Of blood, brains and bacteria, the Amt/Rh transporter family: Emerging role of Amt as a unique microbial sensor

Molecular Microbiology

Volumn 71, Issue 1, 2009, Pages 12-22

  Tremblay, Pier Luc ^a   Hallenbeck, Patrick C ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; BACTERIAL PROTEIN; NITROGENASE; PROTEIN AMT; PROTEIN RH; UNCLASSIFIED DRUG;

CELL METABOLISM; CRYSTALLOGRAPHY; EUKARYOTE; GENOME; GRAM POSITIVE BACTERIUM; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SENSOR; SHORT SURVEY; SIGNAL TRANSDUCTION; YEAST;

BACTERIA; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE TRANSPORT PROTEINS; PII NITROGEN REGULATORY PROTEINS; QUATERNARY AMMONIUM COMPOUNDS;

BACTERIA (MICROORGANISMS); EUKARYOTA; POSIBACTERIA;

EID: 58149136355     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06514.x     Document Type: Short Survey

References (70)

1. Andrade, S.L., Dickmanns, A., Ficner, R. Einsle, O. (2005) Crystal structure of the archaeal ammonium transporter Amt-1 from Archaeoglobus fulgidus. Proc Natl Acad Sci USA 102 : 14994 14999.
2. Andrade, S.L. Einsle, O. (2007) The Amt/Mep/Rh family of ammonium transport proteins. Mol Membr Biol 24 : 357 365.
3. Arcondéguy, T., Jack, R. Merrick, M. (2001) P(II) signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65 : 80 105.
4. Atkinson, M.R. Ninfa, A.J. (1999) Characterization of the GlnK protein of Escherichia coli. Mol Microbiol 32 : 301 313.
5. Atkinson, M.R., Kamberov, E.S., Weiss, R.L. Ninfa, A.J. (1994) Reversible uridylylation of the Escherichia coli PII signal transduction protein regulates its ability to stimulate the dephosphorylation of the transcription factor nitrogen regulator I (NRI or NtrC). J Biol Chem 269 : 28288 28293.
6. Avent, N.D. (2001) A new chapter in Rh research: Rh proteins are ammonium transporters. Trends Mol Med 7 : 94 96.
7. Biswas, K. Morschhäuser, J. (2005) The Mep2 ammonium permease controls nitrogen starvation-induced filamentous growth in Candida albicans. Mol Microbiol 56 : 649 669.
8. Blauwkamp, T.A. Ninfa, A.J. (2003) Antagonism of PII signalling by the AmtB protein of Escherichia coli. Mol Microbiol 48 : 1017 1028.
9. Boeckstaens, M., André, B. Marini, A.M. (2007) The yeast ammonium transport protein Mep2 and its positive regulator, the Npr1 kinase, play an important role in normal and pseudohyphal growth on various nitrogen media through retrieval of excreted ammonium. Mol Microbiol 64 : 534 546.
10. Boeckstaens, M., André, B. Marini, A.M. (2008) Distinct transport mechanisms in yeast ammonium transport/sensor proteins of the Mep/Amt/Rh family and impact on filamentation. J Biol Chem 283 : 21362 21370.
11. Bollmann, A., Bär-Gilissen, M.J. Laanbroek, H.J. (2002) Growth at low ammonium concentrations and starvation response as potential factors involved in niche differentiation among ammonia-oxidizing bacteria. Appl Environ Microbiol 68 : 4751 4757.
12. Bruce, L.J. (2008) Red cell membrane transport abnormalities. Curr Opin Hematol 15 : 184 190.
13. Cherif-Zahar, B., Durand, A., Schmidt, I., Hamdaoui, N., Matic, I., Merrick, M. Matassi, G. (2007) Evolution and functional characterization of the RH50 gene from the ammonia-oxidizing bacterium Nitrosomonas europaea. J Bacteriol 189 : 9090 9100.
14. Conroy, M.J., Durand, A., Lupo, D., Li, X.D., Bullough, P.A., Winkler, F.K. Merrick, M. (2007) The crystal structure of the Escherichia coli AmtB-GlnK complex reveals how GlnK regulates the ammonia channel. Proc Natl Acad Sci USA 104 : 1213 1218.
15. 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.
16. Durand, A. Merrick, M. (2006) In vitro analysis of the Escherichia coli AmtB-GlnK complex reveals a stoichiometric interaction and sensitivity to ATP and 2-oxoglutarate. J Biol Chem 281 : 29558 29567.
17. 2 channel in the human red cell membrane. FASEB J 22 : 64 73.
18. Fong, R.N., Kim, K.S., Yoshihara, C., Inwood, W.B. Kustu, S. (2007) The W148L substitution in the Escherichia coli ammonium channel AmtB increases flux and indicates that the substrate is an ion. Proc Natl Acad Sci USA 104 : 18706 18711.
19. Forchhammer, K. (2008) P(II) signal transducers: novel functional and structural insights. Trends Microbiol 16 : 65 72.
20. Frias-Lopez, J., Shi, Y., Tyson, G.W., Coleman, M.L., Schuster, S.C., Chisholm, S.W. DeLong, E.F. (2008) Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105 : 3805 3810.
21. Gimeno, C.J., Ljungdahl, P.O., Styles, C.A. Finks, G.R. (1992) Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68 : 1077 1090.
22. Gruswitz, F., O'Connell, J., 3rd. Stroud, R.M. (2007) Inhibitory complex of the transmembrane ammonia channel, AmtB, and the cytosolic regulatory protein, GlnK, at 1.96 A. Proc Natl Acad Sci USA 104 : 42 47.
23. Heinrich, A., Wodya, K., Brauburger, K., Meiss, G., Detsch, C., Stülke, J. Forchhammer, K. (2006) Interaction of the membrane-bound GlnK-AmtB complex with the master regulator of nitrogen metabolism TnrA in Bacillus subtilis. J Biol Chem 281 : 34909 34917.
24. Holsbeeks, I., Lagatie, O., Van Nuland, A., Van de Velde, S. Thevelein, J.M. (2004) The eukaryotic plasma membrane as a nutrient-sensing device. Trends Biochem Sci 29 : 556 564.
25. Huergo, L.F., Souza, E.M., Araujo, M.S., Pedrosa, F.O., Chubatsu, L.S., Steffens, M.B. Merrick, M. (2006) ADP-ribosylation of dinitrogenase reductase in Azospirillum brasilense is regulated by AmtB-dependent membrane sequestration of DraG. Mol Microbiol 59 : 326 337.
26. Huergo, L.F., Merrick, M., Pedrosa, F.O., Chubatsu, L.S., Araujo, L.M. Souza, E.M. (2007) Ternary complex formation between AmtB, GlnZ and the nitrogenase regulatory enzyme DraG reveals a novel facet of nitrogen regulation in bacteria. Mol Microbiol 66 : 1523 1535.
27. Javelle, A. Merrick, M. (2005) Complex formation between AmtB and GlnK: an ancestral role in prokaryotic nitrogen control. Biochem Soc Trans 33 : 170 172.
28. Javelle, A., Severi, E., Thornton, J. Merrick, M. (2004) Ammonium sensing in Escherichia coli. Role of the ammonium transporter AmtB and AmtB-GlnK complex formation. J Biol Chem 279 : 8530 8538.
29. Javelle, A., Lupo, D., Ripoche, P., Fulford, T., Merrick, M. Winkler, F.K. (2008) Substrate binding, deprotonation, and selectivity at the periplasmic entrance of the Escherichia coli ammonia channel AmtB. Proc Natl Acad Sci USA 105 : 5040 5045.
30. Kayumov, A., Heinrich, A., Sharipova, M., Iljinskaya, O. Forchhammer, K. (2008) Inactivation of the general transcription factor TnrA in Bacillus subtilis by proteolysis. Microbiology 154 : 2348 2355.
31. Khademi, S., O'Connell, J., 3rd, Remis, J., Robles-Colmenares, Y., Miercke, L.J. Stroud, R.M. (2004) Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 A. Science 305 : 1587 1594.
32. 2 fixation by Klebsiella pneumoniae. FEBS Lett 187 : 237 239.
33. Leigh, J.A. Dodsworth, J.A. (2007) Nitrogen regulation in bacteria and archaea. Annu Rev Microbiol 61 : 349 377.
34. Li, X., Jayachandran, S., Nguyen, H.H. Chan, M.K. (2007) Structure of the Nitrosomonas europaea Rh protein. Proc Natl Acad Sci USA 104 : 19279 19284.
35. Loqué, D., Lalonde, S., Looger, L.L., von Wirén, N. Frommer, W.B. (2007) A cytosolic trans-activation domain essential for ammonium uptake. Nature 446 : 195 198.
36. Ludewig, U., Neuhäuser, B. Dynowsky, M. (2007) Molecular mechanisms of ammonium transport and accumulation in plants. FEBS Lett 581 : 2301 2308.
37. 3 transport by Rhesus family proteins. Proc Natl Acad Sci USA 104 : 19303 19308.
38. Marini, A.M., Soussi-Boudekou, S., Vissers, S. André, B. (1997) A family of ammonium transporters in Saccharomyces cerevisiae. Mol Cell Biol 17 : 4282 4293.
39. Marini, A.M., Boeckstaens, M. André, B. (2006a) From yeast ammonium transporters to Rhesus proteins, isolation and functional characterization. Transfus Clin Biol 13 : 95 96.
40. Marini, A.M., Boeckstaens, M., Benjelloun, F., Cherif-Zahar, B. André, B. (2006b) Structural involvement in substrate recognition of an essential aspartate residue conserved in Mep/Amt and Rh-type ammonium transporters. Curr Genet 49 : 364 374.
41. Marino, R., Melillo, D., Di Filippo, M., Yamada, A., Pinto, M.R., De Santis, R., et al. (2007) Ammonium channel expression is essential for brain development and function in the larva of Ciona intestinalis. J Comp Neurol 503 : 135 147.
42. Missner, A., Kügler, P., Saparov, S.M., Sommer, K., Mathai, J.C., Zeidel, M.L. Pohl, P. (2008) Carbon dioxide transport through membranes. J Biol Chem 283 : 25340 25347.
43. Mulder, N.J., Apweiler, R., Attwood, T.K., Bairoch, A., Bateman, A., Binns, D., et al. (2007) New developments in the InterPro database. Nucleic Acids Res 35 : D224 D228.
44. + transport by essential cross talk between AMT monomers through the carboxyl tails. Plant Physiol 143 : 1651 1659.
45. Nicolas, V., Mouro-Chanteloup, I., Lopez, C., Gane, P., Gimm, A., Mohandas, N., et al. (2006) Functional interaction between Rh proteins and the spectrin-based skeleton in erythroid and epithelial cells. Transfus Clin Biol 13 : 23 28.
46. Ninfa, A.J. Atkinson, M.R. (2000) PII signal transduction proteins. Trends Microbiol 8 : 172 179.
47. 3 gas channels. Transfus Clin Biol 13 : 85 94.
48. Planelles, G. (2007) Ammonium homeostasis and human rhesus glycoproteins. Nephron Physiol 105 : 11 17.
49. Rutherford, J.C., Lin, X., Nielson, K. Heitman, J. (2008a) Amt2 permease is required to induce ammonium responsive invasive growth and mating in Cryptococcus neoformans. Eukaryot Cell 7 : 237 246.
50. Rutherford, J.C., Chua, G., Hughes, T., Cardenas, M.E. Heitman, J. (2008b) A Mep2-dependent transcriptional profile links permease function to gene expression during pseudohyphal growth in Saccharomyces cerevisiae. Mol Biol Cell 19 : 3028 3039.
51. Ryan, R.P., Fouhy, Y., Lucey, J.F. Dow, J.M. (2006) Cyclic di-GMP signaling in bacteria: recent advances and new puzzles. J Bacteriol 188 : 8327 8334.
52. Schwöppe, C., Winkler, H.H. Neuhaus, H.E. (2003) Connection of transport and sensing by UhpC, the sensor for external glucose-6-phosphate in Escherichia coli. Eur J Biochem 270 : 1450 1457.
53. Sohet, F., Colin, Y., Genetet, S., Ripoche, P., Métral, S., Le Van Kim, C. Lopez, C. (2008) Phosphorylation and ankyrin-G binding of the C-terminal domain regulate targeting and function of the ammonium transporter RhBG. J Biol Chem 283 : 26557 26567.
54. Soupene, E., He, L., Yan, D. Kustu, S. (1998) Ammonia acquisition in enteric bacteria: physiological role of the ammonium/methylammonium transport B (AmtB) protein. Proc Natl Acad Sci USA 95 : 7030 7034.
55. 2. Proc Natl Acad Sci USA 101 : 7787 7792.
56. Stips, J., Thummer, R., Neumann, M. Schmitz, R.A. (2004) GlnK effects complex formation between NifA and NifL in Klebsiella pneumoniae. Eur J Biochem 271 : 3379 3388.
57. Strösser, J., Lüdke, A., Schaffer, S., Krämer, R. Burkovski, A. (2004) Regulation of GlnK activity: modification, membrane sequestration and proteolysis as regulatory principles in the network of nitrogen control in Corynebacterium glutamicum. Mol Microbiol 54 : 132 147.
58. Teichert, S., Rutherford, J.C., Wottawa, M., Heitman, J. Tudzynski, B. (2008) Impact of ammonium permeases MepA, MepB, and MepC on nitrogen-regulated secondary metabolism in Fusarium fujikuroi. Eukaryot Cell 7 : 187 201.
59. Teixeira, P.F., Jonsson, A., Frank, M., Wang, H. Nordlund, S. (2008) Interaction of the signal transduction protein GlnJ with the cellular targets AmtB1, GlnE and GlnD in Rhodospirillum rubrum: dependence on manganese, 2-oxoglutarate and the ADP/ATP ratio. Microbiology 154 : 2336 2347.
60. Tremblay, P.-L. Hallenbeck, P.C. (2008) Ammonia-induced formation of an AmtB-GlnK complex is not sufficient for nitrogenase regulation in the photosynthetic bacterium Rhodobacter capsulatus. J Bacteriol 190 : 1588 1594.
61. Tremblay, P.-L., Drepper, T., Masepohl, B. Hallenbeck, P.C. (2007) Membrane sequestration of PII proteins and nitrogenase regulation in the photosynthetic bacterium Rhodobacter capsulatus. J Bacteriol 189 : 5850 5859.
62. Van Nuland, A., Vandormael, P., Donaton, M., Alenquer, M., Lourenço, A., Quintino, E., et al. (2006) Ammonium permease-based sensing mechanism for rapid ammonium activation of the protein kinase A pathway in yeast. Mol Microbiol 59 : 1485 1505.
63. Walter, B., Küspert, M., Ansorge, D., Krämer, R. Burkovski, A. (2008) Dissection of ammonium uptake systems in Corynebacterium glutamicum: mechanism of action and energetics of AmtA and AmtB. J Bacteriol 190 : 2611 2614.
64. Wang, H., Franke, C.C., Nordlund, S. Norén, A. (2005) Reversible membrane association of dinitrogenase reductase activating glycohydrolase in the regulation of nitrogenase activity in Rhodospirillum rubrum; dependence on GlnJ and AmtB1. FEMS. Microbiol Lett 253 : 273 279.
65. Weidinger, K., Neuhäuser, B., Gilch, S., Ludewig, U., Meyer, O. Schmidt, I. (2007) Functional and physiological evidence for a Rhesus-type ammonia transporter in Nitrosomonas europaea. FEMS Microbiol Lett 273 : 260 267.
66. Wolfe, D.M., Zhang, Y. Roberts, G.P. (2007) Specificity and regulation of interaction between the PII and AmtB1 proteins in Rhodospirillum rubrum. J Bacteriol 189 : 6861 6869.
67. +-induced nitrogenase switch-off and ADP-ribosylation in Rhodobacter capsulatus. J Bacteriol 184 : 4081 4088.
68. Yildiz, O., Kalthoff, C., Raunser, S. Kühlbrandt, K. (2007) Structure of GlnK1 with bound effectors indicates regulatory mechanism for ammonia uptake. EMBO J 26 : 589 599.
69. Zhang, Y., Wolfe, D.M., Pohlmann, E.L., Conrad, M.C. Roberts, G.P. (2006) Effect of AmtB homologues on the post-translational regulation of nitrogenase activity in response to ammonium and energy signals in Rhodospirillum rubrum. Microbiology 152 : 2075 2089.
70. Zheng, L., Kostrewa, D., Bernèche, S., Winkler, F.K. Li, X.D. (2004) The mechanism of ammonia transport based on the crystal structure of AmtB of Escherichia coli. Proc Natl Acad Sci USA 101 : 17090 17095.