Oral Neutrophil Transcriptome Changes Result in a Pro-Survival Phenotype in Periodontal Diseases

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Lakschevitz, Flavia S ^a   Aboodi, Guy M ^a   Glogauer, Michael ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

ADULT; ARTICLE; BLOOD SAMPLING; CHRONIC PERIODONTITIS; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE SEQUENCE; HUMAN; LEUKOCYTE MIGRATION; MALE; MICROANALYSIS; MOUTH CAVITY; MOUTH EXAMINATION; NEUTROPHIL; NUCLEOTIDE SEQUENCE; PHENOTYPE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SURVIVAL RATE; UPREGULATION; WESTERN BLOTTING;

APOPTOSIS; CELL MOVEMENT; CHRONIC PERIODONTITIS; DOWN-REGULATION; FEMALE; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; MOUTH; NEUTROPHILS; PERIODONTIUM; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-BCL-2; TRANSCRIPTOME; UP-REGULATION;

EID: 84880073932     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068983     Document Type: Article

References (64)

1. Graves D, (2008) Cytokines that promote periodontal tissue destruction. Journal of Periodontology 79: 1585-1591 doi:10.1902/jop.2008.080183.
2. Guentsch A, Puklo M, Preshaw PM, Glockmann E, Pfister W, et al. (2009) Neutrophils in chronic and aggressive periodontitis in interaction with Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans. J Periodontal Res 44: 368-377 doi:10.1111/j.1600-0765.2008.01113.x.
3. Taba M Jr, Kinney J, Kim AS, Giannobile WV, (2005) Diagnostic Biomarkers for Oral and Periodontal Diseases. Dental Clinics of North America 49: 551-571 doi:10.1016/j.cden.2005.03.009.
4. Offenbacher S, Barros SP, Beck JD, (2008) Rethinking Periodontal Inflammation. Journal of Periodontology 79: 1577-1584 doi:10.1902/jop.2008.080220.
5. Hernández M, Gamonal J, Tervahartiala T, Mäntylä P, Rivera O, et al. (2010) Associations Between Matrix Metalloproteinase-8 and-14 and Myeloperoxidase in Gingival Crevicular Fluid From Subjects With Progressive Chronic Periodontitis: A Longitudinal Study. Journal of Periodontology 81: 1644-1652 doi:10.1902/jop.2010.100196.
6. van Dyke TE, (2007) Control of inflammation and periodontitis. Periodontol 2000 45: 158-166 doi:10.1111/j.1600-0757.2007.00229.x.
7. Hart TC, Shapira L, Van Dyke T (1994) Neutrophil defects as risk factors for periodontal diseases. J Periodontology: 521-529.
8. Aboodi GM, Goldberg MB, Glogauer M, (2011) Refractory Periodontitis Population Characterized by a Hyperactive Oral Neutrophil Phenotype. Journal of Periodontology 82: 726-733 doi:10.1902/jop.2010.100508.
9. Bender JS, Thang H, Glogauer M, (2006) Novel rinse assay for the quantification of oral neutrophils and the monitoring of chronic periodontal disease. J Periodontal Res 41: 214-220 Available: http://doi.wiley.com/10.1111/j.1600-0765.2005.00861.x.
10. Allen EM, Matthews JB, O Halloran DJ, Griffiths HR, Chapple IL, (2011) Oxidative and inflammatory status in Type 2 diabetes patients with periodontitis. J Clin Periodontol 38: 894-901 doi:10.1111/j.1600-051X.2011.01764.x.
11. Dias IHK, Matthews JB, Chapple ILC, Wright HJ, Dunston CR, et al. (2010) Activation of the neutrophil respiratory burst by plasma from periodontitis patients is mediated by pro-inflammatory cytokines. J Clin Periodontol 38: 1-7 doi:10.1111/j.1600-051X.2010.01628.x.
12. Chaussabel D, Pascual V, Banchereau J, (2010) Assessing the human immune system through blood transcriptomics. BMC Biol 8: 1-14 doi:-10.1186/1741-7007-8-84.
13. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Statistical applications in genetics and molecular biology 3: 1-26.
14. Reynier F, Pachot A, Paye M, Xu Q, Turrel-Davin F, et al. (2010) Specific gene expression signature associated with development of autoimmune type-I diabetes using whole-blood microarray analysis. Genes Immun 11: 269-278 doi:10.1038/gene.2009.112.
15. Allantaz F, Chaussabel D, Stichweh D, Bennett L, Allman W, et al. (2007) Blood leukocyte microarrays to diagnose systemic onset juvenile idiopathic arthritis and follow the response to IL-1 blockade. Journal of Experimental Medicine 204: 2131-2144 doi:10.1084/jem.20070070.
16. Chaussabel D, Quinn C, Shen J, Patel P, Glaser C, et al. (2008) A Modular Analysis Framework for Blood Genomics Studies: Application to Systemic Lupus Erythematosus. Immunity 29: 150-164 doi:10.1016/j.immuni.2008.05.012.
17. Papapanou PN, Abron A, Verbitsky M, Picolos D, Yang J, et al. (2004) Gene expression signatures in chronic and aggressive periodontitis: a pilot study. Eur J Oral Sci 112: 216-223 doi:10.1111/j.1600-0722.2004.00124.x.
18. Demmer RT, Behle JH, Wolf DL, Handfield M, Kebschull M, et al. (2008) Transcriptomes in Healthy and Diseased Gingival Tissues. Journal of Periodontology 79: 2112-2124 doi:10.1902/jop.2008.080139.
19. Kubota T, Morozumi T, Shimizu K, Sugita N, Kobayashi T, et al. (2001) Differential gene expression in neutrophils from patients with generalized aggressive periodontitis. J Periodont Res: 390-397.
20. Davanian H, Stranneheim H, Båge T, Lagervall M, Jansson L, et al. (2012) Gene Expression Profiles in Paired Gingival Biopsies from Periodontitis-Affected and Healthy Tissues Revealed by Massively Parallel Sequencing. PLoS ONE 7: e46440 doi:10.1371/journal.pone.0046440.t005.
21. Wright HJ, Matthews JB, Chapple ILC, Ling-Mountford N, Cooper PR, (2008) Periodontitis associates with a type 1 IFN signature in peripheral blood neutrophils. The Journal of Immunology 181: 5775-5784.
22. Covani U, Marconcini S, Giacomelli L, Sivozhelevov V, Barone A, et al. (2008) Bioinformatic Prediction of Leader Genes in Human Periodontitis. Journal of Periodontology 79: 1974-1983 doi:10.1902/jop.2008.080062.
23. Giannobile WV, Beikler T, Kinney JS, Ramseier CA, Morelli T, et al. (2009) Saliva as a diagnostic tool for periodontal disease: current state and future directions. Periodontol 2000 50: 52-64 doi:10.1111/j.1600-0757.2008.00288.x.
24. Lakschevitz FS, Aboodi GM, Glogauer M (2012) Oral Neutrophils Display a Site-Specific Phenotype Characterized by Expression of T-Cell Receptors. Journal of Periodontology: 1-12. doi:10.1902/jop.2012.120477.
25. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological): 289-300.
26. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Annals of statistics: 1165-1188.
27. Huang DW, Sherman BT, Lempicki RA, (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57 doi:10.1038/nprot.2008.211.
28. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868.
29. Zheng Q, Wang XJ, (2008) GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Research 36: W358-W363 doi:10.1093/nar/gkn276.
30. Chu VT, Gottardo R, Raftery AE, Bumgarner RE, Yeung K, (2008) MeV+R: using MeV as a graphical user interface for Bioconductor applications in microarray analysis. Genome Biol 9: R118 doi:10.1186/gb-2008-9-7-r118.
31. Atallah M, Krispin A, Trahtemberg U, Ben-Hamron S, Grau A, et al. (2012) Constitutive Neutrophil Apoptosis: Regulation by Cell Concentration via S100 A8/9 and the MEK - ERK Pathway. PLoS ONE 7: e29333 doi:10.1371/journal.pone.0029333.t001.
32. Wang Y, Inger M, Jiang H, Tenenbaum H, Glogauer M, (2013) CD109 Plays a Role in Osteoclastogenesis. PLoS ONE 8: e61213 doi:10.1371/journal.pone.0061213.
33. National Institute of Dental and Craniofacial Research. Periodontal Disease in Adults (age 20 to 64). Available: http://www.nidcr.nih.gov/datastatistics/finddatabytopic/gumdisease/periodontaldiseaseadults20to64.htm Accessed 01 May 2013.
34. Crawford JM, Wilton JM, Richardson P, (2000) Neutrophils die in the gingival crevice, periodontal pocket, and oral cavity by necrosis and not apoptosis. Journal of Periodontology 71: 1121-1129.
35. Renshaw SA, Loynes CA, Trushell DMI, Elworthy S, Ingham PW, et al. (2006) A transgenic zebrafish model of neutrophilic inflammation. Blood 108: 3976-3978 doi:10.1182/blood-2006-05-024075.
36. Kantarci A, Oyaizu K, van Dyke TE, (2003) Neutrophil-mediated tissue injury in periodontal disease pathogenesis: findings from localized aggressive periodontitis. Journal of Periodontology 74: 66-75 doi:10.1902/jop.2003.74.1.66.
37. van Dyke TE, Hoop GA, (1990) Neutrophil function and oral disease. Crit Rev Oral Biol Med 1: 117-133.
38. Sato EF, Higashino M, Ikeda K, Wake R, Matsuo M, et al. (2003) Oxidative stress-induced cell death of human oral neutrophils. Am J Physiol Cell Physiol 284: C1048-C1053 doi:10.1152/ajpcell.00016.2002.
39. Fredman G, Oh SF, Ayilavarapu S, Hasturk H, Serhan CN, et al. (2011) Impaired Phagocytosis in Localized Aggressive Periodontitis: Rescue by Resolvin E1. PLoS ONE 6: e24422 doi:10.1371/journal.pone.0024422.t001.
40. Zaric S, Shelburne C, Darveau R, Quinn DJ, Weldon S, et al. (2010) Impaired Immune Tolerance to Porphyromonas gingivalis Lipopolysaccharide Promotes Neutrophil Migration and Decreased Apoptosis. Infection and Immunity 78: 4151-4156 doi:10.1128/IAI.00600-10.
41. Matthews JB, Wright HJ, Roberts A, Cooper PR, Chapple ILC, (2006) Hyperactivity and reactivity of peripheral blood neutrophils in chronic periodontitis. Clinical & Experimental Immunology 147: 255-264 doi:10.1111/j.1365-2249.2006.03276.x.
42. Johnstone AM, Koh A, Goldberg MB, Glogauer M, (2007) A Hyperactive Neutrophil Phenotype in Patients With Refractory Periodontitis. Journal of Periodontology 78: 1788-1794 doi:10.1902/jop.2007.070107.
43. Nussbaum G, Shapira L, (2011) How has neutrophil research improved our understanding of periodontal pathogenesis? J Clin Periodontol 38: 49-59 doi:10.1111/j.1600-051X.2010.01678.x.
44. Scott DA, Krauss J, (2011) Neutrophils in Periodontal Inflammation. Neutrophils in periodontal inflammation. Frontiers of Oral Biology. Basel: KARGER, Vol. 15: 56-83 doi:10.1159/000329672.
45. Gamonal J, Sanz M, O'Connor A, Acevedo A, Suarez I, et al. (2003) Delayed neutrophil apoptosis in chronic periodontitis patients. J Clin Periodontol 30: 616-623.
46. Ariel A, Fredman G, Sun Y-P, Kantarci A, van Dyke TE, et al. (2006) Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nat Immunol 7: 1209-1216 doi:10.1038/ni1392.
47. Ottonello L, Montecucco F, Bertolotto M, Arduino N, Mancini M, et al. (2005) CCL3 (MIP-1α) induces in vitro migration of GM-CSF-primed human neutrophils via CCR5-dependent activation of ERK 1/2. Cellular Signalling 17: 355-363 doi:10.1016/j.cellsig.2004.08.002.
48. Assuma R, Oates T, Cochran D, Amar S, Graves D, (1998) IL-1 and TNF antagonists inhibit the inflammatory response and bone loss in experimental periodontitis. J Immunol 160: 403.
49. Suda T, Nakamura I, Jimi E, Takahashi N, (1997) Regulation of osteoclast function. J Bone Miner Res 12: 869-879 doi:10.1359/jbmr.1997.12.6.869.
50. Waris G, Ahsan H, (2006) Reactive oxygen species role in the development of cancer and various chronic conditions. J Carcinog 5: 14 doi:10.1186/1477-3163-5-14.
51. Haziot A, Tsuberi B-Z, Goyert SM, (1993) Neutrophil CD14: biochemical properties and role in the secretion of tumor necrosis factor-alpha in response to lipopolysaccharide. J Immunol 150: 5556-5565.
52. Christenson K, Bjorkman L, Karlsson J, Sundqvist M, Movitz C, et al. (2011) In vivo-transmigrated human neutrophils are resistant to antiapoptotic stimulation. Journal of Leukocyte Biology 90: 1055-1063 doi:10.1189/jlb.0111051.
53. Stefani FA, Viana MB, Dupim AC, Brito JAR, Gomez RS, et al. (2013) Expression, polymorphism and methylation pattern of interleukin-6 in periodontal tissues. Immunobiology: 1-6. doi:10.1016/j.imbio.2012.12.001.
54. Barnes TC, Anderson ME, Moots RJ, (2011) The Many Faces of Interleukin-6: The Role of IL-6 in Inflammation, Vasculopathy, and Fibrosis in Systemic Sclerosis. International Journal of Rheumatology 2011: 1-6 doi:10.1136/ard.2010.133587.
55. Biffl WL, Moore EE, Moore FA, Barnett CC, (1995) Interleukin-6 suppression of neutrophil apoptosis is neutrophil concentration dependent. Journal of Leukocyte Biology 58: 582-584.
56. Ishikawa F, Miyazaki S, (2005) New biodefense strategies by neutrophils. Arch Immunol Ther Exp (Warsz) 53: 226-233.
57. McCormack WJ, Parker AE, O'Neill LA, (2009) Toll-like receptors and NOD-like receptors in rheumatic diseases. Arthritis Res Ther 11: 243 doi:10.1186/ar2729.
58. Fransson M, Adner M, Erjefält J, Jansson L, Uddman R, et al. (2005) Up-regulation of Toll-like receptors 2, 3 and 4 in allergic rhinitis. Respir Res 6: 100 doi:10.1186/1465-9921-6-100.
59. Salomao R, Brunialti MKC, Gomes NE, Mendes ME, Diaz RS, et al. (2009) Toll-like receptor pathway signaling is differently regulated in neutrophils and peripheral mononuclear cells of patients with sepsis, severe sepsis, and septic shock*. Critical Care Medicine 37: 132-139 doi:10.1097/CCM.0b013e318192fbaf.
60. Hayashi F, (2003) Toll-like receptors stimulate human neutrophil function. Blood 102: 2660-2669 doi:10.1182/blood-2003-04-1078.
61. Chakravarti A, Raquil MA, Tessier P, Poubelle PE, (2009) Surface RANKL of Toll-like receptor 4-stimulated human neutrophils activates osteoclastic bone resorption. Blood 114: 1633-1644 doi:10.1182/blood-2008-09-178301.
62. Aliprantis AO, Yang R-B, Weiss DS, Godowski P, Zychlinsky A, (2000) The apoptotic signaling pathway activated by Toll-like receptor-2. Science Signaling 19: 3325.
63. Jablonska E, Garley M, (2010) TLRs and Bcl-2 family proteins in neutrophils of oral cavity cancer patients. Folia Histochemica et Cytobiologica 47: 615-619 doi:10.2478/v10042-008-0118-8.
64. Coldren CD, Nick JA, Poch KR, Woolum MD, Fouty BW, et al. (2006) Functional and genomic changes induced by alveolar transmigration in human neutrophils. AJP: Lung Cellular and Molecular Physiology 291: L1267-L1276 doi:10.1152/ajplung.00097.2006.