Identification of periodontitis associated changes in the proteome of whole human saliva by mass spectrometric analysis

Journal of Clinical Periodontology

Volumn 40, Issue 9, 2013, Pages 825-832

  Salazar, Manuela Gesell ^a   Jehmlich, Nico ^a   Murr, Annette ^a   Dhople, Vishnu M ^a   Holtfreter, Birte ^a   Hammer, Elke ^a   Völker, Uwe ^a   Kocher, Thomas ^a  

^a UNIVERSITY MEDICINE GREIFSWALD   (Germany)

Author keywords

label free quantitation; LC MS MS; periodontitis; protein candidates; whole saliva proteomics

Indexed keywords

ACTIN BINDING PROTEIN; ACUTE PHASE PROTEIN; AUTACOID; BIOLOGICAL MARKER; DEFENSIN; MEMBRANE PROTEIN; NEUTROPHIL DEFENSIN HNP2, HUMAN; PLASTIN; PROTEIN S 100; PROTEOME; SALIVA PROTEIN;

ADULT; ARTICLE; CASE CONTROL STUDY; CHEMISTRY; CHRONIC PERIODONTITIS; COHORT ANALYSIS; COMPARATIVE STUDY; CROSS-SECTIONAL STUDY; FEMALE; GERMANY; HEALTH SURVEY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; LABEL FREE QUANTITATION; LC-MS/MS; MALE; METABOLISM; METHODOLOGY; MIDDLE AGED; PERIODONTAL DISEASE; PERIODONTAL POCKET; PERIODONTICS; PERIODONTITIS; PHYSIOLOGY; PROTEIN CANDIDATES; PROTEIN FOLDING; SALIVA; SIGNAL TRANSDUCTION; SMOKING; TANDEM MASS SPECTROMETRY; WHOLE SALIVA PROTEOMICS;

LABEL FREE QUANTITATION; LC-MS/MS; PERIODONTITIS; PROTEIN CANDIDATES; WHOLE SALIVA PROTEOMICS;

ACUTE-PHASE PROTEINS; ADULT; BIOLOGICAL MARKERS; CASE-CONTROL STUDIES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHRONIC PERIODONTITIS; COHORT STUDIES; CROSS-SECTIONAL STUDIES; DEFENSINS; FEMALE; GERMANY; HUMANS; INFLAMMATION MEDIATORS; MALE; MEMBRANE GLYCOPROTEINS; MICROFILAMENT PROTEINS; MIDDLE AGED; PERIODONTAL ATTACHMENT LOSS; PERIODONTAL INDEX; PERIODONTAL POCKET; POPULATION SURVEILLANCE; PROTEIN FOLDING; PROTEOME; S100 PROTEINS; SALIVA; SALIVARY PROTEINS AND PEPTIDES; SIGNAL TRANSDUCTION; SMOKING; TANDEM MASS SPECTROMETRY;

EID: 84886085713     PISSN: 03036979     EISSN: 1600051X     Source Type: Journal    
DOI: 10.1111/jcpe.12130     Document Type: Article

References (66)

1. Abiko, Y., Nishimura, M., &, Kaku, T., (2003) Defensins in saliva and the salivary glands. Medical Electron Microscopy 36, 247-252.
2. Amado, F. M., Ferreira, R. P., &, Vitorino, R., (2012) One decade of salivary proteomics: current approaches and outstanding challenges. Clinical Biochemistry 46, 509-517.
3. Ambatipudi, K. S., Swatkoski, S., Moresco, J. J., Tu, P. G., Coca, A., Anolik, J. H., Gucek, M., Sanz, I., Yates, J. R. 3rd, &, Melvin, J. E., (2012) Quantitative proteomics of parotid saliva in primary Sjogren's syndrome. Proteomics 12, 3113-3120.
4. Armitage, G. C., (1999) Development of a classification system for periodontal diseases and conditions. Annals of Periodontology 4, 1-6.
5. Baliban, R. C., Sakellari, D., Li, Z., DiMaggio, P. A., Garcia, B. A., &, Floudas, C. A., (2011) Novel protein identification methods for biomarker discovery via a proteomic analysis of periodontally healthy and diseased gingival crevicular fluid samples. Journal of Clinical Periodontology 39, 203-212.
6. Bandhakavi, S., Stone, M. D., Onsongo, G., Van Riper, S. K., &, Griffin, T. J., (2009) A dynamic range compression and three-dimensional peptide fractionation analysis platform expands proteome coverage and the diagnostic potential of whole saliva. Journal of Proteome Research 8, 5590-5600.
7. Bostanci, N., Heywood, W., Mills, K., Parkar, M., Nibali, L., &, Donos, N., (2010) Application of label-free absolute quantitative proteomics in human gingival crevicular fluid by LC/MS E (gingival exudatome). Journal of Proteome Research 9, 2191-2199.
8. Brinkmann, O., Kastratovic, D. A., Dimitrijevic, M. V., Konstantinovic, V. S., Jelovac, D. B., Antic, J., Nesic, V. S., Markovic, S. Z., Martinovic, Z. R., Akin, D., Spielmann, N., Zhou, H., &, Wong, D. T., (2011) Oral squamous cell carcinoma detection by salivary biomarkers in a Serbian population. Oral Oncology 47, 51-55.
9. Buduneli, N., &, Kinane, D. F., (2011) Host-derived diagnostic markers related to soft tissue destruction and bone degradation in periodontitis. Journal of Clinical Periodontology 38 (Suppl 11), 85-105.
10. Carneiro, L. G., Venuleo, C., Oppenheim, F. G., &, Salih, E., (2012) Proteome data set of human gingival crevicular fluid from healthy periodontium sites by multidimensional protein separation and mass spectrometry. Journal of Periodontal Research 47, 248-262.
11. Caseiro, A., Ferreira, R., Padrao, A., Quintaneiro, C., Pereira, A., Marinheiro, R., Vitorino, R., &, Amado, F., (2013) Salivary proteome and peptidome profiling in type 1 diabetes mellitus using a quantitative approach. Journal of Proteome Research 12, 1700-1709.
12. Castagnola, M., Cabras, T., Iavarone, F., Fanali, C., Nemolato, S., Peluso, G., Bosello, S. L., Faa, G., Ferraccioli, G., &, Messana, I., (2012) The human salivary proteome: a critical overview of the results obtained by different proteomic platforms. Expert Review of Proteomics 9, 33-46.
13. Chan, H. H., Rahim, Z. H., Jessie, K., Hashim, O. H., &, Taiyeb-Ali, T. B., (2012) Salivary proteins associated with periodontitis in patients with type 2 diabetes mellitus. International Journal of Molecular Sciences 13, 4642-4654.
14. Choi, Y. H., Heo, S. H., Lee, J. M., &, Cho, J. Y., (2011) Identification of azurocidin as a potential periodontitis biomarker by a proteomic analysis of gingival crevicular fluid. Proteome Science 9. doi: 10.1186/1477-5956-9-42.
15. Christodoulides, N., Floriano, P. N., Miller, C. S., Ebersole, J. L., Mohanty, S., Dharshan, P., Griffin, M., Lennart, A., Ballard, K. L., King, C. P. Jr, Langub, M. C., Kryscio, R. J., Thomas, M. V., &, McDevitt, J. T., (2007) Lab-on-a-chip methods for point-of-care measurements of salivary biomarkers of periodontitis. Annals of the New York Academy of Sciences 1098, 411-428.
16. Craig, R. G., Yip, J. K., So, M. K., Boylan, R. J., Socransky, S. S., &, Haffajee, A. D., (2003) Relationship of destructive periodontal disease to the acute-phase response. Journal of Periodontology 74, 1007-1016.
17. Donato, R., (2001) S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. The International Journal of Biochemistry & Cell Biology 33, 637-668.
18. Ebersole, J. L., Machen, R. L., Steffen, M. J., &, Willmann, D. E., (1997) Systemic acute-phase reactants, C-reactive protein and haptoglobin, in adult periodontitis. Clinical and Experimental Immunology 107, 347-352.
19. Giannobile, W. V., Beikler, T., Kinney, J. S., Ramseier, C. A., Morelli, T., &, Wong, D. T., (2009) Saliva as a diagnostic tool for periodontal disease: current state and future directions. Periodontology 2000 50, 52-64.
20. Golatowski, C., Gesell Salazar, M., Dhople, V. M., Hammer, E., Kocher, T., Jehmlich, N., &, Volker, U., (2013) Comparative evaluation of saliva collection methods for proteome analysis. Clinica Chimica Acta 419C, 42-46.
21. Gonçalves, L. D. R., Soares, M. R., Nogueira, F. C. S., Garcia, C., Camisasca, D. R., Domont, G., Feitosa, A. C. R., Pereira, D., &, d. A., Zingali, R. B., &, Alves, G., (2010) Comparative proteomic analysis of whole saliva from chronic periodontitis patients. Journal of Proteomics 73, 1334-1341.
22. Gonçalves, L. D. R., Soares, M. R., Nogueira, F. C. S., Garcia, C. H. S., Camisasca, D. R., Domont, G., Feitosa, A. C. R., Pereira, D. A., Zingali, R. B., &, Alves, G., (2011) Analysis of the salivary proteome in gingivitis patients. Journal of Periodontal Research 46, 599-606.
23. Good, D. M., Thongboonkerd, V., Novak, J., Bascands, J. L., Schanstra, J. P., Coon, J. J., Dominiczak, A., &, Mischak, H., (2007) Body fluid proteomics for biomarker discovery: lessons from the past hold the key to success in the future. Journal of Proteome Research 6, 4549-4555.
24. Groenink, J., Walgreen-Weterings, E., Nazmi, K., Bolscher, J. G., Veerman, E. C., van Winkelhoff, A. J., &, Nieuw Amerongen, A. V., (1999) Salivary lactoferrin and low-Mr mucin MG2 in Actinobacillus actinomycetemcomitans-associated periodontitis. Journal of Clinical Periodontology 26, 269-275.
25. Guo, T., Rudnick, P. A., Wang, W., Lee, C. S., Devoe, D. L., &, Balgley, B. M., (2006) Characterization of the human salivary proteome by capillary isoelectric focusing/nanoreversed-phase liquid chromatography coupled with ESI-tandem MS. Journal of Proteome Research 5, 1469-1478.
26. Gursoy, U. K., Kononen, E., Huumonen, S., Tervahartiala, T., Pussinen, P. J., Suominen, A. L., &, Sorsa, T., (2013) Salivary type I collagen degradation end-products and related matrix metalloproteinases in periodontitis. Journal of Clinical Periodontology 40, 18-25.
27. Haigh, B. J., Stewart, K. W., Whelan, J. R. K., Barnett, M. P. G., Smolenski, G. A., &, Wheeler, T. T., (2010) Alterations in the salivary proteome associated with periodontitis. Journal of Clinical Periodontology 37, 241-247.
28. Hammer, E., Goritzka, M., Ameling, S., Darm, K., Steil, L., Klingel, K., Trimpert, C., Herda, L. R., Dorr, M., Kroemer, H. K., Kandolf, R., Staudt, A., Felix, S. B., &, Volker, U., (2011) Characterization of the human myocardial proteome in inflammatory dilated cardiomyopathy by label-free quantitative shotgun proteomics of heart biopsies. Journal of Proteome Research 10, 2161-2171.
29. Hensel, E., Gesch, D., Biffar, R., Bernhardt, O., Kocher, T., Splieth, C., Born, G., &, John, U., (2003) Study of Health in Pomerania (SHIP): a health survey in an East German region. Objectives and design of the oral health section. Quintessence International 34, 370-378.
30. Heo, S. H., Choi, Y. J., Lee, J. H., Lee, J. M., &, Cho, J. Y., (2011) S100A2 level changes are related to human periodontitis. Molecules and Cells 32, 445-450.
31. Herr, A. E., Hatch, A. V., Throckmorton, D. J., Tran, H. M., Brennan, J. S., Giannobile, W. V., &, Singh, A. K., (2007) Microfluidic immunoassays as rapid saliva-based clinical diagnostics. Proceedings of the National Academy of Sciences of the United States of America 104, 5268-5273.
32. Hu, S., Arellano, M., Boontheung, P., Wang, J., Zhou, H., Jiang, J., Elashoff, D., Wei, R., Loo, J. A., &, Wong, D. T., (2008) Salivary proteomics for oral cancer biomarker discovery. Clinical Cancer Research 14, 6246-6252.
33. Iwata, T., Kantarci, A., Yagi, M., Jackson, T., Hasturk, H., Kurihara, H., &, Van Dyke, T. E., (2009) Ceruloplasmin induces polymorphonuclear leukocyte priming in localized aggressive periodontitis. Journal of Periodontology 80, 1300-1306.
34. Jehmlich, N., Dinh, K. H., Gesell-Salazar, M., Hammer, E., Steil, L., Dhople, V. M., Schurmann, C., Holtfreter, B., Kocher, T., &, Volker, U., (2013) Quantitative analysis of the intra- and inter-subject variability of the whole salivary proteome. Journal of Periodontal Research 48, 392-403.
35. John, U., Greiner, B., Hensel, E., Ludemann, J., Piek, M., Sauer, S., Adam, C., Born, G., Alte, D., Greiser, E., Haertel, U., Hense, H. W., Haerting, J., Willich, S., &, Kessler, C., (2001) Study of Health In Pomerania (SHIP): a health examination survey in an east German region: objectives and design. Sozial- und Praeventivmedizin 46, 186-194.
36. de Jong, E. P., Xie, H., Onsongo, G., Stone, M. D., Chen, X. B., Kooren, J. A., Refsland, E. W., Griffin, R. J., Ondrey, F. G., Wu, B., Le, C. T., Rhodus, N. L., Carlis, J. V., &, Griffin, T. J., (2010) Quantitative proteomics reveals myosin and actin as promising saliva biomarkers for distinguishing pre-malignant and malignant oral lesions. PLoS ONE 5. doi: 10.1371/journal.pone.0011148.
37. Kido, J., Bando, M., Hiroshima, Y., Iwasaka, H., Yamada, K., Ohgami, N., Nambu, T., Kataoka, M., Yamamoto, T., Shinohara, Y., Sagawa, I., &, Nagata, T., (2012) Analysis of proteins in human gingival crevicular fluid by mass spectrometry. Journal of Periodontal Research 47, 488-499.
38. Kim, H. C., Kim, H. S., Moon, K. S. &, Cho, N. P., (2010) Detection of biomarkers for periodontal diseases using salivary proteomics. Korean Journal of Oral and Maxillofacial Pathology 34, 119-132.
39. Kingman, A., Susin, C., &, Albandar, J. M., (2008) Effect of partial recording protocols on severity estimates of periodontal disease. Journal of Clinical Periodontology 35, 659-667.
40. Kinney, J. S., Ramseier, C. A., &, Giannobile, W. V., (2007) Oral fluid-based biomarkers of alveolar bone loss in periodontitis. Annals of the New York Academy of Sciences 1098, 230-251.
41. Kornman, K. S., &, Duff, G. W., (2012) Personalized medicine: will dentistry ride the wave or watch from the beach? Journal of Dental Research 91, 8S-11S.
42. Lonnerdal, B., &, Iyer, S., (1995) Lactoferrin: molecular structure and biological function. Annual Review of Nutrition 15, 93-110.
43. Miller, C. S., King, C. P. Jr, Langub, M. C., Kryscio, R. J., &, Thomas, M. V., (2006) Salivary biomarkers of existing periodontal disease: a cross-sectional study. The Journal of the American Dental Association 137, 322-329.
44. Mirrielees, J., Crofford, L. J., Lin, Y., Kryscio, R. J., Dawson, D. R. 3rd, Ebersole, J. L., &, Miller, C. S., (2010) Rheumatoid arthritis and salivary biomarkers of periodontal disease. Journal of Clinical Periodontology 37, 1068-1074.
45. Mombelli, A., &, Meier, C., (2001) On the symmetry of periodontal disease. Journal of Clinical Periodontology 28, 741-745.
46. Ozmeric, N., (2004) Advances in periodontal disease markers. Clinica chimica acta 343, 1-16.
47. Pederson, E. D., Stanke, S. R., Whitener, S. J., Sebastiani, P. T., Lamberts, B. L., &, Turner, D. W., (1995) Salivary levels of alpha 2-macroglobulin, alpha 1-antitrypsin, C-reactive protein, cathepsin G and elastase in humans with or without destructive periodontal disease. Archives of Oral Biology 40, 1151-1155.
48. Rai, B., Kharb, S., Jain, R., &, Anand, S. C., (2008) Biomarkers of periodontitis in oral fluids. Journal of Oral Science 50, 53-56.
49. Ramseier, C. A., Kinney, J. S., Herr, A. E., Braun, T., Sugai, J. V., Shelburne, C. A., Rayburn, L. A., Tran, H. M., Singh, A. K., &, Giannobile, W. V., (2009) Identification of pathogen and host-response markers correlated with periodontal disease. Journal of Periodontology 80, 436-446.
50. Range, H., Leger, T., Huchon, C., Ciangura, C., Diallo, D., Poitou, C., Meilhac, O., Bouchard, P., &, Chaussain, C., (2012) Salivary proteome modifications associated with periodontitis in obese patients. Journal of Clinical Periodontology 39, 799-806.
51. Rao, P. V., Reddy, A. P., Lu, X., Dasari, S., Krishnaprasad, A., Biggs, E., Roberts, C. T., &, Nagalla, S. R., (2009) Proteomic identification of salivary biomarkers of type-2 diabetes. Journal of Proteome Research 8, 239-245.
52. Rathnayake, N., Akerman, S., Klinge, B., Lundegren, N., Jansson, H., Tryselius, Y., Sorsa, T., &, Gustafsson, A., (2013) Salivary biomarkers of oral health-a cross-sectional study. Journal of Clinical Periodontology 40, 140-147.
53. Reinhardt, R. A., Stoner, J. A., Golub, L. M., Lee, H. M., Nummikoski, P. V., Sorsa, T., &, Payne, J. B., (2010) Association of gingival crevicular fluid biomarkers during periodontal maintenance with subsequent progressive periodontitis. Journal of Periodontology 81, 251-259.
54. Shimizu, E., Kobayashi, T., Wakabayashi, H., Yamauchi, K., Iwatsuki, K., &, Yoshie, H., (2011) Effects of orally administered lactoferrin and lactoperoxidase-containing tablets on clinical and bacteriological profiles in chronic periodontitis patients. International Journal of Dentistry 2011, doi: 10.1155/2011/405139.
55. Sorsa, T., Tjaderhane, L., &, Salo, T., (2004) Matrix metalloproteinases (MMPs) in oral diseases. Oral Diseases 10, 311-318.
56. Streckfus, C. F., Arreola, D., Edwards, C., &, Bigler, L., (2012) Salivary protein profiles among her2/neu-receptor-positive and -negative breast cancer patients: Support for using salivary protein profiles for modeling breast cancer progression. Journal of Oncology 2012, doi: 10.1155/2012/413256.
57. Susin, C., Kingman, A., &, Albandar, J. M., (2005) Effect of partial recording protocols on estimates of prevalence of periodontal disease. Journal of Periodontology 76, 262-267.
58. Topkas, E., Keith, P., Dimeski, G., Cooper-White, J., &, Punyadeera, C., (2012) Evaluation of saliva collection devices for the analysis of proteins. Clinica Chimica Acta 413, 1066-1070.
59. Tsuchida, S., Satoh, M., Umemura, H., Sogawa, K., Kawashima, Y., Kado, S., Sawai, S., Nishimura, M., Kodera, Y., Matsushita, K., &, Nomura, F., (2012) Proteomic analysis of gingival crevicular fluid for discovery of novel periodontal disease markers. Proteomics 12, 2190-2202.
60. Voelzke, H., Alte, D., Schmidt, C. O., Radke, D., Lorbeer, R., Friedrich, N., Aumann, N., Lau, K., Piontek, M., Born, G., Havemann, C., Ittermann, T., Schipf, S., Haring, R., Baumeister, S. E., Wallaschofski, H., Nauck, M., Frick, S., Arnold, A., Junger, M., Mayerle, J., Kraft, M., Lerch, M. M., Dorr, M., Reffelmann, T., Empen, K., Felix, S. B., Obst, A., Koch, B., Glaser, S., Ewert, R., Fietze, I., Penzel, T., Doren, M., Rathmann, W., Haerting, J., Hannemann, M., Ropcke, J., Schminke, U., Jurgens, C., Tost, F., Rettig, R., Kors, J. A., Ungerer, S., Hegenscheid, K., Kuhn, J. P., Kuhn, J., Hosten, N., Puls, R., Henke, J., Gloger, O., Teumer, A., Homuth, G., Volker, U., Schwahn, C., Holtfreter, B., Polzer, I., Kohlmann, T., Grabe, H. J., Rosskopf, D., Kroemer, H. K., Kocher, T., Biffar, R., John, U., &, Hoffmann, W., (2011) Cohort profile: the study of health in Pomerania. International Journal of Epidemiology 40, 294-307.
61. Wakabayashi, H., Kondo, I., Kobayashi, T., Yamauchi, K., Toida, T., Iwatsuki, K., &, Yoshie, H., (2010) Periodontitis, periodontopathic bacteria and lactoferrin. BioMetals 23, 419-424.
62. World Health Organization (2008) ATC index with DDDs annually guidelines for ATC classification and DDD assignment. Oslo: WHO Collaborating Centre for drug Statistics Methodology.
63. Wu, Y., Shu, R., Luo, L. J., Ge, L. H., &, Xie, Y. F., (2009) Initial comparison of proteomic profiles of whole unstimulated saliva obtained from generalized aggressive periodontitis patients and healthy control subjects. Journal of Periodontal Research 44, 636-644.
64. Xie, H., Rhodus, N. L., Griffin, R. J., Carlis, J. V., &, Griffin, T. J., (2005) A catalogue of human saliva proteins identified by free flow electrophoresis-based peptide separation and tandem mass spectrometry. Molecular and Cellular Proteomics 4, 1826-1830.
65. Zhang, L., Henson, B. S., Camargo, P. M., &, Wong, D. T., (2009) The clinical value of salivary biomarkers for periodontal disease. Periodontology 2000 51, 25-37.
66. Zia, A., Khan, S., Bey, A., Gupta, N. D., &, Mukhtar-Un-Nisar, S., (2011) Oral biomarkers in the diagnosis and progression of periodontal diseases. Biology and Medicine 3, 45-52.