Multivalent Mechanism of Membrane Insertion by the FYVE Domain

Targeting of a wide variety of proteins to membranes involves specific recognition of phospholipid head groups and insertion into lipid bilayers. For example, proteins that contain FYVE domains are recruited to endosomes through interaction with phosphatidylinositol 3-phosphate (PtdIns(3)P). However...

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Published inThe Journal of biological chemistry Vol. 279; no. 4; pp. 3050 - 3057
Main Authors Kutateladze, Tatiana G., Capelluto, Daniel G.S., Ferguson, Colin G., Cheever, Matthew L., Kutateladze, Andrei G., Prestwich, Glenn D., Overduin, Michael
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 23.01.2004
American Society for Biochemistry and Molecular Biology
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Abstract Targeting of a wide variety of proteins to membranes involves specific recognition of phospholipid head groups and insertion into lipid bilayers. For example, proteins that contain FYVE domains are recruited to endosomes through interaction with phosphatidylinositol 3-phosphate (PtdIns(3)P). However, the structural mechanism of membrane docking and insertion by this domain remains unclear. Here, the depth and angle of micelle insertion and the lipid binding properties of the FYVE domain of early endosome antigen 1 are estimated by NMR spectroscopy. Spin label probes incorporated into micelles identify a hydrophobic protuberance that inserts into the micelle core and is surrounded by interfacially active polar residues. A novel proxyl PtdIns(3)P derivative is developed to map the position of the phosphoinositide acyl chains, which are found to align with the membrane insertion element. Dual engagement of the FYVE domain with PtdIns(3)P and dodecylphosphocholine micelles yields a 6-fold enhancement of affinity. The additional interaction of phosphatidylserine with a conserved basic site of the protein further amplifies the micelle binding affinity and dramatically alters the angle of insertion. Thus, the FYVE domain is targeted to endosomes through the synergistic action of stereospecific PtdIns(3)P head group ligation, hydrophobic insertion and electrostatic interactions with acidic phospholipids.
AbstractList Targeting of a wide variety of proteins to membranes involves specific recognition of phospholipid head groups and insertion into lipid bilayers. For example, proteins that contain FYVE domains are recruited to endosomes through interaction with phosphatidylinositol 3-phosphate (PtdIns(3)P). However, the structural mechanism of membrane docking and insertion by this domain remains unclear. Here, the depth and angle of micelle insertion and the lipid binding properties of the FYVE domain of early endosome antigen 1 are estimated by NMR spectroscopy. Spin label probes incorporated into micelles identify a hydrophobic protuberance that inserts into the micelle core and is surrounded by interfacially active polar residues. A novel proxyl PtdIns(3)P derivative is developed to map the position of the phosphoinositide acyl chains, which are found to align with the membrane insertion element. Dual engagement of the FYVE domain with PtdIns(3)P and dodecylphosphocholine micelles yields a 6-fold enhancement of affinity. The additional interaction of phosphatidylserine with a conserved basic site of the protein further amplifies the micelle binding affinity and dramatically alters the angle of insertion. Thus, the FYVE domain is targeted to endosomes through the synergistic action of stereospecific PtdIns(3)P head group ligation, hydrophobic insertion and electrostatic interactions with acidic phospholipids.
Targeting of a wide variety of proteins to membranes involves specific recognition of phospholipid head groups and insertion into lipid bilayers. For example, proteins that contain FYVE domains are recruited to endosomes through interaction with phosphatidylinositol 3-phosphate (PtdIns(3)P). However, the structural mechanism of membrane docking and insertion by this domain remains unclear. Here, the depth and angle of micelle insertion and the lipid binding properties of the FYVE domain of early endosome antigen 1 are estimated by NMR spectroscopy. Spin label probes incorporated into micelles identify a hydrophobic protuberance that inserts into the micelle core and is surrounded by interfacially active polar residues. A novel proxyl PtdIns(3)P derivative is developed to map the position of the phosphoinositide acyl chains, which are found to align with the membrane insertion element. Dual engagement of the FYVE domain with PtdIns(3)P and dodecylphosphocholine micelles yields a 6-fold enhancement of affinity. The additional interaction of phosphatidylserine with a conserved basic site of the protein further amplifies the micelle binding affinity and dramatically alters the angle of insertion. Thus, the FYVE domain is targeted to endosomes through the synergistic action of stereospecific PtdIns(3)P head group ligation, hydrophobic insertion and electrostatic interactions with acidic phospholipids.
Author Prestwich, Glenn D.
Kutateladze, Tatiana G.
Capelluto, Daniel G.S.
Kutateladze, Andrei G.
Ferguson, Colin G.
Overduin, Michael
Cheever, Matthew L.
Author_xml – sequence: 1
  givenname: Tatiana G.
  surname: Kutateladze
  fullname: Kutateladze, Tatiana G.
  email: Tatiana.Kutateladze@UCHSC.edu
  organization: Department of Pharmacology, University of Colorado Health Sciences Center, Denver, Colorado 80262
– sequence: 2
  givenname: Daniel G.S.
  surname: Capelluto
  fullname: Capelluto, Daniel G.S.
  organization: Department of Pharmacology, University of Colorado Health Sciences Center, Denver, Colorado 80262
– sequence: 3
  givenname: Colin G.
  surname: Ferguson
  fullname: Ferguson, Colin G.
  organization: Echelon Biosciences Inc., Salt Lake City, Utah 84108
– sequence: 4
  givenname: Matthew L.
  surname: Cheever
  fullname: Cheever, Matthew L.
  organization: Department of Pharmacology, University of Colorado Health Sciences Center, Denver, Colorado 80262
– sequence: 5
  givenname: Andrei G.
  surname: Kutateladze
  fullname: Kutateladze, Andrei G.
  organization: Department of Chemistry and Biochemistry, The University of Denver, Denver, Colorado 80210
– sequence: 6
  givenname: Glenn D.
  surname: Prestwich
  fullname: Prestwich, Glenn D.
  organization: Department of Medicinal Chemistry, The University of Utah, Salt Lake City, Utah 84108
– sequence: 7
  givenname: Michael
  surname: Overduin
  fullname: Overduin, Michael
  organization: Department of Pharmacology, University of Colorado Health Sciences Center, Denver, Colorado 80262
BackLink https://www.ncbi.nlm.nih.gov/pubmed/14578346$$D View this record in MEDLINE/PubMed
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Snippet Targeting of a wide variety of proteins to membranes involves specific recognition of phospholipid head groups and insertion into lipid bilayers. For example,...
Targeting of a wide variety of proteins to membranes involves specific recognition of phospholipid head groups and insertion into lipid bilayers. For example,...
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SubjectTerms Binding Sites
Cell Membrane - chemistry
Cell Membrane - metabolism
Humans
Membrane Proteins - chemistry
Membrane Proteins - metabolism
Models, Molecular
Protein Binding
Protein Conformation
Protein Structure, Tertiary
Protein Transport
Vesicular Transport Proteins
Title Multivalent Mechanism of Membrane Insertion by the FYVE Domain
URI https://dx.doi.org/10.1074/jbc.M309007200
http://www.jbc.org/content/279/4/3050.abstract
https://www.ncbi.nlm.nih.gov/pubmed/14578346
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