The styrene–maleic acid copolymer: a versatile tool in membrane research

European Biophysics Journal

Volumn 45, Issue 1, 2016, Pages 3-21

  Dörr, Jonas M ^a   Scheidelaar, Stefan ^a   Koorengevel, Martijn C ^a   Dominguez, Juan J ^a   Schäfer, Marre ^a   van Walree, Cornelis A ^a,b   Killian, J Antoinette ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b FLINDERS UNIVERSITY   (Australia)

Author keywords

Lipid protein interactions; Lipodisq; Membrane proteins; Native nanodiscs; SMALPs; Styrene maleic acid copolymers

Indexed keywords

ACID ANHYDRIDE; APOLIPOPROTEIN A1; DETERGENT; LIPID; MALTOSE; MEMBRANE PROTEIN; NANODISC; PHOSPHOLIPID; SCAFFOLD PROTEIN; SOLUBILIZER; STYRENE MALEIC ANHYDRIDE COPOLYMER; LIPID BILAYER; MALEIC ACID DERIVATIVE; POLYSTYRENE DERIVATIVE; STYRENE-MALEIC ACID POLYMER;

CHEMICAL STRUCTURE; HYDROLYSIS; LIPID COMPOSITION; MAGNETIC FIELD; PH; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; SYNTHESIS; CHEMISTRY; LIPID BILAYER; SOLUBILITY;

LIPID BILAYERS; MALEATES; MEMBRANE PROTEINS; POLYSTYRENES; SOLUBILITY;

EID: 84952862273     PISSN: 01757571     EISSN: 14321017     Source Type: Journal    
DOI: 10.1007/s00249-015-1093-y     Document Type: Review

References (97)

1. Alfrey T, Lavin E (1945) The copolymerization of styrene and maleic anhydride. J Am Chem Soc 67:2044–2045
2. Arachea BT, Sun Z, Potente N, Malik R, Isailovic D, Viola RE (2012) Detergent selection for enhanced extraction of membrane proteins. Protein Expression Purif 86:12–20
3. Bai X-C, McMullan G, Scheres SHW (2015a) How cryo-EM is revolutionizing structural biology. Trends Biochem Sci 40:49–57
4. Bai X-C, Yan C, Yang G, Lu P, Ma D, Sun L, Zhou R, Scheres SHW, Shi Y (2015b) An atomic structure of human γ-secretase. Nature 525(7568):212–217
5. Banerjee S, Pal TK, Guha SK (2012) Probing molecular interactions of poly(styrene-co-maleic acid) with lipid matrix models to interpret the therapeutic potential of the co-polymer. BBA-Biomembranes 1818:537–550
6. Bayburt TH, Sligar SG (2010) Membrane protein assembly into nanodiscs. FEBS Lett 584:1721–1727
7. Bayburt TH, Grinkova YV, Sligar SG (2002) Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Lett 2:853–856
8. Bayburt TH et al (2010) Monomeric rhodopsin is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and arrestin-1 binding. J Biol Chem 286:1420–1428
9. Bell AJ, Frankel LK, Bricker TM (2015) High yield non-detergent isolation of photosystem I light-harvesting chlorophyll II membranes from spinach thylakoids. J Biol Chem 290:18429–18437
10. 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 103:11509–11514
11. Bordag N, Keller S (2010) α-Helical transmembrane peptides: a “divide and conquer” approach to membrane proteins. Chem Phys Lipids 163:1–26
12. Chae PS et al (2010) Maltose–neopentyl glycol (MNG) amphiphiles for solubilization, stabilization and crystallization of membrane proteins. Nat Methods 7:1003–1008
13. Chromy BA et al (2007) Different apolipoproteins impact nanolipoprotein particle formation. J Am Chem Soc 129(46):14348–14354
14. Civjan NR, Bayburt TH, Schuler MA, Sligar SG (2003) Direct solubilization of heterologously expressed membrane proteins by incorporation into nanoscale lipid bilayers. Biotechniques 35:556–563
15. Deb PC, Meyerhoff G (1984) Study on kinetics of copolymerisation of styrene and maleic anhydride in dioxane. Eur Polym J 20:713–719
16. Ding Y, Fujimoto LM, Yao Y, Marassi FM (2015) Solid-state NMR of the Yersinia pestis outer membrane protein Ail in lipid bilayer nanodiscs sedimented by ultracentrifugation. J Biomol NMR 61:275–286
17. + channel: the power of native nanodiscs. Proc Natl Acad Sci USA 111:18607–18612
18. Dürr UHN, Soong R, Ramamoorthy A (2013) When detergent meets bilayer: birth and coming of age of lipid bicelles. Prog Nucl Magn Reson Spectrosc 69:1–22
19. Frauenfeld J et al (2011) Cryo-EM structure of the ribosome–SecYE complex in the membrane environment. Nat Struct Mol Biol 18:614–621
20. Fried JR (2003) Polymer science and technology, 2nd edn. Prentice Hall, Upper Saddle River
21. Frotscher E, Danielczak B, Vargas C, Meister A, Durand G, Keller S (2015) A fluorinated detergent for membrane-protein applications. Angew Chem Int Ed 54:5069–5073
22. Garavito RM, Ferguson-Miller S (2001) Detergents as tools in membrane biochemistry. J Biol Chem 276:32403–32406
23. Goddard AD, Dijkman PM, Adamson RJ, dos Reis RI, Watts A (2015) Reconstitution of membrane proteins. Methods Enzymol 556:405–424
24. Grinkova YV, Denisov IG, Sligar SG (2010) Engineering extended membrane scaffold proteins for self-assembly of soluble nanoscale lipid bilayers. Protein Eng Des Sel 23:843–848
25. Gulati S et al (2014) Detergent-free purification of ABC (ATP-binding-cassette) transporters. Biochem J 461:269–278
26. Hagn F, Etzkorn M, Raschle T, Wagner G (2013) Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins. J Am Chem Soc 135:1919–1925
27. He W et al (2015) Cell-free expression of functional receptor tyrosine kinases. Sci Rep 5:12896
28. Heerklotz H (2002) Triton promotes domain formation in lipid raft mixtures. Biophys J 83:2693–2701
29. Henry SM, El-Sayed MEH, Pirie CM, Hoffman AS, Stayton PS (2006) pH-responsive poly(styrene-alt-maleic anhydride) alkylamide copolymers for intracellular drug delivery. Biomacromolecules 7:2407–2414
30. Hill DJT, O’Donnell JH, O’Sullivan PW (1985) Analysis of the mechanism of copolymerization of styrene and maleic anhydride. Macromolecules 18:9–17
31. Howard KP, Opella SJ (1996) High-resolution solid-state NMR spectra of integral membrane proteins reconstituted into magnetically oriented phospholipid bilayers. J Magn Reson Ser B 112:91–94
32. Ilgü H, Jeckelmann J-M, Gachet MS, Boggavarapu R, Ucurum Z, Gertsch J, Fotiadis D (2014) Variation of the detergent-binding capacity and phospholipid content of membrane proteins when purified in different detergents. Biophys J 106:1660–1670
33. Jamshad M et al (2011) Surfactant-free purification of membrane proteins with intact native membrane environment. Biochem Soc Trans 39:813–818
34. Jamshad M et al (2015a) G-protein coupled receptor solubilization and purification for biophysical analysis and functional studies, in the total absence of detergent. Biosci Rep 35:1–10
35. Jamshad M et al (2015b) Structural analysis of a nanoparticle containing a lipid bilayer used for detergent-free extraction of membrane proteins. Nano Research 8:774–789
36. Katayama H et al (2010) Three-dimensional structure of the anthrax toxin pore inserted into lipid nanodiscs and lipid vesicles. Proc Natl Acad Sci 107(8):3453–3457
37. Kiessling V, Domanska MK, Murray D, Wan C, Tamm LK (2008) Supported lipid bilayers: development and applications in chemical biology. In: Begley TP (ed) Wiley encyclopedia of chemical biology. Wiley, Hoboken
38. Klumperman B (2010) Mechanistic considerations on styrene–maleic anhydride copolymerization reactions. Polym Chem 1:558–562
39. Knowles TJ, Finka R, Smith C, Lin Y-P, Dafforn T, Overduin M (2009) Membrane proteins solubilized intact in lipid containing nanoparticles bounded by styrene maleic acid copolymer. J Am Chem Soc 131:7484–7485
40. Koutsopoulos S, Kaiser L, Eriksson HM, Zhang S (2012) Designer peptide surfactants stabilize diverse functional membrane proteins. Chem Soc Rev 41(5):1721–1728
41. le Maire M, Champeil P, Møller JV (2000) Interaction of membrane proteins and lipids with solubilizing detergents. Biochim Biophys Acta 1508:86–111
42. Lee AG (2011) Lipid–protein interactions. Biochem Soc Trans 39:761–766
43. Lichtenberg D, Ahyayauch H, Goñi FM (2013) The mechanism of detergent solubilization of lipid bilayers. Biophys J 105:289–299
44. Long AR, O’Brien CC, Malhotra K, Schwall CT, Albert AD, Watts A, Alder NN (2013) A detergent-free strategy for the reconstitution of active enzyme complexes from native biological membranes into nanoscale discs. BMC Biotechnol 13:41
45. Maeda H (2001) SMANCS and polymer-conjugated macromolecular drugs: advantages in cancer chemotherapy. Adv Drug Del Rev 46:169–185
46. Maeda H, Takeshita J, Kanamaru R (1979) A lipophilic derivative of neocarzinostatin. A polymer conjugation of an antitumor protein antibiotic. Int J Pept Protein Res 14:81–87
47. Mizrachi D et al (2015) Making water-soluble integral membrane proteins in vivo using an amphipathic protein fusion strategy. Nat Commun 6:6826
48. Montaudo MS (2001) Determination of the compositional distribution and compositional drift in styrene/maleic anhydride copolymers. Macromolecules 34:2792–2797
49. Moraes I, Evans G, Sanchez-Weatherby J, Newstead S, Stewart PDS (2014) Membrane protein structure determination—the next generation. BBA-Biomembranes 1838:78–87
50. Nagle JF, Tristram-Nagle S (2000) Structure of lipid bilayers. Biochim Biophys Acta 1469:159–195
51. Oiki S (2015) Channel function reconstitution and re-animation: a single-channel strategy in the postcrystal age. J Physiol 593:2553–2573
52. Orwick MC et al (2012) Detergent-free formation and physicochemical characterization of nanosized lipid–polymer complexes: lipodisq. Angew Chem Int Ed Engl 51:4653–4657
53. Orwick-Rydmark M, Lovett JE, Graziadei A, Lindholm L, Hicks MR, Watts A (2012) Detergent-free incorporation of a seven-transmembrane receptor protein into nanosized bilayer Lipodisq particles for functional and biophysical studies. Nano Lett 12:4687–4692
54. Overington JP, Al-Lazikani B, Hopkins AL (2006) How many drug targets are there? Nat Rev Drug Discov 5:993–996
55. Park SH, Berkamp S, Cook GA, Chan MK, Viadiu H, Opella SJ (2011) Nanodiscs versus macrodiscs for NMR of membrane proteins. Biochemistry 50:8983–8985
56. Paulin S et al (2014) Surfactant-free purification of membrane protein complexes from bacteria: application to the staphylococcal penicillin-binding protein complex PBP2/PBP2a. Nanotechnology 25:285101
57. Popot J-L et al (2011) Amphipols from A to Z. Ann Rev Biophys 40:379–408
58. Postis V et al (2015) The use of SMALPs as a novel membrane protein scaffold for structure study by negative stain electron microscopy. BBA-Biomembranes 1848:496–501
59. Prabudiansyah I, Kusters I, Caforio A, Driessen AJM (2015) Characterization of the annular lipid shell of the Sec translocon. BBA-Biomembranes 1848:2050–2056
60. Privé GG (2007) Detergents for the stabilization and crystallization of membrane proteins. Methods 41:388–397
61. Quick M, Shi L, Zehnpfennig B, Weinstein H, Javitch JA (2012) Experimental conditions can obscure the second high-affinity site in LeuT. Nat Struct Mol Biol 19:207–211
62. 2 adrenergic G-protein-coupled receptor. Nature 450:383–387
63. Rigaud J-L, Lévy D (2003) Reconstitution of membrane proteins into liposomes. Liposomes Part B 372:65–86
64. Roos C et al (2012) Characterization of co-translationally formed nanodisc complexes with small multidrug transporters, proteorhodopsin and with the E. coli MraY translocase. Biochim Biophys Acta 1818:3098–3106
65. Sahu ID et al (2013) DEER EPR measurements for membrane protein structures via bifunctional spin labels and lipodisq nanoparticles. Biochemistry 52:6627–6632
66. Sahu ID et al (2014) Structural investigation of the transmembrane domain of KCNE1 in proteoliposomes. Biochemistry 53:6392–6401
67. Scheidelaar S, Koorengevel MC, Dominguez Pardo J, Meeldijk JD, Breukink E, Killian JA (2015) Molecular model for the solubilization of membranes into nanodisks by styrene–maleic acid copolymers. Biophys J 108:279–290
68. Schuler MA, Denisov IG, Sligar SG (2012) Nanodiscs as a new tool to examine lipid–protein interactions. Methods Mol Biol 974:415–433
69. Seddon AM, Curnow P, Booth PJ (2004) Membrane proteins, lipids and detergents: not just a soap opera. Biochim Biophys Acta 1666:105–117
70. Shi L et al (2012) SNARE proteins: one to fuse and three to keep the nascent fusion pore open. Science 335:1355–1359
71. Shinzawa-Itoh K et al (2007) Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J 26:1713–1725
72. Shirzad-Wasei N, van Oostrum J, Bovee-Geurts PHM, Kusters LJA, Bosman GJCGM, DeGrip WJ (2015) Rapid transfer of overexpressed integral membrane protein from the host membrane into soluble lipid nanodiscs without previous purification. Biol Chem 396:903–915
73. Skaar K, Korza HJ, Tarry M, Sekyrova P, Högbom M (2015) Expression and subcellular distribution of GFP-tagged human tetraspanin proteins in Saccharomyces cerevisiae. PLoS One 10(7):e0134041
74. Sugai S, Ebert G (1985) Conformations of hydrophobic polyelectrolytes. Adv Colloid Interface Sci 24:247–282
75. Sugai S, Nitta K, Ohno N (1982) Studies on conformational transition of the maleic acid copolymer with styrene in aqueous salt solution by derivative spectroscopy. Polymer 23:238–242
76. Swainsbury DJK, Scheidelaar S, van Grondelle R, Killian JA, Jones MR (2014) Bacterial reaction centers purified with styrene–maleic acid copolymer retain native membrane functional properties and display enhanced stability. Angew Chem Int Ed Engl 53:11803–11807
77. Tao H et al (2013) Engineered nanostructured β-sheet peptides protect membrane proteins. Nat Methods 10:759–761
78. Tighe BJ, Tonge SR (2000) Lipid-containing compositions and uses thereof. UK patent number WO/1999/009955
79. Tonge SR (2006) Compositions comprising a lipid and copolymer of styrene maleic acid. UK Patent Number WO/2006/129127
80. Tonge SR, Tighe BJ (2001) Responsive hydrophobically associating polymers: a review of structure and properties. Adv Drug Del Rev 53:109–122
81. Tribet C, Audebert R, Popot JL (1996) Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proc Natl Acad Sci USA 93:15047–15050
82. + channel. Biochemistry 41:10771–10777
83. Vargas C, Cuevas Arenas R, Frotscher E, Keller S (2015) Nanoparticle self-assembly in mixtures of phospholipids with styrene/maleic acid copolymers or fluorinated surfactants. Nanoscale. doi:10.1039/C5NR06353A
84. Vold RR, Prosser RS (1996) Magnetically oriented phospholipid bilayered micelles for structural studies of polypeptides. Does the ideal bicelle exist? J Magn Reson Ser B 113:267–271
85. von Heijne G (2007) The membrane protein universe: what’s out there and why bother? J Intern Med 261:543–557
86. Wallin E, von Heijne G (1998) Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 7:1029–1038
87. Wan C-PL, Chiu MH, Wu X, Lee SK, Prenner EJ, Weers PMM (2011) Apolipoprotein-induced conversion of phosphatidylcholine bilayer vesicles into nanodisks. Biochim Biophys Acta 1808:606–613
88. Wang X, Mu Z, Li Y, Bi Y, Wang Y (2015) Smaller nanodiscs are suitable for studying protein lipid interactions by solution NMR. Protein J 34(3):205–211
89. White SH (2015) Membrane proteins of known structure. http://blanco.biomol.uci.edu/mpstruc/. Accessed 12 Oct 2015
90. Yao Z, Li B-G, Wang W-J, Pan Z-R (1999) Continuous thermal bulk copolymerization of styrene and maleic anhydride. J Appl Polym Sci 73:615–622
91. Zeev-Ben-Mordehai T, Vasishtan D, Siebert CA, Whittle C, Grünewald K (2014) Extracellular vesicles: a platform for the structure determination of membrane proteins by cryo-EM. Structure 22(11):1687–1692
92. Zhang Q et al (2007) Designing facial amphiphiles for the stabilization of integral membrane proteins. Angew Chem Int Ed 46:7023–7025
93. Zhang R, Sahu ID, Liu L, Osatuke A, Comer RG, Dabney-Smith C, Lorigan GA (2015) Characterizing the structure of lipodisq nanoparticles for membrane protein spectroscopic studies. BBA-Biomembranes 1848:329–333
94. Zhou H-X, Cross TA (2013a) Influences of membrane mimetic environments on membrane protein structures. Ann Rev Biophys 42:361–392
95. Zhou H-X, Cross TA (2013b) Modeling the membrane environment has implications for membrane protein structure and function: influenza A M2 protein. Protein Sci 22:381–394
96. Zoonens M, Popot J-L (2014) Amphipols for each season. J Membr Biol 247:759–796
97. Zoonens M, Comer J, Masscheleyn S, Pebay-Peyroula E, Chipot C, Miroux B, Dehez F (2013) Dangerous liaisons between detergents and membrane proteins. The case of mitochondrial uncoupling protein 2. J Am Chem Soc 135:15174–15182