Home LiteratureArticle Details
PMID: 19066337 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Sphingolipids function as downstream effectors of a fungal PAQR.

Molecular pharmacology ·Vol. 75 ·No. 4 ·2009-04-00 ·Pages 866-75

Villa NY, Kupchak BR, Garitaonandia I, Smith JL, Alonso E, Alford C, Cowart LA, Hannun YA, Lyons TJ

Abstract

The Izh2p protein from Saccharomyces cerevisiae belongs to the newly characterized progestin and adipoQ receptor (PAQR) superfamily of receptors whose mechanism of signal transduction is still unknown. Izh2p functions as a receptor for the plant PR-5 defensin osmotin and has pleiotropic effects on cellular biochemistry. One example of this pleiotropy is the Izh2p-dependent repression of FET3, a gene involved in iron-uptake. Although the physiological purpose of FET3 repression by Izh2p is a matter of speculation, it provides a reporter with which to probe the mechanism of signal transduction by this novel class of receptor. Receptors in the PAQR family share sequence similarity with enzymes involved in ceramide metabolism, which led to the hypothesis that sphingolipids are involved in Izh2p-dependent signaling. In this study, we demonstrate that drugs affecting sphingolipid metabolism, such as d-erythro-MAPP and myriocin, inhibit the effect of Izh2p on FET3. We also show that Izh2p causes an increase in steady-state levels of sphingoid base. Moreover, we show that Izh2p-independent increases in sphingoid bases recapitulate the effect of Izh2p on FET3. Finally, our data indicate that the Pkh1p and Pkh2p sphingoid base-sensing kinases are essential components of the Izh2p-dependent signaling pathway. In conclusion, our data indicate that Izh2p produces sphingoid bases and that these bioactive lipids probably function as the second messenger responsible for the effect of Izh2p on FET3.

MeSH Terms
Ceramides/biosynthesis,chemistry,physiology Ceruloplasmin/antagonists & inhibitors,genetics,physiology Membrane Proteins/biosynthesis,genetics,metabolism,physiology Models, Genetic Saccharomyces cerevisiae Proteins/antagonists & inhibitors,biosynthesis,genetics,metabolism,physiology Second Messenger Systems/genetics,physiology Sphingolipids/chemistry,metabolism,physiology
Chemicals
Ceramides IZH2 protein, S cerevisiae Membrane Proteins Saccharomyces cerevisiae Proteins Sphingolipids Ceruloplasmin FET3 protein, S cerevisiae
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Villa Nancy Y
Department of Chemistry, University of Florida, Gainesville, FL 32611, USA.
Kupchak Brian R
Garitaonandia Ibon
Smith Jessica L
Alonso Emilio
Alford Charlene
Cowart L Ashley
Hannun Yusuf A
Lyons Thomas J
References (40)
40 references, click to expand
  1. Phosphorylation and activation of cAMP-dependent protein kinase by phosphoinositide-dependent protein kinase.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):9849-54 PMID: 9707564
  2. BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences.
    FEMS Microbiol Lett. 1999 May 15;174(2):247-50 PMID: 10339815
  3. TopPred II: an improved software for membrane protein structure predictions.
    Comput Appl Biosci. 1994 Dec;10(6):685-6 PMID: 7704669
  4. Ydc1p ceramidase triggers organelle fragmentation, apoptosis and accelerated ageing in yeast.
    Cell Mol Life Sci. 2008 Jun;65(12):1933-42 PMID: 18500447
  5. Cloning of an alkaline ceramidase from Saccharomyces cerevisiae. An enzyme with reverse (CoA-independent) ceramide synthase activity.
    J Biol Chem. 2000 Mar 10;275(10):6876-84 PMID: 10702247
  6. Iterated profile searches with PSI-BLAST--a tool for discovery in protein databases.
    Trends Biochem Sci. 1998 Nov;23(11):444-7 PMID: 9852764
  7. Role of T-loop phosphorylation in PDK1 activation, stability, and substrate binding.
    J Biol Chem. 2005 May 13;280(19):18797-802 PMID: 15741170
  8. Fungal metabolite sulfamisterin suppresses sphingolipid synthesis through inhibition of serine palmitoyltransferase.
    Biochemistry. 2005 Jan 11;44(1):268-77 PMID: 15628868
  9. Crystal structure of osmotin, a plant antifungal protein.
    Proteins. 2004 Jan 1;54(1):170-3 PMID: 14705035
  10. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  11. PDK1 homologs activate the Pkc1-mitogen-activated protein kinase pathway in yeast.
    Mol Cell Biol. 1999 Dec;19(12):8344-52 PMID: 10567559
  12. Metalloregulation of yeast membrane steroid receptor homologs.
    Proc Natl Acad Sci U S A. 2004 Apr 13;101(15):5506-11 PMID: 15060275
  13. Heterologous expression of human mPRalpha, mPRbeta and mPRgamma in yeast confirms their ability to function as membrane progesterone receptors.
    Steroids. 2008 Oct;73(11):1160-73 PMID: 18603275
  14. A rapid method of total lipid extraction and purification.
    Can J Biochem Physiol. 1959 Aug;37(8):911-7 PMID: 13671378
  15. Cloning and characterization of a Saccharomyces cerevisiae alkaline ceramidase with specificity for dihydroceramide.
    J Biol Chem. 2000 Oct 6;275(40):31369-78 PMID: 10900202
  16. Human genetic diseases: a cross-talk between man and yeast.
    Gene. 1997 Aug 11;195(1):1-10 PMID: 9300813
  17. Functional counterparts of mammalian protein kinases PDK1 and SGK in budding yeast.
    Curr Biol. 1999 Feb 25;9(4):186-97 PMID: 10074427
  18. Interaction of the repressors Nrg1 and Nrg2 with the Snf1 protein kinase in Saccharomyces cerevisiae.
    Genetics. 2001 Jun;158(2):563-72 PMID: 11404322
  19. Ceramide triggers meiotic cell cycle progression in Xenopus oocytes. A potential mediator of progesterone-induced maturation.
    J Biol Chem. 1995 Jun 2;270(22):13541-7 PMID: 7768956
  20. Sphingoid base signaling via Pkh kinases is required for endocytosis in yeast.
    EMBO J. 2001 Dec 3;20(23):6783-92 PMID: 11726514
  21. Regulation of lipid biosynthesis in Saccharomyces cerevisiae by fumonisin B1.
    J Biol Chem. 1995 Jun 2;270(22):13171-8 PMID: 7768913
  22. Osmotin is a homolog of mammalian adiponectin and controls apoptosis in yeast through a homolog of mammalian adiponectin receptor.
    Mol Cell. 2005 Jan 21;17(2):171-80 PMID: 15664187
  23. Bakers yeast rises to the challenge: reconstitution of mammalian steroid receptor signalling in S. cerevisiae.
    Trends Genet. 2001 May;17(5):239-43 PMID: 11335020
  24. Ceramide/long-chain base phosphate rheostat in Saccharomyces cerevisiae: regulation of ceramide synthesis by Elo3p and Cka2p.
    Eukaryot Cell. 2003 Apr;2(2):284-94 PMID: 12684378
  25. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry.
    Nature. 2002 Jan 10;415(6868):180-3 PMID: 11805837
  26. Yeast sphingolipids: recent developments in understanding biosynthesis, regulation, and function.
    Biochim Biophys Acta. 2007 Mar;1771(3):421-31 PMID: 16997623
  27. The competitive and noncompetitive antagonism of receptor-mediated drug actions in the presence of spare receptors.
    J Pharmacol Toxicol Methods. 1993 Apr;29(2):85-91 PMID: 8318718
  28. Sphingosine activates protein kinase A type II by a novel cAMP-independent mechanism.
    J Biol Chem. 2005 Jul 15;280(28):26011-7 PMID: 15883165
  29. Cyclic AMP-dependent protein kinase regulates the subcellular localization of Snf1-Sip1 protein kinase.
    Mol Cell Biol. 2004 Mar;24(5):1836-43 PMID: 14966266
  30. Genetic, biochemical, and transcriptional responses of Saccharomyces cerevisiae to the novel immunomodulator FTY720 largely mimic those of the natural sphingolipid phytosphingosine.
    J Biol Chem. 2004 Aug 27;279(35):36720-31 PMID: 15190065
  31. PAQR proteins: a novel membrane receptor family defined by an ancient 7-transmembrane pass motif.
    J Mol Evol. 2005 Sep;61(3):372-80 PMID: 16044242
  32. Nucleocytoplasmic oscillations of the yeast transcription factor Msn2: evidence for periodic PKA activation.
    Curr Biol. 2007 Jun 19;17(12):1044-9 PMID: 17570669
  33. Steroid and G protein binding characteristics of the seatrout and human progestin membrane receptor alpha subtypes and their evolutionary origins.
    Endocrinology. 2007 Feb;148(2):705-18 PMID: 17082257
  34. Signalling functions for sphingolipid long-chain bases in Saccharomyces cerevisiae.
    Biochem Soc Trans. 2005 Nov;33(Pt 5):1170-3 PMID: 16246074
  35. Analysis of sphingoid bases and sphingoid base 1-phosphates by high-performance liquid chromatography.
    Methods Enzymol. 2000;312:3-9 PMID: 11070857
  36. In vivo activation of protein kinase A in Schizosaccharomyces pombe requires threonine phosphorylation at its activation loop and is dependent on PDK1.
    Genetics. 2004 Dec;168(4):1843-53 PMID: 15611161
  37. Novel analogs of D-e-MAPP and B13. Part 1: synthesis and evaluation as potential anticancer agents.
    Bioorg Med Chem. 2008 Jan 15;16(2):1015-31 PMID: 17869115
  38. Probing the mechanism of FET3 repression by Izh2p overexpression.
    Biochim Biophys Acta. 2007 Jul;1773(7):1124-32 PMID: 17553578
  39. Lag1p and Lac1p are essential for the Acyl-CoA-dependent ceramide synthase reaction in Saccharomyces cerevisae.
    Mol Biol Cell. 2001 Nov;12(11):3417-27 PMID: 11694577
  40. Globular adiponectin induces adhesion molecule expression through the sphingosine kinase pathway in vascular endothelial cells.
    Life Sci. 2007 Aug 23;81(11):939-43 PMID: 17822721
Article Info
Journal
Molecular pharmacology
Abbr.
Mol Pharmacol
ISSN
1521-0111
Published
2009-04-00
Epub
2008-00-09
Pages
866-75
Language
English
Region
United States
NLM ID
0035623
PMCID
PMC2684929
Subset
IM
Grants
NIDDK NIH HHS · R21 DK074812-02 · United States
NIDDK NIH HHS · R21 DK074812-01 · United States
NIDDK NIH HHS · R21-DK074812 · United States
NIDDK NIH HHS · R21 DK074812 · United States
NIGMS NIH HHS · GM63265 · United States
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com