Bone-derived IGF mediates crosstalk between bone and breast cancer cells in bony metastases

Cancer Research

Volumn 72, Issue 16, 2012, Pages 4238-4249

  Hiraga, Toru ^a,c   Myoui, Akira ^b   Hashimoto, Nobuyuki ^b   Sasaki, Akira ^d   Hata, Kenji ^a   Morita, Yoshihiro ^a   Yoshikawa, Hideki ^b   Rosen, Clifford J ^f   Mundy, Gregory R ^e,g   Yoneda, Toshiyuki ^a,e  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c MATSUMOTO DENTAL UNIVERSITY   (Japan)

^d OKAYAMA UNIVERSITY   (Japan)

^e UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^f MAINE MEDICAL CENTER   (United States)

^g VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BB; PROTEIN KINASE B; SOMATOMEDIN; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; ZOLEDRONIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHOSPHORYLATION; BONE CELL; BONE METASTASIS; BREAST CANCER; CALVARIA; CANCER CELL; CANCER GROWTH; CANCER PATIENT; CELL CULTURE; COLONY FORMATION; CONTROLLED STUDY; DOSE RESPONSE; ENZYME ACTIVATION; FEMALE; HISTOPATHOLOGY; METASTASIS POTENTIAL; MITOSIS; MOLECULAR INTERACTION; NONHUMAN; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SUPERNATANT;

ANIMALS; BONE NEOPLASMS; BONE RESORPTION; BREAST NEOPLASMS; CELL COMMUNICATION; CELL LINE, TUMOR; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, INBRED BALB C; NF-KAPPA B; ONCOGENE PROTEIN V-AKT; RECEPTOR, IGF TYPE 1; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SOMATOMEDINS; TRANSFECTION;

EID: 84865116604     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-3061     Document Type: Article

References (43)

1. Roodman G. Mechanisms of bone metastasis. N Engl J Med 2004;350:1655-64.
2. Yoneda T, Hiraga T. Crosstalk between cancer cells and bone microenvironment in bone metastasis. Biochem Biophys Res Commun 2005;328:679-87. (Pubitemid 40208305)
3. Weilbaecher KN, Guise TA, McCauley LK. Cancer to bone: a fatal attraction. Nat Rev Cancer 2011;11:411-25.
4. Hiraga T, Williams P, Mundy G, Yoneda T. The bisphosphonate ibandronate promotes apoptosis in MDA-MB-231 human breast cancer cells in bone metastases. Cancer Res 2001;61:4418-24. (Pubitemid 32685769)
5. Coleman R, Cook R, Hirsh V, Major P, Lipton A. Zoledronic acid use in cancer patients: more than just supportive care? Cancer 2011;117:11-23.
6. Hauschka P, Mavrakos A, Iafrati M, Doleman S, Klagsbrun M. Growth factors in bone matrix. Isolation of multiple types by affinity chromatography on heparin-Sepharose. J Biol Chem 1986;261:12665-74. (Pubitemid 17204223)
7. Yoneda T, Sasaki A, Mundy G. Osteolytic bone metastasis in breast cancer. Breast Cancer Res Treat 1994;32:73-84. (Pubitemid 24322250)
8. Pfeilschifter J, Mundy G. Modulation of type beta transforming growth factor activity in bone cultures by osteotropic hormones. Proc Natl Acad Sci U S A 1987;84:2024-8. (Pubitemid 17054142)
9. Yin J, Selander K, Chirgwin J, Dallas M, Grubbs B, Wieser R, et al. TGF-beta signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development. J Clin Invest 1999;103:197-206. (Pubitemid 29053137)
10. Korpal M, Yan J, Lu X, Xu S, Lerit DA, Kang Y. Imaging transforming growth factor-beta signaling dynamics and therapeutic response in breast cancer bone metastasis. Nat Med 2009;15:960-6.
11. Thomas RJ, Guise TA, Yin JJ, Elliott J, Horwood NJ, Martin TJ, et al. Breast cancer cells interact with osteoblasts to support osteoclast formation. Endocrinology 1999;140:4451-8. (Pubitemid 30666108)
12. Samani A, Yakar S, LeRoith D, Brodt P. The role of the IGF system in cancer growth and metastasis: overview and recent insights. Endocr Rev 2007;28:20-47. (Pubitemid 46220849)
13. Maki RG. Small is beautiful: insulin-like growth factors and their role in growth, development, and cancer. J Clin Oncol 2010;28:4985-95.
14. Peyrat J, Bonneterre J, Beuscart R, Djiane J, Demaille A. Insulin-like growth factor 1 receptors in human breast cancer and their relation to estradiol and progesterone receptors. Cancer Res 1988;48:6429-33.
15. Resnik J, Reichart D, Huey K, Webster N, Seely B. Elevated insulin-like growth factor I receptor autophosphorylation and kinase activity in human breast cancer. Cancer Res 1998;58:1159-64. (Pubitemid 28183203)
16. van Golen C, Schwab T, Kim B, Soules M, Su Oh S, Fung K, et al. Insulin-like growth factor-I receptor expression regulates neuroblastoma metastasis to bone. Cancer Res 2006;66:6570-8. (Pubitemid 44085612)
17. Reiss K, D'Ambrosio C, Tu X, Tu C, Baserga R. Inhibition of tumor growth by a dominant negative mutant of the insulin-like growth factor I receptor with a bystander effect. Clin Cancer Res 1998;4:2647-55. (Pubitemid 28523490)
18. Bertrand F, Philippe C, Antoine P, Baud L, Groyer A, Capeau J, et al. Insulin activates nuclear factor kappa B in mammalian cells through a Raf-1-mediated pathway. J Biol Chem 1995;270:24435-41.
19. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006;441:431-6. (Pubitemid 44050137)
20. Mitsiades C, Mitsiades N, Poulaki V, Schlossman R, Akiyama M, Chauhan D, et al. Activation of NF-kappaB and upregulation of intracellular anti-apoptotic proteins via the IGF-1/Akt signaling in human multiple myeloma cells: therapeutic implications. Oncogene 2002;21:5673-83. (Pubitemid 35333000)
21. Manning BD, Cantley LC. AKT/PKB signaling: navigating downstream. Cell 2007;129:1261-74. (Pubitemid 46962095)
22. Nishimura R, Moriyama K, Yasukawa K, Mundy G, Yoneda T. Combination of interleukin-6 and soluble interleukin-6 receptors induces differentiation and activation of JAK-STAT and MAP kinase pathways in MG-63 human osteoblastic cells. J Bone Miner Res 1998;13:777-85. (Pubitemid 28224193)
23. Michigami T, Hiraga T, Williams PJ, Niewolna M, Nishimura R, Mundy GR, et al. The effect of the bisphosphonate ibandronate on breast cancer metastasis to visceral organs. Breast Cancer Res Treat 2002;75:249-58. (Pubitemid 35026118)
24. Garrett I, Mundy G. Relationship between interleukin-1 and prostaglandins in resorbing neonatal calvaria. J Bone Miner Res 1989;4:789-94. (Pubitemid 19265657)
25. Mbalaviele G, Dunstan C, Sasaki A, Williams P, Mundy G, Yoneda T. E-cadherin expression in human breast cancer cells suppresses the development of osteolytic bone metastases in an experimental metastasis model. Cancer Res 1996;56:4063-70. (Pubitemid 26284761)
26. Hiraga T, Nakamura H. Imatinib mesylate suppresses bone metastases of breast cancer by inhibiting osteoclasts through the blockade of c-Fms signals. Int J Cancer 2009;124:215-22.
27. Boyce BF, Aufdemorte TB, Garrett IR, Yates AJ, Mundy GR. Effects of interleukin-1 on bone turnover in normal mice. Endocrinology 1989;125:1142-50. (Pubitemid 19223955)
28. Freedman VH, Shin SI. Cellular tumorigenicity in nude mice: correlation with cell growth in semi-solid medium. Cell 1974;3:355-9.
29. Jackson JG, Zhang X, Yoneda T, Yee D. Regulation of breast cancer cell motility by insulin receptor substrate-2 (IRS-2) in metastatic variants of human breast cancer cell lines. Oncogene 2001;20: 7318-25. (Pubitemid 33078202)
30. Sangai T, Fujimoto H, Miyamoto S, Maeda H, Nakamura M, Ishii G, et al. Roles of osteoclasts and bone-derived IGFs in the survival and growth of human breast cancer cells in human adult bone implanted into nonobese diabetic/severe combined immunodeficient mice. Clin Exp Metastasis 2008;25:401-10.
31. Yoneda T, Williams P, Hiraga T, Niewolna M, Nishimura R. A bone-seeking clone exhibits different biological properties from the MDA-MB-231 parental human breast cancer cells and a brain-seeking clone in vivo and in vitro. J Bone Miner Res 2001;16:1486-95. (Pubitemid 32675200)
32. Lu X, Kang Y. Efficient acquisition of dual metastasis organotropism to bone and lung through stable spontaneous fusion between MDA-MB-231 variants. Proc Natl Acad Sci U S A 2009;106:9385-90.
33. Jennings JC, Mohan S. Heterogeneity of latent transforming growth factor-beta isolated from bone matrix proteins. Endocrinology 1990;126:1014-21. (Pubitemid 20079516)
34. Guise T, Yin J, Taylor S, Kumagai Y, Dallas M, Boyce B, et al. Evidence for a causal role of parathyroid hormone-related protein in the pathogenesis of human breast cancer-mediated osteolysis. J Clin Invest 1996;98:1544-9. (Pubitemid 26327863)
35. Hiraga T, Myoui A, Choi M, Yoshikawa H, Yoneda T. Stimulation of cyclooxygenase-2 expression by bone-derived transforming growth factor-beta enhances bone metastases in breast cancer. Cancer Res 2006;66:2067-73.
36. Sethi N, Dai X, Winter CG, Kang Y. Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells. Cancer Cell 2011;19:192-205.
37. Hiraga T, Kizaka-Kondoh S, Hirota K, Hiraoka M, Yoneda T. Hypoxia and hypoxia-inducible factor-1 expression enhance osteolytic bone metastases of breast cancer. Cancer Res 2007;67:4157-63. (Pubitemid 46815061)
38. Majmundar AJ, Wong WJ, Simon MC. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 2010;40:294-309.
39. Bendinelli P, Matteucci E, Maroni P, Desiderio MA. NF-kappaB activation, dependent on acetylation/deacetylation, contributes to HIF-1 activity and migration of bone metastatic breast carcinoma cells. Mol Cancer Res 2009;7:1328-41.
40. Asagiri M, Takayanagi H. The molecular understanding of osteoclast differentiation. Bone 2007;40:251-64. (Pubitemid 46054562)
41. Park BK, Zhang H, Zeng Q, Dai J, Keller ET, Giordano T, et al. NF-kappaB in breast cancer cells promotes osteolytic bone metastasis by inducing osteoclastogenesis via GM-CSF. Nat Med 2007;13:62-9. (Pubitemid 46067387)
42. Murphy L, Bell G, Friesen H. Tissue distribution of insulin-like growth factor I and II messenger ribonucleic acid in the adult rat. Endocrinology 1987;120:1279-82. (Pubitemid 17053979)
43. WuY, Yakar S, Zhao L, Hennighausen L, LeRoith D. Circulating insulin-like growth factor-I levels regulate colon cancer growth and metastasis. Cancer Res 2002;62:1030-5.