Comparison of Saccharomyces cerevisiae F-BAR Domain Structures Reveals a Conserved Inositol Phosphate Binding Site

Moravcevic, Katarina; Alvarado, Diego; Schmitz, Karl R.; Kenniston, Jon A.; Mendrola, Jeannine M.; Ferguson, Kathryn M.; Lemmon, Mark A.

doi:10.1016/j.str.2014.12.009

Title: Comparison of Saccharomyces cerevisiae F-BAR Domain Structures Reveals a Conserved Inositol Phosphate Binding Site

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Abstract

F-BAR domains control membrane interactions in endocytosis, cytokinesis, and cell signaling. Although they are generally thought to bind curved membranes containing negatively charged phospholipids, numerous functional studies argue that differences in lipid-binding selectivities of F-BAR domains are functionally important. Here in this paper, we compare membrane-binding properties of the Saccharomyces cerevisiae F-BAR domains in vitro and in vivo. Whereas some F-BAR domains (such as Bzz1p and Hof1p F-BARs) bind equally well to all phospholipids, the F-BAR domain from the RhoGAP Rgd1p preferentially binds phosphoinositides. We determined X-ray crystal structures of F-BAR domains from Hof1p and Rgd1p, the latter bound to an inositol phosphate. The structures explain phospholipid-binding selectivity differences and reveal an F-BAR phosphoinositide binding site that is fully conserved in a mammalian RhoGAP called Gmip and is partly retained in certain other F-BAR domains. In conclusion, our findings reveal previously unappreciated determinants of F-BAR domain lipid-binding specificity and provide a basis for its prediction from sequence.

Authors:: Moravcevic, Katarina; Alvarado, Diego; Schmitz, Karl R.; Kenniston, Jon A.; Mendrola, Jeannine M.; Ferguson, Kathryn M.; Lemmon, Mark A.

Publication Date:: Sun Feb 01 00:00:00 EST 2015

Research Org.:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Cancer Institute (NCI); National Science Foudnation (NSF); National Institutes of Health (NIH)

OSTI Identifier:: 1236716

Alternate Identifier(s):: OSTI ID: 1182313; OSTI ID: 1233884

Grant/Contract Number:: W-31-109-ENG-38; DMR-0225180; R01-GM056846; RR-01646; 61-1316; T32-GM008275

Resource Type:: Published Article

Journal Name:: Structure

Additional Journal Information:: Journal Name: Structure Journal Volume: 23 Journal Issue: 2; Journal ID: ISSN 0969-2126

Publisher:: Elsevier

Country of Publication:: United Kingdom

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats


                    Moravcevic, Katarina, Alvarado, Diego, Schmitz, Karl R., Kenniston, Jon A., Mendrola, Jeannine M., Ferguson, Kathryn M., and Lemmon, Mark A. Comparison of Saccharomyces cerevisiae F-BAR Domain Structures Reveals a Conserved Inositol Phosphate Binding Site.  United Kingdom: N. p., 2015. 
Web.  doi:10.1016/j.str.2014.12.009.

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                    Moravcevic, Katarina, Alvarado, Diego, Schmitz, Karl R., Kenniston, Jon A., Mendrola, Jeannine M., Ferguson, Kathryn M., & Lemmon, Mark A. Comparison of Saccharomyces cerevisiae F-BAR Domain Structures Reveals a Conserved Inositol Phosphate Binding Site.  United Kingdom.  https://doi.org/10.1016/j.str.2014.12.009

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                    Moravcevic, Katarina, Alvarado, Diego, Schmitz, Karl R., Kenniston, Jon A., Mendrola, Jeannine M., Ferguson, Kathryn M., and Lemmon, Mark A. Sun .  
"Comparison of Saccharomyces cerevisiae F-BAR Domain Structures Reveals a Conserved Inositol Phosphate Binding Site".  United Kingdom.  https://doi.org/10.1016/j.str.2014.12.009.

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@article{osti_1236716,

  title        = {Comparison of Saccharomyces cerevisiae F-BAR Domain Structures Reveals a Conserved Inositol Phosphate Binding Site},

  author       = {Moravcevic, Katarina and Alvarado, Diego and Schmitz, Karl R. and Kenniston, Jon A. and Mendrola, Jeannine M. and Ferguson, Kathryn M. and Lemmon, Mark A.},

  abstractNote = {F-BAR domains control membrane interactions in endocytosis, cytokinesis, and cell signaling. Although they are generally thought to bind curved membranes containing negatively charged phospholipids, numerous functional studies argue that differences in lipid-binding selectivities of F-BAR domains are functionally important. Here in this paper, we compare membrane-binding properties of the Saccharomyces cerevisiae F-BAR domains in vitro and in vivo. Whereas some F-BAR domains (such as Bzz1p and Hof1p F-BARs) bind equally well to all phospholipids, the F-BAR domain from the RhoGAP Rgd1p preferentially binds phosphoinositides. We determined X-ray crystal structures of F-BAR domains from Hof1p and Rgd1p, the latter bound to an inositol phosphate. The structures explain phospholipid-binding selectivity differences and reveal an F-BAR phosphoinositide binding site that is fully conserved in a mammalian RhoGAP called Gmip and is partly retained in certain other F-BAR domains. In conclusion, our findings reveal previously unappreciated determinants of F-BAR domain lipid-binding specificity and provide a basis for its prediction from sequence.},

  doi          = {10.1016/j.str.2014.12.009},

  journal      = {Structure},

  number       = 2,

  volume       = 23,

  place        = {United Kingdom},

  year         = {Sun Feb 01 00:00:00 EST 2015},

  month        = {Sun Feb 01 00:00:00 EST 2015}

}

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