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. 1998 Dec;75(6):2947–2955. doi: 10.1016/S0006-3495(98)77736-7

Effect of sugars on headgroup mobility in freeze-dried dipalmitoylphosphatidylcholine bilayers: solid-state 31P NMR and FTIR studies.

N M Tsvetkova 1, B L Phillips 1, L M Crowe 1, J H Crowe 1, S H Risbud 1
PMCID: PMC1299966  PMID: 9826615

Abstract

The effect of the carbohydrates trehalose, glucose, and hydroxyethyl starch (HES) on the motional properties of the phosphate headgroup of freeze-dried dipalmitoylphosphatidylcholine (DPPC) liposomes was studied by means of 31P NMR, Fourier transform infrared spectroscopy (FTIR), and differential scanning calorimetry (DSC). The results show that trehalose, which is a strong glass former (Tg = 115 degreesC), elevates the onset of the lipid headgroup rotations and preserves some rotational mobility of the phosphate headgroups after cooling from the liquid-crystalline state. Glucose (Tg = 30 degreesC), a very effective depressant of the phase transition temperature of freeze-dried DPPC, markedly elevates the initiation of the temperature of headgroup rotations. On the other hand, the monosaccharide does not preserve the headgroup disordering when cooled from the liquid-crystalline state. These effects are consistent with formation of hydrogen bonds between the OH groups of the sugar and the polar headgroups of DPPC. They show, however, that hydrogen bonding is not sufficient for preservation of the dynamic properties of freeze-dried DPPC. HES, although a very good glass former (Tg > 110 degreesC), does not depress the phase transition temperature and affects only slightly the rotational properties of freeze-dried DPPC. This lack of effect of HES is associated with the absence of direct interactions with the lipid phosphates, as evidenced by the FTIR results. These data show that vitrification of the additive is not sufficient to affect the dynamic properties of dried DPPC.

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Selected References

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  1. Cameron D. G., Mantsch H. H. The phase transition of 1,2-dipalmitoyl-sn-glycero-3-phosphocholine as seen by Fourier transform infrared difference spectroscopy. Biochem Biophys Res Commun. 1978 Aug 14;83(3):886–892. doi: 10.1016/0006-291x(78)91478-x. [DOI] [PubMed] [Google Scholar]
  2. Casal H. L., Mantsch H. H. Polymorphic phase behaviour of phospholipid membranes studied by infrared spectroscopy. Biochim Biophys Acta. 1984 Dec 4;779(4):381–401. doi: 10.1016/0304-4157(84)90017-0. [DOI] [PubMed] [Google Scholar]
  3. Crowe J. H., Crowe L. M., Carpenter J. F., Rudolph A. S., Wistrom C. A., Spargo B. J., Anchordoguy T. J. Interactions of sugars with membranes. Biochim Biophys Acta. 1988 Jun 9;947(2):367–384. doi: 10.1016/0304-4157(88)90015-9. [DOI] [PubMed] [Google Scholar]
  4. Crowe J. H., Crowe L. M., Chapman D. Infrared spectroscopic studies on interactions of water and carbohydrates with a biological membrane. Arch Biochem Biophys. 1984 Jul;232(1):400–407. doi: 10.1016/0003-9861(84)90555-1. [DOI] [PubMed] [Google Scholar]
  5. Crowe J. H., Crowe L. M., Chapman D. Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science. 1984 Feb 17;223(4637):701–703. doi: 10.1126/science.223.4637.701. [DOI] [PubMed] [Google Scholar]
  6. Crowe J. H., Crowe L. M., Jackson S. A. Preservation of structural and functional activity in lyophilized sarcoplasmic reticulum. Arch Biochem Biophys. 1983 Feb 1;220(2):477–484. doi: 10.1016/0003-9861(83)90438-1. [DOI] [PubMed] [Google Scholar]
  7. Crowe J. H., Hoekstra F. A., Crowe L. M., Anchordoguy T. J., Drobnis E. Lipid phase transitions measured in intact cells with Fourier transform infrared spectroscopy. Cryobiology. 1989 Feb;26(1):76–84. doi: 10.1016/0011-2240(89)90035-7. [DOI] [PubMed] [Google Scholar]
  8. Crowe J. H., Hoekstra F. A., Nguyen K. H., Crowe L. M. Is vitrification involved in depression of the phase transition temperature in dry phospholipids? Biochim Biophys Acta. 1996 Apr 26;1280(2):187–196. doi: 10.1016/0005-2736(95)00287-1. [DOI] [PubMed] [Google Scholar]
  9. Crowe J. H., Oliver A. E., Hoekstra F. A., Crowe L. M. Stabilization of dry membranes by mixtures of hydroxyethyl starch and glucose: the role of vitrification. Cryobiology. 1997 Aug;35(1):20–30. doi: 10.1006/cryo.1997.2020. [DOI] [PubMed] [Google Scholar]
  10. Crowe L. M., Crowe J. H., Rudolph A., Womersley C., Appel L. Preservation of freeze-dried liposomes by trehalose. Arch Biochem Biophys. 1985 Oct;242(1):240–247. doi: 10.1016/0003-9861(85)90498-9. [DOI] [PubMed] [Google Scholar]
  11. Crowe L. M., Crowe J. H. Trehalose and dry dipalmitoylphosphatidylcholine revisited. Biochim Biophys Acta. 1988 Dec 22;946(2):193–201. doi: 10.1016/0005-2736(88)90392-6. [DOI] [PubMed] [Google Scholar]
  12. Crowe L. M., Reid D. S., Crowe J. H. Is trehalose special for preserving dry biomaterials? Biophys J. 1996 Oct;71(4):2087–2093. doi: 10.1016/S0006-3495(96)79407-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Griffin R. G. Letter: Observation of the effect of water on the 31P nuclear magnetic resonance spectra of dipalmitoyllecithin. J Am Chem Soc. 1976 Feb 4;98(3):851–853. doi: 10.1021/ja00419a044. [DOI] [PubMed] [Google Scholar]
  14. Griffin R. G., Powers L., Pershan P. S. Head-group conformation in phospholipids: a phosphorus-31 nuclear magnetic resonance study of oriented monodomain dipalmitoylphosphatidylcholine bilayers. Biochemistry. 1978 Jul 11;17(14):2718–2722. doi: 10.1021/bi00607a004. [DOI] [PubMed] [Google Scholar]
  15. Herzfeld J., Griffin R. G., Haberkorn R. A. Phosphorus-31 chemical-shift tensors in barium diethyl phosphate and urea-phosphoric acid: model compounds for phospholipid head-group studies. Biochemistry. 1978 Jul 11;17(14):2711–2718. doi: 10.1021/bi00607a003. [DOI] [PubMed] [Google Scholar]
  16. Koster K. L., Webb M. S., Bryant G., Lynch D. V. Interactions between soluble sugars and POPC (1-palmitoyl-2-oleoylphosphatidylcholine) during dehydration: vitrification of sugars alters the phase behavior of the phospholipid. Biochim Biophys Acta. 1994 Jul 13;1193(1):143–150. doi: 10.1016/0005-2736(94)90343-3. [DOI] [PubMed] [Google Scholar]
  17. Lee C. W., Das Gupta S. K., Mattai J., Shipley G. G., Abdel-Mageed O. H., Makriyannis A., Griffin R. G. Characterization of the L lambda phase in trehalose-stabilized dry membranes by solid-state NMR and X-ray diffraction. Biochemistry. 1989 Jun 13;28(12):5000–5009. doi: 10.1021/bi00438a015. [DOI] [PubMed] [Google Scholar]
  18. Lee C. W., Waugh J. S., Griffin R. G. Solid-state NMR study of trehalose/1,2-dipalmitoyl-sn-phosphatidylcholine interactions. Biochemistry. 1986 Jul 1;25(13):3737–3742. doi: 10.1021/bi00361a001. [DOI] [PubMed] [Google Scholar]
  19. Leslie S. B., Teter S. A., Crowe L. M., Crowe J. H. Trehalose lowers membrane phase transitions in dry yeast cells. Biochim Biophys Acta. 1994 Jun 1;1192(1):7–13. doi: 10.1016/0005-2736(94)90136-8. [DOI] [PubMed] [Google Scholar]
  20. Quinn P. J., Koynova R. D., Lis L. J., Tenchov B. G. Lamellar gel-lamellar liquid crystal phase transition of dipalmitoylphosphatidylcholine multilayers freeze-dried from aqueous trehalose solutions. A real-time X-ray diffraction study. Biochim Biophys Acta. 1988 Jul 21;942(2):315–323. doi: 10.1016/0005-2736(88)90033-8. [DOI] [PubMed] [Google Scholar]
  21. Slade L., Levine H. Glass transitions and water-food structure interactions. Adv Food Nutr Res. 1995;38:103–269. doi: 10.1016/s1043-4526(08)60084-4. [DOI] [PubMed] [Google Scholar]
  22. Tsvetkov T. D., Tsonev L. I., Tsvetkova N. M., Koynova R. D., Tenchov B. G. Effect of trehalose on the phase properties of hydrated and lyophilized dipalmitoylphosphatidylcholine multilayers. Cryobiology. 1989 Apr;26(2):162–169. doi: 10.1016/0011-2240(89)90047-3. [DOI] [PubMed] [Google Scholar]
  23. Tsvetkova N., Tenchov B., Tsonev L., Tsvetkov T. Dependence of trehalose protective action on the initial phase state of dipalmitoylphosphatidylcholine bilayers. Cryobiology. 1988 Jun;25(3):256–263. doi: 10.1016/0011-2240(88)90033-8. [DOI] [PubMed] [Google Scholar]

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