Overexpression of the PHO84 gene causes heavy metal accumulation and induces Ire1p-dependent unfolded protein response in Saccharomyces cerevisiae cells

Applied Microbiology and Biotechnology

Volumn 94, Issue 2, 2012, Pages 425-435

  Ofiteru, Augustin Minel ^a   Ruta, Lavinia Liliana ^a   Rotaru, Codruta ^a   Dumitru, Ioana ^a   Ene, Cristian Dumitru ^a   Neagoe, Aurora ^a   Farcasanu, Ileana Cornelia ^a  

^a UNIVERSITY OF BUCHAREST   (Romania)

Author keywords

Heavy metal accumulation; Overexpression; PHO84; Saccharomyces cerevisiae

Indexed keywords

HEAVY METAL ACCUMULATION; INORGANIC PHOSPHATES; ION PUMPS; METAL ACCUMULATION; OVER-EXPRESSION; P-TYPE; PHO84; SACCHAROMYCES CEREVISIAE CELLS; UNFOLDED PROTEIN RESPONSE; WILD TYPES; YEAST CELL;

BIOACCUMULATION; CELL MEMBRANES; CYTOLOGY; GENES; HEAVY METALS; MANGANESE; MANGANESE COMPOUNDS; PROTEINS;

YEAST;

BETA GALACTOSIDASE; CALCIUM ION; COBALT; COPPER ION; FUNGAL PROTEIN; HEAVY METAL; MAGNESIUM ION; PH084 PROTEIN; PHOSPHATE; PHOSPHATE TRANSPORTER; PROTEIN IRE1; UNCLASSIFIED DRUG;

BIOLOGICAL UPTAKE; GENE EXPRESSION; HEAVY METAL; HYPERACCUMULATION; MEMBRANE; PROTEIN; YEAST;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CALCIUM TRANSPORT; CELL GROWTH; ENZYME ACTIVITY; FUNGAL GENE; FUNGUS GROWTH; GENE LOCATION; GENE OVEREXPRESSION; GOLGI COMPLEX; HEAVY METAL REMOVAL; NONHUMAN; PHOSPHATE TRANSPORT; PROTEIN UNFOLDING; SACCHAROMYCES CEREVISIAE; YEAST CELL;

GENE EXPRESSION; MEMBRANE GLYCOPROTEINS; METALS, HEAVY; PROTEIN-SERINE-THREONINE KINASES; PROTON-PHOSPHATE SYMPORTERS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UNFOLDED PROTEIN RESPONSE;

EID: 84862642861     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3784-3     Document Type: Article

References (46)

1. Amberg DC, Burke DJ, Strathern JN (2005) Methods in yeast genetics. A Cold Spring Harbor Laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 135-139
2. Antebi A, Fink GR (1992) The yeast Ca2+-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol Biol Cell 3:633-654 (Pubitemid 23098263)
3. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements-a review of their distribution, ecology and phytochemistry. Biorecovery 1:81-126
4. Baker AJM (2002) The use of tolerant plants and hyperaccumulators. In: Wong MH, Bradshaw AD (eds) Restoration and management of derelict land: modern approaches. World Scientific Publishing Co., Singapore, pp 138-148
5. Borst-Pauwels GW (1981) Ion transport in yeast. Biochim Biophys Acta 650:88-127
6. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCRmediated gene disruption and other applications. Yeast 14:115-132 (Pubitemid 28062863)
7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
8. Bun-ya M, Nishimura M, Harashima S, Oshima Y (1991) The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter. Mol Cell Biol 11:3229-3238 (Pubitemid 21895710)
9. Bun-ya M, Shikata K, Nakade S, Yompakdee C, Harashima S, Oshima Y (1996) Two new genes, PHO86 and PHO87, involved in inorganic phosphate uptake in Saccharomyces cerevisiae. Curr Genet 29:344-351 (Pubitemid 26097916)
10. Cocs JS, Walter P (1996) A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87:391-404 (Pubitemid 26374314)
11. Culotta VC, Yang M, Hall MD (2005) Manganese transport and trafficking: lessons learned from Saccharomyces cerevisiae. Eukaryot Cell 4:1159-1165 (Pubitemid 41004129)
12. 2+ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Mol Biol Cell 9:1149-1162 (Pubitemid 28457306)
13. Eide DJ (2009) Homeostatic and adaptive responses to zinc deficiency in Saccharomyces cerevisiae. J Biol Chem 284:18565-18569
14. Farcasanu IC, Ohta N, Miyakawa T (1996) The fate of Mn ions inside the Saccharomyces cerevisiae cells seen by electronic paramagnetic resonance. Biosci Biotechnol Biochem 60:468-471 (Pubitemid 126460925)
15. Feldmann H (2005) Yeast transport. In: Yeast molecular biology, a short compendium on basic features and novel aspects. Adolf-Butenandt-Institute, University of Munich, pp 10-17. http://biochemie.web.med.uni-muenchen.de/Yeast- Biol/
16. Fernando DR, Woodrow IE, Jaffré T, Dumontet V, Marshall AT, Baker AJM (2008) Foliar manganese accumulation by Maytenus founieri (Celastraceae) in its native New Caledonian habitats: populational variation and localization by X-ray microanalysis. New Phytol 177:178-185 (Pubitemid 350222000)
17. Fernando DR, Guymer G, Reeves RD, Woodrow IE, Baker AJ, Batianoff GN (2009) Foliar Mn accumulation in eastern Australian herbarium specimens: prospecting for 'new' Mn hyperaccumulators and potential applications in taxonomy. Ann Bot 103:931-939
18. Gifford S, Dunstan RH, O'Connor W, Koller CE, MacFarlane GR (2007) Aquatic zooremediation: deploying animals to remediate contaminated aquatic environments. Trends Biotechnol 25:60-65 (Pubitemid 46109540)
19. Guthrie C, Fink GR (eds) (1991) Guide to yeast genetics and molecular biology. Academic, New York
20. Jansen G, Wu C, Schade B, Thomas DY, Whiteway M (2005) Drag&Drop cloning in yeast. Gene 344:43-51 (Pubitemid 40126791)
21. Jensen LT, Ajua-Alemanji M, Culotta VC (2003) The Saccharomyces cerevisiae high affinity phosphate transporter encoded by PHO84 also functions in manganese homeostasis. J Biol Chem 278:42036-42040 (Pubitemid 37310468)
22. Kawahara T, Yanagi H, Yura T, Mori K (1997) Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response. Mol Biol Cell 8:1845-1862 (Pubitemid 27451106)
23. Kihn JC, Dassargues CM, Mestdagh MM (1988) Preliminary ESR studies of Mn(II) retention by the yeast Saccharomyces. Can J Microbiol 34:1230-1234
24. Kohno K (2010) Stress-sensing mechanisms in the unfolded protein response: similarities and differences between yeast and mammals. J Biochem 147:27-33
25. Lapinskas PJ, Cunningham KW, Liu XF, Fink GR, Culotta VC (1995) Mutations in PMR1 suppress oxidative damage in yeast lacking superoxide dismutase. Mol Cell Biol 15:1382-1388
26. 2+-ATPase in the Golgi, regulates intracellular levels of the cadmium ion. FEMS Microbiol Lett 285:79-88
27. Machado MD, Santos MS, Gouveia C, Soares HM, Soares EV (2008) Removal of heavy metals using a brewer's yeast strain of Saccharomyces cerevisiae: the flocculation as a separation process. Bioresour Technol 99:2107-2115 (Pubitemid 351208536)
28. Machado MD, Janssens S, Soares HM, Soares EV (2009) Removal of heavy metals using a brewar's yeast strain of Saccharomyces cerevisiae: advantages of using dead biomass. J Appl Biotech 106:1792-1804
29. 778 is essential for cation transport. J Biol Chem 275:23933-23938 (Pubitemid 30624682)
30. Massé E, Arguin M (2005) Ironing out the problem: new mechanisms of iron homeostasis. Trends Biochem Sci 30:462-468 (Pubitemid 41033242)
31. Miller JP, Lo RS, Ben-Hur A, Desmarais C, Stagljar I, Stafford Noble W, Fields S (2005) Large-scale identification of yeast integral membrane protein interactions. Proc Natl Acad Sci U S A 102: 12123-12128 (Pubitemid 41291139)
32. Mori K, Sant A, Kohno K, Normington K, Gething MJ, Sambrook JF (1992) A 22 bp cis-acting element is necessary and sufficient for the induction of the yeast KAR2 (BiP) gene by unfolded proteins. EMBO J 11:2583-2593
33. Nyren P, Nore BF, Baltzcheffsky M (1986) Studies on photosynthetic inorganic pyrophosphate formation in Rhodospirillum rubrum chromatophores. Biochim Biophys Acta 851:276-282
34. Ratherford JC, Bird AJ (2004) Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot Cell 3:1-13 (Pubitemid 38237293)
35. Reddi AR, Jensen LT, Culotta VC (2009) Manganese homeostasis in Saccharomyces cerevisiae. Chem Rev 109:4722-4732
36. Reeves RD (2006) Hyperaccumulation of trace elements by plants. In: Morel J-L, Echevarria G, Goncharova N (eds) Phytoremediation of metal contaminated soils. Springer, Berlin, pp 25-52
37. Rosenfeld L, Reddi AR, Leung E, Aranda K, Jensen LT, Culotta VC (2010) The effect of phosphate accumulation on metal ion homeostasis in Saccharomyces cerevisiae. J Biol Inorg Chem 15:1051-1062
38. 2+ ATPase family. Cell 58:133-145 (Pubitemid 19180086)
39. Ruta L, Paraschivescu C, Matache M, Avramescu S, Farcasanu IC (2010) Removing heavy metals from synthetic effluents using "kamikaze" Saccharomyces cerevisiae cells. Appl Microbiol Biotechnol 85:763-771
40. Schiestl R, Gietz RD (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acid as carrier. Curr Genet 16:339-346 (Pubitemid 20034019)
41. Sherman F (2002) Getting started with yeast. Methods Enzymol 350:3-41 (Pubitemid 34619482)
42. Sherman F, Fink GR, Hicks JB (1986) Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
43. 2+-ATPase in yeast Golgi, has properties distinct from sarco/endoplasmic reticulum and plasma membrane calcium pumps. J Biol Chem 272:9895-9901 (Pubitemid 27171658)
44. Takeda A (2003) Manganese action in brain function. Brain Res Rev 41:79-87 (Pubitemid 36044595)
45. Van Ho A, Ward DM, Kaplan J (2002) Transition metal transport in yeast. Annu Rev Microbiol 56:237-261 (Pubitemid 35217455)
46. Watanabe T, Ozaki N, Iwashita K, Fujii T, Iefuji H (2008) Breeding of wastewater treatment yeasts that accumulate high concentrations of phosphorus. Appl Microbiol Biotechnol 80:331-338