Lipid bilayer nanodisc platform for investigating polyprenol-dependent enzyme interactions and activities

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 52, 2013, Pages 20863-20870

  Hartley, Meredith D ^a   Schneggenburger, Philipp E ^a   Imperiali, Barbara ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISACCHARIDASE; GLYCAN; MEMBRANE ENZYME; NANODISC; PHOSPHATE; UNCLASSIFIED DRUG; UNDECAPRENYL DIPHOSPHATE; UNDECAPRENYL PHOSPHATE;

ARTICLE; BIOCHEMISTRY; CAMPYLOBACTER JEJUNI; CONTROLLED STUDY; EMBEDDING; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME LOCALIZATION; ENZYME RECONSTITUTION; ENZYME SUBSTRATE; FLUORESCENCE; ISOTOPE LABELING; LIPID BILAYER; MEMBRANE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN GLYCOSYLATION; PROTEIN PROTEIN INTERACTION; STOICHIOMETRY; STRUCTURE ACTIVITY RELATION;

EID: 84891366365     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1320852110     Document Type: Article

References (47)

1. Larkin A, Imperiali B (2011) The expanding horizons of asparagine-linked glycosylation. Biochemistry 50(21): 4411-4426.
2. Jones MB, Rosenberg JN, Betenbaugh MJ, Krag SS (2009) Structure and synthesis of polyisoprenoids used in N-glycosylation across the three domains of life. Biochim Biophys Acta 1790(6): 485-494.
3. Krag SS (1998) The importance of being dolichol. Biochem Biophys Res Commun 243(1): 1-5.
4. Hartley MD, Imperiali B (2012) At the membrane frontier: A prospectus on the remarkable evolutionary conservation of polyprenols and polyprenyl- phosphates. Arch Biochem Biophys 517(2): 83-97.
5. Surmacz L, Swiezewska E (2011) Polyisoprenoids - Secondary metabolites or physiologically important superlipids? Biochem Biophys Res Commun 407(4): 627-632.
6. Bouhss A, Trunkfield AE, Bugg TD, Mengin-Lecreulx D (2008) The biosynthesis of peptidoglycan lipid-linked intermediates. FEMS Microbiol Rev 32(2): 208-233.
7. Weerapana E, Imperiali B (2006) Asparagine-linked protein glycosylation: From eukaryotic to prokaryotic systems. Glycobiology 16(6):91R-101R.
8. Szymanski CM, Yao R, Ewing CP, Trust TJ, Guerry P (1999) Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol Microbiol 32(5): 1022-1030.
9. Glover KJ, Weerapana E, Imperiali B (2005) In vitro assembly of the undecaprenylpyrophosphate- linked heptasaccharide for prokaryotic N-linked glycosylation. Proc Natl Acad Sci USA 102(40): 14255-14259.
10. Glover KJ, Weerapana E, Numao S, Imperiali B (2005) Chemoenzymatic synthesis of glycopeptides with PglB, a bacterial oligosaccharyl transferase from Campylobacter jejuni. Chem Biol 12(12): 1311-1315.
11. Glover KJ, Weerapana E, Chen MM, Imperiali B (2006) Direct biochemical evidence for the utilization of UDP-bacillosamine by PglC, an essential glycosyl-1-phosphatetransferase in the C. jejuni N-linked glycosylation pathway. Biochemistry 45(16): 5343-5350.
12. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol 305(3): 567-580.
13. Alaimo C, et al. (2006) Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. EMBO J 25(5): 967-976.
14. Scott NE, et al. (2011) Simultaneous glycan-peptide characterization using hydrophilic interaction chromatography and parallel fragmentation by CID, higher energy collisional dissociation, and electron transfer dissociation MS applied to the N-linked glycoproteome of Campylobacter jejuni. Mol Cell Proteomics 10(2):M000031-MCP201.
15. Karlyshev AV, et al. (2004) The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology 150(Pt 6): 1957-1964.
16. Chen MM, et al. (2007) Polyisoprenol specificity in the Campylobacter jejuni N-linked glycosylation pathway. Biochemistry 46(50): 14342-14348.
17. Rush JS, Rick PD, Waechter CJ (1997) Polyisoprenyl phosphate specificity of UDPGlcNAc: undecaprenyl phosphate N-acetylglucosaminyl 1-P transferase from E. coli. Glycobiology 7(2): 315-322.
18. McLachlan KR, Krag SS (1992) Substrate specificity of N-acetylglucosamine 1-phosphate transferase activity in Chinese hamster ovary cells. Glycobiology 2(4): 313-319.
19. Janas T, Chojnacki T, Swiezewska E, Janas T (1994) The effect of undecaprenol on bilayer lipid membranes. Acta Biochim Pol 41(3): 351-358.
20. Zhou GP, Troy FA, 2nd (2005) NMR study of the preferred membrane orientation of polyisoprenols (dolichol) and the impact of their complex with polyisoprenyl recognition sequence peptides on membrane structure. Glycobiology 15(4): 347-359.
21. Zhou GP, Troy FA, 2nd (2003) Characterization by NMR and molecular modeling of the binding of polyisoprenols and polyisoprenyl recognition sequence peptides: 3D structure of the complexes reveals sites of specific interactions. Glycobiology 13(2): 51-71.
22. Wang X, Mansourian AR, Quinn PJ (2008) The effect of dolichol on the structure and phase behaviour of phospholipid model membranes. Mol Membr Biol 25(6-7): 547-556.
23. Valtersson C, et al. (1985) The influence of dolichol, dolichol esters, and dolichyl phosphate on phospholipid polymorphism and fluidity in model membranes. J Biol Chem 260(5): 2742-2751.
24. van Duijn G, et al. (1986) Dolichyl phosphate induces non-bilayer structures, vesicle fusion and transbilayer movement of lipids: A model membrane study. Biochim Biophys Acta 861(2): 211-223.
25. Denisov IG, Grinkova YV, Lazarides AA, Sligar SG (2004) Directed self-assembly of monodisperse phospholipid bilayer Nanodiscs with controlled size. J Am Chem Soc 126(11): 3477-3487.
26. Grinkova YV, Denisov IG, Sligar SG (2010) Engineering extended membrane scaffold proteins for self-assembly of soluble nanoscale lipid bilayers. Protein Eng Des Sel 23(11): 843-848.
27. Ritchie TK, et al. (2009) Chapter 11 - Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. Methods Enzymol 464: 211-231.
28. Nath A, Atkins WM, Sligar SG (2007) Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane proteins. Biochemistry 46(8): 2059-2069.
29. Boldog T, Li M, Hazelbauer GL (2007) Using Nanodiscs to create water-soluble transmembrane chemoreceptors inserted in lipid bilayers. Methods Enzymol 423: 317-335.
30. Ritchie TK, Kwon H, Atkins WM (2011) Conformational analysis of human ATPbinding cassette transporter ABCB1 in lipid nanodiscs and inhibition by the antibodies MRK16 and UIC2. J Biol Chem 286(45): 39489-39496.
31. Hernández-Rocamora VM, et al. (2012) Dynamic interaction of the Escherichia coli cell division ZipA and FtsZ proteins evidenced in nanodiscs. J Biol Chem 287(36): 30097-30104.
32. Boldog T, Grimme S, Li M, Sligar SG, Hazelbauer GL (2006) Nanodiscs separate chemoreceptor oligomeric states and reveal their signaling properties. Proc Natl Acad Sci USA 103(31): 11509-11514.
33. Inagaki S, et al. (2012) Modulation of the interaction between neurotensin receptor NTS1 and Gq protein by lipid. J Mol Biol 417(1-2): 95-111.
34. Kimmich N, et al. (2007) Electron transfer between cytochrome P450cin and its FMNcontaining redox partner, cindoxin. J Biol Chem 282(37): 27006-27011.
35. Nath A, Grinkova YV, Sligar SG, AtkinsWM(2007) Ligand binding to cytochrome P450 3A4 in phospholipid bilayer nanodiscs: The effect of model membranes. J Biol Chem 282(39): 28309-28320.
36. Denisov IG, Grinkova YV, McLean MA, Sligar SG (2007) The one-electron autoxidation of human cytochrome P450 3A4. J Biol Chem 282(37): 26865-26873.
37. Kawai T, Caaveiro JM, Abe R, Katagiri T, Tsumoto K (2011) Catalytic activity of MsbA reconstituted in nanodisc particles is modulated by remote interactions with the bilayer. FEBS Lett 585(22): 3533-3537.
38. Das A, Sligar SG (2009) Modulation of the cytochrome P450 reductase redox potential by the phospholipid bilayer. Biochemistry 48(51): 12104-12112.
39. Cheng Y, Patel DJ (2004) An efficient system for small protein expression and refolding. Biochem Biophys Res Commun 317(2): 401-405.
40. Popp MW, Antos JM, Ploegh HL (2009) Site-specific protein labeling via sortase-mediated transpeptidation. Curr Protoc Protein Sci, Chapter 15: Unit 15.13.
41. Hanover JA, Lennarz WJ (1979) The topological orientation of N, N'-diacetylchitobiosylpyrophosphoryldolichol in artificial and natural membranes. J Biol Chem 254(18): 9237-9246.
42. McCloskey MA, Troy FA (1980) Paramagnetic isoprenoid carrier lipids. 2. Dispersion and dynamics in lipid membranes. Biochemistry 19(10): 2061-2066.
43. de Ropp JS, Troy FA (1985) 2H NMR investigation of the organization and dynamics of polyisoprenols in membranes. J Biol Chem 260(29): 15669-15674.
44. Katsikas H, Quinn PJ (1982) The polyisoprenoid chain length influences the interaction of ubiquinones with phospholipid bilayers. Biochim Biophys Acta 689(2): 363-369.
45. Nath A, et al. (2010) Single-molecule fluorescence spectroscopy using phospholipid bilayer nanodiscs. Methods Enzymol 472: 89-117.
46. Hartley MD, Larkin A, Imperiali B (2008) Chemoenzymatic synthesis of polyprenyl phosphates. Bioorg Med Chem 16(9): 5149-5156.
47. Olivier NB, Chen MM, Behr JR, Imperiali B (2006) In vitro biosynthesis of UDP-N, N'- diacetylbacillosamine by enzymes of the Campylobacter jejuni general protein glycosylation system. Biochemistry 45(45): 13659-13669.