Non-bacterial protein expression in periodontal pockets by proteome analysis

Journal of Clinical Periodontology

Volumn 40, Issue 6, 2013, Pages 573-582

  Bertoldi, Carlo ^a   Bellei, Elisa ^a   Pellacani, Chiara ^b   Ferrari, Davide ^a   Lucchi, Andrea ^b   Cuoghi, Aurora ^a   Bergamini, Stefania ^a   Cortellini, Pierpaolo ^c   Tomasi, Aldo ^a   Zaffe, Davide ^a   Monari, Emanuela ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b Private practice   (Italy)

^c European Research Group on Periodontology ERGOPerio   (Switzerland)

Author keywords

functionally related proteins; inflammation; intra bony defect; periodontal surgery; periodontitis; proteome analysis; risk factor

Indexed keywords

PROTEIN; PROTEOME;

ADULT; ALVEOLAR BONE LOSS; ARTICLE; CHEMISTRY; CHRONIC PERIODONTITIS; FEMALE; GENE EXPRESSION PROFILING; GENETICS; HUMAN; MALE; MASS SPECTROMETRY; METABOLISM; MIDDLE AGED; PERIODONTAL POCKET; PROTEIN SYNTHESIS; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ADULT; ALVEOLAR BONE LOSS; CHRONIC PERIODONTITIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MALE; MIDDLE AGED; PERIODONTAL POCKET; PROTEIN BIOSYNTHESIS; PROTEINS; PROTEOME; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; YOUNG ADULT;

EID: 84877575166     PISSN: 03036979     EISSN: 1600051X     Source Type: Journal    
DOI: 10.1111/jcpe.12050     Document Type: Article

References (72)

1. Alford, K. A., Glennie, S., Turrell, B. R., Rawlinson, L., Saklatvala, J., &, Dean, J. L., (2007) Heat shock protein 27 functions in inflammatory gene expression and transforming growth factor-beta-activated kinase-1 (TAK1)-mediated signaling. Journal of Biological Chemistry 282, 6232-6241.
2. Anderson, N. L., &, Anderson, N. G., (1998) Proteome and proteomics: new technologies, new concepts, and new words. Electrophoresis 19, 1853-1861.
3. Baliban, R. C., Sakellari, D., Li, Z., DiMaggio, P. A., Garcia, B. A., &, Floudas, C. A., (2012a) 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.
4. Baliban, R. C., Sakellari, D., Li, Z., Guzman, Y., Garcia, B. A., &, Floudas, C. A,. (2012b) Discovery of biomarker combinations that predict periodontal health or disease with high accuracy from GCF samples based on high-throughput proteomic analysis and mixed-integer linear optimization. Journal of Clinical Periodontology doi: 10.1111/jcpe.12037.
5. Bellei, E., Bergamini, S., Monari, E., Fantoni, L. I., Cuoghi, A., Ozben, T., &, Tomasi, A., (2011) High-abundance proteins depletion for serum proteomic analysis: concomitant removal of non-targeted proteins. Amino Acids 40, 145-156.
6. Bellei, E., Rossi, E., Lucchi, L., Uggeri, S., Albertazzi, A., Tomasi, A., &, Iannone, A., (2008) Proteomic analysis of early urinary biomarkers of renal changes in type 2 diabetic patients. Proteomics. Clinical Applications 2, 478-491.
7. Bertoldi, C., Bencivenni, D., Lucchi, A., &, Consolo, U., (2007) Augmentation of keratinized gingiva through bilaminar connective tissue grafts: a comparison between two techniques. Minerva Stomatologica 56, 3-20.
8. Bertoldi, C., Pellacani, C., Lalla, M., Consolo, U., Pinti, M., Cortellini, P., &, Cossarizza, A., (2012) Herpes Simplex I virus impairs regenerative outcomes of periodontal regenerative therapy in intrabony defects. A pilot study. Journal of Clinical Periodontology 39, 385-392.
9. Bradford, M. M., (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
10. Brownstein, C., Deora, A. B., Jacovina, A. T., Weintraub, R., Gertler, M., Khan, K. M., Falcone, D. J., &, Hajjar, K. A., (2004) Annexin II mediates plasminogen-dependent matrix invasion by human monocytes: enhanced expression by macrophages. Blood 103, 317-324.
11. 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.
12. Cáceres, M., Romero, A., Copaja, M., Dìaz-Araya, G., Martìnez, J., &, Smith, P. C., (2011) Simvastatin alters fibroblastic cell responses involved in tissue repair. Journal of Periodontal Research 46, 456-463.
13. Carnevale, G., (2007) Fibre retention osseous resective surgery: a novel conservative approach for pocket elimination. Journal of Clinical Periodontology 34, 182-187.
14. Carnevale, G., Cairo, F., &, Tonetti, M. S., (2007) Long-term effects of supportive therap in periodontal patients treated with fibre retention osseous resective surgery. I: recurrence of pockets, bleeding on probing and tooth loss. Journal of Clinical Periodontology 34, 334-341.
15. Chapple, I. L. C., (2009) Periodontal diagnosis and treatment-where does the future lie? Periodontology 2000 51, 9-24.
16. Chung, E., &, Rylander, M. N., (2012) Response of preosteoblasts to thermal stress conditioning and osteoinductive growth factors. Cell Stress and Chaperones 17, 203-214.
17. Demasi, A. P. D., Ceratti, D., Furuse, C., Cury, P., Junqueira, J. L., &, Araújo, V. C., (2007) Expression of peroxiredoxin I in plasma cells of oral inflammatory diseases. European Journal of Oral Sciences 115, 334-337.
18. Devasagayam, T. P. A., Tilak, J. C., Boloor, K. K., Sane Ketaki, S., GhaskadbiSaroj, S., &, Lele, R. D., (2004) Free Radicals and Antioxidants in Human Health: Current Status and Future Prospects. The Journal of the Association of Physicians of India 52, 794-804.
19. Ekuni, D., Firth, J. D., Nayer, T., Tomofuji, T., Sanbe, T., Irie, K., Yamamoto, T., Oka, T., Liu, Z., Vielkind, J., &, Putnins, E. E., (2009) Lipopolysaccharide-induced epithelial monoamine oxidase mediates alveolar bone loss in a rat chronic wound model. The American Journal of Pathology 175, 1398-1409.
20. Fleissig, Y., Reichenberg, E., Redlich, M., Zaks, B., Deutsch, O., Aframian, D. J., &, Palmon, A., (2010) Comparative proteomic analysis of human oral fluids according to gender and age. Oral Diseases 16, 831-838.
21. Flemmig, T. F., (1999) Periodontitis. Annals of. periodontology 4, 32-38.
22. Ford, P., Gemmell, E., Walker, P., West, M., Cullinan, M., &, Seymour, G., (2005) Characterization of heat shock protein-specific T cells in atherosclerosis. Clinical and Diagnostic Laboratory Immunology 12, 259-267.
23. Friedl, P., &, Wolf, K., (2009) Plasticity of cell migration: a multiscale tuning model. Journal of Cell Biology 188, 11-19.
24. Genetos, D. C., Wong, A., Watari, S., &, Yellowley, C. E., (2010) Hypoxia increases Annexin A2 expression in osteoblastic cells via VEGF and ERK. Bone 47, 1013-1019.
25. Da Rõs Gonçalves, L., Soares, M. R., Nogueira, F. C., Garcia, C., Camisasca, D. R., Domont, G., Feitosa, A. C., De Abreu Pereira, D., Zingali, R. B., &, Alves, G,. (2010) Comparative proteomic analysis of whole saliva from chronic periodontitis patients. Journal of Proteomics 73, 1334-1341.
26. Gorr, S.-U., (2009) Antimicrobial peptides of the oral cavity. Periodontology 2000 51, 152-180.
27. Gorr, S.-U., &, Abdolhosseini, M., (2011) Antimicrobial peptides and periodontal disease. Journal of Clinical Periodontology 38 (Suppl. 11), 126-141.
28. Grant, M. M., Creese, A. J., Barr, G., Ling, M. R., Scott, A. E., Matthews, J. B., Griffiths, H. R., Cooper, H. J., &, Chapple, I. L., (2010) Proteomic analysis of a noninvasive human model of acute inflammation and its resolution: the twenty-one day gingivitis model. Journal of Proteome Research 9, 4732-4744.
29. Guezguez, B., Vigneron, P., Lamerant, N., Kieda, C., Jaffredo, T., &, Dunon, D., (2007) Dual role of melanoma cell adhesion molecule (MCAM)/CD146 in lymphocyte endothelium interaction: MCAM/CD146 promotes rolling via microvilli induction in lymphocyte and is an endothelial adhesion receptor. The Journal of Immunology 179, 6673-6685.
30. 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.
31. Hand, D. J., &, Taylor, C. C,. (1987) Multivariate analysis of variance and repeated measures. London: Chapman and Hall, 1-456.
32. Hronik-Tupaj, M., Rice, W. L., Cronin-Golomb, M., Kaplan, D. L., &, Georgakoudi, I., (2011) Osteoblastic differentiation and stress response of human mesenchymal stem cells exposed to alternating current electric fields. Biomedical Engineering Online 10, 1-22.
33. Hu, S., Li, Y., Wang, J., Xie, Y., Tjon, K., Wolinsky, L., Loo, R. R., Loo, J. A., &, Wong, D. T., (2006) Human saliva proteome and transcriptome. Journal of Dental Research 85, 1129-1133.
34. Huang, R-Y., Lu, S-H., Su, K-W., Chen, J-K., Fang, W-H., Liao, W-N., Chen, S-Y., &, Shieh, Y-S,. (2012) Diacerein: A potential therapeutic drug for periodontal disease. Medical Hypotheses 79, 165-167.
35. Jönsson, D., Ramberg, P., Demmer, R. T., Kebschull, M., Dahlén, G., &, Papapanou, P. N., (2011) Gingival tissue transcriptomes in experimental gingivitis. Journal of Clinical Periodontology 38, 599-611.
36. Kato, K., Adachi, S., Matsushima-Nishiwaki, R., Minamitani, C., Natsume, H., Katagiri, Y., Hirose, Y., Mizutani, J., Tokuda, H., Kozawa, O., &, Otsuka, T., (2011) Regulation by heat shock protein 27 of osteocalcin synthesis in osteoblasts. Endocrinology 152, 1872-1882.
37. Kebschull, M., &, Papapanou, P. N., (2011) Periodontal microbial complexes associated with specific cell and tissue responses. Journal of Clinical Periodontology 38 (Suppl. 11), 17-27.
38. Kinane, D. F., Preshaw, P. M., &, Loos, B. G., (2011) Host-response: understanding the cellular and molecular mechanisms of host-microbial interactions-consensus of the Seventh European Workshop on Periodontology. Journal of Clinical Periodontology 38 (Suppl. 11), 44-48.
39. Kornman, K. S., (2008) Mapping the Pathogenesis of Periodontitis: A New Look. Journal of Periodontology 79, 1560-1568.
40. Koromantzos, P. A., Makrilakis, K., Dereka, X., Offenbacher, S., Katsilambros, N., Vrotsos, I. A., &, Madianos, P. N., (2012) Effect of non-surgical periodontal therapy on C-reactive protein, oxidative stress, and matrix metalloproteinase (MMP)-9 and MMP-2 levels in patients with type 2 diabetes: a randomized controlled study. Journal of Periodontology 83, 3-10.
41. Leonardi, R., Villari, L., Caltabiano, M., &, Travali, S., (2001) Heat shock protein 27 expression in the epithelium of periapical lesions. Journal of Endodontics 27, 89-92.
42. Luan, X., Dangaria, S., Ito, Y., Walker, C. G., Jin, T., Schmidt, M. K., Galang, M. T., &, Druzinsky, R. J., (2009) Neural crest lineage segregation: a blueprint for periodontal regeneration. Journal of Dental Research 88, 781-791.
43. Maier, S. M., Scherer, S. J., Seifert, M., Hanselmann, R. G., Schleehuber, Y., Edelmann, L., Reichrath, J., Krohne, G., &, Resche, r U., Seidl, W., Mutschler, W., Claes, L., Welter, C., &, Schartl, M., (2007) 1[alpha],25-dihydroxyvitamin D(3) enhances annexin II dependent proliferation of osteoblasts. Journal of Cellular Biochemistry 100, 679-692.
44. McCulloch, C. A., (2006) Proteomics for the periodontium: current strategies and future promise. Periodontology 2000 40, 173-183.
45. Mitsuhashi, M., Yamaguchi, M., Kojima, T., Nakajima, R., &, Kasai, K., (2011) Effects of HSP70 on the compression force-induced TNF-α and RANKL expression in human periodontal ligament cells. Inflammation Research 60, 187-194.
46. Mizuno, N., Niitani, M., Shiba, H., Iwata, T., Hayashi, I., Kawaguchi, H., &, Kurihara, H., (2011) Proteome analysis of proteins related to aggressive periodontitis combined with neutrophil chemotaxis dysfunction. Journal of Clinical Periodontology 38, 310-317.
47. Orosz, F., Olah, J., &, Ovadi, J., (2009) Triosephosphateisomerase deficiency: new insights into an enigmatic disease. Biochimica et Biophysica Acta 1792, 1168-1174.
48. Page, R. C., &, Eke, P. I., (2007) Case definitions for use in population-based surveillance of periodontitis. Journal of Periodontology 78 (Suppl. 7), 1387-1399.
49. Page, R. C., &, Kornman, K. S., (1997) The pathogenesis of human periodontitis: An introduction. Periodontology 2000 14, 9-11.
50. Page, R. C., &, Schroeder, H. E., (1976) Pathogenesis of inflammatory periodontal disease. A summary of current work. Laboratory Investigation 34, 235-249.
51. Park, J.-H., Yoon, J.-H., Lim, Y.-S., Hwang, H.-K., Kim, S.-A., Ahn, S.-G., &, Yoon, J.-H., (2010) TAT-Hsp27 promotes adhesion and migration of murine dental papilla-derived MDPC-23 cells through beta1 integrin-mediated signaling. International Journal of Molecular Medicine 26, 373-378.
52. Pham, T. K., Roy, S., Noirel, J., Douglas, I., Wright, P. C., &, Stafford, G. P., (2010) A quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia. Proteomics 10, 3130-3141.
53. Polla, B. S., &, Cossarizza, A., (1996) Stress protein in inflammation. Experientia 77, 375-391.
54. Puri, K. S., Suresh, K. R., Gogtay, N. J., &, Thatte, U. M., (2009) Declaration of Helsinki, 2008: implications for stakeholders in research. Journal of Postgraduate Medicine 55, 131-134.
55. R Development Core Team (2010) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 1-456.ISBN 3-900051-07-0, URL www.R-project.org.
56. Rangè, H., Lèger, 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.
57. Seymour, G. J., (1987) Possible mechanisms involved in the immunoregulation of chronic inflammatory periodontal disease. Journal of Dental Research 66, 2-9.
58. Shih, I. M., (1999) The role of CD146 (Mel-CAM) in biology and pathology. The Journal of Pathology 189, 4-11.
59. Socransky, S. S., &, Haffajee, A. D., (1999) The nature of periodontal disease. Annals of Periodontology 2, 3-10.
60. Sreedharan, R., Riordan, M., Thullin, G., Van Why, S., Siegel, N. J., &, Kashgarian, M., (2011) The maximal cytoprotective function of the heat shock protein 27 is dependent on heat shock protein 70. Biochimica et Biophysica Acta 1813, 129-135.
61. Swisher, J. F., Burton, N., Bacot, S. M., Vogel, S. N., &, Feldman, G. M., (2010) Annexin A2 tetramer activates human and murine macrophages through TLR4. Blood 115, 549-558.
62. Swisher, J. F., Khatri, U., &, Feldman, G. M., (2007) Annexin A2 is a soluble mediator of macrophage activation. Journal of Leukocyte Biology 82, 1174-1184.
63. Tergaonkar, V., (2006) NFkappaB pathway: a good signaling paradigm and therapeutic target. International Journal of Biochemistry Cell Biology 38, 1647-1653.
64. Tonetti, M. S., &, Claffey, N,. (2005) European Workshop in Periodontology group C. Advances in the progression of periodontitis and proposal of definitions of a periodontitis case and disease progression for use in risk factor research. Group C consensus report of the 5th European Workshop in Periodontology. Journal of Clinical Periodontology 32 (Suppl. 6), 210-213.
65. Tripodo, C., Di, Bernardo, &, A., Ternullo, M. P., Guarnotta, C., Porcasi, R., Ingrao, S., Gianelli, U., Boveri, E., Iannitto, E., Franco, G., &, Florena, A. M., (2009) CD146 + bone marrow osteoprogenitors increase in the advanced stages of primary myelofibrosis. Haematologica 94, 127-130.
66. Wolf, H. F., Rateitschak-Plüss, E. M., &, Rateitschak, K. H., (2005) Indici parodontali-PSR. In:, Wolf, H. F., Rateitschak-Plüss, E. M., &, Rateitschak, K. H., (eds). Parodontologia, (p. 73). Milano: Elsevier-Masson.
67. 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.
68. Yamamoto, T., Myokai, F., Nishimura, F., Ohira, T., Shiomi, N., Yamashiro, K., Arai, H., Murayama, Y., &, Takashiba, S., (2003) Gene profiling in human periodontal ligament fibroblasts by subtractive hybridization. Journal of Dental Research 82, 641-645.
69. Yamazaki, K., Ohsawa, Y., Tabeta, K., Ito, H., Ueki, K., Oda, T., Yoshie, H., &, Seymour, G. J., (2002) Accumulation of human heat shock protein 60-reactive T cells in the gingival tissues of periodontitis patients. Infection and Immunity 70, 2492-2501.
70. Yi, W., Sun, Y., Wei, X., Gu, C., Dong, X., Kang, X., Guo, S., &, Dou, K., (2010) Proteomic profiling of human bone marrow mesenchymal stem cells under shear stress. Molecular and cellular biochemistry 341, 9-16.
71. Yokoyama, T., Kobayashi, T., Yamamoto, K., Yamagata, A., Oofusa, K., &, Yoshie, H., (2010) Proteomic profiling of human neutrophils in relation to immunoglobulin G Fc receptor IIIb polymorphism. Journal of Periodontal Research 45, 780-787.
72. Yuan, K., Huang, J.-S., Hsu, C.-W., &, Hung, I.-J., (2007) A mineralization-associated membrane protein plays a role in the biological functions of the peptide-coated bovine hydroxyapatite. Journal of Periodontal Research 42, 420-428.