Proteins that bind and move lipids: MsbA and NPC1

Critical Reviews in Biochemistry and Molecular Biology

Volumn 47, Issue 1, 2012, Pages 75-95

  King, Gavin ^a   Sharom, Frances J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

ABC transporter; Cholesterol; Lipid A; Lipid binding pocket; Lipid flippase; Niemann Pick Type C disease; NPC2 (Niemann Pick disease, Type C2); Sterol trafficking

Indexed keywords

CHOLESTEROL; LIPID BINDING PROTEIN; LIPOPOLYSACCHARIDE; MEMBRANE LIPID; MSBA PROTEIN; PROTEIN NIEMANN PICK DISEASE TYPE C1; PROTEIN NIEMANN PICK DISEASE TYPE C2; STEROL; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BINDING SITE; BIOSYNTHESIS; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; CYTOSOL; ELECTRON SPIN RESONANCE; ENDOSOME; ESCHERICHIA COLI; GENE MUTATION; HUMAN; LYSOSOME; MEMBRANE FLUIDITY; MOLECULAR SIZE; NIEMANN PICK DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; REVIEW;

AMINO ACID SEQUENCE; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BINDING SITES; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CHOLESTEROL; CRYSTALLOGRAPHY, X-RAY; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENDOSOMES; ESCHERICHIA COLI; HUMANS; LYSOSOMES; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NIEMANN-PICK DISEASES; PHOSPHOLIPID TRANSFER PROTEINS; PHOSPHOLIPIDS;

EID: 83755205841     PISSN: 10409238     EISSN: 15497798     Source Type: Journal    
DOI: 10.3109/10409238.2011.636505     Document Type: Review

References (114)

1. Altmann SW, Davis HR Jr, Zhu LJ, Yao X, Hoos LM, Tetzlof G, Iyer SP, Maguire M, Golovko A, Zeng M, Wang L, Murgolo N, Graziano MP. 2004. Niemann-Pick C1 Like 1 protein is critical for intestinal cholesterol absorption. Science 303:1201-1204.
2. Babalola JO, Wendeler M, Breiden B, Arenz C, Schwarzmann G, Locatelli-Hoops S, Sandhof K. 2007. Development of an assay for the intermembrane transfer of cholesterol by Niemann-Pick C2 protein. Biol Chem 388:617-626.
3. Barb AW, McClerren AL, Snehelatha K, Reynolds CM, Zhou P, Raetz CR. 2007. Inhibition of lipid A biosynthesis as the primary mechanism of CHIR-090 antibiotic activity in Escherichia coli. Biochemistry 46:3793-3802.
4. Beh CT, Alfaro G, Duamel G, Sullivan DP, Kersting MC, Dighe S, Kozminski KG, Menon AK. 2009. Yeast oxysterol-binding proteins: sterol transporters or regulators of cell polarization? Mol Cell Biochem 326:9-13.
5. Borbat PP, Surendhran K, Bortolus M, Zou P, Freed JH, Mchaourab HS. 2007. Conformational motion of the ABC transporter MsbA induced by ATP hydrolysis. PLoS Biol 5:e271.
6. Brown JM, Rudel LL, Yu L. 2007. NPC1L1 (Niemann-Pick C1-like 1) mediates sterol-specifc unidirectional transport of non-esterifed cholesterol in McArdle-RH7777 hepatoma cells. Biochem J 406:273-283.
7. Buchaklian AH, Funk AL, Klug CS. 2004. Resting state conformation of the MsbA homodimer as studied by site-directed spin labeling. Biochemistry 43:8600-8606.
8. Buchaklian AH, Klug CS. 2006. Characterization of the LSGGQ and H motifs from the Escherichia coli lipid A transporter MsbA. Biochemistry 45:12539-12546.
9. Campbell JD, Biggin PC, Baaden M, Sansom MS. 2003. Extending the structure of an ABC transporter to atomic resolution: modeling and simulation studies of MsbA. Biochemistry 42:3666-3673.
10. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C, Gu J, Rosenfeld MA, Pavan WJ, Krizman DB, Nagle J, Polymeropoulos MH, Sturley SL, Ioannou YA, Higgins ME, Comly M, Cooney A, Brown A, Kaneski CR, Blanchette-Mackie EJ, Dwyer NK, Neufeld EB, Chang TY, Liscum L, Strauss JF 3rd, Ohno K, Zeigler M, Carmi R, Sokol J, Markie D, O'Neill RR, van Diggelen OP, Elleder M, Patterson MC, Brady RO, Vanier MT, Pentchev PG, Tagle DA. 1997. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 277:228-231.
11. Chang TY, Reid PC, Sugii S, Ohgami N, Cruz JC, Chang CC. 2005. Niemann-Pick type C disease and intracellular cholesterol trafcking. J Biol Chem 280:20917-20920.
12. Cheruku SR, Xu Z, Dutia R, Lobel P, Storch J. 2006. Mechanism of cholesterol transfer from the Niemann-Pick type C2 protein to model membranes supports a role in lysosomal cholesterol transport. J Biol Chem 281:31594-31604.
13. Clementz T, Bednarski JJ, Raetz CR. 1996. Function of the htrB high temperature requirement gene of Escherchia coli in the acylation of lipid A: HtrB catalyzed incorporation of laurate. J Biol Chem 271:12095-12102.
14. Clementz T, Zhou Z, Raetz CR. 1997. Function of the Escherichia coli msbB gene, a multicopy suppressor of htrB knockouts, in the acylation of lipid A. Acylation by MsbB follows laurate incorporation by HtrB. J Biol Chem 272:10353-10360.
15. Davidson AL, Chen J. 2004. ATP-binding cassette transporters in bacteria. Annu Rev Biochem 73:241-268.
16. Davies JP, Chen FW, Ioannou YA. 2000. Transmembrane molecular pump activity of Niemann-Pick C1 protein. Science 290:2295-2298.
17. Davies JP, Ioannou YA. 2000. Topological analysis of Niemann-Pick C1 protein reveals that the membrane orientation of the putative sterol-sensing domain is identical to those of 3-hydroxy-3-methylglutaryl-CoA reductase and sterol regulatory element binding protein cleavage-activating protein. J Biol Chem 275:24367-24374.
18. Davis HR Jr, Zhu LJ, Hoos LM, Tetzlof G, Maguire M, Liu J, Yao X, Iyer SP, Lam MH, Lund EG, Detmers PA, Graziano MP, Altmann SW. 2004. Niemann-Pick C1 Like 1 (NPC1L1) is the intestinal phytosterol and cholesterol transporter and a key modulator of whole-body cholesterol homeostasis. J Biol Chem 279:33586-33592.
19. Dawson RJ, Locher KP. 2006. Structure of a bacterial multidrug ABC transporter. Nature 443:180-185.
20. Doerrler WT, Gibbons HS, Raetz CR. 2004. MsbA-dependent translocation of lipids across the inner membrane of Escherichia coli. J Biol Chem 279:45102-45109.
21. Doerrler W T, Raetz CR. 2002. ATPase activity of the MsbA lipid fippase of Escherichia coli. J Biol Chem 277:36697-36705.
22. Doerrler W T, Reedy MC, Raetz CR. 2001. An Escherichia coli mutant defective in lipid export. J Biol Chem 276:11461-11464.
23. Dong J, Yang G, McHaourab HS. 2005. Structural basis of energy transduction in the transport cycle of MsbA. Science 308:1023-1028.
24. Du X, Kumar J, Ferguson C, Schulz TA, Ong YS, Hong W, Prinz WA, Parton RG, Brown AJ, Yang H. 2011. A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafcking. J Cell Biol 192:121-135.
25. Eckford PD, Sharom FJ. 2005. The reconstituted P-glycoprotein multidrug transporter is a fippase for glucosylceramide and other simple glycosphingolipids. Biochem J 389:517-526.
26. Eckford PD, Sharom FJ. 2008. Functional characterization of Escherichia coli MsbA: interaction with nucleotides and substrates. J Biol Chem 283:12840-12850.
27. Eckford PD, Sharom FJ. 2009. ABC efux pump-based resistance to chemotherapy drugs. Chem Rev 109:2989-3011.
28. Eckford PD, Sharom FJ. 2010. The reconstituted Escherichia coli MsbA protein displays lipid fippase activity. Biochem J 429:195-203.
29. Friedland N, Liou HL, Lobel P, Stock AM. 2003. Structure of a cholesterol-binding protein defcient in Niemann-Pick type C2 disease. Proc Natl Acad Sci USA 100:2512-2517.
30. Galanos C, Lüderitz O, Rietschel ET, Westphal O, Brade H, Brade L, Freudenberg M, Schade U, Imoto M, Yoshimura H. 1985. Synthetic and natural Escherichia coli free lipid A express identical endotoxic activities. Eur J Biochem 148:1-5.
31. Ge L, Wang J, Qi W, Miao HH, Cao J, Qu YX, Li BL, Song BL. 2008. The cholesterol absorption inhibitor ezetimibe acts by blocking the sterol-induced internalization of NPC1L1. Cell Metab 7: 508-519.
32. Greer WL, Dobson MJ, Girouard GS, Byers DM, Riddell DC, Neumann PE. 1999. Mutations in NPC1 highlight a conserved NPC1-specifc cysteine-rich domain. Am J Hum Genet 65:1252-1260.
33. Haberland ME, Reynolds JA. 1973. Self-association of cholesterol in aqueous solution. Proc Natl Acad Sci USA 70:2313-2316.
34. Hamilton JA. 2003. Fast fip-fop of cholesterol and fatty acids in membranes: implications for membrane transport proteins. Curr Opin Lipidol 14:263-271.
35. Higgins C F, Linton KJ. 2004. The ATP switch model for ABC transporters. Nat Struct Mol Biol 11:918-926.
36. Huijbregts RP, de Kroon AI, de Kruijf B. 2000. Topology and transport of membrane lipids in bacteria. Biochim Biophys Acta 1469:43-61.
37. Ikonen E. 2008. Cellular cholesterol trafcking and compartmentalization. Nat Rev Mol Cell Biol 9:125-138.
38. Infante RE, Abi-Mosleh L, Radhakrishnan A, Dale JD, Brown MS, Goldstein JL. 2008a. Purifed NPC1 protein. I. Binding of cholesterol and oxysterols to a 1278-amino acid membrane protein. J Biol Chem 283:1052-1063.
39. Infante RE, Radhakrishnan A, Abi-Mosleh L, Kinch LN, Wang ML, Grishin NV, Goldstein JL, Brown MS. 2008b. Purifed NPC1 protein: II. Localization of sterol binding to a 240-amino acid soluble luminal loop. J Biol Chem 283:1064-1075.
40. Infante RE, Wang ML, Radhakrishnan A, Kwon HJ, Brown MS, Goldstein JL. 2008c. NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes. Proc Natl Acad Sci USA 105:15287-15292.
41. Karow M, Fayet O, Georgopoulos C. 1992. The lethal phenotype caused by null mutations in the Escherichia coli htrB gene is suppressed by mutations in the accBC operon, encoding two subunits of acetyl coenzyme A carboxylase. J Bacteriol 174:7407-7418.
42. Karow M, Georgopoulos C. 1991. Sequencing, mutational analysis, and transcriptional regulation of the Escherichia coli htrB gene. Mol Microbiol 5:2285-2292.
43. Karow M, Georgopoulos C. 1992. Isolation and characterization of the Escherichia coli msbB gene, a multicopy suppressor of null mutations in the high-temperature requirement gene htrB. J Bacteriol 174:702-710.
44. Karow M, Georgopoulos C. 1993. The essential Escherichia coli msbA gene, a multicopy suppressor of null mutations in the htrB gene, is related to the universally conserved family of ATP-dependent translocators. Mol Microbiol 7:69-79.
45. Karow M, Raina S, Georgopoulos C, Fayet O. 1991. Complex phenotypes of null mutations in the htr genes, whose products are essential for Escherichia coli growth at elevated temperatures. Res Microbiol 142:289-294.
46. Kobayashi T, Beuchat MH, Chevallier J, Makino A, Mayran N, Escola JM, Lebrand C, Cosson P, Kobayashi T, Gruenberg J. 2002. Separation and characterization of late endosomal membrane domains. J Biol Chem 277:32157-32164.
47. Kol MA, van Dalen A, de Kroon AI, de Kruijf B. 2003a. Translocation of phospholipids is facilitated by a subset of membrane-spanning proteins of the bacterial cytoplasmic membrane. J Biol Chem 278:24586-24593.
48. Kol MA, van Laak AN, Rijkers DT, Killian JA, de Kroon AI, de Kruijf B. 2003b. Phospholipid fop induced by transmembrane peptides in model membranes is modulated by lipid composition. Biochemistry 42:231-237.
49. Kwon HJ, Abi-Mosleh L, Wang ML, Deisenhofer J, Goldstein JL, Brown MS, Infante RE. 2009. Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 137:1213-1224.
50. Kwon HJ, Palnitkar M, Deisenhofer J. 2011. The structure of the NPC1L1 N-terminal domain in a closed conformation. PLoS ONE 6:e18722.
51. Liou HL, Dixit SS, Xu S, Tint GS, Stock AM, Lobel P. 2006. NPC2, the protein defcient in Niemann-Pick C2 disease, consists of multiple glycoforms that bind a variety of sterols. J Biol Chem 281:36710-36723.
52. Liu B, Turley SD, Burns DK, Miller AM, Repa JJ, Dietschy JM. 2009a. Reversal of defective lysosomal transport in NPC disease ameliorates liver dysfunction and neurodegeneration in the npc1-/-mouse. Proc Natl Acad Sci USA 106:2377-2382.
53. Liu R, Lu P, Chu JW, Sharom FJ. 2009b. Characterization of fuorescent sterol binding to purifed human NPC1. J Biol Chem 284:1840-1852.
54. Lloyd-Evans E, Morgan AJ, He X, Smith DA, Elliot-Smith E, Sillence DJ, Churchill GC, Schuchman EH, Galione A, Platt FM. 2008. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat Med 14:1247-1255.
55. Maxfeld FR, Menon AK. 2006. Intracellular sterol transport and distribution. Curr Opin Cell Biol 18:379-385.
56. Mesmin B, Maxfeld FR. 2009. Intracellular sterol dynamics. Biochim Biophys Acta 1791:636-645.
57. Millard EE, Gale SE, Dudley N, Zhang J, Schafer JE, Ory DS. 2005. The sterol-sensing domain of the Niemann-Pick C1 (NPC1) protein regulates trafcking of low density lipoprotein cholesterol. J Biol Chem 280:28581-28590.
58. Motamed M, Zhang Y, Wang ML, Seemann J, Kwon HJ, Goldstein JL, Brown MS. 2011. Identifcation of luminal Loop 1 of Scap protein as the sterol sensor that maintains cholesterol homeostasis. J Biol Chem 286:18002-18012.
59. Mukherjee S, Maxfeld FR. 2004. Lipid and cholesterol trafcking in NPC. Biochim Biophys Acta 1685:28-37.
60. Naureckiene S, Sleat DE, Lackland H, Fensom A, Vanier MT, Wattiaux R, Jadot M, Lobel P. 2000. Identifcation of HE1 as the second gene of Niemann-Pick C disease. Science 290:2298-2301.
61. Nohturft A, Brown MS, Goldstein JL. 1998. Topology of SREBP cleavage-activating protein, a polytopic membrane protein with a sterol-sensing domain. J Biol Chem 273:17243-17250.
62. Ohgami N, Ko DC, Tomas M, Scott MP, Chang CC, Chang TY. 2004. Binding between the Niemann-Pick C1 protein and a photoactivatable cholesterol analog requires a functional sterol-sensing domain. Proc Natl Acad Sci USA 101:12473-12478.
63. Okamura N, Kiuchi S, Tamba M, Kashima T, Hiramoto S, Baba T, Dacheux F, Dacheux JL, Sugita Y, Jin YZ. 1999. A porcine homolog of the major secretory protein of human epididymis, HE1, specifcally binds cholesterol. Biochim Biophys Acta 1438:377-387.
64. Polissi A, Georgopoulos C. 1996. Mutational analysis and properties of the msbA gene of Escherichia coli, coding for an essential ABC family transporter. Mol Microbiol 20:1221-1233.
65. Quazi F, Molday RS. 2011. Lipid transport by mammalian ABC proteins. Essays Biochem 50:265-290.
66. Radhakrishnan A, Sun LP, Kwon HJ, Brown MS, Goldstein JL. 2004. Direct binding of cholesterol to the purifed membrane region of SCAP: mechanism for a sterol-sensing domain. Mol Cell 15:259-268.
67. Raetz CR, Reynolds CM, Trent MS, Bishop RE. 2007. Lipid A modifcation systems in gram-negative bacteria. Annu Rev Biochem 76:295-329.
68. Raychaudhuri S, Prinz WA. 2010. The diverse functions of oxysterol-binding proteins. Annu Rev Cell Dev Biol 26:157-177.
69. Reuter G, Janvilisri T, Venter H, Shahi S, Balakrishnan L, van Veen HW. 2003. The ATP binding cassette multidrug transporter LmrA and lipid transporter MsbA have overlapping substrate specifcities. J Biol Chem 278:35193-35198.
70. Romsicki Y, Sharom FJ. 2001. Phospholipid fippase activity of the reconstituted P-glycoprotein multidrug transporter. Biochemistry 40:6937-6947.
71. Rosenbaum AI, Maxfeld FR. 2011. Niemann-Pick type C disease: molecular mechanisms and potential therapeutic approaches. J Neurochem 116:789-795.
72. Rothman JE, Kennedy EP. 1977. Asymmetrical distribution of phospholipids in the membrane of Bacillus megaterium. J Mol Biol 110:603-618.
73. Ruiz N, Gronenberg LS, Kahne D, Silhavy TJ. 2008. Identifcation of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 105:5537-5542.
74. Sanyal S, Menon AK. 2009. Flipping lipids: why an' what's the reason for? ACS Chem Biol 4:895-909.
75. Sato R. 2010. Sterol metabolism and SREBP activation. Arch Biochem Biophys 501:177-181.
76. Schmitt L, Benabdelhak H, Blight MA, Holland IB, Stubbs MT. 2003. Crystal structure of the nucleotide-binding domain of the ABC-transporter haemolysin B: identifcation of a variable region within ABC helical domains. J Mol Biol 330:333-342.
77. Schultz KM, Merten JA, Klug CS. 2011. Efects of the L511P and D512G mutations on the Escherichia coli ABC transporter MsbA. Biochemistry 50:2594-2602.
78. Scott C, Higgins ME, Davies JP, Ioannou YA. 2004. Targeting of NPC1 to late endosomes involves multiple signals, including one residing within the putative sterol-sensing domain. J Biol Chem 279:48214-48223.
79. Seeger MA, van Veen HW. 2009. Molecular basis of multidrug transport by ABC transporters. Biochim Biophys Acta 1794:725-737.
80. Sharom FJ. 2011. Flipping and fopping-lipids on the move. IUBMB Life 63:736-746.
81. Sharom FJ, Yu X, Chu JW, Doige CA. 1995. Characterization of the ATPase activity of P-glycoprotein from multidrug-resistant Chinese hamster ovary cells. Biochem J 308 (Pt 2):381-390.
82. Siarheyeva A, Sharom FJ. 2009. The ABC transporter MsbA interacts with lipid A and amphipathic drugs at diferent sites. Biochem J 419:317-328.
83. Sleat DE, Wiseman JA, El-Banna M, Price SM, Verot L, Shen MM, Tint GS, Vanier MT, Walkley SU, Lobel P. 2004. Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc Natl Acad Sci USA 101: 5886-5891.
84. Smith PC, Karpowich N, Millen L, Moody JE, Rosen J, Tomas PJ, Hunt JF. 2002. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol Cell 10:139-149.
85. Smriti, Zou P, McHaourab HS. 2009. Mapping daunorubicin-binding sites in the ATP-binding cassette transporter MsbA using site-specifc quenching by spin labels. J Biol Chem 284:13904-13913.
86. Sperandeo P, Dehò G, Polissi A. 2009. The lipopolysaccharide transport system of Gram-negative bacteria. Biochim Biophys Acta 1791:594-602.
87. Storch J, Xu Z. 2009. Niemann-Pick C2 (NPC2) and intracellular cholesterol trafcking. Biochim Biophys Acta 1791:671-678.
88. Tefsen B, Bos MP, Beckers F, Tommassen J, de Cock H. 2005. MsbA is not required for phospholipid transport in Neisseria meningitidis. J Biol Chem 280:35961-35966.
89. Terakado K, Kodan A, Nakano H, Kimura Y, Ueda K, Nakatsu T, Kato H. 2010. Deleting two C-terminal alpha-helices is efective to crystallize the bacterial ABC transporter Escherichia coli MsbA complexed with AMP-PNP. Acta Crystallogr D Biol Crystallogr 66:319-323.
90. Tseng TT, Gratwick KS, Kollman J, Park D, Nies DH, Gofeau A, Saier MH Jr. 1999. The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J Mol Microbiol Biotechnol 1:107-125.
91. Urano Y, Watanabe H, Murphy SR, Shibuya Y, Geng Y, Peden AA, Chang CC, Chang TY. 2008. Transport of LDL-derived cholesterol from the NPC1 compartment to the ER involves the trans-Golgi network and the SNARE protein complex. Proc Natl Acad Sci USA 105:16513-16518.
92. Urbatsch IL, Sankaran B, Weber J, Senior AE. 1995. P-glycoprotein is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J Biol Chem 270:19383-19390.
93. van Meer G, Halter D, Sprong H, Somerharju P, Egmond MR. 2006. ABC lipid transporters: extruders, fippases, or fopless activators? FEBS Lett 580:1171-1177.
94. van Veen HW, Callaghan R, Soceneantu L, Sardini A, Konings WN, Higgins C F. 1998. A bacterial antibiotic-resistance gene that complements the human multidrug-resistance P-glycoprotein gene. Nature 391:291-295.
95. van Veen HW, Venema K, Bolhuis H, Oussenko I, Kok J, Poolman B, Driessen AJ, Konings WN. 1996. Multidrug resistance mediated by a bacterial homolog of the human multidrug transporter MDR1. Proc Natl Acad Sci USA 93:10668-10672.
96. Vance JE, Peake KB. 2011. Function of the Niemann-Pick type C proteins and their bypass by cyclodextrin. Curr Opin Lipidol 22:204-209.
97. Vanier MT. 2010. Niemann-Pick disease type C. Orphanet J Rare Dis 5:16.
98. Vanier MT, Millat G. 2004. Structure and function of the NPC2 protein. Biochim Biophys Acta 1685:14-21.
99. Wang ML, Motamed M, Infante RE, Abi-Mosleh L, Kwon HJ, Brown MS, Goldstein JL. 2010. Identifcation of surface residues on Niemann-Pick C2 essential for hydrophobic handof of cholesterol to NPC1 in lysosomes. Cell Metab 12:166-173.
100. Wang X, Karbarz MJ, McGrath SC, Cotter RJ, Raetz CR. 2004. MsbA transporter-dependent lipid A 1-dephosphorylation on the periplasmic surface of the inner membrane: topography of francisella novicida LpxE expressed in Escherichia coli. J Biol Chem 279:49470-49478.
101. Wang X, Quinn PJ. 2010. Lipopolysaccharide: Biosynthetic pathway and structure modifcation. Prog Lipid Res 49:97-107.
102. Ward A, Mulligan S, Carragher B, Chang G, Milligan RA. 2009. Nucleotide dependent packing diferences in helical crystals of the ABC transporter MsbA. J Struct Biol 165:169-175.
103. Ward A, Reyes CL, Yu J, Roth CB, Chang G. 2007. Flexibility in the ABC transporter MsbA: Alternating access with a twist. Proc Natl Acad Sci USA 104:19005-19010.
104. Watari H, Blanchette-Mackie EJ, Dwyer NK, Watari M, Neufeld EB, Patel S, Pentchev PG, Strauss JF 3rd. 1999. Mutations in the leucine zipper motif and sterol-sensing domain inactivate the Niemann-Pick C1 glycoprotein. J Biol Chem 274: 21861-21866.
105. Weinglass AB, Kohler M, Schulte U, Liu J, Nketiah EO, Tomas A, Schmalhofer W, Williams B, Bildl W, McMasters DR, Dai K, Beers L, McCann ME, Kaczorowski GJ, Garcia ML. 2008. Extracellular loop C of NPC1L1 is important for binding to ezetimibe. Proc Natl Acad Sci USA 105:11140-11145.
106. Woebking B, Reuter G, Shilling RA, Velamakanni S, Shahi S, Venter H, Balakrishnan L, van Veen HW. 2005. Drug-lipid A interactions on the Escherichia coli ABC transporter MsbA. J Bacteriol 187:6363-6369.
107. Woebking B, Velamakanni S, Federici L, Seeger MA, Murakami S, van Veen HW. 2008. Functional role of transmembrane helix 6 in drug binding and transport by the ABC transporter MsbA. Biochemistry 47:10904-10914.
108. Wu T, McCandlish AC, Gronenberg LS, Chng SS, Silhavy TJ, Kahne D. 2006. Identifcation of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 103:11754-11759.
109. Xu S, Benof B, Liou HL, Lobel P, Stock AM. 2007. Structural basis of sterol binding by NPC2, a lysosomal protein defcient in Niemann-Pick type C2 disease. J Biol Chem 282:23525-23531.
110. Xu Z, Farver W, Kodukula S, Storch J. 2008. Regulation of sterol transport between membranes and NPC2. Biochemistry 47:11134-11143.
111. Yu L. 2008. The structure and function of Niemann-Pick C1-like 1 protein. Curr Opin Lipidol 19:263-269.
112. Yu L, Bharadwaj S, Brown JM, Ma Y, Du W, Davis MA, Michaely P, Liu P, Willingham MC, Rudel LL. 2006. Cholesterol-regulated translocation of NPC1L1 to the cell surface facilitates free cholesterol uptake. J Biol Chem 281:6616-6624.
113. Zhou Z, White KA, Polissi A, Georgopoulos C, Raetz CR. 1998. Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J Biol Chem 273:12466-12475.
114. Zou P, McHaourab HS. 2009. Alternating access of the putative substrate-binding chamber in the ABC transporter MsbA. J Mol Biol 393:574-585.