The response of lactococcus lactis to membrane protein production

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Marreddy, Ravi K R ^a   Pinto, Joao P C ^b   Wolters, Justina C ^a   Geertsma, Eric R ^a,c   Fusetti, Fabrizia ^a   Permentier, Hjalmar P ^a   Kuipers, Oscar P ^b   Kok, Jan ^b   Poolman, Bert ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; MEMBRANE PROTEIN; MESSENGER RNA; PROTEINASE; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BIOENGINEERING; CELLULAR STRESS RESPONSE; CESSR SYSTEM; CONTROLLED STUDY; LACTOCOCCUS LACTIS; METABOLIC REGULATION; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SYNTHESIS; PROTEOMICS; TRANSCRIPTOMICS; UPREGULATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

LACTOCOCCUS LACTIS;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; LACTOCOCCUS LACTIS; MEMBRANE PROTEINS;

EID: 80052341041     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024060     Document Type: Article

References (68)

1. Hopkins AL, Groom CR, (2002) The druggable genome. Nat Rev Drug Discov 1: 727-730.
2. Wallin E, von Heijne G, (1998) Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 7: 1029-1038.
3. Grisshammer R, Tate CG, (1995) Overexpression of integral membrane proteins for structural studies. Q Rev Biophys 28: 315-422.
4. Junge F, Schneider B, Reckel S, Schwarz D, Dotsch V, et al. (2008) Large-scale production of functional membrane proteins. Cell Mol Life Sci 65: 1729-1755.
5. Katzen F, Peterson TC, Kudlicki W, (2009) Membrane protein expression: no cells required. Trends Biotechnol 27: 455-460.
6. Mierau I, Kleerebezem M, (2005) 10 years of the nisin-controlled gene expression system (NICE) in Lactococcus lactis. Appl Microbiol Biotechnol 68: 705-717.
7. Surade S, Klein M, Stolt-Bergner PC, Muenke C, Roy A, et al. (2006) Comparative analysis and "expression space" coverage of the production of prokaryotic membrane proteins for structural genomics. Protein Sci 15: 2178-2189.
8. Quick M, Javitch JA, (2007) Monitoring the function of membrane transport proteins in detergent-solubilized form. Proc Natl Acad Sci U S A 104: 3603-3608.
9. Morello E, Bermudez-Humaran LG, Llull D, Sole V, Miraglio N, et al. (2008) Lactococcus lactis, an efficient cell factory for recombinant protein production and secretion. J Mol Microbiol Biotechnol 14: 48-58.
10. Mulligan C, Geertsma ER, Severi E, Kelly DJ, Poolman B, et al. (2009) The substrate-binding protein imposes directionality on an electrochemical sodium gradient-driven TRAP transporter. Proc Natl Acad Sci U S A 106: 1778-1783.
11. Geertsma ER, Poolman B, (2007) High-throughput cloning and expression in recalcitrant bacteria. Nat Methods 4: 705-707.
12. Kunji ER, Slotboom DJ, Poolman B, (2003) Lactococcus lactis as host for overproduction of functional membrane proteins. Biochim Biophys Acta 1610: 97-108.
13. de Ruyter PG, Kuipers OP, de Vos WM, (1996) Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 62: 3662-3667.
14. Llull D, Poquet I, (2004) New expression system tightly controlled by zinc availability in Lactococcus lactis. Appl Environ Microbiol 70: 5398-5406.
15. Monne M, Chan KW, Slotboom DJ, Kunji ER, (2005) Functional expression of eukaryotic membrane proteins in Lactococcus lactis. Protein Sci 14: 3048-3056.
16. Geertsma ER, Groeneveld M, Slotboom DJ, Poolman B, (2008) Quality control of overexpressed membrane proteins. Proc Natl Acad Sci U S A 105: 5722-5727.
17. Marreddy RK, Geertsma ER, Permentier HP, Pinto JP, Kok J, et al. (2010) Amino acid accumulation limits the overexpression of proteins in Lactococcus lactis. PLoS ONE 5: e10317.
18. Locher KP, Lee AT, Rees DC, (2002) The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296: 1091-1098.
19. Lewinson O, Lee AT, Rees DC, (2008) The funnel approach to the precrystallization production of membrane proteins. J Mol Biol 377: 62-73.
20. Miroux B, Walker JE, (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.
21. Massey-Gendel E, Zhao A, Boulting G, Kim HY, Balamotis MA, et al. (2009) Genetic selection system for improving recombinant membrane protein expression in E. coli. Protein Sci 18: 372-383.
22. Linares DM, Geertsma ER, Poolman B, (2010) Evolved Lactococcus lactis strains for enhanced expression of recombinant membrane proteins. J Mol Biol 401: 45-55.
23. Serrano-Vega MJ, Magnani F, Shibata Y, Tate CG, (2008) Conformational thermostabilization of the beta1-adrenergic receptor in a detergent-resistant form. Proc Natl Acad Sci U S A 105: 877-882.
24. Bonander N, Hedfalk K, Larsson C, Mostad P, Chang C, et al. (2005) Design of improved membrane protein production experiments: quantitation of the host response. Protein Sci 14: 1729-1740.
25. Wagner S, Baars L, Ytterberg AJ, Klussmeier A, Wagner CS, et al. (2007) Consequences of membrane protein overexpression in Escherichia coli. Mol Cell Proteomics 6: 1527-1550.
26. Wagner S, Klepsch MM, Schlegel S, Appel A, Draheim R, et al. (2008) Tuning Escherichia coli for membrane protein overexpression. Proc Natl Acad Sci U S A 105: 14371-14376.
27. Bonander N, Darby RA, Grgic L, Bora N, Wen J, et al. (2009) Altering the ribosomal subunit ratio in yeast maximizes recombinant protein yield. Microb Cell Fact 8: 10.
28. Kuipers OP, de Ruyter PG, Kleerebezem M, de Vos WM, (1998) Quorum sensing-controlled gene expression in lactic acid bacteria. Journal of Biotechnology 64: 15-21.
29. Biemans-Oldehinkel E, Poolman B, (2003) On the role of the two extracytoplasmic substrate-binding domains in the ABC transporter OpuA. EMBO J 22: 5983-5993.
30. Zaitseva J, Jenewein S, Jumpertz T, Holland IB, Schmitt L, (2005) H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. EMBO J 24: 1901-1910.
31. Biemans-Oldehinkel E, Mahmood NA, Poolman B, (2006) A sensor for intracellular ionic strength. Proc Natl Acad Sci U S A 103: 10624-10629.
32. Pinto JP, Kuipers OP, Marreddy RK, Poolman B, Kok J, (2011) Efficient overproduction of membrane proteins in Lactococcus lactis relies on the cell envelope stress sensor/regulator couple CesSR. PLoS ONE Accompanying paper.
33. Kuipers OP, de Jong A, Baerends RJ, van Hijum SA, Zomer AL, et al. (2002) Transcriptome analysis and related databases of Lactococcus lactis. Antonie Van Leeuwenhoek 82: 113-122.
34. Gygi SP, Rochon Y, Franza BR, Aebersold R, (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19: 1720-1730.
35. Ideker T, Thorsson V, Ranish JA, Christmas R, Buhler J, et al. (2001) Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292: 929-934.
36. Martinez B, Zomer AL, Rodriguez A, Kok J, Kuipers OP, (2007) Cell envelope stress induced by the bacteriocin Lcn972 is sensed by the Lactococcal two-component system CesSR. Mol Microbiol 64: 473-486.
37. Veiga P, Bulbarela-Sampieri C, Furlan S, Maisons A, Chapot-Chartier MP, et al. (2007) SpxB regulates O-acetylation-dependent resistance of Lactococcus lactis peptidoglycan to hydrolysis. J Biol Chem 282: 19342-19354.
38. van Bloois E, Dekker HL, Froderberg L, Houben EN, Urbanus ML, et al. (2008) Detection of cross-links between FtsH, YidC, HflK/C suggests a linked role for these proteins in quality control upon insertion of bacterial inner membrane proteins. FEBS Lett 582: 1419-1424.
39. Guedon E, Sperandio B, Pons N, Ehrlich SD, Renault P, (2005) Overall control of nitrogen metabolism in Lactococcus lactis by CodY, and possible models for CodY regulation in Firmicutes. Microbiology 151: 3895-3909.
40. Gitton C, Meyrand M, Wang J, Caron C, Trubuil A, et al. (2005) Proteomic signature of Lactococcus lactis NCDO763 cultivated in milk. Appl Environ Microbiol 71: 7152-7163.
41. Budin-Verneuil A, Pichereau V, Auffray Y, Ehrlich DS, Maguin E, (2005) Proteomic characterization of the acid tolerance response in Lactococcus lactis MG1363. Proteomics 5: 4794-4807.
42. Dressaire C, Redon E, Milhem H, Besse P, Loubiere P, et al. (2008) Growth rate regulated genes and their wide involvement in the Lactococcus lactis stress responses. BMC Genomics 9: 343.
43. Schlame M, (2008) Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes. J Lipid Res 49: 1607-1620.
44. Chang DE, Smalley DJ, Conway T, (2002) Gene expression profiling of Escherichia coli growth transitions: an expanded stringent response model. Mol Microbiol 45: 289-306.
45. Eymann C, Homuth G, Scharf C, Hecker M, (2002) Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis. J Bacteriol 184: 2500-2520.
46. Rallu F, Gruss A, Maguin E, (1996) Lactococcus lactis and stress. Antonie Van Leeuwenhoek 70: 243-251.
47. Budin-Verneuil A, Pichereau V, Auffray Y, Ehrlich D, Maguin E, (2007) Proteome phenotyping of acid stress-resistant mutants of Lactococcus lactis MG1363. Proteomics 7: 2038-2046.
48. van Asseldonk M, Simons A, Visser H, de Vos WM, Simons G, (1993) Cloning, nucleotide sequence, and regulatory analysis of the Lactococcus lactis dnaJ gene. J Bacteriol 175: 1637-1644.
49. Eaton T, Shearman C, Gasson M, (1993) Cloning and sequence analysis of the dnaK gene region of Lactococcus lactis subsp. lactis. J Gen Microbiol 139: 3253-3264.
50. Varmanen P, Ingmer H, Vogensen FK, (2000) ctsR of Lactococcus lactis encodes a negative regulator of clp gene expression. Microbiology 146 (Pt 6): 1447-1455.
51. Kilstrup M, Jacobsen S, Hammer K, Vogensen FK, (1997) Induction of heat shock proteins DnaK, GroEL, and GroES by salt stress in Lactococcus lactis. Appl Environ Microbiol 63: 1826-1837.
52. Steen A, Wiederhold E, Gandhi T, Breitling R, Slotboom DJ, (2010) Physiological adaptation of the bacterium Lactococcus lactis in response to the production of human CFTR. Mol Cell Proteomics doi:10.1074/mcp.M000052-MCP201.
53. Beyer NH, Roepstorff P, Hammer K, Kilstrup M, (2003) Proteome analysis of the purine stimulon from Lactococcus lactis. Proteomics 3: 786-797.
54. Palmfeldt J, Levander F, Hahn-Hagerdal B, James P, (2004) Acidic proteome of growing and resting Lactococcus lactis metabolizing maltose. Proteomics 4: 3881-3898.
55. van der Heide T, Poolman B, (2000) Osmoregulated ABC-transport system of Lactococcus lactis senses water stress via changes in the physical state of the membrane. Proc Natl Acad Sci U S A 97: 7102-7106.
56. Holo H, Nes IF, (1989) High-Frequency Transformation, by Electroporation, of Lactococcus lactis subsp. cremoris Grown with Glycine in Osmotically Stabilized Media. Appl Environ Microbiol 55: 3119-3123.
57. Nolan T, Hands RE, Bustin SA, (2006) Quantification of mRNA using real-time RT-PCR. Nat Protoc 1: 1559-1582.
58. Mahmood NA, Biemans-Oldehinkel E, Poolman B, (2009) Engineering of ion sensing by the cystathionine beta-synthase module of the ABC transporter OpuA. J Biol Chem 284: 14368-14376.
59. van Hijum SA, de Jong A, Buist G, Kok J, Kuipers OP, (2003) UniFrag and GenomePrimer: selection of primers for genome-wide production of unique amplicons. Bioinformatics 19: 1580-1582.
60. van Hijum SA, de Jong A, Baerends RJ, Karsens HA, Kramer NE, et al. (2005) A generally applicable validation scheme for the assessment of factors involved in reproducibility and quality of DNA-microarray data. BMC Genomics 6: 77.
61. Long AD, Mangalam HJ, Chan BY, Tolleri L, Hatfield GW, et al. (2001) Improved statistical inference from DNA microarray data using analysis of variance and a Bayesian statistical framework. Analysis of global gene expression in Escherichia coli K12. J Biol Chem 276: 19937-19944.
62. Tatusov RL, Koonin EV, Lipman DJ, (1997) A genomic perspective on protein families. Science 278: 631-637.
63. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
64. Kanehisa M, Goto S, Hattori M, oki-Kinoshita KF, Itoh M, et al. (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34: D354-D357.
65. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, et al. (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36: D480-D484.
66. Sturn A, Quackenbush J, Trajanoski Z, (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18: 207-208.
67. Gasson MJ, (1983) Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J Bacteriol 154: 1-9.
68. 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: 4581-4584.