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PMID: 7664728 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The PMR2 gene cluster encodes functionally distinct isoforms of a putative Na+ pump in the yeast plasma membrane.

The EMBO journal ·Vol. 14 ·No. 16 ·1995-08-15 ·Pages 3870-82

Wieland J, Nitsche AM, Strayle J, Steiner H, Rudolph HK

Abstract

We report a structural and functional analysis of the PMR2 gene cluster in yeast. We found that several strains of Saccharomyces cerevisiae contain multiple PMR2 genes repeated in tandem, whereas most phylogenetically related yeasts appear to possess only a single PMR2 gene. This unusual tandem array of nearly identical genes encodes putative ion pumps involved in Na+ tolerance. Pmr2a and Pmr2b, the proteins encoded by the first two repeats, differ by only 13 amino acid exchanges. Both proteins share localization to the plasma membrane, but represent distinct isoforms of a putative Na+ pump. When expressed under identical conditions in vivo, Pmr2a and Pmr2b cause different tolerances to Na+ and Li+. Finally, we show that the Na+ tolerance mediated through these pumps is regulated by calmodulin via a calcineurin-independent mechanism which activates the Pmr2 ion pumps post-transcriptionally.

Related Genes
PMR2
MeSH Terms
Adenosine Triphosphatases/biosynthesis,genetics,metabolism Calcineurin Calmodulin/physiology Calmodulin-Binding Proteins/physiology Cation Transport Proteins Cell Fractionation Cell Membrane/enzymology Enzyme Induction Genes, Fungal/genetics Ion Transport/drug effects Isoenzymes/genetics Lithium/pharmacology Multigene Family/genetics Mutation Phosphoprotein Phosphatases/physiology Promoter Regions, Genetic/genetics RNA, Fungal/biosynthesis RNA, Messenger/biosynthesis Recombinant Fusion Proteins/genetics Restriction Mapping Saccharomyces cerevisiae/drug effects,enzymology,genetics Saccharomyces cerevisiae Proteins Sodium/pharmacology Sodium-Potassium-Exchanging ATPase/biosynthesis,genetics,metabolism
Chemicals
Calmodulin Calmodulin-Binding Proteins Cation Transport Proteins ENA1 protein, S cerevisiae Isoenzymes RNA, Fungal RNA, Messenger Recombinant Fusion Proteins Saccharomyces cerevisiae Proteins Lithium Sodium Calcineurin Phosphoprotein Phosphatases Adenosine Triphosphatases Sodium-Potassium-Exchanging ATPase
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Wieland J
Institut für Biochemie der Universität Stuttgart, Germany.
Nitsche A M
Strayle J
Steiner H
Rudolph H K
References (57)
57 references, click to expand
  1. The NUP1 gene encodes an essential component of the yeast nuclear pore complex.
    Cell. 1990 Jun 15;61(6):965-78 PMID: 2190694
  2. Analysis of the regulatory domain of yeast plasma membrane H+-ATPase by directed mutagenesis and intragenic suppression.
    FEBS Lett. 1991 Aug 5;287(1-2):71-4 PMID: 1831768
  3. Differential expression of two genes encoding isoforms of the ATPase involved in sodium efflux in Saccharomyces cerevisiae.
    Mol Gen Genet. 1993 Jan;236(2-3):363-8 PMID: 8437581
  4. Deletion analysis of yeast plasma membrane H+-ATPase and identification of a regulatory domain at the carboxyl-terminus.
    FEBS Lett. 1989 Apr 24;247(2):381-5 PMID: 2523820
  5. High-frequency transformation of yeast: autonomous replication of hybrid DNA molecules.
    Proc Natl Acad Sci U S A. 1979 Mar;76(3):1035-9 PMID: 375221
  6. Isolation of the yeast calmodulin gene: calmodulin is an essential protein.
    Cell. 1986 Nov 7;47(3):423-31 PMID: 3533275
  7. Performance and conservation of osmotic work by proton-coupled solute porter systems.
    J Bioenerg. 1973 Jan;4(1):63-91 PMID: 4268692
  8. Tandem gene amplification mediates copper resistance in yeast.
    Proc Natl Acad Sci U S A. 1982 Sep;79(17):5342-6 PMID: 6291039
  9. The Saccharomyces cerevisiae genes (CMP1 and CMP2) encoding calmodulin-binding proteins homologous to the catalytic subunit of mammalian protein phosphatase 2B.
    Mol Gen Genet. 1991 May;227(1):52-9 PMID: 1646387
  10. ATP formation caused by acid-base transition of spinach chloroplasts.
    Proc Natl Acad Sci U S A. 1966 Jan;55(1):170-7 PMID: 5220864
  11. Two genes required for cell fusion during yeast conjugation: evidence for a pheromone-induced surface protein.
    Mol Cell Biol. 1987 Jul;7(7):2316-28 PMID: 3302672
  12. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants.
    EMBO J. 1994 Jul 15;13(14):3261-71 PMID: 8045256
  13. Calcineurin mediates inhibition by FK506 and cyclosporin of recovery from alpha-factor arrest in yeast.
    Nature. 1992 Dec 17;360(6405):682-4 PMID: 1281518
  14. Interaction of neurotoxins with the selectivity filter and the gating system of the sodium channel.
    Adv Cytopharmacol. 1979;3:353-61 PMID: 382793
  15. Molecular genetics of Na,K-ATPase.
    Prog Nucleic Acid Res Mol Biol. 1990;38:37-89 PMID: 2158121
  16. Rapid and efficient site-specific mutagenesis without phenotypic selection.
    Methods Enzymol. 1987;154:367-82 PMID: 3323813
  17. Dual calcium ion regulation of calcineurin by calmodulin and calcineurin B.
    Biochemistry. 1994 Jun 7;33(22):6859-66 PMID: 8204620
  18. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  19. Identification and primary structure of a calmodulin binding domain of the Ca2+ pump of human erythrocytes.
    J Biol Chem. 1988 Feb 25;263(6):2905-10 PMID: 2963820
  20. Molecular perspectives of monovalent cation selective transmembrane channels.
    Int Rev Neurobiol. 1979;21:311-34 PMID: 94042
  21. FK-506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin.
    Nature. 1992 Jun 25;357(6380):692-4 PMID: 1377361
  22. Nitrogen catabolite repression in yeasts and filamentous fungi.
    Adv Microb Physiol. 1985;26:1-88 PMID: 2869649
  23. cDNA cloning of a calcineurin B homolog in Saccharomyces cerevisiae.
    Biochem Biophys Res Commun. 1991 Oct 31;180(2):1159-63 PMID: 1659397
  24. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation.
    Biol Rev Camb Philos Soc. 1966 Aug;41(3):445-502 PMID: 5329743
  25. Calcineurin.
    Adv Enzymol Relat Areas Mol Biol. 1988;61:149-200 PMID: 2833077
  26. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes.
    Cell. 1991 Aug 23;66(4):807-15 PMID: 1715244
  27. The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca2+ ATPase family.
    Cell. 1989 Jul 14;58(1):133-45 PMID: 2526682
  28. The redundancy of ribosomal and transfer RNA genes in Saccharomyces cerevisiae.
    J Mol Biol. 1969 Mar 14;40(2):261-77 PMID: 5365012
  29. H+-ATPase from plasma membranes of Saccharomyces cerevisiae and Avena sativa roots: purification and reconstitution.
    Methods Enzymol. 1988;157:533-44 PMID: 2906717
  30. Characterization of the plasma membrane ATPase of Saccharomyces cerevisiae.
    Mol Cell Biochem. 1978 Nov 30;22(1):51-63 PMID: 154059
  31. The influence of some cations on an adenosine triphosphatase from peripheral nerves.
    Biochim Biophys Acta. 1957 Feb;23(2):394-401 PMID: 13412736
  32. The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae.
    J Biol Chem. 1994 Mar 25;269(12):8792-6 PMID: 8132612
  33. Gene amplification at a locus encoding a putative Na+/H+ antiporter confers sodium and lithium tolerance in fission yeast.
    EMBO J. 1992 Apr;11(4):1631-40 PMID: 1314171
  34. A temperature-sensitive calmodulin mutant loses viability during mitosis.
    J Cell Biol. 1992 Aug;118(3):607-17 PMID: 1639846
  35. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase.
    Cell. 1982 Jan;28(1):145-54 PMID: 7039847
  36. Proliferation of intracellular structures upon overexpression of the PMA2 ATPase in Saccharomyces cerevisiae.
    J Biol Chem. 1993 Sep 15;268(26):19744-52 PMID: 8366114
  37. Maturation of the yeast plasma membrane [H+]ATPase involves phosphorylation during intracellular transport.
    J Cell Biol. 1991 Oct;115(2):289-95 PMID: 1833410
  38. The essential mitotic target of calmodulin is the 110-kilodalton component of the spindle pole body in Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Dec;13(12):7913-24 PMID: 8247006
  39. A PMR2 tandem repeat with a modified C-terminus is located downstream from the KRS1 gene encoding lysyl-tRNA synthetase in Saccharomyces cerevisiae.
    Mol Gen Genet. 1991 May;227(1):149-54 PMID: 2046655
  40. The yeast Ca(2+)-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution.
    Mol Biol Cell. 1992 Jun;3(6):633-54 PMID: 1379856
  41. Yeast has homologs (CNA1 and CNA2 gene products) of mammalian calcineurin, a calmodulin-regulated phosphoprotein phosphatase.
    Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7376-80 PMID: 1651503
  42. Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PMC1, a homolog of plasma membrane Ca2+ ATPases.
    J Cell Biol. 1994 Feb;124(3):351-63 PMID: 7507493
  43. Can calmodulin function without binding calcium?
    Cell. 1991 Jun 14;65(6):949-59 PMID: 2044154
  44. Positive selection of general amino acid permease mutants in Saccharomyces cerevisiae.
    J Bacteriol. 1975 Feb;121(2):562-70 PMID: 1089636
  45. Membrane protein sorting in the yeast secretory pathway: evidence that the vacuole may be the default compartment.
    J Cell Biol. 1992 Oct;119(1):69-83 PMID: 1527174
  46. The structure of an antigenic determinant in a protein.
    Cell. 1984 Jul;37(3):767-78 PMID: 6204768
  47. Protein phosphatase type 2B (calcineurin)-mediated, FK506-sensitive regulation of intracellular ions in yeast is an important determinant for adaptation to high salt stress conditions.
    EMBO J. 1993 Nov;12(11):4063-71 PMID: 7693452
  48. Diverse essential functions revealed by complementing yeast calmodulin mutants.
    Science. 1994 Feb 18;263(5149):963-6 PMID: 8310294
  49. Regulatory subunit (CNB1 gene product) of yeast Ca2+/calmodulin-dependent phosphoprotein phosphatases is required for adaptation to pheromone.
    Mol Cell Biol. 1992 Aug;12(8):3460-9 PMID: 1321337
  50. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation.
    Nature. 1992 Jun 25;357(6380):695-7 PMID: 1377362
  51. Properties of yeast transformation.
    Cold Spring Harb Symp Quant Biol. 1979;43 Pt 2:1305-13 PMID: 385230
  52. A novel P-type ATPase from yeast involved in sodium transport.
    FEBS Lett. 1991 Oct 21;291(2):189-91 PMID: 1657642
  53. The C-terminal 165 amino acids of the plasma membrane Ca(2+)-ATPase confer Ca2+/calmodulin sensitivity on the Na+,K(+)-ATPase alpha-subunit.
    EMBO J. 1995 Jan 3;14(1):58-67 PMID: 7828596
  54. PMT1, the gene for a key enzyme of protein O-glycosylation in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8164-8 PMID: 8367478
  55. DNA of Saccharomyces cerevisiae.
    Methods Enzymol. 1991;194:169-82 PMID: 2005785
  56. Yeast plasma membrane ATPase is essential for growth and has homology with (Na+ + K+), K+- and Ca2+-ATPases.
    Nature. 1986 Feb 20-26;319(6055):689-93 PMID: 3005867
  57. [Li+ as a Na+ analog in ion transport process in vertebrates].
    Tsitologiia. 1991;33(11):111-7 PMID: 1819169
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1995-08-15
Pages
3870-82
Language
English
Region
England
NLM ID
8208664
PMCID
PMC394466
Subset
IM
Grants
NIGMS NIH HHS · GM-35010 · United States
NIGMS NIH HHS · GM-40266 · United States
External Links
PubMed source PMC Full Text View journal details
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