Home LiteratureArticle Details
PMID: 17707914 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Mechanistic similarities in docking of the FYVE and PX domains to phosphatidylinositol 3-phosphate containing membranes.

Progress in lipid research ·Vol. 46 ·No. 6 ·2007-11-00 ·Pages 315-27

Kutateladze TG

Abstract

Phosphatidylinositol 3-phosphate [PtdIns(3)P], a phospholipid produced by PI 3-kinases in early endosomes and multivesicular bodies, often serves as a marker of endosomal membranes. PtdIns(3)P recruits and activates effector proteins containing the FYVE or PX domain and therefore regulates a variety of biological processes including endo- and exocytosis, membrane trafficking, protein sorting, signal transduction and cytoskeletal rearrangement. Structures and PtdIns(3)P binding modes of several FYVE and PX domains have recently been characterized, unveiling the molecular basis underlying multiple cellular functions of these proteins. Here, structural and functional aspects and current mechanisms of the multivalent membrane anchoring by the FYVE and PX domains are reviewed and compared.

MeSH Terms
Cell Membrane/metabolism Histidine/metabolism Humans Hydrophobic and Hydrophilic Interactions Membrane Proteins/metabolism Molecular Structure Phosphatidylinositol 3-Kinases/metabolism Phosphatidylinositol Phosphates/metabolism Protein Binding/physiology Static Electricity
Chemicals
Membrane Proteins Phosphatidylinositol Phosphates phosphatidylinositol 3-phosphate Histidine Phosphatidylinositol 3-Kinases PIKFYVE protein, human
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Kutateladze Tatiana G
Department of Pharmacology, University of Colorado Health Sciences Center, Aurora, CO 80045, USA. Tatiana.Kutateladze@UCHSC.edu
References (108)
108 references, click to expand
  1. Phosphatidylinositol 3-phosphate recognition and membrane docking by the FYVE domain.
    Biochim Biophys Acta. 2006 Aug;1761(8):868-77 PMID: 16644267
  2. The Phox (PX) domain proteins and membrane traffic.
    Biochim Biophys Acta. 2006 Aug;1761(8):878-96 PMID: 16782399
  3. Orientation and penetration depth of monolayer-bound p40phox-PX.
    Biochemistry. 2006 Nov 14;45(45):13566-75 PMID: 17087510
  4. Molecular mechanism of membrane docking by the Vam7p PX domain.
    J Biol Chem. 2006 Dec 1;281(48):37091-101 PMID: 16984909
  5. Structural and membrane binding analysis of the Phox homology domain of phosphoinositide 3-kinase-C2alpha.
    J Biol Chem. 2006 Dec 22;281(51):39396-406 PMID: 17038310
  6. Full-length p40phox structure suggests a basis for regulation mechanism of its membrane binding.
    EMBO J. 2007 Feb 21;26(4):1176-86 PMID: 17290225
  7. Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes.
    Nat Cell Biol. 2001 Jul;3(7):613-8 PMID: 11433291
  8. SNX3 regulates endosomal function through its PX-domain-mediated interaction with PtdIns(3)P.
    Nat Cell Biol. 2001 Jul;3(7):658-66 PMID: 11433298
  9. The PX domains of p47phox and p40phox bind to lipid products of PI(3)K.
    Nat Cell Biol. 2001 Jul;3(7):675-8 PMID: 11433300
  10. PtdIns(3)P regulates the neutrophil oxidase complex by binding to the PX domain of p40(phox).
    Nat Cell Biol. 2001 Jul;3(7):679-82 PMID: 11433301
  11. Mammalian cell morphology and endocytic membrane homeostasis require enzymatically active phosphoinositide 5-kinase PIKfyve.
    J Biol Chem. 2001 Jul 13;276(28):26141-7 PMID: 11285266
  12. High-affinity binding of a FYVE domain to phosphatidylinositol 3-phosphate requires intact phospholipid but not FYVE domain oligomerization.
    Biochemistry. 2001 Jul 24;40(29):8581-7 PMID: 11456498
  13. Phox homology domains specifically bind phosphatidylinositol phosphates.
    Biochemistry. 2001 Jul 31;40(30):8940-4 PMID: 11467955
  14. A large family of endosome-localized proteins related to sorting nexin 1.
    Biochem J. 2001 Aug 15;358(Pt 1):7-16 PMID: 11485546
  15. Involvement of Hgs/Hrs in signaling for cytokine-mediated c-fos induction through interaction with TAK1 and Pak1.
    J Biol Chem. 2001 Aug 10;276(32):29943-52 PMID: 11397816
  16. Regulation of cytokine-independent survival kinase (CISK) by the Phox homology domain and phosphoinositides.
    J Cell Biol. 2001 Aug 20;154(4):699-705 PMID: 11514587
  17. Hrs recruits clathrin to early endosomes.
    EMBO J. 2001 Sep 3;20(17):5008-21 PMID: 11532964
  18. FYVE domain targets Pib1p ubiquitin ligase to endosome and vacuolar membranes.
    J Biol Chem. 2001 Nov 2;276(44):41388-93 PMID: 11526110
  19. The crystal structure of the PX domain from p40(phox) bound to phosphatidylinositol 3-phosphate.
    Mol Cell. 2001 Oct;8(4):829-39 PMID: 11684018
  20. All phox homology (PX) domains from Saccharomyces cerevisiae specifically recognize phosphatidylinositol 3-phosphate.
    J Biol Chem. 2001 Nov 23;276(47):44179-84 PMID: 11557775
  21. RGS-PX1, a GAP for GalphaS and sorting nexin in vesicular trafficking.
    Science. 2001 Nov 30;294(5548):1939-42 PMID: 11729322
  22. A functional PtdIns(3)P-binding motif.
    Nature. 1998 Jul 30;394(6692):433-4 PMID: 9697765
  23. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion.
    Nature. 1998 Jul 30;394(6692):494-8 PMID: 9697774
  24. Phosphatidylinositol(3)-phosphate signaling mediated by specific binding to RING FYVE domains.
    Mol Cell. 1998 Jul;2(1):157-62 PMID: 9702203
  25. Vam7p, a SNAP-25-like molecule, and Vam3p, a syntaxin homolog, function together in yeast vacuolar protein trafficking.
    Mol Cell Biol. 1998 Sep;18(9):5308-19 PMID: 9710615
  26. Na+/H+ antiport in Swiss 3T3 cells: mitogenic stimulation leads to cytoplasmic alkalinization.
    Proc Natl Acad Sci U S A. 1982 Dec;79(24):7778-82 PMID: 6961450
  27. Na+/H+ exchange and cytoplasmic pH in the action of growth factors in human fibroblasts.
    Nature. 1983 Aug 18-24;304(5927):645-8 PMID: 6410286
  28. Evaluation of pH changes in inflammation of the subcutaneous air pouch lining in the rat, induced by carrageenan, dextran and Staphylococcus aureus.
    J Oral Pathol. 1987 Jan;16(1):36-44 PMID: 2435877
  29. Role of protein kinase C and the Na+/H+ antiporter in suppression of apoptosis by granulocyte macrophage colony-stimulating factor and interleukin-3.
    J Biol Chem. 1992 May 15;267(14):9980-7 PMID: 1315776
  30. Attenuation of methamphetamine-induced neurotoxicity in copper/zinc superoxide dismutase transgenic mice.
    J Neurochem. 1994 Jan;62(1):380-3 PMID: 7505315
  31. The Saccharomyces cerevisiae MVP1 gene interacts with VPS1 and is required for vacuolar protein sorting.
    Mol Cell Biol. 1995 Mar;15(3):1671-8 PMID: 7862158
  32. Cell acidification in apoptosis: granulocyte colony-stimulating factor delays programmed cell death in neutrophils by up-regulating the vacuolar H(+)-ATPase.
    Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5965-8 PMID: 7541139
  33. VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae.
    J Cell Biol. 1995 Nov;131(3):603-17 PMID: 7593183
  34. Cellular pH gradient in tumor versus normal tissue: potential exploitation for the treatment of cancer.
    Cancer Res. 1996 Mar 15;56(6):1194-8 PMID: 8640796
  35. Hypoxia/ischemia and the pH paradox.
    Adv Exp Med Biol. 1996;388:283-92 PMID: 8798824
  36. Endosomal localization of the autoantigen EEA1 is mediated by a zinc-binding FYVE finger.
    J Biol Chem. 1996 Sep 27;271(39):24048-54 PMID: 8798641
  37. Novel domains in NADPH oxidase subunits, sorting nexins, and PtdIns 3-kinases: binding partners of SH3 domains?
    Protein Sci. 1996 Nov;5(11):2353-7 PMID: 8931154
  38. Retrieval of resident late-Golgi membrane proteins from the prevacuolar compartment of Saccharomyces cerevisiae is dependent on the function of Grd19p.
    J Cell Biol. 1998 Feb 9;140(3):577-90 PMID: 9456318
  39. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function.
    Nature. 1998 Mar 12;392(6672):193-7 PMID: 9515966
  40. FYVE fingers bind PtdIns(3)P.
    Nature. 1998 Jul 30;394(6692):432-3 PMID: 9697764
  41. Phosphatidylinositol-3-OH kinases are Rab5 effectors.
    Nat Cell Biol. 1999 Aug;1(4):249-52 PMID: 10559924
  42. Selective membrane recruitment of EEA1 suggests a role in directional transport of clathrin-coated vesicles to early endosomes.
    J Biol Chem. 2000 Feb 11;275(6):3745-8 PMID: 10660521
  43. Crystal structure of the VHS and FYVE tandem domains of Hrs, a protein involved in membrane trafficking and signal transduction.
    Cell. 2000 Feb 18;100(4):447-56 PMID: 10693761
  44. Myotubularin, a protein tyrosine phosphatase mutated in myotubular myopathy, dephosphorylates the lipid second messenger, phosphatidylinositol 3-phosphate.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8910-5 PMID: 10900271
  45. Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities.
    Biochem J. 2000 Oct 1;351(Pt 1):19-31 PMID: 11001876
  46. A FYVE-finger-containing protein, Rabip4, is a Rab4 effector involved in early endosomal traffic.
    Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1637-42 PMID: 11172003
  47. Structural mechanism of endosome docking by the FYVE domain.
    Science. 2001 Mar 2;291(5509):1793-6 PMID: 11230696
  48. Characterization of a novel phosphatidylinositol 3-phosphate-binding protein containing two FYVE fingers in tandem that is targeted to the Golgi.
    Biochem J. 2001 Apr 1;355(Pt 1):113-21 PMID: 11256955
  49. Intracellular trafficking and turnover of phosphatidylinositol 3-phosphate.
    Semin Cell Dev Biol. 2001 Apr;12(2):193-9 PMID: 11292385
  50. Self-assembly and binding of a sorting nexin to sorting endosomes.
    J Cell Sci. 2001 May;114(Pt 9):1743-56 PMID: 11309204
  51. Solution structure of the PX domain, a target of the SH3 domain.
    Nat Struct Biol. 2001 Jun;8(6):526-30 PMID: 11373621
  52. Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes.
    Curr Biol. 1998 Jul 16;8(15):881-4 PMID: 9705936
  53. Phosphoinositide signaling and turnover: PtdIns(3)P, a regulator of membrane traffic, is transported to the vacuole and degraded by a process that requires lumenal vacuolar hydrolase activities.
    EMBO J. 1998 Sep 1;17(17):4930-42 PMID: 9724630
  54. Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis.
    J Cell Biol. 1998 Oct 5;143(1):65-79 PMID: 9763421
  55. The stress-activated phosphatidylinositol 3-phosphate 5-kinase Fab1p is essential for vacuole function in S. cerevisiae.
    Curr Biol. 1998 Nov 5;8(22):1219-22 PMID: 9811604
  56. SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor.
    Cell. 1998 Dec 11;95(6):779-91 PMID: 9865696
  57. Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body.
    Cell. 1998 Dec 11;95(6):847-58 PMID: 9865702
  58. Vac1p coordinates Rab and phosphatidylinositol 3-kinase signaling in Vps45p-dependent vesicle docking/fusion at the endosome.
    Curr Biol. 1999 Feb 11;9(3):159-62 PMID: 10021387
  59. The endosome fusion regulator early-endosomal autoantigen 1 (EEA1) is a dimer.
    Biochem J. 1999 Mar 1;338 ( Pt 2):539-43 PMID: 10024533
  60. Hrs, a FYVE finger protein localized to early endosomes, is implicated in vesicular traffic and required for ventral folding morphogenesis.
    Genes Dev. 1999 Jun 1;13(11):1475-85 PMID: 10364163
  61. Crystal structure of a phosphatidylinositol 3-phosphate-specific membrane-targeting motif, the FYVE domain of Vps27p.
    Cell. 1999 May 28;97(5):657-66 PMID: 10367894
  62. Phosphatidylinositol 3-phosphate recognition by the FYVE domain.
    Mol Cell. 1999 Jun;3(6):805-11 PMID: 10394369
  63. PIKfyve, a mammalian ortholog of yeast Fab1p lipid kinase, synthesizes 5-phosphoinositides. Effect of insulin.
    J Biol Chem. 1999 Jul 30;274(31):21589-97 PMID: 10419465
  64. Mammalian phospholipase D structure and regulation.
    Biochim Biophys Acta. 1999 Jul 30;1439(2):175-86 PMID: 10425394
  65. Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13.
    Cell. 1999 Aug 6;98(3):377-86 PMID: 10458612
  66. Regulation of acidification and apoptosis by SHP-1 and Bcl-2.
    J Biol Chem. 1999 Oct 8;274(41):29549-57 PMID: 10506221
  67. The molecular basis of the differential subcellular localization of FYVE domains.
    J Biol Chem. 2004 Dec 17;279(51):53818-27 PMID: 15452113
  68. Mechanism of membrane binding of the phospholipase D1 PX domain.
    J Biol Chem. 2004 Dec 24;279(52):54918-26 PMID: 15475361
  69. The role of internalization in transforming growth factor beta1-induced Smad2 association with Smad anchor for receptor activation (SARA) and Smad2-dependent signaling in human mesangial cells.
    J Biol Chem. 2005 Mar 4;280(9):8300-8 PMID: 15613484
  70. FENS-1 and DFCP1 are FYVE domain-containing proteins with distinct functions in the endosomal and Golgi compartments.
    J Cell Sci. 2001 Nov;114(Pt 22):3991-4000 PMID: 11739631
  71. Multivalent endosome targeting by homodimeric EEA1.
    Mol Cell. 2001 Nov;8(5):947-58 PMID: 11741531
  72. Synthesis and function of 3-phosphorylated inositol lipids.
    Annu Rev Biochem. 2001;70:535-602 PMID: 11395417
  73. Phosphatidylinositol 3-phosphate-interacting domains in PIKfyve. Binding specificity and role in PIKfyve. Endomenbrane localization.
    J Biol Chem. 2002 Feb 22;277(8):6073-9 PMID: 11706043
  74. The FYVE domain in Smad anchor for receptor activation (SARA) is sufficient for localization of SARA in early endosomes and regulates TGF-beta/Smad signalling.
    Genes Cells. 2002 Mar;7(3):321-31 PMID: 11918675
  75. Solution structure of the Vam7p PX domain.
    Biochemistry. 2002 May 14;41(19):5956-62 PMID: 11993989
  76. Early endosomal regulation of Smad-dependent signaling in endothelial cells.
    J Biol Chem. 2002 May 17;277(20):18046-52 PMID: 11877415
  77. Endosomal localization and function of sorting nexin 1.
    Proc Natl Acad Sci U S A. 2002 May 14;99(10):6767-72 PMID: 11997453
  78. The phosphoinositide 3-kinase pathway.
    Science. 2002 May 31;296(5573):1655-7 PMID: 12040186
  79. Phosphatidylinositol 3-phosphate induces the membrane penetration of the FYVE domains of Vps27p and Hrs.
    J Biol Chem. 2002 Jul 19;277(29):26379-88 PMID: 12006563
  80. Binding of the PX domain of p47(phox) to phosphatidylinositol 3,4-bisphosphate and phosphatidic acid is masked by an intramolecular interaction.
    EMBO J. 2002 Oct 1;21(19):5057-68 PMID: 12356722
  81. TGF beta receptor internalization into EEA1-enriched early endosomes: role in signaling to Smad2.
    J Cell Biol. 2002 Sep 30;158(7):1239-49 PMID: 12356868
  82. Sorting out the cellular functions of sorting nexins.
    Nat Rev Mol Cell Biol. 2002 Dec;3(12):919-31 PMID: 12461558
  83. The phox homology (PX) domain-dependent, 3-phosphoinositide-mediated association of sorting nexin-1 with an early sorting endosomal compartment is required for its ability to regulate epidermal growth factor receptor degradation.
    J Biol Chem. 2002 Dec 13;277(50):48730-6 PMID: 12198132
  84. Retromer and the sorting nexins Snx4/41/42 mediate distinct retrieval pathways from yeast endosomes.
    EMBO J. 2003 Feb 3;22(3):548-57 PMID: 12554655
  85. Membrane binding mechanisms of the PX domains of NADPH oxidase p40phox and p47phox.
    J Biol Chem. 2003 Apr 18;278(16):14469-79 PMID: 12556460
  86. Computer modeling of the membrane interaction of FYVE domains.
    J Mol Biol. 2003 May 2;328(3):721-36 PMID: 12706728
  87. The adaptor protein fish associates with members of the ADAMs family and localizes to podosomes of Src-transformed cells.
    J Biol Chem. 2003 May 9;278(19):16844-51 PMID: 12615925
  88. Vps27 recruits ESCRT machinery to endosomes during MVB sorting.
    J Cell Biol. 2003 Aug 4;162(3):413-23 PMID: 12900393
  89. Evidence for a role of SNX16 in regulating traffic between the early and later endosomal compartments.
    J Biol Chem. 2003 Sep 5;278(36):34617-30 PMID: 12813048
  90. Crystal structure of the yeast Phox homology (PX) domain protein Grd19p complexed to phosphatidylinositol-3-phosphate.
    J Biol Chem. 2003 Dec 12;278(50):50371-6 PMID: 14514667
  91. Multivalent mechanism of membrane insertion by the FYVE domain.
    J Biol Chem. 2004 Jan 23;279(4):3050-7 PMID: 14578346
  92. Structural basis for endosomal targeting by FYVE domains.
    J Biol Chem. 2004 Feb 13;279(7):5958-66 PMID: 14594806
  93. Acquisition of Hrs, an essential component of phagosomal maturation, is impaired by mycobacteria.
    Mol Cell Biol. 2004 May;24(10):4593-604 PMID: 15121875
  94. Characterization of Tollip protein upon Lipopolysaccharide challenge.
    Mol Immunol. 2004 May;41(1):85-92 PMID: 15140579
  95. A role for Hrs in endosomal sorting of ligand-stimulated and unstimulated epidermal growth factor receptor.
    Exp Cell Res. 2004 Jul 15;297(2):380-91 PMID: 15212941
  96. Structural basis of membrane targeting by the Phox homology domain of cytokine-independent survival kinase (CISK-PX).
    J Biol Chem. 2004 Jul 16;279(29):30662-9 PMID: 15126499
  97. Interaction of the EEA1 FYVE finger with phosphatidylinositol 3-phosphate and early endosomes. Role of conserved residues.
    J Biol Chem. 2000 Aug 11;275(32):24595-600 PMID: 10807926
  98. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells.
    EMBO J. 2000 Sep 1;19(17):4577-88 PMID: 10970851
  99. Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain.
    J Cell Biol. 2000 Oct 30;151(3):601-12 PMID: 11062261
  100. Hgs (Hrs), a FYVE domain protein, is involved in Smad signaling through cooperation with SARA.
    Mol Cell Biol. 2000 Dec;20(24):9346-55 PMID: 11094085
  101. Determinants of the endosomal localization of sorting nexin 1.
    Mol Biol Cell. 2005 Apr;16(4):2049-57 PMID: 15673616
  102. Analysis of phosphoinositide binding domain properties within the myotubularin-related protein MTMR3.
    J Cell Sci. 2005 May 1;118(Pt 9):2005-12 PMID: 15840652
  103. Targeting of the FYVE domain to endosomal membranes is regulated by a histidine switch.
    Proc Natl Acad Sci U S A. 2005 Sep 13;102(37):13052-7 PMID: 16141328
  104. Phosphatidylinositol (3,4,5)-trisphosphate specifically interacts with the phox homology domain of phospholipase D1 and stimulates its activity.
    J Cell Sci. 2005 Oct 1;118(Pt 19):4405-13 PMID: 16179605
  105. Sorting nexins.
    Curr Biol. 2005 Oct 25;15(20):R819-20 PMID: 16243015
  106. Investigation of the binding geometry of a peripheral membrane protein.
    Biochemistry. 2005 Dec 13;44(49):16064-71 PMID: 16331966
  107. Regulation of membrane traffic by phosphoinositide 3-kinases.
    J Cell Sci. 2006 Feb 15;119(Pt 4):605-14 PMID: 16467569
  108. Sorting nexin 17, a non-self-assembling and a PtdIns(3)P high class affinity protein, interacts with the cerebral cavernous malformation related protein KRIT1.
    Biochem Biophys Res Commun. 2006 Jul 7;345(3):1264-72 PMID: 16712798
Article Info
Journal
Progress in lipid research
Abbr.
Prog Lipid Res
ISSN
0163-7827
Published
2007-11-00
Epub
2007-00-13
Pages
315-27
Language
English
Region
England
NLM ID
7900832
PMCID
PMC2211451
Subset
IM
Grants
NIGMS NIH HHS · R01 GM071424 · United States
NCI NIH HHS · R01 CA113472 · United States
NIGMS NIH HHS · GM 071424 · United States
NIGMS NIH HHS · R01 GM071424-02 · United States
NCI NIH HHS · CA 113472 · United States
NCI NIH HHS · R01 CA113472-02 · United States
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