wu H, Hu Z, Liu XQ (1998) Protein trans-splicing by a split intein encoded in a split DnaE gene of Synechocystis sp. PCC6803. Proc Natl Acad Sci U S A 95:9226-9231
99. Wu WY, Mee C, Califano F, Banki R, Wood DW (2006) Recombinant protein purification by self-cleaving aggregation tag. Nat Protoc 1:2257-2262
100. Xu MQ, Evans TCJ (2001) Intein-mediated ligation and cyclization of expressed proteins. Methods 24:257-277
101. Zettler J, Schütz V, Mootz HD (2009) The naturally split Npu DnaE intein exhibits an extraordinarily high rate in the protein trans-splicing reaction. FEBS Lett 583:909-914
102. Zhao Z, Lu W, Dun B, Jin D, Ping S, Zhang W, Chen M, Xu MQ, Lin M (2008) Purification of green fluorescent protein using a two-intein system. Appl Microbiol Biotechnol 77:1175-1180
103. Züger S, Iwai H (2005) Intein-based biosynthetic incorporation of unlabeled protein tags into isotopically labeled proteins for NMR studies. Nat Biotechnol 23:736-740