|
Originally published In Press as doi:10.1074/jbc.M309840200 on October 1, 2003
J. Biol. Chem., Vol. 278, Issue 50, 50128-50135, December 12, 2003
Reversible Topological Organization within a Polytopic Membrane Protein Is Governed by a Change in Membrane Phospholipid Composition*
Wei Zhang ,
Mikhail Bogdanov ,
Jing Pi ,
A. James Pittard , and
William Dowhan ¶
From the
Department of Biochemistry and Molecular Biology, University of Texas, Medical School and Graduate School of Biomedical Sciences, Houston, Texas 77030 and the Department of Microbiology and Immunology, University of Melbourne, Victoria 3010, Australia
Once inserted, transmembrane segments of polytopic membrane proteins are generally considered stably oriented due to the large free energy barrier to topological reorientation of adjacent extramembrane domains. However, the topology and function of the polytopic membrane protein lactose permease of Escherichia coli are dependent on the membrane phospholipid composition, revealing topological dynamics of transmembrane domains after stable membrane insertion (Bogdanov, M., Heacock, P. N., and Dowhan, W. (2002) EMBO J. 21, 21072116). In this study, we show that the high affinity phenylalanine permease PheP shares many similarities with lactose permease. PheP assembled in a mutant of E. coli lacking phosphatidylethanolamine (PE) exhibited significantly reduced active transport function and a complete inversion in topological orientation of the N terminus and adjoining transmembrane hairpin loop compared with PheP in a PE-containing strain. Introduction of PE following the assembly of PheP triggered a reorientation of the N terminus and adjacent hairpin to their native orientation associated with regain of wild-type transport function. The reversible orientation of these secondary transport proteins in response to a change in phospholipid composition might be a result of inherent conformational flexibility necessary for transport function or during protein assembly.
Received for publication, September 4, 2003
, and in revised form, October 1, 2003.
* This work was supported in part by National Institutes of Health Grant GM20487 (to W. D.) and the Australian Research Council Large Grants Scheme (to A. J. P.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
¶ To whom correspondence should be addressed: Dept. of Biochemistry and Molecular Biology, University of Texas Medical School, 6431 Fannin St., Suite 6.200, P. O. Box 20708, Houston, TX 77030. Tel.: 713-500-6051; Fax: 713-500-0652; E-mail: William.Dowhan{at}uth.tmc.edu.

CiteULike Complore Connotea Del.icio.us Digg Reddit Technorati What's this?
This article has been cited by other articles:

|
 |

|
 |
 
M. Bogdanov, J. Xie, and W. Dowhan
Lipid-Protein Interactions Drive Membrane Protein Topogenesis in Accordance with the Positive Inside Rule
J. Biol. Chem.,
April 10, 2009;
284(15):
9637 - 9641.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Dowhan
Molecular genetic approaches to defining lipid function
J. Lipid Res.,
April 1, 2009;
50(Supplement):
S305 - S310.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Wikstrom, A. A. Kelly, A. Georgiev, H. M. Eriksson, M. R. Klement, M. Bogdanov, W. Dowhan, and A. Wieslander
Lipid-engineered Escherichia coli Membranes Reveal Critical Lipid Headgroup Size for Protein Function
J. Biol. Chem.,
January 9, 2009;
284(2):
954 - 965.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Bogdanov, J. Xie, P. Heacock, and W. Dowhan
To flip or not to flip: lipid-protein charge interactions are a determinant of final membrane protein topology
J. Cell Biol.,
September 9, 2008;
182(5):
925 - 935.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Soto and G. M. Carman
Regulation of the Saccharomyces cerevisiae CKI1-encoded Choline Kinase by Zinc Depletion
J. Biol. Chem.,
April 11, 2008;
283(15):
10079 - 10088.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Hakizimana, M. Masureel, B. Gbaguidi, J.-M. Ruysschaert, and C. Govaerts
Interactions between Phosphatidylethanolamine Headgroup and LmrP, a Multidrug Transporter: A CONSERVED MECHANISM FOR PROTON GRADIENT SENSING?
J. Biol. Chem.,
April 4, 2008;
283(14):
9369 - 9376.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Xie, M. Bogdanov, P. Heacock, and W. Dowhan
Phosphatidylethanolamine and Monoglucosyldiacylglycerol Are Interchangeable in Supporting Topogenesis and Function of the Polytopic Membrane Protein Lactose Permease
J. Biol. Chem.,
July 14, 2006;
281(28):
19172 - 19178.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Zhang, H. A. Campbell, S. C. King, and W. Dowhan
Phospholipids as Determinants of Membrane Protein Topology: PHOSPHATIDYLETHANOLAMINE IS REQUIRED FOR THE PROPER TOPOLOGICAL ORGANIZATION OF THE {gamma}-AMINOBUTYRIC ACID PERMEASE (GabP) OF ESCHERICHIA COLI
J. Biol. Chem.,
July 15, 2005;
280(28):
26032 - 26038.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. A. Dodd, B. Niederoest, S. Bloechlinger, L. Dupuis, J.-P. Loeffler, and M. E. Schwab
Nogo-A, -B, and -C Are Found on the Cell Surface and Interact Together in Many Different Cell Types
J. Biol. Chem.,
April 1, 2005;
280(13):
12494 - 12502.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Llorente-Cortes and L. Badimon
LDL Receptor-Related Protein and the Vascular Wall: Implications for Atherothrombosis
Arterioscler. Thromb. Vasc. Biol.,
March 1, 2005;
25(3):
497 - 504.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. P. Roosild, J. Greenwald, M. Vega, S. Castronovo, R. Riek, and S. Choe
NMR Structure of Mistic, a Membrane-Integrating Protein for Membrane Protein Expression
Science,
February 25, 2005;
307(5713):
1317 - 1321.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. H. Kim, A. B. Chang, and M. H. Saier Jr
Sequence similarity between multidrug resistance efflux pumps of the ABC and RND superfamilies
Microbiology,
August 1, 2004;
150(8):
2493 - 2495.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Llorente-Cortes, M. Otero-Vinas, S. Camino-Lopez, O. Llampayas, and L. Badimon
Aggregated Low-Density Lipoprotein Uptake Induces Membrane Tissue Factor Procoagulant Activity and Microparticle Release in Human Vascular Smooth Muscle Cells
Circulation,
July 27, 2004;
110(4):
452 - 459.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Wikstrom, J. Xie, M. Bogdanov, E. Mileykovskaya, P. Heacock, A. Wieslander, and W. Dowhan
Monoglucosyldiacylglycerol, a Foreign Lipid, Can Substitute for Phosphatidylethanolamine in Essential Membrane-associated Functions in Escherichia coli
J. Biol. Chem.,
March 12, 2004;
279(11):
10484 - 10493.
[Abstract]
[Full Text]
[PDF]
|
 |
|
Copyright © 2003 by the American Society for Biochemistry and Molecular Biology.
|
Advertisement
Advertisement
|