DEL-1 restrains osteoclastogenesis and inhibits inflammatory bone loss in nonhuman primates

Science Translational Medicine

Volumn 7, Issue 307, 2015, Pages

  Shin, Jieun ^a   Maekawa, Tomoki ^a   Abe, Toshiharu ^a   Hajishengallis, Evlambia ^b   Hosur, Kavita ^a   Pyaram, Kalyani ^a   Mitroulis, Ioannis ^c   Chavakis, Triantafyllos ^c   Hajishengallis, George ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

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

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; BETA3 INTEGRIN; CATHEPSIN K; CD11B ANTIGEN; CD51 ANTIGEN; CELL PROTEIN; DEVELOPMENTAL ENDOTHELIAL LOCUS 1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 1BETA; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MESSENGER RNA; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEIN BCL 6; TRANSCRIPTION FACTOR NFAT; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CARRIER PROTEIN; CYTOKINE; EDIL3 PROTEIN, HUMAN; EDIL3 PROTEIN, MOUSE;

ALVEOLAR BONE; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; MOUSE; MULTINUCLEAR CELL; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; PERIODONTITIS; PRIMATE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; UPREGULATION; ANIMAL; BONE DEVELOPMENT; C57BL MOUSE; CELL MOTION; COMPLICATION; DISEASE MODEL; GINGIVITIS; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; NEUTROPHIL; PATHOLOGY; PREVENTION AND CONTROL; PROTEIN TERTIARY STRUCTURE;

AMINO ACID MOTIFS; ANIMALS; BONE RESORPTION; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL MOVEMENT; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; GINGIVAL CREVICULAR FLUID; HUMANS; INFLAMMATION; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; OSTEOCLASTS; OSTEOGENESIS; PERIODONTITIS; PRIMATES; PROTEIN STRUCTURE, TERTIARY;

EID: 84942881294     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aac5380     Document Type: Article

References (41)

1. G. Hajishengallis, Periodontitis: From microbial immune subversion to systemic inflammation. Nat. Rev. Immunol. 15, 30-44 (2015).
2. R. J. Lamont, G. Hajishengallis, Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol. Med. 21, 172-183 (2015).
3. P. I. Eke, B. A. Dye, L. Wei, G. O. Thornton-Evans, R. J. Genco, Prevalence of periodontitis in adults in the United States: 2009 and 2010. J. Dent. Res. 91, 914-920 (2012).
4. T. Beikler, T. F. Flemmig, Oral biofilm-associated diseases: Trends and implications for quality of life, systemic health and expenditures. Periodontol. 2000 55, 87-103 (2011).
5. M. A. Eskan, R. Jotwani, T. Abe, J. Chmelar, J.-H. Lim, S. Liang, P. A. Ciero, J. L. Krauss, F. Li, M. Rauner, L. C. Hofbauer, E. Y. Choi, K.-J. Chung, A. Hashim, M. A. Curtis, T. Chavakis, G. Hajishengallis, The leukocyte integrin antagonist Del-1 inhibits IL-17-mediated inflammatory bone loss. Nat. Immunol. 13, 465-473 (2012).
6. E. Y. Choi, E. Chavakis, M. A. Czabanka, H. F. Langer, L. Fraemohs, M. Economopoulou, R. K. Kundu, A. Orlandi, Y. Y. Zheng, D. A. Prieto, C. M. Ballantyne, S. L. Constant, W. C. Aird, T. Papayannopoulou, C. G. Gahmberg, M. C. Udey, P. Vajkoczy, T. Quertermous, S. Dimmeler, C. Weber, T. Chavakis, Del-1, an endogenous leukocyte-endothelial adhesion inhibitor, limits inflammatory cell recruitment. Science 322, 1101-1104 (2008).
7. E. Y. Choi, J.-H. Lim, A. Neuwirth, M. Economopoulou, A. Chatzigeorgiou, K.-J. Chung, S. Bittner, S.-H. Lee, H. Langer, M. Samus, H. Kim, G.-S. Cho, T. Ziemssen, K. Bdeir, E. Chavakis, J.-Y. Koh, L. Boon, K. Hosur, S. R. Bornstein, S. G. Meuth, G. Hajishengallis, T. Chavakis, Developmental endothelial locus-1 is a homeostatic factor in the central nervous system limiting neuroinflammation and demyelination. Mol. Psychiatry 20, 880-888 (2015).
8. C. Hidai, T. Zupancic, K. Penta, A.Mikhail, M. Kawana, E. E. Quertermous, Y. Aoka, M. Fukagawa, Y. Matsui, D. Platika, R. Auerbach, B. L. M. Hogan, R. Snodgrass, T. Quertermous, Cloning and characterization of developmental endothelial locus-1: An embryonic endothelial cell protein that binds the avb3 integrin receptor. Genes Dev. 12, 21-33 (1998).
9. S. K. Dasgupta, A. Le, T. Chavakis, R. E. Rumbaut, P. Thiagarajan, Developmental endothelial locus-1 (Del-1) mediates clearance of platelet microparticles by the endothelium. Circulation 125, 1664-1672 (2012).
10. Y.-Y. Kang, D.-Y. Kim, S.-H. Lee, E. Y. Choi, Deficiency of developmental endothelial locus-1 (Del-1) aggravates bleomycin-induced pulmonary fibrosis in mice. Biochem. Biophys. Res. Commun. 445, 369-374 (2014).
11. I. Mitroulis, V. I. Alexaki, I. Kourtzelis, A. Ziogas, G. Hajishengallis, T. Chavakis, Leukocyte integrins: Role in leukocyte recruitment and as therapeutic targets in inflammatory disease. Pharmacol. Ther. 147, 123-135 (2015).
12. C. Hidai, M. Kawana, H. Kitano, S. Kokubun, Discoidin domain of Del1 protein contributes to its deposition in the extracellular matrix. Cell Tissue Res. 330, 83-95 (2007).
13. R. Hanayama, M. Tanaka, K. Miwa, S. Nagata, Expression of developmental endothelial locus-1 in a subset of macrophages for engulfment of apoptotic cells. J. Immunol. 172, 3876-3882 (2004).
14. I. Mitroulis, Y.-Y. Kang, C. G. Gahmberg, G. Siegert, G. Hajishengallis, T. Chavakis, E.-Y. Choi, Developmental endothelial locus-1 attenuates complement-dependent phagocytosis through inhibition of Mac-1-integrin. Thromb. Haemost. 111, 781-1006 (2014).
15. A. Goris, S. Sawcer, K. Vandenbroeck, H. Carton, A. Billiau, E. Setakis, A. Compston, B. Dubois, New candidate loci for multiple sclerosis susceptibility revealed by a whole genome association screen in a Belgian population. J. Neuroimmunol. 143, 65-69 (2003).
16. V. K. Ramanan, S. L. Risacher, K. Nho, S. Kim, S. Swaminathan, L. Shen, T. M. Foroud, H. Hakonarson, M. J. Huentelman, P. S. Aisen, R. C. Petersen, R. C. Green, C. R. Jack, R. A. Koeppe, W. J. Jagust, M. W. Weiner, A. J. Saykin; Alzheimer's Disease Neuroimaging Initiative, APOE and BCHE as modulators of cerebral amyloid deposition: A florbetapir PET genome-wide association study. Mol. Psychiatry 19, 351-357 (2014).
17. Z. Lin, J.-X. Bei, M. Shen, Q. Li, Z. Liao, Y. Zhang, Q. Lv, Q. Wei, H.-Q. Low, Y.-M. Guo, S. Cao, M. Yang, Z. Hu, M. Xu, X. Wang, Y. Wei, L. Li, C. Li, T. Li, J. Huang, Y. Pan, O. Jin, Y. Wu, J. Wu, Z. Guo, P. He, S. Hu, H. Wu, H. Song, F. Zhan, S. Liu, G. Gao, Z. Liu, Y. Li, C. Xiao, J. Li, Z. Ye, W. He, D. Liu, L. Shen, A. Huang, H. Wu, Y. Tao, X. Pan, B. Yu, E. S. Tai, Y.-X. Zeng, E. C. Ren, Y. Shen, J. Liu, J. Gu, A genome-wide association study in Han Chinese identifies new susceptibility loci for ankylosing spondylitis. Nat. Genet. 44, 73-77 (2012).
18. G. Hajishengallis, T. Chavakis, E. Hajishengallis, J. D. Lambris, Neutrophil homeostasis and inflammation: Novel paradigms from studying periodontitis. J. Leukoc. Biol. 10.1189/jlb.3VMR1014-468R (2014).
19. K.-H. Park-Min, E. Y. Lee, N. K. Moskowitz, E. Lim, S.-K. Lee, J. A. Lorenzo, C. Huang, A. M. Melnick, P. E. Purdue, S. R. Goldring, L. B. Ivashkiv, Negative regulation of osteoclast precursor differentiation by CD11b and b2 integrin-B-cell lymphoma 6 signaling. J. Bone Miner. Res. 28, 135-149 (2013).
20. I. Nakamura, L. T. Duong, S. B. Rodan, G. A. Rodan, Involvement of avb3 integrins in osteoclast function. J. Bone Miner. Metab. 25, 337-344 (2007).
21. T. Abe, J. Shin, K. Hosur, M. C. Udey, T. Chavakis, G. Hajishengallis, Regulation of osteoclast homeostasis and inflammatory bone loss by MFG-E8. J. Immunol. 193, 1383-1391 (2014).
22. G. N. Belibasakis, N. Bostanci, The RANKL-OPG system in clinical periodontology. J. Clin. Periodontol. 39, 239-248 (2012).
23. R. C. Page, H. E. Schroeder, Periodontitis in Man and Other Animals: A Comparative Review (Karger, Basel, 1982).
24. G. N. Belibasakis, G. Emingil, B. Saygan, O. Turkoglu, G. Atilla, N. Bostanci, Gene expression of transcription factor NFATc1 in periodontal diseases. APMIS 119, 167-172 (2011).
25. T. Nakashima, M. Hayashi, H. Takayanagi, New insights into osteoclastogenic signaling mechanisms. Trends Endocrinol. Metab. 23, 582-590 (2012).
26. P. Miossec, J. K. Kolls, Targeting IL-17 and TH17 cells in chronic inflammation. Nat. Rev. Drug Discov. 11, 763-776 (2012).
27. H. Carlsten, Immune responses and bone loss: The estrogen connection. Immunol. Rev. 208, 194-206 (2005).
28. A. Chakravarti, M.-A. Raquil, P. Tessier, P. E. Poubelle, Surface RANKL of Toll-like receptor 4-stimulated human neutrophils activates osteoclastic bone resorption. Blood 114, 1633-1644 (2009).
29. J. Seok, H. S. Warren, A. G. Cuenca, M. N. Mindrinos, H. V. Baker, W. Xu, D. R. Richards, G. P. McDonald-Smith, H. Gao, L. Hennessy, C. C. Finnerty, C. M. López, S. Honari, E. E. Moore, J. P. Minei, J. Cuschieri, P. E. Bankey, J. L. Johnson, J. Sperry, A. B. Nathens, T. R. Billiar, M. A.West, M. G. Jeschke, M. B. Klein, R. L. Gamelli, N. S.Gibran, B. H. Brownstein, C.Miller-Graziano, S. E. Calvano, P. H. Mason, J. P. Cobb, L. G. Rahme, S. F. Lowry, R. V. Maier, L. L.Moldawer, D. N. Herndon, R. W. Davis, W. Xiao, R. G. Tompkins, Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. U.S.A. 110, 3507-3512 (2013).
30. J. Shin, K. B. Hosur, K. Pyaram, R. Jotwani, S. Liang, T. Chavakis, G. Hajishengallis, Expression and function of the homeostatic molecule Del-1 in endothelial cells and the periodontal tissue. Clin. Dev. Immunol. 2013, 617809 (2013).
31. B. Baban, J. Y. Liu, R. Abdelsayed, M. S. Mozaffari, Reciprocal relation between GADD153 and Del-1 in regulation of salivary gland inflammation in Sjögren syndrome. Exp. Mol. Pathol. 95, 288-297 (2013).
32. W. Kanczkowski, A. Chatzigeorgiou, S. Grossklaus, D. Sprott, S. R. Bornstein, T. Chavakis, Role of the endothelial-derived endogenous anti-inflammatory factor Del-1 in inflammationmediated adrenal gland dysfunction. Endocrinology 154, 1181-1189 (2013).
33. J. K. Stoller, L. S. Aboussouan, A review of a1-antitrypsin deficiency. Am. J. Respir. Crit. Care Med. 185, 246-259 (2012).
34. A. Fieker, J. Philpott, M. Armand, Enzyme replacement therapy for pancreatic insufficiency: Present and future. Clin. Exp. Gastroenterol. 4, 55-73 (2011).
35. J. A. Gorzelany, M. P. de Souza, Protein replacement therapies for rare diseases: A breeze for regulatory approval? Sci. Transl. Med. 5, 178fs110 (2013).
36. T. Maekawa, T. Abe, E. Hajishengallis, K. B. Hosur, R. A. DeAngelis, D. Ricklin, J. D. Lambris, G. Hajishengallis, Genetic and intervention studies implicating complement C3 as a major target for the treatment of periodontitis. J. Immunol. 192 6020-6027 (2014).
37. T. Abe, G. Hajishengallis, Optimization of the ligature-induced periodontitis model in mice. J. Immunol. Methods 394, 49-54 (2013).
38. T. Abe, K. B. Hosur, E. Hajishengallis, E. S. Reis, D. Ricklin, J. D. Lambris, G. Hajishengallis, Local complement-targeted intervention in periodontitis: Proof-of-concept using a C5a receptor (CD88) antagonist. J. Immunol. 189, 5442-5448 (2012).
39. G. C. Armitage, Periodontal diagnoses and classification of periodontal diseases. Periodontol. 2000 34, 9-21 (2004).
40. N. Takahashi, N. Udagawa, S. Tanaka, T. Suda, Generating murine osteoclasts from bone marrow. Methods Mol. Med. 80, 129-144 (2003).
41. P. Collin-Osdoby, P. Osdoby, RANKL-mediated osteoclast formation from murine RAW 264.7 cells. Methods Mol. Biol. 816, 187-202 (2012).