Binding cooperativity matters: A gm1-like ganglioside-cholera toxin b subunit binding study using a nanocube-based lipid bilayer array

PLoS ONE

Volumn 11, Issue 4, 2016, Pages

  Worstell, Nolan C ^a   Krishnan, Pratik ^a   Weatherston, Joshua D ^a   Wu, Hung Jen ^a  

^a Department of Electrical and Computer Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLERA TOXIN B SUBUNIT; GANGLIOSIDE GM1; GANGLIOSIDE GM2; SILICA NANOPARTICLE; CHOLERA TOXIN; FUCOSYL GM1 GANGLIOSIDE; LIPID BILAYER; METAL NANOPARTICLE; PROTEIN BINDING; SILICON DIOXIDE; SILVER;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DISSOCIATIVE AMNESIA; LIPID ANALYSIS; LIPID BILAYER; MOLECULAR INTERACTION; QUANTITATIVE ANALYSIS; ANALOGS AND DERIVATIVES; BIOLOGICAL MODEL; CHEMISTRY; CRYOELECTRON MICROSCOPY; IN VITRO STUDY; KINETICS; METABOLISM; NANOTECHNOLOGY; SURFACE PLASMON RESONANCE; ULTRASTRUCTURE;

CHOLERA TOXIN; CRYOELECTRON MICROSCOPY; G(M1) GANGLIOSIDE; G(M2) GANGLIOSIDE; IN VITRO TECHNIQUES; KINETICS; LIPID BILAYERS; METAL NANOPARTICLES; MODELS, BIOLOGICAL; NANOTECHNOLOGY; PROTEIN BINDING; SILICON DIOXIDE; SILVER; SURFACE PLASMON RESONANCE;

EID: 84963731514     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0153265     Document Type: Article

References (48)

1. Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, et al. Essentials of Glycobiology. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, et al., editors. Essentials of Glycobiology. Cold Spring Harbor NY2009.
2. Schoen A, Freire E. Thermodynamics of intersubunit interactions in cholera toxin upon binding to the oligosaccharide portion of its cell surface receptor, ganglioside GM1. Biochemistry. 1989; 28 (12):5019-24. doi: 10.1021/bi00438a017 PMID: 2765522
3. Pukin AV, Branderhorst HM, Sisu C, Weijers CAGM, Gilbert M, Liskamp RMJ, et al. Strong Inhibition of Cholera Toxin by Multivalent GM1 Derivatives. ChemBioChem. 2007; 8(13):1500-3. doi: 10.1002/cbic. 200700266 PMID: 17625801
4. Turnbull WB, Precious BL, Homans SW. Dissecting the Cholera Toxin-Ganglioside GM1 Interaction by Isothermal Titration Calorimetry. Journal of the American Chemical Society. 2004; 126(4):1047-54. doi: 10.1021/ja0378207 PMID: 14746472
5. Lin H, Kitova E, Klassen J. Measuring Positive Cooperativity Using the Direct ESI-MS Assay. Cholera Toxin B Subunit Homopentamer Binding to GM1 Pentasaccharide. J Am Soc Mass Spectrom. 2014; 25 (1):104-10. doi: 10.1007/s13361-013-0751-5 PMID: 24122305
6. Cecioni S, Imberty A, Vidal S. Glycomimetics versus multivalent glycoconjugates for the design of high affinity lectin ligands. Chem Rev. 2015; 115(1):525-61. doi: 10.1021/cr500303t PMID: 25495138.
7. Sheikh KA, Deerinck TJ, Ellisman MH, Griffin JW. The distribution of ganglioside-like moieties in peripheral nerves. Brain. 1999; 122(3):449-60. doi: 10.1093/brain/122.3.449
8. Willison HJ, Yuki N. Peripheral neuropathies and anti-glycolipid antibodies. Brain. 2002; 125(12):2591-625. doi: 10.1093/brain/awf272
9. Yanagisawa M, Ariga T, Yu RK. Letter to the Glyco-Forum: Cholera toxin B subunit binding does not correlate with GM1 expression: A study using mouse embryonic neural precursor cells. Glycobiology. 2006; 16(9):19G-22G. doi: 10.1093/glycob/cwl003 PMID: 16964630
10. Park S, Gildersleeve JC, Blixt O, Shin I. Carbohydrate microarrays. Chem Soc Rev. 2013; 42 (10):4310-26. doi: 10.1039/c2cs35401b PMID: 23192235.
11. Wang L, Cummings RD, Smith DF, Huflejt M, Campbell CT, Gildersleeve JC, et al. Cross-platform comparison of glycan microarray formats. Glycobiology. 2014; 24(6):507-17. doi: 10.1093/glycob/cwu019 PMID: 24658466; PubMed Central PMCID: PMC4001710.
12. Lauer S, Goldstein B, Nolan RL, Nolan JP. Analysis of Cholera Toxin-Ganglioside Interactions by Flow Cytometry†. Biochemistry. 2002; 41(6):1742-51. doi: 10.1021/bi0112816 PMID: 11827518
13. Ma Y, Sobkiv I, Gruzdys V, Zhang H, Sun XL. Liposomal glyco-microarray for studying glycolipid-protein interactions. Anal Bioanal Chem. 2012; 404(1):51-8. doi: 10.1007/s00216-012-6096-2 PMID: 22627703.
14. Zhu XY, Holtz B, Wang YN, Wang LX, Orndorff PE, Guo A. Quantitative Glycomics from Fluidic Glycan Microarrays. Journal of the American Chemical Society. 2009; 131(38):13646-50. doi: 10.1021/ja902783n WOS:000270186600033. PMID: 19731906
15. Leney AC, Fan X, Kitova EN, Klassen JS. Nanodiscs and Electrospray Ionization Mass Spectrometry: A Tool for Screening Glycolipids Against Proteins. Analytical Chemistry. 2014; 86(11):5271-7. doi: 10. 1021/ac4041179 PMID: 24779922
16. Yamazaki V, Sirenko O, Schafer RJ, Nguyen L, Gutsmann T, Brade L, et al. Cell membrane array fabrication and assay technology. BMC Biotechnol. 2005; 5:18. doi: 10.1186/1472-6750-5-18 PMID: 15960850; PubMed Central PMCID: PMC1177928.
17. Castellana ET, Cremer PS. Imaging large arrays of supported lipid bilayers with a macroscope. Biointerphases. 2007; 2(2):57-63. doi: 10.1116/1.2732312 PMID: 20408637
18. Tanaka M, Sackmann E. Polymer-supported membranes as models of the cell surface. Nature. 2005; 437(7059):656-63. PMID: 16193040
19. Wu H-J, Henzie J, Lin W-C, Rhodes C, Li Z, Sartorel E, et al. Membrane-protein binding measured with solution-phase plasmonic nanocube sensors. Nat Meth. 2012; 9(12):1189-91. http://www.nature.com/nmeth/journal/v9/n12/abs/nmeth.2211.html#supplementary-information.
20. Tao A, Sinsermsuksakul P, Yang P. Polyhedral Silver Nanocrystals with Distinct Scattering Signatures. Angewandte Chemie International Edition. 2006; 45(28):4597-601. doi: 10.1002/anie.200601277
21. Wang R, Tang J, Liu J, Wang Y, Huang Z. Preparation of Ag@SiO2Dispersion in Different Solvents and Investigation of its Optical Properties. Journal of Dispersion Science and Technology. 2011; 32 (4):532-7. doi: 10.1080/01932691003757082
22. Niitsoo O, Couzis A. Facile synthesis of silver core-silica shell composite nanoparticles. J Colloid Interface Sci. 2011; 354(2):887-90. doi: 10.1016/j.jcis.2010.11.013 PMID: 21145562.
23. Sun Y, Mayers B, Herricks T, Xia Y. Polyol Synthesis of Uniform Silver Nanowires: A Plausible Growth Mechanism and the Supporting Evidence. Nano Letters. 2003; 3(7):955-60. doi: 10.1021/nl034312m
24. Mornet S, Lambert O, Duguet E, Brisson A. The Formation of Supported Lipid Bilayers on Silica Nanoparticles Revealed by Cryoelectron Microscopy. Nano Letters. 2005; 5(2):281-5. doi: 10.1021/nl048153y PMID: 15794611
25. Shi JJ, Yang TL, Kataoka S, Zhang YJ, Diaz AJ, Cremer PS. GM(1) clustering inhibits cholera toxin binding in supported phospholipid membranes. Journal of the American Chemical Society. 2007; 129 (18):5954-61. doi: 10.1021/ja069375w WOS:000246180200044. PMID: 17429973
26. Jung H, Robison AD, Cremer PS. Multivalent ligand-receptor binding on supported lipid bilayers. Journal of Structural Biology. 2009; 168(1):90-4. doi: 10.1016/j.jsb.2009.05.010 PMID: 19508894
27. Kim CS, Seo JH, Cha HJ. Functional Interaction Analysis of GM1-Related Carbohydrates and Vibrio cholerae Toxins Using Carbohydrate Microarray. Analytical Chemistry. 2012; 84(15):6884-90. doi: 10. 1021/ac301511t PMID: 22770420
28. Kuziemko GM, Stroh M, Stevens RC. Cholera Toxin Binding Affinity and Specificity for Gangliosides Determined by Surface Plasmon Resonance. Biochemistry. 1996; 35(20):6375-84. doi: 10.1021/bi952314i PMID: 8639583
29. MacKenzie CR, Hirama T, Lee KK, Altman E, Young NM. Quantitative analysis of bacterial toxin affinity and specificity for glycolipid receptors by surface plasmon resonance. J Biol Chem. 1997; 272 (9):5533-8. WOS:A1997WK74700027. PMID: 9038159
30. Schengrund CL, Ringler NJ. Binding of Vibrio cholera toxin and the heat-labile enterotoxin of Escherichia coli to GM1, derivatives of GM1, and nonlipid oligosaccharide polyvalent ligands. J Biol Chem. 1989; 264(22):13233-7. PMID: 2666416
31. Sly KL, Conboy JC. Determination of Multivalent Protein-Ligand Binding Kinetics by Second-Harmonic Correlation Spectroscopy. Analytical Chemistry. 2014; 86(22):11045-54. doi: 10.1021/ac500094v
32. Winter EM, Groves JT. Surface Binding Affinity Measurements from Order Transitions of Lipid Membrane-Coated Colloidal Particles. Analytical Chemistry. 2006; 78(1):174-80. doi: 10.1021/ac0514927 PMID: 16383325
33. Terrell J, Yadava P, Castro C, Hughes J. Liposome Fluidity Alters Interactions Between the Ganglioside GM1 and Cholera Toxin B Subunit. Journal of Liposome Research. 2008; 18(1):21-9. doi: 10.1080/08982100801893929 PMID: 18348069
34. Masserini M, Freire E, Palestini P, Calappi E, Tettamanti G. Fuc-GM1 ganglioside mimics the receptor function of GM1 for cholera toxin. Biochemistry. 1992; 31(8):2422-6. doi: 10.1021/bi00123a030 PMID: 1311601
35. Iwabuchi K, Nakayama H, Masuda H, Kina K, Ogawa H, Takamori K. Membrane microdomains in immunity: Glycosphingolipid-enriched domain-mediated innate immune responses. BioFactors. 2012; 38(4):275-83. doi: 10.1002/biof.1017 PMID: 22488955
36. Molander-Melin M, Blennow K, Bogdanovic N, Dellheden B, Månsson J-E, Fredman P. Structural membrane alterations in Alzheimer brains found to be associated with regional disease development; increased density of gangliosides GM1 and GM2 and loss of cholesterol in detergent-resistant membrane domains. Journal of Neurochemistry. 2005; 92(1):171-82. doi: 10.1111/j.1471-4159.2004. 02849.x PMID: 15606906
37. Giuliani A, Calappi E, Mineo E, Neri MG, Gallina A, Pessina A. The different inhibiting effect of cholera toxin on two leukemia cell lines does not correlate with their toxin binding capacity. Mol Cell Biochem. 1995; 152(2):103-12. doi: 10.1007/BF01076072 PMID: 8751156
38. Dawson G. Measuring brain lipids. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids. 2015; 1851(8):1026-39. doi: 10.1016/j.bbalip.2015.02.007
39. Yanagisawa M, Yu RK. The expression and functions of glycoconjugates in neural stem cells. Glycobiology. 2007; 17(7):57R-74R. doi: 10.1093/glycob/cwm018 PMID: 17307762
40. Mikhalyov I, Samsonov A. Lipid raft detecting in membranes of live erythrocytes. Biochimica et Biophysica Acta (BBA)-Biomembranes. 2011; 1808(7):1930-9. doi: 10.1016/j.bbamem.2011.04.002
41. Tuosto L, Parolini I, Schröder S, Sargiacomo M, Lanzavecchia A, Viola A. Organization of plasma membrane functional rafts upon T cell activation. European Journal of Immunology. 2001; 31(2):345-9. doi: 10.1002/1521-4141(200102)31:23.0.CO;2-L PMID: 11180097
42. Schwarz A, Futerman AH. Determination of the Localization of Gangliosides Using Anti-ganglioside Antibodies: Comparison of Fixation Methods. Journal of Histochemistry & Cytochemistry. 1997; 45 (4):611-8. doi: 10.1177/002215549704500413
43. Tao SC, Li Y, Zhou J, Qian J, Schnaar RL, Zhang Y, et al. Lectin microarrays identify cell-specific and functionally significant cell surface glycan markers. Glycobiology. 2008; 18(10):761-9. doi: 10.1093/glycob/cwn063 PMID: 18625848; PubMed Central PMCID: PMC2733773.
44. Arnaud J, Audfray A, Imberty A. Binding sugars: From natural lectins to synthetic receptors and engineered neolectins. Chem Soc Rev. 2013; 42(11):4798-813. doi: 10.1039/c2cs35435g PMID: 23353569.
45. Hu S, Wong DT. Lectin microarray. Proteomics Clin Appl. 2009; 3(2):148-54. doi: 10.1002/prca. 200800153 PMID: 21132067; PubMed Central PMCID: PMC2995448.
46. Rinaldi S, Brennan KM, Goodyear CS, O'Leary C, Schiavo G, Crocker PR, et al. Analysis of lectin binding to glycolipid complexes using combinatorial glycoarrays. Glycobiology. 2009; 19(7):789-96. doi: 10.1093/glycob/cwp049 PMID: 19349623; PubMed Central PMCID: PMC2688392.
47. Gallegos KM, Conrady DG, Karve SS, Gunasekera TS, Herr AB, Weiss AA. Shiga Toxin Binding to Glycolipids and Glycans. PLoS ONE. 2012; 7(2):e30368. doi: 10.1371/journal.pone.0030368 PMC3278406. PMID: 22348006
48. Palma AS, Feizi T, Childs RA, Chai W, Liu Y. The neoglycolipid (NGL)-based oligosaccharide microarray system poised to decipher the meta-glycome. Curr Opin Chem Biol. 2014; 18:87-94. doi: 10.1016/j. cbpa.2014.01.007 PMID: 24508828; PubMed Central PMCID: PMC4105633.