Proteinase-activated receptor-2 is required for normal osteoblast and osteoclast differentiation during skeletal growth and repair

Bone

Volumn 50, Issue 3, 2012, Pages 704-712

  Georgy, S R ^a   Pagel, C N ^a   Ghasem Zadeh, A ^a   Zebaze, R M D ^a   Pike, R N ^b   Sims, N A ^a   Mackie, E J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Bone repair; Hepsin; Histomorphometry; Kallikrein 4; Matriptase; Micro CT; Osteoblast; Osteoclast; Proteinase activated receptor 2

Indexed keywords

ALKALINE PHOSPHATASE; CALCITRIOL; COLONY STIMULATING FACTOR 1; FIBROBLAST GROWTH FACTOR 2; INTERLEUKIN 6; KALLIKREIN; KALLIKREIN 4; MATRIPTASE; OSTEOCLAST DIFFERENTIATION FACTOR; PARATHYROID HORMONE; PROTEINASE ACTIVATED RECEPTOR 2; THROMBIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE GROWTH; BONE MARROW; BONE REMODELING; BONE STRUCTURE; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; CORTICAL BONE; DOWN REGULATION; MALE; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOID; PROTEIN EXPRESSION; PROTEIN FUNCTION; TIBIA; TRABECULAR BONE;

ANIMALS; BONE DEVELOPMENT; CALCITRIOL; CELL DIFFERENTIATION; CELLS, CULTURED; INTERLEUKIN-6; MICE; MICE, KNOCKOUT; OSTEOBLASTS; OSTEOCLASTS; PARATHYROID HORMONE; RECEPTOR, PAR-2; TIBIA;

EID: 84856963486     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2011.11.023     Document Type: Article

References (46)

1. Abraham L.A., Chinni C., Jenkins A.L., Lourbakos A., Ally N., Pike R.N., et al. Expression of protease-activated receptor-2 by osteoblasts. Bone 2000, 26:7-14.
2. Mackie E.J., Loh L.H., Sivagurunathan S., Uaesoontrachoon K., Yoo H.J., Wong D., et al. Protease-activated receptors in the musculoskeletal system. Int J Biochem Cell Biol 2008, 40:1169-1184.
3. Smith R., Ransjo M., Tatarczuch L., Song S.J., Pagel C., Morrison J.R., et al. Activation of protease-activated receptor-2 leads to inhibition of osteoclast differentiation. J Bone Miner Res 2004, 19:507-516.
4. Nystedt S., Emilsson K., Wahlestedt C., Sundelin J. Molecular cloning of a potential proteinase activated receptor. Proc Natl Acad Sci U S A 1994, 91:9208-9212.
5. Colognato R., Slupsky J.R., Jendrach M., Burysek L., Syrovets T., Simmet T. Differential expression and regulation of protease-activated receptors in human peripheral monocytes and monocyte-derived antigen-presenting cells. Blood 2003, 102:2645-2652.
6. Ossovskaya V.S., Bunnett N.W. Protease-activated receptors: contribution to physiology and disease. Physiol Rev 2004, 84:579-621.
7. Vesey D.A., Hooper J.D., Gobe G.C., Johnson D.W. Potential physiological and pathophysiological roles for protease-activated receptor-2 in the kidney. Nephrology (Carlton) 2007, 12:36-43.
8. Oikonomopoulou K., Hansen K.K., Saifeddine M., Vergnolle N., Tea I., Blaber M., et al. Kallikrein-mediated cell signalling: targeting proteinase-activated receptors (PARs). Biol Chem 2006, 387:817-824.
9. Ramsay A.J., Dong Y., Hunt M.L., Linn M., Samaratunga H., Clements J.A., et al. Kallikrein-related peptidase 4 (KLK4) initiates intracellular signaling via protease-activated receptors (PARs). KLK4 and PAR-2 are co-expressed during prostate cancer progression. J Biol Chem 2008, 283:12293-12304.
10. Adams M.N., Ramachandran R., Yau M.K., Suen J.Y., Fairlie D.P., Hollenberg M.D., et al. Structure, function and pathophysiology of protease activated receptors. Pharmacol Ther 2011, 130:248-282.
11. Soh U.J., Dores M.R., Chen B., Trejo J. Signal transduction by protease-activated receptors. Br J Pharmacol 2010, 160:191-203.
12. Ramachandran R., Mihara K., Chung H., Renaux B., Lau C.S., Muruve D.A., et al. Neutrophil elastase acts as a biased agonist for proteinase-activated receptor-2 (PAR2). J Biol Chem 2011, 286:24638-24648.
13. Busso N., Frasnelli M., Feifel R., Cenni B., Steinhoff M., Hamilton J., et al. Evaluation of protease-activated receptor 2 in murine models of arthritis. Arthritis Rheum 2007, 56:101-107.
14. Ferrell W.R., Lockhart J.C., Kelso E.B., Dunning L., Plevin R., Meek S.E., et al. Essential role for proteinase-activated receptor-2 in arthritis. J Clin Invest 2003, 111:35-41.
15. Holzhausen M., Spolidorio L.C., Ellen R.P., Jobin M.C., Steinhoff M., Andrade-Gordon P., et al. Protease-activated receptor-2 activation: a major role in the pathogenesis of Porphyromonas gingivalis infection. Am J Pathol 2006, 168:1189-1199.
16. Schmidlin F., Amadesi S., Dabbagh K., Lewis D.E., Knott P., Bunnett N.W., et al. Protease-activated receptor 2 mediates eosinophil infiltration and hyperreactivity in allergic inflammation of the airway. J Immunol 2002, 169:5315-5321.
17. Wee J.L., Chionh Y.T., Ng G.Z., Harbour S.N., Allison C., Pagel C.N., et al. Protease-activated receptor-1 down-regulates the murine inflammatory and humoral response to Helicobacter pylori. Gastroenterology 2010, 138:573-582.
18. Wong D.M., Tam V., Lam R., Walsh K.A., Tatarczuch L., Pagel C.N., et al. Protease-activated receptor 2 has pivotal roles in cellular mechanisms involved in experimental periodontitis. Infect Immun 2010, 78:629-638.
19. Seeliger S., Derian C.K., Vergnolle N., Bunnett N.W., Nawroth R., Schmelz M., et al. Proinflammatory role of proteinase-activated receptor-2 in humans and mice during cutaneous inflammation in vivo. FASEB J 2003, 17:1871-1885.
20. Palmer H.S., Kelso E.B., Lockhart J.C., Sommerhoff C.P., Plevin R., Goh F.G., et al. Protease-activated receptor 2 mediates the proinflammatory effects of synovial mast cells. Arthritis Rheum 2007, 56:3532-3540.
21. Vergnolle N., Cellars L., Mencarelli A., Rizzo G., Swaminathan S., Beck P., et al. A role for proteinase-activated receptor-1 in inflammatory bowel diseases. J Clin Invest 2004, 114:1444-1456.
22. Georgy S.R., Pagel C.N., Wong D.M., Sivagurunathan S., Loh L.H., Myers D.E., et al. Proteinase-activated receptor-2 (PAR2) and mouse osteoblasts: regulation of cell function and lack of specificity of PAR2-activating peptides. Clin Exp Pharmacol Physiol 2010, 37:328-336.
23. Damiano B.P., Cheung W.M., Santulli R.J., Fung-Leung W.P., Ngo K., Ye R.D., et al. Cardiovascular responses mediated by protease-activated receptor-2 (PAR-2) and thrombin receptor (PAR-1) are distinguished in mice deficient in PAR-2 or PAR-1. J Pharmacol Exp Ther 1999, 288:671-678.
24. Lindner J.R., Kahn M.L., Coughlin S.R., Sambrano G.R., Schauble E., Bernstein D., et al. Delayed onset of inflammation in protease-activated receptor-2-deficient mice. J Immunol 2000, 165:6504-6510.
25. Uehara A., Muramoto K., Takada H., Sugawara S. Neutrophil serine proteinases activate human nonepithelial cells to produce inflammatory cytokines through protease-activated receptor 2. J Immunol 2003, 170:5690-5696.
26. Sokolova E., Reiser G. A novel therapeutic target in various lung diseases: airway proteases and protease-activated receptors. Pharmacol Ther 2007, 115:70-83.
27. McIntosh K.A., Plevin R., Ferrell W.R., Lockhart J.C. The therapeutic potential of proteinase-activated receptors in arthritis. Curr Opin Pharmacol 2007, 7:334-338.
28. Bushell T. The emergence of proteinase-activated receptor-2 as a novel target for the treatment of inflammation-related CNS disorders. J Physiol 2007, 581:7-16.
29. Barry G.D., Suen J.Y., Le G.T., Cotterell A., Reid R.C., Fairlie D.P. Novel agonists and antagonists for human protease activated receptor 2. J Med Chem 2010, 53:7428-7440.
30. Campbell T.M., Wong W.T., Mackie E.J. Establishment of a model of cortical bone repair in mice. Calcif Tissue Int 2003, 73:49-55.
31. Chiang C., Chiu M., Moore A.J., Anderson P.H., Ghasem-Zadeh A., McManus J.F., et al. Mineralization and bone resorption are regulated by the androgen receptor in male mice. J Bone Miner Res 2009, 24:621-631.
32. Hildebrand T., Laib A., Muller R., Dequeker J., Ruegsegger P. Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 1999, 14:1167-1174.
33. Bouxsein M.L., Boyd S.K., Christiansen B.A., Guldberg R.E., Jepsen K.J., Muller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 2010, 25:1468-1486.
34. Sims N.A., Clement-Lacroix P., Da Ponte F., Bouali Y., Binart N., Moriggl R., et al. Bone homeostasis in growth hormone receptor-null mice is restored by IGF-I but independent of Stat5. J Clin Invest 2000, 106:1095-1103.
35. Hankenson K.D., Bain S.D., Kyriakides T.R., Smith E.A., Goldstein S.A., Bornstein P. Increased marrow-derived osteoprogenitor cells and endosteal bone formation in mice lacking thrombospondin 2. J Bone Miner Res 2000, 15:851-862.
36. Song S.J., Pagel C.N., Campbell T.M., Pike R.N., Mackie E.J. The role of protease-activated receptor-1 in bone healing. Am J Pathol 2005, 166:857-868.
37. Sims N.A., Jenkins B.J., Nakamura A., Quinn J.M., Li R., Gillespie M.T., et al. Interleukin-11 receptor signaling is required for normal bone remodeling. J Bone Miner Res 2005, 20:1093-1102.
38. Pagel C.N., Song S.J., Loh L.H., Tudor E.M., Murray-Rust T.A., Pike R.N., et al. Thrombin-stimulated growth factor and cytokine expression in osteoblasts is mediated by protease-activated receptor-1 and prostanoids. Bone 2009, 44:813-821.
39. Rozen S., Skaletsky H.J. Primer3 on the WWW for general users and for biologist programmers. Bioinformatics methods and protocols: methods in molecular biology 2000, 365-386. Humana Press, Totowa, NJ. S.M.S. Krawetz (Ed.).
40. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36.
41. Wu C.A., Pettit A.R., Toulson S., Grondahl L., Mackie E.J., Cassady A.I. Responses in vivo to purified poly(3-hydroxybutyrate-co-3-hydroxyvalerate) implanted in a murine tibial defect model. J Biomed Mater Res A 2009, 91:845-854.
42. Camerer E., Barker A., Duong D.N., Ganesan R., Kataoka H., Cornelissen I., et al. Local protease signaling contributes to neural tube closure in the mouse embryo. Dev Cell 2010, 18:25-38.
43. Walker E.C., McGregor N.E., Poulton I.J., Solano M., Pompolo S., Fernandes T.J., et al. Oncostatin M promotes bone formation independently of resorption when signaling through leukemia inhibitory factor receptor in mice. J Clin Invest 2010, 120:582-592.
44. Orr S.L., Hughes T.P., Sawyers C.L., Kato R.M., Quan S.G., Williams S.P., et al. Isolation of unknown genes from human bone marrow by differential screening and single-pass cDNA sequence determination. Proc Natl Acad Sci U S A 1994, 91:11869-11873.
45. Jilka R.L., Weinstein R.S., Bellido T., Roberson P., Parfitt A.M., Manolagas S.C. Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J Clin Invest 1999, 104:439-446.
46. Nakamura T., Hara Y., Tagawa M., Tamura M., Yuge T., Fukuda H., et al. Recombinant human basic fibroblast growth factor accelerates fracture healing by enhancing callus remodeling in experimental dog tibial fracture. J Bone Miner Res 1998, 13:942-949.