Direct sensing of nutrient availability by fungi

Fungal Biology Reviews

Volumn 25, Issue 2, 2011, Pages 111-119

  Rutherford, Julian ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Ammonium transporter; Copper transcription factor; Pseudohyphal growth; Yeast

Indexed keywords

FUNGI;

EID: 79957681300     PISSN: 17494613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fbr.2011.04.004     Document Type: Review

References (58)

1. Andrade S.L., Dickmanns A., Ficner R., Einsle O. Crystal structure of the archaeal ammonium transporter Amt-1 from Archaeoglobus fulgidus. Proceedings National Academy Sciences of the United States of America 2005, 102:14994-14999.
2. Barwell C.J., Woodward B., Brunt R.V. Regulation of pyruvate kinase by fructose 1,6-diphosphate in Saccharomyces cerevisiae. European Journal of Biochemistry 1971, 18:59-64.
3. Beaudoin J., Labbé S. The fission yeast copper-sensing transcription factor Cuf1 regulates the copper transporter gene expression through an Ace1/Amt1-like recognition sequence. The Journal of Biological Chemistry 2001, 276:15472-15480.
4. Beaudoin J., Mercier A., Langlois R., Labbé S. The Schizosaccharomyces pombe Cuf1 is composed of functional modules from two distinct classes of copper metalloregulatory transcription factors. The Journal of Biological Chemistry 2003, 278:14565-14577.
5. Beaudoin J., Labbé S. Copper induces cytoplasmic retention of fission yeast transcription factor cuf1. Eukaryotic Cell 2006, 5:277-292.
6. Beaudoin J., Labbé S. Crm1-mediated nuclear export of the Schizosaccharomyces pombe transcription factor Cuf1 during a shift from low to high copper concentrations. Eukaryotic Cell 2007, 6:764-775.
7. Biswas K., Morschhäuser J. The Mep2 ammonium permease controls nitrogen starvation-induced filamentous growth in Candida albicans. Molecular Microbiology 2005, 56:649-669.
8. Boeckstaens M., André B., Marini A.M. 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. Molecular Microbiology 2007, 64:534-546.
9. Boeckstaens M., André B., Marini A.M. Distinct transport mechanisms in yeast ammonium transport/sensor proteins of the Mep/Amt/Rh family and impact on filamentation. The Journal of Biological Chemistry 2008, 283:21362-21370.
10. Brown K.R., Keller G.L., Pickering I.J., Harris H.H., George G.N., Winge D.R. Structures of the cuprous-thiolate clusters of the Mac1 and Ace1 transcriptional activators. Biochemistry 2002, 41:6469-6476.
11. Donaton M.C., Holsbeeks I., Lagatie O., Van Zeebroeck G., Crauwels M., Winderickx J., Thevelein J.M. The Gap1 general amino acid permease acts as an amino acid sensor for activation of protein kinase A targets in the yeast Saccharomyces cerevisiae. Molecular Microbiology 2003, 50:911-929.
12. Fong R.N., Kim K.S., Yoshihara C., Inwood W.B., Kustu S. The W148L substitution in the Escherichia coli ammonium channel AmtB increases flux and indicates that the substrate is an ion. Proceedings National Academy Sciences of the United States of America 2007, 104:18706-18711.
13. Gimeno C.J., Ljungdahl P.O., Styles C.A., Fink G.R. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 1992, 68:1077-1090.
14. Giots F., Donaton M.C., Thevelein J.M. Inorganic phosphate is sensed by specific phosphate carriers and acts in concert with glucose as a nutrient signal for activation of the protein kinase A pathway in the yeast Saccharomyces cerevisiae. Molecular Microbiology 2003, 47:1163-1181.
15. Graden J.A., Winge D.R. Copper-mediated repression of the activation domain in the yeast Mac1p transcription factor. Proceedings National Academy Sciences of the United States of America 1997, 94:5550-5555.
16. Gross C., Kelleher M., Iyer V.R., Brown P.O., Winge D.R. Identification of the copper regulon in Saccharomyces cerevisiae by DNA microarrays. The Journal of Biological Chemistry 2000, 275:32310-32316.
17. Haurie V., Boucherie H., Sagliocco F. The Snf1 protein kinase controls the induction of genes of the iron uptake pathway at the diauxic shift in Saccharomyces cerevisiae. The Journal of Biological Chemistry 2003, 278:45391-45396.
18. Heredia J., Crooks M., Zhu Z. Phosphorylation and Cu+ coordination-dependent DNA binding of the transcription factor Mac1p in the regulation of copper transport. The Journal of Biological Chemistry 2001, 276:8793-8797.
19. Hinnebusch A.G. Translational regulation of GCN4 and the general amino acid control of yeast. Annual Review of Microbiology 2005, 59:407-450.
20. Inwood W.B., Hall J.A., Kim K.S., Fong R., Kustu S. Genetic evidence for an essential oscillation of transmembrane-spanning segment 5 in the Escherichia coli ammonium channel AmtB. Genetics 2009, 183:1341-1355.
21. Jamison McDaniels C.P., Jensen L.T., Srinivasan C., Winge D.R., Tullius T.D. The yeast transcription factor Mac1 binds to DNA in a modular fashion. The Journal of Biological Chemistry 1999, 274:26962-26967.
22. Javelle A., Lupo D., Zheng L., Li X.D., Winkler F.K., Merrick M. An unusual twin-his arrangement in the pore of ammonia channels is essential for substrate conductance. The Journal of Biological Chemistry 2006, 281:39492-39498.
23. Javelle A., Lupo D., Ripoche P., Fulford T., Merrick M., Winkler F.K. Substrate binding, deprotonation, and selectivity at the periplasmic entrance of the Escherichia coli ammonia channel AmtB. Proceedings National Academy Sciences of the United States of America 2008, 105:5040-5045.
24. Jensen L.T., Winge D.R. Identification of a copper-induced intramolecular interaction in the transcription factor Mac1 from Saccharomyces cerevisiae. EMBO Journal 1998, 17:5400-5408.
25. Jensen L.T., Posewitz M.C., Srinivasan C., Winge D.R. Mapping of the DNA binding domain of the copper-responsive transcription factor Mac1 from Saccharomyces cerevisiae. The Journal of Biological Chemistry 1998, 273:23805-23811.
26. Joshi A., Serpe M., Kosman D.J. Evidence for (Mac1p)2 DNA ternary complex formation in Mac1p-dependent transactivation at the CTR1 promoter. The Journal of Biological Chemistry 1999, 274:218-226.
27. Jungmann J., Reins H.A., Lee J., Romeo A., Hassett R., Kosman D., Jentsch S. MAC1, a nuclear regulatory protein related to Cu-dependent transcription factors is involved in Cu/Fe utilization and stress resistance in yeast. EMBO Journal 1993, 12:5051-5056.
28. Keller G., Gross C., Kelleher M., Winge D.R. Functional independence of the two cysteine-rich activation domains in the yeast Mac1 transcription factor. The Journal of Biological Chemistry 2000, 275:29193-29199.
29. Keller G., Bird A., Winge D.R. Independent metalloregulation of Ace1 and Mac1 in Saccharomyces cerevisiae. Eukaryotic Cell 2005, 4:1863-1871.
30. Khademi S., O'Connell J., Remis J., Robles-Colmenares Y., Miercke L.J., Stroud R.M. Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 Å. Science 2004, 305:1587-1594.
31. Labbé S., Zhu Z., Thiele D.J. Copper-specific transcriptional repression of yeast genes encoding critical components in the copper transport pathway. The Journal of Biological Chemistry 1997, 272:15951-15958.
32. Labbé S., Peña M.M., Fernandes A.R., Thiele D.J. A copper-sensing transcription factor regulates iron uptake genes in Schizosaccharomyces pombe. The Journal of Biological Chemistry 1999, 274:36252-36260.
33. Lamoureux G., Javelle A., Baday S., Wang S., Bernèche S. Transport mechanisms in the ammonium transporter family. Transfusion Clinique et Biologique 2010, 17:168-175.
34. Lin Y., Cao Z., Mo Y. Molecular dynamics simulations on the Escherichia coli ammonia channel protein AmtB: mechanism of ammonia/ammonium transport. Journal American Chemical Society 2006, 128:10876-10884.
35. Lorenz M.C., Heitman J. The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae. EMBO Journal 1998, 17:1236-1247.
36. Marini A.M., Soussi-Boudekou S., Vissers S., André B. A family of ammonium transporters in Saccharomyces cerevisiae. Molecular Biology of the Cell 1997, 17:4282-4293.
37. Marini A.M., Boeckstaens M., Benjelloun F., Chérif-Zahar B., André B. Structural involvement in substrate recognition of an essential aspartate residue conserved in Mep/Amt and Rh-type ammonium transporters. Current Genetics 2006, 49:364-374.
38. Mayer M., Dynowski M., Ludewig U. Ammonium ion transport by the AMT/Rh homologue LeAMT1;1. Biochemistry Journal 2006, 396:431-437.
39. Mihlan M., Homann V., Liu T.W., Tudzynski B. AREA directly mediates nitrogen regulation of gibberellin biosynthesis in Gibberella fujikuroi, but its activity is not affected by NMR. Molecular Microbiology 2003, 47:975-991.
40. Nygaard T.P., Rovira C., Peters G.H., Jensen M.Ø. Ammonium recruitment and ammonia transport by E. coli ammonia channel AmtB. Biophysical Journal 2006, 91:4401-4412.
41. Rutherford J.C., Jaron S., Ray E., Brown P.O., Winge D.R. A second iron-regulatory system in yeast independent of Aft1p. Proceedings National Academy Sciences of the United States of America 2001, 98:14322-14327.
42. Rutherford J.C., Lin X., Nielsen K., Heitman J. Amt2 permease is required to induce ammonium-responsive invasive growth and mating in Cryptococcus neoformans. Eukaryotic Cell 2008, 7:237-246.
43. Rutherford J.C., Chua G., Hughes T., Cardenas M.E., Heitman J. A Mep2-dependent transcriptional profile links permease function to gene expression during pseudohyphal growth in Saccharomyces cerevisiae. Molecular Biology of the Cell 2008, 19:3028-3039.
44. Serpe M., Joshi A., Kosman D.J. Structure-function analysis of the protein-binding domains of Mac1p, a copper-dependent transcriptional activator of copper uptake in Saccharomyces cerevisiae. The Journal of Biological Chemistry 1999, 274:9211-9219.
45. Smith D.G., Garcia-Pedrajas M.D., Gold S.E., Perlin M.H. Isolation and characterization from pathogenic fungi of genes encoding ammonium permeases and their roles in dimorphism. Molecular Microbiology 2003, 50:259-275.
46. Teichert S., Rutherford J.C., Wottawa M., Heitman J., Tudzynski B. Impact of ammonium permeases mepA, mepB, and mepC on nitrogen-regulated secondary metabolism in Fusarium fujikuroi. Eukaryotic Cell 2008, 7:187-201.
47. Thevelein J.M., Voordeckers K. Functioning and evolutionary significance of nutrient transceptors. Molecular Biology and Evolution 2009, 26:2407-2414.
48. Van Nuland A., Vandormael P., Donaton M., Alenquer M., Lourenço A., Quintino E., Versele M., Thevelein J.M. Ammonium permease based sensing mechanism for rapid ammonium activation of the protein kinase A pathway in yeast. Molecular Microbiology 2006, 59:1485-1505.
49. Voutsina A., Fragiadakis G.S., Boutla A., Alexandraki D. The second cysteine-rich domain of Mac1p is a potent transactivator that modulates DNA binding efficiency and functionality of the protein. FEBS Letters 2001, 494:38-43.
50. Wilkinson B.M., James C.M., Walmsley R.M. Partial deletion of the Saccharomyces cerevisiae GDH3 gene results in novel starvation phenotypes. Microbiology 1996, 142:1667-1673.
51. Wegner S.V., Sun F., Hernandez N., He C. The tightly regulated copper window in yeast. Chemical Communications 2011, 47:2571-2573.
52. Wood L.K., Thiele D.J. Transcriptional activation in yeast in response to copper deficiency involves copper-zinc superoxide dismutase. The Journal of Biological Chemistry 2009, 284:404-413.
53. Yamaguchi-Iwai Y., Dancis A., Klausner R.D. AFT1: a mediator of iron regulated transcriptional control in Saccharomyces cerevisiae. EMBO Journal 1995, 14:1231-1239.
54. Yamaguchi-Iwai Y., Serpe M., Haile D., Yang W., Kosman D.J., Klausner R.D., Dancis A. Homeostatic regulation of copper uptake in yeast via direct binding of MAC1 protein to upstream regulatory sequences of FRE1 and CTR1. The Journal of Biological Chemistry 1997, 272:17711-17718.
55. Zhao H., Eide D.J. Zap1p, a metalloregulatory protein involved in zinc-responsive transcriptional regulation in Saccharomyces cerevisiae. Molecular and Cellular Biology 1997, 17:5044-5052.
56. Zheng L., Kostrewa D., Bernèche S., Winkler F.K., Li X.D. The mechanism of ammonia transport based on the crystal structure of AmtB of Escherichia coli. Proceedings National Academy Sciences of the United States of America 2004, 101:17090-17095.
57. Zhu Z., Labbé S., Peña M.M., Thiele D.J. Copper differentially regulates the activity and degradation of yeast Mac1 transcription factor. The Journal of Biological Chemistry 1998, 273:1277-1280.
58. Zurita-Martinez S.A., Puria R., Pan X., Boeke J.D., Cardenas M.E. Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae. Genetics 2007, 176:2139-2150.