Etanercept administration to neonatal SH3BP2 knock-in cherubism mice prevents TNF-α-induced inflammation and bone loss

Journal of Bone and Mineral Research

Volumn 29, Issue 5, 2014, Pages 1170-1182

  Yoshitaka, Teruhito ^a   Ishida, Shu ^a,b   Mukai, Tomoyuki ^a   Kittaka, Mizuho ^a,b   Reichenberger, Ernst J ^c   Ueki, Yasuyoshi ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^b HIROSHIMA UNIVERSITY   (Japan)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

bone loss; cherubism; etanercept; inflammation; TNF

Indexed keywords

ETANERCEPT; TUMOR NECROSIS FACTOR ALPHA; IMMUNOGLOBULIN G; NONSTEROID ANTIINFLAMMATORY AGENT; SH3BP2 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TNFR-FC FUSION PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE EROSION; CALVARIA; CONTROLLED STUDY; DRUG EFFECT; DRUG MEGADOSE; FEMALE; FIBROUS DYSPLASIA; INFLAMMATION; JAW; JOINT DESTRUCTION; LOW DRUG DOSE; MALE; MORPHOMETRICS; MOUSE; NEWBORN; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; POSTNATAL DEVELOPMENT; SWELLING; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE DISEASES, METABOLIC; CHERUBISM; GENE TARGETING; GENETICS; HUMAN; METABOLISM; MUTANT MOUSE STRAIN; PATHOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BONE DISEASES, METABOLIC; CHERUBISM; GENE KNOCK-IN TECHNIQUES; HUMANS; IMMUNOGLOBULIN G; INFLAMMATION; MICE; MICE, MUTANT STRAINS; RECEPTORS, TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84899058307     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2125     Document Type: Article

References (59)

1. Von Wowern N,. Cherubism: a 36-year long-term follow-up of 2 generations in different families and review of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2000; 90 (6): 765-72.
2. Papadaki ME, Lietman SA, Levine MA, Olsen BR, Kaban LB, Reichenberger EJ,. Cherubism: best clinical practice. Orphanet J Rare Dis. 2012; 7 (Suppl 1): S6.
3. Tiziani V, Reichenberger E, Buzzo CL, et al. The gene for cherubism maps to chromosome 4p16. Am J Hum Genet. 1999; 65 (1): 158-66.
4. Ueki Y, Tiziani V, Santanna C, et al. Mutations in the gene encoding c-Abl-binding protein SH3BP2 cause cherubism. Nat Genet. 2001; 28 (2): 125-6.
5. Ren R, Mayer BJ, Cicchetti P, Baltimore D,. Identification of a ten-amino acid proline-rich SH3 binding site. Science. 1993; 259 (5098): 1157-61.
6. Deckert M, Tartare-Deckert S, Hernandez J, Rottapel R, Altman A,. Adaptor function for the Syk kinases-interacting protein 3BP2 in IL-2 gene activation. Immunity. 1998; 9 (5): 595-605.
7. Foucault I, Liu YC, Bernard A, Deckert M,. The chaperone protein 14-3-3 in teracts with 3BP2/SH3BP2 and regulates its adapter function. J Biol Chem. 2003; 278 (9): 7146-53.
8. Foucault I, Le Bras S, Charvet C, Moon C, Altman A, Deckert M,. The adaptor protein 3BP2 associates with VAV guanine nucleotide exchange factors to regulate NFAT activation by the B-cell antigen receptor. Blood. 2005; 105 (3): 1106-13.
9. Maeno K, Sada K, Kyo S, et al. Adaptor protein 3BP2 is a potential ligand of Src homology 2 and 3 domains of Lyn protein-tyrosine kinase. J Biol Chem. 2003; 278 (27): 24912-20.
10. Le Bras S, Moon C, Foucault I, Breittmayer JP, Deckert M,. Abl-SH3 binding protein 2, 3BP2, interacts with CIN85 and HIP-55. FEBS Lett. 2007; 581 (5): 967-74.
11. Jevremovic D, Billadeau DD, Schoon RA, Dick CJ, Leibson PJ,. Regulation of NK cell-mediated cytotoxicity by the adaptor protein 3BP2. J Immunol. 2001; 166 (12): 7219-28.
12. Yu Z, Maoui M, Zhao ZJ, Li Y, Shen SH,. SHP-1 dephosphorylates 3BP2 and potentially downregulates 3BP2-mediated T cell antigen receptor signaling. FEBS J. 2006; 273 (10): 2195-205.
13. Chihara K, Nakashima K, Takeuchi K, Sada K,. Association of 3BP2 with SHP-1 regulates SHP-1-mediated production of TNF-alpha in RBL-2H3 cells. Genes Cells. 2011; 16 (12): 1133-45.
14. Shukla U, Hatani T, Nakashima K, Ogi K, Sada K,. Tyrosine phosphorylation of 3BP2 regulates B cell receptor-mediated activation of NFAT. J Biol Chem. 2009; 284 (49): 33719-28.
15. Levaot N, Simoncic PD, Dimitriou ID, et al. 3BP2-deficient mice are osteoporotic with impaired osteoblast and osteoclast functions. J Clin Invest. 2011; 121 (8): 3244-57.
16. Ueki Y, Lin CY, Senoo M, et al. Increased myeloid cell responses to M-CSF and RANKL cause bone loss and inflammation in SH3BP2 "cherubism" mice. Cell. 2007; 128 (1): 71-83.
17. Ferguson PJ, El-Shanti HI,. Autoinflammatory bone disorders. Curr Opin Rheumatol. 2007; 19 (5): 492-8.
18. Masters SL, Simon A, Aksentijevich I, Kastner DL,. Horror autoinflammaticus: the molecular pathophysiology of autoinflammatory disease. Annu Rev Immunol. 2009; 27: 621-68.
19. Levaot N, Voytyuk O, Dimitriou I, et al. Loss of Tankyrase-mediated destruction of 3BP2 Is the underlying pathogenic mechanism of cherubism. Cell. 2011; 147 (6): 1324-39.
20. Guettler S, LaRose J, Petsalaki E, et al. Structural basis and sequence rules for substrate recognition by Tankyrase explain the basis for cherubism disease. Cell. 2011; 147 (6): 1340-54.
21. Pasparakis M, Alexopoulou L, Episkopou V, Kollias G,. Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J Exp Med. 1996; 184 (4): 1397-411.
22. Caporali R, Pallavicini FB, Filippini M, et al. Treatment of rheumatoid arthritis with anti-TNF-alpha agents: a reappraisal. Autoimmun Rev. 2009; 8 (3): 274-80.
23. Kerensky TA, Gottlieb AB, Yaniv S, Au SC,. Etanercept: efficacy and safety for approved indications. Expert Opin Drug Saf. 2012; 11 (1): 121-39.
24. Venegas-Pont M, Manigrasso MB, Grifoni SC, et al. Tumor necrosis factor-alpha antagonist etanercept decreases blood pressure and protects the kidney in a mouse model of systemic lupus erythematosus. Hypertension. 2010; 56 (4): 643-9.
25. Liu R, Bal HS, Desta T, Behl Y, Graves DT,. Tumor necrosis factor-alpha mediates diabetes-enhanced apoptosis of matrix-producing cells and impairs diabetic healing. Am J Pathol. 2006; 168 (3): 757-64.
26. Genovese T, Mazzon E, Crisafulli C, et al. Immunomodulatory effects of etanercept in an experimental model of spinal cord injury. J Pharmacol Exp Ther. 2006; 316 (3): 1006-16.
27. Nemoto H, Konno S, Sugimoto H, et al. Anti-TNF therapy using etanercept suppresses degenerative and inflammatory changes in skeletal muscle of older SJL/J mice. Exp Mol Pathol. 2011; 90 (3): 264-70.
28. Rose S, Eren M, Murphy S, et al. A novel mouse model that develops spontaneous arthritis and is predisposed towards atherosclerosis. Ann Rheum Dis. 2013; 72 (1): 89-95.
29. Wallis RS, Broder M, Wong J, Beenhouwer D,. Granulomatous infections due to tumor necrosis factor blockade: correction. Clin Infect Dis. 2004; 39 (8): 1254-5.
30. Wallis RS, Broder MS, Wong JY, Hanson ME, Beenhouwer DO,. Granulomatous infectious diseases associated with tumor necrosis factor antagonists. Clin Infect Dis. 2004; 38 (9): 1261-5.
31. Plessner HL, Lin PL, Kohno T, et al. Neutralization of tumor necrosis factor (TNF) by antibody but not TNF receptor fusion molecule exacerbates chronic murine tuberculosis. J Infect Dis. 2007; 195 (11): 1643-50.
32. Khan OM, Ibrahim MX, Jonsson IM, et al. Geranylgeranyltransferase type I (GGTase-I) deficiency hyperactivates macrophages and induces erosive arthritis in mice. J Clin Invest. 2011; 121 (2): 628-39.
33. Park CH, Abramson ZR, Taba M Jr, et al. Three-dimensional micro-computed tomographic imaging of alveolar bone in experimental bone loss or repair. J Periodontol. 2007; 78 (2): 273-81.
34. Faul F, Erdfelder E, Lang AG, Buchner A,. GPower 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007; 39 (2): 175-91.
35. Lories RJ, Derese I, de Bari C, Luyten FP,. Evidence for uncoupling of inflammation and joint remodeling in a mouse model of spondylarthritis. Arthritis Rheum. 2007; 56 (2): 489-97.
36. Hero M, Suomalainen A, Hagstrom J, et al. Anti-tumor necrosis factor treatment in cherubism: clinical, radiological and histological findings in two children. Bone. 2013; 52 (1): 347-53.
37. Palladino MA, Bahjat FR, Theodorakis EA, Moldawer LL,. Anti-TNF-alpha therapies: the next generation. Nat Rev Drug Discov. 2003; 2 (9): 736-46.
38. Thomas D, Henshaw R, Skubitz K, et al. Denosumab in patients with giant-cell tumour of bone: an open-label, phase 2 study. Lancet Oncol. 2010; 11 (3): 275-80.
39. Kaugars GE, Niamtu J 3rd, Svirsky JA,. Cherubism: diagnosis, treatment, and comparison with central giant cell granulomas and giant cell tumors. Oral Surg Oral Med Oral Pathol. 1992; 73 (3): 369-74.
40. Reichenberger EJ, Levine MA, Olsen BR, Papadaki ME, Lietman SA,. The role of SH3BP2 in the pathophysiology of cherubism. Orphanet J Rare Dis. 2012; 7 (Suppl 1): S5.
41. Scott DL, Kingsley GH,. Tumor necrosis factor inhibitors for rheumatoid arthritis. N Engl J Med. 2006; 355 (7): 704-12.
42. Listing J, Strangfeld A, Kary S, et al. Infections in patients with rheumatoid arthritis treated with biologic agents. Arthritis Rheum. 2005; 52 (11): 3403-12.
43. Dixon WG, Symmons DP, Lunt M, Watson KD, Hyrich KL, Silman AJ,. Serious infection following anti-tumor necrosis factor alpha therapy in patients with rheumatoid arthritis: lessons from interpreting data from observational studies. Arthritis Rheum. 2007; 56 (9): 2896-04.
44. Dixon WG, Watson K, Lunt M, Hyrich KL, Silman AJ, Symmons DP,. Rates of serious infection, including site-specific and bacterial intracellular infection, in rheumatoid arthritis patients receiving anti-tumor necrosis factor therapy: results from the British Society for Rheumatology Biologics Register. Arthritis Rheum. 2006; 54 (8): 2368-76.
45. Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V,. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA. 2006; 295 (19): 2275-85.
46. Rosenblum H, Amital H,. Anti-TNF therapy: safety aspects of taking the risk. Autoimmun Rev. 2011; 10 (9): 563-8.
47. Gilbert L, He X, Farmer P, et al. Inhibition of osteoblast differentiation by tumor necrosis factor-alpha. Endocrinology. 2000; 141 (11): 3956-64.
48. Nanes MS,. Tumor necrosis factor-alpha: molecular and cellular mechanisms in skeletal pathology. Gene. 2003; 321: 1-15.
49. Li Y, Li A, Strait K, Zhang H, Nanes MS, Weitzmann MN,. Endogenous TNFalpha lowers maximum peak bone mass and inhibits osteoblastic Smad activation through NF-kappaB. J Bone Miner Res. 2007; 22 (5): 646-55.
50. Kobayashi K, Takahashi N, Jimi E, et al. Tumor necrosis factor alpha stimulates osteoclast differentiation by a mechanism independent of the ODF/RANKL-RANK interaction. J Exp Med. 2000; 191 (2): 275-86.
51. Nakashima T, Hayashi M, Fukunaga T, et al. Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med. 2011; 17 (10): 1231-4.
52. Xiong J, Onal M, Jilka RL, Weinstein RS, Manolagas SC, O'Brien CA,. Matrix-embedded cells control osteoclast formation. Nat Med. 2011; 17 (10): 1235-41.
53. Cheung WY, Simmons CA, You L,. Osteocyte apoptosis regulates osteoclast precursor adhesion via osteocytic IL-6 secretion and endothelial ICAM-1 expression. Bone. 2012; 50 (1): 104-10.
54. Al-Dujaili SA, Lau E, Al-Dujaili H, Tsang K, Guenther A, You L,. Apoptotic osteocytes regulate osteoclast precursor recruitment and differentiation in vitro. J Cell Biochem. 2011; 112 (9): 2412-23.
55. Haraoui B,. Differentiating the efficacy of the tumor necrosis factor inhibitors. Semin Arthritis Rheum. 2005; 34 (5 Suppl 1): 7-11.
56. Rigby WF,. Drug insight: different mechanisms of action of tumor necrosis factor antagonists-passive-aggressive behavior ? Nat Clin Pract Rheumatol. 2007; 3 (4): 227-33.
57. Sandborn WJ, Hanauer SB, Katz S, et al. Etanercept for active Crohn's disease: a randomized, double-blind, placebo-controlled trial. Gastroenterology. 2001; 121 (5): 1088-94.
58. ten Hove T, van Montfrans C, Peppelenbosch MP, van Deventer SJ,. Infliximab treatment induces apoptosis of lamina propria T lymphocytes in Crohn's disease. Gut. 2002; 50 (2): 206-11.
59. Papadakis KA, Shaye OA, Vasiliauskas EA, et al. Safety and efficacy of adalimumab (D2E7) in Crohn's disease patients with an attenuated response to infliximab. Am J Gastroenterol. 2005; 100 (1): 75-9.