Docosahexaenoic acid (DHA) alters the structure and composition of membranous vesicles exfoliated from the surface of a murine leukemia cell line

Biochimica et Biophysica Acta - Biomembranes

Volumn 1371, Issue 2, 1998, Pages 351-362

  Williams, E Eugene ^a   Jenski, Laura J ^a   Stillwell, William ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Docosahexaenoic acid; Lipid microdomain; Membrane exfoliation; Membrane microdomain; Membrane structure; Shed vesicle

Indexed keywords

DOCOSAHEXAENOIC ACID; MEMBRANE LIPID;

ANISOTROPY; ARTICLE; CHEMICAL COMPOSITION; HUMAN; HUMAN CELL; LEUKEMIA CELL; LIPID COMPOSITION; MEMBRANE FUSION; MEMBRANE STRUCTURE; MEMBRANE VESICLE; PRIORITY JOURNAL;

ANIMALS; CELL DIVISION; CELL MEMBRANE; CELL SURVIVAL; DOCOSAHEXAENOIC ACIDS; LEUKEMIA, MYELOID; MEMBRANE LIPIDS; MICE; ORGANELLES; TUMOR CELLS, CULTURED;

MURINAE;

EID: 0032574954     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0005-2736(98)00039-X     Document Type: Article

References (70)

1. Black P.H. Shedding from the cell surface of normal and cancer cells. Adv. Cancer Res. 32:1980;75-199.
2. Beaudoin A.R., Grondin G. Shedding of vesicular material from the cell surface of eukaryotic cells: different cellular phenomena. Biochim. Biophys. Acta. 1071:1991;203-219.
3. Armstrong M.J., Storch J., Dainiak N. Structurally distinct plasma membrane regions give rise to extracellular membrane vesicles in normal and transformed lymphocytes. Biochim. Biophys. Acta. 946:1988;106-112.
4. Tuck D.P., Cerretti D.P., Hand A., Guha A., Sorba S., Dainiak N. Human macrophage colony-stimulating factor is expressed and shed from the cell surface. Blood. 84:1994;2182-2188.
5. Lerner M.P., Lucid S.W., Wen G.J., Norquist R.E. Selected area membrane shedding by tumor cells. Cancer Lett. 20:1983;125-130.
6. 3H -thymidine incorporation, are neutralised by anti TGF-β antibodies J. Submicrosc. Cytol. Pathol. 27:1995;535-541.
7. Dolo V., Adobati E., Canevari S., Picone M.A., Vittorelli M.L. Membrane vesicles shed into the extracellular medium by human breast carcinoma cells carry tumor-associated surface antigens. Clin. Exp. Metastasis. 13:1995;277-286.
8. Van Blitterswijk W.J., De Veer G., Krol J.H., Emmelot P. Comparative lipid analysis of purified plasma membranes and shed extracellular membrane vesicles from normal murine thymocytes and leukemic GRSL cells. Biochim. Biophys. Acta. 688:1982;495-504.
9. Van Blitterswijk W.J., Emmelot P., Hilkmann H.A.M., Hilgers J., Feltkamp C.A. Rigid plasma-membrane-derived vesicles, enriched in tumor-associated surface antigens (MLr), occurring in the ascites fluid of a murine leukemia (GRSL). Int. J. Cancer. 23:1979;62-70.
10. Glaser M. Lipid domains in biological membranes. Curr. Opin. Struct. Biol. 3:1993;475-481.
11. Welti R., Glaser M. Lipid domains in model and biological membranes. Chem. Phys. Lipids. 73:1994;121-137.
12. Thompson T.E., Sankaram M.B., Biltonen R.L. Biological membrane domains: functional significance. Comments Mol. Cell. Biophys. 8:1992;1-15.
13. Edidin M. The variety of cell surface membrane domains. Comments Mol. Cell. Biophys. 8:1992;73-82.
14. Tocanne J.-F., Cézanne L., Lopez A., Piknova B., Schram V., Tournier J.-F., Welby M. Lipid domains and lipid/protein interactions in biological membranes. Chem. Phys. Lipids. 73:1994;139-158.
15. Rodgers W., Glaser M. Characterization of lipid domains in erythrocyte membranes. Proc. Natl. Acad. Sci. U.S.A. 88:1991;1364-1368.
16. Edidin M. Lipid microdomains in cell surface membranes. Curr. Opin. Struct. Biol. 7:1997;528-532.
17. Hendriks T., Klompmakers A.A., Daemen F.J.M., Bonting S.L. Biochemical aspects of the visual process: XXXII. Movement of sodium ions through bilayers composed of retinal and rod outer segment lipids. Biochim. Biophys. Acta. 433:1976;271-281.
18. N. Salem, Jr., H.-Y. Kim, J.A. Yergey, Docosahexaenoic acid: membrane function and metabolism, in: A.P. Simopoulos, R.R. Kifer, R.E. Martin (Eds.), Health Effects of Polyunsaturated Fatty Acids in Seafoods, Academic Press, Orlando, FL, 1986, pp. 263-317.
19. Zerouga M., Stillwell W., Stone J., Powner A., Dumaual A.C., Jenski L.J. Phospholipid class as a determinant in docosahexaenoic acid's effect on tumor cell viability. Anticancer Res. 16:1996;2863-2868.
20. Jenski L.J., Sturdevant L.K., Ehringer W.D., Stillwell W. Omega-3 fatty acid modification of membrane structure and function: I. Dietary manipulation of tumor cell susceptibility to cell- and complement-mediated lysis. Nutr. Cancer. 19:1993;135-146.
21. Pascale A.W., Ehringer W.D., Stillwell W., Sturdevant L.K., Jenski L.J. Omega-3 fatty acid modification of membrane structure and function: II. Alteration by docosahexaenoic acid of tumor cell sensitivity to immune cytolysis. Nutr. Cancer. 19:1993;147-157.
22. Wiegand R.D., Koutz C.A., Stinson A.M., Anderson R.E. Conservation of docosahexaenoic acid in rod outer segments of rat retina during n-3 and n-6 fatty acid deficiency. J. Neurochem. 57:1991;1690-1699.
23. Stinson A.M., Wiegand R.D., Anderson R.E. Recycling of docosahexaenoic acid in rat retinas during n-3 fatty acid deficiency. J. Lipid Res. 32:1991;2009-2017.
24. Stillwell W., Ehringer W.D., Jenski L.J. Docosahexaenoic acid increases permeability of lipid vesicles and tumor cells. Lipids. 28:1993;103-108.
25. Demel R.A., Geurts van Kessel W.S.M., Van Deenen L.L.M. The properties of polyunsaturated lecithins in monolayers and liposomes and the interactions of these lecithins with cholesterol. Biochim. Biophys. Acta. 266:1972;26-40.
26. Pasenkiewicz-Gierula M., Subczynski W.K., Kusumi A. Rotational diffusion of a steroid molecule in phosphatidylcholine-cholesterol membranes: fluid-phase microimmiscibility in unsaturated phosphatidylcholine-cholesterol membranes. Biochemistry. 29:1990;4059-4069.
27. Stillwell W., Wassall S.R., Dumaual A.C., Ehringer W.D., Browning C.W., Jenski L.J. Use of merocyanine (MC540) in quantifying lipid domains and packing in phospholipid vesicles and tumor cells. Biochim. Biophys. Acta. 1146:1993;136-144.
28. Stillwell W., Dallman T., Dumaual A.C., Crump F.T., Jenski L.J. Cholesterol versus α-tocopherol: effect on properties of bilayers made from heteroacid phosphatidylcholines. Biochemistry. 35:1996;13353-13362.
29. Ehringer W., Belcher D., Wassall S.R., Stillwell W. A comparison of the effects of linolenic (18:3 omega3) and docosahexaenoic (22:6 omega3) acids on phospholipid bilayers. Chem. Phys. Lipids. 54:1990;79-88.
30. Cullis P.R., De Kruijff B. Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim. Biophys. Acta. 559:1979;399-420.
31. Lipowsky R. Domain-induced budding of fluid membranes. Biophys. J. 64:1993;1133-1138.
32. Chesebro B., Wehrly K., Chesebro K., Portis J. Characterization of Ia8 antigen, Thy-1.2 antigen, complement receptors, and virus production in a group of murine virus-induced leukemia cell lines. J. Immunol. 117:1976;1267-1274.
33. Jenski L.J., Bowker G.M., Johnson M.A., Ehringer W.D., Fetterhoff T., Stillwell W. Docosahexaenoic acid-induced alteration of THY-1 and CD8 expression on murine splenocytes. Biochim. Biophys. Acta. 1236:1995;39-50.
34. Kaduce T.L., Awad A.B., Fontenelle L.J., Spector A.A. Effect of fatty acid saturation on α-aminoisobutyric acid transport in Ehrlich ascites cells. J. Biol. Chem. 252:1977;6624-6630.
35. Molnar J., Markovic G., Chao H., Molnar Z. Glycoproteins of Ehrlich ascites carcinoma cells: separation of plasma and endoplasmic reticular membrane fragments. Arch. Biochem. Biophys. 134:1969;524-532.
36. Contreras J.A., Castro M., Bocos C., Herrera E., Lasunción M.A. Combination of an enzymatic method and HPLC for the quantitation of cholesterol in cultured cells. J. Lipid Res. 33:1992;931-936.
37. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:1959;911-917.
38. Eder K., Reichlmayr-Lais A.M., Kirchgessner M. Studies on the methanolysis of small amounts of purified phospholipids for gas chromatographic analysis of fatty acid methyl esters. J. Chromatogr. 607:1992;55-67.
39. Williams E.E., Hazel J.R. Membrane fluidity and hemilayer temperature sensitivity in trout hepatocytes during brief in vitro cold exposure. Am. J. Physiol. 266:1994;R773-R780.
40. Houslay M.D., Dipple I., Gordon L.M. Phenobarbital selectively modulates the glucagon-stimulated activity of adenylate cyclase by depressing the lipid phase separation occurring in the outer half of the bilayer of plasma membranes. Biochem. J. 197:1981;675-681.
41. Pendergast F.G., Haugland R.P., Callahan P.J. 1-[4-(Trimethylamino)phenyl]-6-phenylhexa-1,3,5-triene: synthesis, fluorescence properties and use as a fluorescence probe of lipid bilayers. Biochemistry. 20:1981;7333-7338.
42. Kuhry J.-G., Fonteneau P., Duportail G., Maechling C., Laustriat G. TMA-DPH: a suitable fluorescence polarization probe for specific plasma membrane fluidity studies in intact living cells. Cell Biophys. 5:1983;129-140.
43. Kitagawa S., Matsubayashi M., Kotani K., Usui K., Kametani F. Asymmetry of membrane fluidity in the lipid bilayer of blood platelets: fluorescence study with diphenylhexatriene and analogs. J. Mol. Biol. 119:1991;221-227.
44. Shinitzky M., Barenholz Y. Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim. Biophys. Acta. 515:1978;367-394.
45. J.R. Lakowicz, Principles of fluorescence spectroscopy, Plenum, New York, 1983.
46. R.R. Sokal, F.J. Rohlf, Biometry, W.H. Freeman, New York, 1981.
47. L.J. Jenski, L.K. Sturdevant, W.D. Ehringer, W. Pascale, W. Stillwell, Fish oil-rich diets increase tumor cell sensitivity to cell-mediated lysis and alter tumor cell antigen expression, in: R.K. Chandra (Ed.), Nutrition and Immunology, ARTS Biomedical Publishers and Distributors, St John's, Newfoundland, Canada, 1992, pp. 297-307.
48. Burns C.P., Petersen E.S., North J.A., Ingraham L.M. Effect of docosahexaenoic acid on rate of differentiation of HL-60 human leukemia. Cancer Res. 49:1989;3252-3258.
49. Holub B.J., Kuksis A. Metabolism of molecular species of diacylglycerophospholipids. Adv. Lipid Res. 16:1978;1-125.
50. Stillwell W., Ehringer W.D., Dumaual A.C., Wassall S.R. Cholesterol condensation of alpha-linolenic and gamma-linolenic acid-containing phosphatidylcholine monolayers and bilayers. Biochim. Biophys. Acta. 1214:1994;131-136.
51. Van Blitterswijk W.J., Van Hoeven R.P., van der Meer B.W. Lipid structural order parameters (reciprocal of fluidity) in biomembranes derived from steady-state fluorescence polarization measurements. Biochim. Biophys. Acta. 644:1981;323-332.
52. Barz D., Goppelt M., Szamel M., Schirrmacher V., Resch K. Characterization of cellular and extracellular plasma membrane vesicles from a non-metastasizing lymphoma (Eb) and its metastasizing variant (ESb). Biochim. Biophys. Acta. 814:1985;77-84.
53. Araki T. Release of cholesterol-enriched microvesicles from human erythrocytes caused by hypertonic saline at low temperatures. FEBS Lett. 97:1979;237-240.
54. Van Blitterswijk W.J., Emmelot P., Hilkmann H.A.M., Oomen-Meulemans E.L.P., Inbar M. Differences in lipid fluidity among isolated plasma membranes of normal and leukemic lymphocytes and membranes exfoliated from their cell surface. Biochim. Biophys. Acta. 467:1977;309-320.
55. Trams E.G., Lauter C.J., Salem N. Jr., Heine U. Exfoliation of membrane ectoenzymes in the form of micro-vesicles. Biochim. Biophys. Acta. 645:1981;63-70.
56. Zerouga M., Jenski L.J., Stillwell W. Comparison of phosphatidylcholines containing one or two docosahexaenoic acyl chains on properties of phospholipid monolayers and bilayers. Biochim. Biophys. Acta. 1236:1995;266-272.
57. Coleman P.S. Membrane cholesterol and tumor bioenergetics. Ann. N.Y. Acad. Sci. 488:1986;451-467.
58. P.S. Coleman, L. Sepp-Lorenzino, The role of the cholesterol synthesis pathway during tumor cell proliferation, in: M. Esfahani, J.B. Swaney, (Eds.), Advances in Cholesterol Research, The Telford Press, Caldwell, NJ, 1990, pp. 201-270.
59. Taylor D.D., Taylor C.G., Jiang C.-G., Black P.H. Characterization of plasma membrane shedding from murine melanoma cells. Int. J. Cancer. 41:1988;629-645.
60. Taylor D.D., Black P.H. Neoplastic and developmental importance of shed plasma membrane fragments. Am. Zool. 26:1986;511-514.
61. Lee A.G. Lipid phase transitions and phase diagrams: II. Mixtures involving lipids. Biochim. Biophys. Acta. 472:1977;285-344.
62. Nag K., Boland C., Rich N., Keough K.M.W. Epifluorescence microscopic observation of monolayers of dipalmitoylphosphatidylcholine: dependence of domain size on compression rate. Biochim. Biophys. Acta. 1068:1991;157-160.
63. Karnovsky M.J., Kleinfeld A.M., Hoover R.L., Klausner R.D. The concept of lipid domains in membranes. J. Cell Biol. 94:1982;1-6.
64. Sankaram M.B., Thompson T.E. Cholesterol-induced fluid-phase immiscibility in membranes. Proc. Natl. Acad. Sci. U.S.A. 88:1991;8686-8690.
65. A.P. Simopoulous, R.R. Kifer, R.E. Martin (Eds.), Health Effects of Polyunsaturated Fatty Acids in Seafoods, Academic Press, Orlando, FL, USA, 1986.
66. Jenski L.J., Zerouga M., Stillwell W. Omega-3 fatty acid containing liposomes in cancer therapy. Proc. Soc. Exp. Biol. Med. 210:1995;227-233.
67. Schroeder F., Kier A.B., Olson C.D., Dempsey M.E. Correlation of tumor metastasis with sterol carrier protein and plasma membrane sterol levels. Biochem. Biophys. Res. Commun. 124:1984;283-289.
68. Jenski L.J., Sturdevant K.S., Ehringer W.D., Stillwell W. Omega-3 fatty acids increase spontaneous release of cytosolic components from tumor cells. Lipids. 26:1991;353-358.
69. E.A. Dratz, A.J. Deese, The role of docosahexaenoic acid (22:6n-3) in biological membranes: examples from photoreceptors and model membrane bilayers, in: A.P. Simopoulos, R.R. Kifer, R.E. Martin (Eds.), Health Effects of Polyunsaturated Fatty Acids in Seafoods, Academic Press, Orlando, FL, 1986, pp. 319-351.
70. Jenski L.J., Bowker G.M., Scherer J.M., Dumaual A.C., Stone J., Zhang L., Stillwell W. Modulation of membrane structure and antigen expression by docosahexaenoic acid. FASEB J. 8:1994;A2321.