Metastatic breast cancer induces an osteoblast inflammatory response

Experimental Cell Research

Volumn 314, Issue 1, 2008, Pages 173-183

  Kinder, Michelle ^a   Chislock, Elizabeth ^a   Bussard, Karen M ^a   Shuman, Laurie ^a   Mastro, Andrea M ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Breast cancer; IL 6; IL 8; Inflammation; MCP 1; Metastasis; Osteoblasts

Indexed keywords

CYTOKINE; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 2; MATRIX PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL CELL; ARTICLE; BONE MINERALIZATION; BREAST CANCER; CANCER CELL; CELL ACTIVATION; CELL DIFFERENTIATION; CONTROLLED STUDY; FETUS; HUMAN; HUMAN CELL; INFLAMMATION; METASTASIS; MICROENVIRONMENT; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

MURINAE;

EID: 36549049974     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.09.021     Document Type: Article

References (77)

1. Solomayer E.F., Diel I.J., Meyberg G.C., Gollan C., and Bastert G. Metastatic breast cancer: clinical course, prognosis and therapy related to the first site of metastasis. Breast Cancer Res. Treat. 59 (2000) 271-278
2. Rubens R.D., and Mundy G.R. Cancer and the skeleton (2000), Martin Dunitz, London
3. Rubens R.D. Bone metastases-the clinical problem. Eur. J. Cancer 34 (1998) 210-213
4. Mundy G.R., Chen D., and Oyajobi B.O. Bone Remodeling. In: Favus M.J. (Ed). Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism (2003), American Society for Bone and Mineral Research, Washington D.C. Number of 567 pp.
5. Kozlow W., and Guise T. Breast cancer metastasis to bone: mechanisms of osteolysis and implications for therapy. J. Mammary Gland Biol. Neoplasia 10 (2005) 169-180
6. Guise T.A., and Chirgwin J.M. Transforming growth factor-beta in osteolytic breast cancer bone metastases. Clin. Orthop. Relat. Res. 4155 (2003) 532-538
7. Roodman G.D. Biology of osteoclast activation in cancer. J. Clin. Oncol. 19 (2001) 3562-3571
8. Bendre M., Gaddy-Kurten D., Foote-Mon T., Akel N.S., Skinner R.A., Nicholas R.W., and Suva L.J. Expression of interleukin 8 and not parathyroid hormone-related protein by human breast cancer cells correlates with bone metastasis in vivo. Cancer Res. 62 (2002) 5571-5579
9. de Visser K., and Coussens L. The inflammatory tumor microenvironment and its impact on cancer development. Contrib. Microbiol. 13 (2006) 118-137
10. Marriott I. Osteoblast responses to bacterial pathogens: a previously unappreciated role for bone-forming cells in host defense and disease progression. Immunol. Res. 30 (2004) 291-308
11. Wright K.M., and Friedland J.S. Regulation of chemokine gene expression and secretion in Staphylococcus aureus-infected osteoblasts. Microbes Infect. 6 (2004) 844-852
12. Fritz E., Glant T., Vermes C., Jacobs J., and Roebuck K. Titanium particles induce the immediate early stress responsive chemokines IL-8 and MCP-1 in osteoblasts. J. Orthop. Res. 20 (2002) 490-498
13. Fitzgerald K.A., O'Neill L.A.J., Gearing A.J.H., and Callard R.E. The Cytokine Facts Book (2001), Academic Press, New York
14. Clemons M., Dranitsaris G., Cole D., and Gainford M.C. Too much, too little, too late to start again? Assessing the efficacy of bisphosphonates in patients with bone metastases from breast cancer. Oncologist 11 (2006) 227-233
15. Lipton A. Bisphosphonates and breast carcinoma: present and future. Cancer 88 (2000) 3033-3037
16. Mastro A.M., Gay C.V., Welch D.R., Donahue H.J., Jewell J., Mercer R., DiGirolamo D., Chislock E.M., and Guttridge K. Breast cancer cells induce osteoblast apoptosis: a possible contributor to bone degradation. J. Cell. Biochem. 91 (2004) 265-276
17. Mercer R., Miyasaka C., and Mastro A.M. Metastatic breast cancer cells suppress osteoblast adhesion and differentiation. Clin. Exp. Metastasis 21 (2004) 427-435
18. Mercer R.M., and Mastro A.M. Cytokines secreted by bone-metastatic breast cancer cells alter the expression pattern of f-actin and reduce focal adhesion plaques in osteoblasts through PI 3K. Exp. Cell Res. 310 (2005) 270-281
19. Harris S.A., Enger R.J., Riggs B.L., and Spelsberg T.C. Development and characterization of a conditionally immortalized human fetal osteoblastic cell line. J. Bone Miner. Res. 10 (1995) 178-186
20. Sudo H., Kodama H.A., Amagai Y., Yamamoto S., and Kasai S. In vitro differentiation and calcification in a new clonal osteogenic cell line derived from newborn mouse calvaria. J. Cell Biol. 96 (1983) 191-198
21. Cailleau R., Olive M., and Cruciger Q.V. Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization. In Vitro 14 (1978) 911-915
22. A. Bakker, J. Klein-Nulend, in: M.P. Helfrich, S.H. Ralston (Ed.), Bone Research Protocols, Humana Press, Totowa, New Jersey, 2003, pp. 19-28.
23. Pederson L., Winding B., Foged N.T., Spelsberg T.C., and Oursler M.J. Identification of breast cancer cell line-derived paracrine factors that stimulate osteoclast activity. Cancer Res. 59 (1999) 5849-5855
24. Guise T.A., Yin J.J., Taylor S.D., Kumagai Y., Dallas M., Boyce B.F., Y.T., and M.G.R. Evidence for a causal role of parathyroid hormone-related protein in the pathogenesis of human breast-cancer-mediated osteolysis. J. Clin. Invest. 98 (1996) 1544-1549
25. Phadke P.A., Mercer R.R., Harms J.F., Jia Y., Frost A.R., Jewell J.L., Bussard K.M., Nelson S., Moore C., Kappes J.C., Gay C.V., Mastro A.M., and Welch D.R. Kinetics of metastatic breast cancer cell trafficking in bone. Clin. Cancer Res. 12 (2006) 1431-1440
26. Fritz E., Jacobs J., Glant T., and Roebuck K. Chemokine IL-8 induction by particulate wear debris in osteoblasts is mediated by NF-kappaB. J. Orthop. Res. 23 (2005) 1249-1257
27. Wright K., and Friedland J. Complex patterns of regulation of chemokine secretion by Th2-cytokines, dexamethasone, PGE2 in tuberculous osteomyelitis. J. Clin. Immunol. 23 (2003) 184-193
28. Bost K.L., Bento J.L., Petty C.C., Schrum L.W., Hudson M.C., and Marriott I. Monocyte chemoattractant protein-1 expression by osteoblasts following infection with Staphylococcus aureus or Salmonella. J. Interferon Cytokine Res. 21 (2001) 297-304
29. Kurihara N., Bertolini D., Suda T., Akiyama Y., and Roodman G.D. IL-6 stimulates osteoclast-like multinucleated cell formation in long term human marrow cultures by inducing IL-1 release. J. Immunol. 144 (1990) 4226-4230
30. Black K., Garrett I.R., and Mundy G.R. Chinese hamster ovarian cells transfected with the murine interleukin-6 gene cause hypercalcemia as well as cachexia, leukocytosis and thrombocytosis in tumor-bearing nude mice. Endocrinology 128 (1991) 2657-2659
31. Roodman G.D., Kurihara N., Ohsaki Y., Kukita A., Hosking D., Demulder A., Smith J.F., and Singer F.R. Interleukin 6. A potential autocrine/paracrine factor in Paget's disease of bone. J. Clin. Invest. 89 (1992) 46-52
32. Devlin R.D., Bone III H.G., and Roodman G.D. Stimulation of osteoclast-like multinucleated cell (MNC) formation in long-term human bone marrow culture by the serum of patients with Gorham-Stout or disappearing bone disease. J. Bone Miner. Res. 9 (1994) S140
33. Klein B., Wijdenes J., Zhang X.-G., Jourdan M., Boiron J.-M., Brochier J., Liautard J., Merlin M., Clement C., Morel-Fournier B., Lu Z.-Y., Mannoni P., Sany J., and Bataille R. Murine anti-interleukin-6 monoclonal antibody therapy for a patient with plasma cell leukemia. Blood 78 (1991) 1198-1204
34. Guillen C., de Gortazar A.R., and Esbrit P. The interleukin-6/soluble interleukin-6 receptor system induces parathyroid hormone-related protein in human osteoblastic cells. Calcif. Tissue Int. 75 (2004) 153-159
35. Mundy G. Metastasis to bone: causes, consequences and therapeutic opportunities. Nat. Rev., Cancer 2 (2002) 584-593
36. Nishimoto N., and Kishimoto T. Interleukin 6: from bench to bedside. Nat. Clin. Pract. Rheumatol. 2 (2006) 691
37. Leu C.M., Wong F.H., Chang C., Huang S.F., and Hu C.P. Interleukin-6 acts as an antiapoptotic factor in human esophageal carcinoma cells through the activation of both STAT3 and mitogen-activated protein kinase pathways. Oncogene 22 (2003) 7809-7818
38. Brocke-Heidrich K., Kretzschmar A.K., Pfeifer G., Henze C., Loffler D., Koczan D., Thiesen H.J., Burger R., Gramatzki M., and Horn F. Interleukin-6-dependent gene expression profiles in multiple myeloma INA-6 cells reveal a Bcl-2 family-independent survival pathway closely associated with Stat3 activation. Blood 103 (2004) 242-251
39. Goldberg-Bittman L., Neumark E., Sagi-Assif O., Azenshtein E., Meshel T., Witz I.P., and Ben-Baruch A. The expression of the chemokine receptor CXCR3 and its ligand, CXCL10, in human breast adenocarcinoma cell lines. Immunol. Lett. 92 (2004) 171-178
40. Badache A., and Hynes N.E. Interleukin 6 inhibits proliferation and, in cooperation with an epidermal growth factor receptor autocrine loop, increases migration of T47D breast cancer cells. Cancer Res. 61 (2001) 383-391
41. Selander K.S., Li L., Watson L., Merrell M., Dahmen H., Heinrich P.C., Muller-Newen G., and Harris K.W. Inhibition of gp130 signaling in breast cancer blocks constitutive activation of Stat3 and inhibits in vivo malignancy. Cancer Res. 64 (2004) 6924-6933
42. Kozlowski L., Zakrzewska I., Tokajuk P., and Wojtukiewicz M.Z. Concentration of interleukin-6 (IL-6), interleukin-8 (IL-8), and interleukin-10 (IL-10) in blood serum of breast cancer patients. Rocz. Akad. Med. Bailymst. 48 (2003) 82-84
43. Benoy I., Salgado R., Colpaert C., Weytjens R., Vermeulen P.B., and Dirix L.Y. Serum interleukin 6, plasma VEGF, serum VEGF, and VEGF platelet load in breast cancer patients. Clin. Breast Cancer 2 (2002)
44. Mettler L., Salmassi A., Heyer M., Schmutzier A., Schollmeyer R., and Jonat W. Perioperative levels of interleukin-1beta and interleukin-6 in women with breast cancer. Clin. Exp. Obstet. Gynecol. 31 (2004) 20-22
45. Zhang G.J., and Adachi I. Serum interleukin-6 levels correlate to tumour progression and prognosis in metastatic breast carcinoma. Anticancer Res. 19 (1999) 1427-1432
46. Bozcuk H.U., Samur G.M., Yildiz M., Ozben T., Ozdogan M., Artac M., Altunbas H., Akan I., and Savas B. Tumour necrosis factor-alpha, interleukin-6, and fasting serum insulin correlate with clinical outcome in metastatic breast cancer patients treated with chemotherapy. Cytokine 27 (2004) 58-65
47. Salgado R., Junius S., Benoy I., Van Dam P., Vermeulen P.B., Van Marck E., Huget P., and Dirix L.Y. Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int. J. Cancer 103 (2003) 642-646
48. Graves D.T., Jiang Y., and Valente A.J. The expression of monocyte chemoattractant protein-1 and other chemokines by osteoblasts. Front. Biosci. 4 (1999) D571-D580
49. Goede V., Brogelli L., Ziche M., and Augustin H.G. Induction of inflammatory angiogenesis by monocyte chemoattractant protein-1. Int. J. Cancer 82 (1999) 765-770
50. Horowitz M.C., and Lorenzo J.A. Principles of Bone Biology (2002), Academic Press, San Diego
51. Neumark E., Cohn M.A., Lukanidin E., Witz I.P., and Ben-Baruch A. Possible co-regulation of genes associated with enhanced progression of mammary adenocarcinomas. Immunol. Lett. 82 (2002) 111-121
52. Lu Y., Cai Z., Galson D., Xiao G., Liu Y., George D., Melhem M., Yao Z., and Zhang J. Monocyte chemotactic protein-1 (MCP-1) acts as a paracrine and autocrine factor for prostate cancer growth and invasion. Prostate 66 (2006) 1311-1318
53. Lu Y., Cai Z., Xiao G., Keller E.T., Mizokami A., Yao Z., Roodman G.D., and Zhang J. Monocyte chemotactic protein-1 mediates prostate cancer-induced bone resorption. Cancer Res. 67 (2007) 3646-3653
54. Lebrecht A., Hefler L., Tempfer C., and Koelbl H. Interleukin-4, interferon-gamma, and monocyte chemoattractant protein-1. Gynecol. Oncol. 83 (2001) 170-171
55. Hefler L., Tempfer C., Heinze G., Mayerhofer K., Breitenecker G., Leodolter S., Reinthaller A., and Kainz C. Monocyte chemoattractant protein-1 serum levels in ovarian cancer patients. Br. J. Cancer 81 (1999) 855-859
56. Koide N., Nishio A., Sato T., Sugiyama A., and Miyagawa S. Significance of macrophage chemoattractant protein-1 expression and macrophage infiltration in squamous cell carcinoma of the esophagus. Am. J. Gastroenterol. 99 (2004) 1667-1674
57. Johrer K., Janke K., Krugmann J., Fiegl M., and Greil R. Transendothelial migration of myeloma cells is increased by tumor necrosis factor (TNF)-alpha via TNF receptor 2 and autocrine upregulation of MCP-1. Clin. Cancer Res. 10 (2004) 1901-1910
58. Bendre M., Gaddy D., Nicholas R.W., and Suva L.J. Breast cancer metastasis to bone: it is not all about PTHrP. Clin. Orthop. Relat. Res. 415S (2003) S39-S45
59. Mukaida N., Ketlunsky S.A., and Matsushima K. The Cytokine Handbook (2003), Academic Press, Amsterdam
60. Chaudhary L.R., and Avioli L.V. Dexamethasone regulates IL-1 beta and TNF-alpha-induced interleukin-8 production in human bone marrow stromal and osteoblast-like cells. Calcif. Tissue Int. 55 (1994) 16-20
61. Fuller K., Owens J.M., and Chambers T.J. Macrophage inflammatory protein-1 alpha and IL-8 stimulate the motility but suppress the resorption of isolated rat osteoclasts. J. Immunol. 154 (1995) 6065-6072
62. Rothe L., Collin-Osdoby P., Chen Y., Sunyer T., Chaudhary L., Tsay A., Goldring S., Avioli L., and Osdoby P. Human osteoclasts and osteoclast-like cells synthesize and release high basal and inflammatory stimulated levels of the potent chemokine interleukin-8. Endocrinology 139 (1998) 4353-4363
63. Bendre M.S., Margulies A.G., Walser B., Akel N.S., Bhattacharrya S., Skinner R.A., Swain F., Ramani V., Mohammad K.S., Wessner L.L., Martinez A., Guise T.A., Chirgwin J.M., Gaddy D., and Suva L.J. Tumor-derived interleukin-8 stimulates osteolysis independent of the receptor activator of nuclear factor-kappaB ligand pathway. Cancer Res. 65 (2005) 11001-11009
64. Arenberg D., Kunkel S., Polverini P., Glass M., Burdick M.D., and Strieter R.M. Inhibition of interleukin-8 reduces tumorigenesis of human non-small cell lung cancer in SCID mice. J. Clin. Invest. 97 (1996) 2792-2802
65. Kim S., Uehara H., Karashima T., Mccarty M., Shih N., and Fidler I.J. Expression of interleukin 8 correlates with angiogenesis, tumorigenicity, and metastasis of human prostate cancer cells implanted orthotopically in nude mice. Neoplasia 3 (2001) 33-42
66. Singh R., and Varney M. IL-8 expression in malignant melanoma: implications in growth and metastases. Histol. Histopathol. 15 (2000) 843-849
67. Bendre M., Montague D.C., Peery T., Akel N.S., Gaddy D., and Suva L.J. Interleukin-8 stimulation of osteoclastogenesis and bone resorption is a mechanism for the increased osteolysis of metastatic bone disease. Bone 33 (2003) 28-37
68. Benoy I., Salgado R., Van Dam P., Geboers K., Van Marck E., Scharpe S., Vermeulen P.B., and Dirix L.Y. Increased serum interleukin-8 in patients with early and metastatic breast cancer correlates with early dissemination and survival. Clin. Cancer Res. 10 (2004) 7157-7162
69. Muller A., Homey B., Soto H., Ge N., Catron D., Buchanan M., McClanahan T., Murphy E., Yuan W., Wagner S., Barrera J., Mohar A., Verastegui E., and Zlotnik A. Involvement of chemokine receptors in breast cancer metastasis. Nature 410 (2001) 50-56
70. Bendre M.S., Margulies A.G., Walser B., Akel N.S., Bhattacharrya S., Skinner R.A., Swain F., Ramani V., Mohammad K.S., Wessner L.L., Martinez A., Guise T.A., Chirgwin J.M., Gaddy D., and Suva L.J. Tumor-derived interleukin-8 stimulates osteolysis independent of the receptor activator of nuclear factor-kB ligand pathway. Cancer Res. 65 (2005) 11001-11009
71. Douglas A.M., Goss G.A., Sutherland R.L., Hilton D.J., Berndt M.C., Nicola N.A., and Begley C.G. Expression and function of members of the cytokine receptor superfamily on breast cancer cells. Oncogene 14 (1997) 661-669
72. Chiu J.J., Sgagias M.K., and Cowan K.H. Interleukin 6 acts as a paracrine growth factor in human mammary carcinoma cell lines. Clin. Cancer Res. 2 (1996) 215-221
73. Danforth Jr. D.N., and Sgagias M.K. Interleukin-1 alpha and interleukin-6 act additively to inhibit growth of MCF-7 breast cancer cells in vitro. Cancer Res. 53 (1993) 1538-1545
74. Nam J.S., Kang M.J., Suchar A.M., Shimamura T., Kohn E.A., Michalowska A.M., Jordan V.C., Hirohashi S., and Wakefield L.M. Chemokine (C-C motif) ligand 2 mediates the prometastatic effect of dysadherin in human breast cancer cells. Cancer Res. 66 (2006) 7176-7184
75. Singh B., Berry J.A., Vincent L.E., and Lucci A. Involvement of IL-8 in COX-2-mediated bone metastases from breast cancer. J. Surg. Res. 134 (2006) 44-51
76. Roodman G., and Choi S. MIP-1 alpha and myeloma bone disease. Cancer Treat. Res. 118 (2004) 83-100
77. Kwan Tat S., Padrines M., Theoleyre S., Heymann D., and Fortun Y. IL-6, RANKL, TNF-alpha/IL-1: interrelations in bone resorption pathophysiology. Cytokine Growth Factor Rev. 15 (2004) 49-60