Attenuated Wnt/β-catenin signalling mediates methotrexate chemotherapy-induced bone loss and marrow adiposity in rats

Bone

Volumn 50, Issue 6, 2012, Pages 1223-1233

  Georgiou, Kristen R ^a,b   King, Tristan J ^a,b   Scherer, Michaela A ^a,c   Zhou, Hong ^d   Foster, Bruce K ^c   Xian, Cory J ^a,b,c  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c WOMEN S AND CHILDREN S HOSPITAL   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Adipogenesis; Cancer chemotherapy; Osteoclastogenesis; Osteogenesis; Wnt signalling

Indexed keywords

BETA CATENIN; CYCLIN D1; DICKKOPF 1 PROTEIN; MESSENGER RNA; METHOTREXATE; RNA; SECRETED FRIZZLED RELATED PROTEIN 1; WNT PROTEIN;

ADIPOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MARROW; BONE MARROW CELL; CANCER CHEMOTHERAPY; CELL DENSITY; CELL DIFFERENTIATION; COLONY FORMING UNIT; CONTROLLED STUDY; EX VIVO STUDY; GENE; GRANULOCYTE; HEMATOPOIETIC CELL; LEF 1 GENE; MACROPHAGE; MALE; MORPHOMETRICS; NONHUMAN; OSTEOCLASTOGENESIS; OSTEOLYSIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; STROMA CELL;

ADIPOGENESIS; ADIPOSITY; ANIMALS; ANTINEOPLASTIC AGENTS; BETA CATENIN; BONE AND BONES; BONE MARROW; BONE RESORPTION; CELL DIFFERENTIATION; GLYCOGEN SYNTHASE KINASE 3; HEMATOPOIESIS; MALE; METHOTREXATE; MODELS, ANIMAL; OSTEOBLASTS; OSTEOCLASTS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; WNT SIGNALING PATHWAY;

EID: 84859647462     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2012.03.027     Document Type: Article

References (59)

1. Papaconstantinou H.T., Xie C., Zhang W., Ansari N.H., Hellmich M.R., Townsend C.M., et al. The role of caspases in methotrexate-induced gastrointestinal toxicity. Surgery 2001, 130:859-865.
2. Schriock E.A., Schell M.J., Carter M., Hustu O., Ochs J.J. Abnormal growth patterns and adult short stature in 115 long-term survivors of childhood leukemia. J Clin Oncol 1991, 9:400-405.
3. Halton J.M., Atkinson S.A., Fraher L., Webber C., Gill G.J., Dawson S., et al. Altered mineral metabolism and bone mass in children during treatment for acute lymphoblastic leukemia. J Bone Miner Res 1996, 11:1774-1783.
4. Ahmed S.F., Wallace W.H., Kelnar C.J. An anthropometric study of children during intensive chemotherapy for acute lymphoblastic leukaemia. Horm Res 1997, 48:178-183.
5. Haddy T.B., Mosher R.B., Reaman G.H. Osteoporosis in survivors of acute lymphoblastic leukemia. Oncologist 2001, 6:278-285.
6. Wittels B. Bone marrow biopsy changes following chemotherapy for acute leukemia. Am J Surg Pathol 1980, 4:135-142.
7. Brody J.P., Krause J.R., Penchansky L. Bone marrow response to chemotherapy in acute lymphocytic leukaemia and acute non-lymphocytic leukaemia. Scand J Haematol 1985, 35:240-245.
8. Gerard E.L., Ferry J.A., Amrein P.C., Harmon D.C., McKinstry R.C., Hoppel B.E., et al. Compositional changes in vertebral bone marrow during treatment for acute leukemia: assessment with quantitative chemical shift imaging. Radiology 1992, 183:39-46.
9. Fan C., Cool J.C., Scherer M.A., Foster B.K., Shandala T., Tapp H., et al. Damaging effects of chronic low-dose methotrexate usage on primary bone formation in young rats and potential protective effects of folinic acid supplementary treatment. Bone 2009, 44:61-70.
10. Xian C.J., Cool J.C., Scherer M.A., Fan C., Foster B.K. Folinic acid attenuates methotrexate chemotherapy-induced damages on bone growth mechanisms and pools of bone marrow stromal cells. J Cell Physiol 2008, 214:777-785.
11. Xian C.J., Cool J.C., Scherer M.A., Macsai C.E., Fan C., Covino M., et al. Cellular mechanisms for methotrexate chemotherapy-induced bone growth defects. Bone 2007, 41:842-850.
12. Georgiou K.R., Scherer M.A., Fan C.M., Cool J.C., King T.J., Foster B.K., et al. Methotrexate chemotherapy reduces osteogenesis but increases adipogenic potential in the bone marrow. J Cell Physiol 2012, 227:909-918.
13. Friedenstein A.J., Chailakhjan R.K., Lalykina K.S. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 1970, 3:393-403.
14. Owen M., Friedenstein A.J. Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found Symp 1988, 136:42-60.
15. Bennett C.N., Longo K.A., Wright W.S., Suva L.J., Lane T.F., Hankenson K.D., et al. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci U S A 2005, 102:3324-3329.
16. Das B., Antoon R., Tsuchida R., Lotfi S., Morozova O., Farhat W., et al. Squalene selectively protects mouse bone marrow progenitors against cisplatin and carboplatin-induced cytotoxicity in vivo without protecting tumor growth. Neoplasia 2008, 10:1105-1119.
17. Georgiou K.R., Foster B.K., Xian C.J. Damage and recovery of the bone marrow microenvironment induced by cancer chemotherapy - potential regulatory role of chemokine CXCL12/receptor CXCR4 signalling. Curr Mol Med 2010, 10:440-453.
18. Kulkarni N.H., Onyia J.E., Zeng Q., Tian X., Liu M., Halladay D.L., et al. Orally bioavailable GSK-3alpha/beta dual inhibitor increases markers of cellular differentiation in vitro and bone mass in vivo. J Bone Miner Res 2006, 21:910-920.
19. Reya T., Duncan A.W., Ailles L., Domen J., Scherer D.C., Willert K., et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 2003, 423:409-414.
20. Bodine P.V., Komm B.S. Wnt signaling and osteoblastogenesis. Rev Endocr Metab Disord 2006, 7:33-39.
21. Glass D.A., Karsenty G. In vivo analysis of Wnt signaling in bone. Endocrinology 2007, 148:2630-2634.
22. Boyden L.M., Mao J., Belsky J., Mitzner L., Farhi A., Mitnick M.A., et al. High bone density due to a mutation in LDL-receptor-related protein 5. N Engl J Med 2002, 346:1513-1521.
23. Zhou H., Mak W., Zheng Y., Dunstan C.R., Seibel M.J. Osteoblasts directly control lineage commitment of mesenchymal progenitor cells through Wnt signaling. J Biol Chem 2008, 283:1936-1945.
24. Macsai C.E., Foster B.K., Xian C.J. Roles of Wnt signalling in bone growth, remodelling, skeletal disorders and fracture repair. J Cell Physiol 2008, 215:578-587.
25. Liu F., Kohlmeier S., Wang C.Y. Wnt signaling and skeletal development. Cell Signal 2008, 20:999-1009.
26. Kirstetter P., Anderson K., Porse B.T., Jacobsen S.E., Nerlov C. Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multilineage differentiation block. Nat Immunol 2006, 7:1048-1056.
27. Scheller M., Huelsken J., Rosenbauer F., Taketo M.M., Birchmeier W., Tenen D.G., et al. Hematopoietic stem cell and multilineage defects generated by constitutive beta-catenin activation. Nat Immunol 2006, 7:1037-1047.
28. Brandon C., Eisenberg L.M., Eisenberg C.A. WNT signaling modulates the diversification of hematopoietic cells. Blood 2000, 96:4132-4141.
29. Van Den Berg D.J., Sharma A.K., Bruno E., Hoffman R. Role of members of the Wnt gene family in human hematopoiesis. Blood 1998, 92:3189-3202.
30. Krause U., Harris S., Green A., Ylostalo J., Zeitouni S., Lee N., et al. Pharmaceutical modulation of canonical Wnt signaling in multipotent stromal cells for improved osteoinductive therapy. Proc Natl Acad Sci U S A 2010, 107:4147-4152.
31. Wang F.S., Ko J.Y., Weng L.H., Yeh D.W., Ke H.J., Wu S.L. Inhibition of glycogen synthase kinase-3beta attenuates glucocorticoid-induced bone loss. Life Sci 2009, 85:685-692.
32. Friedlaender G.E., Tross R.B., Doganis A.C., Kirkwood J.M., Baron R. Effects of chemotherapeutic agents on bone. I. Short-term methotrexate and doxorubicin (adriamycin) treatment in a rat model. J Bone Joint Surg Am 1984, 66:602-607.
33. Xian C., Cool J., Pyragius T., Foster B. Damage and recovery of the bone growth mechanism in young rats following 5-fluorouracil acute chemotherapy. J Cell Biochem 2006, 99:1688-1704.
34. Chung R., Foster B.K., Zannettino A.C., Xian C.J. Potential roles of growth factor PDGF-BB in the bony repair of injured growth plate. Bone 2009, 44:878-885.
35. May K.P., West S.G., McDermott M.T., Huffer W.E. The effect of low-dose methotrexate on bone metabolism and histomorphometry in rats. Arthritis Rheum 1994, 37:201-206.
36. Wheeler D., Vander Griend R., Wronski T., Miller G., Keith E., Graves J. The short- and long-term effects of methotrexate on the rat skeleton. Bone 1995, 16:215-221.
37. Nuttall M.E., Gimble J.M. Is there a therapeutic opportunity to either prevent or treat osteopenic disorders by inhibiting marrow adipogenesis?. Bone 2000, 27:177-184.
38. Nuttall M.E., Gimble J.M. Controlling the balance between osteoblastogenesis and adipogenesis and the consequent therapeutic implications. Curr Opin Pharmacol 2004, 4:290-294.
39. Ducy P., Amling M., Takeda S., Priemel M., Schilling A.F., Beil F.T., et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000, 100:197-207.
40. Kajkenova O., Lecka-Czernik B., Gubrij I., Hauser S.P., Takahashi K., Parfitt A.M., et al. Increased adipogenesis and myelopoiesis in the bone marrow of SAMP6, a murine model of defective osteoblastogenesis and low turnover osteopenia. J Bone Miner Res 1997, 12:1772-1779.
41. Ahdjoudj S., Kaabeche K., Holy X., Fromigue O., Modrowski D., Zerath E., et al. Transforming growth factor-beta inhibits CCAAT/enhancer-binding protein expression and PPARgamma activity in unloaded bone marrow stromal cells. Exp Cell Res 2005, 303:138-147.
42. Bennett C.N., Ross S.E., Longo K.A., Bajnok L., Hemati N., Johnson K.W., et al. Regulation of Wnt signaling during adipogenesis. J Biol Chem 2002, 277:30998-31004.
43. Bodine P.V., Zhao W., Kharode Y.P., Bex F.J., Lambert A.J., Goad M.B., et al. The Wnt antagonist secreted frizzled-related protein-1 is a negative regulator of trabecular bone formation in adult mice. Mol Endocrinol 2004, 18:1222-1237.
44. Tang Q.Q., Gronborg M., Huang H., Kim J.W., Otto T.C., Pandey A., et al. Sequential phosphorylation of CCAAT enhancer-binding protein beta by MAPK and glycogen synthase kinase 3beta is required for adipogenesis. Proc Natl Acad Sci U S A 2005, 102:9766-9771.
45. Backesjo C.M., Li Y., Lindgren U., Haldosen L.A. Activation of Sirt1 decreases adipocyte formation during osteoblast differentiation of mesenchymal stem cells. J Bone Miner Res 2006, 21:993-1002.
46. Backesjo C.M., Li Y., Lindgren U., Haldosen L.A. Activation of Sirt1 decreases adipocyte formation during osteoblast differentiation of mesenchymal stem cells. Cells Tissues Organs 2009, 189:93-97.
47. Picard F., Kurtev M., Chung N., Topark-Ngarm A., Senawong T., Machado De Oliveira R., Leid M., McBurney M.W., Guarente L. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 2004, 429:771-776.
48. Jin Q., Zhang F., Yan T., Liu Z., Wang C., Ge X., et al. C/EBPalpha regulates SIRT1 expression during adipogenesis. Cell Res 2010, 20:470-479.
49. Huang J., Zhang Y., Bersenev A., O'Brien W.T., Tong W., Emerson S.G., et al. Pivotal role for glycogen synthase kinase-3 in hematopoietic stem cell homeostasis in mice. J Clin Invest 2009, 119:3519-3529.
50. Congdon K.L., Voermans C., Ferguson E.C., Dimascio L.N., Uqoezwa M., Zhao C., et al. Activation of Wnt signaling in hematopoietic regeneration. Stem Cells 2008, 26:1202-1210.
51. Qiang Y.W., Chen Y., Brown N., Hu B., Epstein J., Barlogie B., et al. Characterization of Wnt/beta-catenin signalling in osteoclasts in multiple myeloma. Br J Haematol 2010, 148:726-738.
52. Holmen S.L., Zylstra C.R., Mukherjee A., Sigler R.E., Faugere M.C., Bouxsein M.L., et al. Essential role of beta-catenin in postnatal bone acquisition. J Biol Chem 2005, 280:21162-21168.
53. Kramer I., Halleux C., Keller H., Pegurri M., Gooi J.H., Weber P.B., et al. Osteocyte Wnt/beta-catenin signaling is required for normal bone homeostasis. Mol Cell Biol 2010, 30:3071-3085.
54. Glass D.A., Karsenty G. Canonical Wnt signaling in osteoblasts is required for osteoclast differentiation. Ann N Y Acad Sci 2006, 1068:117-130.
55. Spencer G.J., Utting J.C., Etheridge S.L., Arnett T.R., Genever P.G. Wnt signalling in osteoblasts regulates expression of the receptor activator of NFkappaB ligand and inhibits osteoclastogenesis in vitro. J Cell Sci 2006, 119:1283-1296.
56. King TJ, Georgiou KR, Cool JC, Scherer MA, Ang ESM, Foster BK, Xu J, Xian CJ. Methotrexate chemotherapy promotes osteoclast formation in the long bone of rats via increased pro-inflammatory cytokines and enhanced NF-κB activation. Am J Pathol in press.
57. He J., Sheng T., Stelter A.A., Li C., Zhang X., Sinha M., et al. Suppressing Wnt signaling by the hedgehog pathway through sFRP-1. J Biol Chem 2006, 281:35598-35602.
58. Kansara M., Tsang M., Kodjabachian L., Sims N.A., Trivett M.K., Ehrich M., et al. Wnt inhibitory factor 1 is epigenetically silenced in human osteosarcoma, and targeted disruption accelerates osteosarcomagenesis in mice. J Clin Invest 2009, 119:837-851.
59. Enders G.H. Wnt therapy for bone loss: golden goose or Trojan horse?. J Clin Invest 2009, 119:758-760.