Skeletal consequences of RANKL-blocking antibody (IK22-5) injections during growth: Mouse strain disparities and synergic effect with zoledronic acid

Bone

Volumn 73, Issue , 2015, Pages 51-59

  Lézot, Frédéric ^a,b   Chesneau, Julie ^a,b   Navet, Benjamin ^a,b   Gobin, Bérengère ^a,b   Amiaud, Jérome ^a,b   Choi, YongWon ^c   Yagita, Hideo ^d   Castaneda, Beatriz ^e,f   Berdal, Ariane ^e   Mueller, Christopher G ^g   Rédini, Françoise ^a,b   Heymann, Dominique ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e CENTRE DE RECHERCHE DES CORDELIERS   (France)

^f UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^g UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Bone resorption; RANKL; Side effect; Skeleton growth; Zoledronic acid

Indexed keywords

BISPHOSPHONIC ACID DERIVATIVE; BLOCKING ANTIBODY; OSTEOCLAST DIFFERENTIATION FACTOR BLOCKING ANTIBODY; UNCLASSIFIED DRUG; ZOLEDRONIC ACID; ANTIBODY; BONE DENSITY CONSERVATION AGENT; IMIDAZOLE DERIVATIVE; OSTEOCLAST DIFFERENTIATION FACTOR; TNFSF11 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE GROWTH; BONE TISSUE; CONTROLLED STUDY; FACIAL BONE; FEMALE; GROWTH DISORDER; LONG BONE; MALE; MOUSE; NEWBORN; NONHUMAN; OSTEOLYSIS; SKULL; TIBIA; TOOTH; TOOTH DISEASE; TOOTH ERUPTION; ANIMAL; BONE DEVELOPMENT; C57BL MOUSE; DRUG EFFECTS; IMMUNOLOGY; PREGNANCY;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; BONE DENSITY CONSERVATION AGENTS; BONE DEVELOPMENT; DIPHOSPHONATES; FEMALE; IMIDAZOLES; MICE; MICE, INBRED C57BL; PREGNANCY; RANK LIGAND; TOOTH ERUPTION;

EID: 84920269177     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2014.12.011     Document Type: Article

References (70)

1. Silverman S.L. Bisphosphonate use in conditions other than osteoporosis. Ann N Y Acad Sci 2011, 1218:33-37. 10.1111/j.1749-6632.2010.05769.x.
2. Tella S.H., Gallagher J.C. Prevention and treatment of postmenopausal osteoporosis. J Steroid Biochem Mol Biol 2013, 10.1016/j.jsbmb.2013.09.008.
3. Zwolak P., Dudek A.Z. Antineoplastic activity of zoledronic acid and denosumab. Anticancer Res 2013, 33:2981-2988.
4. Eriksen E.F., Halse J., Moen M.H. New developments in the treatment of osteoporosis. Acta Obstet Gynecol Scand 2013, 92:620-636. 10.1111/j.1600-0412.2012.01473.x.
5. Reid I.R., Cornish J. Epidemiology and pathogenesis of osteonecrosis of the jaw. Nat Rev Rheumatol 2012, 8:90-96. 10.1038/nrrheum.2011.181.
6. Barros E.R., Saraiva G.L., de Oliveira T.P., Lazaretti-Castro M. Safety and efficacy of a 1-year treatment with zoledronic acid compared with pamidronate in children with osteogenesis imperfecta. J Pediatr Endocrinol Metab 2012, 25:485-491.
7. Bishop N., Adami S., Ahmed S.F., Antón J., Arundel P., Burren C.P., et al. Risedronate in children with osteogenesis imperfecta: a randomised, double-blind, placebo-controlled trial. Lancet 2013, 382:1424-1432. 10.1016/S0140-6736(13)61091-0.
8. Ward L.M., Rauch F. Oral bisphosphonates for paediatric osteogenesis imperfecta?. Lancet 2013, 382:1388-1389. 10.1016/S0140-6736(13)61531-7.
9. Sousa T., Bompadre V., White K.K. Musculoskeletal functional outcomes in children with osteogenesis imperfecta: associations with disease severity and pamidronate therapy. J Pediatr Orthop 2014, 34:118-122. 10.1097/BPO.0b013e3182a006a0.
10. Demir E., Bereket A., Ozkan B., Topçu M. Effect of alendronate treatment on the clinical picture and bone turnover markers in chronic idiopathic hyperphosphatasia. J Pediatr Endocrinol Metab 2000, 13:217-221.
11. Cundy T., Wheadon L., King A. Treatment of idiopathic hyperphosphatasia with intensive bisphosphonate therapy. J Bone Miner Res 2004, 19:703-711. 10.1359/JBMR.040127.
12. Polyzos S.A., Anastasilakis A.D., Litsas I., Efstathiadou Z., Kita M., Arsos G., et al. Profound hypocalcemia following effective response to zoledronic acid treatment in a patient with juvenile Paget's disease. J Bone Miner Metab 2010, 28:706-712. 10.1007/s00774-010-0198-8.
13. Saki F., Karamizadeh Z., Nasirabadi S., Mumm S., McAlister W.H., Whyte M.P. Juvenile paget's disease in an Iranian kindred with vitamin D deficiency and novel homozygous TNFRSF11B mutation. J Bone Miner Res 2013, 28:1501-1508. 10.1002/jbmr.1868.
14. Goldsby R.E., Fan T.M., Villaluna D., Wagner L.M., Isakoff M.S., Meyer J., et al. Feasibility and dose discovery analysis of zoledronic acid with concurrent chemotherapy in the treatment of newly diagnosed metastatic osteosarcoma: a report from the Children's Oncology Group. Eur J Cancer 2013, 49:2384-2391. 10.1016/j.ejca.2013.03.018.
15. Semler O., Netzer C., Hoyer-Kuhn H., Becker J., Eysel P., Schoenau E. First use of the RANKL antibody denosumab in osteogenesis imperfecta type VI. J Musculoskelet Neuronal Interact 2012, 12:183-188.
16. Chawla S., Henshaw R., Seeger L., Choy E., Blay J.-Y., Ferrari S., et al. Safety and efficacy of denosumab for adults and skeletally mature adolescents with giant cell tumour of bone: interim analysis of an open-label, parallel-group, phase 2 study. Lancet Oncol 2013, 14:901-908. 10.1016/S1470-2045(13)70277-8.
17. Demirsoy U., Karadogan M., Selek O., Anik Y., Aksu G., Müezzinoglu B., et al. Golden bullet-denosumab: early rapid response of metastatic giant cell tumor of the bone. J Pediatr Hematol Oncol 2013, 10.1097/MPH.0000000000000034.
18. Federman N., Brien E.W., Narasimhan V., Dry S.M., Sodhi M., Chawla S.P. Giant cell tumor of bone in childhood: clinical aspects and novel therapeutic targets. Paediatr Drugs 2013, 10.1007/s40272-013-0051-3.
19. Karras N.A., Polgreen L.E., Ogilvie C., Manivel J.C., Skubitz K.M., Lipsitz E. Denosumab treatment of metastatic giant-cell tumor of bone in a 10-year-old girl. J Clin Oncol 2013, 31:e200-e202. 10.1200/JCO.2012.46.4255.
20. Grasemann C., Schündeln M.M., Hövel M., Schweiger B., Bergmann C., Herrmann R., et al. Effects of RANK-ligand antibody (denosumab) treatment on bone turnover markers in a girl with juvenile Paget's disease. J Clin Endocrinol Metab 2013, 98:3121-3126. 10.1210/jc.2013-1143.
21. Lange T., Stehling C., Fröhlich B., Klingenhöfer M., Kunkel P., Schneppenheim R., et al. Denosumab: a potential new and innovative treatment option for aneurysmal bone cysts. Eur Spine J 2013, 22:1417-1422. 10.1007/s00586-013-2715-7.
22. Boyce A.M., Chong W.H., Yao J., Gafni R.I., Kelly M.H., Chamberlain C.E., et al. Denosumab treatment for fibrous dysplasia. J Bone Miner Res 2012, 27:1462-1470. 10.1002/jbmr.1603.
23. Battaglia S., Dumoucel S., Chesneau J., Heymann M.-F., Picarda G., Gouin F., et al. Impact of oncopediatric dosing regimen of zoledronic acid on bone growth: preclinical studies and case report of an osteosarcoma pediatric patient. J Bone Miner Res 2011, 26:2439-2451. 10.1002/jbmr.453.
24. Lézot F., Chesneau J., Battaglia S., Brion R., Castaneda B., Farges J.-C., et al. Preclinical evidence of potential craniofacial adverse effect of zoledronic acid in pediatric patients with bone malignancies. Bone 2014, 68:146-152. 10.1016/j.bone.2014.08.018.
25. Russell R.G.G. Bisphosphonates: from bench to bedside. Ann N Y Acad Sci 2006, 1068:367-401. 10.1196/annals.1346.041.
26. Dougall W.C., Glaccum M., Charrier K., Rohrbach K., Brasel K., De Smedt T., et al. RANK is essential for osteoclast and lymph node development. Genes Dev 1999, 13:2412-2424.
27. Kim D., Mebius R.E., MacMicking J.D., Jung S., Cupedo T., Castellanos Y., et al. Regulation of peripheral lymph node genesis by the tumor necrosis factor family member TRANCE. J Exp Med 2000, 192:1467-1478.
28. Bargman R., Posham R., Boskey A., Carter E., DiCarlo E., Verdelis K., et al. High- and low-dose OPG-Fc cause osteopetrosis-like changes in infant mice. Pediatr Res 2012, 72:495-501. 10.1038/pr.2012.118.
29. Lee J.C., Spiguel L., Shenaq D.S., Zhong M., Wietholt C., He T.-C., et al. Role of RANK-RANKL-OPG axis in cranial suture homeostasis. J Craniofac Surg 2011, 22:699-705. 10.1097/SCS.0b013e3182077fbd.
30. Castaneda B., Simon Y., Jacques J., Hess E., Choi Y.-W., Blin-Wakkach C., et al. Bone resorption control of tooth eruption and root morphogenesis: involvement of the receptor activator of NF-κB (RANK). J Cell Physiol 2011, 226:74-85. 10.1002/jcp.22305.
31. Castaneda B., Simon Y., Ferbus D., Robert B., Chesneau J., Mueller C., et al. Role of RANKL (TNFSF11)-dependent osteopetrosis in the dental phenotype of Msx2 null mutant mice. PLoS One 2013, 8:e80054. 10.1371/journal.pone.0080054.
32. Russell R.G.G. Bisphosphonates: the first 40years. Bone 2011, 49:2-19. 10.1016/j.bone.2011.04.022.
33. Hanley D.A., Adachi J.D., Bell A., Brown V. Denosumab: mechanism of action and clinical outcomes. Int J Clin Pract 2012, 66:1139-1146. 10.1111/ijcp.12022.
34. Ory B., Moriceau G., Trichet V., Blanchard F., Berreur M., Rédini F., et al. Farnesyl diphosphate synthase is involved in the resistance to zoledronic acid of osteosarcoma cells. J Cell Mol Med 2008, 12:928-941. 10.1111/j.1582-4934.2008.00141.x.
35. O'Day K., Gorlick R. Novel therapeutic agents for osteosarcoma. Expert Rev Anticancer Ther 2009, 9:511-523. 10.1586/era.09.7.
36. Morii T., Ohtsuka K., Ohnishi H., Mochizuki K., Satomi K. Inhibition of heat-shock protein 27 expression eliminates drug resistance of osteosarcoma to zoledronic acid. Anticancer Res 2010, 30:3565-3571.
37. Heymann D., Ory B., Blanchard F., Heymann M.-F., Coipeau P., Charrier C., et al. Enhanced tumor regression and tissue repair when zoledronic acid is combined with ifosfamide in rat osteosarcoma. Bone 2005, 37:74-86. 10.1016/j.bone.2005.02.020.
38. Zhou Z., Guan H., Duan X., Kleinerman E.S. Zoledronic acid inhibits primary bone tumor growth in Ewing sarcoma. Cancer 2005, 104:1713-1720. 10.1002/cncr.21383.
39. Kubista B., Trieb K., Sevelda F., Toma C., Arrich F., Heffeter P., et al. Anticancer effects of zoledronic acid against human osteosarcoma cells. J Orthop Res 2006, 24:1145-1152. 10.1002/jor.20129.
40. Iguchi T., Miyakawa Y., Saito K., Nakabayashi C., Nakanishi M., Saya H., et al. Zoledronate-induced S phase arrest and apoptosis accompanied by DNA damage and activation of the ATM/Chk1/cdc25 pathway in human osteosarcoma cells. Int J Oncol 2007, 31:285-291.
41. Labrinidis A., Hay S., Liapis V., Ponomarev V., Findlay D.M., Evdokiou A. Zoledronic acid inhibits both the osteolytic and osteoblastic components of osteosarcoma lesions in a mouse model. Clin Cancer Res 2009, 15:3451-3461. 10.1158/1078-0432.CCR-08-1616.
42. Odri G.A., Dumoucel S., Picarda G., Battaglia S., Lamoureux F., Corradini N., et al. Zoledronic acid as a new adjuvant therapeutic strategy for Ewing's sarcoma patients. Cancer Res 2010, 70:7610-7619. 10.1158/0008-5472.CAN-09-4272.
43. Siddiqui T., Marsh R.de W., Allegra C., Whittaker D., Scarborough M., Gibbs P., et al. Effective salvage treatment of recurrent Ewing sarcoma utilizing chemotherapy and zoledronic acid. Clin Adv Hematol Oncol 2010, 8:499-504.
44. Açil Y., Möller B., Niehoff P., Rachko K., Gassling V., Wiltfang J., et al. The cytotoxic effects of three different bisphosphonates in-vitro on human gingival fibroblasts, osteoblasts and osteogenic sarcoma cells. J Craniomaxillofac Surg 2012, 40:e229-e235. 10.1016/j.jcms.2011.10.024.
45. Chang J., Wang W., Zhang H., Hu Y., Yin Z. Bisphosphonates regulate cell proliferation, apoptosis and pro-osteoclastic expression in MG-63 human osteosarcoma cells. Oncol Lett 2012, 4:299-304. 10.3892/ol.2012.723.
46. Benassi M.S., Chiechi A., Ponticelli F., Pazzaglia L., Gamberi G., Zanella L., et al. Growth inhibition and sensitization to cisplatin by zoledronic acid in osteosarcoma cells. Cancer Lett 2007, 250:194-205. 10.1016/j.canlet.2006.10.004.
47. Moriceau G., Ory B., Mitrofan L., Riganti C., Blanchard F., Brion R., et al. Zoledronic acid potentiates mTOR inhibition and abolishes the resistance of osteosarcoma cells to RAD001 (Everolimus): pivotal role of the prenylation process. Cancer Res 2010, 70:10329-10339. 10.1158/0008-5472.CAN-10-0578.
48. Koto K., Murata H., Kimura S., Horie N., Matsui T., Nishigaki Y., et al. Zoledronic acid inhibits proliferation of human fibrosarcoma cells with induction of apoptosis, and shows combined effects with other anticancer agents. Oncol Rep 2010, 24:233-239.
49. Ryu K., Murata H., Koto K., Horie N., Matsui T., Nishigaki Y., et al. Combined effects of bisphosphonate and radiation on osteosarcoma cells. Anticancer Res 2010, 30:2713-2720.
50. Li Z., Peng H., Xu Q., Ye Z. Sensitization of human osteosarcoma cells to Vγ9Vδ2 T-cell-mediated cytotoxicity by zoledronate. J Orthop Res 2012, 30:824-830. 10.1002/jor.21579.
51. Dos Santos M.P., de Farias C.B., Roesler R., Brunetto A.L., Abujamra A.L. In vitro antitumor effect of sodium butyrate and zoledronic acid combined with traditional chemotherapeutic drugs: a paradigm of synergistic molecular targeting in the treatment of Ewing sarcoma. Oncol Rep 2014, 31:955-968. 10.3892/or.2013.2907.
52. Wittrant Y., Lamoureux F., Mori K., Riet A., Kamijo A., Heymann D., et al. RANKL directly induces bone morphogenetic protein-2 expression in RANK-expressing POS-1 osteosarcoma cells. Int J Oncol 2006, 28:261-269.
53. Mori K., Ando K., Heymann D., Rédini F. Receptor activator of nuclear factor-kappa B ligand (RANKL) stimulates bone-associated tumors through functional RANK expressed on bone-associated cancer cells?. Histol Histopathol 2009, 24:235-242.
54. Mori K., Le Goff B., Berreur M., Riet A., Moreau A., Blanchard F., et al. Human osteosarcoma cells express functional receptor activator of nuclear factor-kappa B. J Pathol 2007, 211:555-562. 10.1002/path.2140.
55. Mori K., Berreur M., Blanchard F., Chevalier C., Guisle-Marsollier I., Masson M., et al. Receptor activator of nuclear factor-kappaB ligand (RANKL) directly modulates the gene expression profile of RANK-positive Saos-2 human osteosarcoma cells. Oncol Rep 2007, 18:1365-1371.
56. Elias L.S.A., Costa R.F., Carvalho M.A., Batista A.C., Silva T.A., Leles C.R., et al. Markers of bone remodeling in neoplastic and bone-related lesions. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010, 110:624-631. 10.1016/j.tripleo.2010.06.014.
57. Hanada R., Hanada T., Penninger J.M. Physiology and pathophysiology of the RANKL/RANK system. Biol Chem 2010, 391:1365-1370. 10.1515/BC.2010.149.
58. Hanada R., Hanada T., Sigl V., Schramek D., Penninger J.M. RANKL/RANK-beyond bones. J Mol Med 2011, 89:647-656. 10.1007/s00109-011-0749-z.
59. Hanada R., Leibbrandt A., Hanada T., Kitaoka S., Furuyashiki T., Fujihara H., et al. Central control of fever and female body temperature by RANKL/RANK. Nature 2009, 462:505-509. 10.1038/nature08596.
60. Gutierrez H., Kisiswa L., O'Keeffe G.W., Smithen M.J., Wyatt S., Davies A.M. Regulation of neurite growth by tumour necrosis superfamily member RANKL. Open Biol 2013, 3:120150. 10.1098/rsob.120150.
61. Kong Y.Y., Yoshida H., Sarosi I., Tan H.L., Timms E., Capparelli C., et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 1999, 397:315-323. 10.1038/16852.
62. Hess E., Duheron V., Decossas M., Lézot F., Berdal A., Chea S., et al. RANKL induces organized lymph node growth by stromal cell proliferation. J Immunol 2012, 188:1245-1254. 10.4049/jimmunol.1101513.
63. Mueller C.G., Hess E. Emerging functions of RANKL in lymphoid tissues. Front Immunol 2012, 3:261. 10.3389/fimmu.2012.00261.
64. Sugiyama M., Nakato G., Jinnohara T., Akiba H., Okumura K., Ohno H., et al. Expression pattern changes and function of RANKL during mouse lymph node microarchitecture development. Int Immunol 2012, 24:369-378. 10.1093/intimm/dxs002.
65. Loser K., Mehling A., Loeser S., Apelt J., Kuhn A., Grabbe S., et al. Epidermal RANKL controls regulatory T-cell numbers via activation of dendritic cells. Nat Med 2006, 12:1372-1379. 10.1038/nm1518.
66. Yamaguchi T., Sakaguchi S. Skin controls immune regulators. Nat Med 2006, 12:1358-1359. 10.1038/nm1206-1358.
67. Barbaroux J.-B.O., Beleut M., Brisken C., Mueller C.G., Groves R.W. Epidermal receptor activator of NF-kappaB ligand controls Langerhans cells numbers and proliferation. J Immunol 2008, 181:1103-1108.
68. Duheron V., Hess E., Duval M., Decossas M., Castaneda B., Klöpper J.E., et al. Receptor activator of NF-kappaB (RANK) stimulates the proliferation of epithelial cells of the epidermo-pilosebaceous unit. Proc Natl Acad Sci U S A 2011, 108:5342-5347. 10.1073/pnas.1013054108.
69. Leibbrandt A., Penninger J.M. Novel functions of RANK(L) signaling in the immune system. Adv Exp Med Biol 2010, 658:77-94. 10.1007/978-1-4419-1050-9_9.
70. Akiyama T., Shinzawa M., Akiyama N. RANKL-RANK interaction in immune regulatory systems. World J Orthop 2012, 3:142-150. 10.5312/wjo.v3.i9.142.