Tannerella forsythia infection-induced calvarial bone and soft tissue transcriptional profiles.

Tannerella forsythia is associated with subgingival biofilms in adult periodontitis, although the molecular mechanisms contributing to chronic inflammation and loss of periodontal bone remain unclear. We examined changes in the host transcriptional profiles during a T. forsythia infection using a murine calvarial model of inflammation and bone resorption. Tannerella forsythia was injected into the subcutaneous soft tissue over calvariae of BALB/c mice for 3 days, after which the soft tissues and calvarial bones were excised. RNA was isolated and Murine GeneChip (Affymetrix, Santa Clara, CA) array analysis of transcript profiles showed that 3226 genes were differentially expressed in the infected soft tissues (P < 0.05) and 2586 genes were differentially transcribed in calvarial bones after infection. Quantitative real-time reverse transcription-polymerase chain reaction analysis of transcription levels of selected genes corresponded well with the microarray results. Biological pathways significantly impacted by T. forsythia infection in calvarial bone and soft tissue included leukocyte transendothelial migration, cell adhesion molecules (immune system), extracellular matrix-receptor interaction, adherens junction, and antigen processing and presentation. Histologic examination revealed intense inflammation and increased osteoclasts in calvariae compared with controls. In conclusion, localized T. forsythia infection differentially induces transcription of a broad array of host genes, and the profiles differ between inflamed soft tissues and calvarial bone.

[1]  H. Baker,et al.  Polymicrobial periodontal pathogen transcriptomes in calvarial bone and soft tissue. , 2011, Molecular oral microbiology.

[2]  H. Baker,et al.  Molecular characterization of Treponema denticola infection-induced bone and soft tissue transcriptional profiles. , 2010, Molecular oral microbiology.

[3]  H. Baker,et al.  Porphyromonas gingivalis infection-induced tissue and bone transcriptional profiles. , 2010, Molecular oral microbiology.

[4]  A. Watkinson.  Message from the Publisher , 2010 .

[5]  A. Biesbrock,et al.  Gingival transcriptome patterns during induction and resolution of experimental gingivitis in humans. , 2009, Journal of periodontology.

[6]  P. Pavlidis,et al.  Subgingival bacterial colonization profiles correlate with gingival tissue gene expression , 2009, BMC Microbiology.

[7]  M. Wirth,et al.  Validation of reference genes for qPCR studies on Caco-2 cell differentiation. , 2008, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[8]  H. Baker,et al.  Role of Porphyromonas gingivalis SerB in Gingival Epithelial Cell Cytoskeletal Remodeling and Cytokine Production , 2008, Infection and Immunity.

[9]  H. Baker,et al.  Beyond Good and Evil in the Oral Cavity: Insights into Host-Microbe Relationships Derived from Transcriptional Profiling of Gingival Cells , 2008, Journal of dental research.

[10]  T. Ogawa,et al.  Possible requirement of intercellular adhesion molecule-1 for invasion of gingival epithelial cells by Treponema medium. , 2007, Canadian journal of microbiology.

[11]  G. Hajishengallis,et al.  Toll-Like Receptor 2-Mediated Interleukin-8 Expression in Gingival Epithelial Cells by the Tannerella forsythia Leucine-Rich Repeat Protein BspA , 2007, Infection and Immunity.

[12]  P. Khatri,et al.  A systems biology approach for pathway level analysis. , 2007, Genome research.

[13]  J. Hillman,et al.  Identification of Tannerella forsythia antigens specifically expressed in patients with periodontal disease. , 2007, FEMS microbiology letters.

[14]  Purvesh Khatri,et al.  Onto-Tools: new additions and improvements in 2006 , 2007, Nucleic Acids Res..

[15]  Leo Tjäderhane,et al.  The role of matrix metalloproteinases in the oral environment , 2007, Acta odontologica Scandinavica.

[16]  Nayoung Kim,et al.  Critical Role of Methylglyoxal and AGE in Mycobacteria-Induced Macrophage Apoptosis and Activation , 2006, PloS one.

[17]  I. Ishikawa,et al.  Isolation and identification of a cytopathic activity in Tannerella forsythia. , 2006, Biochemical and biophysical research communications.

[18]  J. Izard,et al.  Tannerella forsythia, a periodontal pathogen entering the genomic era. , 2006, Periodontology 2000.

[19]  S. Socransky,et al.  Association of Eubacterium nodatum and Treponema denticola with human periodontitis lesions. , 2006, Oral microbiology and immunology.

[20]  H. Kuramitsu,et al.  Porphyromonas gingivalis Vesicles Enhance Attachment, and the Leucine-Rich Repeat BspA Protein Is Required for Invasion of Epithelial Cells by “Tannerella forsythia” , 2006, Infection and Immunity.

[21]  Jian Q. Feng,et al.  periostin Null Mice Exhibit Dwarfism, Incisor Enamel Defects, and an Early-Onset Periodontal Disease-Like Phenotype , 2005, Molecular and Cellular Biology.

[22]  T. Ogawa,et al.  Requirement for Intercellular Adhesion Molecule 1 and Caveolae in Invasion of Human Oral Epithelial Cells by Porphyromonas gingivalis , 2005, Infection and Immunity.

[23]  F. C. Gibson,et al.  Porphyromonas gingivalis Fimbria-Dependent Activation of Inflammatory Genes in Human Aortic Endothelial Cells , 2005, Infection and Immunity.

[24]  Giri Narasimhan,et al.  Distinct transcriptional profiles characterize oral epithelium‐microbiota interactions , 2005, Cellular microbiology.

[25]  Ashu Sharma,et al.  Tannerella forsythia-induced Alveolar Bone Loss in Mice Involves Leucine-rich-repeat BspA Protein , 2005, Journal of dental research.

[26]  M. Yoneda,et al.  Stimulation of growth of Porphyromonas gingivalis by cell extracts from Tannerella forsythia. , 2005, Journal of periodontal research.

[27]  Y. Izumi,et al.  Expression of Major Histocompatibility Complex Class II and CD80 by Gingival Epithelial Cells Induces Activation of CD4+ T Cells in Response to Bacterial Challenge , 2005, Infection and Immunity.

[28]  A. Hannigan,et al.  Soluble cell adhesion molecules in gingival crevicular fluid in periodontal health and disease. , 2004, Journal of periodontology.

[29]  S. Kashket,et al.  Glucose toxicity effect and accumulation of methylglyoxal by the periodontal anaerobe Bacteroides forsythus. , 2004, Anaerobe.

[30]  N. Tsuchida,et al.  Cloning of the Tannerella forsythensis (Bacteroides forsythus) siaHI gene and purification of the sialidase enzyme. , 2003, Journal of medical microbiology.

[31]  Seok-Woo Lee,et al.  The surface (S-) layer is a virulence factor of Bacteroides forsythus. , 2003, Microbiology.

[32]  H. Baker,et al.  Molecular Characterization of the Acute Inflammatory Response to Infections with Gram-Negative versus Gram-Positive Bacteria , 2003, Infection and Immunity.

[33]  A. Tanner,et al.  Cloning and expression of alpha-D-glucosidase and N-acetyl-beta-glucosaminidase from the periodontal pathogen, Tannerella forsythensis (Bacteroides forsythus). , 2003, Oral microbiology and immunology.

[34]  B. Berridge,et al.  Gene expression analysis of the acute phase response using a canine microarray. , 2003, Toxicological sciences : an official journal of the Society of Toxicology.

[35]  J. Tanaka,et al.  DNA microarray analysis of human gingival fibroblasts from healthy and inflammatory gingival tissues. , 2003, Biochemical and biophysical research communications.

[36]  G. Splitter,et al.  Microarray Analysis of mRNA Levels from RAW264.7 Macrophages Infected with Brucella abortus , 2003, Infection and Immunity.

[37]  H. Nakamura,et al.  Bacteroides forsythus hemagglutinin is inhibited by N-acetylneuraminyllactose. , 2002, Oral microbiology and immunology.

[38]  T. Salo,et al.  Collagenase-2 (MMP-8) and collagenase-3 (MMP-13) in adult periodontitis: molecular forms and levels in gingival crevicular fluid and immunolocalisation in gingival tissue. , 2002, Journal of clinical periodontology.

[39]  C. Li,et al.  Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[40]  T. Salo,et al.  The in vivo Expression of the Collagenolytic Matrix Metalloproteinases (MMP-2, -8, -13, and -14) and Matrilysin (MMP-7) in Adult and Localized Juvenile Periodontitis , 2000, Journal of dental research.

[41]  S. Ichinose,et al.  Novel Apoptosis-Inducing Activity inBacteroides forsythus: a Comparative Study with Three Serotypes of Actinobacillus actinomycetemcomitans , 2000, Infection and Immunity.

[42]  Pierre Casellas,et al.  Monitoring Cellular Responses to Listeria monocytogenes with Oligonucleotide Arrays* , 2000, The Journal of Biological Chemistry.

[43]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[44]  R. Genco,et al.  Cloning, Expression, and Sequencing of a Cell Surface Antigen Containing a Leucine-Rich Repeat Motif from Bacteroides forsythus ATCC 43037 , 1998, Infection and Immunity.

[45]  L. Kesavalu,et al.  Bone Resorption Caused by Three Periodontal Pathogens In Vivo in Mice Is Mediated in Part by Prostaglandin , 1998, Infection and Immunity.

[46]  R. Kent,et al.  Microbiota of health, gingivitis, and initial periodontitis. , 1998, Journal of clinical periodontology.

[47]  S. Socransky,et al.  Microbial complexes in subgingival plaque. , 1998, Journal of clinical periodontology.

[48]  T. Kato,et al.  Cloning, expression, and sequencing of a protease gene from Bacteroides forsythus ATCC 43037 in Escherichia coli , 1997, Infection and immunity.

[49]  J. Hayashi,et al.  Effects of cytokines and periodontopathic bacteria on the leukocyte function-associated antigen 1/intercellular adhesion molecule 1 pathway in gingival fibroblasts in adult periodontitis , 1994, Infection and immunity.

[50]  G. Mundy,et al.  Effects of interleukin-1 on bone turnover in normal mice. , 1989, Endocrinology.

[51]  D. Graves,et al.  Animal models to study host-bacteria interactions involved in periodontitis. , 2012, Frontiers of oral biology.

[52]  J. Enghild,et al.  A novel matrix metalloprotease-like enzyme (karilysin) of the periodontal pathogen Tannerella forsythia ATCC 43037 , 2010, Biological chemistry.

[53]  L. Bonewald,et al.  Periostin is essential for the integrity and function of the periodontal ligament during occlusal loading in mice. , 2008, Journal of periodontology.

[54]  P. Pavlidis,et al.  Transcriptomes in healthy and diseased gingival tissues. , 2008, Journal of periodontology.

[55]  N. Savage,et al.  Adhesion molecule expression in chronic inflammatory periodontal disease tissue. , 1994, Journal of periodontal research.