Mass spectrometric analyses of peptides and proteins in human gingival crevicular fluid

Journal of Proteome Research

Volumn 9, Issue 4, 2010, Pages 1683-1693

  Ngo, Luan H ^a   Veith, Paul D ^a   Chen, Yu Yen ^a   Chen, Dina ^a   Darby, Ivan B ^a   Reynolds, Eric C ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Gingival crevicular fluid proteome; Liquid chromatography mass spectrometry; Matrixassisted laser desorption ionization mass spectrometry; MS MS tandem mass spectrometry; Periodontal disease

Indexed keywords

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; FEMALE; GINGIVITIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; PEPTIDE ANALYSIS; PERIODONTAL DISEASE; PERIODONTAL EXAMINATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ADULT; ALPHA-DEFENSINS; AMINO ACID SEQUENCE; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GINGIVAL CREVICULAR FLUID; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PERIODONTAL DISEASES; PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 77950634380     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr900775s     Document Type: Article

References (82)

1. Socransky, S. S.; Haffajee, A. D.; Cugini, M. A.; Smith, C.; Kent, R. L., Jr. Microbial complexes in subgingival plaque J. Clin. Periodontol. 1998, 25, 134 - 144
2. Brecx, M. C.; Gautschi, M.; Gehr, P.; Lang, N. P. Variability of histologic criteria in clinically healthy human gingiva J. Periodontal Res. 1987, 22, 468 - 472
3. Koch, G.; Lindhe, J. The effect of supervised oral hygiene on the gingiva of children. The effect of toothbrushing Odontol. Revy. 1965, 16, 327 - 335
4. Lindhe, J.; Rylander, H. Experimental gingivitis in young dogs Scand. J. Dent. Res 1975, 83, 314 - 326
5. Mann, W. V. The correlation of gingivitis, pocket depth and exudate from the gingival crevice J. Periodontol. 1963, 34, 379 - 387
6. Egelberg, J. Gingival exudate measurements for evaluation of inflammatory changes of the gingiva Odontol. Revy. 1964, 15, 381 - 398
7. Egelberg, J. The topography and permeability of vessels at the dento-gingival junction in dogs J. Periodontal Res. Suppl. 1967, 1, 1 - 39
8. Cimasoni, G., Crevicular fluid updated. In Monographs in Oral Sciences, Karger: Basel, 1983; pp 45 - 102.
9. Embery, G.; Waddington, R. Gingival crevicular fluid: biomarkers of periodontal tissue activity Adv. Dent. Res. 1994, 8, 329 - 336
10. Fine, D. H.; Mandel, I. D. Indicators of periodontal disease activity: an evaluation J. Clin. Periodontol. 1986, 13, 533 - 546
11. Lamster, I. B.; Grbic, J. T. Diagnosis of periodontal disease based on analysis of the host response Periodontol. 2000 1995, 7, 83 - 99
12. Curtis, M. A.; Sterne, J. A.; Price, S. J.; Griffiths, G. S.; Coulthurst, S. K.; Wilton, J. M.; Johnson, N. W. 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
13. Estreicher, A.; Broggiato, A.; Duroux, P.; Andersen, E.; Cimasoni, G. Low molecular-weight proteins in human gingival crevicular fluid Arch. Oral Biol. 1996, 41, 733 - 738
14. Kojima, T.; Andersen, E.; Sanchez, J. C.; Wilkins, M. R.; Hochstrasser, D. F.; Pralong, W. F.; Cimasoni, G. Human gingival crevicular fluid contains MRP8 (S100A8) and MRP14 (S100A9), two calcium-binding proteins of the S100 family J. Dent. Res. 2000, 79, 740 - 747
15. Lundy, F. T.; Chalk, R.; Lamey, P. J.; Shaw, C.; Linden, G. J. Identification of MRP-8 (calgranulin A) as a major responsive protein in chronic periodontitis J. Pathol. 2000, 192, 540 - 544
16. Pisano, E.; Cabras, T.; Montaldo, C.; Piras, V.; Inzitari, R.; Olmi, C.; Castagnola, M.; Messana, I. Peptides of human gingival crevicular fluid determined by HPLC-ESI-MS Eur. J. Oral Sci. 2005, 113, 462 - 468
17. Adonogianaki, E.; Mooney, J.; Kinane, D. F. Detection of stable and active periodontitis sites by clinical assessment and gingival crevicular acute-phase protein levels J. Periodontal Res. 1996, 31, 135 - 143
18. Chapple, I. L.; Garner, I.; Saxby, M. S.; Moscrop, H.; Matthews, J. B. Prediction and diagnosis of attachment loss by enhanced chemiluminescent assay of crevicular fluid alkaline phosphatase levels J. Clin. Periodontol. 1999, 26, 190 - 198
19. Eley, B. M.; Cox, S. W. Correlation between gingivain/gingipain and bacterial dipeptidyl peptidase activity in gingival crevicular fluid and periodontal attachment loss in chronic periodontitis patients. A 2-year longitudinal study J. Periodontol. 1996, 67, 703 - 716
20. Eley, B. M.; Cox, S. W. 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
21. Alpagot, T.; Bell, C.; Lundergan, W.; Chambers, D. W.; Rudin, R. Longitudinal evaluation of GCF MMP-3 and TIMP-1 levels as prognostic factors for progression of periodontitis J. Clin. Periodontol. 2001, 28, 353 - 359
22. Kinane, D. F.; Darby, I. B.; Said, S.; Luoto, H.; Sorsa, T.; Tikanoja, S.; Mantyla, P. Changes in gingival crevicular fluid matrix metalloproteinase-8 levels during periodontal treatment and maintenance J. Periodontal Res. 2003, 38, 400 - 404
23. Teng, Y. T.; Sodek, J.; McCulloch, C. A. Gingival crevicular fluid gelatinase and its relationship to periodontal disease in human subjects J. Periodontal Res. 1992, 27, 544 - 552
24. Talonpoika, J. T.; Hamalainen, M. M. Type I collagen carboxyterminal telopeptide in human gingival crevicular fluid in different clinical conditions and after periodontal treatment J. Clin. Periodontol. 1994, 21, 320 - 326
25. Palys, M. D.; Haffajee, A. D.; Socransky, S. S.; Giannobile, W. V. Relationship between C-telopeptide pyridinoline cross-links (ICTP) and putative periodontal pathogens in periodontitis J. Clin. Periodontol. 1998, 25, 865 - 871
26. Jepsen, S.; Springer, I. N.; Buschmann, A.; Hedderich, J.; Acil, Y. Elevated levels of collagen cross-link residues in gingival tissues and crevicular fluid of teeth with periodontal disease Eur. J. Oral Sci. 2003, 111, 198 - 202
27. Nakashima, K.; Giannopoulou, C.; Andersen, E.; Roehrich, N.; Brochut, P.; Dubrez, B.; Cimasoni, G. A longitudinal study of various crevicular fluid components as markers of periodontal disease activity J. Clin. Periodontol. 1996, 23, 832 - 838
28. Lang, N. P.; Adler, R.; Joss, A.; Nyman, S. Absence of bleeding on probing. An indicator of periodontal stability J. Clin. Periodontol. 1990, 17, 714 - 721
29. Badersten, A.; Nilveus, R.; Egelberg, J. Scores of plaque, bleeding, suppuration and probing depth to predict probing attachment loss. 5 years of observation following nonsurgical periodontal therapy J. Clin. Periodontol. 1990, 17, 102 - 107 (Pubitemid 20078164)
30. Claffey, N.; Nylund, K.; Kiger, R.; Garrett, S.; Egelberg, J. Diagnostic predictability of scores of plaque, bleeding, suppuration and probing depth for probing attachment loss. 3 1/2 years of observation following initial periodontal therapy J. Clin. Periodontol. 1990, 17, 108 - 114 (Pubitemid 20078165)
31. Page, R. C.; Schroeder, H. E. Pathogenesis of inflammatory periodontal disease. A summary of current work Lab. Invest. 1976, 34, 235 - 249
32. Lobene, R. R.; Weatherford, T.; Ross, N. M.; Lamm, R. A.; Menaker, L. A modified gingival index for use in clinical trials Clin. Prev. Dent. 1986, 8, 3 - 6
33. Giannobile, W. V.; Riviere, G. R.; Gorski, J. P.; Tira, D. E.; Cobb, C. M. Glycosaminoglycans and periodontal disease: analysis of GCF by safranin O J. Periodontol. 1993, 64, 186 - 190
34. Nakashima, K.; Demeurisse, C.; Cimasoni, G. The recovery efficiency of various materials for sampling enzymes and polymorphonuclear leukocytes from gingival crevices J. Clin. Periodontol. 1994, 21, 479 - 483
35. Silness, J.; Loe, H. Periodontal Disease in Pregnancy. Ii. Correlation between Oral Hygiene and Periodontal Condtion Acta Odontol. Scand. 1964, 22, 121 - 135
36. Mortz, E.; Krogh, T. N.; Vorum, H.; Gorg, A. Improved silver staining protocols for high sensitivity protein identification using matrix-assisted laser desorption/ionization-time of flight analysis Proteomics 2001, 1, 1359 - 1363
37. Lundy, F. T.; Orr, D. F.; Shaw, C.; Lamey, P. J.; Linden, G. J. Detection of individual human neutrophil alpha-defensins (human neutrophil peptides 1, 2 and 3) in unfractionated gingival crevicular fluid? - ?a MALDI-MS approach Mol. Immunol. 2005, 42, 575 - 579
38. Pardi, A.; Zhang, X. L.; Selsted, M. E.; Skalicky, J. J.; Yip, P. F. NMR studies of defensin antimicrobial peptides. 2. Three-dimensional structures of rabbit NP-2 and human HNP-1 Biochemistry 1992, 31, 11357 - 11364
39. Agerberth, B.; Charo, J.; Werr, J.; Olsson, B.; Idali, F.; Lindbom, L.; Kiessling, R.; Jornvall, H.; Wigzell, H.; Gudmundsson, G. H. The human antimicrobial and chemotactic peptides LL-37 and alpha-defensins are expressed by specific lymphocyte and monocyte populations Blood 2000, 96, 3086 - 3093
40. Tao, R.; Jurevic, R. J.; Coulton, K. K.; Tsutsui, M. T.; Roberts, M. C.; Kimball, J. R.; Wells, N.; Berndt, J.; Dale, B. A. Salivary antimicrobial peptide expression and dental caries experience in children Antimicrob. Agents Chemother. 2005, 49, 3883 - 3888
41. Potempa, J.; Banbula, A.; Travis, J. Role of bacterial proteinases in matrix destruction and modulation of host responses Periodontol. 2000 2000, 24, 153 - 192
42. Karelin, A. A.; Philippova, M. M.; Ivanov, V. T. Proteolytic degradation of hemoglobin in erythrocytes leads to biologically active peptides Peptides 1995, 16, 693 - 697
43. Ivanov, V. T.; Karelin, A. A.; Philippova, M. M.; Nazimov, I. V.; Pletnev, V. Z. Hemoglobin as a source of endogenous bioactive peptides: the concept of tissue-specific peptide pool Biopolymers 1997, 43, 171 - 188
44. Mak, P.; Wojcik, K.; Silberring, J.; Dubin, A. Antimicrobial peptides derived from heme-containing proteins: hemocidins Antonie Van Leeuwenhoek 2000, 77, 197 - 207
45. Daoud, R.; Dubois, V.; Bors-Dodita, L.; Nedjar-Arroume, N.; Krier, F.; Chihib, N. E.; Mary, P.; Kouach, M.; Briand, G.; Guillochon, D. New antibacterial peptide derived from bovine hemoglobin Peptides 2005, 26, 713 - 719
46. Liepke, C.; Baxmann, S.; Heine, C.; Breithaupt, N.; Standker, L.; Forssmann, W. G. Human hemoglobin-derived peptides exhibit antimicrobial activity: a class of host defense peptides J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 2003, 791, 345 - 356
47. Mak, P.; Wojcik, K.; Wicherek, L.; Suder, P.; Dubin, A. Antibacterial hemoglobin peptides in human menstrual blood Peptides 2004, 25, 1839 - 1847
48. Mak, P.; Wicherek, L.; Suder, P.; Dubin, A.; Banas, T.; Kaim, I.; Klimek, M. Analysis of free hemoglobin level and hemoglobin peptides from human puerperal uterine secretions J. Soc. Gynecol. Invest. 2006, 13, 285 - 291
49. Richter, R.; Schulz-Knappe, P.; Schrader, M.; Standker, L.; Jurgens, M.; Tammen, H.; Forssmann, W. G. Composition of the peptide fraction in human blood plasma: database of circulating human peptides J. Chromatogr., B: Biomed. Sci. Appl. 1999, 726, 25 - 35
50. Tirumalai, R. S.; Chan, K. C.; Prieto, D. A.; Issaq, H. J.; Conrads, T. P.; Veenstra, T. D. Characterization of the low molecular weight human serum proteome Mol. Cell. Proteomics 2003, 2, 1096 - 1103
51. Koomen, J. M.; Li, D.; Xiao, L. C.; Liu, T. C.; Coombes, K. R.; Abbruzzese, J.; Kobayashi, R. Direct tandem mass spectrometry reveals limitations in protein profiling experiments for plasma biomarker discovery J. Proteome Res. 2005, 4, 972 - 981
52. Makinen, K. K.; Sewon, L.; Makinen, P. Analysis in gingival crevicular fluid of two oligopeptides derived from human hemoglobin beta-chain J. Periodontal Res. 1996, 31, 43 - 46
53. Murillo, L.; Piot, J. M.; Coitoux, C.; Fruitier-Arnaudin, I. Brain processing of hemorphin-7 peptides in various subcellular fractions from rats Peptides 2006
54. John, H.; Schulz, S.; Forssmann, W. G. Validated multi-component CZE-UV procedure for the quantification of human hemorphin LVV-H7 in plasma stability studies Anal. Bioanal. Chem. 2006, 386, 235 - 243
55. Dashper, S. G.; Cross, K. J.; Slakeski, N.; Lissel, P.; Aulakh, P.; Moore, C.; Reynolds, E. C. Hemoglobin hydrolysis and heme acquisition by Porphyromonas gingivalis Oral Microbiol. Immunol. 2004, 19, 50 - 56
56. Johnson, R. B.; Streckfus, C. F.; Dai, X.; Tucci, M. A. Protein recovery from several paper types used to collect gingival crevicular fluid J. Periodontal Res. 1999, 34, 283 - 289
57. Kido, J.; Kido, R.; Suryono; Kataoka, M.; Fagerhol, M. K.; Nagata, T. Induction of calprotectin release by Porphyromonas gingivalis lipopolysaccharide in human neutrophils Oral Microbiol. Immunol. 2004, 19, 182 - 187
58. Nisapakultorn, K.; Ross, K. F.; Herzberg, M. C. Calprotectin expression in vitro by oral epithelial cells confers resistance to infection by Porphyromonas gingivalis Infect. Immun. 2001, 69, 4242 - 4247
59. McLaughlin, W. S.; Kirkham, J.; Kowolik, M. J.; Robinson, C. Human gingival crevicular fluid keratin at healthy, chronic gingivitis and chronic adult periodontitis sites J. Clin. Periodontol. 1996, 23, 331 - 335
60. Huang, C. M. Comparative proteomic analysis of human whole saliva Arch. Oral. Biol. 2004, 49, 951 - 962
61. Saltel, F.; Destaing, O.; Bard, F.; Eichert, D.; Jurdic, P. Apatite-mediated actin dynamics in resorbing osteoclasts Mol. Biol. Cell 2004, 15, 5231 - 5241
62. Giannobile, W. V.; Lynch, S. E.; Denmark, R. G.; Paquette, D. W.; Fiorellini, J. P.; Williams, R. C. Crevicular fluid osteocalcin and pyridinoline cross-linked carboxyterminal telopeptide of type I collagen (ICTP) as markers of rapid bone turnover in periodontitis. A pilot study in beagle dogs J. Clin. Periodontol. 1995, 22, 903 - 910
63. Chang, K. M.; Lehrhaupt, N.; Lin, L. M.; Feng, J.; Wu-Wang, C. Y.; Wang, S. L. Epidermal growth factor in gingival crevicular fluid and its binding capacity in inflamed and non-inflamed human gingiva Arch. Oral Biol. 1996, 41, 719 - 724
64. Lundy, F. T.; Shaw, C.; McKinnell, J.; Lamey, P. J.; Linden, G. J. Calcitonin gene-related peptide in gingival crevicular fluid in periodontal health and disease J. Clin. Periodontol. 1999, 26, 212 - 216
65. Hirose, K.; Isogai, E.; Miura, H.; Ueda, I. Levels of Porphyromonas gingivalis Fimbriae and inflammatory cytokines in gingival crevicular fluid from adult human subjects Microbiol. Immunol. 1997, 41, 21 - 26
66. Petropoulos, G.; McKay, I. J.; Hughes, F. J. The association between neutrophil numbers and interleukin-1alpha concentrations in gingival crevicular fluid of smokers and non-smokers with periodontal disease J. Clin. Periodontol. 2004, 31, 390 - 395
67. 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
68. Yuan, Z. N.; Tolo, K.; Helgeland, K. Soluble Fc gamma receptors in periodontal lesions Oral Microbiol. Immunol. 1998, 13, 310 - 314
69. Zaiou, M.; Nizet, V.; Gallo, R. L. Antimicrobial and protease inhibitory functions of the human cathelicidin (hCAP18/LL-37) prosequence J. Invest. Dermatol. 2003, 120, 810 - 816
70. Turner, J.; Cho, Y.; Dinh, N. N.; Waring, A. J.; Lehrer, R. I. Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils Antimicrob. Agents Chemother. 1998, 42, 2206 - 2214
71. Nagaoka, I.; Tamura, H.; Hirata, M. An antimicrobial cathelicidin peptide, human CAP18/LL-37, suppresses neutrophil apoptosis via the activation of formyl-peptide receptor-like 1 and P2X7 J. Immunol. 2006, 176, 3044 - 3052
72. Wang, Y.; Griffiths, W. J.; Jornvall, H.; Agerberth, B.; Johansson, J. Antibacterial peptides in stimulated human granulocytes: characterization of ubiquitinated histone H1A Eur. J. Biochem. 2002, 269, 512 - 518
73. Brinkmann, V.; Reichard, U.; Goosmann, C.; Fauler, B.; Uhlemann, Y.; Weiss, D. S.; Weinrauch, Y.; Zychlinsky, A. Neutrophil extracellular traps kill bacteria Science 2004, 303, 1532 - 1535
74. Walz, A.; Stuhler, K.; Wattenberg, A.; Hawranke, E.; Meyer, H. E.; Schmalz, G.; Bluggel, M.; Ruhl, S. Proteome analysis of glandular parotid and submandibular-sublingual saliva in comparison to whole human saliva by two-dimensional gel electrophoresis Proteomics 2006, 6, 1631 - 1639
75. Hardt, M.; Thomas, L. R.; Dixon, S. E.; Newport, G.; Agabian, N.; Prakobphol, A.; Hall, S. C.; Witkowska, H. E.; Fisher, S. J. Toward defining the human parotid gland salivary proteome and peptidome: identification and characterization using 2D SDS-PAGE, ultrafiltration, HPLC, and mass spectrometry Biochemistry 2005, 44, 2885 - 2899
76. Hu, S.; Xie, Y.; Ramachandran, P.; Ogorzalek Loo, R. R.; Li, Y.; Loo, J. A.; Wong, D. T. Large-scale identification of proteins in human salivary proteome by liquid chromatography/mass spectrometry and two-dimensional gel electrophoresis-mass spectrometry Proteomics 2005, 5, 1714 - 1728
77. Vitorino, R.; Lobo, M. J.; Ferrer-Correira, A. J.; Dubin, J. R.; Tomer, K. B.; Domingues, P. M.; Amado, F. M. Identification of human whole saliva protein components using proteomics Proteomics 2004, 4, 1109 - 1115
78. Smith, Q. T.; Camp, S. J. Salivary amylase in crevicular fluid J. Clin. Periodontol. 1993, 20, 418 - 424
79. Hanioka, T.; Matsuse, R.; Shigemoto, Y.; Ojima, M.; Shizukuishi, S. Relationship between periodontal disease status and combination of biochemical assays of gingival crevicular fluid J. Periodontal Res. 2005, 40, 331 - 338
80. Lamster, I. B.; Hartley, L. J.; Vogel, R. I. 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
81. Armitage GC, Development of a Classification System for Periodontal Diseases and Conditions. Ann. Periodontol 1999, 4, 1 - 6.
82. Vitkov, L.; Klappacher, M.; Hannig, M.; Krautgartner, W. D. Extracellular neutrophil traps in periodontitis. J. Periodont. Res. 2009, 44, 664 - 672