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Biochem J. 2001 Feb 1; 353(Pt 3): 681–688.
PMCID: PMC1221615

Multiple polyamine transport systems on the vacuolar membrane in yeast.


We recently identified a gene (TPO1, YLL028w) that encodes a polyamine transport protein on the vacuolar membrane in yeast [Tomitori, Kashiwagi, Sakata, Kakinuma and Igarashi (1999) J. Biol. Chem. 274, 3265-3267]. Because the existence of one or more other genes for a polyamine transport protein on the vacuolar membrane was expected, we searched sequence databases for homologues of the protein encoded by TPO1. Membrane proteins encoded by the open reading frames YGR138c (TPO2), YPR156c (TPO3) and YOR273c (TPO4) were postulated to be polyamine transporters and, indeed, were subsequently shown to be polyamine transport proteins on the vacuolar membrane. Cells overexpressing these genes were resistant to polyamine toxicity and showed an increase in polyamine uptake activity and polyamine content in vacuoles. Furthermore, cells in which these genes were disrupted showed an increased sensitivity to polyamine toxicity and a decrease in polyamine uptake activity and polyamine content in vacuoles. Resistance to polyamine toxicity in cells overexpressing the genes was overcome by bafilomycin A(1), an inhibitor of the vacuolar H(+)-ATPase. Among the four polyamine transporters, those encoded by TPO2 and TPO3 were specific for spermine, whereas those encoded by TPO1 and TPO4 recognized spermidine and spermine. These results suggest that polyamine content in the cytoplasm of yeast is elaborately regulated by several polyamine transport systems in vacuoles. Furthermore, it was shown that Glu-207, Glu-324 (or Glu-323) and Glu-574 of TPO1 protein were important for the transport activity.

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Selected References

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  • Tabor CW, Tabor H. Polyamines. Annu Rev Biochem. 1984;53:749–790. [PubMed]
  • Kashiwagi K, Hosokawa N, Furuchi T, Kobayashi H, Sasakawa C, Yoshikawa M, Igarashi K. Isolation of polyamine transport-deficient mutants of Escherichia coli and cloning of the genes for polyamine transport proteins. J Biol Chem. 1990 Dec 5;265(34):20893–20897. [PubMed]
  • Ames GF. Bacterial periplasmic transport systems: structure, mechanism, and evolution. Annu Rev Biochem. 1986;55:397–425. [PubMed]
  • Higgins CF. The ABC of channel regulation. Cell. 1995 Sep 8;82(5):693–696. [PubMed]
  • Igarashi K, Kashiwagi K. Polyamine transport in bacteria and yeast. Biochem J. 1999 Dec 15;344(Pt 3):633–642. [PMC free article] [PubMed]
  • Kashiwagi K, Suzuki T, Suzuki F, Furuchi T, Kobayashi H, Igarashi K. Coexistence of the genes for putrescine transport protein and ornithine decarboxylase at 16 min on Escherichia coli chromosome. J Biol Chem. 1991 Nov 5;266(31):20922–20927. [PubMed]
  • Kashiwagi K, Miyamoto S, Suzuki F, Kobayashi H, Igarashi K. Excretion of putrescine by the putrescine-ornithine antiporter encoded by the potE gene of Escherichia coli. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4529–4533. [PMC free article] [PubMed]
  • Kashiwagi K, Shibuya S, Tomitori H, Kuraishi A, Igarashi K. Excretion and uptake of putrescine by the PotE protein in Escherichia coli. J Biol Chem. 1997 Mar 7;272(10):6318–6323. [PubMed]
  • Kakinuma Y, Maruyama T, Nozaki T, Wada Y, Ohsumi Y, Igarashi K. Cloning of the gene encoding a putative serine/threonine protein kinase which enhances spermine uptake in Saccharomyces cerevisiae. Biochem Biophys Res Commun. 1995 Nov 22;216(3):985–992. [PubMed]
  • Nozaki T, Nishimura K, Michael AJ, Maruyama T, Kakinuma Y, Igarashi K. A second gene encoding a putative serine/threonine protein kinase which enhances spermine uptake in Saccharomyces cerevisiae. Biochem Biophys Res Commun. 1996 Nov 12;228(2):452–458. [PubMed]
  • Kaouass M, Audette M, Ramotar D, Verma S, De Montigny D, Gamache I, Torossian K, Poulin R. The STK2 gene, which encodes a putative Ser/Thr protein kinase, is required for high-affinity spermidine transport in Saccharomyces cerevisiae. Mol Cell Biol. 1997 Jun;17(6):2994–3004. [PMC free article] [PubMed]
  • Kaouass M, Gamache I, Ramotar D, Audette M, Poulin R. The spermidine transport system is regulated by ligand inactivation, endocytosis, and by the Npr1p Ser/Thr protein kinase in Saccharomyces cerevisiae. J Biol Chem. 1998 Jan 23;273(4):2109–2117. [PubMed]
  • Woolridge DP, Vazquez-Laslop N, Markham PN, Chevalier MS, Gerner EW, Neyfakh AA. Efflux of the natural polyamine spermidine facilitated by the Bacillus subtilis multidrug transporter Blt. J Biol Chem. 1997 Apr 4;272(14):8864–8866. [PubMed]
  • Tomitori H, Kashiwagi K, Sakata K, Kakinuma Y, Igarashi K. Identification of a gene for a polyamine transport protein in yeast. J Biol Chem. 1999 Feb 5;274(6):3265–3267. [PubMed]
  • Goffeau A, Park J, Paulsen IT, Jonniaux JL, Dinh T, Mordant P, Saier MH., Jr Multidrug-resistant transport proteins in yeast: complete inventory and phylogenetic characterization of yeast open reading frames with the major facilitator superfamily. Yeast. 1997 Jan;13(1):43–54. [PubMed]
  • Maruyama T, Masuda N, Kakinuma Y, Igarashi K. Polyamine-sensitive magnesium transport in Saccharomyces cerevisiae. Biochim Biophys Acta. 1994 Sep 14;1194(2):289–295. [PubMed]
  • Hill JE, Myers AM, Koerner TJ, Tzagoloff A. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast. 1986 Sep;2(3):163–167. [PubMed]
  • Ito H, Fukuda Y, Murata K, Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. [PMC free article] [PubMed]
  • Joho M, Ishikawa Y, Kunikane M, Inouhe M, Tohoyama H, Murayama T. The subcellular distribution of nickel in Ni-sensitive and Ni-resistant strains of Saccharomyces cerevisiae. Microbios. 1992;71(287):149–159. [PubMed]
  • Igarashi K, Kashiwagi K, Hamasaki H, Miura A, Kakegawa T, Hirose S, Matsuzaki S. Formation of a compensatory polyamine by Escherichia coli polyamine-requiring mutants during growth in the absence of polyamines. J Bacteriol. 1986 Apr;166(1):128–134. [PMC free article] [PubMed]
  • LOWRY OH, ROSEBROUGH NJ, FARR AL, RANDALL RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed]
  • Suzuki T, Sadakata Y, Kashiwagi K, Hoshino K, Kakinuma Y, Shirahata A, Igarashi K. Overproduction of S-adenosylmethionine decarboxylase in ethylglyoxal-bis(guanylhydrazone)-resistant mouse FM3A cells. Eur J Biochem. 1993 Jul 15;215(2):247–253. [PubMed]
  • Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. [PMC free article] [PubMed]
  • Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. [PubMed]
  • Bowman EJ, Siebers A, Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7972–7976. [PMC free article] [PubMed]
  • Kakinuma Y, Masuda N, Igarashi K. Proton potential-dependent polyamine transport by vacuolar membrane vesicles of Saccharomyces cerevisiae. Biochim Biophys Acta. 1992 Jun 11;1107(1):126–130. [PubMed]
  • Hashimoto Y, Soderling TR. Regulation of calcineurin by phosphorylation. Identification of the regulatory site phosphorylated by Ca2+/calmodulin-dependent protein kinase II and protein kinase C. J Biol Chem. 1989 Oct 5;264(28):16524–16529. [PubMed]
  • Kashiwagi K, Kuraishi A, Tomitori H, Igarashi A, Nishimura K, Shirahata A, Igarashi K. Identification of the putrescine recognition site on polyamine transport protein PotE. J Biol Chem. 2000 Nov 17;275(46):36007–36012. [PubMed]

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