Differential proteomic analysis of synovial fluid from rheumatoid arthritis and osteoarthritis patients

Clinical Proteomics

Akhilesh Pandey⁹  Subramanian Shankar^1,10  Harsha Gowda⁷  Sujatha Mohan¹  TS Keshava Prasad²  Nandini A Sahasrabuddhe⁷  YL Ramachandra⁵  Vivek Vasudev⁶  Ramesh Jois³  Navjyot Kaur^1,10  Mukesh Dhillon^1,10  Rajesh Raju⁷  Srinivas M Srikanth⁴  Arivusudar Marimuthu⁷  Yashwanth Subbannayya^1,11  Santosh Renuse⁸  Raja Sekhar Nirujogi⁴  Sartaj Ahmad²  Mitali Bhattacharjee⁸  Lavanya Balakrishnan⁵ 

[1] Laboratory for Integrated Bioinformatics, RIKEN Center for Integrative Medical Sciences (IMS-RCAI), Yokohama Institute, Kanagawa 230-0045, Japan;Manipal University, Madhava Nagar, Manipal 576104, India;Department of Rheumatology, Fortis Hospitals, Bangalore 560076, India;Centre for Excellence in Bioinformatics, School of Life Sciences, Pondicherry University, Puducherry 605014, India;Department of Biotechnology, Kuvempu University, Shankaraghatta 577451, India;Department of Rheumatology, Command Airforce Hospital, Bangalore 560008, India;Institute of Bioinformatics, International Technology Park, Bangalore 560066, India;Amrita School of Biotechnology, Amrita Vishwa Vidyapeetham, Kollam 690525, India;Department of Biological Chemistry, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA;Department of Internal Medicine, Armed Forces Medical College, Pune 411040, India;Rajiv Gandhi University of Health Sciences, Bangalore 560041, India

关键词: Extracellular matrix;    Cartilage degradation;    Joint inflammation;    Arthritis;   

Others  :  803342
DOI  :  10.1186/1559-0275-11-1

 received in 2013-04-30, accepted in 2013-12-10,  发布年份 2014

【 摘 要 】

Background

Rheumatoid arthritis and osteoarthritis are two common musculoskeletal disorders that affect the joints. Despite high prevalence rates, etiological factors involved in these disorders remain largely unknown. Dissecting the molecular aspects of these disorders will significantly contribute to improving their diagnosis and clinical management. In order to identify proteins that are differentially expressed between these two conditions, a quantitative proteomic profiling of synovial fluid obtained from rheumatoid arthritis and osteoarthritis patients was carried out by using iTRAQ labeling followed by high resolution mass spectrometry analysis.

Results

We have identified 575 proteins out of which 135 proteins were found to be differentially expressed by ≥3-fold in the synovial fluid of rheumatoid arthritis and osteoarthritis patients. Proteins not previously reported to be associated with rheumatoid arthritis including, coronin-1A (CORO1A), fibrinogen like-2 (FGL2), and macrophage capping protein (CAPG) were found to be upregulated in rheumatoid arthritis. Proteins such as CD5 molecule-like protein (CD5L), soluble scavenger receptor cysteine-rich domain-containing protein (SSC5D), and TTK protein kinase (TTK) were found to be upregulated in the synovial fluid of osteoarthritis patients. We confirmed the upregulation of CAPG in rheumatoid arthritis synovial fluid by multiple reaction monitoring assay as well as by Western blot. Pathway analysis of differentially expressed proteins revealed a significant enrichment of genes involved in glycolytic pathway in rheumatoid arthritis.

Conclusions

We report here the largest identification of proteins from the synovial fluid of rheumatoid arthritis and osteoarthritis patients using a quantitative proteomics approach. The novel proteins identified from our study needs to be explored further for their role in the disease pathogenesis of rheumatoid arthritis and osteoarthritis.

Sartaj Ahmad and Raja Sekhar Nirujogi contributed equally to this article.

【 授权许可】

   
2014 Balakrishnan et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Scott DL, Wolfe F, Huizinga TW: Rheumatoid arthritis. Lancet 2010, 376:1094-1108.
• [2]Chang X, Wei C: Glycolysis and rheumatoid arthritis. Int J Rheum Dis 2011, 14:217-222.
• [3]Klareskog L, Catrina AI, Paget S: Rheumatoid arthritis. Lancet 2009, 373:659-672.
• [4]Rousseau J, Garnero P: Biological markers in osteoarthritis. Bone 2012, 51:265-277.
• [5]Attur M, Krasnokutsky-Samuels S, Samuels J, Abramson SB: Prognostic biomarkers in osteoarthritis. Curr Opin Rheumatol 2013, 25:136-144.
• [6]Da Mota LM, Dos Santos Neto LL, De Carvalho JF: Autoantibodies and other serological markers in rheumatoid arthritis: predictors of disease activity? Clin Rheumatol 2009, 28:1127-1134.
• [7]Van Boekel MA, Vossenaar ER, van den Hoogen FH, Van Venrooij WJ: Autoantibody systems in rheumatoid arthritis: specificity, sensitivity and diagnostic value. Arthritis Res 2002, 4:87-93.
• [8]Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS, et al.: The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988, 31:315-324.
• [9]Kuhn KA, Kulik L, Tomooka B, Braschler KJ, Arend WP, Robinson WH, Holers VM: Antibodies against citrullinated proteins enhance tissue injury in experimental autoimmune arthritis. J Clin Invest 2006, 116:961-973.
• [10]Lee DM, Schur PH: Clinical utility of the anti-CCP assay in patients with rheumatic diseases. Ann Rheum Dis 2003, 62:870-874.
• [11]Goldbach-Mansky R, Lee J, McCoy A, Hoxworth J, Yarboro C, Smolen JS, Steiner G, Rosen A, Zhang C, Menard HA, et al.: Rheumatoid arthritis associated autoantibodies in patients with synovitis of recent onset. Arthritis Res 2000, 2:236-243. BioMed Central Full Text
• [12]Rousseau JC, Delmas PD: Biological markers in osteoarthritis. Nat Clin Pract Rheumatol 2007, 3:346-356.
• [13]Mobasheri A: Osteoarthritis year 2012 in review: biomarkers. Osteoarthritis Cartilage 2012, 20:1451-1464.
• [14]Hui AY, McCarty WJ, Masuda K, Firestein GS, Sah RL: A systems biology approach to synovial joint lubrication in health, injury, and disease. Wiley Interdiscip Rev Syst Biol Med 2012, 4:15-37.
• [15]Uchida T, Fukawa A, Uchida M, Fujita K, Saito K: Application of a novel protein biochip technology for detection and identification of rheumatoid arthritis biomarkers in synovial fluid. J Proteome Res 2002, 1:495-499.
• [16]Sinz A, Bantscheff M, Mikkat S, Ringel B, Drynda S, Kekow J, Thiesen HJ, Glocker MO: Mass spectrometric proteome analyses of synovial fluids and plasmas from patients suffering from rheumatoid arthritis and comparison to reactive arthritis or osteoarthritis. Electrophoresis 2002, 23:3445-3456.
• [17]Mateos J, Lourido L, Fernandez-Puente P, Calamia V, Fernandez-Lopez C, Oreiro N, Ruiz-Romero C, Blanco FJ: Differential protein profiling of synovial fluid from rheumatoid arthritis and osteoarthritis patients using LC-MALDI TOF/TOF. J Proteomics 2012, 75:2869-2878.
• [18]Biswas S, Sharma S, Saroha A, Bhakuni DS, Malhotra R, Zahur M, Oellerich M, Das HR, Asif AR: Identification of novel autoantigen in the synovial fluid of rheumatoid arthritis patients using an immunoproteomics approach. PLoS One 2013, 8:e56246.
• [19]Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, et al.: Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 2004, 3:1154-1169.
• [20]Chaerkady R, Harsha HC, Nalli A, Gucek M, Vivekanandan P, Akhtar J, Cole RN, Simmers J, Schulick RD, Singh S, et al.: A quantitative proteomic approach for identification of potential biomarkers in hepatocellular carcinoma. J Proteome Res 2008, 7:4289-4298.
• [21]Pawar H, Kashyap MK, Sahasrabuddhe NA, Renuse S, Harsha HC, Kumar P, Sharma J, Kandasamy K, Marimuthu A, Nair B, et al.: Quantitative tissue proteomics of esophageal squamous cell carcinoma for novel biomarker discovery. Cancer Biol Ther 2011, 12:510-522.
• [22]Polisetty RV, Gautam P, Sharma R, Harsha HC, Nair SC, Gupta MK, Uppin MS, Challa S, Puligopu AK, Ankathi P: LC-MS/MS analysis of differentially expressed glioblastoma membrane proteome reveals altered calcium signaling and other protein groups of regulatory functions. Mol Cell Proteomics 2012., 11M111 013565
• [23]Gautam P, Nair SC, Gupta MK, Sharma R, Polisetty RV, Uppin MS, Sundaram C, Puligopu AK, Ankathi P, Purohit AK, et al.: Proteins with altered levels in plasma from glioblastoma patients as revealed by iTRAQ-based quantitative proteomic analysis. PLoS One 2012, 7:e46153.
• [24]Kristjansdottir B, Levan K, Partheen K, Carlsohn E, Sundfeldt K: Potential tumor biomarkers identified in ovarian cyst fluid by quantitative proteomic analysis, iTRAQ. Clin Proteomics 2013, 10:4. BioMed Central Full Text
• [25]Kumar GS, Venugopal AK, Mahadevan A, Renuse S, Harsha HC, Sahasrabuddhe NA, Pawar H, Sharma R, Kumar P, Rajagopalan S, et al.: Quantitative proteomics for identifying biomarkers for tuberculous meningitis. Clin Proteomics 2012, 9:12. BioMed Central Full Text
• [26]Venugopal AK, Ghantasala SS, Selvan LD, Mahadevan A, Renuse S, Kumar P, Pawar H, Sahasrabhuddhe NA, Suja MS, Ramachandra YL, et al.: Quantitative proteomics for identifying biomarkers for rabies. Clin Proteomics 2013, 10:3. BioMed Central Full Text
• [27]Keshava Prasad TS, Goel R, Kandasamy K, Keerthikumar S, Kumar S, Mathivanan S, Telikicherla D, Raju R, Shafreen B, Venugopal A, et al.: Human Protein reference database–2009 update. Nucleic Acids Res 2009, 37:D767-D772.
• [28]Prasad TS, Kandasamy K, Pandey A: Human protein reference database and human proteinpedia as discovery tools for systems biology. Methods Mol Biol 2009, 577:67-79.
• [29]Foell D, Roth J: Proinflammatory S100 proteins in arthritis and autoimmune disease. Arthritis Rheum 2004, 50:3762-3771.
• [30]Baillet A, Trocme C, Berthier S, Arlotto M, Grange L, Chenau J, Quetant S, Seve M, Berger F, Juvin R, et al.: Synovial fluid proteomic fingerprint: S100A8, S100A9 and S100A12 proteins discriminate rheumatoid arthritis from other inflammatory joint diseases. Rheumatology (Oxford) 2010, 49:671-682.
• [31]Murphy G, Knauper V, Atkinson S, Butler G, English W, Hutton M, Stracke J, Clark I: Matrix metalloproteinases in arthritic disease. Arthritis Res 2002, 4(Suppl 3):S39-S49. BioMed Central Full Text
• [32]Tchetverikov I, Ronday HK, Van El B, Kiers GH, Verzijl N, TeKoppele JM, Huizinga TW, DeGroot J, Hanemaaijer R: MMP profile in paired serum and synovial fluid samples of patients with rheumatoid arthritis. Ann Rheum Dis 2004, 63:881-883.
• [33]Benarafa C: The SerpinB1 knockout mouse a model for studying neutrophil protease regulation in homeostasis and inflammation. Methods Enzymol 2011, 499:135-148.
• [34]Clausen T, Southan C, Ehrmann M: The HtrA family of proteases: implications for protein composition and cell fate. Mol Cell 2002, 10:443-455.
• [35]Rosenthal AK, Gohr CM, Ninomiya J, Wakim BT: Proteomic analysis of articular cartilage vesicles from normal and osteoarthritic cartilage. Arthritis Rheum 2011, 63:401-411.
• [36]Wu J, Liu W, Bemis A, Wang E, Qiu Y, Morris EA, Flannery CR, Yang Z: Comparative proteomic characterization of articular cartilage tissue from normal donors and patients with osteoarthritis. Arthritis Rheum 2007, 56:3675-3684.
• [37]Polur I, Lee PL, Servais JM, Xu L, Li Y: Role of HTRA1, a serine protease, in the progression of articular cartilage degeneration. Histol Histopathol 2010, 25:599-608.
• [38]Hadfield KD, Rock CF, Inkson CA, Dallas SL, Sudre L, Wallis GA, Boot-Handford RP, Canfield AE: HtrA1 inhibits mineral deposition by osteoblasts: requirement for the protease and PDZ domains. J Biol Chem 2008, 283:5928-5938.
• [39]Grau S, Richards PJ, Kerr B, Hughes C, Caterson B, Williams AS, Junker U, Jones SA, Clausen T, Ehrmann M: The role of human HtrA1 in arthritic disease. J Biol Chem 2006, 281:6124-6129.
• [40]Bauer S, Jendro MC, Wadle A, Kleber S, Stenner F, Dinser R, Reich A, Faccin E, Godde S, Dinges H, et al.: Fibroblast activation protein is expressed by rheumatoid myofibroblast-like synoviocytes. Arthritis Res Ther 2006, 8:R171. BioMed Central Full Text
• [41]Dohi O, Ohtani H, Hatori M, Sato E, Hosaka M, Nagura H, Itoi E, Kokubun S: Histogenesis-specific expression of fibroblast activation protein and dipeptidylpeptidase-IV in human bone and soft tissue tumours. Histopathology 2009, 55:432-440.
• [42]Stamp LK, Khalilova I, Tarr JM, Senthilmohan R, Turner R, Haigh RC, Winyard PG, Kettle AJ: Myeloperoxidase and oxidative stress in rheumatoid arthritis. Rheumatology (Oxford) 2012, 51:1796-1803.
• [43]Tschesche H, Zolzer V, Triebel S, Bartsch S: The human neutrophil lipocalin supports the allosteric activation of matrix metalloproteinases. Eur J Biochem 2001, 268:1918-1928.
• [44]Gupta K, Shukla M, Cowland JB, Malemud CJ, Haqqi TM: Neutrophil gelatinase-associated lipocalin is expressed in osteoarthritis and forms a complex with matrix metalloproteinase 9. Arthritis Rheum 2007, 56:3326-3335.
• [45]Katano M, Okamoto K, Arito M, Kawakami Y, Kurokawa MS, Suematsu N, Shimada S, Nakamura H, Xiang Y, Masuko K, et al.: Implication of granulocyte-macrophage colony-stimulating factor induced neutrophil gelatinase-associated lipocalin in pathogenesis of rheumatoid arthritis revealed by proteome analysis. Arthritis Res Ther 2009, 11:R3. BioMed Central Full Text
• [46]Wang Q, Rozelle AL, Lepus CM, Scanzello CR, Song JJ, Larsen DM, Crish JF, Bebek G, Ritter SY, Lindstrom TM, et al.: Identification of a central role for complement in osteoarthritis. Nat Med 2011, 17:1674-1679.
• [47]Ritter SY, Subbaiah R, Bebek G, Crish J, Scanzello CR, Krastins B, Sarracino D, Lopez MF, Crow MK, Aigner T, et al.: Proteomic analysis of synovial fluid from the osteoarthritic knee: comparison with transcriptome analyses of joint tissues. Arthritis Rheum 2013, 65:981-992.
• [48]Lorenzo P, Neame P, Sommarin Y, Heinegard D: Cloning and deduced amino acid sequence of a novel cartilage protein (CILP) identifies a proform including a nucleotide pyrophosphohydrolase. J Biol Chem 1998, 273:23469-23475.
• [49]Valdes AM, Hart DJ, Jones KA, Surdulescu G, Swarbrick P, Doyle DV, Schafer AJ, Spector TD: Association study of candidate genes for the prevalence and progression of knee osteoarthritis. Arthritis Rheum 2004, 50:2497-2507.
• [50]Tsuruha J, Masuko-Hongo K, Kato T, Sakata M, Nakamura H, Nishioka K: Implication of cartilage intermediate layer protein in cartilage destruction in subsets of patients with osteoarthritis and rheumatoid arthritis. Arthritis Rheum 2001, 44:838-845.
• [51]Gobezie R, Kho A, Krastins B, Sarracino DA, Thornhill TS, Chase M, Millett PJ, Lee DM: High abundance synovial fluid proteome: distinct profiles in health and osteoarthritis. Arthritis Res Ther 2007, 9:R36. BioMed Central Full Text
• [52]Yan M, Di Ciano-Oliveira C, Grinstein S, Trimble WS: Coronin function is required for chemotaxis and phagocytosis in human neutrophils. J Immunol 2007, 178:5769-5778.
• [53]Mueller P, Massner J, Jayachandran R, Combaluzier B, Albrecht I, Gatfield J, Blum C, Ceredig R, Rodewald HR, Rolink AG, Pieters J: Regulation of T cell survival through coronin-1-mediated generation of inositol-1,4,5-trisphosphate and calcium mobilization after T cell receptor triggering. Nat Immunol 2008, 9:424-431.
• [54]Kaminski S, Hermann-Kleiter N, Meisel M, Thuille N, Cronin S, Hara H, Fresser F, Penninger JM, Baier G: Coronin 1A is an essential regulator of the TGFbeta receptor/SMAD3 signaling pathway in Th17 CD4(+) T cells. J Autoimmun 2011, 37:198-208.
• [55]Marazzi S, Blum S, Hartmann R, Gundersen D, Schreyer M, Argraves S, Von Fliedner V, Pytela R, Ruegg C: Characterization of human fibroleukin, a fibrinogen-like protein secreted by T lymphocytes. J Immunol 1998, 161:138-147.
• [56]Chan CW, Kay LS, Khadaroo RG, Chan MW, Lakatoo S, Young KJ, Zhang L, Gorczynski RM, Cattral M, Rotstein O, Levy GA: Soluble fibrinogen-like protein 2/fibroleukin exhibits immunosuppressive properties: suppressing T cell proliferation and inhibiting maturation of bone marrow-derived dendritic cells. J Immunol 2003, 170:4036-4044.
• [57]Yuwaraj S, Ding J, Liu M, Marsden PA, Levy GA: Genomic characterization, localization, and functional expression of FGL2, the human gene encoding fibroleukin: a novel human procoagulant. Genomics 2001, 71:330-338.
• [58]Shalev I, Liu H, Koscik C, Bartczak A, Javadi M, Wong KM, Maknojia A, He W, Liu MF, Diao J, et al.: Targeted deletion of fgl2 leads to impaired regulatory T cell activity and development of autoimmune glomerulonephritis. J Immunol 2008, 180:249-260.
• [59]Melnyk MC, Shalev I, Zhang J, Bartczak A, Gorczynski RM, Selzner N, Inman R, Marsden PA, Phillips MJ, Clark DA, Levy GA: The prothrombinase activity of FGL2 contributes to the pathogenesis of experimental arthritis. Scand J Rheumatol 2011, 40:269-278.
• [60]Wilker E, Yaffe MB: 14–3–3 Proteins–a focus on cancer and human disease. J Mol Cell Cardiol 2004, 37:633-642.
• [61]Calvo J, Places L, Padilla O, Vila JM, Vives J, Bowen MA, Lozano F: Interaction of recombinant and natural soluble CD5 forms with an alternative cell surface ligand. Eur J Immunol 1999, 29:2119-2129.
• [62]Sarrias MR, Padilla O, Monreal Y, Carrascal M, Abian J, Vives J, Yelamos J, Lozano F: Biochemical characterization of recombinant and circulating human Spalpha. Tissue Antigens 2004, 63:335-344.
• [63]Gebe JA, Kiener PA, Ring HZ, Li X, Francke U, Aruffo A: Molecular cloning, mapping to human chromosome 1 q21-q23, and cell binding characteristics of Spalpha, a new member of the scavenger receptor cysteine-rich (SRCR) family of proteins. J Biol Chem 1997, 272:6151-6158.
• [64]Haruta I, Kato Y, Hashimoto E, Minjares C, Kennedy S, Uto H, Yamauchi K, Kobayashi M, Yusa S, Muller U, et al.: Association of AIM, a novel apoptosis inhibitory factor, with hepatitis via supporting macrophage survival and enhancing phagocytotic function of macrophages. J Biol Chem 2001, 276:22910-22914.
• [65]Kuwata K, Watanabe H, Jiang SY, Yamamoto T, Tomiyama-Miyaji C, Abo T, Miyazaki T, Naito M: AIM inhibits apoptosis of T cells and NKT cells in Corynebacterium-induced granuloma formation in mice. Am J Pathol 2003, 162:837-847.
• [66]Goncalves CM, Castro MA, Henriques T, Oliveira MI, Pinheiro HC, Oliveira C, Sreenu VB, Evans EJ, Davis SJ, Moreira A, Carmo AM: Molecular cloning and analysis of SSc5D, a new member of the scavenger receptor cysteine-rich superfamily. Mol Immunol 2009, 46:2585-2596.
• [67]Miro-Julia C, Rosello S, Martinez VG, Fink DR, Escoda-Ferran C, Padilla O, Vazquez-Echeverria C, Espinal-Marin P, Pujades C, Garcia-Pardo A, et al.: Molecular and functional characterization of mouse S5D-SRCRB: a new group B member of the scavenger receptor cysteine-rich superfamily. J Immunol 2011, 186:2344-2354.
• [68]Fisk HA, Mattison CP, Winey M: Human Mps1 protein kinase is required for centrosome duplication and normal mitotic progression. Proc Natl Acad Sci USA 2003, 100:14875-14880.
• [69]Ah-Kim H, Zhang X, Islam S, Sofi JI, Glickberg Y, Malemud CJ, Moskowitz RW, Haqqi TM: Tumour necrosis factor alpha enhances the expression of hydroxyl lyase, cytoplasmic antiproteinase-2 and a dual specificity kinase TTK in human chondrocyte-like cells. Cytokine 2000, 12:142-150.
• [70]Schmandt R, Hill M, Amendola A, Mills GB, Hogg D: IL-2-induced expression of TTK, a serine, threonine, tyrosine kinase, correlates with cell cycle progression. J Immunol 1994, 152:96-105.
• [71]Yu FX, Johnston PA, Sudhof TC, Yin HL: gCap39, a calcium ion- and polyphosphoinositide-regulated actin capping protein. Science 1990, 250:1413-1415.
• [72]Hubert T, Van Impe K, Vandekerckhove J, Gettemans J: The actin-capping protein CapG localizes to microtubule-dependent organelles during the cell cycle. Biochem Biophys Res Commun 2009, 380:166-170.
• [73]Henderson B, Bitensky L, Chayen J: Glycolytic activity in human synovial lining cells in rheumatoid arthritis. Ann Rheum Dis 1979, 38:63-67.
• [74]Ciurtin C, Cojocaru VM, Miron IM, Preda F, Milicescu M, Bojinca M, Costan O, Nicolescu A, Deleanu C, Kovacs E, Stoica V: Correlation between different components of synovial fluid and pathogenesis of rheumatic diseases. Rom J Intern Med 2006, 44:171-181.
• [75]Zborovskaia IA: Serum hexokinase isoenzymes in rheumatoid arthritis. Sov Med 1983, 12:6-11.
• [76]Logvinenko Iu B, Lokshina EG, Shepotinovskii VI, Chernikova LM: Diagnostic role of determination of hexokinase activity in the synovial fluid of knee joints. Lab Delo 1982, 4:212-214.
• [77]Schaller M, Burton DR, Ditzel HJ: Autoantibodies to GPI in rheumatoid arthritis: linkage between an animal model and human disease. Nat Immunol 2001, 2:746-753.
• [78]Schaller M, Stohl W, Benoit V, Tan SM, Johansen L, Ditzel HJ: Patients with inflammatory arthritic diseases harbor elevated serum and synovial fluid levels of free and immune-complexed glucose-6-phosphate isomerase (G6PI). Biochem Biophys Res Commun 2006, 349:838-845.
• [79]Fan LY, Zong M, Wang Q, Yang L, Sun LS, Ye Q, Ding YY, Ma JW: Diagnostic value of glucose-6-phosphate isomerase in rheumatoid arthritis. Clin Chim Acta 2010, 411:2049-2053.
• [80]Saulot V, Vittecoq O, Charlionet R, Fardellone P, Lange C, Marvin L, Machour N, Le Loet X, Gilbert D, Tron F: Presence of autoantibodies to the glycolytic enzyme alpha-enolase in sera from patients with early rheumatoid arthritis. Arthritis Rheum 2002, 46:1196-1201.
• [81]Ukaji F, Kitajima I, Kubo T, Shimizu C, Nakajima T, Maruyama I: Serum samples of patients with rheumatoid arthritis contain a specific autoantibody to “denatured” aldolase A in the osteoblast-like cell line, MG-63. Ann Rheum Dis 1999, 58:169-174.
• [82]Kinloch A, Tatzer V, Wait R, Peston D, Lundberg K, Donatien P, Moyes D, Taylor PC, Venables PJ: Identification of citrullinated alpha-enolase as a candidate autoantigen in rheumatoid arthritis. Arthritis Res Ther 2005, 7:R1421-R1429. BioMed Central Full Text
• [83]Kandasamy K, Keerthikumar S, Goel R, Mathivanan S, Patankar N, Shafreen B, Renuse S, Pawar H, Ramachandra YL, Acharya PK, et al.: Human proteinpedia: a unified discovery resource for proteomics research. Nucleic Acids Res 2009, 37:D773-D781.
• [84]Altman R, Asch E, Bloch D, Bole G, Borenstein D, Brandt K, Christy W, Cooke TD, Greenwald R, Hochberg M, et al.: Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association. Arthritis Rheum 1986, 29:1039-1049.
• [85]Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 1951, 193:265-275.
• [86]Rappsilber J, Mann M, Ishihama Y: Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2007, 2:1896-1906.
• [87]Olsen JV, De Godoy LM, Li G, Macek B, Mortensen P, Pesch R, Makarov A, Lange O, Horning S, Mann M: Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics 2005, 4:2010-2021.
• [88]Kandasamy K, Pandey A, Molina H: Evaluation of several MS/MS search algorithms for analysis of spectra derived from electron transfer dissociation experiments. Anal Chem 2009, 81:7170-7180.
• [89]Lange V, Picotti P, Domon B, Aebersold R: Selected reaction monitoring for quantitative proteomics: a tutorial. Mol Syst Biol 2008, 4:222.
• [90]MacLean B, Tomazela DM, Shulman N, Chambers M, Finney GL, Frewen B, Kern R, Tabb DL, Liebler DC, MacCoss MJ: Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 2010, 26:966-968.
• [91]Barbhuiya MA, Sahasrabuddhe NA, Pinto SM, Muthusamy B, Singh TD, Nanjappa V, Keerthikumar S, Delanghe B, Harsha HC, Chaerkady R, et al.: Comprehensive proteomic analysis of human bile. Proteomics 2011, 11:4443-4453.
• [92]Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al.: Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 2000, 25:25-29.