Anti-transforming growth factor ß antibody treatment rescues bone loss and prevents breast cancer metastasis to bone

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Biswas, Swati ^a   Nyman, Jeffry S ^a   Alvarez, JoAnn ^a   Chakrabarti, Anwesa ^a   Ayres, Austin ^a   Sterling, Julie ^a   Edwards, James ^a   Rana, Tapasi ^a   Johnson, Rachelle ^a   Perrien, Daniel S ^a,b   Lonning, Scott ^c   Shyr, Yu ^a   Matrisian, Lynn M ^a   Mundy, Gregory R ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c GENZYME CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; MINERAL; PARATHYROID HORMONE RELATED PROTEIN; TRANSCRIPTION FACTOR GLI2; TRANSFORMING GROWTH FACTOR BETA ANTIBODY; ANTIBODY; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE DENSITY; BONE METASTASIS; BREAST CANCER; CANCER PREVENTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG EFFECT; DRUG EFFICACY; EX VIVO STUDY; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; OSTEOCLASTOGENESIS; OSTEOLYSIS; PROTEIN EXPRESSION; TRABECULAR BONE; TREATMENT DURATION; TUMOR VOLUME; ANIMAL; BONE; BONE DEVELOPMENT; BONE TUMOR; BREAST TUMOR; CELL DIFFERENTIATION; CYTOLOGY; DRUG ANTAGONISM; METABOLISM; METASTASIS; NUDE MOUSE; OSTEOBLAST; OSTEOCLAST; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

MURINAE; MUS;

ANIMALS; ANTIBODIES; BONE AND BONES; BONE NEOPLASMS; BREAST NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; COLLAGEN; FEMALE; HUMANS; MICE; MICE, NUDE; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS; REAL-TIME POLYMERASE CHAIN REACTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 80855128847     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027090     Document Type: Article

References (52)

1. Hortobagyi GN, Piccart-Gebhart MJ, (1996) Current management of advanced breast cancer. Semin Oncol 23: 1-5.
2. Theriault RL, Lipton A, Hortobagyi GN, Leff R, Gluck S, et al. (1999) Pamidronate reduces skeletal morbidity in women with advanced breast cancer and lytic bone lesions: a randomized, placebo-controlled trial. Protocol 18 Aredia Breast Cancer Study Group. J Clin Oncol 17: 846-854.
3. Coleman RE, Lipton A, Roodman GD, Guise TA, Boyce BF, et al. Metastasis and bone loss: advancing treatment and prevention. Cancer Treat Rev 36: 615-620.
4. Mundy GR, (2002) Metastasis to bone: causes, consequences and therapeutic opportunities. Nat Rev Cancer 2: 584-593.
5. Hortobagyi GN, Theriault RL, Porter L, Blayney D, Lipton A, et al. (1996) Efficacy of pamidronate in reducing skeletal complications in patients with breast cancer and lytic bone metastases. Protocol 19 Aredia Breast Cancer Study Group. N Engl J Med 335: 1785-1791.
6. Kanis JA, McCloskey EV, (2000) Bisphosphonates in multiple myeloma. Cancer 88: 3022-3032.
7. Berenson JR, Lipton A, (1998) Use of bisphosphonates in patients with metastatic bone disease. Oncology (Williston Park) 12: 1573-1579; discussion 1579-1581.
8. Berenson JR, Rosen LS, Howell A, Porter L, Coleman RE, et al. (2001) Zoledronic acid reduces skeletal-related events in patients with osteolytic metastases. Cancer 91: 1191-1200.
9. Djulbegovic B, Wheatley K, Ross J, Clark O, Bos G, et al. (2002) Bisphosphonates in multiple myeloma. Cochrane Database Syst Rev: pp. CD003188.
10. Rosen LS, Gordon D, Kaminski M, Howell A, Belch A, et al. (2003) Long-term efficacy and safety of zoledronic acid compared with pamidronate disodium in the treatment of skeletal complications in patients with advanced multiple myeloma or breast carcinoma: a randomized, double-blind, multicenter, comparative trial. Cancer 98: 1735-1744.
11. Stopeck AT, Lipton A, Body JJ, Steger GG, Tonkin K, et al. Denosumab compared with zoledronic acid for the treatment of bone metastases in patients with advanced breast cancer: a randomized, double-blind study. J Clin Oncol 28: 5132-5139.
12. Mundy GR, Edwards JR, (2008) PTH-related peptide (PTHrP) in hypercalcemia. J Am Soc Nephrol 19: 672-675.
13. Mundy GR, Guise TA, (1997) Hypercalcemia of malignancy. Am J Med 103: 134-145.
14. Jemal A, Siegel R, Xu J, Ward E, (2010) Cancer statistics, 2010. CA Cancer J Clin 60: 277-300.
15. Jemal A, Center MM, DeSantis C, Ward EM,.
16. Balooch G, Balooch M, Nalla RK, Schilling S, Filvaroff EH, et al. (2005) TGF-beta regulates the mechanical properties and composition of bone matrix. Proc Natl Acad Sci U S A 102: 18813-18818.
17. Geiser AG, Zeng QQ, Sato M, Helvering LM, Hirano T, et al. (1998) Decreased bone mass and bone elasticity in mice lacking the transforming growth factor-beta1 gene. Bone 23: 87-93.
18. Erlebacher A, Derynck R, (1996) Increased expression of TGF-beta 2 in osteoblasts results in an osteoporosis-like phenotype. J Cell Biol 132: 195-210.
19. Borton AJ, Frederick JP, Datto MB, Wang XF, Weinstein RS, (2001) The loss of Smad3 results in a lower rate of bone formation and osteopenia through dysregulation of osteoblast differentiation and apoptosis. J Bone Miner Res 16: 1754-1764.
20. Yang X, Chen L, Xu X, Li C, Huang C, et al. (2001) TGF-beta/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. J Cell Biol 153: 35-46.
21. Mundy GR, (1997) Mechanisms of bone metastasis. Cancer 80: 1546-1556.
22. Bierie B, Moses HL, (2006) Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer 6: 506-520.
23. Yin JJ, Selander K, Chirgwin JM, Dallas M, Grubbs BG, et al. (1999) TGF-beta signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development. J Clin Invest 103: 197-206.
24. Baselga J, Rothenberg ML, Tabernero J, Seoane J, Daly T, et al. (2008) TGF-beta signalling-related markers in cancer patients with bone metastasis. Biomarkers 13: 217-236.
25. Sterling JA, Oyajobi BO, Grubbs B, Padalecki SS, Munoz SA, et al. (2006) The hedgehog signaling molecule Gli2 induces parathyroid hormone-related peptide expression and osteolysis in metastatic human breast cancer cells. Cancer Res 66: 7548-7553.
26. Pfeilschifter J, Oechsner M, Naumann A, Gronwald RG, Minne HW, et al. (1990) Stimulation of bone matrix apposition in vitro by local growth factors: a comparison between insulin-like growth factor I, platelet-derived growth factor, and transforming growth factor beta. Endocrinology 127: 69-75.
27. Mundy GR, Varani J, Orr W, Gondek MD, Ward PA, (1978) Resorbing bone is chemotactic for monocytes. Nature 275: 132-135.
28. Alliston T, Choy L, Ducy P, Karsenty G, Derynck R, (2001) TGF-beta-induced repression of CBFA1 by Smad3 decreases cbfa1 and osteocalcin expression and inhibits osteoblast differentiation. EMBO J 20: 2254-2272.
29. Yingling JM, Blanchard KL, Sawyer JS, (2004) Development of TGF-beta signalling inhibitors for cancer therapy. Nat Rev Drug Discov 3: 1011-1022.
30. Yang YA, Dukhanina O, Tang B, Mamura M, Letterio JJ, et al. (2002) Lifetime exposure to a soluble TGF-beta antagonist protects mice against metastasis without adverse side effects. J Clin Invest 109: 1607-1615.
31. Nam JS, Terabe M, Mamura M, Kang MJ, Chae H, et al. (2008) An anti-transforming growth factor beta antibody suppresses metastasis via cooperative effects on multiple cell compartments. Cancer Res 68: 3835-3843.
32. Bandyopadhyay A, Agyin JK, Wang L, Tang Y, Lei X, et al. (2006) Inhibition of pulmonary and skeletal metastasis by a transforming growth factor-beta type I receptor kinase inhibitor. Cancer Res 66: 6714-6721.
33. Mohammad KS, Javelaud D, Fournier PG, Niewolna M, McKenna CR, et al. (2011) TGF-beta-RI kinase inhibitor SD-208 reduces the development and progression of melanoma bone metastases. Cancer Res 71: 175-184.
34. Mohammad KS, Chen CG, Balooch G, Stebbins E, McKenna CR, et al. (2009) Pharmacologic inhibition of the TGF-beta type I receptor kinase has anabolic and anti-catabolic effects on bone. PLoS One 4: e5275.
35. Edwards JR, Nyman JS, Lwin ST, Moore MM, Esparza J, et al. (2010) Inhibition of TGF-beta signaling by 1D11 antibody treatment increases bone mass and quality in vivo. J Bone Miner Res 25: 2419-2426.
36. Dasch JR, Pace DR, Waegell W, Inenaga D, Ellingsworth L, (1989) Monoclonal antibodies recognizing transforming growth factor-beta. Bioactivity neutralization and transforming growth factor beta 2 affinity purification. J Immunol 142: 1536-1541.
37. Khanna AK, Plummer MS, Hilton G, Pieper GM, Ledbetter S, (2004) Anti-transforming growth factor antibody at low but not high doses limits cyclosporine-mediated nephrotoxicity without altering rat cardiac allograft survival: potential of therapeutic applications. Circulation 110: 3822-3829.
38. Ling H, Li X, Jha S, Wang W, Karetskaya L, et al. (2003) Therapeutic role of TGF-beta-neutralizing antibody in mouse cyclosporin A nephropathy: morphologic improvement associated with functional preservation. J Am Soc Nephrol 14: 377-388.
39. Guise TA, Yin JJ, Taylor SD, Kumagai Y, Dallas M, et al. (1996) Evidence for a causal role of parathyroid hormone-related protein in the pathogenesis of human breast cancer-mediated osteolysis. J Clin Invest 98: 1544-1549.
40. Aslakson CJ, Miller FR, (1992) Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res 52: 1399-1405.
41. Michigami T, Hiraga T, Williams PJ, Niewolna M, Nishimura R, et al. (2002) The effect of the bisphosphonate ibandronate on breast cancer metastasis to visceral organs. Breast Cancer Res Treat 75: 249-258.
42. Gallwitz WE, Guise TA, Mundy GR, (2002) Guanosine nucleotides inhibit different syndromes of PTHrP excess caused by human cancers in vivo. J Clin Invest 110: 1559-1572.
43. Robey PG, Termine JD, (1985) Human bone cells in vitro. Calcif Tissue Int 37: 453-460.
44. Karsenty G, Wagner EF, (2002) Reaching a genetic and molecular understanding of skeletal development. Dev Cell 2: 389-406.
45. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, et al. (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93: 165-176.
46. Bucay N, Sarosi I, Dunstan CR, Morony S, Tarpley J, et al. (1998) osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev 12: 1260-1268.
47. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, et al. (1998) Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci U S A 95: 3597-3602.
48. Wada T, Nakashima T, Hiroshi N, Penninger JM, (2006) RANKL-RANK signaling in osteoclastogenesis and bone disease. Trends Mol Med 12: 17-25.
49. Ganapathy V, Ge R, Grazioli A, Xie W, Banach-Petrosky W, et al. (2010) Targeting the Transforming Growth Factor-beta pathway inhibits human basal-like breast cancer metastasis. Mol Cancer 9: 122.
50. Dunn LK, Mohammad KS, Fournier PG, McKenna CR, Davis HW, et al. (2009) Hypoxia and TGF-beta drive breast cancer bone metastases through parallel signaling pathways in tumor cells and the bone microenvironment. PLoS One 4: e6896.
51. Stewart AF, Vignery A, Silverglate A, Ravin ND, LiVolsi V, et al. (1982) Quantitative bone histomorphometry in humoral hypercalcemia of malignancy: uncoupling of bone cell activity. J Clin Endocrinol Metab 55: 219-227.
52. Harris SE, Bonewald LF, Harris MA, Sabatini M, Dallas S, et al. (1994) Effects of transforming growth factor beta on bone nodule formation and expression of bone morphogenetic protein 2, osteocalcin, osteopontin, alkaline phosphatase, and type I collagen mRNA in long-term cultures of fetal rat calvarial osteoblasts. J Bone Miner Res 9: 855-863.