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. 2020 Jun 4;6(6):e04022. doi: 10.1016/j.heliyon.2020.e04022

Table 1.

Proteomics studies of periodontal diseases.

Author (Year) Diagnosis Criteria Sample Number of Subjects Protein Analysis Main Findings
Marinho MC, et al. (2019) [11] CP with DM; PH with DM; CP without DM; PH without DM GCF 20 subjects (5 for each group) iTRAQ labeling;
LC-MS/MS
- There were 104 proteins exhibiting significant differences between the controlled and the diseased groups
Shin MS, et al. (2019) [12] P; H WUS 207 subjects (107 P, 100 H) LC MS/MS; ELISA - There were 744 proteins identified
- S100A8 and S100A9 were the highest total relative abundance proteins
Tang H, et al. (2019) [13] CP; G; PH WUS
GCF
BS
50 subjects (17 CP; 17 G; 16 PH) MALDI-TOF; Nano-LC/ESI-MS/MS - There were 91 peptides detected, seven of which showed significant differences between the CP and the PH group
- Fifty-eight peptide peaks were found in BC, 13 of which showed significant differences between the CP and the PH groups, 10 peaks exhibited significantly upregulated in G group
- Forty-eight peptide peaks were found in GCF, four of them were significantly higher in the CP group than in the PH group
- One hundred and thirteen salivary peptide peaks were detected in G groups, three of which were significantly different from the PH group
Bostanci N, et al. (2018) [14] CP; gAP; G; PH WUS 67 subjects in study group phase 1 (17 CP; 17 gAP, 17 gingivitis; 16 PH) and 82 subjects in study group phase 2 (21 CP; 21 gAP; 20 G; 20 PH) LFQ LC-MS/MS;
LC-SRM-MS
- One hundred an nineteen proteins significant difference between PH and disease subjects
- Five proteins with high predictive value for CP and gAP group (AUC >0.97);
Guzman YA, et al. (2018) [15] CP GCF 10 subjects before and after treatment LC-MS/MS - Azurocidin, lysozyme C, and myosin-9 as biomarkers candidate at baseline
- α-smooth muscle actin as biomarker candidate 13 weeks after treatment
Mertens B, et al. (2018) [16] CP; gAP; PH WUS 33 subjects (10 CP; 11 gAP, 12 PH) SDS-PAGE;
LC-MRM
- Hemopexin, plasminogen, and α-fibrinogen related to the presence of periodontitis compare with healthy subjects
- Apolipoprotein H was found higher in gAP compare with CP
Aboodi GM, et al. (2016) [17] Plaque-induced gingivitis WUS 5 healthy (experimental model) Oral neutrophil quantification; LC-ESI-MS/MS - Eighty-nine proteins showed significant level changes during experiment on gingivitis
- Neutrophil count in G has a moderate correlation with salivary β-globin, thioredoxin, and albumin
- Neutrophil count in G has a strong correlation with collagen α-1 and G protein–coupled receptor 98
Kerishnan JP, et al. (2016) [18] PH; mild CP; moderate CP; severe CP; gAP BS 90 subjects (42 PH; 9 mild CP; 12 moderate CP; 19 severe CP; 8 gAP) 2DE; MALDI-TOF/TOF; WB - Fourteen protein clusters identified
- α1-antitrypsin, haptoglobin, Ig κ chain C region, kininogen significantly expressed in all stages of periodontitis compare to normal subjects.
Bostanci N, et al. (2015) [19] Biofilm with red complex; Biofilm without red complex Gingival epithelial culture secretome Gingival epithelial culture LC MS/MS - One hundred and ninety-two proteins were quantified
- The red complex bacteria in the biofilm was responsible for down-regulated effect
- The upregulated proteins were associated with inflammation and apoptosis
- The down regulated ones were associated with the alteration of epithelial tissue robustness and disablement of tissue turnover
Trindade F, et al. (2015) [20] CP; PH WUS 9 CP; 10 PH Nano-HPLC-MALDI-TOF/TOF; Protease prediction carried out in silico with Proteasix; Slot blot - Protease prediction showed a different protease profiles in CP and H subjects
- Histatin-1 increased in CP subjects compare to PH subjects
- Eight peptides showed a specific association with CP
Monari E, et al. (2015) [21] CP; PH Periodontal pocket tissue 15 CP; 15 PH 2DE; LC MS/MS; Western blot - Thirty-two proteins identified
- Four proteins (S100A9, heat shock protein β1, galectin-7, and 14-3-3) were over-expressed in CP compared with PH subjects
Carneiro LG, et al. (2014) [22] PH; Moderate- severe P GCF 40 PH; 40 moderate-severe P LC-ESI-MS/MS; ICAT labeling; mTRAQ labeling; SDS-PAGE; ELISA - One hundred and eighty proteins were quantified in both groups
- Twenty six and 32 proteins were found only in PH and moderate-severe P subjects respectively
- Immunoglobulin A2, lactotransferrin, neutrophil defensin-1, myeloperoxidase, and S100A8 proteins were upregulated in moderate-severe P
- Fifty host proteins and 16 bacterial proteins were upregulated
Huynh AH, et al. (2014) [23] PH; G; CP GCF 15 PH; 15 G; 15 CP SDS-PAGE; LC-ESI-MS/MS - One hundred and twentyone proteins were detected, two-thirds of which were identified in all three groups
- Forty-two proteins were significant different according to specified criteria
Bertoldi C, et al. (2013) [24] Moderate-advance CP Pocket-associated and healthy tissues 25 subjects before and after osseous resective surgery 2DE; LC–MS/MS - Fifteen proteins were differently expressed between pathological and healthy tissues
- Annexin A2, actin cytoplasmic 1, carbonic anhydrase 1 & 2; Immunoglobulin κ chain C region and flavin reductase were upregulated in pathological condition
- Heat shock protein β-1, 14-3-3 proteins sigma and zeta/delta, triosephosphate isomerase, peroxiredoxin-1, fatty acid-binding protein-epidermal, and galectin-7 were downregulated in pathological
Tsuchida S, et al. (2013) [25] CP; PH GCF 31 CP; 16 PH LC–MS/MS Six hundred and nineteen proteins were identified
Silva-Boghossian CM, et al. (2013) [26] CP; PH GCF 5 CP; 5 PH LC–MS/MS PH subjects (145 proteins) and CP subjects consist of three probing depth sites: P (deep probing depth sites: 214 proteins), G (shallow probing depth sites with bleeding on probing: 154 proteins), and H (shallow sites without bleeding on probing: 133 proteins)
Salazar MG, et al. (2013) [27] P; H WSS 20 P; 20 H LC–MS/MS Three hundred and forty-four proteins identified
Bostanci N, et al. (2013) [28] G GCF 20 H (experimental model) LC–MS/MS Two hundred and fifty-four human proteins, 18 bacterial proteins
Tsuchida S, et al. (2012) [29] H; mild P; moderate P; severe P GCF 5 H; 3 mild P; 3 moderate P; 5 severe P 2DE; SDS-PAGE; LC–MS/MS Three hundred and twenty-seven proteins, including superoxide dismutase 1, apolipoprotein A-I and dermcidin were identified
Baliban RC, et al. (2012) [30] CP; PH GCF 12 CP; 12 PH LC-MS/MS - Four hundred and thirty-two human and 30 bacterial proteins were detected
- Angiotensinogen, clusterin, and thymidine phosphorylase found only in PH group
- Neutrophil defensin-1, carbonic anhydrase-1, and elongation factor-1 gamma were associated with CP
Kido J, et al. (2012) [31] PH; P GCF 1 PH; 8 P SDS-PAGE;
LC-MS/MS
Two hundred and thirty-one proteins detected; 64 proteins were found only in PH sites and 63 proteins were founded only in P sites.
Zhang J, et al. (2012) [32] OT-H; OT-P; P WUS 24 subjects (8 OT-H; 8 OT-P; 8 P) MALDI-TOF MS combined with magnetic bead; nano-LC/ESI-MS/MS - One hundred and nine protein mass peak detected
- There are nine intensities peak differ among three groups
Gonçalves Lda R, et al. (2011) [33] G; H WUS 10 G; 10 H 2DE; MALDI-TOF; LC-MS/MS - Ten proteins detected from 2DE and MALDI-TOF
- Twenty-four proteins detected from LC-MS/MS
Mizuno N, et al. (2011) [34] gAP Neutrophil 10 gAP with chemotaxis dysfunction; 10 gAP without dysfunction; 15 CP; 15 PH 2DE; MALDI-TOF - Lactoferrin, caldesmon, heat shock protein 70, and STAC showed a higher protein expression level in gAP with neutrophil dysfunction group than in the control group
- The caldesmon mRNA levels in neutrophils from gAP with chemotaxis dysfunction were upregulated compared with other groups
Choi YJ, et al. (2011) [35] CP GCF 12 CP; 11 PH SDS-PAGE; LC-MS/MS Three hundred and five proteins identified
Gonçalves Lda R, et al. (2010) [36] CP WUS 10 CP; 10 PH 2DE; MALDI-TOF; LC-MS/MS - Four proteins detected from 2DE and MALDI-TOF with different abundance among groups
- Twenty-seven proteins detected from LC-MS/MS
Haigh BJ, et al (2010) [37] Severe P WUS 9 severe P before and after 2DE; MALDI-TOF; LC-MS/MS - One hundred and twenty-eight proteins identified across all saliva samples
- Fifteen protein spots with altered abundance
Bostanci N, et al. (2010) [38] gAP; PH GCF 5 gAP; 5 PH LC-MS - One hundred and fifteen proteins identified in gAP and 88 proteins in PH group
- Four sources of origin were identified: human, bacterial, yeast, and virus
- L-plastin detected only in gAP and annexin-A1 was upregulated 5-fold in PH group
Ngo LH, et al. (2010) [39] CP; PH GCF 12 CP SDS-PAGE; MALDI-TOF; LC-MS/MS Sixty-six proteins were positively identified
Wu Y, et al. (2009) [40] gAP; PH WUS 5 gAP; 5 PH 2DE; LC-MS/MS Eleven proteins exhibited a different level between gAP and PH subjects

2DE: two dimensional electrophoresis; DM: diabetes mellitus; AUC: area under curve; BS: blood serum; CP: chronic periodontitis; ELISA: enzyme-linked immunosorbent assay; ESI: electrospray ionization; gAP: generalized aggressive periodontitis; GCF: gingival crevicular fluid; G: gingivitis; H: healthy; HPLC: high performance liquid chromatography; ICAT: isotope coded affinity tag; LC: liquid chromatography; LFQ: label-free quantitative; MALDI: matrix-assisted laser desorption/ionization; MRM: multiple-reaction monitoring; MS/MS: tandem mass spectrometry; mTRAQ: mass differential tags for relative and absolute quantification; P: periodontitis; PH: periodontally healthy; SDS-PAGE: sodium dodecyl sulfate-polyacrylamide gel electrophoresis; SRM: selected reaction monitoring; OT: orthodontic treatment; WB: western blot; WUS: whole unstimulated saliva; WSS: whole stimulated saliva.