Piroxicam treatment augments bone abnormalities in interleukin-10 knockout mice

Inflammatory Bowel Diseases

Volumn 21, Issue 2, 2015, Pages 257-266

  Holgersen, Kristine ^a,c   Dobie, Ross ^d   Farquharson, Colin ^d   Van't Hof, Rob ^e   Ahmed, Syed Faisal ^b   Hansen, Axel Kornerup ^c   Holm, Thomas L ^a  

^a NOVO NORDISK A S   (Denmark)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Bone metabolism; Inflammatory bowel disease; Interleukin 10 knockout mouse; Osteoporosis; Piroxicam

Indexed keywords

INTERLEUKIN 10; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PIROXICAM; NONSTEROID ANTIINFLAMMATORY AGENT;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DISEASE; COLON; CONTROLLED STUDY; CORTICAL BONE; CROHN DISEASE; DISEASE SEVERITY; EXPERIMENTAL COLITIS; FEMALE; GEOMETRY; HYPERPLASIA; METABOLIC PARAMETERS; MICRO-COMPUTED TOMOGRAPHY; MICROSCOPY; MOUSE; MUSCULOSKELETAL SYSTEM PARAMETERS; NONHUMAN; OSSIFICATION; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SYSTEMATIC REVIEW; SYSTEMIC DISEASE; TIBIA; TRABECULAR BONE; TRABECULAR THICKNESS; WILD TYPE; ANIMAL; BONE DENSITY; BONE DISEASES, METABOLIC; C57BL MOUSE; CHEMICALLY INDUCED; COLITIS; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; OSTEOPOROSIS; PATHOLOGY; PHYSIOLOGY;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BONE DENSITY; BONE DISEASES, METABOLIC; COLITIS; DISEASE MODELS, ANIMAL; FEMALE; INFLAMMATION; INTERLEUKIN-10; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOPOROSIS; PIROXICAM; X-RAY MICROTOMOGRAPHY;

EID: 84927771654     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000269     Document Type: Article

References (64)

1. Sandler RS, Everhart JE, Donowitz M, et al. The burden of selected digestive diseases in the United States. Gastroenterology. 2002;122: 1500-1511.
2. Lakatos PL. Recent trends in the epidemiology of inflammatory bowel diseases: up or down? World J Gastroenterol. 2006;12:6102-6108.
3. Wallace KL, Zheng LB, Kanazawa Y, et al. Immunopathology of inflammatory bowel disease. World J Gastroenterol. 2014;20:6-21.
4. Baumgart DC, Carding SR. Inflammatory bowel disease: cause and immunobiology. Lancet. 2007;369:1627-1640.
5. Ordas I, Eckmann L, Talamini M, et al. Ulcerative colitis. Lancet. 2012; 380:1606-1619.
6. Baumgart DC, Sandborn WJ. Inflammatory bowel disease: clinical aspects and established and evolving therapies. Lancet. 2007;369:1641-1657.
7. Baumgart DC, Sandborn WJ. Crohn's disease. Lancet. 2012;380: 1590-1605.
8. Danese S, Fiocchi C. Ulcerative colitis. N Engl J Med. 2011;365: 1713-1725.
9. Vavricka SR, Brun L, Ballabeni P, et al. Frequency and risk factors for extraintestinal manifestations in the Swiss inflammatory bowel disease cohort. Am J Gastroenterol. 2011;106:110-119.
10. Larsen S, Bendtzen K, Nielsen OH. Extraintestinal manifestations of inflammatory bowel disease: epidemiology, diagnosis, and management. Ann Med. 2010;42:97-114.
11. Bernstein CN, Leslie WD, Leboff MS. AGA technical review on osteoporosis in gastrointestinal diseases. Gastroenterology. 2003;124:795-841.
12. Van staa TP, Cooper C, Samuels Brusse L, et al. Inflammatory bowel disease and the risk of fracture. Gastroenterology. 2003;125:1591-1597.
13. Bernstein CN, Blanchard JF, Leslie W, et al. The incidence of fracture among patients with inflammatory bowel disease. A population-based cohort study. Ann Intern Med. 2000;133:795-799.
14. Rodriguez-Bores L, Barahona-Garrido J, Yamamoto-Furusho JK. Basic and clinical aspects of osteoporosis in inflammatory bowel disease. World J Gastroenterol. 2007;13:6156-6165.
15. Ali T, Lam D, Bronze MS, et al. Osteoporosis in inflammatory bowel disease. Am J Med. 2009;122:599-604.
16. Takayanagi H. Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat Rev Immunol. 2007;7: 292-304.
17. Tilg H, Moschen AR, Kaser A, et al. Gut, inflammation and osteoporosis: basic and clinical concepts. Gut. 2008;57:684-694.
18. Hamdani G, Gabet Y, Rachmilewitz D, et al. Dextran sodium sulfateinduced colitis causes rapid bone loss in mice. Bone. 2008;43:945-950.
19. Lin CL, Moniz C, Chambers TJ, et al. Colitis causes bone loss in rats through suppression of bone formation. Gastroenterology. 1996;111: 1263-1271.
20. Cohen SL, Moore AM, Ward WE. Interleukin-10 k.o. mouse: A model for studying bone metabolism during intestinal inflammation. Inflamm Bowel Dis. 2004;10:557-563.
21. Dresner-Pollak R, Gelb N, Rachmilewitz D, et al. Interleukin 10-deficient mice develop osteopenia, decreased bone formation, and mechanical fragility of long bones. Gastroenterology. 2004;127:792-801.
22. Irwin R, Lee T, Young VB, et al. Colitis-induced bone loss is gender dependent and associated with increased inflammation. Inflamm Bowel Dis. 2013;19:1586-1597.
23. Berg DJ, Zhang J, Weinstock JV, et al. Rapid development of colitis in NSAID-treated IL-10-deficient mice. Gastroenterology. 2002;123: 1527-1542.
24. Holgersen K, Kvist PH, Hansen AK, et al. Predictive validity and immune cell involvement in the pathogenesis of piroxicam-accelerated colitis in interleukin-10 k.o. mice. Int Immunopharmacol. 2014;21:137-147.
25. Holgersen K, Kvist PH, Markholst H, et al. Characterisation of enterocolitis in the piroxicam-accelerated interleukin-10 knock out mouse-a model mimicking inflammatory bowel disease. J Crohns Colitis. 2014;8:147-160.
26. Cooper HS, Murthy SN, Shah RS, et al. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest. 1993;69:238-249.
27. Okayasu I, Hatakeyama S, Yamada M, et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990;98:694-702.
28. Elson CO, Beagley KW, Sharmanov AT, et al. Hapten-induced model of murine inflammatory bowel disease: mucosa immune responses and protection by tolerance. J Immunol. 1996;157:2174-2185.
29. Hale LP, Gottfried MR, Swidsinski A. Piroxicam treatment of IL-10- deficient mice enhances colonic epithelial apoptosis and mucosal exposure to intestinal bacteria. Inflamm Bowel Dis. 2005;11:1060-1069.
30. Dobie R, MacRae VE, Huesa C, et al. Direct stimulation of bone mass by increased GH signalling in osteoblasts of Socs2-/- mice. J Endocrinol. 2014; 223:93-106.
31. Huesa C, Yadav MC, Finnilä MAJ, et al. PHOSPHO1 is essential for mechanically competent mineralization and the avoidance of spontaneous fractures. Bone. 2011;48:1066-1074.
32. Bouxsein ML, Boyd SK, Christiansen BA, et al. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. 2010;25:1468-1486.
33. Compston JE, Judd D, Crawley EO, et al. Osteoporosis in patients with inflammatory bowel disease. Gut. 1987;28:410-415.
34. Tsampalieros A, Lam CK, Spencer JC, et al. Long-term inflammation and glucocorticoid therapy impair skeletal modeling during growth in childhood Crohn disease. J Clin Endocrinol Metab. 2013;98:3438-3445.
35. Dubner SE, Shults J, Baldassano RN, et al. Longitudinal assessment of bone density and structure in an incident cohort of children with Crohn's disease. Gastroenterology. 2009;136:123-130.
36. Wong S, Catto-Smith AGA, Zacharin M. Pathological fractures in paediatric patients with inflammatory bowel disease. Eur J Pediatr. 2014;173: 141-151.
37. Laakso S, Valta H, Verkasalo M, et al. Impaired bone health in inflammatory bowel disease: A case-control study in 80 pediatric patients. Calcif Tissue Int. 2012;91:121-130.
38. Laakso S, Valta H, Verkasalo M, et al. Compromised peak bone mass in patients with inflammatory bowel disease-a prospective study. J Pediatr. 2014;164:1436-1443.
39. Bernstein CN, Leslie WD. The pathophysiology of bone disease in gastrointestinal disease. Eur J Gastroenterol Hepatol. 2003;15:857-864.
40. Kotlarz D, Beier R, Murugan D, et al. Loss of interleukin-10 signaling and infantile inflammatory bowel disease: implications for diagnosis and therapy. Gastroenterology. 2012;143:347-355.
41. Glocker EO, Kotlarz D, Boztug K, et al. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Engl J Med. 2009;361: 2033-2045.
42. Shah N, Kammermeier J, Elawad M, et al. Interleukin-10 and interleukin- 10-receptor defects in inflammatory bowel disease. Curr Allergy Asthma Rep. 2012;12:373-379.
43. Barrett JC, Hansoul S, Nicolae DL, et al. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat Genet. 2008;40:955-962.
44. Jostins L, Ripke S, Weersma RK, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491:119-124.
45. Meyer A, Ramzan N, Heigh R, et al. Relapse of inflammatory bowel disease associated with use of nonsteroidal anti-inflammatory drugs. Dig Dis Sci. 2006;51:168-172.
46. Kaufmann HJ, Taubin HL. Nonsteroidal anti-inflammatory drugs activate quiescent inflammatory bowel disease. Ann Intern Med. 1987;107:513-516.
47. Evans KE, Fox SW. Interleukin-10 inhibits osteoclastogenesis by reducing NFATc1 expression and preventing its translocation to the nucleus. BMC Cell Biol. 2007;8:4.
48. Xu LX, Kukita T, Kukita A, et al. Interleukin-10 selectively inhibits osteoclastogenesis by inhibiting differentiation of osteoclast progenitors into preosteoclast-like cells in rat bone marrow culture system. J Cell Physiol. 1995;165:624-629.
49. Sellon RK, Tonkonogy S, Schultz M, et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun. 1998;66: 5224-5231.
50. Kuhn R, Lohler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75:263-274.
51. Chichlowski M, Sharp JM, Vanderford DA, et al. Helicobacter typhlonius and Helicobacter rodentium differentially affect the severity of colon inflammation and inflammation-associated neoplasia in IL10-deficient mice. Comp Med. 2008;58:534-541.
52. Konstantinidis I, Papageorgiou SN, Kyrgidis A, et al. Effect of nonsteroidal anti-inflammatory drugs on bone turnover: An evidence-based review. Rev Recent Clin Trials. 2013;8:48-60.
53. Barry S. Non-steroidal anti-inflammatory drugs inhibit bone healing: A review. Vet Comp Orthop Traumatol. 2010;23:385-392.
54. Bauer DC, Orwoll ES, Fox KM, et al. Aspirin and NSAID use in older women: effect on bone mineral density and fracture risk. J Bone Miner Res. 1996;11:29-35.
55. Harris L, Senagore P, Young VB, et al. Inflammatory bowel disease causes reversible suppression of osteoblast and chondrocyte function in mice. Am J Physiol Gastrointest Liver Physiol. 2009;296:G1020-G1029.
56. Clarke B. Normal bone anatomy and physiology. Clin J Am Soc Nephrol. 2008;3(suppl 3):S131-S139.
57. Christenson RH. Biochemical markers of bone metabolism: An overview. Clin Biochem. 1997;30:573-593.
58. Roberts-Thomson IC, Fon J, Uylaki W, et al. Cells, cytokines and inflammatory bowel disease: A clinical perspective. Expert Rev Gastroenterol Hepatol. 2011;5:703-716.
59. Schulte CMS, Dignass AU, Goebell H, et al. Genetic factors determine extent of bone loss in inflammatory bowel disease. Gastroenterology. 2000;119:909-920.
60. Lacey DL, Boyle WJ, Simonet WS, et al. Bench to bedside: elucidation of the OPG-RANK-RANKL pathway and the development of denosumab. Nat Rev Drug Discov. 2012;11:401-419.
61. Gallagher JC, Sai AJ. Molecular biology of bone remodeling: Implications for new therapeutic targets for osteoporosis. Maturitas. 2010;65: 301-307.
62. Lee MS, Kim HS, Yeon JT, et al. GM-CSF regulates fusion of mononuclear osteoclasts into bone-resorbing osteoclasts by activating the Ras/ERK pathway. J Immunol. 2009;183:3390-3399.
63. Moschen AR, Kaser A, Enrich B, et al. The RANKL/OPG system is activated in inflammatory bowel disease and relates to the state of bone loss. Gut. 2005;54:479-487.
64. Wong SC, Smyth A, McNeill E, et al. The growth hormone insulin-like growth factor 1 axis in children and adolescents with inflammatory bowel disease and growth retardation. Clin Endocrinol. 2010;73:220-228.