In situ cell surface proteomics reveals differentially expressed membrane proteins in retinal pigment epithelial cells during autoimmune uveitis

Journal of Proteomics

Volumn 109, Issue , 2014, Pages 50-62

  Uhl, P B ^a   Szober, C M ^a   Amann, B ^a   Alge Priglinger, C ^a   Ueffing, M ^b,c   Hauck, S M ^b   Deeg, C A ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Basigin; Collectrin; In situ biotinylation; Proteomics; Retinal pigment epithelium; Synaptotagmin 1

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM) BETA1; APOLIPOPROTEIN D; CD147 ANTIGEN; CELL SURFACE PROTEIN; CHONDROITIN SULFATE PROTEOGLYCAN 5; COLLECTRIN; FETUIN A; GABA TRANSPORTER 2; GLUCOSE TRANSPORTER 4; GLYCOPROTEIN; GLYCOPROTEIN M6A; GLYCOPROTEIN M6B; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HERMES ANTIGEN; LACTADHERIN; MALATE DEHYDROGENASE; MITOCHONDRIAL PHOSPHATE CARRIER PROTEIN; NEUROTRIMIN; PERIPHERIN; PERIPHERIN 2; PROTEOCHONDROITIN SULFATE; RETINA S ANTIGEN; RHODOPSIN; RPE65 PROTEIN; SODIUM POTASSIUM CALCIUM EXCHANGER 1; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; EYE PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE UVEITIS; BIOTINYLATION; BLOOD RETINA BARRIER; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; EQUIDAE; HORSE DISEASE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PATHOPHYSIOLOGY; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RETINA CELL; TANDEM MASS SPECTROMETRY; ANIMAL EXPERIMENT; FLOW CYTOMETRY; HORSE; PROTEIN ANALYSIS; ANIMAL; AUTOIMMUNE DISEASE; BIOSYNTHESIS; FEMALE; GENE EXPRESSION REGULATION; HUMAN; MALE; METABOLISM; PATHOLOGY; UVEITIS; VETERINARY;

ANIMALS; AUTOIMMUNE DISEASES; CHROMATOGRAPHY, LIQUID; EYE PROTEINS; FEMALE; GENE EXPRESSION REGULATION; HORSE DISEASES; HORSES; HUMANS; MALE; MASS SPECTROMETRY; PROTEOMICS; RETINAL PIGMENT EPITHELIUM; UVEITIS;

EID: 84904126477     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.06.020     Document Type: Article

References (56)

1. Olaya-Abril A., Jimenez-Munguia I., Gomez-Gascon L., Rodriguez-Ortega M.J. Surfomics: shaving live organisms for a fast proteomic identification of surface proteins. J Proteome 2014, 97:164-176.
2. Hauck S.M., Dietter J., Kramer R.L., Hofmaier F., Zipplies J.K., Amann B., et al. Deciphering membrane-associated molecular processes in target tissue of autoimmune uveitis by label-free quantitative mass spectrometry. Mol Cell Proteomics 2010, 9:2292-2305.
3. Stevens T.J., Arkin I.T. Do more complex organisms have a greater proportion of membrane proteins in their genomes?. Proteins 2000, 39:417-420.
4. Wu C.C., Yates J.R. The application of mass spectrometry to membrane proteomics. Nat Biotechnol 2003, 21:262-267.
5. Macher B.A., Yen T.Y. Proteins at membrane surfaces - a review of approaches. Mol BioSyst 2007, 3:705-713.
6. Hauck S.M., Hofmaier F., Dietter J., Swadzba M.E., Blindert M., Amann B., et al. Label-free LC-MSMS analysis of vitreous from autoimmune uveitis reveals a significant decrease in secreted Wnt signalling inhibitors DKK3 and SFRP2. J Proteome 2012, 75:4545-4554.
7. Degroote R.L., Hauck S.M., Treutlein G., Amann B., Frohlich K.J., Kremmer E., et al. Expression changes and novel interaction partners of talin 1 in effector cells of autoimmune uveitis. J Proteome Res 2013, 12:5812-5819.
8. Szober C.M., Hauck S.M., Euler K.N., Frohlich K.J., Alge-Priglinger C., Ueffing M., et al. Profound re-organization of cell surface proteome in equine retinal pigment epithelial cells in response to in vitro culturing. Int J Mol Sci 2012, 13:14053-14072.
9. De Schaepdrijver L., Simoens P., Lauwers H., De Geest J.P. Retinal vascular patterns in domestic animals. Res Vet Sci 1989, 47:34-42.
10. Deeg C.A., Thurau S.R., Gerhards H., Ehrenhofer M., Wildner G., Kaspers B. Uveitis in horses induced by interphotoreceptor retinoid-binding protein is similar to the spontaneous disease. Eur J Immunol 2002, 32:2598-2606.
11. Deeg C.A., Ehrenhofer M., Thurau S.R., Reese S., Wildner G., Kaspers B. Immunopathology of recurrent uveitis in spontaneously diseased horses. Exp Eye Res 2002, 75:127-133.
12. Deeg C.A., Hauck S.M., Amann B., Kremmer E., Stangassinger M., Ueffing M. Major retinal autoantigens remain stably expressed during all stages of spontaneous uveitis. Mol Immunol 2007, 44:3291-3296.
13. Ehrenhofer M.C., Deeg C.A., Reese S., Liebich H.G., Stangassinger M., Kaspers B. Normal structure and age-related changes of the equine retina. Vet Ophthalmol 2002, 5:39-47.
14. Keller A., Nesvizhskii A.I., Kolker E., Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002, 74:5383-5392.
15. Deeg C.A., Eberhardt C., Hofmaier F., Amann B., Hauck S.M. Osteopontin and fibronectin levels are decreased in vitreous of autoimmune uveitis and retinal expression of both proteins indicates ECM re-modeling. PLoS ONE 2011, 6:e27674.
16. Diniz B., Thomas P., Thomas B., Ribeiro R., Hu Y., Brant R., et al. Subretinal implantation of retinal pigment epithelial cells derived from human embryonic stem cells: improved survival when implanted as a monolayer. Invest Ophthalmol Vis Sci 2013, 54:5087-5096.
17. Alge C.S., Suppmann S., Priglinger S.G., Neubauer A.S., May C.A., Hauck S., et al. Comparative proteome analysis of native differentiated and cultured dedifferentiated human RPE cells. Invest Ophthalmol Vis Sci 2003, 44:3629-3641.
18. Swadzba M.E., Hauck S.M., Naim H.Y., Amann B., Deeg C.A. Retinal glycoprotein enrichment by concanavalin a enabled identification of novel membrane autoantigen synaptotagmin-1 in equine recurrent uveitis. PLoS ONE 2012, 7:e50929.
19. Nishibaba R., Higashi Y., Su J., Furukawa T., Kawai K., Kanekura T. CD147-targeting siRNA inhibits cell-matrix adhesion of human malignant melanoma cells by phosphorylating focal adhesion kinase. J Dermatol 2012, 39:63-67.
20. Philp N.J., Wang D., Yoon H., Hjelmeland L.M. Polarized expression of monocarboxylate transporters in human retinal pigment epithelium and ARPE-19 cells. Invest Ophthalmol Vis Sci 2003, 44:1716-1721.
21. Gu X., Neric N.J., Crabb J.S., Crabb J.W., Bhattacharya S.K., Rayborn M.E., et al. Age-related changes in the retinal pigment epithelium (RPE). PLoS ONE 2012, 7:e38673.
22. Kay P., Yang Y.C., Paraoan L. Directional protein secretion by the retinal pigment epithelium: roles in retinal health and the development of age-related macular degeneration. J Cell Mol Med 2013, 17:833-843.
23. Alge C.S., Hauck S.M., Priglinger S.G., Kampik A., Ueffing M. Differential protein profiling of primary versus immortalized human RPE cells identifies expression patterns associated with cytoskeletal remodeling and cell survival. J Proteome Res 2006, 5:862-878.
24. Deeg C.A., Pompetzki D., Raith A.J., Hauck S.M., Amann B., Suppmann S., et al. Identification and functional validation of novel autoantigens in equine uveitis. Mol Cell Proteomics 2006, 5:1462-1470.
25. Deeg C.A., Hauck S.M., Amann B., Pompetzki D., Altmann F., Raith A., et al. Equine recurrent uveitis - a spontaneous horse model of uveitis. Ophthalmic Res 2008, 40:151-153.
26. West K.A., Yan L., Shadrach K., Sun J., Hasan A., Miyagi M., et al. Protein database, human retinal pigment epithelium. Mol Cell Proteomics 2003, 2:37-49.
27. Maeda R., Hiroshima M., Yamashita T., Wada A., Nishimura S., Sako Y., et al. Single-molecule observation of the ligand-induced population shift of rhodopsin, a G-protein-coupled receptor. Biophys J 2014, 106:915-924.
28. Deeg C.A., Reese S., Gerhards H., Wildner G., Kaspers B. The uveitogenic potential of retinal S-antigen in horses. Invest Ophthalmol Vis Sci 2004, 45:2286-2292.
29. Zipplies J.K., Kirschfink M., Amann B., Hauck S.M., Stangassinger M., Deeg C.A. Complement factor B expression profile in a spontaneous uveitis model. Immunobiology 2010, 215:949-955.
30. Zipplies J.K., Hauck S.M., Schoeffmann S., Amann B., van der Meijden C.H., Stangassinger M., et al. Kininogen in autoimmune uveitis: decrease in peripheral blood stream versus increase in target tissue. Invest Ophthalmol Vis Sci 2010, 51:375-382.
31. Wagner B. Immunoglobulins and immunoglobulin genes of the horse. Dev Comp Immunol 2006, 30:155-164.
32. Zipplies J.K., Hauck S.M., Schoeffmann S., Amann B., Stangassinger M., Ueffing M., et al. Serum PEDF levels are decreased in a spontaneous animal model for human autoimmune uveitis. J Proteome Res 2009, 8:992-998.
33. Deeg C.A., Kaspers B., Gerhards H., Thurau S.R., Wollanke B., Wildner G. Immune responses to retinal autoantigens and peptides in equine recurrent uveitis. Invest Ophthalmol Vis Sci 2001, 42:393-398.
34. Deeg C.A., Altmann F., Hauck S.M., Schoeffmann S., Amann B., Stangassinger M., et al. Down-regulation of pigment epithelium-derived factor in uveitic lesion associates with focal vascular endothelial growth factor expression and breakdown of the blood-retinal barrier. Proteomics 2007, 7:1540-1548.
35. Hauck S.M., Schoeffmann S., Amann B., Stangassinger M., Gerhards H., Ueffing M., et al. Retinal Mueller glial cells trigger the hallmark inflammatory process in autoimmune uveitis. J Proteome Res 2007, 6:2121-2131.
36. Gilger B.C., Malok E., Cutter K.V., Stewart T., Horohov D.W., Allen J.B. Characterization of T-lymphocytes in the anterior uvea of eyes with chronic equine recurrent uveitis. Vet Immunol Immunopathol 1999, 71:17-28.
37. Schlichtenbrede F.C., da Cruz L., Stephens C., Smith A.J., Georgiadis A., Thrasher A.J., et al. Long-term evaluation of retinal function in Prph2Rd2/Rd2 mice following AAV-mediated gene replacement therapy. J Gene Med 2003, 5:757-764.
38. de Sousa Dias M., Hernan I., Pascual B., Borras E., Mane B., Gamundi M.J., et al. Detection of novel mutations that cause autosomal dominant retinitis pigmentosa in candidate genes by long-range PCR amplification and next-generation sequencing. Mol Vis 2013, 19:654-664.
39. Arnouk H., Lee H., Zhang R., Chung H., Hunt R.C., Jahng W.J. Early biosignature of oxidative stress in the retinal pigment epithelium. J Proteome 2011, 74:254-261.
40. Moiseyev G., Chen Y., Takahashi Y., Wu B.X., Ma J.X. RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc Natl Acad Sci U S A 2005, 102:12413-12418.
41. Ahmado A., Carr A.J., Vugler A.A., Semo M., Gias C., Lawrence J.M., et al. Induction of differentiation by pyruvate and DMEM in the human retinal pigment epithelium cell line ARPE-19. Invest Ophthalmol Vis Sci 2011, 52:7148-7159.
42. Milyushina L.A., Verdiev B.I., Kuznetsova A.V., Aleksandrova M.A. Expression of multipotent and retinal markers in pigment epithelium of adult human in vitro. Bull Exp Biol Med 2012, 153:157-162.
43. Alizadeh M., Wada M., Gelfman C.M., Handa J.T., Hjelmeland L.M. Downregulation of differentiation specific gene expression by oxidative stress in ARPE-19 cells. Invest Ophthalmol Vis Sci 2001, 42:2706-2713.
44. Cordeiro J.M., Boda B., Goncalves P.P., Dunant Y. Synaptotagmin 1 is required for vesicular Ca(2)(+)/H(+)-antiport activity. J Neurochem 2013, 126:37-46.
45. Poskanzer K.E., Marek K.W., Sweeney S.T., Davis G.W. Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 2003, 426:559-563.
46. Glavan G., Schliebs R., Zivin M. Synaptotagmins in neurodegeneration. Anat Rec 2009, 292:1849-1862.
47. Reddy P.H., Mani G., Park B.S., Jacques J., Murdoch G., Whetsell W., et al. Differential loss of synaptic proteins in Alzheimer's disease: implications for synaptic dysfunction. J Alzheimers Dis 2005, 7:103-117. [discussion 73-80].
48. Pablo K.A., Ochrietor J.D. Deletion of the basigin gene results in reduced mitochondria in the neural retina. Biochem Biophys Res Commun 2013, 438:546-550.
49. Philp N.J., Ochrietor J.D., Rudoy C., Muramatsu T., Linser P.J. Loss of MCT1, MCT3, and MCT4 expression in the retinal pigment epithelium and neural retina of the 5A11/basigin-null mouse. Invest Ophthalmol Vis Sci 2003, 44:1305-1311.
50. Marmorstein A.D., Gan Y.C., Bonilha V.L., Finnemann S.C., Csaky K.G., Rodriguez-Boulan E. Apical polarity of N-CAM and EMMPRIN in retinal pigment epithelium resulting from suppression of basolateral signal recognition. J Cell Biol 1998, 142:697-710.
51. Hori K., Katayama N., Kachi S., Kondo M., Kadomatsu K., Usukura J., et al. Retinal dysfunction in basigin deficiency. Invest Ophthalmol Vis Sci 2000, 41:3128-3133.
52. Zhang H., Wada J., Hida K., Tsuchiyama Y., Hiragushi K., Shikata K., et al. Collectrin, a collecting duct-specific transmembrane glycoprotein, is a novel homolog of ACE2 and is developmentally regulated in embryonic kidneys. J Biol Chem 2001, 276:17132-17139.
53. Danilczyk U., Sarao R., Remy C., Benabbas C., Stange G., Richter A., et al. Essential role for collectrin in renal amino acid transport. Nature 2006, 444:1088-1091.
54. Fukui K., Yang Q., Cao Y., Takahashi N., Hatakeyama H., Wang H., et al. The HNF-1 target collectrin controls insulin exocytosis by SNARE complex formation. Cell Metab 2005, 2:373-384.
55. Cechova S., Zeng Q., Billaud M., Mutchler S., Rudy C.K., Straub A.C., et al. Loss of collectrin, an angiotensin-converting enzyme 2 homolog, uncouples endothelial nitric oxide synthase and causes hypertension and vascular dysfunction. Circulation 2013, 128:1770-1780.
56. Pepaj M., Gjerlaugsen N., Julien K., Thorsby P.M. Tmem27 is upregulated by vitamin D in INS-1 cells and its serum concentrations are low in patients with autoimmune diabetes. Scand J Clin Lab Invest 2014, 74:358-365.