Skip to main content
SpringerLink
Log in
Book cover

Molecular Mechanisms Controlling Transmembrane Transport pp 47–66Cite as

Transport-dependent gene regulation by sequestration of transcriptional regulators

  • Chapter
  • First Online:

Part of the book series: Topics in Current Genetics ((TCG,volume 9))

Abstract

We describe a new principle of signal transduction in prokaryotes: certain transport systems have an additional function in signaling. Depending on the activity of the transporter, transcription factors are sequestered, thus shuttling between the inner face of the cytoplasmic membrane and their target promoters. The change in their subcellular address corresponds to the on/off state of the respective signal transduction cascade. For example, Escherichia coli MalT is kept in an inactive form by the idling maltodextrin ABC transporter. When the transporter is activated by maltodextrin transport, MalT is released and binds to its cognate operators. E. coli Mlc is bound to its operators when the glucose-specific enzyme II (EIICBGlc) of the phosphoenolpyruvate:carbohydrate phosphotransferase system is not transporting; when glucose transport starts, Mlc is captured by the dephosphorylated form of EIICBGlc, thus allowing transcription of its cognate operons. Salmonella typhimurium PutA, E. coli GlnK and Klebsiella pneumoniae NifL are discussed as additional examples.

This is a preview of subscription content, log in via an institution.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • 1. Amster-Choder O, Wright A (1993) Transcriptional regulation of the bgl operon of Escherichia coli involves phosphotransferase system-mediated phosphorylation of a transcriptional antiterminator. J Cell Biochem 51:83-90

    Article  PubMed  CAS  Google Scholar 

  • 2. Böhm A (2002) Mechanismus und physiologische Bedeutung der MalK-vermittelten Repression des Escherichia coli Maltose Regulons. PhD thesis. Universität Konstanz

    Google Scholar 

  • 3. Böhm A, Diez J, Diederichs K, Welte W, Boos W (2002) Structural model of MalK, the ABC subunit of the maltose transporter of Escherichia coli: implications for mal gene regulation, inducer exclusion, and subunit assembly. J Biol Chem 277:3708-3717

    Article  PubMed  Google Scholar 

  • 4. Boos W, Böhm A (2000) Learning new tricks from an old dog. MalT of the Escherichia coli maltose system is part of a complex regulatory network. Trends Genet 16:404-409

    Article  PubMed  CAS  Google Scholar 

  • 5. Boos W, Lucht JM (1996) Periplasmic binding protein-dependent ABC transporters. In: Neidhardt FC et al. (eds) Escherichia coli and Salmonella typhimurium; cellular and molecular biology. vol. 1, American Society of Microbiology, Washington, DC, pp 1175-1209

    Google Scholar 

  • 6. Boos W, Shuman HA (1998) The maltose/maltodextrin system of Escherichia coli; transport, metabolism and regulation. Microbiol Mol Biol Rev 62:204-229

    PubMed  CAS  Google Scholar 

  • 7. Bukau B, Ehrmann M, Boos W (1986) Osmoregulation of the maltose regulon in Escherichia coli. J. Bacteriol. 166:884-891

    Google Scholar 

  • 8. Chen J, Lu G, Lin J, Davidson AL, Quiocho FA (2003) A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol Cell 12:651-661

    Article  PubMed  CAS  Google Scholar 

  • 9. Chen J, Sharma S, Quiocho FA, Davidson AL (2001) Trapping the transition state of an ATP-binding cassette transporter: evidence for a concerted mechanism of maltose transport. Proc Natl Acad Sci USA 98:1525-1530

    Article  PubMed  CAS  Google Scholar 

  • 10. Chen Q, Amster-Choder O (1998) BglF, the sensor of the bgl system and the b-glucosides permease of Escherichia coli: Evidence for dimerization and intersubunit phosphotransfer. Biochemistry 37:8714-8723

    Article  PubMed  CAS  Google Scholar 

  • 11. Clausen T, Schlegel A, Peist R, Schneider E, Steegborn C, Chang Y-S, Haase A, Bourenkov GP, Bartunik HD, Boos W (2000) X-ray structure of MalY from Escherichia coli: a pyridoxal 5’-phosphate-dependent enzyme acting as a modulator in mal gene expression. EMBO J 19:831-842

    Article  PubMed  CAS  Google Scholar 

  • 12. Coutts G, Thomas G, Blakey D, Merrick M (2002) Membrane sequestration of the signal transduction protein GlnK by the ammonium transporter AmtB. EMBO J 21:536-545

    Article  PubMed  CAS  Google Scholar 

  • 13. Covitz KMY, Panagiotidis CH, Hor LI, Reyes M, Treptow NA, Shuman HA (1994) Mutations that alter the transmembrane signalling pathway in an ATP binding cassette (ABC) transporter. EMBO J 13:1752-1759

    PubMed  CAS  Google Scholar 

  • 14. Dassa E, Hofnung M, Paulsen IT, Saier MH (1999) The Escherichia coli ABC transporters: an update. Mol Microbiol 32:887-889

    Article  PubMed  CAS  Google Scholar 

  • 15. Davidson AL, Nikaido H (1991) Purification and characterization of the membrane-associated components of the maltose transport system from Escherichia coli. J Biol Chem 266:8946-8951

    PubMed  CAS  Google Scholar 

  • 16. Dean DA, Davidson AL, Nikaido H (1989) Maltose transport in membrane vesicles of Escherichia coli is linked to ATP hydrolysis. Proc Natl Acad Sci USA 86:9134-9138

    Article  PubMed  CAS  Google Scholar 

  • 17. Dean DA, Reizer J, Nikaido H, Saier M (1990) Regulation of the maltose transport system of Escherichia coli by the glucose-specific enzyme III of the phosphoenolpyruvate-sugar phosphotransferase system. Characterization of inducer exclusion-resistant mutants and reconstitution of inducer exclusion in proteoliposomes. J Biol Chem 265:21005-21010

    PubMed  CAS  Google Scholar 

  • 18. Débarbouillé M, Shuman HA, Silhavy TJ, Schwartz M (1978) Dominant constitutive mutations in malT, the positive regulator of the maltose regulon in Escherichia coli. J Mol Biol 124:359-371

    Article  PubMed  Google Scholar 

  • 19. Decker K, Peist R, Reidl J, Kossmann M, Brand B, Boos W (1993) Maltose and maltotriose can be formed endogenously in Escherichia coli from glucose and glucose-1-phosphate independently of enzymes of the maltose system. J Bacteriol 175:5655-5665

    PubMed  CAS  Google Scholar 

  • 20. Decker K, Plumbridge J, Boos W (1998) Negative transcriptional regulation of a positive regulator: the expression of malT, encoding the transcriptional activator of the maltose regulon of Escherichia coli, is negatively controlled by Mlc. Mol Microbiol 27:381-390

    Article  PubMed  CAS  Google Scholar 

  • 21. DeLano WL (2002) The PyMol molecular graphics system. http://www.pymol.org

    Google Scholar 

  • 22. Diederichs K, Diez J, Greller G, Müller C, Breed J, Schnell C, Vonrhein C, Boos W, Welte W (2000) Crystal structure of MalK, the ATPase subunit of the trehalose/maltose ABC transporter of the archaeon Thermococcus litoralis. EMBO J 19:5951-5961

    Article  PubMed  CAS  Google Scholar 

  • 23. Dixon R (1998) The oxygen-responsive NIFL-NIFA complex: a novel two-component regulatory system controlling nitrogenase synthesis in gamma-proteobacteria. Arch Microbiol 169:371-380

    Article  PubMed  CAS  Google Scholar 

  • 24. Englesberg E, Wilcox G (1974) Regulation: positive control. Annu Rev Genet 8:219-242

    Article  PubMed  CAS  Google Scholar 

  • 25. Fetsch EE, Davidson AL (2002) Vanadate-catalyzed photocleavage of the signature motif of an ATP-binding cassette (ABC) transporter. Proc Natl Acad Sci USA 99:9685-9690

    Article  PubMed  CAS  Google Scholar 

  • 26. Greller G, Horlacher R, DiRuggiero J, Boos W (1999) Molecular and biochemical analysis of MalK, the ATP-hydrolyzing subunit of the trehalose maltose transport system of the hyperthermophilic archaeon Thermococcus litoralis. J Biol Chem 274:20259-20264

    Article  PubMed  CAS  Google Scholar 

  • 27. Hall DR, Gourley DG, Leonard GA, Duke EMH, Anderson LA, Boxer DH, Hunter WN (1999) The high-resolution crystal structure of the molybdate-dependent transcriptional regulator (ModE) from Escherichia coli: a novel combination of domain folds. EMBO J 18:1435-1446

    Article  PubMed  CAS  Google Scholar 

  • 28. Hanada K, Yoshida T, Yamato I, Anraku Y (1992) Sodium ion and proline binding sites in the Na+/proline symport carrier of Escherichia coli. Biochim Biophys Acta 1105:61-66

    Article  PubMed  CAS  Google Scholar 

  • 29. Higgins CF (2001) ABC transporters: physiology, structure, and mechanism. An overview. Res Microbiol 152:205-210

    Article  PubMed  CAS  Google Scholar 

  • 30. Hopfner K-P, Karcher A, Shin DS, Craig L, Arthur LM, Carney JP, Tainer JA (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101:789-800

    Article  PubMed  CAS  Google Scholar 

  • 31. Hosono K, Kakuda H, Ichihara S (1995) Decreasing accumulation of acetate in a rich medium by Escherichia coli on introduction of genes on a multicopy plasmid. Biosci Biotech Biochem 59:256-261

    Article  CAS  Google Scholar 

  • 32. Hung L-W, Wang IX, Nikaido K, Liu P-Q, Ames GF-L, Kim S-H (1998) Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 396:703-707

    Article  PubMed  CAS  Google Scholar 

  • 33. Hunke S, Landmesser H, Schneider E (2000) Novel missense mutations that affect the transport function of MalK, the ATP-binding-cassette subunit of the Salmonella enterica serovar typhimurium maltose transport system. J Bacteriol 182:1432-1436

    Article  PubMed  CAS  Google Scholar 

  • 34. Jacob F, Monod J (1961) Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3:318-356

    Article  PubMed  CAS  Google Scholar 

  • 35. Joly N, Danot O, Schlegel A, Boos W, Richet E (2002) The Aes protein directly controls the activity of MalT, the central transcriptional activator of the Escherichia coli maltose regulon. J Biol Chem 277:16606-16613

    Article  PubMed  CAS  Google Scholar 

  • 36. Karpowich N, Martsinkevich O, Millen L, Yuan YR, Dai PL, MacVey K, Thomas PJ, Hunt JF (2001) Crystal structures of the MJ1267 ATP binding cassette reveal an induced-fit effect at the ATPase active site of an ABC transporter. Structure 9:571-586

    Article  PubMed  CAS  Google Scholar 

  • 37. Klopprogge K, Grabbe R, Hoppert M, Schmitz RA (2002) Membrane association of Klebsiella pneumoniae NifL is affected by molecular oxygen and combined nitrogen. Arch Microbiol 177:223-234

    Article  PubMed  CAS  Google Scholar 

  • 38. Kühnau S, Reyes M, Sievertsen A, Shuman HA, Boos W (1991) The activities of the Escherichia coli MalK protein in maltose transport, regulation and inducer exclusion can be separated by mutations. J Bacteriol 173:2180-2186

    PubMed  Google Scholar 

  • 39. Lee S-J, Boos W, Bouché J-P, Plumbridge J (2000) Signal transduction between a membrane bound transporter, PtsG, and a soluble transcription factor, Mlc, of Escherichia coli. EMBO J 19:5353-5361

    Article  PubMed  CAS  Google Scholar 

  • 40. Lloyd G, Landini P, Busby S (2001) Activation and repression of transcription initiation in bacteria. Essays Biochem 37:17-31

    PubMed  CAS  Google Scholar 

  • 41. Locher KP, Lee AT, Rees DC (2002) The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296:1091-1098

    Article  PubMed  CAS  Google Scholar 

  • 42. Margolin W (2000) Green fluorescent protein as a reporter for macromolecular localization in bacterial cells. Methods 20:62-72

    Article  PubMed  CAS  Google Scholar 

  • 43. Menzel R, Roth J (1981) Purification of the putA gene product. A bifunctional membrane-bound protein from Salmonella typhimurium responsible for the two-step oxidation of proline to glutamate. J Biol Chem 256:9755-9761

    PubMed  CAS  Google Scholar 

  • 44. Moody JE, Millen L, Binns D, Hunt JF, Thomas PJ (2002) Cooperative, ATP-dependent association of the nucleotide binding cassettes during the catalytic cycle of ATP-binding cassette transporters. J Biol Chem 277:21111-21114

    Article  PubMed  CAS  Google Scholar 

  • 45. Mourez M, Hofnung M, Dassa E (1997) Subunit interactions in ABC transporters: a conserved sequence in hydrophobic membrane proteins of periplasmic permeases defines an important site of interaction with the ATPase subunits. EMBO J 16:3066-3077

    Article  PubMed  CAS  Google Scholar 

  • 46. Muro-Pastor AM, Ostrovsky P, Maloy S (1997) Regulation of gene expression by repressor localization: biochemical evidence that membrane and DNA binding by the PutA protein are mutually exclusive. J Bacteriol 179:2788-2791

    PubMed  CAS  Google Scholar 

  • 47. Nam T-W, Cho S-H, Shin D, Kim J-H, Jeong J-Y, Lee J-H, Roe J-H, Peterkofsky A, Kang S-O, Ryu S, Seok Y-J (2001) The Escherichia coli glucose transporter enzyme IICBGlc recruits the global repressor Mlc. EMBO J 20:491-498

    Article  PubMed  CAS  Google Scholar 

  • 48. Notley-McRobb L, Ferenci T (2000) Substrate specificity and signal transduction pathways in the glucose-specific enzyme II (EIIGlc) component of the Escherichia coli phosphotransferase system. J Bacteriol 182:4437-4442

    Article  PubMed  CAS  Google Scholar 

  • 49. Ostrovsky de Spicer P, Maloy S (1993) PutA protein, a membrane-associated flavin dehydrogenase, acts as a redox-dependent transcriptional regulator. Proc Natl Acad Sci USA 90:4295-4298

    Article  Google Scholar 

  • 50. Ostrovsky de Spicer P, O’Brien K, Maloy S (1991) Regulation of proline utilization in Salmonella typhimurium: a membrane-associated dehydrogenase binds DNA in vitro. J Bacteriol 173:211-219

    Google Scholar 

  • 51. Panagiotidis CH, Boos W, Shuman HA (1998) The ATP-binding cassette subunit of the maltose transporter MalK antagonizes MalT, the activator of the Escherichia coli mal regulon. Mol Microbiol 30:535-546

    Article  PubMed  CAS  Google Scholar 

  • 52. Parkinson JS, Kofoid EC (1992) Communication modules in bacterial signaling proteins. Annu Rev Genet 26:71-112

    Article  PubMed  CAS  Google Scholar 

  • 53. Peist R, Koch A, Bolek P, Sewitz S, Kolbus T, Boos W (1997) Characterization of the aes gene of Escherichia coli encoding an enzyme with esterase activity. J Bacteriol 179:7679-7686

    PubMed  CAS  Google Scholar 

  • 54. Plumbridge J (1998) Control of the expression of the manXYZ operon in Escherichia coli: Mlc is a negative regulator of the mannose PTS. Mol Microbiol 27:369-380

    Article  PubMed  CAS  Google Scholar 

  • 55. Plumbridge J (1999) Expression of the phosphotransferase system both mediates and is mediated by Mlc regulation in Escherichia coli. Mol Microbiol 33:260-273

    Article  PubMed  CAS  Google Scholar 

  • 56. Plumbridge J (2000) A mutation which affects both the specificity of PtsG sugar transport and the regulation of ptsG expression by Mlc in Escherichia coli. Microbiology 146:2655-2663

    PubMed  CAS  Google Scholar 

  • 57. Plumbridge J (2001) DNA binding sites for the Mlc and NagC proteins: regulation of nagE, encoding the N-acetylglucosamine-specific transporter in Escherichia coli. Nucl Acid Res 29:506-514

    Article  CAS  Google Scholar 

  • 58. Plumbridge J (2002) Regulation of gene expression in the PTS in Escherichia coli: the role and interactions of Mlc. Curr Opin Microbiol 5:187-193

    Article  PubMed  CAS  Google Scholar 

  • 59. Postma PW, Lengeler JW, Jacobson GR (1996) Phosphoenolpyruvate:carbohydrate phosphotransferase system. In: Neidhardt FC et al. (eds) Escherichia coli and Salmonella typhimurium; cellular and molecular biology, American Society of Microbiology, Washington, DC, pp 1149-1174

    Google Scholar 

  • 60. Reidl J, Boos W (1991) The malX malY operon of Escherichia coli encodes a novel enzyme II of the phosphotransferase system recognizing glucose and maltose and an enzyme abolishing the endogenous induction of the maltose system. J Bacteriol 173:4862-4876

    PubMed  CAS  Google Scholar 

  • 61. Reyes M, Shuman HA (1988) Overproduction of MalK protein prevents expression of the Escherichia coli mal regulon. J Bacteriol 170:4598-4602

    PubMed  CAS  Google Scholar 

  • 62. Richet E, Raibaud O (1989) MalT, the regulatory protein of the Escherichia coli maltose system, is an ATP-dependent transcriptional activator. EMBO J 8:981-987

    PubMed  CAS  Google Scholar 

  • 63. Samanta S, Ayvaz T, Reyes M, Shuman HA, Chen J, Davidson AL (2003) Disulfide cross-linking reveals a site of stable interaction between C-terminal regulatory domains of the two MalK subunits in the maltose transport complex. J Biol Chem 278:35265-35271

    Article  PubMed  CAS  Google Scholar 

  • 64. Schirmer T, Keller TA, Wang YF, Rosenbusch JP (1995) Structural basis for sugar translocation through maltoporin channels at 3.1 Å resolution. Science 267:512-514

    Article  PubMed  CAS  Google Scholar 

  • 65. Schlegel A, Danot O, Richet E, Ferenci T, Boos W (2002) The N terminus of the Escherichia coli transcription activator MalT is the domain of interaction with MalY. J Bacteriol 184:3069-3077.

    Article  PubMed  CAS  Google Scholar 

  • 66. Schleif R (1996) Two positively regulated systems, ara and mal. In: Neidhardt FC et al. (eds) Escherichia coli and Salmonella typhimurium; cellular and molecular biology. vol. 1, American Society of Microbiology, Washington, DC, pp 1300-1309

    Google Scholar 

  • 67. Schreiber V, Richet E (1999) Self-association of the Escherichia coli transcription activator MalT in the presence of maltotriose and ATP. J Biol Chem 274:33220-33226

    Article  PubMed  CAS  Google Scholar 

  • 68. Schreiber V, Steegborn C, Clausen T, Boos W, Richet E (2000) A new mechanism for the control of a prokaryotic transcriptional regulator: antagonistic binding of positive and negative effectors. Mol Microbiol 35:765-776

    Article  PubMed  CAS  Google Scholar 

  • 69. Schwartz M (1987) The maltose regulon. In: Neidhardt FC et al. (eds) Escherichia coli and Salmonella typhimurium: cellular and molecular biology. vol. 2, American Society of Microbiology, Washington D. C., pp 1482-1502

    Google Scholar 

  • 70. Seitz S, Lee SJ, Pennetier C, Boos W, Plumbridge J (2003) Analysis of the interaction between the global regulator Mlc and EIIBGlc of the glucose-specific phosphotransferase system in Escherichia coli. J Biol Chem 278:10744-10751

    Article  PubMed  CAS  Google Scholar 

  • 71. Shapiro L, Losick R (2000) Dynamic spatial regulation in the bacterial cell. Cell 100:89-98

    Article  PubMed  CAS  Google Scholar 

  • 72. Shin D, Lim S, Seok YJ, Ryu S (2001) Heat shock RNA polymerase (Es32) is involved in the transcription of mlc and crucial for induction of the Mlc regulon by glucose in Escherichia coli. J Biol Chem 276:25871-25875

    Article  PubMed  CAS  Google Scholar 

  • 73. Surber MW, Maloy S (1998) The PutA protein of Salmonella typhimurium catalyzes the two steps of proline degradation via a leaky channel. Arch Biochem Biophys 354:281-287

    Article  PubMed  CAS  Google Scholar 

  • 74. Surber MW, Maloy S (1999) Regulation of flavin dehydrogenase compartmentalization: requirements for PutA-membrane association in Salmonella typhimurium. Biochim Biophys Acta 1421:5-18

    Article  PubMed  CAS  Google Scholar 

  • 75. Tanaka Y, Kimata K, Aiba H (2000) A novel regulatory role of glucose transporter of Escherichia coli: membrane sequestration of a global repressor Mlc. EMBO J 19:5344-5352

    Article  PubMed  CAS  Google Scholar 

  • 76. Vandromme M, Gauthier-Rouviere C, Lamb N, Fernandez A (1996) Regulation of transcription factor localization: fine-tuning of gene expression. Trends Biochem Sci 21:59-64

    PubMed  CAS  Google Scholar 

  • 77. Verdon G, Albers SV, Dijkstra BW, Driessen AJ, Thunnissen AM (2003) Crystal structures of the ATPase subunit of the glucose ABC transporter from Sulfolobus solfataricus: nucleotide-free and nucleotide-bound conformations. J Mol Biol 330:343-358

    Article  PubMed  CAS  Google Scholar 

  • 78. West AH, Stock AM (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26:369-376

    Article  PubMed  CAS  Google Scholar 

  • 79. Zdych E, Peist R, Reidl J, Boos W (1995) MalY of Escherichia coli is an enzyme with the activity of a bC-S lyase (cystathionase). J Bacteriol 177:5035-5039

    PubMed  CAS  Google Scholar 

  • 80. Zeppenfeld T, Larisch C, Lengeler JW, Jahreis K (2000) Glucose transporter mutants of Escherichia coli K-12 with changes in substrate recognition of the IICBGlc and induction behavior of the ptsG gene. J Bacteriol 182:4443-4452

    Article  PubMed  CAS  Google Scholar 

  • 81. Zhu W, Becker DF (2003) Flavin redox state triggers conformational changes in the PutA protein from Escherichia coli. Biochemistry 42:5469-5477

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of Konstanz, Universitätsstrasse 10, 78457 Konstanz, Germany

    Alex Böhm & Winfried Boos

Authors
  1. Alex Böhm
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Winfried Boos
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 2004 Springer-Verlag Berlin/Heidelberg

About this chapter

Cite this chapter

Böhm, A., Boos, W. (2004). Transport-dependent gene regulation by sequestration of transcriptional regulators. In: Molecular Mechanisms Controlling Transmembrane Transport. Topics in Current Genetics, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/b95774

Download citation

  • DOI: https://doi.org/10.1007/b95774

  • Published:

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-540-21837-1

  • Online ISBN: 978-3-540-40912-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation