Properties of fiber cell plasma membranes isolated from the cortex and nucleus of the porcine eye lens

Experimental Eye Research

Volumn 97, Issue 1, 2012, Pages 117-129

  Mainali, Laxman ^a   Raguz, Marija ^a,b   O'Brien, William J ^a   Subczynski, Witold K ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF SPLIT   (Croatia)

Author keywords

Cholesterol; EPR; Fluidity; Hydrophobic barrier; Membrane domains; Oxygen permeation; Spin labeling

Indexed keywords

LIPID; MEMBRANE PROTEIN;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CELL MEMBRANE; CELL MEMBRANE FLUIDITY; CELL NUCLEUS MEMBRANE; FIBER; HYDROPHOBICITY; LENS; LIPID MEMBRANE; NONHUMAN; OXYGEN TRANSPORT; PRIORITY JOURNAL; SWINE;

ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CHOLESTEROL; ELECTRON SPIN RESONANCE SPECTROSCOPY; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LENS CORTEX, CRYSTALLINE; LENS NUCLEUS, CRYSTALLINE; LIPID BILAYERS; MEMBRANE FLUIDITY; OXYGEN; PHOSPHOLIPIDS; SPIN LABELS; SWINE;

EID: 84859494957     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2012.01.012     Document Type: Article

References (89)

1. Agre P. Nobel Lecture. Aquaporin water channels. Biosci. Rep. 2004, 24:127-163.
2. Altenbach C., Greenhalgh D.A., Khorana H.G., Hubbell W.L. A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: application to spin-labeled mutants of bacteriorhodopsin. Proc. Natl. Acad. Sci. U S A 1994, 91:1667-1671.
3. Ashikawa I., Yin J.J., Subczynski W.K., Kouyama T., Hyde J.S., Kusumi A. Molecular organization and dynamics in bacteriorhodopsin-rich reconstituted membranes: discrimination of lipid environments by the oxygen transport parameter using a pulse ESR spin-labeling technique. Biochemistry 1994, 33:4947-4952.
4. Bassnett S., Shi Y., Vrensen G.F. Biological glass: structural determinants of eye lens transparency. Philos. Trans. R Soc. Lond B. Biol. Sci. 2011, 366:1250-1264.
5. Beebe D.C. The lens. Physiology of the Eye 2003, 117-158. Mosby-Year Book, St Louis. P.L. Kaufman (Ed.).
6. Bloemendal H., Zweers A., Vermorken F., Dunia I., Benedetti E.L. The plasma membranes of eye lens fibres. Biochemical and structural characterization. Cell Differ. 1972, 1:91-106.
7. Borchman D., Cenedella R.J., Lamba O.P. Role of cholesterol in the structural order of lens membrane lipids. Exp. Eye Res. 1996, 62:191-197.
8. Borchman D., Delamere N.A., McCauley L.A., Paterson C.A. Studies on the distribution of cholesterol, phospholipid, and protein in the human and bovine lens. Lens Eye Toxic Res. 1989, 6:703-724.
9. Borchman D., Yappert M.C. Lipids and the ocular lens. J. Lipid Res. 2010, 51:2473-2488.
10. Borchman D., Yappert M.C., Afzal M. Lens lipids and maximum lifespan. Exp. Eye Res. 2004, 79:761-768.
11. Boyle D.L., Takemoto L. EM immunolocalization of alpha-crystallins: association with the plasma membrane from normal and cataractous human lenses. Curr. Eye Res. 1996, 15:577-582.
12. Broekhuyse R.M., Kuhlmann E.D. Lens membranes 1. Composition of urea-treated plasma membranes from calf lens. Exp. Eye Res. 1974, 19:297-302.
13. Broekhuyse R.M., Kuhlmann E.D. Lens membranes. IV. Preparative isolation and characterization of membranes and various membrane proteins from calf lens. Exp. Eye Res. 1978, 26:305-320.
14. Brown D.A., London E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 1998, 14:111-136.
15. Buzhynskyy N., Hite R.K., Walz T., Scheuring S. The supramolecular architecture of junctional microdomains in native lens membranes. EMBO Rep. 2007, 8:51-55.
16. Cenedella R.J., Fleschner C.R. Selective association of crystallins with lens 'native' membrane during dynamic cataractogenesis. Curr. Eye Res. 1992, 11:801-815.
17. Cenedella R.J., Sexton P.S., Brako L., Lo W.K., Jacob R.F. Status of caveolin-1 in various membrane domains of the bovine lens. Exp. Eye Res. 2007, 85:473-481.
18. Chandrasekher G., Cenedella R.J. Protein associated with human lens 'native' membrane during aging and cataract formation. Exp. Eye Res. 1995, 60:707-717.
19. Chung J., Berthoud V.M., Novak L., Zoltoski R., Heilbrunn B., Minogue P.J., Liu X., Ebihara L., Kuszak J., Beyer E.C. Transgenic overexpression of connexin50 induces cataracts. Exp. Eye Res. 2007, 84:513-528.
20. Cobb B.A., Petrash J.M. alpha-Crystallin chaperone-like activity and membrane binding in age-related cataracts. Biochemistry 2002, 41:483-490.
21. Costello M.J., McIntosh T.J., Robertson J.D. Distribution of gap junctions and square array junctions in the mammalian lens. Invest. Ophthalmol. Vis. Sci. 1989, 30:975-989.
22. de Almeida R.F., Fedorov A., Prieto M. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys. J. 2003, 85:2406-2416.
23. Deeley J.M., Mitchell T.W., Wei X., Korth J., Nealon J.R., Blanksby S.J., Truscott R.J. Human lens lipids differ markedly from those of commonly used experimental animals. Biochim. Biophys. Acta 2008, 1781:288-298.
24. Dunia I., Cibert C., Gong X., Xia C.H., Recouvreur M., Levy E., Kumar N., Bloemendal H., Benedetti E.L. Structural and immunocytochemical alterations in eye lens fiber cells from Cx46 and Cx50 knockout mice. Eur. J. Cell Biol. 2006, 85:729-752.
25. Edidin M. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 2003, 32:257-283.
26. Epand R.M. Role of membrane lipids in modulating the activity of membrane-bound enzymes. The Structure of Biological Membrane 2005, 499-509. CRC Press, Boca Raton. P.L. Yeagle (Ed.).
27. Estrada R., Yappert M.C. Regional phospholipid analysis of porcine lens membranes by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J. Mass Spectrom. 2004, 39:1531-1540.
28. Fleschner C.R., Cenedella R.J. Lipid composition of lens plasma membrane fractions enriched in fiber junctions. J. Lipid Res. 1991, 32:45-53.
29. Folch J., Lees M., Sloane Stanley G.H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 1957, 226:497-509.
30. Ge M., Freed J.H. An electron spin resonance study of interactions between gramicidin A' and phosphatidylcholine bilayers. Biophys. J. 1993, 65:2106-2123.
31. Gooden M.M., Takemoto L.J., Rintoul D.A. Evidence for reduced lipid order in plasma membranes from cataractous human lenses. Curr. Eye Res. 1982, 2:367-375.
32. Grami V., Marrero Y., Huang L., Tang D., Yappert M.C., Borchman D. alpha-Crystallin binding in vitro to lipids from clear human lenses. Exp. Eye Res. 2005, 81:138-146.
33. Heerklotz H. Triton promotes domain formation in lipid raft mixtures. Biophys. J. 2002, 83:2693-2701.
34. Jacob R.F., Cenedella R.J., Mason R.P. Direct evidence for immiscible cholesterol domains in human ocular lens fiber cell plasma membranes. J. Biol. Chem. 1999, 274:31613-31618.
35. Jacob R.F., Cenedella R.J., Mason R.P. Evidence for distinct cholesterol domains in fiber cell membranes from cataractous human lenses. J. Biol. Chem. 2001, 276:13573-13578.
36. Jost P.C., Griffith O.H., Capaldi R.A., Vanderkooi G. Evidence for boundary lipid in membranes. Proc. Natl. Acad. Sci. U S A 1973, 70:480-484.
37. Kawasaki K., Yin J.-J., Subczynski W.K., Hyde J.S., Kusumi A. Pulse EPR detection of lipid exchange between protein rich raft and bulk domains in the membrane: methodology development and its application to studies of influenza viral membrane. Biophys. J. 2001, 80:738-748.
38. Kusumi A., Subczynski W.K., Hyde J.S. Oxygen transport parameter in membranes as deduced by saturation recovery measurements of spin-lattice relaxation times of spin labels. Proc. Natl. Acad. Sci. U S A 1982, 79:1854-1858.
39. Kusumi A., Subczynski W.K., Pasenkiewicz-Gierula M., Hyde J.S., Merkle H. Spin-label studies on phosphatidylcholine-cholesterol membranes: effects of alkyl chain length and unsaturation in the fluid phase. Biochim. Biophys. Acta 1986, 854:307-317.
40. Kuszak J.R., Costello M.J. The structure of the vertebrate lens. Development of the Ocular Lens 2004, 71-118. Cambridge University Press, Cambridge, UK. F.J. Lovicu, M.L. Robinson (Eds.).
41. Kuszak J.R., Zoltoski R.K., Tiedemann C.E. Development of lens sutures. Int. J. Dev. Biol. 2004, 48:889-902.
42. Li L.K., So L. Age dependent lipid and protein changes in individual bovine lenses. Curr. Eye Res. 1987, 6:599-605.
43. Li L.K., So L., Spector A. Membrane cholesterol and phospholipid in consecutive concentric sections of human lenses. J. Lipid Res. 1985, 26:600-609.
44. Li L.K., So L., Spector A. Age-dependent changes in the distribution and concentration of human lens cholesterol and phospholipids. Biochim. Biophys. Acta 1987, 917:112-120.
45. Lichtenberg D., Goni F.M., Heerklotz H. Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem. Sci. 2005, 30:430-436.
46. Ligeza A., Tikhonov A.N., Hyde J.S., Subczynski W.K. Oxygen permeability of thylakoid membranes: electron paramagnetic resonance spin labeling study. Biochim. Biophys. Acta 1998, 1365:453-463.
47. Lim J., Lam Y.C., Kistler J., Donaldson P.J. Molecular characterization of the cystine/glutamate exchanger and the excitatory amino acid transporters in the rat lens. Invest. Ophthalmol. Vis. Sci. 2005, 46:2869-2877.
48. Mainali L., Feix J.B., Hyde J.S., Subczynski W.K. Membrane fluidity profiles as deduced by saturation-recovery EPR measurements of spin-lattice relaxation times of spin labels. J. Magn. Reson. 2011, 212:418-425.
49. Mainali L., Raguz M., Camenisch T.G., Hyde J.S., Subczynski W.K. Spin-label saturation-recovery EPR at W-band: applications to eye lens lipid membranes. J. Magn. Reson. 2011, 212:86-94.
50. Mainali L., Raguz M., Subczynski W.K. Phase-separation and domain-formation in cholesterol-sphingomyelin mixture: pulse EPR oxygen probing. Biophys. J. 2011, 101:837-846.
51. Mainali L., Raguz M., Subczynski W.K. Phases and domains in sphingomyelin-cholesterol membranes: structure and properties using EPR spin-labeling methods. Eur. Biophys. J. 2012, 41:147-159.
52. Marsh D. Electron spin resonance in membrane research: protein-lipid interactions. Methods 2008, 46:83-96.
53. Marsh D. Electron spin resonance in membrane research: protein-lipid interactions from challenging beginnings to state of the art. Eur. Biophys. J. 2010, 39:513-525.
54. Mason R.P., Tulenko T.N., Jacob R.F. Direct evidence for cholesterol crystalline domains in biological membranes: role in human pathobiology. Biochim. Biophys. Acta 2003, 1610:198-207.
55. Munro S. Lipid rafts: elusive or illusive?. Cell 2003, 115:377-388.
56. Plesnar E., Subczynski W.K., Pasenkiewicz-Gierula M. Saturation with cholesterol increases vertical order and smoothes the surface of the phosphatidylcholine bilayer: a molecular simulation study. Biochim. Biophys. Acta 2012, 1818:520-529.
57. Raguz M., Mainali L., Widomska J., Subczynski W.K. The immiscible cholesterol bilayer domain exists as an integral part of phospholipid bilayer membranes. Biochim. Biophys. Acta 2011, 1808:1072-1080.
58. Raguz M., Mainali L., Widomska J., Subczynski W.K. Using spin-label electron paramagnetic resonance (EPR) to discriminate and characterize the cholesterol bilayer domain. Chem. Phys. Lipids 2011, 164:819-829.
59. Raguz M., Widomska J., Dillon J., Gaillard E.R., Subczynski W.K. Characterization of lipid domains in reconstituted porcine lens membranes using EPR spin-labeling approaches. Biochim. Biophys. Acta 2008, 1778:1079-1090.
60. Raguz M., Widomska J., Dillon J., Gaillard E.R., Subczynski W.K. Physical properties of the lipid bilayer membrane made of cortical and nuclear bovine lens lipids: EPR spin-labeling studies. Biochim. Biophys. Acta 2009, 1788:2380-2388.
61. Rujoi M., Jin J., Borchman D., Tang D., Yappert M.C. Isolation and lipid characterization of cholesterol-enriched fractions in cortical and nuclear human lens fibers. Invest. Ophthalmol. Vis. Sci. 2003, 44:1634-1642.
62. Ryba N.J., Horvath L.I., Watts A., Marsh D. Molecular exchange at the lipid-rhodopsin interface: spin-label electron spin resonance studies of rhodopsin-dimyristoylphosphatidylcholine recombinants. Biochemistry 1987, 26:3234-3240.
63. Sato H., Borchman D., Ozaki Y., Lamba O.P., Byrdwell W.C., Yappert M.C., Paterson C.A. Lipid-protein interactions in human and bovine lens membranes by Fourier transform Raman and infrared spectroscopies. Exp. Eye Res. 1996, 62:47-53.
64. Simons K., Ikonen E. Functional rafts in cell membranes. Nature 1997, 387:569-572.
65. Simons K., Vaz W.L. Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 2004, 33:269-295.
66. Subczynski W.K., Felix C.C., Klug C.S., Hyde J.S. Concentration by centrifugation for gas exchange EPR oximetry measurements with loop-gap resonators. J. Magn. Reson. 2005, 176:244-248.
67. Subczynski W.K., Hopwood L.E., Hyde J.S. Is the mammalian cell plasma membrane a barrier to oxygen transport?. J. Gen. Physiol. 1992, 100:69-87.
68. Subczynski W.K., Hyde J.S., Kusumi A. Oxygen permeability of phosphatidylcholine-cholesterol membranes. Proc. Natl. Acad. Sci. U S A 1989, 86:4474-4478.
69. Subczynski W.K., Lewis R.N., McElhaney R.N., Hodges R.S., Hyde J.S., Kusumi A. Molecular organization and dynamics of 1-palmitoyl-2-oleoylphosphatidylcholine bilayers containing a transmembrane alpha-helical peptide. Biochemistry 1998, 37:3156-3164.
70. Subczynski W.K., Pasenkiewicz-Gierula M., McElhaney R.N., Hyde J.S., Kusumi A. Molecular dynamics of 1-palmitoyl-2-oleoylphosphatidylcholine membranes containing transmembrane alpha-helical peptides with alternating leucine and alanine residues. Biochemistry 2003, 42:3939-3948.
71. Subczynski W.K., Raguz M., Widomska J., Mainali L., Konovalov A. Functions of cholesterol and the cholesterol bilayer domain specific to the fiber-cell plasma membrane of the eye lens. Rev. Article, J. Membr. Biol. 2012, 10.1007/s00232-011-9412-4.
72. Subczynski W.K., Renk G.E., Crouch R.K., Hyde J.S., Kusumi A. Oxygen diffusion-concentration product in rhodopsin as observed by a pulse ESR spin labeling method. Biophys. J. 1992, 63:573-577.
73. Subczynski W.K., Widomska J., Wisniewska A., Kusumi A. Saturation-recovery electron paramagnetic resonance discrimination by oxygen transport (DOT) method for characterizing membrane domains. Methods in Molecular Biology, Lipid Rafts 2007, 143-157. Humana Press, Totowa. T.J. McIntosh (Ed.).
74. Subczynski W.K., Wisniewska A., Yin J.-J., Hyde J.S., Kusumi A. Hydrophobic barriers of lipid bilayer membranes formed by reduction of water penetration by alkyl chain unsaturation and cholesterol. Biochemistry 1994, 33:7670-7681.
75. Tang D., Borchman D. Temperature induced structural changes of beta-crystallin and sphingomyelin binding. Exp. Eye Res. 1998, 67:113-118.
76. Tang D., Borchman D., Yappert M.C. Alpha-crystallin/lens lipid interactions using resonance energy transfer. Ophthalmic Res. 1999, 31:452-462.
77. Tenbroek E., Arneson M., Jarvis L., Louis C. The distribution of the fiber cell intrinsic membrane proteins MP20 and connexin46 in the bovine lens. J. Cell Sci. 1992, 103(Pt 1):245-257.
78. Tong J., Briggs M.M., Mlaver D., Vidal A., McIntosh T.J. Sorting of lens aquaporins and connexins into raft and nonraft bilayers: role of protein homo-oligomerization. Biophys. J. 2009, 97:2493-2502.
79. Tulenko T.N., Chen M., Mason P.E., Mason R.P. Physical effects of cholesterol on arterial smooth muscle membranes: evidence of immiscible cholesterol domains and alterations in bilayer width during atherogenesis. J. Lipid Res. 1998, 39:947-956.
80. Veatch S.L., Keller S.L. A closer look at the canonical 'Raft Mixture' in model membrane studies. Biophys. J. 2003, 84:725-726.
81. White T.W., Bruzzone R. Intercellular communication in the eye: clarifying the need for connexin diversity. Brain Res. Brain Res. Rev. 2000, 32:130-137.
82. White T.W., Goodenough D.A., Paul D.L. Targeted ablation of connexin50 in mice results in microphthalmia and zonular pulverulent cataracts. J. Cell Biol. 1998, 143:815-825.
83. Widomska J., Raguz M., Dillon J., Gaillard E.R., Subczynski W.K. Physical properties of the lipid bilayer membrane made of calf lens lipids: EPR spin labeling studies. Biochim. Biophys. Acta 2007, 1768:1454-1465.
84. Widomska J., Raguz M., Subczynski W.K. Oxygen permeability of the lipid bilayer membrane made of calf lens lipids. Biochim. Biophys. Acta 2007, 1768:2635-2645.
85. Wisniewska A., Subczynski W.K. Spin-label study on gramicidin-phosphatidylcholine interface: fluidity, hydrophobicity and ion penetration. Curr. Top. Biophys. 1996, 20:86-92.
86. Yappert M.C., Rujoi M., Borchman D., Vorobyov I., Estrada R. Glycero- versus sphingo-phospholipids: correlations with human and non-human mammalian lens growth. Exp. Eye Res. 2003, 76:725-734.
87. Yin J.J., Subczynski W.K. Effects of lutein and cholesterol on alkyl chain bending in lipid bilayers: a pulse electron spin resonance spin labeling study. Biophys. J. 1996, 71:832-839.
88. Zampighi G.A., Eskandari S., Hall J.E., Zampighi L., Kreman M. Micro-domains of AQP0 in lens equatorial fibers. Exp. Eye Res. 2002, 75:505-519.
89. Zhang Z., Zeng J., Yin H., Tang D., Borchman D., Paterson C.A. Membrane lipid alpha-crystallin interaction and membrane Ca2+ -ATPase activities. Curr. Eye Res. 1999, 18:56-61.