Proteomics and phosphoproteomics analysis of human lens fiber cell membranes

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 2, 2013, Pages 1135-1143

  Wang, Zhen ^a   Han, Jun ^b   David, Larry L ^c   Schey, Kevin L ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VICTORIA   (Canada)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ACTIN; ALPHA CATENIN; ALPHA CRYSTALLIN; ANKYRIN; AQUAPORIN; BETA CRYSTALLIN; CARBONATE DEHYDRATASE; CARBONYL REDUCTASE; CONNEXIN 46; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; FIBRILLIN 1; FILAMIN A; FILENSIN; FRUCTOSE BISPHOSPHATE ALDOLASE; GAMMA CRYSTALLIN; GLUTATHIONE SYNTHASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NERVE CELL ADHESION MOLECULE; PHOSPHOGLYCERATE KINASE; PHOSPHOPROTEOME; PLECTIN; PROTEOME; PYRUVATE KINASE; RETINAL DEHYDROGENASE; UNCLASSIFIED DRUG; VIMENTIN;

ADULT; ARTICLE; CARBOHYDRATE METABOLISM; CELL MEMBRANE; ELECTROSPRAY MASS SPECTROMETRY; GLUTATHIONE METABOLISM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN TISSUE; LENS FIBER; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEOMICS;

ADULT; CELL MEMBRANE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EYE PROTEINS; HUMANS; LENS, CRYSTALLINE; MIDDLE AGED; PHOSPHOPEPTIDES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOMICS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 84874976592     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-11168     Document Type: Article

References (52)

1. Engelman DM. Membranes are more mosaic than fluid. Nature. 2005;438:578-580.
2. Bassnett S. On the mechanism of organelle degradation in the vertebrate lens. Exp Eye Res. 2009;88:133-139.
3. Bateman JB, Johannes M, Flodman P, et al. A new locus for autosomal dominant cataract on chromosome 12q13. Invest Ophthalmol Vis Sci. 2000;41:2665-2670.
4. Berry V, Francis P, Kaushal S, Moore A, Bhattacharya S. Missense mutations in MIP underlie autosomal dominant 'polymorphic' and lamellar cataracts linked to 12q. Nat Genet. 2000;25:15-17.
5. Steele EC Jr, Kerscher S, Lyon MF, et al. Identification of a mutation in the MP19 gene, Lim2, in the cataractous mouse mutant To3. Mol Vis. 1997;3:5.
6. Steele EC Jr, Wang JH, Lo WK, et al. 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. 2000;6:85-94.
7. Graw J, Loster J, Soewarto D, et al. Characterization of a mutation in the lens specific MP70 encoding gene of the mouse leading to a dominant cataract. Exp Eye Res. 2001;73: 867-876.
8. Mackay D, Ionides A, Kibar Z, et al. Connexin 46 mutations in autosomal dominant congenital cataract. Am J Hum Genet. 1999;64:1357-1364.
9. Domon B, Aebersold R. Mass spectrometry and protein analysis. Science. 2006;312:212-217.
10. MacCoss MJ, McDonald WH, Saraf A, et al. Shotgun identification of protein modifications from protein complexes and lens tissue. Proc Natl Acad Sci U S A. 2002;99:7900-7905.
11. Su SP, McArthur JD, Truscott RJ, Aquilina JA. Truncation, crosslinking and interaction of crystallins and intermediate filament proteins in the aging human lens. Biochim Biophys Acta. 2011;1814:647-656.
12. Yao Z, Yu H, Xuan D, Sha Q, Hu J, Zhang J. Analysis of proteinprotein interactions and proteomic profiles of normal human lenses. Curr Eye Res. 2010;35:605-619.
13. Han J, Schey KL. Proteolysis and mass spectrometric analysis of an integral membrane: aquaporin 0. J Proteome Res. 2004; 3:807-812.
14. Schey KL, Gutierrez DB, Wang Z, Wei J, Grey AC. Novel fatty acid acylation of lens integral membrane protein aquaporin-0. Biochemistry. 2010;49:9858-9865.
15. Su S, Liu P, Zhang H, et al. Proteomic analysis of human agerelated nuclear cataracts and normal lens nuclei. Invest Ophthalmol Vis Sci. 2011;52:4182-4191.
16. Harrington V, Srivastava OP, Kirk M. Proteomic analysis of water insoluble proteins from normal and cataractous human lenses. Mol Vis. 2007;13:1680-1694.
17. Santoni V, Molloy M, Rabilloud T. Membrane proteins and proteomics: un amour impossible? Electrophoresis. 2000;21: 1054-1070.
18. Wallin E, von Heijne G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci. 1998;7:1029-1038.
19. Truscott RJ, Comte-Walters S, Ablonczy Z, et al. Tight binding of proteins to membranes from older human cells. Age. 2011; 33:543-554.
20. Bassnett S, Wilmarth PA, David LL. The membrane proteome of the mouse lens fiber cell. Mol Vis. 2009;15:2448-2463.
21. Hunter T. Signaling-2000 and beyond. Cell. 2000;100:113-127.
22. Beausoleil SA, Jedrychowski M, Schwartz D, et al. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci U S A. 2004;101:12130-12135.
23. Nita-Lazar A, Saito-Benz H, White FM. Quantitative phosphoproteomics by mass spectrometry: past, present, and future. Proteomics. 2008;8:4433-4443.
24. Schaefer H, Marcus K, Sickmann A, et al. Identification of phosphorylation and acetylation sites in alphaA-crystallin of the eye lens (mus musculus) after two-dimensional gel electrophoresis. Anal Bioanal Chem. 2003;376:966-972.
25. Shearer D, Ens W, Standing K, Valdimarsson G. Posttranslational modifications in lens fiber connexins identified by offline-HPLC MALDI-quadrupole time-of-flight mass spectrometry. Invest Ophthalmol Vis Sci. 2008;49:1553-1562.
26. Wang Z, Schey KL. Phosphorylation and truncation sites of bovine lens connexin 46 and connexin 50. Exp Eye Res. 2009; 89:898-904.
27. Wang Z, Obidike JE, Schey KL. Posttranslational modifications of the bovine lens beaded filament proteins filensin and CP49. Invest Ophthalmol Vis Sci. 2010;51:1565-1574.
28. Huang CH, Wang YT, Tsai CF, et al. Phosphoproteomics characterization of novel phosphorylated sites of lens proteins from normal and cataractous human eye lenses. Mol Vis. 2011; 17:186-198.
29. Chiou SH, Huang CH, Lee IL, et al. Identification of in vivo phosphorylation sites of lens proteins from porcine eye lenses by a gel-free phosphoproteomics approach. Mol Vis. 2010;16: 294-302.
30. Wang Z, Schey KL. Aquaporin-0 interacts with the FERM domain of ezrin/radixin/moesin proteins in the ocular lens. Invest Ophthalmol Vis Sci. 2011;52:5079-5087.
31. Dasari S, Chambers MC, Slebos RJ, et al. TagRecon: highthroughput mutation identification through sequence tagging. J Proteome Res. 2010;9:1716-1726.
32. Eng JK, McCormack AL, Yates JR III. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom. 1994;5:976-989.
33. Ma ZQ, Dasari S, Chambers MC, et al. IDPicker 2.0: improved protein assembly with high discrimination peptide identification filtering. J Proteome Res. 2009;8:3872-3881.
34. Duncan DT, Prodduturi N, Zhang B. WebGestalt2: an updated and expanded version of the Web-based Gene Set Analysis Toolkit. BMC Bioinformatics. 2010;11:10.
35. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305:567-580.
36. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protoc. 2009;4:44-57.
37. Højlund K, Bowen BP, Hwang H, et al. In vivo phosphoproteome of human skeletal muscle revealed by phosphopeptide enrichment and HPLC-ESI-MS/MS. J Proteome Res. 2009;8: 4954-4965.
38. Olsen JV, Blagoev B, Gnad F, et al. Global, in vivo, and sitespecific phosphorylation dynamics in signaling networks. Cell. 2006;127:635-648.
39. Rigbolt KT, Prokhorova TA, Akimov V, et al. System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci Signal. 2011;4:rs3.
40. Schwartz D, Gygi SP. An iterative statistical approach to the identification of protein phosphorylation motifs from largescale data sets. Nat Biotechnol. 2005;23:1391-1398.
41. Linding R, Jensen LJ, Ostheimer GJ, et al. Systematic discovery of in vivo phosphorylation networks. Cell. 2007;29:1415-1426.
42. Winkler BS, Riley MV. Relative contributions of epithelial cells and fibers to rabbit lens ATP content and glycolysis. Invest Ophthalmol Vis Sci. 1991;32:2593-2598.
43. Jiang JX, Paul DL, Goodenough DA. Posttranslational phosphorylation of lens fiber connexin46: a slow occurrence. Invest Ophthalmol Vis Sci. 1993;34:3558-3565.
44. Das S, Wang H, Molina SA, et al. PKCc, role in lens differentiation and gap junction coupling. Curr Eye Res. 2011;36:620-631.
45. Solan JL, Lampe PD. Connexin43 phosphorylation: structural changes and biological effects. Biochem J. 2009;419:261-272.
46. Shakespeare TI, Sellitto C, Li L, et al. Interaction between Connexin50 and mitogen-activated protein kinase signaling in lens homeostasis. Mol Biol Cell. 2009;20:2582-2592.
47. Kamei A. Glutathione levels of the human crystalline lens in aging and its antioxidant effect against the oxidant of lens proteins. Biol Pharm Bull. 1993;116:870-875.
48. Ireland M, Lieska N, Maisel H. Lens actin: purification and localization. Exp Eye Res. 1983;37:393-408.
49. Ramaekers F, Jap P, Mungyer G, Bloemendal H. Microfilament assembly during lens cell elongation in vitro. Curr Eye Res. 1982;2:169-181.
50. Zandy AJ, Bassnett S. Proteolytic mechanisms underlying mitochondrial degradation in the ocular lens. Invest Ophthalmol Vis Sci. 2007;48:293-302.
51. Gold MG, Reichow SL, O'Neill SE, et al. AKAP2 anchors PKA with aquaporin-0 to support ocular lens transparency. EMBO Mol Med. 2012;4:15-16.
52. Calvin HI, Wu K, Li W, et al. Induction of cortical cataracts in cultured mouse lenses with H-89, an inhibitor of protein kinase A. Curr Eye Res. 2003;27:269-278.