Nitrogen coordinated import and export of arginine across the yeast vacuolar membrane

English version

Autoři: Melody Cools ^aff001; Simon Lissoir ^aff001; Elisabeth Bodo ^aff003; Judith Ulloa-Calzonzin ^aff004; Alexander DeLuna ^aff004; Isabelle Georis ^aff002; Bruno André ^aff001
Působiště autorů: Molecular Physiology of the Cell, Université Libre de Bruxelles (ULB), Biopark, Gosselies, Belgium ^aff001; Métabolisme des micro-organismes modèles, LABIRIS, Brussels, Belgium ^aff002; Développement des bioprocédés et microbiologie appliquée, LABIRIS, Brussels, Belgium ^aff003; Unidad de Genómica Avanzada (Langebio), Centro de Investigación y de Estudios Avanzados del IPN, Irapuato, Guanajuato, Mexico ^aff004
Vyšlo v časopise: Nitrogen coordinated import and export of arginine across the yeast vacuolar membrane. PLoS Genet 16(8): e32767. doi:10.1371/journal.pgen.1008966
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008966

Souhrn

The vacuole of the yeast Saccharomyces cerevisiae plays an important role in nutrient storage. Arginine, in particular, accumulates in the vacuole of nitrogen-replete cells and is mobilized to the cytosol under nitrogen starvation. The arginine import and export systems involved remain poorly characterized, however. Furthermore, how their activity is coordinated by nitrogen remains unknown. Here we characterize Vsb1 as a novel vacuolar membrane protein of the APC (amino acid-polyamine-organocation) transporter superfamily which, in nitrogen-replete cells, is essential to active uptake and storage of arginine into the vacuole. A shift to nitrogen starvation causes apparent inhibition of Vsb1-dependent activity and mobilization of stored vacuolar arginine to the cytosol. We further show that this arginine export involves Ypq2, a vacuolar protein homologous to the human lysosomal cationic amino acid exporter PQLC2 and whose activity is detected only in nitrogen-starved cells. Our study unravels the main arginine import and export systems of the yeast vacuole and suggests that they are inversely regulated by nitrogen.

Klíčová slova:

Arginine – Cytosol – Lysosomes – Phenotypes – Vacuoles – Vesicles – Yeast – Radiolabeling

Zdroje

1. Li SC, Kane PM. The yeast lysosome-like vacuole: Endpoint and crossroads. Biochim Biophys Acta—Mol Cell Res. 2009;1793 : 650–663. doi: 10.1016/j.bbamcr.2008.08.003 18786576

2. Reggiori F, Klionsky DJ. Autophagic processes in yeast: Mechanism, machinery and regulation. Genetics. 2013;194 : 341–361. doi: 10.1534/genetics.112.149013 23733851

3. Winchester B, Vellodi A, Young E. The molecular basis of lysosomal storage diseases and their treatment. Biochem Soc Trans. 2000;28 : 150–154. doi: 10.1042/bst0280150 10816117

4. Town M, Jean G, Cherqui S, Attard M, Forestier L, Whitmore SA, et al. A novel gene encoding an integral membrane protein is mutated in nephropathic cystinosis. Nat Genet. 1998;18 : 319–24. doi: 10.1038/ng0498-319 9537412

5. Jezegou A, Llinares E, Anne C, Kieffer-Jaquinod S, O’Regan S, Aupetit J, et al. Heptahelical protein PQLC2 is a lysosomal cationic amino acid exporter underlying the action of cysteamine in cystinosis therapy. Proc Natl Acad Sci. 2012;109: E3434–E3443. doi: 10.1073/pnas.1211198109 23169667

6. Llinares E, Barry AO, André B. The AP-3 adaptor complex mediates sorting of yeast and mammalian PQ-loop-family basic amino acid transporters to the vacuolar/lysosomal membrane. Sci Rep. 2015;5 : 16665. doi: 10.1038/srep16665 26577948

7. Sekito T, Nakamura K, Manabe K, Tone J, Sato Y, Murao N, et al. Loss of ATP-dependent lysine uptake in the vacuolar membrane vesicles of Saccharomyces cerevisiae ypq1Δ mutant. Biosci Biotechnol Biochem. 2014;78 : 1199–202. doi: 10.1080/09168451.2014.918489 25229858

8. Manabe K, Kawano-Kawada M, Ikeda K, Sekito T, Kakinuma Y. Ypq3p-dependent histidine uptake by the vacuolar membrane vesicles of Saccharomyces cerevisiae. Biosci Biotechnol Biochem. 2016;80 : 1125–30. doi: 10.1080/09168451.2016.1141041 26928127

9. Kawano-Kawada M, Manabe K, Ichimura H, Kimura T, Harada Y, Ikeda K, et al. A PQ-loop protein Ypq2 is involved in the exchange of arginine and histidine across the vacuolar membrane of Saccharomyces cerevisiae. Sci Rep. 2019;9 : 15018. doi: 10.1038/s41598-019-51531-z 31636363

10. Li M, Rong Y, Chuang Y-S, Peng D, Emr SD. Ubiquitin-dependent lysosomal membrane protein sorting and degradation. Mol Cell. 2015;57 : 467–478. doi: 10.1016/j.molcel.2014.12.012 25620559

11. Zhu L, Jorgensen JR, Li M, Chuang YS, Emr SD. ESCRTS function directly on the lysosome membrane to downregulate ubiquitinated lysosomal membrane proteins. Elife. 2017;6 : 1–20. doi: 10.7554/eLife.26403 28661397

12. Boller T, Dürr M, Wiemken A. Characterization of a specific transport system for arginine in isolated yeast vacuoles. Eur J Biochem. 1975;54 : 81–91. doi: 10.1111/j.1432-1033.1975.tb04116.x 238849

13. Shimazu M, Sekito T, Akiyama K, Ohsumi Y, Kakinuma Y. A family of basic amino acid transporters of the vacuolar membrane from Saccharomyces cerevisiae. J Biol Chem. 2005;280 : 4851–7. doi: 10.1074/jbc.M412617200 15572352

14. Sekito T, Chardwiriyapreecha S, Sugimoto N, Ishimoto M, Kawano-Kawada M, Kakinuma Y. Vacuolar transporter Avt4 is involved in excretion of basic amino acids from the vacuoles of Saccharomyces cerevisiae. Biosci Biotechnol Biochem. 2014;78 : 969–975. doi: 10.1080/09168451.2014.910095 25036121

15. Russnak R, Konczal D, McIntire SL. A family of yeast proteins mediating bidirectional vacuolar amino acid transport. J Biol Chem. 2001;276 : 23849–57. doi: 10.1074/jbc.M008028200 11274162

16. Tone J, Yoshimura A, Manabe K, Murao N, Sekito T, Kawano-Kawada M, et al. Characterization of Avt1p as a vacuolar proton/amino acid antiporter in Saccharomyces cerevisiae. Biosci Biotechnol Biochem. 2015;79 : 782–789. doi: 10.1080/09168451.2014.998621 25747199

17. Messenguy F, Colin D, ten Have JP. Regulation of compartmentation of amino acid pools in Saccharomyces cerevisiae and its effects on metabolic control. Eur J Biochem. 1980;108 : 439–47. doi: 10.1111/j.1432-1033.1980.tb04740.x 6997042

18. Ohsumi Y, Kitamoto K, Anraku Y. Changes induced in the permeability barrier of the yeast plasma membrane by cupric ion. J Bacteriol. 1988;170 : 2676–82. doi: 10.1128/jb.170.6.2676-2682.1988 3286617

19. Dürr M, Urech K, Boller T, Wiemken A, Schwencke J, Nagy M. Sequestration of arginine by polyphosphate in vacuoles of yeast (Saccharomyces cerevisiae). Arch Microbiol. 1979;121 : 169–175. doi: 10.1007/BF00689982

20. Hothorn M, Neumann H, Lenherr ED, Wehner M, Rybin V, Hassa PO, et al. Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science. 2009;324 : 513–516. doi: 10.1126/science.1168120 19390046

21. Urech K, Dürr M, Boller T, Wiemken A, Schwencke J. Localization of polyphosphate in vacuoles of Saccharomyces cerevisiae. Arch Microbiol. 1978;116 : 275–278. doi: 10.1007/BF00417851 348146

22. Okorokov LA, Lichko LP, Kulaev IS. Vacuoles: main compartments of potassium, magnesium, and phosphate ions in Saccharomyces carlsbergenis cells. J Bacteriol. 1980;144 : 661–5. doi: 10.1128/JB.144.2.661-665.1980 7430066

23. Stawiecka-Mirota M, Pokrzywa W, Morvan J, Zoladek T, Haguenauer-Tsapis R, Urban-Grimal D, et al. Targeting of Sna3p to the endosomal pathway depends on its interaction with Rsp5p and multivesicular body sorting on its ubiquitylation. Traffic. 2007;8 : 1280–1296. doi: 10.1111/j.1600-0854.2007.00610.x 17645729

24. De Block J, Szopinska A, Guerriat B, Dodzian J, Villers J, Hochstenbach J-F, et al. Yeast Pmp3p has an important role in plasma membrane organization. J Cell Sci. 2015;128 : 3646–3659. doi: 10.1242/jcs.173211 26303201

25. Cabrera M, Ungermann C. Purification and in vitro analysis of yeast vacuoles. 1st ed. Methods in Enzymology. 1st ed. 2008. pp. 177–96. doi: 10.1016/S0076-6879(08)03213-8

26. Tarsio M, Zheng H, Smardon AM, Martínez-Muñoz GA, Kane PM. Consequences of loss of Vph1 protein-containing vacuolar ATPases (V-ATPases) for overall cellular pH homeostasis. J Biol Chem. 2011;286 : 28089–28096. doi: 10.1074/jbc.M111.251363 21669878

27. Boller T, Dürr M, Wiemken A. Transport in isolated yeast vacuoles: Characterization of arginine permease. Methods in Enzymology. 1989. pp. 504–518. doi: 10.1016/0076-6879(89)74034-9 2698990

28. Ohsumi Y, Anraku Y. Active transport of basic amino acids driven by a proton motive force in vacuolar membrane vesicles of Saccharomyces cerevisiae. J Biol Chem. 1981;256 : 2079–82. 6450764

29. Kitamoto K, Yoshizawa K, Ohsumi Y, Anraku Y. Dynamic aspects of vacuolar and cytosolic amino acid pools of Saccharomyces cerevisiae. J Bacteriol. 1988;170 : 2683–6. doi: 10.1128/jb.170.6.2683-2686.1988 3131304

30. Gerasimaité R, Sharma S, Desfougeres Y, Schmidt A, Mayer A. Coupled synthesis and translocation restrains polyphosphate to acidocalcisome-like vacuoles and prevents its toxicity. J Cell Sci. 2014;127 : 5093–5104. doi: 10.1242/jcs.159772 25315834

31. Mülleder M, Calvani E, Alam MT, Wang RK, Eckerstorfer F, Zelezniak A, et al. Functional metabolomics describes the yeast biosynthetic regulome. Cell. 2016;167 : 553–565.e12. doi: 10.1016/j.cell.2016.09.007 27693354

32. Brohée S, Barriot R, Moreau Y, André B. YTPdb: a wiki database of yeast membrane transporters. Biochim Biophys Acta. 2010;1798 : 1908–12. doi: 10.1016/j.bbamem.2010.06.008 20599686

33. Cherest H, Davidian JC, Thomas D, Benes V, Ansorge W, Surdin-Kerjan Y. Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae. Genetics. 1997;145 : 627–35. doi: 10.1515/BC.2011.017 9055073

34. Wiederhold E, Gandhi T, Permentier HP, Breitling R, Poolman B, Slotboom DJ. The yeast vacuolar membrane proteome. Mol Cell Proteomics. 2009;8 : 380–92. doi: 10.1074/mcp.M800372-MCP200 19001347

35. Gournas C, Saliba E, Krammer E-M, Barthelemy C, Prévost M, André B. Transition of yeast Can1 transporter to the inward-facing state unveils an α-arrestin target sequence promoting its ubiquitylation and endocytosis. Mol Biol Cell. 2017;28 : 2819–2832. doi: 10.1091/mbc.E17-02-0104 28814503

36. Ghaddar K, Merhi A, Saliba E, Krammer E-M, Prévost M, André B. Substrate-induced ubiquitylation and endocytosis of yeast amino acid permeases. Mol Cell Biol. 2014;34 : 4447–63. doi: 10.1128/MCB.00699-14 25266656

37. Wiemken A, Nurse P. Isolation and characterization of the amino-acid pools located within the cytoplasm and vacuoles of Candida utilis. Planta. 1973;109 : 293–306. doi: 10.1007/BF00387098 24474206

38. Cools M, Rompf M, Mayer A, André B. Measuring the activity of plasma membrane and vacuolar transporters in yeast. Yeast Systems Biology 2nd edition. 2019. pp. 247–261. doi: 10.1007/978-1-4939-9736-7_15 31602616

39. Oku M, Maeda Y, Kagohashi Y, Kondo T, Yamada M, Fujimoto T, et al. Evidence for ESCRT -⁠ and clathrin-dependent microautophagy. J Cell Biol. 2017;216 : 3263–3274. doi: 10.1083/jcb.201611029 28838958

40. McNally EK, Karim MA, Brett CL. Selective lysosomal transporter degradation by organelle membrane fusion. Dev Cell. 2017;40 : 151–167. doi: 10.1016/j.devcel.2016.11.024 28017618

41. Li M, Koshi T, Emr SD. Membrane-anchored ubiquitin ligase complex is required for the turnover of lysosomal membrane proteins. J Cell Biol. 2015;211 : 639–652. doi: 10.1083/jcb.201505062 26527740

42. Liu B, Du H, Rutkowski R, Gartner A, Wang X. LAAT-1 is the lysosomal lysine/arginine transporter that maintains amino acid homeostasis. Science. 2012;337 : 351–4. doi: 10.1126/science.1220281 22822152

43. Guan L, Kaback HR. Lessons from lactose permease. Annu Rev Biophys Biomol Struct. 2006;35 : 67–91. doi: 10.1146/annurev.biophys.35.040405.102005 16689628

44. Pisoni RL, Thoene JG, Christensen HN. Detection and characterization of carrier-mediated cationic amino acid transport in lysosomes of normal and cystinotic human fibroblasts. Role in therapeutic cystine removal? J Biol Chem. 1985;260 : 4791–8. 3921538

45. Pisoni RL, Thoene JG, Lemons RM, Christensen HN. Important differences in cationic amino acid transport by lysosomal system c and system y+ of the human fibroblast. J Biol Chem. 1987;262 : 15011–8. 3499437

46. Amick J, Tharkeshwar AK, Talaia G, Ferguson SM. PQLC2 recruits the C9orf72 complex to lysosomes in response to cationic amino acid starvation. J Cell Biol. 2020;219 : 1–30. doi: 10.1083/jcb.201906076 31851326

47. Bechet J, Greenson M, Wiame JM. Mutations affecting the repressibility of arginine biosynthetic enzymes in Saccharomyces cerevisiae. Eur J Biochem. 1970;12 : 31–9. doi: 10.1111/j.1432-1033.1970.tb00817.x 5434281

48. Grenson M, Acheroy B. Mutations affecting the activity and the regulation of the general amino-acid permease of Saccharomyces cerevisiae. Mol Gen Genet. 1982;188 : 261–265. doi: 10.1007/BF00332685 6759873

49. Garay E, Campos SE, González de la Cruz J, Gaspar AP, Jinich A, DeLuna A. High-resolution profiling of stationary-phase survival reveals yeast longevity factors and their genetic interactions. PLoS Genet. 2014;10. doi: 10.1371/journal.pgen.1004168 24586198

50. Ghaddar K, Krammer EM, Mihajlovic N, Brohée S, André B, Prévost M. Converting the yeast arginine Can1 permease to a lysine permease. J Biol Chem. 2014;289 : 7232–7246. doi: 10.1074/jbc.M113.525915 24448798

51. Fayyad-Kazan M, Feller A, Bodo E, Boeckstaens M, Marini AM, Dubois E, et al. Yeast nitrogen catabolite repression is sustained by signals distinct from glutamine and glutamate reservoirs. Mol Microbiol. 2016;99 : 360–379. doi: 10.1111/mmi.13236 26419331

52. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: An open-source platform for biological-image analysis. Nat Methods. 2012;9 : 676–682. doi: 10.1038/nmeth.2019 22743772

53. Vida TA, Emr SD. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol. 1995;128 : 779–792. doi: 10.1083/jcb.128.5.779 7533169

54. Orij R, Postmus J, Beek A Ter, Brul S, Smits GJ. In vivo measurement of cytosolic and mitochondrial pH using a pH-sensitive GFP derivative in Saccharomyces cerevisiae reveals a relation between intracellular pH and growth. Microbiology. 2009;155 : 268–278. doi: 10.1099/mic.0.022038-0 19118367

55. Zimmermannova O, Salazar A, Sychrova H, Ramos J. Zygosaccharomyces rouxii Trk1 is an efficient potassium transporter providing yeast cells with high lithium tolerance. FEMS Yeast Res. 2015;15 : 1–11. doi: 10.1093/femsyr/fov029 26019147

56. Saliba E, Evangelinos M, Gournas C, Corrillon F, Georis I, André B. The yeast H+-ATPase Pma1 promotes Rag/Gtr-dependent TORC1 activation in response to H+-coupled nutrient uptake. Elife. 2018;7: e31981. doi: 10.7554/eLife.31981 29570051

Článek Immediate activation of chemosensory neuron gene expression by bacterial metabolites is selectively induced by distinct cyclic GMP-dependent pathways in Caenorhabditis elegans

Článek Gα/GSA-1 works upstream of PKA/KIN-1 to regulate calcium signaling and contractility in the Caenorhabditis elegans spermatheca

Článek Mutation of CFAP57, a protein required for the asymmetric targeting of a subset of inner dynein arms in Chlamydomonas, causes primary ciliary dyskinesia

Článek Transcriptional regulators of the Golli/myelin basic protein locus integrate additive and stealth activities

Článek DAnkrd49 and Bdbt act via Casein kinase Iε to regulate planar polarity in Drosophila

Článek Mapping gene flow between ancient hominins through demography-aware inference of the ancestral recombination graph

Článek Endogenization and excision of human herpesvirus 6 in human genomes

Článek A subset of broadly responsive Type III taste cells contribute to the detection of bitter, sweet and umami stimuli

Článek How many familial relationship testing results could be wrong?

Článek Long noncoding RNA functionality in imprinted domain regulation

Článek A point mutation decouples the lipid transfer activities of microsomal triglyceride transfer protein

Článek Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69