Polymorphic Assemblies and Crystalline Arrays of Lens Tetraspanin MP20

Journal of Molecular Biology

Volumn 376, Issue 2, 2008, Pages 380-392

  Gonen, Tamir ^a,b   Hite, Richard K ^b   Cheng, Yifan ^b   Petre, Benjamin M ^b   Kistler, Joerg ^a   Walz, Thomas ^b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

MP20; single particle electron microscopy; tetraspanin; tetraspanin enriched microdomains; two dimensional crystal

Indexed keywords

DIVALENT CATION; EYE PROTEIN; MAGNESIUM; PROTEIN MP20; TETRASPANIN; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; ENZYME RECONSTITUTION; LENS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ISOLATION; PROTEIN PURIFICATION; THREE DIMENSIONAL IMAGING;

EID: 38349170947     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.09.001     Document Type: Article

References (48)

1. Levy S., and Shoham T. The tetraspanin web modulates immune-signalling complexes. Nature Rev. Immunol. 5 (2005) 136-148
2. Hemler M.E. Tetraspanin functions and associated microdomains. Nature Rev. Mol. Cell. Biol. 6 (2005) 801-811
3. Zemni R., Bienvenu T., Vinet M.C., Sefiani A., Carrie A., Billuart P., et al. A new gene involved in X-linked mental retardation identified by analysis of an X;2 balanced translocation. Nature Genet. 24 (2000) 167-170
4. Kajiwara K., Berson E.L., and Dryja T.P. Digenic retinitis pigmentosa due to mutations at the unlinked peripherin/RDS and ROM1 loci. Science 264 (1994) 1604-1608
5. Dryja T.P., Hahn L.B., Kajiwara K., and Berson E.L. Dominant and digenic mutations in the peripherin/RDS and ROM1 genes in retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 38 (1997) 1972-1982
6. Pras E., Levy-Nissenbaum E., Bakhan T., Lahat H., Assia E., Geffen-Carmi N., et al. A missense mutation in the LIM2 gene is associated with autosomal recessive presenile cataract in an inbred Iraqi Jewish family. Am. J. Hum. Genet. 70 (2002) 1363-1367
7. Kovalenko O.V., Yang X., Kolesnikova T.V., and Hemler M.E. Evidence for specific tetraspanin homodimers: inhibition of palmitoylation makes cysteine residues available for cross-linking. Biochem. J. 377 (2004) 407-417
8. Shoham T., Rajapaksa R., Kuo C.C., Haimovich J., and Levy S. Building of the tetraspanin web: distinct structural domains of CD81 function in different cellular compartments. Mol. Cell. Biol. 26 (2006) 1373-1385
9. Charrin S., Manie S., Oualid M., Billard M., Boucheix C., and Rubinstein E. Differential stability of tetraspanin/tetraspanin interactions: role of palmitoylation. FEBS Letters 516 (2002) 139-144
10. Boesze-Battaglia K., Dispoto J., and Kahoe M.A. Association of a photoreceptor-specific tetraspanin protein, ROM-1, with Triton X-100-resistant membrane rafts from rod outer segment disk membranes. J. Biol. Chem. 277 (2002) 41843-41849
11. Kitadokoro K., Bordo D., Galli G., Petracca R., Falugi F., Abrignani S., et al. CD81 extracellular domain 3D structure: insight into the tetraspanin superfamily structural motifs. EMBO J. 20 (2001) 12-18
12. Kitadokoro K., Ponassi M., Galli G., Petracca R., Falugi F., Grandi G., and Bolognesi M. Subunit association and conformational flexibility in the head subdomain of human CD81 large extracellular loop. J. Biol. Chem. 383 (2002) 1447-1452
13. Min G., Wang H., Sun T.T., and Kong X.P. Structural basis for tetraspanin functions as revealed by the cryo-EM structure of uroplakin complexes at 6-Å resolution. J. Cell Biol. 173 (2006) 975-983
14. Louis C.F., Hur K.C., Galvan A.C., TenBroek E.M., Jarvis L.J., Eccleston E.D., and Howard J.B. Identification of an 18,000-dalton protein in mammalian lens fiber cell membranes. J. Biol. Chem. 264 (1989) 19967-19973
15. Taylor V., Welcher A.A., Program A.E., and Suter U. Epithelial membrane protein-1, peripheral myelin protein 22, and lens membrane protein 20 define a novel gene family. J. Biol. Chem. 270 (1995) 28824-28833
16. Welcher A.A., Suter U., De Leon M., Snipes G.J., and Shooter E.M. A myelin protein is encoded by the homologue of a growth arrest-specific gene. Proc. Natl Acad. Sci. USA 88 (1991) 7195-7199
17. Lobsiger C.S., Magyar J.P., Taylor V., Wulf P., Welcher A.A., Program A.E., and Suter U. Identification and characterization of a cDNA and the structural gene encoding the mouse epithelial membrane protein-1. Genomics 36 (1996) 379-387
18. Taylor V., and Suter U. Epithelial membrane protein-2 and epithelial membrane protein-3: two novel members of the peripheral myelin protein 22 gene family. Gene 175 (1996) 115-120
19. Alcala J., Lieska N., and Maisel H. Protein composition of bovine lens cortical fiber cell membranes. Exp. Eye Res. 21 (1975) 581-595
20. Steele Jr. E.C., Kerscher S., Lyon M.F., Glenister P.H., Favor J., Wang J., and Church R.L. Identification of a mutation in the MP19 gene, Lim2, in the cataractous mouse mutant To3. Mol. Vis. 3 (1997) 5
21. Steele Jr. E.C., Wang J.H., Lo W.K., Saperstein D.A., Li X., and Church R.L. Lim2(To3) transgenic mice establish a causative relationship between the mutation identified in the lim2 gene and cataractogenesis in the To3 mouse mutant. Mol. Vis. 6 (2000) 85-94
22. Louis C.F., Johnson R., Johnson K., and Turnquist J. Characterization of the bovine lens plasma membrane substrates for cAMP-dependent protein kinase. Eur. J. Biochem. 150 (1985) 279-286
23. Louis C.F., Hogan P., Visco L., and Strasburg G. Identity of the calmodulin-binding proteins in bovine lens plasma membranes. Exp. Eye Res. 50 (1990) 495-503
24. Gonen T., Donaldson P., and Kistler J. Galectin-3 is associated with the plasma membrane of lens fiber cells. Invest. Ophthalmol. Vis. Sci. 41 (2000) 199-203
25. Gonen T., Grey A.C., Jacobs M.D., Donaldson P.J., and Kistler J. MP20, the second most abundant lens membrane protein and member of the tetraspanin superfamily, joins the list of ligands of galectin-3. BMC Cell Biol. 2 (2001) 17
26. Grey A.C., Jacobs M.D., Gonen T., Kistler J., and Donaldson P.J. Insertion of MP20 into lens fibre cell plasma membranes correlates with the formation of an extracellular diffusion barrier. Exp. Eye Res. 77 (2003) 567-574
27. Ervin L.A., Ball L.E., Crouch R.K., and Schey K.L. Phosphorylation and glycosylation of bovine lens MP20. Invest. Ophthalmol. Vis. Sci. 46 (2005) 627-635
28. Jarvis L.J., and Louis C.F. Purification and oligomeric state of the major lens fiber cell membrane proteins. Curr. Eye Res. 14 (1995) 799-808
29. Ohi M., Li Y., Cheng Y., and Walz T. Negative staining and image classification - powerful tools in modern electron microscopy. Biol. Proced. Online 6 (2004) 23-34
30. Broekhuyse R.M., and Kuhlmann E.D. Lipids in tissues of the eye. VI. Sphingomyelins and cholesterol esters in human sclera. Exp. Eye Res. 14 (1972) 111-113
31. Gonen T., Cheng Y., Sliz P., Hiroaki Y., Fujiyoshi Y., Harrison S.C., and Walz T. Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438 (2005) 633-638
32. Hasler L., Walz T., Tittmann P., Gross H., Kistler J., and Engel A. Purified lens major intrinsic protein (MIP) forms highly ordered tetragonal two-dimensional arrays by reconstitution. J. Mol. Biol. 279 (1998) 855-864
33. Henderson R., and Unwin P.N. Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257 (1975) 28-32
34. Jensen T.W., Hu B.H., Delatore S.M., Garcia A.S., Messersmith P.B., and Miller W.M. Lipopeptides incorporated into supported phospholipid monolayers have high specific activity at low incorporation levels. J. Am. Chem. Soc. 126 (2004) 15223-15230
35. Lee A.G. Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta 1612 (2003) 1-40
36. Lee A.G. Cell biology: a greasy grip. Nature 438 (2005) 569-570
37. Swamy-Mruthinti S. Glycation decreases calmodulin binding to lens transmembrane protein, MIP. Biochim. Biophys. Acta 1536 (2001) 64-72
38. Donaldson P., Kistler J., and Mathias R.T. Molecular solutions to mammalian lens transparency. News Physiol. Sci. 16 (2001) 118-123
39. Piatigorsky J., and Wistow G.J. Enzyme/crystallins: gene sharing as an evolutionary strategy. Cell 57 (1989) 197-199
40. Chandy G., Zampighi G.A., Kreman M., and Hall J.E. Comparison of the water transporting properties of MIP and AQP1. J. Membr. Biol. 159 (1997) 29-39
41. Mulders S.M., Preston G.M., Deen P.M., Guggino W.B., van Os C.H., and Agre P. Water channel properties of major intrinsic protein of lens. J. Biol. Chem. 270 (1995) 9010-9016
42. Gonen T., Cheng Y., Kistler J., and Walz T. Aquaporin-0 membrane junctions form upon proteolytic cleavage. J. Mol. Biol. 342 (2004) 1337-1345
43. Nemeth-Cahalan K.L., and Hall J.E. pH and calcium regulate the water permeability of aquaporin 0. J. Biol. Chem. 275 (2000) 6777-6782
44. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., and Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 (1996) 190-199
45. Radermacher M., Wagenknecht T., Verschoor A., and Frank J. Three-dimensional reconstruction from a single-exposure, random conical tilt series applied to the 50S ribosomal subunit of Escherichia coli. J. Microsc. 146 (1987) 113-136
46. Crowther R.A., Henderson R., and Smith J.M. MRC image processing programs. J. Struct. Biol. 116 (1996) 9-16
47. Amos L.A., Henderson R., and Unwin P.N. Three-dimensional structure determination by electron microscopy of two-dimensional crystals. Prog. Biophys. Mol. Biol. 39 (1982) 183-231
48. Valpuesta J.M., Carrascosa J.L., and Henderson R. Analysis of electron microscope images and electron diffraction patterns of thin crystals of phi 29 connectors in ice. J. Mol. Biol. 240 (1994) 281-287