Home LiteratureArticle Details
PMID: 1700061 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Properties of channels reconstituted from the major intrinsic protein of lens fiber membranes.

The Journal of general physiology ·Vol. 96 ·No. 3 ·1990-09-00 ·Pages 631-64

Ehring GR, Zampighi G, Horwitz J, Bok D, Hall JE

Abstract

Detergent-solubilized plasma membrane protein of either adult bovine or calf lens and high-performance liquid chromatography-purified major intrinsic protein (MIP) of the lens were reconstituted into unilamellar vesicles and planar lipid bilayers. Freeze-fracture studies showed that the density of intramembrane particles in the vesicles was proportional to the protein/lipid ratio. At high ratios, these particles crystallized into tetragonal arrays as does MIP in lens fibers. Channels induced by either purified MIP or detergent-solubilized protein had essentially identical properties. The conductance of multichannel membranes was maximal near 0 mV and decreased to 0.49 +/- 0.08 of the maximum value at voltages greater than 80 mV. The dependence of the conductance on voltage was well fit by a two-state Boltzmann distribution. Voltage steps greater than 30 mV elicited an ohmic current step followed by a slow (seconds) biexponential decrease. The amplitudes and time constants depended on the magnitude but not the sign of the voltage. Steps from 100 mV to voltages less than 30 mV caused the channels to open exponentially with a millisecond time constant. Analysis of latency to first closure after a voltage step gave nearly the same time constants as multichannel kinetics. Single-channel conductance is proportional to salt concentration from 0.1 to 1.0 M in KCl. In 0.1M KCl, the channel had two preferred conductance states with amplitudes of 380 and 160 pS, as well as three additional substates. Multi- and single-channel data suggest that the channel has two kinetically important open states. The channel is slightly anion selective. The properties of the channel do not vary appreciably from pH 7.4 to 5.8 or from pCa 7 to 2. We propose that a channel with these properties could contribute to maintenance of lens transparency and fluid balance.

MeSH Terms
Animals Aquaporins Cattle Chromatography, High Pressure Liquid Electric Conductivity Eye Proteins/chemistry,isolation & purification,metabolism Freeze Fracturing Hydrogen-Ion Concentration In Vitro Techniques Ion Channels/chemistry,metabolism Kinetics Membrane Glycoproteins Molecular Structure Potassium Chloride
Chemicals
Aquaporins Eye Proteins Ion Channels Membrane Glycoproteins aquaporin 0 Potassium Chloride
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Ehring G R
Department of Physiology and Biophysics, University of California, Irvine, 92717.
Zampighi G
Horwitz J
Bok D
Hall J E
References (68)
68 references, click to expand
  1. Simulation of electrical interaction of cardiac cells.
    Biophys J. 1970 Nov;10(11):1057-75 PMID: 5471697
  2. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  3. Mechanisms for the regulation of cell volume with particular reference to the lens.
    Exp Eye Res. 1969 Oct;8(4):421-8 PMID: 5358238
  4. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  5. A fluorescence-quenching assay for measuring permeability of reconstituted lens MIP26.
    Invest Ophthalmol Vis Sci. 1989 May;30(5):961-6 PMID: 2722450
  6. Is the C-terminal arm of lens gap junction channel protein the channel gate?
    Biochem Biophys Res Commun. 1985 Dec 17;133(2):688-95 PMID: 2417598
  7. Reconstitution of MIP26 from single human lenses into artificial membranes. I. Differences in pH sensitivity of cataractous vs. normal human lens fiber cell proteins.
    Curr Eye Res. 1985 Nov;4(11):1107-15 PMID: 3907982
  8. Purified lens junctional protein forms channels in planar lipid films.
    Proc Natl Acad Sci U S A. 1985 Dec;82(24):8468-72 PMID: 2417221
  9. Functional reconstitution of lens gap junction proteins into proteoliposomes.
    J Membr Biol. 1985;85(1):87-92 PMID: 2991529
  10. Major intrinsic polypeptide (MIP26K) from lens membrane: reconstitution into vesicles and inhibition of channel forming activity by peptide antiserum.
    Biochem Biophys Res Commun. 1985 Apr 30;128(2):993-9 PMID: 2581574
  11. Membrane specializations in mammalian lens fiber cells: distribution of square arrays.
    Curr Eye Res. 1985 Nov;4(11):1183-201 PMID: 4075818
  12. Structural comparison of native and deoxycholate-treated purple membrane.
    Biophys J. 1985 Nov;48(5):775-80 PMID: 4074837
  13. Steady state voltages in the frog lens.
    Curr Eye Res. 1985 Apr;4(4):421-30 PMID: 4017633
  14. Lens cell-to-cell channel protein: II. Conformational change in the presence of calmodulin.
    J Membr Biol. 1985;83(3):227-33 PMID: 3999122
  15. On gap junction structure.
    J Cell Biol. 1980 Jul;86(1):190-8 PMID: 6158517
  16. Comparative analysis of the major polypeptides from liver gap junctions and lens fiber junctions.
    J Cell Biol. 1982 Jan;92(1):53-9 PMID: 6173389
  17. Alamethicin. A rich model for channel behavior.
    Biophys J. 1984 Jan;45(1):233-47 PMID: 6324906
  18. Differences between liver gap junction protein and lens MIP 26 from rat: implications for tissue specificity of gap junctions.
    Cell. 1983 Mar;32(3):967-78 PMID: 6299583
  19. Equilibrium properties of a voltage-dependent junctional conductance.
    J Gen Physiol. 1981 Jan;77(1):77-93 PMID: 6259274
  20. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A.
    Anal Biochem. 1981 Apr;112(2):195-203 PMID: 6266278
  21. Immunocytochemical localization of the main intrinsic polypeptide (MIP) in ultrathin frozen sections of rat lens.
    J Cell Biol. 1983 Nov;97(5 Pt 1):1491-9 PMID: 6355119
  22. The electrical coupling of epithelium and fibers in the frog lens.
    Exp Eye Res. 1983 Mar;36(3):317-26 PMID: 6601018
  23. Preparation, characterization, and localization of antisera against bovine MP26, an integral protein from lens fiber plasma membrane.
    J Cell Biol. 1983 Mar;96(3):625-32 PMID: 6339520
  24. Dye transfer between cells of the embryonic chick lens becomes less sensitive to CO2 treatment with development.
    J Cell Biol. 1982 Mar;92(3):694-705 PMID: 6806303
  25. Gap junction crystallization in lens fibers after an increase in cell calcium.
    Invest Ophthalmol Vis Sci. 1981 Aug;21(2):291-9 PMID: 6788727
  26. Immunocytochemical localization of the lens main intrinsic polypeptide (MIP26) in communicating junctions.
    J Cell Biol. 1982 Jan;92(1):213-20 PMID: 7035467
  27. Orthorhombic two-dimensional crystal form of purple membrane.
    Proc Natl Acad Sci U S A. 1980 Jan;77(1):338-42 PMID: 6928627
  28. The structure of junctions between lens fiber cells.
    Biosci Rep. 1982 May;2(5):333-41 PMID: 7093443
  29. On the structural organization of isolated bovine lens fiber junctions.
    J Cell Biol. 1982 Apr;93(1):175-89 PMID: 7068755
  30. The lens as a nonuniform spherical syncytium.
    Biophys J. 1981 Apr;34(1):61-83 PMID: 7213932
  31. Gap junction dynamics: reversible effects of hydrogen ions.
    J Cell Biol. 1980 Dec;87(3 Pt 1):719-27 PMID: 7462322
  32. Gap junction dynamics: reversible effects of divalent cations.
    J Cell Biol. 1980 Dec;87(3 Pt 1):708-18 PMID: 7462321
  33. Structure of cytochrome c oxidase in deoxycholate-drived two-dimensional crystals.
    J Mol Biol. 1979 Oct 25;134(2):305-27 PMID: 231668
  34. The electrophysiology of the crystalline lens.
    Curr Top Eye Res. 1979;1:37-90 PMID: 233657
  35. Freeze-fracture replica of the primate lens fibers.
    Albrecht Von Graefes Arch Klin Exp Ophthalmol. 1978 Dec 8;209(1):51-8 PMID: 105647
  36. Electrical properties of structural components of the crystalline lens.
    Biophys J. 1979 Jan;25(1):181-201 PMID: 262384
  37. Heat induced aggregation of the sodium dodecyl sulfate-solubilized main intrinsic polypeptide isolated from bovine lens plasma membrane.
    Biochem Biophys Res Commun. 1978 Sep 14;84(1):158-65 PMID: 728124
  38. Calcium effects on gap junction structure and cell coupling.
    Nature. 1978 Feb 16;271(5646):669-71 PMID: 625335
  39. A portrait of plasma membrane specializations in eye lens epithelium and fibers.
    Biochim Biophys Acta. 1976 Dec 14;457(3-4):353-84 PMID: 793636
  40. Interlocking patterns on primate lens fibers.
    Invest Ophthalmol. 1972 Oct;11(10):809-15 PMID: 4627255
  41. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties.
    Proc Natl Acad Sci U S A. 1972 Dec;69(12):3561-6 PMID: 4509315
  42. Cell contacts in human and bovine lenses.
    Exp Eye Res. 1975 Sep;21(3):205-19 PMID: 1183488
  43. The maturation of the lens cell: a morphologic study.
    Exp Eye Res. 1975 May;20(5):427-43 PMID: 1126408
  44. Lens cell-to-cell channel protein: I. Self-assembly into liposomes and permeability regulation by calmodulin.
    J Membr Biol. 1985;83(3):217-25 PMID: 3999121
  45. Cloning and characterization of human and rat liver cDNAs coding for a gap junction protein.
    J Cell Biol. 1986 Sep;103(3):767-76 PMID: 2875078
  46. Homologies between gap junction proteins in lens, heart and liver.
    Nature. 1988 Feb 25;331(6158):721-3 PMID: 2830542
  47. Molecular cloning of cDNA for rat liver gap junction protein.
    J Cell Biol. 1986 Jul;103(1):123-34 PMID: 3013898
  48. Expression of functional cell-cell channels from cloned rat liver gap junction complementary DNA.
    Science. 1987 Jun 5;236(4806):1290-3 PMID: 3035715
  49. Topology of gap junction protein and channel function.
    Ciba Found Symp. 1987;125:128-39 PMID: 3030672
  50. Evidence for two physiologically distinct gap junctions expressed by the chick lens epithelial cell.
    J Cell Biol. 1986 Jan;102(1):194-9 PMID: 3079768
  51. Formation of gap junctions by expression of connexins in Xenopus oocyte pairs.
    Cell. 1989 Apr 7;57(1):145-55 PMID: 2467743
  52. Cloning and expression of a Xenopus embryonic gap junction protein.
    Science. 1989 Mar 3;243(4895):1194-5 PMID: 2466337
  53. Topological distribution of two connexin32 antigenic sites in intact and split rodent hepatocyte gap junctions.
    J Cell Biol. 1988 Nov;107(5):1817-24 PMID: 2460469
  54. Single channel properties of lens MIP 28 reconstituted into planar lipid bilayers.
    Proc West Pharmacol Soc. 1988;31:251-3 PMID: 2463637
  55. Structure and function of sodium channel.
    J Recept Res. 1987;7(1-4):467-97 PMID: 2442385
  56. Topological mapping and the ionic channel in an acetylcholine receptor.
    Soc Gen Physiol Ser. 1987;41:67-75 PMID: 2436314
  57. Isolated liver gap junctions: gating of transjunctional currents is similar to that in intact pairs of rat hepatocytes.
    Proc Natl Acad Sci U S A. 1986 Aug;83(15):5494-7 PMID: 2426699
  58. The application of patch clamp methods to ocular epithelia.
    Curr Eye Res. 1985 Apr;4(4):409-20 PMID: 2410192
  59. A non-connexon protein (MIP) is involved in eye lens gap-junction formation.
    J Cell Sci. 1989 Jul;93 ( Pt 3):509-13 PMID: 2691517
  60. The structural organization and protein composition of lens fiber junctions.
    J Cell Biol. 1989 Jun;108(6):2255-75 PMID: 2738093
  61. Distribution of gap junctions and square array junctions in the mammalian lens.
    Invest Ophthalmol Vis Sci. 1989 May;30(5):975-89 PMID: 2722452
  62. The major intrinsic protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning.
    Cell. 1984 Nov;39(1):49-59 PMID: 6207938
  63. Conformational properties of the main intrinsic polypeptide (MIP26) isolated from lens plasma membranes.
    Biochemistry. 1987 Dec 15;26(25):8092-8 PMID: 3442647
  64. Immunolocalization of MP70 in lens fiber 16-17-nm intercellular junctions.
    J Cell Biol. 1987 Mar;104(3):565-72 PMID: 3818793
  65. Functional assembly of gap junction conductance in lipid bilayers: demonstration that the major 27 kd protein forms the junctional channel.
    Cell. 1987 Mar 13;48(5):733-43 PMID: 3815522
  66. The distribution of the main intrinsic membrane polypeptide in ocular lens.
    Curr Eye Res. 1985 Nov;4(11):1203-18 PMID: 3907985
  67. Identification of a 70,000-D protein in lens membrane junctional domains.
    J Cell Biol. 1985 Jul;101(1):28-35 PMID: 3891760
  68. Junctions between lens fiber cells are labeled with a monoclonal antibody shown to be specific for MP26.
    J Cell Biol. 1985 Jan;100(1):216-25 PMID: 3880752
Article Info
Journal
The Journal of general physiology
Abbr.
J Gen Physiol
ISSN
0022-1295
Published
1990-09-00
Pages
631-64
Language
English
Region
United States
NLM ID
2985110R
PMCID
PMC2229003
Subset
IM
Grants
NEI NIH HHS · EY-04110 · United States
NEI NIH HHS · EY-05661 · United States
NEI NIH HHS · EY-06075 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com