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Volume 152, Issue 8

A survey of all 11 ABC transporters in fission yeast: two novel ABC transporters are required for red pigment accumulation in a adenine biosynthetic mutant Free

Abstract

ATP-binding cassette (ABC) proteins transport a wide variety of substrates, including sugars, amino acids, metal ions, lipids, peptides and proteins, across membranes, and most ABC proteins contain transmembrane domains (ABC transporters). Sequencing of the genome has allowed identification of all genes encoding ABC transporters in fission yeast. To date, six such genes have been characterized, and an additional five genes encoding ABC transporters were identified from the genome sequence. In an attempt to characterize all of the ABC transporters in fission yeast, all 11 genes were disrupted. While all the genes were found to be dispensable for cell viability, some disruptants lacked apparent phenotypes. GFP-tagged ABC transporters were localized to membranes as follows: plasma membrane (2), vacuolar membrane (4), mitochondrial membrane (2), endoplasmic reticulum membrane (2), and endosome and Golgi membranes (1). Two Cluster II. 1 proteins, Abc2p (SPAC3F10.11c) and Abc4p (SPAC30.04c), were found to be localized to vacuolar membranes, and to be responsible for accumulation of a characteristic red pigment in the vacuole of an adenine biosynthetic mutant. The doubly disrupted mutant Δ Δ exhibited drug sensitivity, and a decreased accumulation of monochlorobimane, suggesting that both of the proteins encoded by these genes are involved in detoxification of xenobiotics, and vacuolar sequestration of glutathione -conjugates.

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Keyword(s): 4-NQO, 4-nitroquinoline oxide , ABC, ATP-binding cassette , BfA, brefeldin A , CHX, cycloheximide , ER, endoplasmic reticulum , GS-X pump, glutathione S-conjugate transporting ATPase , GS-X, glutathione S-conjugate , MClB, monochlorobimane , NBD, nucleotide-binding domain , TMD, transmembrane domain and V-ATPase, V-type ATPase
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2006-08-01
2024-04-25
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References

  1. Balakrishnan L, Venter H, Shilling R. A, van Veen H. W. 2004; Reversible transport by the ATP-binding cassette multidrug export pump LmrA. ATP synthesis at the expense of downhill ethidium uptake. J Biol Chem 279:11273–11280 [CrossRef]
     [Google Scholar]
  2. Bauer B. E, Wolfger H, Kuchler K. 1999; Inventory and function of yeast ABC proteins: about sex, stress, pleiotropic drug and heavy metal resistance. Biochim Biophys Acta 1461217–236 [CrossRef]
     [Google Scholar]
  3. Bresnahan P. A, Barber L. D, Brodsky F. M. 1997; Localization of class I histocompatibility molecule assembly by subfractionation of the early secretory pathway. Hum Immunol 53:129–139 [CrossRef]
     [Google Scholar]
  4. Chaudhuri B, Ingavale S, Bachhawat A. K. 1996; apd1 [sup]+[/sup], a gene required for red pigment formation in ade6 mutants of Schizosaccharomyces pombe , encodes an enzyme required for glutathione biosynthesis: a role for glutathione and glutathione-conjugate pump. Genetics 145:75–83
     [Google Scholar]
  5. Chen C.-A, Cowan J. A. 2003; Characterization of the soluble domain of the ABC7 type transporter Atm1. J Biol Chem 278:52681–52688 [CrossRef]
     [Google Scholar]
  6. Christensen P. U, Davey J, Nielsen O. 1997a; The Schizosaccharomyces pombe mam1 gene encodes an ABC transporter mediating secretion of M-factor. Mol Gen Genet 255:226–236 [CrossRef]
     [Google Scholar]
  7. Christensen P. U, Davis K, Nielsen O, Davey J. 1997b; Abc1: a new ABC transporter from the fission yeast Schizosaccharomyces pombe . FEMS Microbiol Lett 147:97–102 [CrossRef]
     [Google Scholar]
  8. Cobbett C. S. 2000; Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832 [CrossRef]
     [Google Scholar]
  9. Cui Z, Hirata D, Tsuchiya E, Osada H, Miyakawa T. 1996; The multidrug resistance-associated protein (MRP) subfamily (Yrs1/Yor1) of Saccharomyces cerevisiae is important for the tolerance to a broad range of organic anions. J Biol Chem 271:14712–14716 [CrossRef]
     [Google Scholar]
  10. Dean M, Allikmets R, Gerrard B, Stewart C, Kistler A, Shafer B, Michaelis S, Strathern J. 1994; Mapping and sequencing of two yeast genes belonging to the ATP-binding cassette superfamily. Yeast 10:377–383 [CrossRef]
     [Google Scholar]
  11. Dean M, Hamon Y, Allikmet R. 2001a; The human ATP-binding cassette (ABC) transporter superfamily. J Lipid Res 42:1007–1017
     [Google Scholar]
  12. Dean M, Rzhetsky A, Allikmets R. 2001b; The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11:1156–1166 [CrossRef]
     [Google Scholar]
  13. Decottignies A, Goffeau A. 1997; Complete inventory of the yeast ABC proteins. Nature Genet 15:137–145 [CrossRef]
     [Google Scholar]
  14. Decottignies A, Grant A. M, Nichols J. W, McIntosh D. B, Goffeau A, de Wet H. 1998; ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J Biol Chem 273:12612–12622 [CrossRef]
     [Google Scholar]
  15. Dong J, Lai R, Nielsen K, Fekete C. A, Qiu H, Hinnebusch A. G. 2004; The essential ATP-binding protein RLI1 functions in translation by promoting preinitiation complex assembly. J Biol Chem 279:42157–42168 [CrossRef]
     [Google Scholar]
  16. Fisher C. R. 1969; Enzymology of the pigmented adenine-requiring mutants of Saccharomyces and Schizosaccharomyces . Biochem Biophys Res Commun 34:306–310 [CrossRef]
     [Google Scholar]
  17. Gaur M, Choudhury D, Prasad R. 2005; Complete inventory of ABC proteins in human pathogenic yeast, Candida albicans . J Mol Microbiol Biotechnol 9:3–15 [CrossRef]
     [Google Scholar]
  18. Henikoff S, Greene E. A, Pietrokovski S, Bork P, Attwood T. K, Hood L. 1997; Gene families: the taxonomy of protein paralogs and chimeras. Science 278:609–614 [CrossRef]
     [Google Scholar]
  19. Hughes A. L, Todd B. L, Espenshade P. J. 2005; SREBP pathway responds to sterols and functions as an oxygen sensor in fission yeast. Cell 120:831–842 [CrossRef]
     [Google Scholar]
  20. Huyer G, Longsworth G. L, Mason D. L, Mallampali M. P, McCaffery J. M, Wright R. L, Michaelis S. 2004; A striking quality control subcompartment in Saccharomyces cerevisiae : the endoplasmic reticulum-associated compartment. Mol Biol Cell 15:908–921
     [Google Scholar]
  21. Ishikawa T, Wright C. D, Ishizuka H. 1994; GS-X pump is functionally overexpressed in cis -diamminedichloroplatinum (II)-resistant human leukemia HL-60 cells and down-regulated by cell differentiation. J Biol Chem 269:29085–29093
     [Google Scholar]
  22. Iwaki T, Takegawa K. 2004; A set of loxP marker cassettes for Cre-mediated multiple gene disruption in Schizosaccharomyces pombe . Biosci Biotechnol Biochem 68:545–550 [CrossRef]
     [Google Scholar]
  23. Iwaki T, Osawa F, Onishi M, Koga T, Fujita Y, Hosomi A, Tanaka N, Fukui Y, Takegawa K. 2003; Characterization of vps33 [sup]+[/sup], a gene required for vacuolar biogenesis and protein sorting in Schizosaccharomyces pombe . Yeast 20:845–855 [CrossRef]
     [Google Scholar]
  24. Iwaki T, Goa T, Tanaka N, Takegawa K. 2004; Characterization of Schizosaccharomyces pombe mutants defective in vacuolar acidification and protein sorting. Mol Genet Genomics 271:197–207 [CrossRef]
     [Google Scholar]
  25. Iwaki T, Fujita Y, Tanaka N, Giga-Hama Y, Takegawa K. 2005; Mitochondrial ABC transporter Atm1p is required for protection against oxdative stress and vacuolar functions in Schizosaccharomyces pombe . Biosci Biotechnol Biochem 69:2109–2116 [CrossRef]
     [Google Scholar]
  26. Jones P. M, George A. M. 2004; The ABC transporter structure and mechanism: perspectives on recent research. Cell Mol Life Sci 61:682–699 [CrossRef]
     [Google Scholar]
  27. Katzmann D. J, Hallstrom T. C, Voet M, Wysock W, Golin J, Volckaert G, Moye-Rowley W. S. 1995; Expression of an ATP-binding cassette transporter-encoding gene (YOR1) is required for oligomycin resistance in Saccharomyces cerevisiae . Mol Cell Biol 15:6875–6883
     [Google Scholar]
  28. Kelm K. B, Huyer G, Huang J. C, Michaelis S. 2004; The internalization of yeast Ste6p follows an ordered series of events involving phosphorylation, ubiquitination, recognition and endocytosis. Traffic 5:165–180 [CrossRef]
     [Google Scholar]
  29. Kispal G, Csere P, Guiard B, Lill R. 1997; The ABC transporter Atm1p is required for mitochondrial iron homeostasis. FEBS Lett 418:346–350 [CrossRef]
     [Google Scholar]
  30. Klein M, Mamnun Y. M, Eggmann T, Schuller C, Wolfger H, Martinoia E, Kuchler K. 2002; The ATP-binding cassette (ABC) transporter Bpt1p mediates vacuolar sequestration of glutathione conjugates in yeast. FEBS Lett 520:63–67 [CrossRef]
     [Google Scholar]
  31. Kuchler K, Sterne R. E, Thorner J. 1989; Saccharomyces cerevisiae STE6 gene product: a novel pathway for protein export in eukaryotic cells. EMBO J 8:3973–3984
     [Google Scholar]
  32. Kumar A, Agarwal S, Heyman J. A. 12 other authors 2002; Subcellular localization of the yeast proteome. Gene Dev 16:707–719 [CrossRef]
     [Google Scholar]
  33. Leighton J, Schatz G. 1995; An ABC transporter in the mitochondrial inner membrane is required for normal growth of yeast. EMBO J 14:188–195
     [Google Scholar]
  34. Li Y, Printz W. A. 2004; ATP-binding cassette (ABC) transporters mediate nonvesicular, raft-modulated sterol movement from the plasma membrane to the endoplasmic reticulum. J Biol Chem 279:45226–45234 [CrossRef]
     [Google Scholar]
  35. Li Z.-S, Szczypka M, Lu Y.-P, Thiele D. J, Rea P. A. 1996; The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S -conjugate pump. J Biol Chem 271:6509–6517 [CrossRef]
     [Google Scholar]
  36. Moreno S, Klar A, Nurse P. 1991; Molecular genetic analysis of fission yeast Schizosaccharomyces pombe . Methods Enzymol 194:795–823
     [Google Scholar]
  37. Nagao K, Taguchi Y, Arioka M, Kadokura H, Takatsuki A, Yoda K, Yamasaki M. 1995; bfr1 [sup]+[/sup], a novel gene of Schizosaccharomyces pombe which confers brefeldin A resistance, is related to the ATP-binding cassette superfamily. J Bacteriol 177:1536–1543
     [Google Scholar]
  38. Nakamura T, Nakamura-Kubo M, Hirata A, Shimoda C. 2001; The Schizosaccharomyces pombe spo3 [sup]+[/sup] gene is required for assembly of the forespore membrane and genetically interacts with psy1 [sup]+[/sup] - encoding syntaxin-like protein. Mol Biol Cell 12:3955–3972 [CrossRef]
     [Google Scholar]
  39. Nishi K, Yoshida M, Nishimura M, Nishikawa M, Nishiyama M, Horinouchi S, Beppu T. 1992; A leptomycin B resistance gene of Schizosaccharomyces pombe encodes a protein similar to the mammalian P-glycoproteins. Mol Microbiol 6:761–769 [CrossRef]
     [Google Scholar]
  40. Ortiz D. F, Kreppel L, Speiser D. M, Scheel G, McDonald G, Ow D. W. 1992; Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter. EMBO J 11:3491–3499
     [Google Scholar]
  41. Ortiz D. F, Ruscitti T, McCue K. F, Ow D. W. 1995; Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J Biol Chem 270:4721–4728 [CrossRef]
     [Google Scholar]
  42. Ortiz D. F, St Pierre M. V, Abdulmessih A, Arias I. M. 1997; A yeast ATP-binding cassette-type protein mediating ATP-dependent bile acid transport. J Biol Chem 272:15358–15365 [CrossRef]
     [Google Scholar]
  43. Oude Elferink R. P, Bakker C. T, Roelofsen H, Middelkoop E, Ottenhoff R, Heijn M, Jansen P. L. 1993; Accumulation of organic anion in intracellular vesicles of cultured rat hepatocytes is mediated by the canalicular multispecific organic anion transporter. Hepatology 17:434–444 [CrossRef]
     [Google Scholar]
  44. Penninckx M. J. 2002; An overview on glutathione in Saccharomyces versus non-conventional yeasts. FEMS Yeast Res 2:295–305
     [Google Scholar]
  45. Sánchez-Fernández R, Davies T. G. E, Coleman J. O. D, Rea P. A. 2001; The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276:30231–30244 [CrossRef]
     [Google Scholar]
  46. Shani N, Valle D. 1996; A Saccharomyces cerevisiae homolog of the human adrenoleukodystrophy transporter is a heterodimer of two half ATP-binding cassette transporters. Proc Natl Acad Sci U S A 93:11901–11906 [CrossRef]
     [Google Scholar]
  47. Shani N, Watkins P. A, Valle D. 1995; PXA1 , a possible Saccharomyces cerevisiae ortholog of the human adrenoleukodystrophy gene. Proc Natl Acad Sci U S A 92:6012–6016 [CrossRef]
     [Google Scholar]
  48. Sharma K. G, Mason D. L, Liu G, Rea P. A, Bachhawat A. K, Michaelis S. 2002; Localization, regulation, and substrate transport properties of Bpt1p, a Saccharomyces cerevisiae MRP-type ABC transporter. Eukaryotic Cell 1:391–400 [CrossRef]
     [Google Scholar]
  49. Sharma K. G, Kaur R, Bachhawat A. K. 2003; The glutathione-mediated detoxification pathway in yeast: an analysis using the red pigment that accumulates in certain adenine biosynthetic mutants of yeasts reveals the involvement of novel genes. Arch Microbiol 180:108–117 [CrossRef]
     [Google Scholar]
  50. Sheps J. A, Ralph S, Zhao Z, Baillie D. L, Ling V. 2004; The ABC transporter gene family of Caenorhabditis elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes. Genome Biol 5:R15 [CrossRef]
     [Google Scholar]
  51. Shrieve D. C, Bump E. A, Rice G. C. 1988; Heterogeneity of cellular glutathione among cells derived from a murine fibrosarcoma or a human renal cell carcinoma detected by flow cytometric analysis. J Biol Chem 263:14107–14114
     [Google Scholar]
  52. Smirnov M. N, Smirnov V. N, Budowsky E. I, Inge-Vechtomov S. G, Serebrjakov N. G. 1967; Red pigment of adenine-deficient yeast Saccharomyces cerevisiae . Biochem Biophys Res Commun 27:299–304 [CrossRef]
     [Google Scholar]
  53. Suga M, Hatakeyama T. 2001; High efficiency transformation of Schizosaccharomyces pombe pretreated with thiol compounds by electroporation. Yeast 18:1015–1021 [CrossRef]
     [Google Scholar]
  54. Supek F, Supekova L, Nelson N. 1994; Features of vacuolar H[sup]+[/sup]-ATPase revealed by yeast suppressor mutants. J Biol Chem 269:26479–26485
     [Google Scholar]
  55. Turi T. G, Rose J. K. 1995; Characterization of a novel Schizosaccharomyces pombe multidrug resistance transporter conferring brefeldin A resistance. Biochem Biophys Res Commun 213:410–418 [CrossRef]
     [Google Scholar]
  56. Venter H, Shilling R. A, Velamakanni S, Balakrishnan L, van Veen H. W. 2003; An ABC transporter with a secondary-active multidrug transporter domain. Nature 426:866–870 [CrossRef]
     [Google Scholar]
  57. Vida T. A, Emr S. D. 1995; A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128:779–792 [CrossRef]
     [Google Scholar]
  58. Wood V, Gwilliam R, Rajandream M.-A. 131 other authors 2002; The genome sequence of Schizosaccharomyces pombe . Nature 415:871–880 [CrossRef]
     [Google Scholar]
  59. Young L, Leonhard K, Tatsuta T, Trowsdale J, Langer T. 2001; Role of the ABC trasnporter Mdl1 in peptide export from mitochondria. Science 291:2135–2138 [CrossRef]
     [Google Scholar]
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A survey of all 11 ABC transporters in fission yeast: two novel ABC transporters are required for red pigment accumulation in a Schizosaccharomyces pombe adenine biosynthetic mutant
Microbiology 152, 2309 (2006); https://doi.org/10.1099/mic.0.28952-0
/content/journal/micro/10.1099/mic.0.28952-0
/content/journal/micro/10.1099/mic.0.28952-0
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