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PMID: 23569283 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Newly characterized Golgi-localized family of proteins is involved in calcium and pH homeostasis in yeast and human cells.

Demaegd D, Foulquier F, Colinet AS, Gremillon L, Legrand D, Mariot P, Peiter E, Van Schaftingen E, Matthijs G, Morsomme P

Abstract

Defects in the human protein TMEM165 are known to cause a subtype of Congenital Disorders of Glycosylation. Transmembrane protein 165 (TMEM165) belongs to an uncharacterized family of membrane proteins called Uncharacterized Protein Family 0016, which are well conserved throughout evolution and share characteristics reminiscent of the cation/Ca(2+) exchanger superfamily. Gcr1 dependent translation factor 1 (Gdt1p), the budding yeast member of this family, contributes to Ca(2+) homeostasis via an uncharacterized Ca(2+) transport pathway localized in the Golgi apparatus. The gdt1Δ mutant was found to be sensitive to high concentrations of Ca(2+), and interestingly, this sensitivity was suppressed by expression of TMEM165, the human ortholog of Gdt1p, indicating conservation of function among the members of this family. Patch-clamp analyses on human cells indicated that TMEM165 expression is linked to Ca(2+) ion transport. Furthermore, defects in TMEM165 affected both Ca(2+) and pH homeostasis. Based on these results, we propose that Gdt1p and TMEM165 could be members of a unique family of Golgi-localized Ca(2+)/H(+) antiporters and that modification of the Golgi Ca(2+) and pH balance could explain the glycosylation defects observed in TMEM165-deficient patients.

MeSH Terms
Antiporters/metabolism Blotting, Western Calcium/metabolism Cation Transport Proteins Cell Fractionation Flow Cytometry Fluorescent Antibody Technique Gene Expression Regulation/genetics,physiology Golgi Apparatus/metabolism HeLa Cells Homeostasis/physiology Humans Hydrogen/metabolism Hydrogen-Ion Concentration Membrane Proteins/metabolism Patch-Clamp Techniques RNA, Small Interfering/genetics Saccharomycetales/metabolism
Chemicals
Antiporters Cation Transport Proteins Membrane Proteins RNA, Small Interfering TMEM165 protein, human Hydrogen Calcium
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Demaegd Didier
Institut des Sciences de la Vie, Université Catholique de Louvain, B-1348 Louvain-la-Neuve, Belgium.
Foulquier François
Colinet Anne-Sophie
Gremillon Louis
Legrand Dominique
Mariot Pascal
Peiter Edgar
Van Schaftingen Emile
Matthijs Gert
Morsomme Pierre
References (37)
37 references, click to expand
  1. Mutations in ATP2C1, encoding a calcium pump, cause Hailey-Hailey disease.
    Nat Genet. 2000 Jan;24(1):61-5 PMID: 10615129
  2. 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
  3. Vacuolar Ca(2+) uptake.
    Cell Calcium. 2011 Aug;50(2):139-46 PMID: 21310481
  4. The Golgi-localization of yeast Emp47p depends on its di-lysine motif but is not affected by the ret1-1 mutation in alpha-COP.
    J Cell Biol. 1995 Nov;131(4):895-912 PMID: 7490292
  5. Cloning and characterization of a putative Ca2+/H+ antiporter gene from Escherichia coli upon functional complementation of Na+/H+ antiporter-deficient strains by the overexpressed gene.
    J Biol Chem. 1993 May 25;268(15):11296-303 PMID: 8496184
  6. A global view of pleiotropy and phenotypically derived gene function in yeast.
    Mol Syst Biol. 2005;1:2005.0001 PMID: 16729036
  7. Steady-state free Ca(2+) in the yeast endoplasmic reticulum reaches only 10 microM and is mainly controlled by the secretory pathway pump pmr1.
    EMBO J. 1999 Sep 1;18(17):4733-43 PMID: 10469652
  8. Mutation of the COG complex subunit gene COG7 causes a lethal congenital disorder.
    Nat Med. 2004 May;10(5):518-23 PMID: 15107842
  9. 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
  10. Structural insight into the ion-exchange mechanism of the sodium/calcium exchanger.
    Science. 2012 Feb 10;335(6069):686-90 PMID: 22323814
  11. The genetic landscape of a cell.
    Science. 2010 Jan 22;327(5964):425-31 PMID: 20093466
  12. Calcium homeostasis and signaling in yeast cells and cardiac myocytes.
    FEMS Yeast Res. 2009 Dec;9(8):1137-47 PMID: 19678847
  13. The product of HUM1, a novel yeast gene, is required for vacuolar Ca2+/H+ exchange and is related to mammalian Na+/Ca2+ exchangers.
    Mol Cell Biol. 1996 Jul;16(7):3730-41 PMID: 8668190
  14. The Golgi apparatus plays a significant role in the maintenance of Ca2+ homeostasis in the vps33Delta vacuolar biogenesis mutant of Saccharomyces cerevisiae.
    J Biol Chem. 1999 Feb 26;274(9):5939-47 PMID: 10026219
  15. Structures of membrane proteins.
    Q Rev Biophys. 2010 Feb;43(1):65-158 PMID: 20667175
  16. Golgi function and dysfunction in the first COG4-deficient CDG type II patient.
    Hum Mol Genet. 2009 Sep 1;18(17):3244-56 PMID: 19494034
  17. A new inborn error of glycosylation due to a Cog8 deficiency reveals a critical role for the Cog1-Cog8 interaction in COG complex formation.
    Hum Mol Genet. 2007 Apr 1;16(7):717-30 PMID: 17220172
  18. Calcineurin inhibits VCX1-dependent H+/Ca2+ exchange and induces Ca2+ ATPases in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 May;16(5):2226-37 PMID: 8628289
  19. Human keratinocyte ATP2C1 localizes to the Golgi and controls Golgi Ca2+ stores.
    J Invest Dermatol. 2003 Oct;121(4):688-94 PMID: 14632183
  20. How Golgi glycosylation meets and needs trafficking: the case of the COG complex.
    Glycobiology. 2011 Jul;21(7):853-63 PMID: 21112967
  21. The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2+ and Mn2+ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation.
    Mol Biol Cell. 1998 May;9(5):1149-62 PMID: 9571246
  22. Zebrafish (Danio rerio) endomembrane antiporter similar to a yeast cation/H(+) transporter is required for neural crest development.
    Biochemistry. 2010 Aug 10;49(31):6557-66 PMID: 20578725
  23. Induction of vacuolar Ca2+-ATPase and H+/Ca2+ exchange activity in yeast mutants lacking Pmr1, the Golgi Ca2+-ATPase.
    FEBS Lett. 1999 Jul 9;454(3):181-6 PMID: 10431803
  24. Distinction between Ca(2+) pump and Ca(2+)/H(+) antiport activities in synaptic vesicles of sheep brain cortex.
    Neurochem Int. 2000 Oct;37(4):387-96 PMID: 10825579
  25. TMEM165 deficiency causes a congenital disorder of glycosylation.
    Am J Hum Genet. 2012 Jul 13;91(1):15-26 PMID: 22683087
  26. 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
  27. The versatility and universality of calcium signalling.
    Nat Rev Mol Cell Biol. 2000 Oct;1(1):11-21 PMID: 11413485
  28. Acidic calcium stores open for business: expanding the potential for intracellular Ca2+ signaling.
    Trends Cell Biol. 2010 May;20(5):277-86 PMID: 20303271
  29. Aequorin luminescence: relation of light emission to calcium concentration--a calcium-independent component.
    Science. 1977 Mar 11;195(4282):996-8 PMID: 841325
  30. Calcium signalling: dynamics, homeostasis and remodelling.
    Nat Rev Mol Cell Biol. 2003 Jul;4(7):517-29 PMID: 12838335
  31. Vacuolar H+-ATPase meets glycosylation in patients with cutis laxa.
    Biochim Biophys Acta. 2009 Sep;1792(9):903-14 PMID: 19171192
  32. Live imaging of yeast Golgi cisternal maturation.
    Nature. 2006 Jun 22;441(7096):1007-10 PMID: 16699523
  33. Conserved oligomeric Golgi complex subunit 1 deficiency reveals a previously uncharacterized congenital disorder of glycosylation type II.
    Proc Natl Acad Sci U S A. 2006 Mar 7;103(10):3764-9 PMID: 16537452
  34. The cation/Ca(2+) exchanger superfamily: phylogenetic analysis and structural implications.
    Mol Biol Evol. 2004 Sep;21(9):1692-703 PMID: 15163769
  35. Impaired glycosylation and cutis laxa caused by mutations in the vesicular H+-ATPase subunit ATP6V0A2.
    Nat Genet. 2008 Jan;40(1):32-4 PMID: 18157129
  36. Identification and characterization of Vnx1p, a novel type of vacuolar monovalent cation/H+ antiporter of Saccharomyces cerevisiae.
    J Biol Chem. 2007 Aug 17;282(33):24284-93 PMID: 17588950
  37. The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling.
    Plant Physiol. 2007 Sep;145(1):192-203 PMID: 17631529
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2013-04-23
Epub
2013-00-08
Pages
6859-64
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3637739
Subset
IM
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