Novel fatty acid acylation of lens integral membrane protein aquaporin-0

Biochemistry

Volumn 49, Issue 45, 2010, Pages 9858-9865

  Schey, Kevin L ^a,c   Gutierrez, Danielle B ^b   Wang, Zhen ^a   Wei, Junhua ^a   Grey, Angus C ^a,c  

^a VANDERBILT UNIVERSITY   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURATE MASS; ACID MODIFICATION; AMIDE LINKAGES; AQUAPORINS; C-TERMINAL PEPTIDES; CORTICAL REGIONS; CYSTEINE RESIDUES; DETERGENT-RESISTANT MEMBRANES; HUMAN LENS; IMAGING MASS SPECTROMETRY; INTEGRAL MEMBRANE PROTEINS; LC/MS/MS; LENS FIBERS; LYSINE RESIDUES; MEMBRANE ANCHORING; MEMBRANE DOMAIN; MEMBRANE PROTEINS; MEMBRANE TRAFFICKING; METHIONINE RESIDUES; MYRISTOYLATION; N-TERMINALS; PALMITOYLATION; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN ACYLATION; PROTEOMIC ANALYSIS; SPECIFIC SITES; TRYPTIC PEPTIDES;

ACYLATION; AMIDES; AMINO ACIDS; BIOLOGICAL MEMBRANES; CELL MEMBRANES; LENSES; OLEIC ACID; OPTICAL INSTRUMENTS; PEPTIDES; SECONDARY ION MASS SPECTROMETRY; SPECTROMETRY;

MEMBRANES;

AQUAPORIN; CYSTEINE; DETERGENT; FATTY ACID; LYSINE; METHIONINE; OLEIC ACID;

ACYLATION; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; HYDROPHOBICITY; LENS EPITHELIUM; LENS FIBER; LENS NUCLEUS; MASS SPECTROMETRY; MYRISTYLATION; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEOMICS;

ACYLATION; ANIMALS; AQUAPORINS; CATTLE; CHROMATOGRAPHY, LIQUID; EYE PROTEINS; HUMANS; LENS, CRYSTALLINE; LIPOYLATION; MASS SPECTROMETRY; MEMBRANE PROTEINS; PEPTIDE FRAGMENTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRYPSIN;

BOVINAE;

EID: 78149421964     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101415w     Document Type: Article

References (47)

1. Neubert, T. A. and Hurley, J. B. (1998) Functional heterogeneity of transducin alpha subunits FEBS Lett. 422, 343-345
2. Lobanova, E. S., Finkelstein, S., Song, H., Tsang, S. H., Chen, C. K., Sokolov, M., Skiba, N. P., and Arshavsky, V. Y. (2007) Transducin translocation in rods is triggered by saturation of the GTPase-activating complex J. Neurosci. 27, 1151-1160
3. Kokame, K., Fukada, Y., Yoshizawa, T., Takao, T., and Shimonishi, Y. (1992) Lipid modification at the N terminus of photoreceptor G-protein alpha-subunit Nature 359, 749-752
4. Kerov, V., Rubin, W. W., Natochin, M., Melling, N. A., Burns, M. E., and Artemyev, N. O. (2007) N-terminal fatty acylation of transducin profoundly influences its localization and the kinetics of photoresponse in rods J. Neurosci. 27, 10270-10277
5. Sakmar, T. P. (2002) Structure of rhodopsin and the superfamily of seven-helical receptors: the same and not the same Curr. Opin. Cell Biol. 14, 189-195
6. Gustafsson, M., Curstedt, T., Jornvall, H., and Johansson, J. (1997) Reverse-phase HPLC of the hydrophobic pulmonary surfactant proteins: detection of a surfactant protein C isoform containing Nepsilon-palmitoyl-lysine Biochem. J. 326 (Patt 3) 799-806
7. Stevenson, F. T., Bursten, S. L., Fanton, C., Locksley, R. M., and Lovett, D. H. (1993) The 31-kDa precursor of interleukin 1 alpha is myristoylated on specific lysines within the 16-kDa N-terminal propiece Proc. Natl. Acad. Sci. U.S.A. 90, 7245-7249
8. Stevenson, F. T., Bursten, S. L., Locksley, R. M., and Lovett, D. H. (1992) Myristyl acylation of the tumor necrosis factor alpha precursor on specific lysine residues J. Exp. Med. 176, 1053-1062
9. Resh, M. D. (2006) Trafficking and signaling by fatty-acylated and prenylated proteins Nat. Chem. Biol. 2, 584-590
10. Liang, X., Nazarian, A., Erdjument-Bromage, H., Bornmann, W., Tempst, P., and Resh, M. D. (2001) Heterogeneous fatty acylation of Src family kinases with polyunsaturated fatty acids regulates raft localization and signal transduction J. Biol. Chem. 276, 30987-30994
11. Suzuki, H., Nishikawa, K., Hiroaki, Y., and Fujiyoshi, Y. (2008) Formation of aquaporin-4 arrays is inhibited by palmitoylation of N-terminal cysteine residues Biochim. Biophys. Acta 1778, 1181-1189
12. Ishikawa, Y., Yuan, Z., Inoue, N., Skowronski, M. T., Nakae, Y., Shono, M., Cho, G., Yasui, M., Agre, P., and Nielsen, S. (2005) Identification of AQP5 in lipid rafts and its translocation to apical membranes by activation of M3 mAChRs in interlobular ducts of rat parotid gland Am. J. Physiol. Cell. Physiol. 289, C1303-C1311
13. Mazzone, A., Tietz, P., Jefferson, J., Pagano, R., and LaRusso, N. F. (2006) Isolation and characterization of lipid microdomains from apical and basolateral plasma membranes of rat hepatocytes Hepatology 43, 287-296
14. Tong, J., Briggs, M. M., Mlaver, D., Vidal, A., and McIntosh, T. J. (2009) Sorting of lens aquaporins and connexins into raft and nonraft bilayers: role of protein homo-oligomerization Biophys. J. 97, 2493-2502
15. Manenti, S., Dunia, I., and Benedetti, E. L. (1990) Fatty acid acylation of lens fiber plasma membrane proteins. MP26 and alpha-crystallin are palmitoylated FEBS Lett. 262, 356-358
16. Cenedella, R. J. (1990) Palmitoylation of ocular lens membrane proteins Invest. Ophthalmol. Visual Sci. 31, 368-373
17. Chandy, G., Zampighi, G. A., Kreman, M., and Hall, J. E. (1997) Comparison of the water transporting properties of MIP and AQP1 J. Membr. Biol. 159, 29-39
18. Varadaraj, K., Kushmerick, C., Baldo, G. J., Bassnett, S., Shiels, A., and Mathias, R. T. (1999) The role of MIP in lens fiber cell membrane transport J. Membr. Biol. 170, 191-203
19. Michea, L. F., Andrinolo, D., Ceppi, H., and Lagos, N. (1995) Biochemical evidence for adhesion-promoting role of major intrinsic protein isolated from both normal and cataractous human lenses Exp. Eye Res. 61, 293-301
20. Gonen, T., Cheng, Y., Kistler, J., and Walz, T. (2004) Aquaporin-0 membrane junctions form upon proteolytic cleavage J. Mol. Biol. 342, 1337-13345
21. Kumari, S. S. and Varadaraj, K. (2009) Intact AQP0 performs cell-to-cell adhesion Biochem. Biophys. Res. Commun. 390, 1034-1039
22. Ball, L. E., Garland, D. L., Crouch, R. K., and Schey, K. L. (2004) Post-translational modifications of aquaporin 0 (AQP0) in the normal human lens: spatial and temporal occurrence Biochemistry 43, 9856-9865
23. Korlimbinis, A., Berry, Y., Thibault, D., Schey, K. L., and Truscott, R. J. (2009) Protein aging: truncation of aquaporin 0 in human lens regions is a continuous age-dependent process Exp. Eye Res. 88, 966-973
24. Grey, A. C. and Schey, K. L. (2009) Age-related changes in the spatial distribution of human lens alpha-crystallin products by MALDI imaging mass spectrometry Invest. Ophthalmol. Visual Sci. 50, 4319-4329
25. Lin, J. S., Eckert, R., Kistler, J., and Donaldson, P. (1998) Spatial differences in gap junction gating in the lens are a consequence of connexin cleavage Eur. J. Cell Biol. 76, 246-250
26. Reichow, S. L. and Gonen, T. (2008) Noncanonical binding of calmodulin to aquaporin-0: implications for channel regulation Structure 16, 1389-1398
27. Rose, K. M., Wang, Z., Magrath, G. N., Hazard, E. S., Hildebrandt, J. D., and Schey, K. L. (2008) Aquaporin 0-calmodulin interaction and the effect of aquaporin 0 phosphorylation Biochemistry 47, 339-347
28. Nemeth-Cahalan, K. L. and Hall, J. E. (2000) pH and calcium regulate the water permeability of aquaporin 0 J. Biol. Chem. 275, 6777-6782
29. Varadaraj, K., Kumari, S., Shiels, A., and Mathias, R. T. (2005) Regulation of aquaporin water permeability in the lens Invest. Ophthalmol. Visual Sci. 46, 1393-1402
30. Lindsey Rose, K. M., Gourdie, R. G., Prescott, A. R., Quinlan, R. A., Crouch, R. K., and Schey, K. L. (2006) The C terminus of lens aquaporin 0 interacts with the cytoskeletal proteins filensin and CP49 Invest. Ophthalmol. Visual Sci. 47, 1562-1570
31. Thibault, D. B., Gillam, C. J., Grey, A. C., Han, J., and Schey, K. L. (2008) MALDI tissue profiling of integral membrane proteins from ocular tissues J. Am. Soc. Mass Spectrom. 19, 814-822
32. Grey, A., Chaurand, P., Caprioli, R., and Schey, K. (2009) MALDI imaging mass spectrometry of integral membrane proteins from ocular lens and retinal tissue J Proteome Res. 8, 3278-3283
33. Groseclose, M. R., Andersson, M., Hardesty, W. M., and Caprioli, R. M. (2007) Identification of proteins directly from tissue: in situ tryptic digestions coupled with imaging mass spectrometry J. Mass Spectrom. 42, 254-262
34. Grey, A. C., Chaurand, P., Caprioli, R. M., and Schey, K. L. (2009) MALDI imaging mass spectrometry of integral membrane proteins from ocular lens and retinal tissue J. Proteome Res. 8, 3278-3283
35. Schey, K. L., Little, M., Fowler, J. G., and Crouch, R. K. (2000) Characterization of human lens major intrinsic protein structure Invest. Ophthalmol. Visual Sci. 41, 175-182
36. Johansson, J. (1998) Structure and properties of surfactant protein C Biochim. Biophys. Acta 1408, 161-172
37. Li, L. K., So, L., and Spector, A. (1987) Age-dependent changes in the distribution and concentration of human lens cholesterol and phospholipids Biochim. Biophys. Acta 917, 112-120
38. Golczak, M. and Palczewski, K. (2010) An acyl-covalent enzyme intermediate of lecithin:retinol acyltransferase J. Biol. Chem. 285, 29217-29222
39. Noda, Y. and Sasaki, S. (2005) Trafficking mechanism of water channel aquaporin-2 Biol. Cell 97, 885-892
40. Zampighi, G. A., Eskandari, S., Hall, J. E., Zampighi, L., and Kreman, M. (2002) Micro-domains of AQP0 in lens equatorial fibers Exp. Eye Res. 75, 505-519
41. Grey, A. C., Li, L., Jacobs, M. D., Schey, K. L., and Donaldson, P. J. (2009) Differentiation-dependent modification and subcellular distribution of aquaporin-0 suggests multiple functional roles in the rat lens Differentiation 77, 70-83
42. Costello, M. J., McIntosh, T. J., and Robertson, J. D. (1989) Distribution of gap junctions and square array junctions in the mammalian lens Invest. Ophthalmol. Visual Sci. 30, 975-989
43. Zampighi, G. A., Hall, J. E., Ehring, G. R., and Simon, S. A. (1989) The structural organization and protein composition of lens fiber junctions J. Cell Biol. 108, 2255-2275
44. Dunia, I., Recouvreur, M., Nicolas, P., Kumar, N., Bloemendal, H., and Benedetti, E. L. (1998) Assembly of connexins and MP26 in lens fiber plasma membranes studied by SDS-fracture immunolabeling J. Cell Sci. 111 (Part 15) 2109-2120
45. Al-Ghoul, K. J., Kirk, T., Kuszak, A. J., Zoltoski, R. K., Shiels, A., and Kuszak, J. R. (2003) Lens structure in MIP-deficient mice Anat. Rec., Part A 273, 714-730
46. Gonen, T., Sliz, P., Kistler, J., Cheng, Y., and Walz, T. (2004) Aquaporin-0 membrane junctions reveal the structure of a closed water pore Nature 429, 193-197
47. Harries, W. E., Akhavan, D., Miercke, L. J., Khademi, S., and Stroud, R. M. (2004) The channel architecture of aquaporin 0 at a 2.2-Å resolution Proc. Natl. Acad. Sci. U.S.A. 101, 14045-14050