Three-dimensional (3D) culture of bone-derived human 786-O renal cell carcinoma retains relevant clinical characteristics of bone metastases

Cancer Letters

Volumn 365, Issue 1, 2015, Pages 89-95

  Pan, Tianhong ^a   Fong, Eliza L S ^b   Martinez, Mariane ^c   Harrington, Daniel A ^c   Lin, Sue Hwa ^a   Farach Carson, Mary C ^b,c   Satcher, Robert L ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b Rice University   (United States)

^c RICE UNIVERSITY   (United States)

Author keywords

Bone metastasis; Hyaluronic acid; Hydrogel; Renal cell carcinoma; Three dimensional culture

Indexed keywords

ANGIOPOIETIN 1; CADHERIN 11; CELL ADHESION MOLECULE; CHEMOKINE RECEPTOR CXCR4; HYALURONIC ACID; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 6; MESSENGER RNA; OSTEOCLAST DIFFERENTIATION FACTOR; PARATHYROID HORMONE RELATED PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; ANGIOGENIC PROTEIN; HYDROGEL; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE METASTASIS; CANCER CELL CULTURE; CELL AGGREGATION; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HYDROGEL; IN VIVO STUDY; KIDNEY CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR SPHEROID; ANIMAL; BONE TUMOR; CELL SEPARATION; CELL SHAPE; COMPARATIVE STUDY; CULTURE TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; KIDNEY TUMOR; METABOLISM; MULTICELLULAR SPHEROID; OSTEOLYSIS; PATHOLOGY; PHENOTYPE; SCID MOUSE; SECONDARY; TIME; TUMOR CELL CULTURE;

ANGIOGENIC PROTEINS; ANIMALS; BIOMARKERS, TUMOR; BONE NEOPLASMS; CARCINOMA, RENAL CELL; CELL ADHESION MOLECULES; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CELL SEPARATION; CELL SHAPE; CELL SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYALURONIC ACID; HYDROGELS; KIDNEY NEOPLASMS; MICE, SCID; OSTEOLYSIS; PHENOTYPE; RNA, MESSENGER; SPHEROIDS, CELLULAR; TIME FACTORS; TUMOR CELLS, CULTURED;

EID: 84930819565     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.05.019     Document Type: Article

References (49)

1. Amato R.J. Renal cell carcinoma: review of novel single-agent therapeutics and combination regimens. Ann. Oncol 2005, 16:7-15.
2. Sourbier C., Massfelder T. Parathyroid hormone-related protein in human renal cell carcinoma. Cancer Lett 2006, 240:170-182.
3. Gupta K., Miller J.D., Li J.Z., Russell M.W., Charbonneau C. Epidemiologic and socioeconomic burden of metastatic renal cell carcinoma (mRCC): a literature review. Cancer Treat. Rev 2008, 34:193-205.
4. Wood S.L., Brown J.E. Skeletal metastasis in renal cell carcinoma: current and future management options. Cancer Treat. Rev 2012, 38:284-291.
5. Woodward E., Jagdev S., McParland L., Clark K., Gregory W., Newsham A., et al. Skeletal complications and survival in renal cancer patients with bone metastases. Bone 2011, 48:160-166.
6. Lee J., Cuddihy M.J., Kotov N.A. Three-dimensional cell culture matrices: state of the art. Tissue Eng. Part B Rev 2008, 14:61-86.
7. Sasser A.K., Mundy B.L., Smith K.M., Studebaker A.W., Axel A.E., Haidet A.M., et al. Human bone marrow stromal cells enhance breast cancer cell growth rates in a cell line-dependent manner when evaluated in 3D tumor environments. Cancer Lett 2007, 254:255-264.
8. Yamada K.M., Cukierman E. Modeling tissue morphogenesis and cancer in 3D. Cell 2007, 130:601-610.
9. DeVolder R., Kong H.J. Hydrogels for in vivo-like three-dimensional cellular studies. WIREs Syst. Biol. Med 2012, 4:351-365.
10. Alemany-Ribes M., Semino C.E. Bioengineering 3D environments for cancer models. Adv. Drug Deliv. Rev 2014, 79-80:40-49.
11. Wang R., Xu J., Juliette L., Castilleja A., Love J., Sung S.Y., et al. Three-dimensional co-culture models to study prostate cancer growth, progression, and metastasis to bone. Semin. Cancer Biol 2005, 15:353-364.
12. Windus L.C., Glover T.T., Avery V.M. Bone-stromal cells up-regulate tumourigenic markers in a tumour-stromal 3D model of prostate cancer. Mol. Cancer 2013, 12:112.
13. Fong E.L., Martinez M., Yang J., Mikos A.G., Navone N.M., Harrington D.A., et al. Hydrogel-based 3D model of patient-derived prostate xenograft tumors suitable for drug screening. Mol. Pharm 2014, 11:2040-2050.
14. Gurski L.A., Jha A.K., Zhang C., Jia X., Farach-Carson M.C. Hyaluronic acid-based hydrogels as 3D matrices for in vitro evaluation of chemotherapeutic drugs using poorly adherent prostate cancer cells. Biomaterials 2009, 30:6076-6085.
15. Xu X., Gurski L.A., Zhang C., Harrington D.A., Farach-Carson M.C., Jia X. Recreating the tumor microenvironment in a bilayer, hyaluronic acid hydrogel construct for the growth of prostate cancer spheroids. Biomaterials 2012, 33:9049-9060.
16. Gurski L.A., Xu X., Labrada L.N., Nguyen N.T., Xiao L., van Golen K.L., et al. Hyaluronan (HA) interacting proteins RHAMM and hyaluronidase impact prostate cancer cell behavior and invadopodia formation in 3D HA-based hydrogels. PLoS ONE 2012, 7:e50075.
17. Satcher R.L., Pan T., Cheng C.J., Lee Y.C., Lin S.C., Yu G., et al. Cadherin-11 in renal cell carcinoma bone metastasis. PLoS ONE 2014, 9:e89880.
18. Pan T., Rawal P., Wu Y., Xie W., Jankovic J., Le W. Rapamycin protects against rotenone-induced apoptosis through autophagy induction. Neuroscience 2009, 164:541-551.
19. Le W., Pan T., Huang M., Xu P., Xie W., Zhu W., et al. Decreased NURR1 gene expression in patients with Parkinson's disease. J. Neurol. Sci 2008, 273:29-33.
20. D'Alterio C., Consales C., Polimeno M., Franco R., Cindolo L., Portella L., et al. Concomitant CXCR4 and CXCR7 expression predicts poor prognosis in renal cancer. Curr. Cancer Drug Targets 2010, 10:772-781.
21. Pan J., Mestas J., Burdick M.D., Phillips R.J., Thomas G.V., Reckamp K., et al. Stromal derived factor-1 (SDF-1/CXCL12) and CXCR4 in renal cell carcinoma metastasis. Mol. Cancer 2006, 5:56.
22. Wehler T.C., Graf C., Biesterfeld S., Brenner W., Schadt J., Gockel I., et al. Strong expression of chemokine receptor CXCR4 by renal cell carcinoma correlates with advanced disease. J. Oncol 2008, 2008:626340.
23. Xie C., Schwarz E.M., Sampson E.R., Dhillon R.S., Li D., O'Keefe R.J., et al. Unique angiogenic and vasculogenic properties of renal cell carcinoma in a xenograft model of bone metastasis are associated with high levels of vegf-a and decreased ang-1 expression. J. Orthop. Res 2012, 30:325-333.
24. Yamakawa M., Liu L.X., Belanger A.J., Date T., Kuriyama T., Goldberg M.A., et al. Expression of angiopoietins in renal epithelial and clear cell carcinoma cells: regulation by hypoxia and participation in angiogenesis. Am. J. Physiol. Renal Physiol 2004, 287:F649-F657.
25. Foster B.A., Gingrich J.R., Kwon E.D., Madias C., Greenberg N.M. Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res 1997, 57:3325-3330.
26. Xu X., Sabanayagam C.R., Harrington D.A., Farach-Carson M.C., Jia X. A hydrogel-based tumor model for the evaluation of nanoparticle-based cancer therapeutics. Biomaterials 2014, 35:3319-3330.
27. Lee Y.C., Cheng C.J., Huang M., Bilen M.A., Ye X., Navone N.M., et al. Androgen depletion up-regulates cadherin-11 expression in prostate cancer. J. Pathol 2010, 221:68-76.
28. Huang C.F., Lira C., Chu K., Bilen M.A., Lee Y.C., Ye X., et al. Cadherin-11 increases migration and invasion of prostate cancer cells and enhances their interaction with osteoblasts. Cancer Res 2010, 70:4580-4589.
29. Chu K., Cheng C.J., Ye X., Lee Y.C., Zurita A.J., Chen D.T., et al. Cadherin-11 promotes the metastasis of prostate cancer cells to bone. Mol. Cancer Res 2008, 6:1259-1267.
30. Tamura D., Hiraga T., Myoui A., Yoshikawa H., Yoneda T. Cadherin-11-mediated interactions with bone marrow stromal/osteoblastic cells support selective colonization of breast cancer cells in bone. Int. J. Oncol 2008, 33:17-24.
31. Taichman R.S., Cooper C., Keller E.T., Pienta K.J., Taichman N.S., McCauley L.K. Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res 2002, 62:1832-1837.
32. Chan D.A., Sutphin P.D., Yen S.E., Giaccia A.J. Coordinate regulation of the oxygen-dependent degradation domains of hypoxia-inducible factor 1 alpha. Mol. Cell. Biol 2005, 25:6415-6426.
33. Wiesener M.S., Munchenhagen P.M., Berger I., Morgan N.V., Roigas J., Schwiertz A., et al. Constitutive activation of hypoxia-inducible genes related to overexpression of hypoxia-inducible factor-1alpha in clear cell renal carcinomas. Cancer Res 2001, 61:5215-5222.
34. Blancher C., Moore J.W., Robertson N., Harris A.L. Effects of ras and von Hippel-Lindau (VHL) gene mutations on hypoxia-inducible factor (HIF)-1alpha, HIF-2alpha, and vascular endothelial growth factor expression and their regulation by the phosphatidylinositol 3'-kinase/Akt signaling pathway. Cancer Res 2001, 61:7349-7355.
35. Fukuhara S., Sako K., Noda K., Zhang J., Minami M., Mochizuki N. Angiopoietin-1/Tie2 receptor signaling in vascular quiescence and angiogenesis. Histol. Histopathol 2010, 25:387-396.
36. Guise T.A., Yin J.J., Thomas R.J., Dallas M., Cui Y., Gillespie M.T. Parathyroid hormone-related protein (PTHrP)-(1-139) isoform is efficiently secreted in vitro and enhances breast cancer metastasis to bone in vivo. Bone 2002, 30:670-676.
37. Kakonen S.M., Mundy G.R. Mechanisms of osteolytic bone metastases in breast carcinoma. Cancer 2003, 97:834-839.
38. Sottnik J.L., Keller E.T. Understanding and targeting osteoclastic activity in prostate cancer bone metastases. Curr. Mol. Med 2013, 13:626-639.
39. Martin T.J. Osteoblast-derived PTHrP is a physiological regulator of bone formation. J. Clin. Invest 2005, 115:2322-2324.
40. Negrier S., Perol D., Menetrier-Caux C., Escudier B., Pallardy M., Ravaud A., et al. Interleukin-6, interleukin-10, and vascular endothelial growth factor in metastatic renal cell carcinoma: prognostic value of interleukin-6 - from the Groupe Francais d'Immunotherapie. J. Clin. Oncol 2004, 22:2371-2378.
41. Paule B. [Interleukin-6 and bone metastasis of renal cancer: molecular bases and therapeutic implications]. Prog. Urol 2001, 11:368-375.
42. de la Mata J., Uy H.L., Guise T.A., Story B., Boyce B.F., Mundy G.R., et al. Interleukin-6 enhances hypercalcemia and bone resorption mediated by parathyroid hormone-related protein in vivo. J. Clin. Invest 1995, 95:2846-2852.
43. Grey A., Mitnick M.A., Masiukiewicz U., Sun B.H., Rudikoff S., Jilka R.L., et al. A role for interleukin-6 in parathyroid hormone-induced bone resorption in vivo. Endocrinology 1999, 140:4683-4690.
44. Delk N.A., Farach-Carson M.C. Interleukin-6: a bone marrow stromal cell paracrine signal that induces neuroendocrine differentiation and modulates autophagy in bone metastatic PCa cells. Autophagy 2012, 8:650-663.
45. Grimaud E., Soubigou L., Couillaud S., Coipeau P., Moreau A., Passuti N., et al. Receptor activator of nuclear factor kappaB ligand (RANKL)/osteoprotegerin (OPG) ratio is increased in severe osteolysis. Am. J. Pathol 2003, 163:2021-2031.
46. Wada T., Nakashima T., Hiroshi N., Penninger J.M. RANKL-RANK signaling in osteoclastogenesis and bone disease. Trends Mol. Med 2006, 12:17-25.
47. Coleman R.E. Metastatic bone disease: clinical features, pathophysiology and treatment strategies. Cancer Treat. Rev 2001, 27:165-176.
48. Castellano D., Sepulveda J.M., Garcia-Escobar I., Rodriguez-Antolin A., Sundlov A., Cortes-Funes H. The role of RANK-ligand inhibition in cancer: the story of denosumab. Oncologist 2011, 16:136-145.
49. Mikami S., Katsube K., Oya M., Ishida M., Kosaka T., Mizuno R., et al. Increased RANKL expression is related to tumour migration and metastasis of renal cell carcinomas. J. Pathol 2009, 218:530-539.