Using Haloarcula marismortui Bacteriorhodopsin as a Fusion Tag for Enhancing and Visible Expression of Integral Membrane Proteins in Escherichia coli

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Hsu, Min Feng ^a,b   Yu, Tsung Fu ^a,c   Chou, Chia Cheng ^a,b   Fu, Hsu Yuan ^d   Yang, Chii Shen ^d   Wang, Andrew H J ^a,b,d  

^a INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^b ACADEMIA SINICA   (Taiwan)

^c NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPORTER; ASPARAGINE; ASPARTIC ACID; BACTERIORHODOPSIN; CARNITINE BUTYROBETAINE ANTIPORTER; HISTIDINE; HYBRID PROTEIN; MEMBRANE PROTEIN; PROTEINASE; UNCLASSIFIED DRUG; UNDECAPRENYL PYROPHOSPHATE PHOSPHATASE ANTIPORTER;

ARTICLE; ESCHERICHIA COLI; GENE EXPRESSION SYSTEM; HALOARCULA MARISMORTUI; HIGH THROUGHPUT SCREENING; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN TARGETING;

AMINO ACID SEQUENCE; BACTERIORHODOPSINS; ESCHERICHIA COLI; GENE EXPRESSION; GENETIC ENGINEERING; HALOARCULA MARISMORTUI; HISTIDINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; ORGANIC CATION TRANSPORT PROTEINS; PROTEIN STRUCTURE, SECONDARY; PROTEOLYSIS; PYROPHOSPHATASES; RECOMBINANT FUSION PROTEINS;

EID: 84874053298     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056363     Document Type: Article

References (41)

1. Douglas SM, Chou JJ, Shih WM, (2007) DNA-nanotube-induced alignment of membrane proteins for NMR structure determination. Proc Natl Acad Sci U S A 104: 6644-6648.
2. Lundstrom K, (2004) Structural genomics on membrane proteins: the MePNet approach. Curr Opin Drug Discov Devel 7: 342-346.
3. Katzen F, Peterson TC, Kudlicki W, (2009) Membrane protein expression: no cells required. Trends Biotechnol 27: 455-460.
4. White SH, (2009) Biophysical dissection of membrane proteins. Nature 459: 344-346.
5. Esposito D, Chatterjee DK, (2006) Enhancement of soluble protein expression through the use of fusion tags. Curr Opin Biotechnol 17: 353-358.
6. Shih YP, Kung WM, Chen JC, Yeh CH, Wang AH, et al. (2002) High-throughput screening of soluble recombinant proteins. Protein Sci 11: 1714-1719.
7. Finn RD, Kapelioukh I, Paine MJ (2005) Rainbow tags: a visual tag system for recombinant protein expression and purification. Biotechniques 38: 387-388, 390-382.
8. Wagner S, Bader ML, Drew D, de Gier JW, (2006) Rationalizing membrane protein overexpression. Trends Biotechnol 24: 364-371.
9. Roosild TP, Greenwald J, Vega M, Castronovo S, Riek R, et al. (2005) NMR structure of Mistic, a membrane-integrating protein for membrane protein expression. Science 307: 1317-1321.
10. Neophytou I, Harvey R, Lawrence J, Marsh P, Panaretou B, et al. (2007) Eukaryotic integral membrane protein expression utilizing the Escherichia coli glycerol-conducting channel protein (GlpF). Appl Microbiol Biotechnol 77: 375-381.
11. Manley DM, McComb ME, Perreault H, Donald LJ, Duckworth HW, et al. (2000) Secondary structure and oligomerization of the E. coli glycerol facilitator. Biochemistry 39: 12303-12311.
12. Drew D, Lerch M, Kunji E, Slotboom DJ, de Gier JW, (2006) Optimization of membrane protein overexpression and purification using GFP fusions. Nat Methods 3: 303-313.
13. Chun E, Thompson AA, Liu W, Roth CB, Griffith MT, et al. (2012) Fusion partner toolchest for the stabilization and crystallization of G protein-coupled receptors. Structure 20: 967-976.
14. Ng WV, Kennedy SP, Mahairas GG, Berquist B, Pan M, et al. (2000) Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci U S A 97: 12176-12181.
15. Baliga NS, Bonneau R, Facciotti MT, Pan M, Glusman G, et al. (2004) Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. Genome Res 14: 2221-2234.
16. Bolhuis H, Palm P, Wende A, Falb M, Rampp M, et al. (2006) The genome of the square archaeon Haloquadratum walsbyi: life at the limits of water activity. BMC Genomics 7: 169.
17. Falb M, Pfeiffer F, Palm P, Rodewald K, Hickmann V, et al. (2005) Living with two extremes: conclusions from the genome sequence of Natronomonas pharaonis. Genome Res 15: 1336-1343.
18. Falb M, Muller K, Konigsmaier L, Oberwinkler T, Horn P, et al. (2008) Metabolism of halophilic archaea. Extremophiles 12: 177-196.
19. Pebay-Peyroula E, Rummel G, Rosenbusch JP, Landau EM, (1997) X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science 277: 1676-1681.
20. Belrhali H, Nollert P, Royant A, Menzel C, Rosenbusch JP, et al. (1999) Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 A resolution. Structure 7: 909-917.
21. Daggett V, Fersht AR, (2009) Protein folding and binding: moving into unchartered territory. Curr Opin Struct Biol 19: 1-2.
22. Mogi T, Stern LJ, Marti T, Chao BH, Khorana HG, (1988) Aspartic acid substitutions affect proton translocation by bacteriorhodopsin. Proc Natl Acad Sci U S A 85: 4148-4152.
23. Otto H, Marti T, Holz M, Mogi T, Lindau M, et al. (1989) Aspartic acid-96 is the internal proton donor in the reprotonation of the Schiff base of bacteriorhodopsin. Proc Natl Acad Sci U S A 86: 9228-9232.
24. Fu HY, Lin YC, Chang YN, Tseng H, Huang CC, et al. (2010) A novel six-rhodopsin system in a single archaeon. J Bacteriol 192: 5866-5873.
25. Lu T, Li BF, Jaiang L, Rothe U, Bakowsky U, (1998) Temperature and pH-dependent inversion of photoelectric response in bacteriorhodopsin. J Chem Soc Faraday trans 94: 79-81.
26. Yokoyama Y, Sonoyama M, Nakano T, Mitaku S, (2007) Structural change of bacteriorhodopsin in the purple membrane above pH 10 decreases heterogeneity of the irreversible photobleaching components. J Biochem 142: 325-333.
27. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK, (1999) Structural changes in bacteriorhodopsin during ion transport at 2 angstrom resolution. Science 286: 255-261.
28. Kapust RB, Tozser J, Fox JD, Anderson DE, Cherry S, et al. (2001) Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency. Protein Eng 14: 993-1000.
29. Miroux B, Walker J, (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 260: 289-298.
30. Yokoyama Y, Sonoyama M, Mitaku S, (2002) Irreversible photobleaching of bacteriorhodopsin in a high-temperature intermediate state. J Biochem 131: 785-790.
31. El Ghachi M, Bouhss A, Blanot D, Mengin-Lecreulx D, (2004) The bacA gene of Escherichia coli encodes an undecaprenyl pyrophosphate phosphatase activity. J Biol Chem 279: 30106-30113.
32. Vinothkumar KR, Raunser S, Jung H, Kuhlbrandt W, (2006) Oligomeric structure of the carnitine transporter CaiT from Escherichia coli. J Biol Chem 281: 4795-4801.
33. Touze T, Blanot D, Mengin-Lecreulx D, (2008) Substrate specificity and membrane topology of Escherichia coli PgpB, an undecaprenyl pyrophosphate phosphatase. J Biol Chem 283: 16573-16583.
34. Jung H, Buchholz M, Clausen J, Nietschke M, Revermann A, et al. (2002) CaiT of Escherichia coli, a new transporter catalyzing L-carnitine/gamma-butyrobetaine exchange. J Biol Chem 277: 39251-39258.
35. Drew DE, von Heijne G, Nordlund P, de Gier JW, (2001) Green fluorescent protein as an indicator to monitor membrane protein overexpression in Escherichia coli. FEBS Lett 507: 220-224.
36. Braiman MS, Stern LJ, Chao BH, Khorana HG, (1987) Structure-function studies on bacteriorhodopsin. IV. Purification and renaturation of bacterio-opsin polypeptide expressed in Escherichia coli. J Biol Chem 262: 9271-9276.
37. Dunn RJ, Hackett NR, McCoy JM, Chao BH, Kimura K, et al. (1987) Structure-function studies on bacteriorhodopsin. I. Expression of the bacterio-opsin gene in Escherichia coli. J Biol Chem 262: 9246-9254.
38. Schmies G, Chizhov I, Engelhard M, (2000) Functional expression of His-tagged sensory rhodopsin I in Escherichia coli. FEBS Lett 466: 67-69.
39. Tang L, Bai L, Wang WH, Jiang T, (2010) Crystal structure of the carnitine transporter and insights into the antiport mechanism. Nat Struct Mol Biol 17: 492-496.
40. Otwinowski Z, Minor W, (1997) Processing of X-ray diffraction data collected in oscillation mode. Macromolecular Crystallography, Pt A 276: 307-326.
41. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.