Characterization of the conformational and orientational dynamics of ganglioside GM1 in a dipalmitoylphosphatidylcholine bilayer by molecular dynamics simulations

Biochimica et Biophysica Acta - Biomembranes

Volumn 1768, Issue 6, 2007, Pages 1628-1640

  Patel, Ronak Y ^a   Balaji, Petety V ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

Author keywords

Cell surface recognition; Conformational restriction; DPPC bilayer; Glycolipids; Lipid environment; Local perturbation of bilayer

Indexed keywords

DIPALMITOYLPHOSPHATIDYLCHOLINE; GANGLIOSIDE GM1;

ARTICLE; BILAYER MEMBRANE; CHEMICAL STRUCTURE; CONFORMATION; HUMAN; LIPID BILAYER; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING;

1,2-DIPALMITOYLPHOSPHATIDYLCHOLINE; COMPUTER SIMULATION; G(M1) GANGLIOSIDE; LIPID BILAYERS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN CONFORMATION;

EID: 34249106746     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2007.02.020     Document Type: Article

References (86)

1. Brodsky V.Y. Direct cell-cell communication: a new approach derived from recent data on the nature and self-organisation of ultradian (circahoralian) intracellular rhythms. Biol. Rev. Camb. Philos. Soc. 81 (2006) 143-162
2. d'Azzo A., Tessitore A., and Sano R. Gangliosides as apoptotic signals in ER stress response. Cell Death Differ. 13 (2006) 404-414
3. Hakomori S.I. The glycosynapse. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 225-232
4. Lauc G., and Heffer-Lauc M. Shedding and uptake of gangliosides and glycosylphosphatidylinositol-anchored proteins. Biochim. Biophys. Acta, Gen. Subj. 1760 (2006) 584-602
5. Lovat P.E., Corazzari M., Di Sano F., Piacentini M., and Redfern C.P.F. The role of gangliosides in fenretinide-induced apoptosis of neuroblastoma. Cancer Lett. 228 (2005) 105-110
6. Mocchetti I. Exogenous gangliosides, neuronal plasticity and repair, and the neurotrophins. Cell Mol. Life Sci. 62 (2005) 2283-2294
7. Schnaar R.L. Glycolipid-mediated cell-cell recognition in inflammation and nerve regeneration. Arch. Biochem. Biophys. 426 (2004) 163-172
8. Yu R.K., Bieberich E., Xia T., and Zeng G. Regulation of ganglioside biosynthesis in the nervous system. J. Lipid Res. 45 (2004) 783-793
9. Yuki N. Carbohydrate mimicry: a new paradigm of autoimmune diseases. Curr. Opin. Immunol. 17 (2005) 577-582
10. Schengrund C.L. "Multivalent" saccharides: development of new approaches for inhibiting the effects of glycosphingolipid-binding pathogens. Biochem. Pharmacol. 65 (2003) 699-707
11. Yowler B.C., and Schengrund C.L. Botulinum neurotoxin A changes conformation upon binding to ganglioside GT1b. Biochemistry 43 (2004) 9725-9731
12. Acquotti D., Poppe L., Dabrowski J., Von der Lieth C.W., Sonnino S., and Tettamanti G. Three-dimensional structure of the oligosaccharide chain of GM1 ganglioside revealed by a distance-mapping procedure: a rotating and laboratory frame nuclear Overhauser enhancement investigation of native glycolipid in dimethyl sulfoxide and in water-dodecylphosphocholine solutions. J. Am. Chem. Soc. 112 (1990) 7772-7778
13. Scarsdale J.N., Prestegard J.H., and Yu R.K. NMR and computational studies of interactions between remote residues in gangliosides. Biochemistry 29 (1990) 9843-9855
14. Vasudevan S.V., and Balaji P.V. Dynamics of ganglioside headgroup in lipid environment: molecular dynamics simulations of GM1 embedded in dodecylphosphocholine micelle. J. Phys. Chem., B 105 (2001) 7033-7041
15. Roy D., and Mukhopadhyay C. Molecular dynamics simulation of GM1 in phospholipid bilayer. J. Biomol. Struct. Dyn. 19 (2002) 1121-1132
16. Bach D., Sela B., and Miller I.R. Compositional aspects of lipid hydration. Chem. Phys. Lipids 31 (1982) 381-394
17. McDaniel R.V., McLaughlin A., Winiski A.P., Eisenberg M., and McLaughlin S. Bilayer membranes containing the ganglioside GM1: models for electrostatic potentials adjacent to biological membranes. Biochemistry 23 (1984) 4618-4624
18. Goins B., Masserini M., Barisas B.G., and Freire E. Lateral diffusion of ganglioside GM1 in phospholipid bilayer membranes. Biophys. J. 49 (1986) 849-856
19. Reed R.A., Mattai J., and Shipley G.G. Interaction of cholera toxin with ganglioside G(M1) receptors in supported lipid monolayers. Biochemistry 26 (1987) 824-832
20. Ollmann M., Schwarzmann G., Sandhoff K., and Galla H.J. Pyrene-labeled gangliosides: micelle formation in aqueous solution, lateral diffusion, and thermotropic behavior in phosphatidylcholine bilayers. Biochemistry 26 (1987) 5943-5952
21. McIntosh T.J., and Simon S.A. Long- and short-range interactions between phospholipid/ganglioside GM1 bilayers. Biochemistry 33 (1994) 10477-10486
22. Arnulphi C., Levstein P.R., Ramia M.E., Martin C.A., and Fidelio G.D. Ganglioside hydration study by 2H-NMR: dependence on temperature and water/lipid ratio. J. Lipid Res. 38 (1997) 1412-1420
23. Majewski J., Kuhl T.L., Kjaer K., and Smith G.S. Packing of ganglioside-phospholipid monolayers: an X-ray diffraction and reflectivity study. Biophys. J. 81 (2001) 2707-2715
24. Hayakawa T., and Hirai M. Hydration and thermal reversibility of glycolipids depending on sugar chains. Eur. Biophys. J. 31 (2002) 62-72
25. Hirai M., Iwase H., Hayakawa T., Koizumi M., and Takahashi H. Determination of asymmetric structure of ganglioside-DPPC mixed vesicle using SANS, SAXS, and DLS. Biophys. J. 85 (2003) 1600-1610
26. Rao V.S.R., Qasba P.K., Balaji P.V., and Chandrasekaran R. Conformation of Carbohydrates (1998), Harwood Academic, Singapore Chap. 4
27. Vasudevan S.V., and Balaji P.V. Comparative analysis of ganglioside conformations by MD simulations: implications for specific recognition by proteins. J. Mol. Struct. (Theochem) 583 (2002) 215-232
28. Pascher I., and Sundell S. Molecular arrangements in sphingolipids. The crystal structure of cerebroside. Chem. Phys. Lipids 20 (1977) 175-191
29. Patel R.Y., and Balaji P.V. Effect of the choice of the pressure coupling method on the spontaneous aggregation of DPPC molecules. J. Phys. Chem., B 109 (2005) 14667-14674
30. Berendsen H.J.C., van der Spoel D., and van Drunen R. GROMACS: a message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 91 (1995) 43-56
31. Lindahl E., Hess B., and van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model 7 (2001) 306-317
32. Berendsen H.J.C., Postma J.P.M., van Gunsteren W.F., DiNola A., and Haak J.R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81 (1984) 3684-3690
33. Tristram-Nagle S., and Nagle J.F. Lipid bilayers: thermodynamics, structure, fluctuations, and interactions. Chem. Phys. Lipids 127 (2004) 3-14
34. Berger O., Edholm O., and Jahnig F. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72 (1997) 2002-2013
35. Chiu S.W., Clark M., Balaji V., Subramaniam S., Scott H.L., and Jakobsson E. Incorporation of surface tension into molecular dynamics simulation of an interface: a fluid phase lipid bilayer membrane. Biophys. J. 69 (1995) 1230-1245
36. Patra M., Karttunen M., Hyvonen M.T., Falck E., Lindqvist P., and Vattulainen I. Molecular dynamics simulations of lipid bilayers: major artifacts due to truncating electrostatic interactions. Biophys. J. 84 (2003) 3636-3645
37. Patra M., Karttunen M., Hyvonen M.T., Falck E., and Vattulainen I. Lipid bilayers driven to a wrong lane in molecular dynamics simulations by subtle changes in long-range electrostatic interactions. J. Phys. Chem., B 108 (2004) 4485-4494
38. Spieser S.A.H., Van Kuik J.A., Kroon-Batenburg L.M.J., and Kroon J. Improved carbohydrate force field for GROMOS: ring and hydroxymethyl group conformations and exo-anomeric effect. Carbohydr. Res. 322 (1999) 264-273
39. Sega M., Brocca P., Melchionna S., and Vallauri R. Molecular dynamics simulation of a GM3 ganglioside bilayer. J. Phys. Chem., B 108 (2004) 20322-20330
40. Chiu S.W., Vasudevan S., Jakobsson E., Mashl R.J., and Scott Jr. H.L. Structure of sphingomyelin bilayers: a simulation study. Biophys. J. 85 (2003) 3624-3635
41. Lee B., and Richards F.M. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55 (1971) 379-400
42. Brocca P., Bernardi A., Raimondi L., and Sonnino S. Modeling ganglioside headgroups by conformational analysis and molecular dynamics. Glycoconj. J. 17 (2000) 283-299
43. Harris R., Kiddle G.R., Field R.A., Milton M.J., Ernst B., Magnani J.L., and Homans S.W. Stable-isotope-assisted NMR studies on 13C-enriched sialyl Lewis(X) in solution and bound to E-selectin. J. Am. Chem. Soc. 121 (1999) 2546-2551
44. Poppe L., Dabrowski J., Von Der Lieth C.W., Numata M., and Ogawa T. Solution conformation of sialosylcerebroside (G(M4)) and its NeuAc(alpha2-3)Gal sugar component. Eur. J. Biochem. 180 (1989) 337-342
45. Poppe L., Brown G.S., Philo J.S., Nikrad P.V., and Shah B.H. Conformation of sLe(x) tetrasaccharide, free in solution and bound to E-, P-, and l-selectin. J. Am. Chem. Soc. 119 (1997) 1727-1736
46. Siebert H.C., Andre S., Lu S.Y., Frank M., Kaltner H., Van Kuik J.A., Korchagina E.Y., Bovin N., Tajkhorshid E., Kaptein R., Vliegenthart J.F.G., Von Der Lieth C.W., Jimenez-Barbero J., Kopitz J., and Gabius H.J. Unique conformer selection of human growth-regulatory lectin Galectin-1 for ganglioside GM1 versus bacterial toxins. Biochemistry 42 (2003) 14762-14773
47. Veluraja K., and Rao V.S.R. Theoretical studies on the conformation of monosialogangliosides and disialogangliosides. Carbohydr. Polym. 3 (1983) 175-192
48. Jarrell H., Singh D., and Grant C.W.M. Oligosaccharide order in a membrane-incorporated complex glycosphingolipid. Biochim. Biophys. Acta, Biomembr. 1103 (1992) 331-334
49. Sabesan S., Block K., and Lemieux R.U. The conformational properties of the ganglioside GM2 and GM1 based on 1H and 13C nuclear magnetic resonance studies. Can. J. Chem. 62 (1984) 1034-1045
50. Nyholm P., and Pascher I. Steric presentation and recognition of the saccharide chains of glycolipids at the cell surface: favoured conformations of the saccharide-lipid linkage calculated using molecular mechanics (MM3). Int. J. Biol. Macromol. 15 (1993) 43-51
51. Nyholm P.G., and Pascher I. Orientation of the saccharide chains of glycolipids at the membrane surface: conformational analysis of the glucose-ceramide and the glucose-glyceride linkages using molecular mechanics (MM3). Biochemistry 32 (1993) 1225-1234
52. Nagle J.F., and Tristram-Nagle S. Lipid bilayer structure. Curr. Opin. Struct. Biol. 10 (2000) 474-480
53. Almond A. Towards understanding the interaction between oligosaccharides and water molecules. Carbohydr. Res. 340 (2005) 907-920
54. Maggio B., Bianco I.D., Montich G.G., Fidelio G.D., and Yu R.K. Regulation by gangliosides and sulfatides of phospholipase A2 activity against dipalmitoyl- and dilauroylphosphatidylcholine in small unilamellar bilayer vesicles and mixed monolayers. Biochim. Biophys. Acta, Biomembr. 1190 (1994) 137-148
55. Daniele J.J., Maggio B., Bianco I.D., Goni F.M., Alonso A., and Fidelio G.D. Inhibition by gangliosides of Bacillus cereus phospholipase C activity against monolayers, micelles and bilayer vesicles. Eur. J. Biochem. 239 (1996) 105-110
56. Jain M.K., Rogers J., and DeHaas G.H. Kinetics of binding of phospholipase A2 to lipid/water interfaces and its relationship to interfacial activation. Biochim. Biophys. Acta, Biomembr. 940 (1988) 51-62
57. Langner M., and Kubica K. The electrostatics of lipid surfaces. Chem. Phys. Lipids 101 (1999) 3-35
58. Reed R.A., and Shipley G.G. Properties of ganglioside GM1 in phosphatidylcholine bilayer membranes. Biophys. J. 70 (1996) 1363-1372
59. Safran S.A. Statistical Thermodynamics of Surfaces, Interfaces, and Membranes (1994), Addison-Wesley, Reading, MA
60. Lindahl E., and Edholm O. Mesoscopic undulations and thickness fluctuations in lipid bilayers from molecular dynamics simulations. Biophys. J. 79 (2000) 426-433
61. Brannigan G., and Brown F.L.H. A consistent model for thermal fluctuations and protein-induced deformations in lipid bilayers. Biophys. J. 90 (2006) 1501-1520
62. Ravichandra B., and Joshi P.G. Gangliosides asymmetrically alter the membrane order in cultured PC-12 cells. Biophys. Chem. 76 (1999) 117-132
63. Bertoli E., Masserini M., and Sonnino S. Electron paramagnetic resonance studies on the fluidity and surface dynamics of egg phosphatidylcholine vesicles containing gangliosides. Biochim. Biophys. Acta 647 (1981) 196-202
64. Kopitz J., Von Reitzenstein C., Andre S., Kaltner H., Uhl J., Ehemann V., Cantz M., and Gabius H.J. Negative regulation of neuroblastoma cell growth by carbohydrate-dependent surface binding of Galectin-1 and functional divergence from Galectin-3. J. Biol. Chem. 276 (2001) 35917-35923
65. Kopitz J., Andre S., Von Reitzenstein C., Versluis K., Kaltner H., Pieters R.J., Wasano K., Kuwabara I., Liu F.T., Cantz M., Heck A.J.R., and Gabius H.J. Homodimeric galectin-7 (p53-induced gene 1) is a negative growth regulator for human neuroblastoma cells. Oncogene 22 (2003) 6277-6288
66. Van Heyningen S. Cholera toxin: interaction of subunits with ganglioside G(M1). Science 183 (1974) 656-657
67. Allende M.L., and Proia R.L. Lubricating cell signaling pathways with gangliosides. Curr. Opin. Struct. Biol. 12 (2002) 587-592
68. Fishman P.H., and Brady R.O. Biosynthesis and function of gangliosides. Science 194 (1976) 906-915
69. Kalka D., Von Reitzenstein C., Kopitz J., and Cantz M. The plasma membrane ganglioside sialidase cofractionates with markers of lipid rafts. Biochem. Biophys. Res. Commun. 283 (2001) 989-993
70. Evans S.V., and Roger MacKenzie C. Characterization of protein-glycolipid recognition at the membrane bilayer. J. Mol. Recognit. 12 (1999) 155-168
71. Rock P., Allietta M., Young Jr. W.W., Thompson T.E., and Tillack T.W. Ganglioside G(M1) and asialo-G(M1) at low concentration are preferentially incorporated into the gel phase in two-component, two-phase phosphatidylcholine bilayers. Biochemistry 30 (1991) 19-25
72. Delmelle M., Dufrane S.P., Brasseur R., and Ruysschaert J.M. Clustering of gangliosides in phospholipid bilayers. FEBS Lett. 121 (1980) 11-14
73. Peters M.W., and Grant C.W.M. Freeze-etch study of an unmodified lectin interacting with its receptors in model membranes. Biochim. Biophys. Acta 775 (1984) 273-282
74. Peters M.W., Mehlhorn I.E., Barber K.R., and Grant C.W.M. Evidence of a distribution difference between two gangliosides in bilayer membranes. Biochim. Biophys. Acta, Biomembr. 778 (1984) 419-428
75. Harder T., Scheiffele P., Verkade P., and Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141 (1998) 929-942
76. Gellermann G.P., Appel T.R., Tannert A., Radestock A., Hortschansky P., Schroeckh V., Leisner C., Lutkepohl T., Shtrasburg S., Rocken C., Pras M., Linke R.P., Diekmann S., and Fandrich M. Raft lipids as common components of human extracellular amyloid fibrils. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 6297-6302
77. Bacia K., Scherfeld D., Kahya N., and Schwille P. Fluorescence correlation spectroscopy relates rafts in model and native membranes. Biophys. J. 87 (2004) 1034-1043
78. Palestini P., Masserini M., and Tettamanti G. Exposure to galactose oxidase of GM1 ganglioside molecular species embedded into phospholipid vesicles. FEBS Lett. 350 (1994) 219-222
79. Pitto M., Palestini P., and Masserini M. Dependence of rat liver CMP-N-acetylneuraminate:GM1 sialyltransferase (SAT IV) activity on the ceramide composition of GM1 ganglioside. FEBS Lett. 383 (1996) 223-226
80. Sayle R.A., and Milner-White E.J. RASMOL: biomolecular graphics for all. Trends Biochem. Sci. 20 (1995) 374-376
81. DeLano W.L. The PyMOL Molecular Graphics System (2002), DeLano Scientific, San Carlos, CA, USA
82. Rodgers J.C., and Portoghese P.S. Molecular modeling of the conformational and sodium ion binding properties of the oligosaccharide component of ganglioside GM1. Biopolymers 34 (1994) 1311-1326
83. Bernardi A., and Raimondi L. Conformational analysis of GM1 oligosaccharide in water solution with a new set of parameters for the Neu5Ac moiety. J. Org. Chem. 60 (1995) 3370-3377
84. Sharmila D.J., and Veluraja K. Monosialogangliosides and their interaction with cholera toxin-investigation by molecular modeling and molecular mechanics. J. Biomol. Struct. Dyn. 21 (2004) 591-614
85. Merritt E.A., Kuhn P., Sarfaty S., Erbe J.L., Holmes R.K., and Hol W.G. The 1.25 A resolution refinement of the cholera toxin B-pentamer: evidence of peptide backbone strain at the receptor-binding site. J. Mol. Biol. 282 (1998) 1043-1059
86. Engelsen S.B., Monteiro C., Herve de Penhoat C., and Perez S. The diluted aqueous solvation of carbohydrates as inferred from molecular dynamics simulations and NMR spectroscopy. Biophys. Chem. 93 (2001) 103-127