Unified superresolution experiments and stochastic theory provide mechanistic insight into protein ion-exchange adsorptive separations

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

Volumn 111, Issue 6, 2014, Pages 2075-2080

  Kisley, Lydia ^a   Chen, Jixin ^a   Mansur, Andrea P ^a   Shuang, Bo ^a   Kourentzi, Katerina ^b   Poongavanam, Mohan Vivekanandan ^c   Chen, Wen Hsiang ^b   Dhamane, Sagar ^c   Willson, Richard C ^b,c,d   Landes, Christy F ^a,e  

^a RICE UNIVERSITY   (United States)

^b Rice University   (United States)

^c UNIVERSITY OF HOUSTON   (United States)

^d HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^e SCHOOL OF ENGINEERING AND SCIENCES   (Mexico)

Author keywords

Bioseparations; Ion exchange chromatography; Optical nanoscopy; Single molecule kinetics

Indexed keywords

BIOSEPARATIONS; ION-EXCHANGE CHROMATOGRAPHY; OPTICAL NANOSCOPY; SINGLE-MOLECULE KINETICS;

ADSORPTION; CHROMATOGRAPHY, ION EXCHANGE; KINETICS; LACTALBUMIN; LIMIT OF DETECTION; PROTEINS; STOCHASTIC PROCESSES;

EID: 84893850297     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1318405111     Document Type: Article

References (69)

1. Walsh G (2010) Biopharmaceutical benchmarks 2010. Nat Biotechnol 28(9):917-924.
2. Regnier FE (1983) High-performance liquid chromatography of biopolymers. Science 222(4621):245-252.
3. Dziennik SR, et al. (2003) Nondiffusive mechanisms enhance protein uptake rates in ion exchange particles. Proc Natl Acad Sci USA 100(2):420-425.
4. Chung WK, Freed AS, Holstein MA, McCallum SA, Cramer SM (2010) Evaluation of protein adsorption and preferred binding regions in multimodal chromatography using NMR. Proc Natl Acad Sci USA 107(39):16811-16816.
5. Novotny MV (1989) Recent developments in analytical chromatography. Science 246(4926):51-57.
6. Freed AS, Garde S, Cramer SM (2011) Molecular simulations of multimodal ligandprotein binding: Elucidation of binding sites and correlation with experiments. J Phys Chem B 115(45):13320-13327.
7. Schellekens H (2004) How similar do 'biosimilars' need to be? Nat Biotechnol 22(11): 1357-1359.
8. Chen WH, Fu JY, Kourentzi K, Willson RC (2011) Nucleic acid affinity of clusteredcharge anion exchange adsorbents: Effects of ionic strength and ligand density. J Chromatogr A 1218(2):258-262.
9. Fu JY, Balan S, Potty A, Nguyen V, Willson RC (2007) Enhanced protein affinity and selectivity of clustered-charge anion-exchange adsorbents. Anal Chem 79(23):9060-9065.
10. Wu D, Walters RR (1992) Effects of stationary phase ligand density on high-performance ion-exchange chromatography of proteins. J Chromatogr A 598(1):7-13.
11. Müller W (1990) New ion exchangers for the chromatography of biopolymers. J Chromatogr A 510:133-140.
12. Atkinson A, Jack GW (1973) Precipitation of nucleic acids with polyethyleneimine and the chromatography of nucleic acids and proteins on immobilised polyethyleneimine. Biochim Biophys Acta 308(7):41-52.
13. Millot M-C, et al. (2003) Ion-exchange chromatographic supports obtained by formation of polyelectrolyte multi-layers for the separation of proteins. Chromatographia 58(5-6):365-373.
14. Daly SM, Przybycien TM, Tilton RD (2005) Adsorption of poly(ethylene glycol)-modified lysozyme to silica. Langmuir 21(4):1328-1337.
15. Gill DS, Roush DJ, Willson RC (1994) Presence of a preferred anion-exchange binding site on cytochrome b5: Structural and thermodynamic considerations. J Chromatogr A 684(1):55-63.
16. Ramsden J, et al. (1995) Protein adsorption kinetics drastically altered by repositioning a single charge. J Am Chem Soc 117(33):8511-8516.
17. Asthagiri D, Lenhoff AM (1997) Influence of structural details in modeling electrostatically driven protein adsorption. Langmuir 13(25):6761-6768.
18. Jennissen HP (2005) Hydrophobic interaction chromatography: Harnessing multivalent protein-surface interactions for purification procedures. Methods Mol Biol 305: 81-99.
19. Jennissen HP (1976) Multivalent adsorption of proteins on hydrophobic agaroses. Hoppe Seylers Z Physiol Chem 357(8):1201-1203.
20. Hogg PJ, Winzor DJ (1985) Effects of solute multivalency in quantitative affinity chromatography: Evidence for cooperative binding of horse liver alcohol dehydrogenase to blue Sepharose. Arch Biochem Biophys 240(1):70-76.
21. Johnson RD, Arnold FH (1995) Review: Multipoint binding and heterogeneity in immobilized metal affinity chromatography. Biotechnol Bioeng 48(5):437-443.
22. Arnold FH (1991) Metal-affinity separations: A new dimension in protein processing. Biotechnology (N Y) 9(2):151-156.
23. Jendeberg L, et al. (1995) Kinetic analysis of the interaction between protein A domain variants and human Fc using plasmon resonance detection. J Mol Recognit 8(4): 270-278.
24. Mammen M, Choi S-K, Whitesides GM (1998) Polyvalent interactions in biological systems: Implications for design and use of multivalent ligands and inhibitors. Angew Chem Int Ed 37(20):2754-2794.
25. Mourez M, et al. (2001) Designing a polyvalent inhibitor of anthrax toxin. Nat Biotechnol 19(10):958-961.
26. Martin AJ, Synge RL (1941) A new form of chromatogram employing two liquid phases: A theory of chromatography. Application to the micro-determination of the higher monoamino-acids in proteins. Biochem J 35(12):1358-1368
27. Yamamoto S, Yoshimoto N, Nishizumi Y (2009) Theoretical background of monolithic short layer ion-exchange chromatography for separation of charged large biomolecules or bioparticles. J Chromatogr A 1216(13):2612-2615.
28. Gétaz D, Butté A, Morbidelli M (2013) Model-based design space determination of peptide chromatographic purification processes. J Chromatogr A 1284:80-87.
29. Gallant SR, Kundu A, Cramer SM (1995) Modeling non-linear elution of proteins in ion-exchange chromatography. J Chromatogr A 702(1):125-142.
30. Moerner WE (2007) New directions in single-molecule imaging and analysis. Proc Natl Acad Sci USA 104(31):12596-12602.
31. Klar TA, Jakobs S, Dyba M, Egner A, Hell SW (2000) Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc Natl Acad Sci USA 97(15):8206-8210.
32. Gustafsson MGL (2005) Nonlinear structured-illumination microscopy: Wide-field fluorescence imaging with theoretically unlimited resolution. Proc Natl Acad Sci USA 102(37):13081-13086.
33. Westphal V, et al. (2008) Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320(5873):246-249.
34. Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3(10):793-795.
35. Betzig E, et al. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313(5793):1642-1645.
36. Burnette DT, Sengupta P, Dai Y, Lippincott-Schwartz J, Kachar B (2011) Bleaching/ blinking assisted localization microscopy for superresolution imaging using standard fluorescent molecules. Proc Natl Acad Sci USA 108(52):21081-21086.
37. Sharonov A, Hochstrasser RM (2006) Wide-field subdiffraction imaging by accumulated binding of diffusing probes. Proc Natl Acad Sci USA 103(50):18911-18916.
38. Zhou X, et al. (2012) Quantitative super-resolution imaging uncovers reactivity patterns on single nanocatalysts. Nat Nanotechnol 7(4):237-241.
39. Jungmann R, et al. (2010) Single-molecule kinetics and super-resolution microscopy by fluorescence imaging of transient binding on DNA origami. Nano Lett 10(11): 4756-4761.
40. Wu D, Liu Z, Sun C, Zhang X (2008) Super-resolution imaging by random adsorbed molecule probes. Nano Lett 8(4):1159-1162.
41. Walder R, Nelson N, Schwartz DK (2011) Super-resolution surface mapping using the trajectories of molecular probes. Nat Commun 2:515.
42. Skaug MJ, Schwartz DK (2012) Using the dynamics of fluorescent cations to probe and map charged surfaces. Soft Matter 8(48):12017-12024.
43. Kastantin M, Keller TF, Jandt KD, Schwartz DK (2012) Single-molecule tracking of fibrinogen dynamics on nanostructured poly(ethylene) films. Adv Funct Mater 22(12): 2617-2623.
44. Lippincott-Schwartz J, Manley S (2009) Putting super-resolution fluorescence microscopy to work. Nat Methods 6(1):21-23.
45. Kang SH, Shortreed MR, Yeung ES (2001) Real-time dynamics of single-DNA molecules undergoing adsorption and desorption at liquid-solid interfaces. Anal Chem 73(6): 1091-1099.
46. Xu X-HN, Yeung ES (1998) Long-range electrostatic trapping of single-protein molecules at a liquid-solid interface. Science 281(5383):1650-1653.
47. Cuppett CM, Doneski LJ, Wirth MJ (2000) Irreversible adsorption of lysozyme to polishing marks on silica. Langmuir 16(18):7279-7284.
48. Ludes MD, Wirth MJ (2002) Single-molecule resolution and fluorescence imaging of mixed-mode sorption of a dye at the interface of C18 and acetonitrile/water. Anal Chem 74(2):386-393.
49. Wirth MJ, Legg MA (2007) Single-molecule probing of adsorption and diffusion on silica surfaces. Annu Rev Phys Chem 58:489-510.
50. Wirth MJ, Swinton DJ, Ludes MD (2003) Adsorption and diffusion of single molecules at chromatographic interfaces. J Phys Chem B 107(26):6258-6268.
51. Zhong Z, Lowry M, Wang G, Geng L (2005) Probing strong adsorption of solute onto C18-silica gel by fluorescence correlation imaging and single-molecule spectroscopy under RPLC conditions. Anal Chem 77(8):2303-2310.
52. Fang N, Zhang H, Li J, Li HW, Yeung ES (2007) Mobility-based wall adsorption isotherms for comparing capillary electrophoresis with single-molecule observations. Anal Chem 79(16):6047-6054.
53. Myers GA, Gacek DA, Peterson EM, Fox CB, Harris JM (2012) Microscopic rates of peptide-phospholipid bilayer interactions from single-molecule residence times. J Am Chem Soc 134(48):19652-19660.
54. Skaug MJ, Mabry J, Schwartz DK (2013) Intermittent molecular hopping at the solidliquid interface. Phys Rev Lett 110(25):256101.
55. Giddings JC (1965) Dynamics of Chromatography (CRC, Boca Raton, FL).
56. Giddings JC, Eyring H (1955) A molecular dynamic theory of chromatography. J Phys Chem 59(5):416-421.
57. Pasti L, Cavazzini A, Felinger A, Martin M, Dondi F (2005) Single-molecule observation and chromatography unified by Lévy process representation. Anal Chem 77(8): 2524-2535.
58. Daniels CR, et al. (2012) Fluorescence correlation spectroscopy study of protein transport and dynamic interactions with clustered-charge peptide adsorbents. J Mol Recognit 25(8):435-442.
59. Boschetti E (1994) Advanced sorbents for preparative protein separation purposes. J Chromatogr A 658(2):207-236.
60. Daniels CR, Reznik C, Landes CF (2010) Dye diffusion at surfaces: Charge matters. Langmuir 26(7):4807-4812.
61. Stuart DI, et al. (1986) Alpha-lactalbumin possesses a novel calcium binding loop. Nature 324(6092):84-87.
62. Wirth MJ, Fairbank RW, Fatunmbi HO (1997) Mixed self-assembled monolayers in chemical separations. Science 275(5296):44-47.
63. McQuarrie DA (1963) On the stochastic theory of chromatography. J Chem Phys 38(2): 437-445.
64. Kastantin M, Walder R, Schwartz DK (2012) Identifying mechanisms of interfacial dynamics using single-molecule tracking. Langmuir 28(34):12443-12456.
65. Zielesny A (2011) From Curve Fitting to Machine Learning: An Illustrative Guide to Scientific Data Analysis and Computational Intelligence (Springer, Berlin).
66. Pernodet N, Maaloum M, Tinland B (1997) Pore size of agarose gels by atomic force microscopy. Electrophoresis 18(1):55-58.
67. Cuatrecasas P (1970) Protein purification by affinity chromatography: Derivatizations of agarose and polyacrylamide beads. J Biol Chem 245(12):3059-3065.
68. Dondi F, Cavazzini A, Pasti L (2006) Chromatography as Lévy stochastic process. J Chromatogr A 1126(1-2):257-267.
69. Chandra N, Brew K, Acharya KR (1998) Structural evidence for the presence of a secondary calcium binding site in human α-lactalbumin. Biochemistry 37(14):4767-4772.