Reconciliation of opposing views on membrane-sugar interactions

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

Volumn 108, Issue 5, 2011, Pages 1874-1878

  Andersen, Heidi D ^a   Wang, Chunhua ^a,b   Arleth, Lise ^c   Peters, Günther H ^b,d   Westh, Peter ^a,b  

^a ROSKILDE UNIVERSITY   (Denmark)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Interaction free energy; Membrane interface; Membrane structure; Preferential binding; Preferential exclusion

Indexed keywords

1,2 DIMYRISTOYL SN GLYCERO 3 PHOSPHOCHOLINE; 1,2 DIOLEOYL SN GLYCERO 3 PHOSPHOCHOLINE; GLUCOSE; PHOSPHOLIPID; SUCROSE; SUGAR; TREHALOSE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARBOHYDRATE ANALYSIS; CONFORMATION; DENSITOMETRY; LIPID BILAYER; MEMBRANE; MEMBRANE STRUCTURE; MOLECULAR INTERACTION; NEUTRON; NEUTRON SCATTERING; OSMOLALITY; PRIORITY JOURNAL; THERMODYNAMICS;

CARBOHYDRATE METABOLISM; CELL MEMBRANE; LIPID BILAYERS; NEUTRONS; SCATTERING, RADIATION; THERMODYNAMICS;

EID: 79952167898     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1012516108     Document Type: Article

References (59)

1. Somero GN (1994) Adapting to water stress: Convergence on common solutions. Water and Life, eds GN Somero, CB Osmond, and CL Bolis (Springer, Berlin).
2. Gilles R (1997) "Compensatory" organic osmolytes in high osmolarity and dehydration stresses: History and perspectives. Comp Biochem Phys A 117:279-290.
3. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water-stress - Evolution of osmolyte systems. Science 217:1214-1222. (Pubitemid 13283134)
4. Crowe JH (2007) Trehalose as a "chemical chaperone": Fact and fantasy. Molecular Aspects of the Stress Response: Chaperones, Membranes and Networks, eds P Csermely and L Vígh (Springer, New York), pp 143-158.
5. Crowe LM, Reid DS, Crowe JH (1996) Is trehalose special for preserving dry biomaterials? Biophys J 71:2087-2093.
6. Singer MA, Lindquist S (1998) Thermotolerance in Saccharomyces cerevisiae: The Yin and Yang of trehalose. Trends Biotechnol 16:460-468. (Pubitemid 28532702)
7. Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev 65:799-832.
8. Lee JC (2000) Biopharmaceutical formulation. Curr Opin Biotechnol 11:81-84.
9. Crowe JH, et al. (2001) The trehalose myth revisited: Introduction to a symposium on stabilization of cells in the dry state. Cryobiology 43:89-105. (Pubitemid 33780248)
10. Joo WH, et al. (2000) Intracellular changes of trehalose content in toluene tolerant Pseudomonas sp BCNU 171 after exposure to toluene. Biotechnol Lett 22:1021-1024. (Pubitemid 30469386)
11. Zavaglia AG, Tymczyszyn E, De Antoni G, Disalvo EA (2003) Action of trehalose on the preservation of Lactobacillus delbrueckii ssp. bulgaricus by heat and osmotic dehydration. J Appl Microbiol 95:1315-1320. (Pubitemid 37506121)
12. Fabrie C, Dekruijff B, Degier J (1990) Protection by sugars against phase transition-induced leak in hydrated dimyristoylphosphatidylcholine liposomes. Biochim Biophys Acta 1024:380-384. (Pubitemid 20182825)
13. Rudolph AS, Crowe JH (1985) Membrane stabilization during freezing - The role of 2 natural cryoprotectants, trehalose and proline. Cryobiology 22:367-377. (Pubitemid 15007575)
14. Deme B, Dubois M, Zemb T (2002) Swelling of a lecithin lamellar phase induced by small carbohydrate solutes. Biophys J 82:215-225. (Pubitemid 34289796)
15. Genova J, Zheliaskova A, Mitov MD (2007) Monosaccharides (fructose, glucose) and disaccharides (sucrose, trehalose) influence the elasticity of SOPC membranes. J Optoelectron Adv M 9:427-430.
16. Crowe JH, Whittam MA, Chapman D, Crowe LM (1984) Interactions of phospholipid monolayers with carbohydrates. Biochim Biophys Acta 769:151-159.
17. Lairion F, Disalvo EA (2007) Effect of trehalose on the contributions to the dipole potential of lipid monolayers. Chem Phys Lipids 150:117-124. (Pubitemid 47539360)
18. Lambruschini C, Relini N, Ridi A, Cordone L, Gliozzi A (2000) Trehalose interacts with phospholipid polar heads in Langmuir monolayers. Langmuir 16:5467-5470.
19. Luzardo MD, et al. (2000) Effect of trehalose and sucrose on the hydration and dipole potential of lipid bilayers. Biophys J 78:2452-2458.
20. Strauss G, Schurtenberger P, Hauser H (1986) The interaction of saccharides with lipid bilayer vesicles - Stabilization during freeze-thawing and freeze-drying. Biochim Biophys Acta 858:169-180.
21. Leekumjorn S, Sum AK (2006) Molecular investigation of the interactions of trehalose with lipid bilayers of DPPC, DPPE and their mixture. Mol Simul 32:219-230. (Pubitemid 44155062)
22. Skibinsky A, Venable RM, Pastor RW (2005) A molecular dynamics study of the response of lipid bilayers and monolayers to trehalose. Biophys J 89:4111-4121. (Pubitemid 41725631)
23. Villarreal MA, Diaz SB, Disalvo EA, Montich GG (2004) Molecular dynamics simulation study of the interaction of trehalose with lipid membranes. Langmuir 20:7844-7851.
24. van den Bogaart G, Hermans N, Krasnikov V, de Vries AH, Poolman B (2007) On the decrease in lateral mobility of phospholipids by sugars. Biophys J 92:1598-1605. (Pubitemid 46393470)
25. Cevc G (1988) Effect of lipid headgroups and (nonelectrolyte) solution on the structural and phase properties of bilayer-membranes. Ber Bunsen Phys Chem 92:953-961.
26. Deme B, Zemb T (2000) Measurement of sugar depletion from uncharged lamellar phases by SANS contrast variation. J Appl Crystallogr 33:569-573. (Pubitemid 32120526)
27. Rudolph AS, Goins B (1991) The effect of hydration stress solutes on the phase-behavior of hydrated dipalmitoylphosphatidylcholine. Biochim Biophys Acta 1066:90-94.
28. Soderlund T, Alakoskela JMI, Pakkanen AL, Kinnunen PKJ (2003) Comparison of the effects of surface tension and osmotic pressure on the interfacial hydration of a fluid phospholipid bilayer. Biophys J 85:2333-2341. (Pubitemid 37210783)
29. Stumpel J, Vaz WLC, Hallmann D (1985) An x-ray-diffraction and differential scanning calorimetric study on the effect of sucrose on the properties of phosphatidylcholine bilayers. Biochim Biophys Acta 821:165-168. (Pubitemid 16233578)
30. Takahashi H, Matsuo A, Hatta I (2002) Effects of salt on the lamellar and bicontinuous cubic phases of fully hydrated monoacylglycerol (monoelaidin). Phys Chem Chem Phys 4:2365-2370.
31. Johnston DS, Coppard E, Parera GV, Chapman D (1984) Langmuir film balance study of the interactions between carbohydrates and phospholipid monolayers. Biochemistry 23:6912-6919.
32. Diaz S, Amalfa F, de Lopez ACB, Disalvo EA (1999) Effect of water polarized at the carbonyl groups of phosphatidylcholines on the dipole potential of lipid bilayers. Langmuir 15:5179-5182.
33. Viera LI, Alonsoromanowski S, Borovyagin V, Feliz MR, Disalvo EA (1993) Properties of gel phase lipid-trehalose bilayers upon rehydration. Biochim Biophys Acta 1145:157-167. (Pubitemid 23026365)
34. Koynova R, Brankov J, Tenchov B (1997) Modulation of lipid phase behavior by kosmotropic and chaotropic solutes - Experiment and thermodynamic theory. Eur Biophys J Biophy 25:261-274. (Pubitemid 27305782)
35. Sanderson PW, Lis LJ, Quinn PJ, Williams WP (1991) The Hofmeister effect in relation to membrane lipid phase-stability. Biochim Biophys Acta 1067:43-50.
36. Kent B, et al. (2010) Measurement of glucose exclusion from the fully hydrated DOPE inverse hexagonal phase. Soft Matter 6:1197-1202.
37. Takahashi H, Ohmae H, Hatta I (1997) Trehalose-induced destabilization of interdigitated gel phase in dihexadecylphosphatidylcholine. Biophys J 73:3030-3038. (Pubitemid 27525769)
38. Lenne T, Bryant G, Garvey CJ, Kelderling U, Koster KL (2006) Location of sugars in multilamellar membranes at low hydration. Physica B 385-386:862-864. (Pubitemid 44792906)
39. Westh P (2008) Glucose, sucrose and trehalose are partially excluded from the interface of hydrated DMPC bilayers. Phys Chem Chem Phys 10:4110-4112.
40. Lenné T, Garvey CJ, Koster KL, Bryant G (2009) Effects of sugars on lipid bilayers during dehydration - SAXS/WAXS measurements and quantitative model. J Phys Chem B 113:2486-2491.
41. Luzzati V, Husson F (1962) Structure of liquid-crystalline phases of lipid-water systems. J Cell Biol 12:207-219.
42. Hayter JB, Zemb T (1982) Concentration-dependent structure of sodium octanoate micelles. Chem Phys Lett 93:91-94.
43. Hayter JB, Penfold J (1981) An analytic structure factor for macroion solutions. Mol Phys 42:109-118.
44. Kucerka N, et al. (2008) Lipid bilayer structure determined by the simultaneous analysis of neutron and x-ray scattering data. Biophys J 95:2356-2367.
45. Uhrikova D, Kucerka N, Teixeira J, Gordeliy V, Balgavy P (2008) Structural changes in dipalmitoylphosphatidylcholine bilayer promoted by Ca2p ions: A small-angle neutron scattering study. Chem Phys Lipids 155:80-89.
46. McGlashan ML (1979) Chemical Thermodynamics (Academic, London).
47. Peters GH, Hansen FY, Moller MS, Westh P (2009) Effects of fatty acid inclusion in a DMPC bilayer membrane. J Phys Chem B 113:92-102.
48. Golovina EA, Golovin A, Hoekstra FA, Faller R (2010) Water replacement hypothesis in atomic details: Effect of trehalose on the structure of single dehydrated POPC bilayers. Langmuir 26:11118-11126.
49. Pegram LM, Record MT (2009) Using surface tension data to predict differences in surface and bulk concentrations of nonelectrolytes in water. J Phys Chem C 113:2171-2174.
50. Crowe LM, Crowe JH (1991) Solution effects on the thermotropic phase-transition of unilamellar liposomes. Biochim Biophys Acta 1064:267-274.
51. Leontidis E, Aroti A, Belloni L, Dubois M, Zemb T (2007) Effects of monovalent anions of the Hofmeister series on DPPC lipid Bilayers part II: Modeling the perpendicular and lateral equation-of-state. Biophys J 93:1591-1607. (Pubitemid 47403301)
52. Coster HGL, Laver DR (1986) The effect of benzyl alcohol and cholesterol on the acyl chain order and alkane solubility of bimolecular phosphatidylcholine membranes. Biochim Biophys Acta 861:406-412.
53. Pedersen UR, Peters GH, Westh P (2007) Molecular packing in 1-hexanol-DMPC bilayers studied by molecular dynamics simulation. Biophys Chem 125:104-111. (Pubitemid 44709389)
54. Takahashi H, Matsuo A, Hatta I (2000) Effects of chaotropic and kosmotropic solutes on the structure of lipid cubic phase: Monoolein-water systems. Mol Cryst Liq Cryst 347:475-482.
55. Collins KD, Washabaugh MW (1985) The Hofmeister effect and the behavior of water at interfaces. Q Rev Biophys 18:323-422.
56. Bechinger B, Macdonald PM, Seelig J (1988) Deuterium NMR-studies of the interactions of polyhydroxyl compounds and of glycolipids with lipid model membranes. Biochim Biophys Acta 943:381-385.
57. Lindner P (2002) Scattering experiments: Experimental aspects, initial data reduction and absolute calibration. Neutrons, X-Rays and Light: Scattering Methods Applied to Soft Condensed Matter, eds P Linder and Th Zemb (Elsevier, Amsterdam).
58. Pedersen JS, Posselt D, Mortensen K (1990) Analytical treatment of the resolution function for small-angle scattering. J Appl Crystallogr 23:321-333.
59. Hays LM, Crowe JH, Wolkers W, Rudenko S (2001) Factors affecting leakage of trapped solutes from phospholipid vesicles during thermotropic phase transitions. Cryobiology 42:88-102. (Pubitemid 32614080)