Gingival crevicular fluid proteomes in health, gingivitis and chronic periodontitis

Journal of Periodontal Research

Volumn 50, Issue 5, 2015, Pages 637-649

  Huynh, A H S ^a   Veith, P D ^a   Mcgregor, N R ^a   Adams, G G ^a   Chen, D ^a   Reynolds, E C ^a   Ngo, L H ^a   Darby, I B ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Gingival crevicular fluid; Liquid chromatography mass spectrometry; Periodontitis; Proteome

Indexed keywords

PROTEOME;

CHRONIC PERIODONTITIS; GINGIVITIS; HUMAN; MALE; PERIODONTAL INDEX;

CHRONIC PERIODONTITIS; GINGIVAL CREVICULAR FLUID; GINGIVITIS; HUMANS; MALE; PERIODONTAL INDEX; PROTEOME;

EID: 84940832138     PISSN: 00223484     EISSN: 16000765     Source Type: Journal    
DOI: 10.1111/jre.12244     Document Type: Article

References (108)

1. Griffiths GS. Formation, collection and significance of gingival crevice fluid. Periodontol 2000 2003;31:32-42.
2. Polson AM, Goodson JM. Periodontal diagnosis: current status and future needs. J Periodontol 1985;56:25-34.
3. Socransky S, Haffajee A, Goodson J, Lindhe J. New concepts of destructive periodontal disease. J Clin Periodontol 1984;11:21-32.
4. Egelberg J. Gingival exudate measurements for evaluation of inflammatory changes of the gingivae. Odontol Rev 1964;15:381-399.
5. Lindhe J, Rylander H. Experimental gingivitis in young dogs. Eur J Oral Sci 1975;83:314-326.
6. Mann WV. The correlation of gingivitis, pocket depth and exudate from the gingival crevice. J Periodont 1963;34:379-387.
7. Thunell D, Tymkiw K, Johnson G et al. A multiplex immunoassay demonstrates reductions in gingival crevicular fluid cytokines following initial periodontal therapy. J Periodontal Res 2010;45:148-152.
8. Teles RP, Sakellari D, Konstantinidis A, Socransky SS, Haffajee AD. Application of the checkerboard immunoblotting technique to the quantification of host biomarkers in gingival crevicular fluid. J Periodontol 2009;80:447-456.
9. Demmer RT, Behle JH, Wolf DL et al. Transcriptomes in healthy and diseased gingival tissues. J Periodontol 2008;79:2112-2124.
10. Lamster IB, Hartley LJ, Vogel RI. Development of a biochemical profile for gingival crevicular fluid: methodological considerations and evaluation of collagen-degrading and ground substance-degrading enzyme activity during experimental gingivitis. J Periodontol 1985;56:13-21.
11. Grant MM, Creese AJ, Barr G et al. Proteomic analysis of a noninvasive human model of acute inflammation and its resolution: the twenty-one day gingivitis model. J Proteome Res 2010;9:4732-4744.
12. Nakashima K, Roehrich N, Cimasoni G. Osteocalcin, prostaglandin E2 and alkaline phosphatase in gingival crevicular fluid: their relations to periodontal status. J Clin Periodontol 1994;21:327-333.
13. Nakashima K, Giannopoulou C, Andersen E et al. A longitudinal study of various crevicular fluid components as markers of periodontal disease activity. J Clin Periodontol 1996;23:832-838.
14. Uitto VJ, Overall CM, McCulloch C. Proteolytic host cell enzymes in gingival crevice fluid. Periodontology 2000;2003(31):77-104.
15. Eley B, Cox S. The relationship between gingival crevicular fluid cathepsin B activity and periodontal attachment loss in chronic periodontitis patients: a 2-year longitudinal study. J Periodontal Res 1996;31:381-392.
16. Magnusson I, Persson RG, Page RC et al. A multi-center clinical trial of a new chairside test in distinguishing between diseased and healthy periodontal sites. II. Association between site type and test outcome before and after therapy. J Periodontol 1996;67:589.
17. Teles R, Sakellari D, Teles F et al. Relationships among gingival crevicular fluid biomarkers, clinical parameters of periodontal disease, and the subgingival microbiota. J Periodontol 2010;81:89-98.
18. Ngo LH, Veith PD, Chen Y-Y, Chen D, Darby IB, Reynolds EC. Mass spectrometric analyses of peptides and proteins in human gingival crevicular fluid. J Proteome Res 2010;9:1683-1693.
19. Bostanci N, Heywood W, Mills K, Parkar M, Nibali L, Donos N. Application of label-free absolute quantitative proteomics in human gingival crevicular fluid by LC/MSE (gingival exudatome). J Proteome Res 2010;9:2191-2199.
20. Tsuchida S, Satoh M, Umemura H et al. Proteomic analysis of gingival crevicular fluid for discovery of novel periodontal disease markers. Proteomics 2012;12:2190-2202.
21. Oppenheim F. Preliminary observations on the presence and origin of serum albumin in human saliva. Helv Odontol Acta 1970;14:10.
22. Giannobile WV, Riviere GR, Gorski JP, Tira DE, Cobb CM. Glycosaminoglycans and periodontal disease: analysis of GCF by safranin O. J Periodontol 1993;64:186-190.
23. Suelter C, DeLuca M. How to prevent losses of protein by adsorption to glass and plastic. Anal Biochem 1983;135:112-119.
24. Guentsch A, Kramesberger M, Sroka A, Pfister W, Potempa J, Eick S. Comparison of gingival crevicular fluid sampling methods in patients with severe chronic periodontitis. J Periodontol 2011;82:1051-1060.
25. Curtis M, Griffiths G, Price S, Coulthurst S, Johnson N. The total protein concentration of gingival crevicular fluid. J Clin Periodontol 1988;15:628-632.
26. Curtis MA, Sterne JA, Price SJ et al. The protein composition of gingival crevicular fluid sampled from male adolescents with no destructive periodontitis: baseline data of a longitudinal study. J Periodontal Res 1990;25:6-16.
27. Domon B, Aebersold R. Mass spectrometry and protein analysis. Sci STKE 2006;312:212.
28. Pitt JJ. Principles and applications of liquid chromatography-mass spectrometry in clinical biochemistry. Clin Biochem Rev 2009;30:19.
29. Badersten A, Nilvéaus R, Egelberg J. Reproducibility of probing attachment level measurements. J Clin Periodontol 1984;11:475-485.
30. Lobene RR, Weatherford T, Ross NM, Lamm RA, Menaker L. A modified gingival index for use in clinical trials. Clin Prev Dent 1986;8:3-6.
31. Roberts-Thomson KF, Do L. Oral health status. In: Slade G, Spencer A, Roberts-Thomson K, eds. Australia's Dental Generations: The National Survey of Adult Oral Health 2004-06. Canberra Australian Institute of Health and Welfare (cat. no. DEN 165.), 2007:81-142.
32. Ebersole J, Machen R, Steffen M, Willmann D. Systemic acute-phase reactants, C-reactive protein and haptoglobin, in adult periodontitis. Clin Exp Immunol 1997;107:347-352.
33. Makela M, Salo T, Uitto V-J, Larjava H. Matrix metalloproteinases (MMP-2 and MMP-9) of the oral cavity: cellular origin and relationship to periodontal status. J Dent Res 1994;73:1397-1406.
34. Offenbacher S, Soskolne W, Collins J. Prostaglandins and other eicosanoids in gingival crevicular fluid as markers of periodontal disease susceptibility and activity. Risk Markers for Oral Diseases. 1991;3:313-337.
35. Heasman P, Collins J, Offenbacher S. Changes in crevicular fluid levels of interleukin-1β, leukotriene B4, prostaglandin E2, thromboxane B2 and tumour necrosis factor α in experimental gingivitis in humans. J Periodontal Res 1993;28:241-247.
36. Curtis MA, Gillett IR, Griffiths GS et al. Detection of high-risk groups and individuals for periodontal diseases: laboratory markers from analysis of gingival crevicular fluid. J Clin Periodontol 1989;16:1-11.
37. Silva-Boghossian CM, Colombo APV, Tanaka M, Rayo C, Xiao Y, Siqueira WL. Quantitative proteomic analysis of gingival crevicular fluid in different periodontal conditions. PLoS One 2013;8:e75898.
38. Short L, Zoellner H, Hunter N. Association of amyloid P protein with pathology in periodontal tissues. J Oral Pathol Med 1994;23:354-357.
39. Kinane DF, Preshaw PM, Loos BG. Host-response: understanding the cellular and molecular mechanisms of host-microbial interactions-Consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol 2011;38:44-48.
40. Alfano MC. The origin of gingival fluid. J Theor Biol 1974;47:127-136.
41. Pashley D. A mechanistic analysis of gingival fluid production. J Periodontal Res 1976;11:121-134.
42. Baliban RC, Sakellari D, Li Z, DiMaggio PA, Garcia BA, Floudas CA. Novel protein identification methods for biomarker discovery via a proteomic analysis of periodontally healthy and diseased gingival crevicular fluid samples. J Clin Periodontol 2012;39:203-212.
43. Carneiro LG, Venuleo C, Oppenheim FG, Salih E. Proteome data set of human gingival crevicular fluid from healthy periodontium sites by multidimensional protein separation and mass spectrometry. J Periodontal Res 2012;47:248-262.
44. Bostanci N, Ramberg P, Wahlander Å et al. Label-free quantitative proteomics reveals differentially regulated proteins in experimental gingivitis. J Proteome Res 2013;12:657-678.
45. Kido J-I, Bando M, Hiroshima Y et al. Analysis of proteins in human gingival crevicular fluid by mass spectrometry. J Periodontal Res 2012;47:488-499.
46. Tsuchida S, Satoh M, Sogawa K et al. Application of proteomic technologies to discover and identify biomarkers for periodontal diseases in gingival crevicular fluid: a review. Proteomics Clin Appl 2014;8:232-240.
47. Vitkov L, Klappacher M, Hannig M, Krautgartner WD. Neutrophil fate in gingival crevicular fluid. Ultrastruct Pathol 2010;34:25-30.
48. Chapple I. Reactive oxygen species and antioxidants in inflammatory diseases. J Clin Periodontol 1997;24:287-296.
49. Page RC, Schroeder HE. Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest 1976;34:235-249.
50. Wilson AG. Epigenetic regulation of gene expression in the inflammatory response and relevance to common diseases. J Periodontol 2008;79:1514-1519.
51. Berger SL. Histone modifications in transcriptional regulation. Curr Opin Genet Dev 2002;12:142-148.
52. Imai K, Ochiai K. Role of histone modification on transcriptional regulation and HIV-1 gene expression: possible mechanisms of periodontal diseases in AIDS progression. J Oral Sci 2011;53:1-13.
53. Foster SL, Medzhitov R. Gene-specific control of the TLR-induced inflammatory response. Clin Immunol 2009;130:7-15.
54. Kurita-Ochiai T, Fukushima K, Ochiai K. Volatile fatty acids, metabolic by-products of periodontopathic bacteria, inhibit lymphocyte proliferation and cytokine production. J Dent Res 1995;74:1367-1373.
55. Riggs M, Neumann R, Whittaker J, Ingram V. n-Butyrate causes histone modification in HeLa and Friend erythroleukaemia cells. Nature 1977;268:462-464.
56. Niederman R, Buyle-Bodin Y, Lu B-Y, Robinson P, Naleway C. Short-chain carboxylic acid concentration in human gingival crevicular fluid. J Dent Res 1997;76:575-579.
57. Hodin RA, Meng S, Archer S, Tang R. Cellular growth state differentially regulates enterocyte gene expression in butyrate-treated HT-29 cells. Cell Growth Differ 1996;7:647-653.
58. Axelsson P, Lindhe J. Effect of controlled oral hygiene procedures on caries and periodontal disease in adults. J Clin Periodontol 1978;5:133-151.
59. Herrera Abreu MT, Wang Q, Vachon E et al. Tyrosine phosphatase SHP-2 regulates IL-1 signaling in fibroblasts through focal adhesions. J Cell Physiol 2006;207:132-143.
60. Saba JA, McComb ME, Potts DL, Costello CE, Amar S. Proteomic mapping of stimulus-specific signaling pathways involved in THP-1 cells exposed to Porphyromonas gingivalis or its purified components. J Proteome Res 2007;6:2211-2221.
61. Bamburg JR, McGough A, Ono S. Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol 1999;9:364-370.
62. McLaughlin W, Kirkham J, Kowolik M, Robinson C. Human gingival crevicular fluid keratin at healthy, chronic gingivitis and chronic adult periodontitis sites. J Clin Periodontol 1996;23:331-335.
63. Moll R, Divo M, Langbein L. The human keratins: biology and pathology. Histochem Cell Biol 2008;129:705-733.
64. Sandholm L. Proteases and their inhibitors in chronic inflammatory periodontal disease. J Clin Periodontol 1986;13:19-26.
65. Niekrash CE, Patters MR. Simultaneous assessment of complement components C3, C4, and B and their cleavage products in human gingival fluid. J Periodontal Res 1985;20:260-267.
66. Patters M, Niekrash C, Lang N. Assessment of complement cleavage in gingival fluid during experimental gingivitis in man. J Clin Periodontol 1989;16:33-37.
67. Attströum R, Laurel AB, Lahsson U, Sjöuholm A. Complement factors in gingival crevice material from healthy and inflamed gingiva in humans. J Periodontal Res 1975;10:19-27.
68. Schenkein HA, Genco RJ. Gingival fluid and serum in periodontal diseases: II. Evidence for cleavage of complement components C3, C3 proactivator (Factor B) and C4 in gingival fluid. J Periodontol 1977;48:778-784.
69. Challacombe S, Shirlaw P. Immunology of diseases of the oral cavity. Mucosal immunology, 2nd edition. London: Academic Press, 1999:1313.
70. Cutler CW, Arnold RR, Schenkein HA. Inhibition of C3 and IgG proteolysis enhances phagocytosis of Porphyromonas gingivalis. J Immunol 1993;151:7016-7029.
71. Seppänen M, Lokki ML, Notkola IL et al. Complement and c4 null alleles in severe chronic adult periodontitis. Scand J Immunol 2007;65:176-181.
72. Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol 2012;10:717-725.
73. Slaney JM, Gallagher A, Aduse-Opoku J, Pell K, Curtis MA. Mechanisms of resistance of Porphyromonas gingivalis to killing by serum complement. Infect Immun 2006;74:5352-5361.
74. Hajishengallis G. Porphyromonas gingivalis-host interactions: open war or intelligent guerilla tactics? Microbes Infect 2009;11:637-645.
75. Hajishengallis G, Liang S, Payne MA et al. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 2011;10:497-506.
76. Potempa M, Potempa J, Kantyka T et al. Interpain A, a cysteine proteinase from Prevotella intermedia, inhibits complement by degrading complement factor C3. PLoS Pathog 2009;5:e1000316.
77. Gorr S-U, Abdolhosseini M. Antimicrobial peptides and periodontal disease. J Clin Periodontol 2011;38:126-141.
78. Lopatin DE, Caffesse ER, Bye F, Caffesse RG. Concentrations of fibronectin in the sera and crevicular fluid in various stages of periodontal disease. J Clin Periodontol 1989;16:359-364.
79. Wang PL, Azuma Y, Shinohara M, Ohura K. Effect of Actinobacillus actinomycetemcomitans protease on the proliferation of gingival epithelial cells. Oral Dis 2001;7:233-237.
80. Talonpoika J, Heino J, Larjava H, Hakkinen L, Paunio K. Gingival crevicular fluid fibronectin degradation in periodontal health and disease. Eur J Oral Sci 1989;97:415-421.
81. Kalfas S, Andersson M, Edwardsson S, Forsgren A, Naidu AS. Human lactoferrin binding to Porphyromonas gingivalis, Prevotella intermedia and Prevotella melaninogenica. Oral Microbiol Immunol 1991;6:350-355.
82. Wakabayashi H, Kondo I, Kobayashi T et al. Periodontitis, periodontopathic bacteria and lactoferrin. Biometals 2010;23:419-424.
83. Levay PF, Viljoen M. Lactoferrin: a general review. Haematologica 1995;80:252-267.
84. Goodson J, Tanner A, Haffajee A, Sornberger G, Socransky S. Patterns of progression and regression of advanced destructive periodontal disease. J Clin Periodontol 1982;9:472-481.
85. Pisano E, Cabras T, Montaldo C et al. Peptides of human gingival crevicular fluid determined by HPLC-ESI-MS. Eur J Oral Sci 2005;113:462-468.
86. Elkaim R, Werner S, Kocgozlu L, Tenenbaum H. P. gingivalis regulates the expression of Cathepsin B and Cystatin C. J Dent Res 2008;87:932-936.
87. Dommisch H, Vorderwülbecke S, Eberhard J, Steglich M, Jepsen S. SELDI-TOF-MS of gingival crevicular fluid-a methodological approach. Arch Oral Biol 2009;54:803-809.
88. Yoneyama T, Okamoto H, Lindhe J, Socransky S, Haffajee A. Probing depth, attachment loss and gingival recession. J Clin Periodontol 1988;15:581-591.
89. Armitage GC, Svanberc GK, Löe H. Microscopic evaluation of clinical measurements of connective tissue attachment levels. J Clin Periodontol 1977;4:173-190.
90. Puklo M, Guentsch A, Hiemstra P, Eick S, Potempa J. Analysis of neutrophil-derived antimicrobial peptides in gingival crevicular fluid suggests importance of cathelicidin LL-37 in the innate immune response against periodontogenic bacteria. Oral Microbiol Immunol 2008;23:328-335.
91. Lehrer RI, Lichtenstein AK, Ganz T. Defensins: antimicrobial and cytotoxic peptides of mammalian cells. Annu Rev Immunol 1993;11:105-128.
92. Brennan DS, Spencer AJ, Slade GD. Prevalence of periodontal conditions among public-funded dental patients in Australia. Aust Dent J 2001;46:114-121.
93. Sorsa T, Ingman T, Suomalainen K et al. Identification of proteases from periodontopathogenic bacteria as activators of latent human neutrophil and fibroblast-type interstitial collagenases. Infect Immun 1992;60:4491-4495.
94. Beklen A, Tüter G, Sorsa T et al. Gingival tissue and crevicular fluid co-operation in adult periodontitis. J Dent Res 2006;85:59-63.
95. Marcaccini AM, Meschiari CA, Zuardi LR et al. Gingival crevicular fluid levels of MMP-8, MMP-9, TIMP-2, and MPO decrease after periodontal therapy. J Clin Periodontol 2010;37:180-190.
96. Tsuchida S, Satoh M, Kawashima Y et al. Application of quantitative proteomic analysis using tandem mass tags for discovery and identification of novel biomarkers in periodontal disease. Proteomics 2013;13:2339-2350.
97. Golub LM, Kaplan R, Mulvihill JE, Ramamurthy N. Collagenolytic activity of crevicular fluid and of adjacent gingival tissue. J Dent Res 1979;58:2132-2136.
98. Fu H, Subramanian RR, Masters SC. 14-3-3 proteins: structure, function, and regulation. Annu Rev Pharmacol Toxicol 2000;40:617-647.
99. Hermeking H, Lengauer C, Polyak K et al. 14-3-3σ is a p53-regulated inhibitor of G2/M progression. Mol Cell 1997;1:3-11.
100. Wu Y, Shu R, Luo LJ, Ge LH, Xie YF. Initial comparison of proteomic profiles of whole unstimulated saliva obtained from generalized aggressive periodontitis patients and healthy control subjects. J Periodontal Res 2009;44:636-644.
101. Bertoldi C, Bellei E, Pellacani C et al. Non-bacterial protein expression in periodontal pockets by proteome analysis. J Clin Periodontol 2013;40:573-582.
102. Löe H, Ånerud Å, Boysen H, Smith M. The natural history of periodontal disease in man. J Periodontal Res 1978;13:550-562.
103. Ebersole J, Singer R, Steffensen B, Filloon T, Kornman K. Inflammatory mediators and immunoglobulins in GCF from healthy, gingivitis and periodontitis sites. J Periodontal Res 1993;28:543-546.
104. Holm-Peedersen P, Löe H. Flow of gingival exudate as related to menstruation and pregnancy. J Periodontal Res 1967;2:13-20.
105. Hugoson A. Gingival inflammation and female sex hormones. J Periodontal Res 1970;5:6-18.
106. Amar S, Chung KM. Influence of hormonal variation on the periodontium in women. Periodontol 2000 1994;6:79-87.
107. Grossi S, Genco R, Machtet E et al. Assessment of risk for periodontal disease. II. Risk indicators for alveolar bone loss. J Periodontol 1995;66:23-29.
108. Velden U. Probing force and the relationship of the probe tip to the periodontal tissues. J Clin Periodontol 1979;6:106-114.