Bone, inflammation, and inflammatory bowel disease

Current Osteoporosis Reports

Volumn 9, Issue 4, 2011, Pages 251-257

  Agrawal, Manasi ^a   Arora, Shitij ^b   Li, Jianjun ^a   Rahmani, Rabin ^a   Sun, Li ^c   Steinlauf, Adam F ^c   Mechanick, Jeffrey I ^c   Zaidi, Mone ^c  

^a MAIMONIDES MEDICAL CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Bone; Bone loss; Cytokines; Inflammation; Inflammatory bowel disease; Osteoblast; Osteoclast

Indexed keywords

BISPHOSPHONIC ACID DERIVATIVE; C REACTIVE PROTEIN; INFLIXIMAB; INTERLEUKIN 1BETA; INTERLEUKIN 6; KLOTHO PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PHOSPHATE REGULATING NEUTRAL ENDOPEPTIDASE; PREDNISONE; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; SOMATOMEDIN; SOMATOMEDIN BINDING PROTEIN; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BONE DENSITY; COMBINATION CHEMOTHERAPY; DISEASE ASSOCIATION; DOWN REGULATION; ENTERITIS; HUMAN; INFLAMMATION; MOLECULAR INTERACTION; MONOTHERAPY; MORBIDITY; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPENIA; OSTEOPOROSIS; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

CELL COMMUNICATION; HUMANS; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; OSTEOBLASTS; OSTEOCLASTS; OSTEOPOROSIS; SIGNAL TRANSDUCTION; VITAMIN D DEFICIENCY;

EID: 81255142138     PISSN: 15441873     EISSN: 15442241     Source Type: Journal    
DOI: 10.1007/s11914-011-0077-9     Document Type: Article

References (57)

1. EFFO and NOF 1997 Who are candidates for prevention and treatment for osteoporosis? Osteoporos Int 7 1 1 6 10.1007/BF01623453 (Pubitemid 27077780)
2. R Burge B Dawson-Hughes DH Solomon, et al. 2007 Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025 J Bone Miner Res 22 465 17144789 10.1359/jbmr.061113 (Pubitemid 46797130)
3. IR Reid 1997 Glucocorticoid osteoporosis - mechanisms and management Eur J Endocrinol 137 209 9330580 10.1530/eje.0.1370209 1:CAS:528:DyaK2sXntVyksrk%3D (Pubitemid 27405101)
4. M Pazianas M Zaidi JM Subhani PJ Finch L Ang JD Maxwell 2003 Efferent loop small intestinal vitamin D receptor concentration and bone mineral density after Billroth II (Polya) gastrectomy in humans Calcif Tissue Int 72 4 485 90 12574872 10.1007/s00223-001-2135-2 1:CAS:528:DC%2BD3sXjt1aktr8%3D (Pubitemid 36919514)
5. C Schulte AU Dignass K Mann H Goebell 1998 Reduced bone mineral density and unbalanced bone metabolism in patients with inflammatory bowel disease Inflamm Bowel Dis 4 4 268 75 9836078 10.1002/ibd.3780040403 1:STN:280: DyaK1M%2Flt1Oqug%3D%3D (Pubitemid 128699865)
6. B Shen FH Remzi IK Oikonomou H Lu BA Lashner JP Hammel M Skugor AE Bennett A Brzezinski E Queener VW Fazio 2009 Risk factors for low bone mass in patients with ulcerative colitis following ileal pouch-anal anastomosis Am J Gastroenterol 104 3 639 46 19262520 10.1038/ajg.2008.78
7. AS Tignor BU Wu TL Whitlock R Lopez K Repas PA Banks D Conwell 2010 High prevalence of low-trauma fracture in chronic pancreatitis Am J Gastroenterol 105 12 2680 6 20736937 10.1038/ajg.2010.325
8. LM Ward F Rauch MA Matzinger EI Benchimol M Boland DR Mack 2010 Iliac bone histomorphometry in children with newly diagnosed inflammatory bowel disease Osteoporos Int 21 331 337 19504034 10.1007/s00198-009-0969-z 1:STN:280:DC%2BC3c%2Fgtl2ktw%3D%3D
9. J Turner G Pellerin D Mager 2009 Prevalence of metabolic bone disease in children with celiac disease is independent of symptoms at diagnosis J Pediatr Gastroenterol Nutr 49 5 589 93 19644400 10.1097/MPG.0b013e31819ca18e
10. AE Oostlander, et al. 2011 Dutch Initiative on Crohn and Colitis (ICC). Histomorphometric analysis reveals reduced bone mass and bone formation in patients with quiescent Crohn's disease Gastroenterology 140 1 116 23 20854819 10.1053/j.gastro.2010.09.007 This study identifies that bone loss occurs even before clinically significant bowel disease has occurred, implicating chronic inflammation as the earliest cause for metabolic bone disease in IBD
11. JD Godfrey, et al. 2010 Morbidity and mortality among older individuals with undiagnosed celiac disease Gastroenterology 139 3 763 9 20685275 10.1053/j.gastro.2010.05.041
12. M Pazianas GP Butcher JM Subhani PJ Finch L Ang C Collins RP Heaney M Zaidi JD Maxwell 2005 Calcium absorption and bone mineral density in celiacs after long term treatment with gluten-free diet and adequate calcium intake Osteoporos Int 16 1 56 63 15221205 10.1007/s00198-004-1641-2 1:CAS:528:DC%2BD2MXntF2msQ%3D%3D (Pubitemid 40193219)
13. RJ Weiss MC Wick PW Ackermann SM Montgomery 2010 Increased fracture risk in patients with rheumatic disorders and other inflammatory diseases-a case-control study with 53,108 patients with fracture J Rheumatol 37 11 2247 50 20889599 10.3899/jrheum.100363
14. AJ Ashcroft, et al. 2003 Colonic dendritic cells, intestinal inflammation, and T cell-mediated bone destruction are modulated by recombinant osteoprotegerin Immunity 19 6 849 61 14670302 10.1016/S1074-7613(03)00326-1 1:CAS:528:DC%2BD3sXhtVWnsrjP (Pubitemid 37542305)
15. AR Moschen, et al. 2005 The RANKL/OPG system is activated in inflammatory bowel disease and relates to the state of bone loss Gut 54 4 479 87 15753532 10.1136/gut.2004.044370 1:CAS:528:DC%2BD2MXjtFamsrs%3D (Pubitemid 40395499)
16. P Miheller, et al. 2007 Changes of OPG and RANKL concentrations in Crohn's disease after infliximab therapy Inflamm Bowel Dis 13 11 1379 84 17663430 10.1002/ibd.20234 This study demonstrates that IBD treatment targeted at inflammatory cytokines can alter bone metabolism favorably, thereby establishing inflammation as a cause for bone loss (Pubitemid 350206849)
17. M Paganelli, et al. 2007 Inflammation is the main determinant of low bone mineral density in pediatric inflammatory bowel disease Inflamm Bowel Dis 13 4 416 23 17206686 10.1002/ibd.20039 (Pubitemid 46668246)
18. S Kumar BJ Votta DJ Rieman AM Badger M Gowen JC Lee 2001 IL-1- and TNF-induced bone resorption is mediated by p38 mitogen activated protein kinase J Cell Physiol 187 3 294 303 11319753 10.1002/jcp.1082 1:CAS:528: DC%2BD3MXjtF2itr4%3D (Pubitemid 32378354)
19. L Rovedatti, et al. 2009 Differential regulation of interleukin 17 and interferon gamma production in inflammatory bowel disease Gut 58 12 1629 36 19740775 10.1136/gut.2009.182170 1:CAS:528:DC%2BD1MXhs1SjtbjE
20. YH Zhang A Heulsmann MM Tondravi A Mukherjee Y Abu-Amer 2001 Tumor necrosis factor-alpha (TNF) stimulates RANKL-induced osteoclastogenesis via coupling of TNF type 1 receptor and RANK signaling pathways J Biol Chem 276 1 563 8 11032840 10.1074/jbc.M008198200 1:CAS:528:DC%2BD3MXmtFSquw%3D%3D (Pubitemid 32050352)
21. YR Mahida K Wu DP Jewell 1989 Enhanced production of interleukin 1-beta by mononuclear cells isolated from mucosa with active ulcerative colitis of Crohn's disease Gut 30 835 838 2787769 10.1136/gut.30.6.835 1:CAS:528: DyaL1MXkslKgsrg%3D (Pubitemid 19167787)
22. A Nemetz M Tóth MA García-González T Zágoni J Fehér AS Peña Z Tulassay 2001 Allelic variation at the interleukin 1beta gene is associated with decreased bone mass in patients with inflammatory bowel diseases Gut 49 5 644 9 11600466 10.1136/gut.49.5.644 1:CAS:528:DC%2BD3MXosVWqtro%3D (Pubitemid 32989200)
23. K Kusugami, et al. 1995 Elevation of interleukin-6 in inflammatory bowel disease is macrophage- and epithelial cell-dependent Dig Dis Sci 40 5 949 59 7729284 10.1007/BF02064182 1:STN:280:DyaK2M3ks1Gkug%3D%3D
24. C Shen CJ Landers C Derkowski CO Elson SR Targan 2008 Enhanced CBir1- specific innate and adaptive immune responses in Crohn's disease Inflamm Bowel Dis 14 12 1641 51 18825772 10.1002/ibd.20645
25. SR Targan CJ Landers H Yang, et al. 2005 Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn's disease Gastroenterology 128 2020 2028 15940634 10.1053/j.gastro.2005. 03.046 1:CAS:528:DC%2BD2MXlvFKltrs%3D (Pubitemid 40824710)
26. R Axmann C Böhm G Krönke J Zwerina J Smolen G Schett 2009 Inhibition of interleukin-6 receptor directly blocks OC formation in vitro and in vivo Arthritis Rheum 60 9 2747 56 19714627 10.1002/art.24781 1:CAS:528:DC%2BD1MXht1WhtLbJ
27. P Garnero E Thompson T Woodworth JS Smolen 2010 Rapid and sustained improvement in bone and cartilage turnover markers with the anti-interleukin-6 receptor inhibitor tocilizumab plus methotrexate in rheumatoid arthritis patients with an inadequate response to methotrexate: results from a substudy of the multicenter double-blind, placebo-controlled trial of tocilizumab in inadequate responders to methotrexate alone Arthritis Rheum 62 1 33 43 20039425 10.1002/art.25053 1:CAS:528:DC%2BC3cXhtFGnurnI
28. J Li, et al. 2000 RANK is the intrinsic hematopoietic cell surface receptor that controls osteoclastogenesis and regulation of bone mass and calcium metabolism Proc Natl Acad Sci USA 97 1566 1571 10677500 10.1073/pnas.97.4.1566 1:CAS:528:DC%2BD3cXhsFCrsL4%3D (Pubitemid 30118482)
29. K Fuller C Murphy B Kirstein SW Fox TJ Chambers 2002 TNFα potently activates osteoclasts, through a direct action independent of and strongly synergistic with RANKL Endocrinology 143 1108 1118 11861538 10.1210/en.143.3. 1108 1:CAS:528:DC%2BD38XhvVeisLY%3D (Pubitemid 34164059)
30. J Lam S Takeshita JE Barker O Kanagawa FP Ross SL Teitelbaum 2000 TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand J Clin Invest 106 1481 1488 11120755 10.1172/JCI11176 1:CAS:528:DC%2BD3cXovFagtbo%3D (Pubitemid 32038586)
31. MS Friedman SM Oyserman KD Hankenson 2009 Wnt11 promotes osteoblast maturation and mineralization through R-spondin 2 J Biol Chem 284 21 14117 25 19213727 10.1074/jbc.M808337200 1:CAS:528:DC%2BD1MXlvV2jtb4%3D
32. M Thayu MB Leonard JS Hyams WV Crandall S Kugathasan AR Otley A Olson J Johanns CW Marano RB Heuschkel G Veereman-Wauters AM Griffiths RN Baldassano Reach Study Group 2008 Improvement in biomarkers of bone formation during infliximab therapy in pediatric Crohn's disease: results of the REACH study Clin Gastroenterol Hepatol 6 12 1378 84 19081527 10.1016/j.cgh.2008.07.010 1:CAS:528:DC%2BD1MXhtFSlurc%3D
33. M Bernstein S Irwin GR Greenberg 2005 Maintenance infliximab treatment is associated with improved bone mineral density in Crohn's disease Am J Gastroenterol 100 9 2031 5 16128948 10.1111/j.1572-0241.2005.50219.x 1:CAS:528:DC%2BD2MXhtFWmsL%2FL This study corroborates inflammation as a major cause of bone disease in IBD, and its reversal with blocking TNF-α with infliximab
34. M Pazianas AD Rhim AM Weinberg C Su GR Lichtenstein 2006 The effect of anti-TNF-alpha therapy on spinal bone mineral density in patients with Crohn's disease Ann N Y Acad Sci 1068 543 56 16831950 10.1196/annals.1346.055 1:CAS:528:DC%2BD28XntFemsrs%3D (Pubitemid 43832924)
35. SC Wong A Smyth E McNeill PJ Galloway K Hassan P McGrogan SF Ahmed 2010 The growth hormone insulin-like growth factor 1 axis in children and adolescents with inflammatory bowel disease and growth retardation Clin Endocrinol (Oxf) 73 2 220 8 1:CAS:528:DC%2BC3cXhtFSmtb7J
36. M Eivindson H Grønbaek A Flyvbjerg J Frystyk E Zimmermann-Nielsen JF Dahlerup 2007 The insulin-like growth factor (IGF)-system in active ulcerative colitis and Crohn's disease: relations to disease activity and corticosteroid treatment Growth Horm IGF Res 17 1 33 40 17126585 10.1016/j.ghir.2006.10.003 1:CAS:528:DC%2BD2sXitl2itbg%3D
37. ME Street, et al. 2004 Relationships between serum IGF-1, IGFBP-2, interleukin-1beta and interleukin-6 in inflammatory bowel disease Horm Res 61 4 159 64 14691340 10.1159/000075699 1:CAS:528:DC%2BD2cXisFOru7k%3D (Pubitemid 38437684)
38. MR Corkins AD Gohil JF Fitzgerald 2003 The insulin-like growth factor axis in children with inflammatory bowel disease J Pediatr Gastroenterol Nutr 36 2 228 34 12548059 10.1097/00005176-200302000-00014 1:CAS:528: DC%2BD3sXmtVWlsQ%3D%3D (Pubitemid 39272975)
39. A Ballinger 2002 Fundamental mechanisms of growth failure in inflammatory bowel disease Horm Res 58 Suppl 1 7 10 12373006 10.1159/000064756 1:CAS:528:DC%2BD38XnslWqsrg%3D (Pubitemid 35316829)
40. Wolf M, Bohm S, Brand M, Kreymann G. Proinflammatory cytokines interleukin 1 beta and tumor necrosis factor alpha inhibit growth hormone stimulation of Insulin-like growth factor I synthesis and growth hormone receptor mRNA levels in cultured rat liver cells. Eur J Endocrinol. 1996;135729-737.
41. P Sarzi-Puttini F Atzeni J Schölmerich M Cutolo RH Straub 2006 Anti-TNF antibody treatment improves glucocorticoid induced insulin-like growth factor 1 (IGF1) resistance without influencing myoglobin and IGF1 binding proteins 1 and 3 Ann Rheum Dis 65 3 301 5 16079165 10.1136/ard.2005.040816 1:CAS:528:DC%2BD28XisFCjt7s%3D (Pubitemid 43268216)
42. A gene (PEX) with homologies to endopeptidases is mutated in patients with X-linked hypophosphatemic rickets. The HYP Consortium. Nat Genet. 1995;11(2):130-6.
43. PM Majewski RD Thurston R Ramalingam PR Kiela FK Ghishan 2010 Cooperative role of NF-κB and poly(ADP-ribose) polymerase 1 (PARP-1) in the TNF-induced inhibition of PHEX expression in osteoblasts J Biol Chem 285 45 34828 38 20817730 10.1074/jbc.M110.152868 1:CAS:528:DC%2BC3cXhtlGktbvP This study identifies another mechanism by which TNF mediates bone loss in IBD, and implicates NF-κB and PARP-1 in the same, raising the possibility of therapeutic intervention.
44. H Hanai T Iida K Takeuchi F Watanabe Y Maruyama A Andoh T Tsujikawa Y Fujiyama K Mitsuyama M Sata M Yamada Y Iwaoka K Kanke H Hiraishi K Hirayama H Arai S Yoshii M Uchijima T Nagata Y Koide 2006 Curcumin maintenance therapy for ulcerative colitis: randomized, multicenter, double-blind, placebo-controlled trial Clin Gastroenterol Hepatol 4 12 1502 6 17101300 10.1016/j.cgh.2006.08.008 1:CAS:528:DC%2BD2sXpsFGlsw%3D%3D (Pubitemid 44880023)
45. JK Uno OI Kolek ER Hines H Xu BN Timmermann PR Kiela FK Ghishan 2006 The role of tumor necrosis factor alpha in down-regulation of osteoblast Phex gene expression in experimental murine colitis Gastroenterology 131 2 497 509 16890604 10.1053/j.gastro.2006.05.020 1:CAS:528:DC%2BD28XpsFyksLk%3D (Pubitemid 44142455)
46. VY Ung RR Foshaug SM MacFarlane TA Churchill JS Doyle BC Sydora RN Fedorak 2010 Oral administration of curcumin emulsified in carboxymethyl cellulose has a potent anti-inflammatory effect in the IL-10 gene-deficient mouse model of IBD Dig Dis Sci 55 5 1272 7 19513843 10.1007/s10620-009-0843-z 1:CAS:528:DC%2BC3cXlsFaitL4%3D This study identifies curcumin as anti-inflammatory in colitis, and further elucidates pathways of inflammation-mediated bone loss
47. A Lubbad MA Oriowo I Khan 2009 Curcumin attenuates inflammation through inhibition of TLR-4 receptor in experimental colitis Mol Cell Biochem 322 1-2 127 35 19002562 10.1007/s11010-008-9949-4 1:CAS:528:DC%2BD1MXhtVWhsbY%3D
48. MV Venkataranganna M Rafiq S Gopumadhavan G Peer UV Babu SK Mitra 2007 NCB-02 (standardized Curcumin preparation) protects dinitrochlorobenzene- induced colitis through down-regulation of NFkappa-B and iNOS World J Gastroenterol 13 7 1103 7 17373747 1:CAS:528:DC%2BD2sXkvVajuro%3D (Pubitemid 46511014)
49. L Camacho-Barquero I Villegas JM Sánchez-Calvo E Talero S Sánchez-Fidalgo V Motilva C Alarcón de la Lastra 2007 Curcumin, a Curcuma longa constituent, acts on MAPK p38 pathway modulating COX-2 and iNOS expression in chronic experimental colitis Int Immunopharmacol 7 3 333 42 17276891 10.1016/j.intimp.2006.11.006 1:CAS:528:DC%2BD2sXhtlSlt7Y%3D (Pubitemid 46186172)
50. ZS Xiao M Crenshaw R Guo T Nesbitt MK Drezner LD Quarles 1998 Intrinsic mineralization defect in Hyp mouse osteoblasts Am J Physiol 275 4 Pt 1 E700 8 9755091 1:CAS:528:DyaK1cXmsl2itr0%3D
51. JS Hyams N Wyzga DL Kreutzer CJ Justinich GA Gronowicz 1997 Alterations in bone metabolism in children with inflammatory bowel disease: an in vitro study J Pediatr Gastroenterol Nutr 24 3 289 95 9138175 10.1097/00005176- 199703000-00011 1:CAS:528:DyaK2sXjt1artLs%3D (Pubitemid 27199618)
52. S Varghese N Wyzga AM Griffiths FA Sylvester 2002 Effects of serum from children with newly diagnosed Crohn disease on primary cultures of rat osteoblasts J Pediatr Gastroenterol Nutr 35 5 641 8 12454579 10.1097/00005176-200211000-00010 1:CAS:528:DC%2BD38XptVShsbk%3D (Pubitemid 35417735)
53. J Chang Z Wang E Tang Z Fan L McCauley R Franceschi K Guan PH Krebsbach CY Wang 2009 Inhibition of osteoblastic bone formation by nuclear factor-kappaB Nat Med 15 6 682 9 19448637 10.1038/nm.1954 1:CAS:528:DC%2BD1MXmtVOqsrk%3D This study implicates NF-κB in bone loss and identifies it as a point of therapeutic intervention
54. W Jochum JP David C Elliott A Wutz H Plenk Jr K Matsuo EF Wagner 2000 Increased bone formation and osteosclerosis in mice overexpressing the transcription factor Fra-1 Nat Med 6 9 980 4 10973316 10.1038/79676 1:CAS:528:DC%2BD3cXms12lt7s%3D
55. R Eferl A Hoebertz AF Schilling M Rath F Karreth L Kenner M Amling EF Wagner 2004 The Fos-related antigen Fra-1 is an activator of bone matrix formation EMBO J 23 14 2789 99 15229648 10.1038/sj.emboj.7600282 1:CAS:528:DC%2BD2cXlvValtrs%3D (Pubitemid 39013551)
56. •• Thurston RD, Larmonier CB, Majewski PM, Ramalingam R, Midura-Kiela M, Laubitz D, Vandewalle A, Besselsen DG, Mühlbauer M, Jobin C, Kiela PR, Ghishan FK. Tumor necrosis factor and interferon-gamma down-regulate Klotho in mice with colitis. Gastroenterology. 2010;138(4):1384-94, 1394. This study identifies the role of Klotho, a novel pathway, in inflammation-mediated bone loss in IBD.
57. Y Maekawa K Ishikawa O Yasuda R Oguro H Hanasaki I Kida Y Takemura M Ohishi T Katsuya H Rakugi 2009 Klotho suppresses TNF-alpha-induced expression of adhesion molecules in the endothelium and attenuates NF-kappaB activation Endocrine 35 3 341 6 19367378 10.1007/s12020-009-9181-3 1:CAS:528: DC%2BD1MXpsVGjsbk%3D