An Approach to Membrane Protein Structure Without Crystals

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2002 Oct 23

PMID 12391320

Citations 26

Authors

Paul L Sorgen

Yonglin Hu

Lan Guan

H Ronald Kaback

Mark E Girvin

Affiliations

Soon will be listed here.

Abstract

The lactose permease of Escherichia coli catalyzes coupled translocation of galactosides and H(+) across the cell membrane. It is the best-characterized member of the Major Facilitator Superfamily, a related group of membrane proteins with 12 transmembrane domains that mediate transport of various substrates across cell membranes. Despite decades of effort and their functional importance in all kingdoms of life, no high-resolution structures have been solved for any member of this family. However, extensive biochemical, genetic, and biophysical studies on lactose permease have established its transmembrane topology, secondary structure, and numerous interhelical contacts. Here we demonstrate that this information is sufficient to calculate a structural model at the level of helix packing or better.

Citing Articles

Gate-controlled proton diffusion and protonation-induced ratchet motion in the stator of the bacterial flagellar motor.

Nishihara Y, Kitao A Proc Natl Acad Sci U S A. 2015; 112(25):7737-42.

PMID: 26056313 PMC: 4485142. DOI: 10.1073/pnas.1502991112.

Insights to the evolution of Nucleobase-Ascorbate Transporters (NAT/NCS2 family) from the Cys-scanning analysis of xanthine permease XanQ.

Frillingos S Int J Biochem Mol Biol. 2012; 3(3):250-72.

PMID: 23097742 PMC: 3476789.

Proton-coupled dynamics in lactose permease.

Andersson M, Bondar A, Freites J, Tobias D, Kaback H, White S Structure. 2012; 20(11):1893-904.

PMID: 23000385 PMC: 3496080. DOI: 10.1016/j.str.2012.08.021.

Proline-proline-glutamic acid (PPE) protein Rv1168c of Mycobacterium tuberculosis augments transcription from HIV-1 long terminal repeat promoter.

Bhat K, Chaitanya C, Parveen N, Varman R, Ghosh S, Mukhopadhyay S J Biol Chem. 2012; 287(20):16930-46.

PMID: 22427668 PMC: 3351301. DOI: 10.1074/jbc.M111.327825.

Lactose permease and the alternating access mechanism.

Smirnova I, Kasho V, Kaback H Biochemistry. 2011; 50(45):9684-93.

PMID: 21995338 PMC: 3210931. DOI: 10.1021/bi2014294.

References

Wu J, Hardy D, Kaback H . Tilting of helix I and ligand-induced changes in the lactose permease determined by site-directed chemical cross-linking in situ. Biochemistry. 1998; 37(45):15785-90. DOI: 10.1021/bi981501o. View

He M, Voss J, Hubbell W, Kaback H . Use of designed metal-binding sites to study helix proximity in the lactose permease of Escherichia coli. 1. Proximity of helix VII (Asp237 and Asp240) with helices X (Lys319) and XI (Lys358). Biochemistry. 1995; 34(48):15661-6. DOI: 10.1021/bi00048a009. View

Wang Q, Voss J, Hubbell W, Kaback H . Proximity of helices VIII (Ala273) and IX (Met299) in the lactose permease of Escherichia coli. Biochemistry. 1998; 37(14):4910-5. DOI: 10.1021/bi972990f. View

Stein E, Rice L, Brunger A . Torsion-angle molecular dynamics as a new efficient tool for NMR structure calculation. J Magn Reson. 1997; 124(1):154-64. DOI: 10.1006/jmre.1996.1027. View

Sahin-Toth M, Lawrence M, Nishio T, Kaback H . The C-4 hydroxyl group of galactopyranosides is the major determinant for ligand recognition by the lactose permease of Escherichia coli. Biochemistry. 2001; 40(43):13015-9. DOI: 10.1021/bi011233l. View

Kwaw I, Sun J, Kaback H . Thiol cross-linking of cytoplasmic loops in the lactose permease of Escherichia coli. Biochemistry. 2000; 39(11):3134-40. DOI: 10.1021/bi992509g. View

Venkatesan P, Liu Z, Hu Y, Kaback H . Site-directed sulfhydryl labeling of the lactose permease of Escherichia coli: N-ethylmaleimide-sensitive face of helix II. Biochemistry. 2000; 39(35):10649-55. DOI: 10.1021/bi0004394. View

HEYMANN J, Sarker R, Hirai T, Shi D, Milne J, Maloney P . Projection structure and molecular architecture of OxlT, a bacterial membrane transporter. EMBO J. 2001; 20(16):4408-13. PMC: 125264. DOI: 10.1093/emboj/20.16.4408. View

Guan L, Weinglass A, Kaback H . Helix packing in the lactose permease of Escherichia coli: localization of helix VI. J Mol Biol. 2001; 312(1):69-77. DOI: 10.1006/jmbi.2001.4933. View

10.

Wang Q, Kaback H . Proximity relationships between helices I and XI or XII in the lactose permease of Escherichia coli determined by site-directed thiol cross-linking. J Mol Biol. 1999; 291(3):683-92. DOI: 10.1006/jmbi.1999.2948. View

11.

Costello M, Escaig J, Matsushita K, Viitanen P, Menick D, Kaback H . Purified lac permease and cytochrome o oxidase are functional as monomers. J Biol Chem. 1987; 262(35):17072-82. View

12.

Wu J, Kaback H . Helix proximity and ligand-induced conformational changes in the lactose permease of Escherichia coli determined by site-directed chemical crosslinking. J Mol Biol. 1997; 270(2):285-93. DOI: 10.1006/jmbi.1997.1099. View

13.

Frillingos S, Kaback H . Probing the conformation of the lactose permease of Escherichia coli by in situ site-directed sulfhydryl modification. Biochemistry. 1996; 35(13):3950-6. DOI: 10.1021/bi952601m. View

14.

Zhang W, Guan L, Kaback H . Helices VII and X in the lactose permease of Escherichia coli: proximity and ligand-induced distance changes. J Mol Biol. 2002; 315(1):53-62. DOI: 10.1006/jmbi.2001.5206. View

15.

le Coutre J, Kaback H, Patel C, Heginbotham L, Miller C . Fourier transform infrared spectroscopy reveals a rigid alpha-helical assembly for the tetrameric Streptomyces lividans K+ channel. Proc Natl Acad Sci U S A. 1998; 95(11):6114-7. PMC: 27594. DOI: 10.1073/pnas.95.11.6114. View

16.

Kaback H, Wu J . From membrane to molecule to the third amino acid from the left with a membrane transport protein. Q Rev Biophys. 1998; 30(4):333-64. DOI: 10.1017/s0033583597003387. View

17.

Sahin-Toth M, Gunawan P, Lawrence M, Toyokuni T, Kaback H . Binding of hydrophobic D-galactopyranosides to the lactose permease of Escherichia coli. Biochemistry. 2002; 41(43):13039-45. DOI: 10.1021/bi0203076. View

18.

Venkatesan P, Hu Y, Kaback H . Site-directed sulfhydryl labeling of the lactose permease of Escherichia coli: helix X. Biochemistry. 2000; 39(35):10656-61. DOI: 10.1021/bi0004403. View

19.

He M, Voss J, Hubbell W, Kaback H . Arginine 302 (helix IX) in the lactose permease of Escherichia coli is in close proximity to glutamate 269 (helix VIII) as well as glutamate 325. Biochemistry. 1997; 36(44):13682-7. DOI: 10.1021/bi971531b. View

20.

Guan L, Murphy F, Kaback H . Surface-exposed positions in the transmembrane helices of the lactose permease of Escherichia coli determined by intermolecular thiol cross-linking. Proc Natl Acad Sci U S A. 2002; 99(6):3475-80. PMC: 122548. DOI: 10.1073/pnas.052703699. View