Advertisement

Lactococcus lactis: Recent Developments in Functional Expression of Membrane Proteins

  • Sana Bakari
  • François André
  • Daphné Seigneurin-Berny
  • Marcel Delaforge
  • Norbert Rolland
  • Annie Frelet-BarrandEmail author
Chapter

Abstract

Membrane proteins (MPs) play key roles in most important cellular processes ranging from cell-to-cell communication to signaling processes. Despite recent improvements, the expression of functionally folded MPs in sufficient amounts for functional and structural characterization remains a challenge. Indeed, it is still difficult to predict whether a protein can be overproduced in a functional state in some expression system(s), although studies of high-throughput screens have been issued in recent years. Prokaryotic expression systems present several advantages over eukaryotic ones. Among them, Lactococcus lactis (L. lactis) has emerged in the past years as a good alternative expression system to Escherichia coli. The purpose of this chapter is to describe L. lactis and its tightly inducible system, nisin-controlled gene expression (NICE), for the expression of MPs from both prokaryotic and eukaryotic origins. Moreover, we will describe the functional characterization of some MPs produced in L. lactis.

Keywords

Cystic Fibrosis Transmembrane Conductance Regulator Lactococcus Lactis Expression Yield Chloroplast Envelope Nice System 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work has been supported by the Region Ile de France (DIM SeNt, PhD fellowship to SB AAP2010-3-10T6). We thank Edmund Kunji for his kind help and critical reading of the chapter.

References

  1. Avall-Jääskeläinen S, Kylä-Nikkilä K, Kahala M, Miikkulainen-Lahti T, Palva A (2002) Surface display of foreign epitopes on the Lactobacillus brevis S-layer. Appl Environ Microbiol 68:5943–5951PubMedCentralPubMedCrossRefGoogle Scholar
  2. Berlec A, Štrukelj B (2012) Generating a custom TA-cloning expression plasmid for Lactococcus lactis. Biotechniques 52:51–53PubMedCrossRefGoogle Scholar
  3. Bernaudat F, Frelet-Barrand A, Pochon N, Dementin S, Hivin P, Boutigny S, Rioux JB, Salvi D, Seigneurin-Berny D, Richaud P, Joyard J, Pignol D, Sabaty M, Desnos T, Pebay-Peyroula E, Darrouzet E, Vernet T, Rolland N (2011) Heterologous expression of membrane proteins: choosing the appropriate host. PLoS ONE 6:e29191PubMedCentralPubMedCrossRefGoogle Scholar
  4. Berntsson RP, Alia Oktaviani N, Fusetti F, Thunnissen AM, Poolman B, Slotboom DJ (2009) Selenomethionine incorporation in proteins expressed in Lactococcus lactis. Protein Sci 18:1121–1127PubMedCentralPubMedCrossRefGoogle Scholar
  5. Berntsson RP, ter Beek J, Majsnerowska M, Duurkens RH, Puri P, Poolman B, Slotboom DJ (2012) Structural divergence of paralogous S components from ECF-type ABC transporters. Proc Natl Acad Sci U S A 109:13990–13995PubMedCentralPubMedCrossRefGoogle Scholar
  6. Block MA, Douce R, Joyard J, Rolland N (2007) Chloroplast envelope membranes: a dynamic interface between plastids and the cytosol. Photosynth Res 92:225–244PubMedCentralPubMedCrossRefGoogle Scholar
  7. Catty P, Boutigny S, Miras R, Joyard J, Rolland N, Seigneurin-Berny D (2011) Biochemical characterization of AtHMA6/PAA1, a chloroplast envelope Cu(I)-ATPase. J Biol Chem 286:36188–36197PubMedCentralPubMedCrossRefGoogle Scholar
  8. Chen R (2012) Bacterial expression systems for recombinant protein production: E. coli and beyond. Biotechnol Adv 30:1102–1107PubMedCrossRefGoogle Scholar
  9. Delves-Broughton J, Blackburn P, Evans RJ, Hugenholtz J (1996) Applications of the bacteriocin, nisin. Antonie Van Leeuwenhoek 69:193–202PubMedCrossRefGoogle Scholar
  10. de Ruyter PG, Kuipers OP, Beerthuyzen MM, Alen-Boerrigter I, de Vos WM (1996a) Functional analysis of promoters in the nisin gene cluster of Lactococcus lactis. J Bacteriol 178:3434–3439Google Scholar
  11. de Ruyter PG, Kuipers OP, de Vos WM (1996b) Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 62:3662–3667Google Scholar
  12. de Vos WD (1987) Gene cloning and expression in lactic streptococci. FEMS Microbiol Lett 46:281–295CrossRefGoogle Scholar
  13. de Vos WM, Simons GFM (1994) Gene cloning and expression systems in Lactococci. In: Gasson MJ, de Vos WM (eds) Genetics and biotechnology of lactic acid bacteria’. Blackie Academic and Professional, LondonGoogle Scholar
  14. Doeven MK, van den Bogaart G, Krasnikov V, Poolman B (2008) Probing receptor-translocator interactions in the oligopeptide ABC transporter by fluorescence correlation spectroscopy. Biophys J 94:3956–3965PubMedCentralPubMedCrossRefGoogle Scholar
  15. Doshi R, Woebking B, van Veen HW (2010) Dissection of the conformational cycle of the multidrug/lipidA ABC exporter MsbA. Proteins 78:2867–2872PubMedCrossRefGoogle Scholar
  16. Doshi R, van Veen HW (2013) Substrate binding stabilizes a pre-translocation intermediate in the ATP-binding cassette transport protein MsbA. J Biol Chem 288:21638–21647PubMedCentralPubMedCrossRefGoogle Scholar
  17. Douillard FP, Mahony J, Campanacci V, Cambillau C, van Sinderen D (2011) Construction of two Lactococcus lactis expression vectors combining the Gateway and the NIsin controlled expression systems. Plasmid 66:129–135PubMedCrossRefGoogle Scholar
  18. Duurkens RH, Tol MB, Geertsma ER, Permentier HP, Slotboom DJ (2007) Flavin binding to the high affinity riboflavin transporter RibU. J Biol Chem 282:10380–10386PubMedCrossRefGoogle Scholar
  19. Eichenbaum Z, Federle MJ, Marra D, de Vos WM, Kuipers OP, Kleerebezem M, Scott JR (1998) Use of the lactococcal nisA promoter to regulate gene expression in gram-positive bacteria: comparison of induction level and promoter strength. Appl Environ Microbiol 64:2763–2769PubMedCentralPubMedGoogle Scholar
  20. Eren E, Kennedy DC, Maroney MJ, Argüello JM (2006) A novel regulatory metal binding domain is present in the C terminus of Arabidopsis Zn2+-ATPase HMA2. J Biol Chem 281:33881–33891PubMedCrossRefGoogle Scholar
  21. Erkens GB, Slotboom DJ (2010) Biochemical characterization of ThiT from Lactococcus lactis: a thiamin transporter with picomolar substrate binding affinity. Biochemistry 49:3203–3212PubMedCrossRefGoogle Scholar
  22. Erkens GB, Berntsson RP, Fulyani F, Majsnerowska M, Vujičić-Žagar A, Ter Beek J, Poolman B, Slotboom DJ (2011) The structural basis of modularity in ECF-type ABC transporters. Nat Struct Mol Biol 18:755–760PubMedCrossRefGoogle Scholar
  23. Eshaghi S, Hedrén M, Nasser MI, Hammarberg T, Thornell A, Nordlund P (2005) An efficient strategy for high-throughput expression screening of recombinant integral membrane proteins. Protein Sci 14:676–683PubMedCentralPubMedCrossRefGoogle Scholar
  24. Filipic B, Golic N, Jovcic B, Tolinacki M, Bay DC, Turner RJ, Antic-Stankovic J, Kojic M, Topisirovic L (2013) The cmbT gene encodes a novel major facilitator multidrug resistance transporter in Lactococcus lactis. Res Microbiol 164:46–54PubMedCrossRefGoogle Scholar
  25. Folgering JH, Moe PC, Schuurman-Wolters GK, Blount P, Poolman B (2005) Lactococcus lactis uses MscL as its principal mechanosensitive channel. J Biol Chem 280:8784–8792PubMedCrossRefGoogle Scholar
  26. Freigassner M, Pichler H, Glieder A (2009) Tuning microbial hosts for membrane protein production. Microb Cell Fact 8:69PubMedCentralPubMedCrossRefGoogle Scholar
  27. Frelet-Barrand A, Boutigny S, Kunji ER, Rolland N (2010a) Membrane protein expression in Lactococcus lactis. Method Mol Biol 601:67–85CrossRefGoogle Scholar
  28. Frelet-Barrand A, Boutigny S, Moyet L, Deniaud A, Seigneurin-Berny D, Salvi D, Bernaudat F, Richaud P, Pebay-Peyroula E, Joyard J, Rolland N (2010b) Lactococcus lactis, an alternative system for functional expression of peripheral and intrinsic Arabidopsis membrane proteins. PLoS ONE 5:e8746CrossRefGoogle Scholar
  29. Gasson MJ (1983) Genetic transfer systems in lactic acid bacteria. Antonie Van Leeuwenhoek 49:275–282PubMedCrossRefGoogle Scholar
  30. Gasson MJ, de Vos WM (1994) Genetics and biotechnology of lactic acid bacteria. Blackie, LondonGoogle Scholar
  31. Geertsma ER, Poolman B (2007) High-throughput cloning and expression in recalcitrant bacteria. Nat Method 4:705–707CrossRefGoogle Scholar
  32. Gordon E, Horsefield R, Swarts HG, de Pont JJ, Neutze R, Snijder A (2008) Effective high-throughput overproduction of membrane proteins in Escherichia coli. Protein Expr Purif 62:1–8PubMedCrossRefGoogle Scholar
  33. Grisshammer R, Tate CG (1995) Overexpression of integral membrane proteins for structural studies. Q Rev Biophys 28:315–422PubMedCrossRefGoogle Scholar
  34. Groeneveld M, Weme RG, Duurkens RH, Slotboom DJ (2010) Biochemical characterization of the C4-dicarboxylate transporter DctA from Bacillus subtilis. J Bacteriol 192:2900–2907PubMedCentralPubMedCrossRefGoogle Scholar
  35. Halestrap AP (1978) Stimulation of pyruvate transport in metabolizing mitochondria through changes in the transmembrane pH gradient induced by glucagon treatment of rats. Biochem J 172:389–398PubMedCentralPubMedGoogle Scholar
  36. Hartley JL, Temple GF, Brasch MA (2000) DNA cloning using in vitro site-specific recombination. Genome Res 10(11):1788–1795Google Scholar
  37. Hasper HE, de Kruijff B, Breukink E (2004) Assembly and stability of nisin-lipid II pores. Biochemistry 43:11567–11575PubMedCrossRefGoogle Scholar
  38. Hellmich UA, Lyubenova S, Kaltenborn E, Doshi R, van Veen HW, Prisner TF, Glaubitz C (2012) Probing the ATP hydrolysis cycle of the ABC multidrug transporter LmrA by pulsed EPR spectroscopy. J Am Chem Soc 134:5857–5862PubMedCrossRefGoogle Scholar
  39. Herzig S, Raemy E, Montessuit S, Veuthey JL, Zamboni N, Westermann B, Kunji ER, Martinou JC (2012) Identification and functional expression of the mitochondrial pyruvate carrier. Science 337:93–96PubMedCrossRefGoogle Scholar
  40. Hofacker M, Gompf S, Zutz A, Presenti C, Haase W, van der Does C, Model K, Tampé R (2007) Structural and functional fingerprint of the mitochondrial ATP-binding cassette transporter Mdl1 from Saccharomyces cerevisiae. J Biol Chem 282:3951–3961PubMedCrossRefGoogle Scholar
  41. Hohl M, Briand C, Grütter MG, Seeger MA (2012) Crystal structure of a heterodimeric ABC transporter in its inward-facing conformation. Nat Struct Mol Biol 19:395–402PubMedCrossRefGoogle Scholar
  42. Hugenholtz J, Sybesma W, Groot MN, Wisselink W, Ladero V, Burgess K, van Sinderen D, Piard JC, Eggink G, Smid EJ, Savoy G, Sesma F, Jansen T, Hols P, Kleerebezem M (2002) Metabolic engineering of lactic acid bacteria for the production of nutraceuticals. Antonie Van Leeuwenhoek 82:217–235PubMedCrossRefGoogle Scholar
  43. Ingram LO (1977) Changes in lipid composition of Escherichia coli resulting from growth with organic solvents and with food additives. Appl Environ Microbiol 33:1233–1236PubMedCentralPubMedGoogle Scholar
  44. Janvilisri T, Venter H, Shahi S, Reuter G, Balakrishnan L, van Veen HW (2003) Sterol transport by the human breast cancer resistance protein (ABCG2) expressed in Lactococcus lactis. J Biol Chem 278:20645–20651PubMedCrossRefGoogle Scholar
  45. Junge F, Schneider B, Reckel S, Schwarz D, Dötsch V, Bernhard F (2008) Large-scale production of functional membrane proteins. Cell Mol Life Sci 65:1729–1755PubMedCrossRefGoogle Scholar
  46. Kleerebezem M, Beerthuyzen MM, Vaughan EE, de Vos WM, Kuipers OP (1997) Controlled gene expression systems for lactic acid bacteria: transferable nisin-inducible expression cassettes for Lactococcus, Leuconostoc, and Lactobacillus spp. Appl Environ Microbiol 63:4581–4584PubMedCentralPubMedGoogle Scholar
  47. Kok J, van der Vossen JM, Venema G (1984) Construction of plasmid cloning vectors for lactic streptococci which also replicate in Bacillus subtilis and Escherichia coli. Appl Environ Microbiol 48:726–731PubMedCentralPubMedGoogle Scholar
  48. Kühlbrandt W (2004) Biology, structure and mechanism of P-type ATPases. Nat Rev Mol Cell Biol 5:282–295PubMedCrossRefGoogle Scholar
  49. Kuipers OP, Beerthuyzen MM, Siezen RJ, de Vos WM (1993) Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis. Requirement of expression of the nisA and nisI genes for development of immunity. Eur J Biochem 216:281–291PubMedCrossRefGoogle Scholar
  50. Kuipers OP, de Ruyter PGGA, Kleerebezem M, de Vos WM (1998) Quorum sensing-controlled gene expression in lactic acid bacteria. J Biotechnol 64:15–21CrossRefGoogle Scholar
  51. Kunji ERS, Slotboom DJ, Poolman B (2003) Lactococcus lactis as host for overproduction of functional membrane proteins. Biochim Biophys Acta 1610:97–108PubMedCrossRefGoogle Scholar
  52. Kunji ERS, Chan KW, Slotboom DJ, Floyd S, O’Connor R, Monné M (2005) Eukaryotic membrane protein overproduction in Lactococcus lactis. Curr Opin Biotechnol 16:546–551PubMedCrossRefGoogle Scholar
  53. Lacapere JJ, Pebay-Peyroula E, Neumann JM, Etchebest C (2007) Determining membrane protein structures: still a challenge. Trends Biochem Sci 32:259–270PubMedCrossRefGoogle Scholar
  54. Linares DM, Geertsma ER, Poolman B (2010) Evolved Lactococcus lactis strains for enhanced expression of recombinant membrane proteins. J Mol Biol 401:45–55PubMedCrossRefGoogle Scholar
  55. Lubelski J, de Jong A, van Merkerk R, Agustiandari H, Kuipers OP, Kok J, Driessen AJ (2006) LmrCD is a major multidrug resistance transporter in Lactococcus lactis. Mol Microbiol 61:771–781PubMedCrossRefGoogle Scholar
  56. Lubelski J, Konings WN, Driessen AJ (2007) Distribution and physiology of ABC-type transporters contributing to multidrug resistance in bacteria. Microbiol Mol Biol Rev 71:463–476PubMedCentralPubMedCrossRefGoogle Scholar
  57. Lubelski J, Rink R, Khusainov R, Moll GN, Kuipers OP (2008) Biosynthesis, immunity, regulation, mode of action and engineering of the model lantibiotic nisin. Cell Mol Life Sci 65:455–476PubMedCrossRefGoogle Scholar
  58. Lundstrom K (2007) Structural genomics and drug discovery. J Cell Mol Med 11:224–238PubMedCrossRefGoogle Scholar
  59. Majsnerowska M, Hänelt I, Wunnicke D, Schäfer LV, Steinhoff HJ, Slotboom DJ (2013) Substrate-induced conformational changes in the S-component ThiT from an energy coupling factor transporter. Structure 21:861–867PubMedCrossRefGoogle Scholar
  60. Margolles A, Flórez AB, Moreno JA, van Sinderen D, de los Reyes-Gavilán CG (2006) Two membrane proteins from Bifidobacterium breve UCC2003 constitute an ABC-type multidrug transporter. Microbiology 152:3497–3505PubMedCrossRefGoogle Scholar
  61. Marreddy RK, Geertsma ER, Permentier HP, Pinto JP, Kok J, Poolman B (2010) Amino acid accumulation limits the overexpression of proteins in Lactococcus lactis. PLoS ONE 5:e10317PubMedCentralPubMedCrossRefGoogle Scholar
  62. Marreddy RKR, Geertsma ER, Poolman B (2011a) Recombinant membrane protein production: past, present and future. In: Brnjas-Kraljević J, Pifat-Mrzljak G (eds) Supramolecular structure and function 10. Springer, HeidelbergGoogle Scholar
  63. Marreddy RK, Pinto JP, Wolters JC, Geertsma ER, Fusetti F, Permentier HP, Kuipers OP, Kok J, Poolman B (2011b) The response of Lactococcus lactis to membrane protein production. PLoS ONE 6:e24060CrossRefGoogle Scholar
  64. Midgett CR, Madden DR (2007) Breaking the bottleneck: eukaryotic membrane protein expression for high-resolution structural studies. J Struct Biol 160:265–274PubMedCrossRefGoogle Scholar
  65. Mierau I, Kleerebezem M (2005) 10 years of the nisin-controlled gene expression system (NICE) in Lactococcus lactis. Appl Microbiol Biotechnol 68:705–717PubMedCrossRefGoogle Scholar
  66. Mierau I, Olieman K, Mond J, Smid EJ (2005) Optimization of the Lactococcus lactis nisin-controlled gene expression system NICE for industrial applications. Microb Cell Fact 4:16PubMedCentralPubMedCrossRefGoogle Scholar
  67. Mifsud J, Ravaud S, Krammer EM, Chipot C, Kunji ER, Pebay-Peyroula E, Dehez F (2013) The substrate specificity of the human ADP/ATP carrier AAC1. Mol Membr Biol 30:160–168PubMedCrossRefGoogle Scholar
  68. Miras S, Salvi D, Ferro M, Grunwald D, Garin J, Joyard J, Rolland N (2002) Non-canonical transit peptide for import into the chloroplast. J Biol Chem 277:47770–47778PubMedCrossRefGoogle Scholar
  69. Monné M, Chan KW, Slotboom DJ, Kunji ERS (2005) Functional expression of eukaryotic membrane proteins in Lactococcus lactis. Protein Sci 14:3048–3056PubMedCentralPubMedCrossRefGoogle Scholar
  70. Monné M, Robinson AJ, Boes C, Harbour ME, Fearnley IM, Kunji ER (2007) The mimivirus genome encodes a mitochondrial carrier that transports dATP and dTTP. J Virol 81:3181–3186PubMedCentralPubMedCrossRefGoogle Scholar
  71. Morello E, Bermúdez-Humarán LG, Llull D, Solé V, Miraglio N, Langella P, Poquet I (2008) Lactococcus lactis, an efficient cell factory for recombinant protein production and secretion. J Mol Microbiol Biotechnol 14:48–58PubMedCrossRefGoogle Scholar
  72. Mu D, Montalbán-López M, Masuda Y, Kuipers OP (2013) Zirex: a novel zinc-regulated expression system for Lactococcus lactis. Appl Environ Microbiol 79:4503–4508PubMedCentralPubMedCrossRefGoogle Scholar
  73. Neuhaus HE, Thom E, Möhlmann T, Steup M, Kampfenkel K (1997) Characterization of a novel eukaryotic ATP/ADP translocator located in the plastid envelope of Arabidopsis thaliana L. Plant J 11:73–82PubMedCrossRefGoogle Scholar
  74. Noreen N, Hooi WY, Baradaran A, Rosfarizan M, Sieo CC, Rosli MI, Yusoff K, Raha AR (2011) Lactococcus lactis M4, a potential host for the expression of heterologous proteins. Microb Cell Fact 10:28PubMedCentralPubMedCrossRefGoogle Scholar
  75. Oliveira AP, Nielsen J, Förster J (2005) Modelling Lactococcus lactis using a genome-scale flux model. BMC Microbiol 5:39PubMedCentralPubMedCrossRefGoogle Scholar
  76. Opekarova M, Tanner W (2003) Specific lipid requirements of membrane proteins—a putative bottleneck in heterologous expression. Biochim Biophys Acta 1610:11–22PubMedCrossRefGoogle Scholar
  77. Pavan S, Hols P, Delcour J, Geoffroy MC, Grangette C, Kleerebezem M, Mercenier A (2000) Adaptation of the nisin-controlled expression system in Lactobacillus plantarum: a tool to study in vivo biological effects. Appl Environ Microbiol 66:4427–4432PubMedCentralPubMedCrossRefGoogle Scholar
  78. Pinto JP, Kuipers OP, Marreddy RK, Poolman B, Kok J (2011) Efficient overproduction of membrane proteins in Lactococcus lactis requires the cell envelope stress sensor/regulator couple CesSR. PLoS ONE 6(7):e21873PubMedCentralPubMedCrossRefGoogle Scholar
  79. Pontes DS, de Azevedo MS, Chatel JM, Langella P, Azevedo V, Miyoshi A (2011) Lactococcus lactis as a live vector: heterologous protein production and DNA delivery systems. Protein Expr Purif 79:165–175PubMedCrossRefGoogle Scholar
  80. Pudlik AM, Lolkema JS (2012) Rerouting citrate metabolism in Lactococcus lactis to citrate-driven transamination. Appl Environ Microbiol 78:6665–6673PubMedCentralPubMedCrossRefGoogle Scholar
  81. Quick M, Javitch JA (2007) Monitoring the function of membrane transport proteins in detergent-solubilized form. Proc Natl Acad Sci U S A 104:3603–3608PubMedCentralPubMedCrossRefGoogle Scholar
  82. Sakamoto K, Margolles A, van Veen HW, Konings WN (2001) Hop resistance in the beer spoilage bacterium Lactobacillus brevis is mediated by the ATP-binding cassette multidrug transporter HorA. J Bacteriol 183:5371–5375PubMedCentralPubMedCrossRefGoogle Scholar
  83. Schaedler TA, Tong Z, van Veen HW (2012) The multidrug transporter LmrP protein mediates selective calcium efflux. J Biol Chem 287:27682–27690PubMedCentralPubMedCrossRefGoogle Scholar
  84. Schlegel S, Klepsch M, Gialama D, Wickström D, Slotboom DJ, de Gier JW (2010) Revolutionizing membrane protein overexpression in bacteria. Microb Biotechnol 3:403–411PubMedCentralPubMedCrossRefGoogle Scholar
  85. Schleifer KH, Kraus J, Dvorak C, Kilpper-Bälz R, Collins MD, Fischer W (1985) Transfer of Streptococcus lactis and related streptococci to the genus Lactococcus gen. nov. Syst Appl Microbiol 6:183–195CrossRefGoogle Scholar
  86. Schuurman-Wolters GK, Poolman B (2005) Substrate specificity and ionic regulation of GlnPQ from Lactococcus lactis. An ATP-binding cassette transporter with four extracytoplasmic substrate-binding domains. J Biol Chem 280:23785–23790PubMedCrossRefGoogle Scholar
  87. Seeger MA, Mittal A, Velamakanni S, Hohl M, Schauer S, Salaa I, Grütter MG, van Veen HW (2012) Tuning the drug efflux activity of an ABC transporter in vivo by in vitro selected DARPin binders. PLoS ONE 7:e37845PubMedCentralPubMedCrossRefGoogle Scholar
  88. Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, Finazzi G, Grunwald D, Rappaport F, Vavasseur A, Joyard J, Richaud P, Rolland N (2006) HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J Biol Chem 281:2882–2892PubMedCrossRefGoogle Scholar
  89. Shilling R, Federici L, Walas F, Venter H, Velamakanni S, Woebking B, Balakrishnan L, Luisi B, van Veen HW (2005) A critical role of a carboxylate in proton conduction by the ATP-binding cassette multidrug transporter LmrA. FASEB J 19:1698–1700PubMedGoogle Scholar
  90. Steen A, Wiederhold E, Gandhi T, Breitling R, Slotboom DJ (2011) Physiological adaptation of the bacterium Lactococcus lactis in response to the production of human CFTR. Mol Cell Proteomics 10:M000052MCP200Google Scholar
  91. Surade S, Klein M, Stolt-Bergner PC, Muenke C, Roy A, Michel H (2006) Comparative analysis and “expression space” coverage of the production of prokaryotic membrane proteins for structural genomics. Protein Sci 15:2178–2189PubMedCentralPubMedCrossRefGoogle Scholar
  92. Ter Horst R, Lolkema JS (2010) Rapid screening of membrane topology of secondary transport proteins. Biochim Biophys Acta 1798:672–680Google Scholar
  93. Trip H, Mulder NL, Lolkema JS (2013) Cloning, expression, and functional characterization of secondary amino acid transporters of Lactococcus lactis. J Bacteriol 195:340–350PubMedCentralPubMedCrossRefGoogle Scholar
  94. Tjaden J, Schwöppe C, Möhlmann T, Quick PW, Neuhaus HE (1998) Expression of a plastidic ATP/ADP transporter gene in Escherichia coli leads to a functional adenine nucleotide transport system in the bacterial cytoplasmic membrane. J Biol Chem 273:9630–9636PubMedCrossRefGoogle Scholar
  95. Velamakanni S, Yao Y, Gutmann DA, van Veen HW (2008) Multidrug transport by the ABC transporter Sav1866 from Staphylococcus aureus. Biochemistry 47:9300–9308PubMedCrossRefGoogle Scholar
  96. Venter H, Shilling RA, Velamakanni S, Balakrishnan L, Van Veen HW (2003) An ABC transporter with a secondary-active multidrug translocator domain. Nature 426:866–870PubMedCrossRefGoogle Scholar
  97. Vest KE, Leary SC, Winge DR, Cobine PA (2013) Copper import into the mitochondrial matrix in Saccharomyces cerevisiae is mediated by Pic2, a mitochondrial carrier family protein. J Biol Chem 288(33):23884–23892, Accessed 11 July 2013Google Scholar
  98. Wallin E, von Heijne G (1998) Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 7:1029–1038PubMedCentralPubMedCrossRefGoogle Scholar
  99. Wegmann U, O’Connell-Motherway M, Zomer A, Buist G, Shearman C, Canchaya C, Ventura M, Goesmann A, Gasson MJ, Kuipers OP, van Sinderen D, Kok J (2007) Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J Bacteriol 189:3256–3270PubMedCentralPubMedCrossRefGoogle Scholar
  100. Woebking B, Reuter G, Shilling RA, Velamakanni S, Shahi S, Venter H, Balakrishnan L, van Veen HW (2005) Drug-lipid A interactions on the Escherichia coli ABC transporter MsbA. J Bacteriol 187:6363–6369PubMedCentralPubMedCrossRefGoogle Scholar
  101. Woebking B, Velamakanni S, Federici L, Seeger MA, Murakami S, van Veen HW (2008) Functional role of transmembrane helix 6 in drug binding and transport by the ABC transporter MsbA. Biochemistry 47:10904–10914PubMedCrossRefGoogle Scholar
  102. Yashiroda Y, Matsuyama A, Yoshida M (2008) New insights into chemical biology from ORFeome libraries. Curr Opin Chem Biol 12:55–59PubMedCrossRefGoogle Scholar
  103. Zhou XX, Li WF, Ma GX, Pan YJ (2006) The nisin-controlled gene expression system: construction, application and improvements. Biotechnol Adv 24:285–295PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Sana Bakari
    • 1
  • François André
    • 1
  • Daphné Seigneurin-Berny
    • 2
  • Marcel Delaforge
    • 1
  • Norbert Rolland
    • 2
  • Annie Frelet-Barrand
    • 1
    Email author
  1. 1.Oxidative Stress and Detoxification Laboratory, UMR-CNRS 8221Institute of Biology and Technology of Saclay, SB2SM, and Centre for Nuclear Studies and Université Paris-SudsGif-sur-YvetteFrance
  2. 2.Cell & Plant Physiology Laboratory, Institute of Sciences Research and Technologies, UMR-CNRS 5168National Institute of Agronomical Research, Centre for Nuclear Studies, Université Grenoble AlpesGrenobleFrance

Personalised recommendations