Silencing of skeletal metastasis-associated genes impairs migration of breast cancer cells and reduces osteolytic bone lesions

Clinical and Experimental Metastasis

Volumn 29, Issue 5, 2012, Pages 441-456

  Reufsteck, Christina ^a   Lifshitz Shovali, Rinat ^b   Zepp, Michael ^a   Bäuerle, Tobias ^a   Kübler, Dieter ^a   Golomb, Gershon ^b   Berger, Martin R ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Bone sialoprotein; Breast cancer bone metastasis; Nanoparticles; Osteolysis; Osteopontin; SiRNA

Indexed keywords

ANTINEOPLASTIC AGENT; BETA3 INTEGRIN; BONE SIALOPROTEIN; BONE SIALOPROTEIN SMALL INTERFERING RNA; GELATINASE A; NANOPARTICLE; OSTEOPONTIN; OSTEOPONTIN SMALL INTERFERING RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG; MESSENGER RNA;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIODEGRADABILITY; BIOLOGICAL ACTIVITY; BONE ATROPHY; BONE METASTASIS; BREAST CANCER; CANCER CELL; CANCER GENE THERAPY; CANCER INCIDENCE; CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; GENE; GENE SILENCING; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULARLY TARGETED THERAPY; NANOENCAPSULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOTIC PUMP; PARTICLE SIZE; PROTEIN EXPRESSION; RAT; TREATMENT DURATION; ZETA POTENTIAL; ANIMAL; BONE TUMOR; BREAST TUMOR; CELL MOTION; DRUG ANTAGONISM; FEMALE; GENETICS; HUMAN; METABOLISM; NUDE RAT; OSTEOLYSIS; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SECRETION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BONE NEOPLASMS; BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; HUMANS; INTEGRIN-BINDING SIALOPROTEIN; OSTEOLYSIS; OSTEOPONTIN; RATS; RATS, NUDE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED;

EID: 84862335808     PISSN: 02620898     EISSN: 15737276     Source Type: Journal    
DOI: 10.1007/s10585-012-9462-8     Document Type: Article

References (53)

1. Weinberg RA (2006) The biology of cancer. Garland Science, Oxford
2. Berenson JR (2001) Zoledronic acid in cancer patients with bone metastases: results of Phase I and II trials. Semin Oncol 28(2 Suppl 6):25-34 (Pubitemid 32494622)
3. Hortobagyi GN (1998) Treatment of breast cancer. New Engl J Med 339(14):974-984 (Pubitemid 28455101)
4. McArthur HL, Hudis CA (2009) Trastuzumab: a picky partner? Clin Cancer Res 15(20):6311-6313
5. Slamon DJ, Leyland-Jones B, Shak S et al (2001) Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. New Engl J Med 344(11):783-792 (Pubitemid 32222155)
6. Theriault RL, Lipton A, Hortobagyi GN 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(3):846-854 (Pubitemid 29109314)
7. Bos PD, Zhang XH, Nadal C et al (2009) Genes that mediate breast cancer metastasis to the brain. Nature 459(7249):1005- 1009
8. Kang Y, Siegel PM, Shu W et al (2003) A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3(6):537-549 (Pubitemid 36808649)
9. Heinegard D, Oldberg A (1989) Structure and biology of cartilage and bone matrix noncollagenous macromolecules. FASEB J 3(9):2042-2051 (Pubitemid 19187613)
10. Fisher LW, Whitson SW, Avioli LV et al (1983) Matrix sialoprotein of developing bone. J Biol Chem 258(20):12723-12727 (Pubitemid 14231187)
11. Fisher LW, Torchia DA, Fohr B et al (2001) Flexible structures of SIBLING proteins, bone sialoprotein, and osteopontin. Biochem Biophys Res Commun 280(2):460-465 (Pubitemid 32912812)
12. Noda M, Rodan GA (1989) Type beta transforming growth factor regulates expression of genes encoding bone matrix proteins. Connect Tissue Res 21(1-4):71-75
13. Ogata Y, Yamauchi M, Kim RH et al (1995) Glucocorticoid regulation of bone sialoprotein (BSP) gene expression. Identification of a glucocorticoid response element in the bone sialoprotein gene promoter. Eur J Biochem/FEBS 230(1):183-192
14. Pratap J, Lian JB, Javed A et al (2006) Regulatory roles of Runx2 in metastatic tumor and cancer cell interactions with bone. Cancer Metastasis Rev 25(4):589-600 (Pubitemid 46071865)
15. Byzova TV, Kim W, Midura RJ et al (2000) Activation of integrin alpha(V)beta(3) regulates cell adhesion and migration to bone sialoprotein. Exp Cell Res 254(2):299-308 (Pubitemid 30080586)
16. Das R, Mahabeleshwar GH, Kundu GC (2003) Osteopontin stimulates cell motility and nuclear factor kappaB-mediated secretion of urokinase type plasminogen activator through phosphatidylinositol 3-kinase/Akt signaling pathways in breast cancer cells. J Biol Chem 278(31):28593-28606 (Pubitemid 36935765)
17. DeMali KA, Wennerberg K, Burridge K (2003) Integrin signaling to the actin cytoskeleton. Curr Opin Cell Biol 15(5):572-582 (Pubitemid 37176966)
18. Gordon JA, Sodek J, Hunter GK et al (2009) Bone sialoprotein stimulates focal adhesion-related signaling pathways: role in migration and survival of breast and prostate cancer cells. J Cell Biochem 107(6):1118-1128
19. Guo W, Giancotti FG (2004) Integrin signalling during tumour progression. Nat Rev Mol Cell Biol 5(10):816-826 (Pubitemid 39336275)
20. Kiosses WB, Shattil SJ, Pampori N et al (2001) Rac recruits highaffinity integrin alphavbeta3 to lamellipodia in endothelial cell migration. Nat Cell Biol 3(3):316-320 (Pubitemid 32201329)
21. Rangaswami H, Bulbule A, Kundu GC (2006) Osteopontin: role in cell signaling and cancer progression. Trends Cell Biol 16(2): 79-87 (Pubitemid 43247403)
22. Sharp JA, Waltham M, Williams ED et al (2004) Transfection of MDA-MB-231 human breast carcinoma cells with bone sialoprotein (BSP) stimulates migration and invasion in vitro and growth of primary and secondary tumors in nude mice. Clin Exp Metastasis 21(1):19-29 (Pubitemid 38365654)
23. Bellahcene A, Castronovo V, Ogbureke KU et al (2008) Small integrin-binding ligand N-linked glycoproteins (SIBLINGs): multifunctional proteins in cancer. Nat Rev Cancer 8(3):212-226 (Pubitemid 351301854)
24. Fedarko NS, Jain A, Karadag A et al (2001) Elevated serum bone sialoprotein and osteopontin in colon, breast, prostate, and lung cancer. Clin Cancer Res 7(12):4060-4066 (Pubitemid 34044628)
25. Bellahcene A, Kroll M, Liebens F et al (1996) Bone sialoprotein expression in primary human breast cancer is associated with bone metastases development. J Bone Miner Res 11(5):665-670 (Pubitemid 26123917)
26. Bellahcene A, Menard S, Bufalino R et al (1996) Expression of bone sialoprotein in primary human breast cancer is associated with poor survival. Int J Cancer 69(4):350-353 (Pubitemid 26298303)
27. Bramwell VH, Doig GS, Tuck AB et al (2006) Serial plasma osteopontin levels have prognostic value in metastatic breast cancer. Clin Cancer Res 12(11 Pt 1):3337-3343
28. Diel IJ, Solomayer EF, Seibel MJ et al (1999) Serum bone sialoprotein in patients with primary breast cancer is a prognostic marker for subsequent bone metastasis. Clin Cancer Res 5(12):3914-3919 (Pubitemid 30013765)
29. Rudland PS, Platt-Higgins A, El-Tanani M et al (2002) Prognostic significance of the metastasis-associated protein osteopontin in human breast cancer. Cancer Res 62(12):3417-3427 (Pubitemid 34651388)
30. Shevde LA, Das S, Clark DW et al (2010) Osteopontin: an effector and an effect of tumor metastasis. Curr Mol Med 10(1): 71-81
31. Hedley BD, Welch DR, Allan AL et al (2008) Downregulation of osteopontin contributes to metastasis suppression by breast cancer metastasis suppressor 1. Int J Cancer 123(3):526-534 (Pubitemid 351898409)
32. Adwan H, Bauerle T, Najajreh Y et al (2004) Decreased levels of osteopontin and bone sialoprotein II are correlated with reduced proliferation, colony formation, and migration of GFP-MDAMB- 231 cells. Int J Oncol 24(5):1235-1244
33. Adwan H, Bauerle TJ, Berger MR (2004) Downregulation of osteopontin and bone sialoprotein II is related to reduced colony formation and metastasis formation of MDA-MB-231 human breast cancer cells. Cancer Gene Ther 11(2):109-120 (Pubitemid 38141773)
34. Uccello M, Malaguarnera G, Vacante M et al (2011) Serum bone sialoprotein levels and bone metastases. J Cancer Res Ther 7(2):115-119
35. Bauerle T, Adwan H, Kiessling F et al (2005) Characterization of a rat model with site-specific bone metastasis induced by MDAMB- 231 breast cancer cells and its application to the effects of an antibody against bone sialoprotein. Int J Cancer 115(2):177-186 (Pubitemid 40586725)
36. Weber GF (2001) The metastasis gene osteopontin: a candidate target for cancer therapy. Biochim Biophys Acta 1552(2):61-85 (Pubitemid 34124131)
37. Elazar V, Adwan H, Bauerle T et al (2010) Sustained delivery and efficacy of polymeric nanoparticles containing osteopontin and bone sialoprotein antisenses in rats with breast cancer bone metastasis. Int J Cancer 126(7):1749-1760
38. Dias N, Stein CA (2002) Antisense oligonucleotides: basic concepts and mechanisms. Mol Cancer Ther 1(5):347-355
39. Cohen-Sacks H, Najajreh Y, Tchaikovski V et al (2002) Novel PDGFbetaR antisense encapsulated in polymeric nanospheres for the treatment of restenosis. Gene Ther 9(23):1607-1616 (Pubitemid 35414523)
40. Elazar V, Adwan H, Rohekar K et al (2010) Biodistribution of antisense nanoparticles in mammary carcinoma rat model. Drug Deliv 17(6):408-418
41. Park JS, Na K, Woo DG et al (2010) Non-viral gene delivery of DNA polyplexed with nanoparticles transfected into human mesenchymal stem cells. Biomaterials 31(1):124-132
42. Senger DR, Perruzzi CA (1996) Cell migration promoted by a potent GRGDS-containing thrombin-cleavage fragment of osteopontin. Biochim Biophys Acta 1314(1-2):13-24 (Pubitemid 26395494)
43. Dahlgren C, Zhang HY, Du Q et al (2008) Analysis of siRNA specificity on targets with double-nucleotide mismatches. Nucleic Acids Res 36(9):e53
44. He J, Zhang JF, Yi C et al (2010) miRNA-mediated functional changes through co-regulating function related genes. PLoS ONE 5(10):e13558
45. Soldani C, Scovassi AI (2002) Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis 7(4):321-328 (Pubitemid 34832256)
46. Gross A, McDonnell JM, Korsmeyer SJ (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev 13(15): 1899-1911 (Pubitemid 29407357)
47. Duffy MJ, Maguire TM, Hill A et al (2000) Metalloproteinases: role in breast carcinogenesis, invasion and metastasis. Breast Cancer Res 2(4):252-257 (Pubitemid 32223594)
48. Bauerle T, Peterschmitt J, Hilbig H et al (2006) Treatment of bone metastasis induced by MDA-MB-231 breast cancer cells with an antibody against bone sialoprotein. Int J Oncol 28(3): 573-583
49. Peterschmitt J, Bauerle T, Berger MR (2007) Effect of zoledronic acid and an antibody against bone sialoprotein II on MDA-MB- 231(GFP) breast cancer cells in vitro and on osteolytic lesions induced in vivo by this cell line in nude rats. Clin Exp Metastasis 24(6):449-459 (Pubitemid 47367687)
50. Bauerle T, Hilbig H, Bartling S et al (2008) Bevacizumab inhibits breast cancer-induced osteolysis, surrounding soft tissue metastasis, and angiogenesis in rats as visualized by VCT and MRI. Neoplasia 10(5):511-520 (Pubitemid 351657393)
51. Shevde LA, Samant RS, Paik JC et al (2006) Osteopontin knockdown suppresses tumorigenicity of human metastatic breast carcinoma, MDA-MB-435. Clin Exp Metastasis 23(2):123-133 (Pubitemid 44440172)
52. Davis ME, Zuckerman JE, Choi CH et al (2010) Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles. Nature 464(7291):1067-1070
53. Lundberg BB (1997) Ether lipids enhance the cytotoxic effect of teniposide and paclitaxel in liposomes against leukaemic cells in culture. Anticancer Drug Des 12(6):503-513. (Pubitemid 27375906)