FOXO1 deletion reduces dendritic cell function and enhances susceptibility to periodontitis

American Journal of Pathology

Volumn 185, Issue 4, 2015, Pages 1085-1093

  Xiao, Wenmei ^a,b   Dong, Guangyu ^b   Pacios, Sandra ^b   Alnammary, Maher ^b   Barger, Laura A ^b   Wang, Yu ^b,c   Wu, Yingying ^b   Graves, Dana T ^b  

^a PEKING UNIVERSITY SCHOOL AND HOSPITAL OF STOMATOLOGY   (China)

^b UNIVERSITY OF PENNSYLVANIA SCHOOL OF DENTAL MEDICINE   (United States)

^c JILIN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN; CD51 ANTIGEN; CRE RECOMBINASE; GELATINASE A; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; OSTEOCLAST DIFFERENTIATION FACTOR; TRANSCRIPTION FACTOR FKHR; AUTACOID; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, MOUSE; GLYCOPROTEIN P 15095; MESSENGER RNA;

ALVEOLAR BONE LOSS; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BACTERIAL INFECTION; CELL ACTIVATION; CELL FUNCTION; CELL MIGRATION; CELL SURVIVAL; CERVICAL LYMPH NODE; CONNECTIVE TISSUE; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENETIC SUSCEPTIBILITY; GINGIVA; IMMUNOFLUORESCENCE; IN VITRO STUDY; LYMPH NODE; MOUSE; MOUTH INFECTION; NONHUMAN; OSTEOCLAST; OSTEOCLAST ACTIVITY; OSTEOCLASTOGENESIS; OSTEOLYSIS; PERIODONTITIS; PLASMA CELL; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; SPLEEN CELL; T LYMPHOCYTE; ADAPTIVE IMMUNITY; ANIMAL; CELL COUNT; CELL LINEAGE; COMPLICATION; DISEASE PREDISPOSITION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY;

ADAPTIVE IMMUNITY; ALVEOLAR BONE LOSS; ANIMALS; ANTIGENS, CD11C; CELL COUNT; CELL LINEAGE; CYTOKINES; DENDRITIC CELLS; DISEASE SUSCEPTIBILITY; FORKHEAD TRANSCRIPTION FACTORS; GENE DELETION; GINGIVA; INFLAMMATION MEDIATORS; LYMPH NODES; MICE; OSTEOCLASTS; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; RNA, MESSENGER;

EID: 84925310631     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.12.006     Document Type: Article

References (37)

1. B.J. Paster, I. Olsen, J.A. Aas, and F.E. Dewhirst The breadth of bacterial diversity in the human periodontal pocket and other oral sites Periodontol 2000 42 2006 80 87
2. G.P. Garlet Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints J Dent Res 89 2010 1349 1363
3. A. Cekici, A. Kantarci, H. Hasturk, and T.E. Van Dyke Inflammatory and immune pathways in the pathogenesis of periodontal disease Periodontol 2000 64 2014 57 80
4. L.N. Borrell, B.A. Burt, and G.W. Taylor Prevalence and trends in periodontitis in the USA: the [corrected] NHANES, 1988 to 2000 J Dent Res 84 2005 924 930
5. D.T. Graves, J. Li, and D.L. Cochran Inflammation and uncoupling as mechanisms of periodontal bone loss J Dent Res 90 2011 143 153
6. M.A. Curtis, C. Zenobia, and R.P. Darveau The relationship of the oral microbiotia to periodontal health and disease Cell Host Microbe 10 2011 302 306
7. M. Benakanakere, and D.F. Kinane Innate cellular responses to the periodontal biofilm Front Oral Biol 15 2012 41 55
8. D.T. Graves Cytokines that promote periodontal tissue destruction J Periodontol 79 2008 1585 1591
9. L.C. Hofbauer, S. Khosla, C.R. Dunstan, D.L. Lacey, W.J. Boyle, and B.L. Riggs The roles of osteoprotegerin and osteoprotegerin ligand in the paracrine regulation of bone resorption J Bone Miner Res 15 2000 2 12
10. R. Pacifici The immune system and bone Arch Biochem Biophys 503 2010 41 53
11. M. Alnaeeli, J. Park, D. Mahamed, J.M. Penninger, and Y.T. Teng Dendritic cells at the osteo-immune interface: implications for inflammation-induced bone loss J Bone Miner Res 22 2007 775 780
12. Y.Y. Kong, U. Feige, I. Sarosi, B. Bolon, A. Tafuri, S. Morony, C. Capparelli, J. Li, R. Elliott, S. McCabe, T. Wong, G. Campagnuolo, E. Moran, E.R. Bogoch, G. Van, L.T. Nguyen, P.S. Ohashi, D.L. Lacey, E. Fish, W.J. Boyle, and J.M. Penninger Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand Nature 402 1999 304 309
13. U.H. Lerner Inflammation-induced bone remodeling in periodontal disease and the influence of post-menopausal osteoporosis J Dent Res 85 2006 596 607
14. A. Beklen, M. Ainola, M. Hukkanen, C. Gürgan, T. Sorsa, and Y.T. Konttinen MMPs, IL-1, and TNF are regulated by IL-17 in periodontitis J Dent Res 86 2007 347 351
15. M. Arizon, I. Nudel, H. Segev, G. Mizraji, M. Elnekave, K. Furmanov, L. Eli-Berchoer, B.E. Clausen, L. Shapira, A. Wilensky, and A.H. Hovav Langerhans cells down-regulate inflammation-driven alveolar bone loss Proc Natl Acad Sci U S A 109 2012 7043 7048
16. Y. Wang, Y. Zhou, and D.T. Graves FOXO transcription factors: their clinical significance and regulation Biomed Res Int 2014 2014 925350
17. Y. Behl, M. Siqueira, J. Ortiz, J. Li, T. Desta, D. Faibish, and D.T. Graves Activation of the acquired immune response reduces coupled bone formation in response to a periodontal pathogen J Immunol 181 2008 8711 8718
18. J. Brown, H. Wang, J. Suttles, D.T. Graves, and M. Martin mTORC2 negatively regulates the toll-like receptor 4-mediated inflammatory response via FoxO1 J Biol Chem 286 2011 44295 44305
19. S. Li, G. Dong, A. Moschidis, J. Ortiz, M.R. Benakanakere, D.F. Kinane, and D.T. Graves P. Gingivalis modulates keratinocytes through FOXO transcription factors PLos One 8 2013 e78541
20. P. Chae, M. Im, F. Gibson, Y. Jiang, and D.T. Graves Mice lacking monocyte chemoattractant protein 1 have enhanced susceptibility to an interstitial polymicrobial infection due to impaired monocyte recruitment Infect Immun 70 2002 3164 3169
21. Q. Luan, T. Desta, L. Chehab, V.J. Sanders, J. Plattner, and D.T. Graves Inhibition of experimental periodontitis by a topical boron-based antimicrobial J Dent Res 87 2008 148 152
22. R. Liu, H.S. Bal, T. Desta, N. Krothapalli, M. Alyassi, Q. Luan, and D.T. Graves Diabetes enhances periodontal bone loss through enhanced resorption and diminished bone formation J Dent Res 85 2006 510 514
23. G. Schlecht, J. Mouries, M. Poitrasson-Riviere, C. Leclerc, and G. Dadaglio Purification of splenic dendritic cells induces maturation and capacity to stimulate Th1 response in vivo Int Immunol 18 2006 445 452
24. A. Lacy-Hulbert, A.M. Smith, H. Tissire, M. Barry, D. Crowley, R.T. Bronson, J.T. Roes, J.S. Savill, and R.O. Hynes Ulcerative colitis and autoimmunity induced by loss of myeloid alphav integrins Proc Natl Acad Sci U S A 104 2007 15823 15828
25. S. Koch, K. Kohl, E. Klein, D. von Bubnoff, and T. Bieber Skin homing of Langerhans cell precursors: adhesion, chemotaxis, and migration J Allergy Clin Immunol 117 2006 163 168
26. A. Delima, K. Spyros, S. Amar, and D.T. Graves Inflammation and tissue loss caused by periodontal pathogens is reduced by IL-1 antagonists J Infect Dis 186 2002 511 516
27. N.M. Moutsopoulos, J. Konkel, M. Sarmadi, M.A. Eskan, T. Wild, N. Dutzan, L. Abusleme, C. Zenobia, K.B. Hosur, T. Abe, G. Uzel, W. Chen, T. Chavakis, S.M. Holland, and G. Hajishengallis Defective neutrophil recruitment in leukocyte adhesion deficiency type I disease causes local IL-17-driven inflammatory bone loss Sci Transl Med 6 2014 229 240
28. L. Xing, Y. Xiu, and B.F. Boyce Osteoclast fusion and regulation by RANKL-dependent and independent factors World J Orthop 3 2012 212 222
29. D. Polak, A. Wilensky, L. Shapira, A. Halabi, D. Goldstein, E.I. Weiss, and Y. Houri-Haddad Mouse model of experimental periodontitis induced by Porphyromonas gingivalis/Fusobacterium nucleatum infection: bone loss and host response J Clin Periodontol 36 2009 406 410
30. Y. Teng, H. Nguyen, X. Gao, Y.Y. Kong, R.M. Gorczynski, B. Singh, R.P. Ellen, and J.M. Penninger Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infection J Clin Invest 106 2000 R59 R67
31. S. Karmakar, J. Kay, and E.M. Gravallese Bone damage in rheumatoid arthritis: mechanistic insights and approaches to prevention Rheum Dis Clin North Am 36 2010 385 404
32. H. Ohyama, N. Kato-Kogoe, A. Kuhara, F. Nishimura, K. Nakasho, K. Yamanegi, N. Yamada, M. Hata, J. Yamane, and N. Terada The involvement of IL-23 and the Th17 pathway in periodontitis J Dent Res 88 2009 633 638
33. A.E. Zeituni, R. Jotwani, J. Carrion, and C.W. Cutler Targeting of DC-SIGN on human dendritic cells by minor fimbriated Porphyromonas gingivalis strains elicits a distinct effector T cell response J Immunol 183 2009 5694 5704
34. X.E. Dereka, K.I. Tosios, E. Chrysomali, and E. Angelopoulou Factor XIIIa+ dendritic cells and S-100 protein+ Langerhans' cells in adult periodontitis J Periodontal Res 39 2004 447 452
35. S. Seth, L. OberdÖrfer, R. Hyde, K. Hoff, V. Thies, T. Worbs, S. Schmitz, and R. Förster CCR7 essentially contributes to the homing of plasmacytoid dendritic cells to lymph nodes under steady-state as well as inflammatory conditions J Immunol 186 2011 3364 3372
36. Y.M. Kerdiles, D.R. Beisner, R. Tinoco, A.S. Dejean, D.H. Castrillon, R.A. DePinho, and S.M. Hedrick Foxo1 links homing and survival of naive T cells by regulating L-selectin, CCR7 and interleukin 7 receptor Nat Immunol 10 2009 176 184
37. L.E. Mkonyi, A. Bletsa, A.I. Bolstad, V. Bakken, H. Wiig, and E. Berggreen Gingival lymphatic drainage protects against Porphyromonas gingivalis-induced bone loss in mice Am J Pathol 181 2012 907 916