Skip to main content
Top
Published in: Journal of Experimental & Clinical Cancer Research 1/2018

Open Access 01-12-2018 | Research

Inhibitory effects of low intensity pulsed ultrasound on osteoclastogenesis induced in vitro by breast cancer cells

Authors: Valeria Carina, Viviana Costa, Stefania Pagani, Angela De Luca, Lavinia Raimondi, Daniele Bellavia, Stefania Setti, Milena Fini, Gianluca Giavaresi

Published in: Journal of Experimental & Clinical Cancer Research | Issue 1/2018

Login to get access

Abstract

Background

Bone tissue is one of the main sites for breast metastasis; patients diagnosed with advanced breast cancer mostly develop bone metastasis characterized by severe osteolytic lesions, which heavily influence their life quality. Low Intensity Pulsed Ultrasound (LIPUS) is a form of mechanical energy able to modulate various molecular pathways both in cancer and in health cells.
The purpose of the present study was to evaluate for the first time, the ability of LIPUS to modulate osteolytic capability of breast cancer cells.

Methods

Two different approaches were employed: a) Indirect method -conditioned medium obtained by MDA-MB-231 cell line treated or untreated with LIPUS was used to induce osteoclast differentiation of murine macrophage Raw264.7 cell line; and b) Direct method -MDA-MB-231 were co-cultured with Raw264.7 cells and treated or untreated with LIPUS.

Results

LIPUS treatment impaired MDA-MB-231 cell dependentosteoclast differentiation and produced a reduction of osteoclast markers such as Cathepsin K, Matrix Metalloproteinase 9 and Tartrate Resistant Acid Phosphatase, suggesting its role as an effective and safe adjuvant in bone metastasis management.

Conclusion

LIPUS treatment could be a good and safety therapeutic adjuvant in osteolyitic bone metastasis not only for the induction properties of bone regeneration, but also for the reduction of osteolysis.
Literature
1.
go back to reference Carvalho AF, Hyphantis T, Sales PMG, Soeiro-de-Souza MG, Macêdo DS, Cha DS, et al. Major depressive disorder in breast cancer: a critical systematic review of pharmacological and psychotherapeutic clinical trials. Cancer Treat Rev. 2014;40:349–55.CrossRefPubMed Carvalho AF, Hyphantis T, Sales PMG, Soeiro-de-Souza MG, Macêdo DS, Cha DS, et al. Major depressive disorder in breast cancer: a critical systematic review of pharmacological and psychotherapeutic clinical trials. Cancer Treat Rev. 2014;40:349–55.CrossRefPubMed
3.
go back to reference Eckhardt BL, Francis PA, Parker BS, Anderson RL. Strategies for the discovery and development of therapies for metastatic breast cancer. Nat Rev Drug Discov. 2012;11:479–97.CrossRefPubMed Eckhardt BL, Francis PA, Parker BS, Anderson RL. Strategies for the discovery and development of therapies for metastatic breast cancer. Nat Rev Drug Discov. 2012;11:479–97.CrossRefPubMed
4.
go back to reference Kennecke H, Yerushalmi R, Woods R, Cheang MCU, Voduc D, Speers CH, et al. Metastatic behavior of breast cancer subtypes. J Clin Oncol Off J Am Soc Clin Oncol. 2010;28:3271–7.CrossRef Kennecke H, Yerushalmi R, Woods R, Cheang MCU, Voduc D, Speers CH, et al. Metastatic behavior of breast cancer subtypes. J Clin Oncol Off J Am Soc Clin Oncol. 2010;28:3271–7.CrossRef
5.
go back to reference Largillier R, Ferrero J-M, Doyen J, Barriere J, Namer M, Mari V, et al. Prognostic factors in 1,038 women with metastatic breast cancer. Ann Oncol Off J Eur Soc Med Oncol. 2008;19:2012–9.CrossRef Largillier R, Ferrero J-M, Doyen J, Barriere J, Namer M, Mari V, et al. Prognostic factors in 1,038 women with metastatic breast cancer. Ann Oncol Off J Eur Soc Med Oncol. 2008;19:2012–9.CrossRef
6.
go back to reference Chang J, Clark GM, Allred DC, Mohsin S, Chamness G, Elledge RM. Survival of patients with metastatic breast carcinoma: importance of prognostic markers of the primary tumor. Cancer. 2003;97:545–53.CrossRefPubMed Chang J, Clark GM, Allred DC, Mohsin S, Chamness G, Elledge RM. Survival of patients with metastatic breast carcinoma: importance of prognostic markers of the primary tumor. Cancer. 2003;97:545–53.CrossRefPubMed
8.
go back to reference Coleman RE. Metastatic bone disease: clinical features, pathophysiology and treatment strategies. Cancer Treat Rev. 2001;27:165–76.CrossRefPubMed Coleman RE. Metastatic bone disease: clinical features, pathophysiology and treatment strategies. Cancer Treat Rev. 2001;27:165–76.CrossRefPubMed
9.
go back to reference Bendre MS, Montague DC, Peery T, Akel NS, Gaddy D, Suva LJ. Interleukin-8 stimulation of osteoclastogenesis and bone resorption is a mechanism for the increased osteolysis of metastatic bone disease. Bone. 2003;33:28–37.CrossRefPubMed Bendre MS, Montague DC, Peery T, Akel NS, Gaddy D, Suva LJ. Interleukin-8 stimulation of osteoclastogenesis and bone resorption is a mechanism for the increased osteolysis of metastatic bone disease. Bone. 2003;33:28–37.CrossRefPubMed
10.
go back to reference Bendre MS, Margulies AG, Walser B, Akel NS, Bhattacharrya S, Skinner RA, et al. Tumor-derived interleukin-8 stimulates osteolysis independent of the receptor activator of nuclear factor-kappaB ligand pathway. Cancer Res. 2005;65:11001–9.CrossRefPubMed Bendre MS, Margulies AG, Walser B, Akel NS, Bhattacharrya S, Skinner RA, et al. Tumor-derived interleukin-8 stimulates osteolysis independent of the receptor activator of nuclear factor-kappaB ligand pathway. Cancer Res. 2005;65:11001–9.CrossRefPubMed
11.
go back to reference Ohshiba T, Miyaura C, Ito A. Role of prostaglandin E produced by osteoblasts in osteolysis due to bone metastasis. Biochem Biophys Res Commun. 2003;300:957–64.CrossRefPubMed Ohshiba T, Miyaura C, Ito A. Role of prostaglandin E produced by osteoblasts in osteolysis due to bone metastasis. Biochem Biophys Res Commun. 2003;300:957–64.CrossRefPubMed
13.
go back to reference Morgan H, Tumber A, Hill PA. Breast cancer cells induce osteoclast formation by stimulating host IL-11 production and downregulating granulocyte/macrophage colony-stimulating factor. Int J Cancer. 2004;109:653–60.CrossRefPubMed Morgan H, Tumber A, Hill PA. Breast cancer cells induce osteoclast formation by stimulating host IL-11 production and downregulating granulocyte/macrophage colony-stimulating factor. Int J Cancer. 2004;109:653–60.CrossRefPubMed
14.
go back to reference Piccioli A, Maccauro G, Scaramuzzo L, Graci C, Spinelli MS. Surgical treatment of impending and pathological fractures of tibia. Injury. 2013;44:1092–6.CrossRefPubMed Piccioli A, Maccauro G, Scaramuzzo L, Graci C, Spinelli MS. Surgical treatment of impending and pathological fractures of tibia. Injury. 2013;44:1092–6.CrossRefPubMed
15.
go back to reference Piccioli A, Maccauro G, Rossi B, Scaramuzzo L, Frenos F, Capanna R. Surgical treatment of pathologic fractures of humerus. Injury. 2010;41:1112–6.CrossRefPubMed Piccioli A, Maccauro G, Rossi B, Scaramuzzo L, Frenos F, Capanna R. Surgical treatment of pathologic fractures of humerus. Injury. 2010;41:1112–6.CrossRefPubMed
16.
go back to reference Palma E, Correia JDG, Campello MPC, Santos I. Bisphosphonates as radionuclide carriers for imaging or systemic therapy. Mol BioSyst. 2011;7:2950–66.CrossRefPubMed Palma E, Correia JDG, Campello MPC, Santos I. Bisphosphonates as radionuclide carriers for imaging or systemic therapy. Mol BioSyst. 2011;7:2950–66.CrossRefPubMed
17.
go back to reference Paes FM, Serafini AN. Systemic metabolic radiopharmaceutical therapy in the treatment of metastatic bone pain. Semin Nucl Med. 2010;40:89–104.CrossRefPubMed Paes FM, Serafini AN. Systemic metabolic radiopharmaceutical therapy in the treatment of metastatic bone pain. Semin Nucl Med. 2010;40:89–104.CrossRefPubMed
18.
go back to reference Bodei L, Lam M, Chiesa C, Flux G, Brans B, Chiti A, et al. EANM procedure guideline for treatment of refractory metastatic bone pain. Eur J Nucl Med Mol Imaging. 2008;35:1934–40.CrossRefPubMed Bodei L, Lam M, Chiesa C, Flux G, Brans B, Chiti A, et al. EANM procedure guideline for treatment of refractory metastatic bone pain. Eur J Nucl Med Mol Imaging. 2008;35:1934–40.CrossRefPubMed
20.
go back to reference Simon CJ, Dupuy DE. Percutaneous minimally invasive therapies in the treatment of bone tumors: thermal ablation. Semin Musculoskelet Radiol. 2006;10:137–44.CrossRefPubMed Simon CJ, Dupuy DE. Percutaneous minimally invasive therapies in the treatment of bone tumors: thermal ablation. Semin Musculoskelet Radiol. 2006;10:137–44.CrossRefPubMed
21.
go back to reference Capanna R, Campanacci DA. The treatment of metastases in the appendicular skeleton. J Bone Joint Surg Br. 2001;83:471–81.CrossRefPubMed Capanna R, Campanacci DA. The treatment of metastases in the appendicular skeleton. J Bone Joint Surg Br. 2001;83:471–81.CrossRefPubMed
22.
go back to reference Nakada K, Kasai K, Watanabe Y, Katoh C, Kanegae K, Tsukamoto E, et al. Treatment of radioiodine-negative bone metastasis from papillary thyroid carcinoma with percutaneous ethanol injection therapy. Ann Nucl Med. 1996;10:441–4.CrossRefPubMed Nakada K, Kasai K, Watanabe Y, Katoh C, Kanegae K, Tsukamoto E, et al. Treatment of radioiodine-negative bone metastasis from papillary thyroid carcinoma with percutaneous ethanol injection therapy. Ann Nucl Med. 1996;10:441–4.CrossRefPubMed
24.
go back to reference Catane R, Beck A, Inbar Y, Rabin T, Shabshin N, Hengst S, et al. MR-guided focused ultrasound surgery (MRgFUS) for the palliation of pain in patients with bone metastases--preliminary clinical experience. Ann Oncol Off J Eur Soc Med Oncol. 2007;18:163–7.CrossRef Catane R, Beck A, Inbar Y, Rabin T, Shabshin N, Hengst S, et al. MR-guided focused ultrasound surgery (MRgFUS) for the palliation of pain in patients with bone metastases--preliminary clinical experience. Ann Oncol Off J Eur Soc Med Oncol. 2007;18:163–7.CrossRef
25.
go back to reference Xin Z, Lin G, Lei H, Lue TF, Guo Y. Clinical applications of low-intensity pulsed ultrasound and its potential role in urology. Transl Androl Urol. 2016;5:255–66.CrossRefPubMedPubMedCentral Xin Z, Lin G, Lei H, Lue TF, Guo Y. Clinical applications of low-intensity pulsed ultrasound and its potential role in urology. Transl Androl Urol. 2016;5:255–66.CrossRefPubMedPubMedCentral
26.
go back to reference Chu KF, Dupuy DE. Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat Rev Cancer. 2014;14:199–208.CrossRefPubMed Chu KF, Dupuy DE. Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat Rev Cancer. 2014;14:199–208.CrossRefPubMed
27.
28.
go back to reference Nolte PA, van der Krans A, Patka P, Janssen IM, Ryaby JP, Albers GH. Low-intensity pulsed ultrasound in the treatment of nonunions. J Trauma. 2001;51:693–702. discussion 702-703CrossRefPubMed Nolte PA, van der Krans A, Patka P, Janssen IM, Ryaby JP, Albers GH. Low-intensity pulsed ultrasound in the treatment of nonunions. J Trauma. 2001;51:693–702. discussion 702-703CrossRefPubMed
29.
go back to reference Rutten S, Nolte PA, Guit GL, Bouman DE, Albers GHR. Use of low-intensity pulsed ultrasound for posttraumatic nonunions of the tibia: a review of patients treated in the Netherlands. J Trauma. 2007;62:902–8.CrossRefPubMed Rutten S, Nolte PA, Guit GL, Bouman DE, Albers GHR. Use of low-intensity pulsed ultrasound for posttraumatic nonunions of the tibia: a review of patients treated in the Netherlands. J Trauma. 2007;62:902–8.CrossRefPubMed
30.
go back to reference Foley JL, Vaezy S, Crum LA. Applications of high-intensity focused ultrasound in medicine: spotlight on neurological applications. Appl Acoust. 2007;68:245–59.CrossRef Foley JL, Vaezy S, Crum LA. Applications of high-intensity focused ultrasound in medicine: spotlight on neurological applications. Appl Acoust. 2007;68:245–59.CrossRef
31.
go back to reference Mauck RL, Nicoll SB, Seyhan SL, Ateshian GA, Hung CT. Synergistic action of growth factors and dynamic loading for articular cartilage tissue engineering. Tissue Eng. 2003;9:597–611.CrossRefPubMed Mauck RL, Nicoll SB, Seyhan SL, Ateshian GA, Hung CT. Synergistic action of growth factors and dynamic loading for articular cartilage tissue engineering. Tissue Eng. 2003;9:597–611.CrossRefPubMed
32.
go back to reference Schulte FA, Ruffoni D, Lambers FM, Christen D, Webster DJ, Kuhn G, et al. Local mechanical stimuli regulate bone formation and resorption in mice at the tissue level. PLoS One. 2013;8:e62172.CrossRefPubMedPubMedCentral Schulte FA, Ruffoni D, Lambers FM, Christen D, Webster DJ, Kuhn G, et al. Local mechanical stimuli regulate bone formation and resorption in mice at the tissue level. PLoS One. 2013;8:e62172.CrossRefPubMedPubMedCentral
33.
go back to reference Costa V, Carina V, Fontana S, De Luca A, Monteleone F, Pagani S, et al. Osteogenic commitment and differentiation of human mesenchymal stem cells by low-intensity pulsed ultrasound stimulation. J Cell Physiol. 2018;233:1558–73.CrossRefPubMed Costa V, Carina V, Fontana S, De Luca A, Monteleone F, Pagani S, et al. Osteogenic commitment and differentiation of human mesenchymal stem cells by low-intensity pulsed ultrasound stimulation. J Cell Physiol. 2018;233:1558–73.CrossRefPubMed
34.
go back to reference Erdogan O, Esen E. Biological aspects and clinical importance of ultrasound therapy in bone healing. J Ultrasound Med Off J Am Inst Ultrasound Med. 2009;28:765–76.CrossRef Erdogan O, Esen E. Biological aspects and clinical importance of ultrasound therapy in bone healing. J Ultrasound Med Off J Am Inst Ultrasound Med. 2009;28:765–76.CrossRef
35.
go back to reference Fung C-H, Cheung W-H, Pounder NM, Harrison A, Leung K-S. Osteocytes exposed to far field of therapeutic ultrasound promotes osteogenic cellular activities in pre-osteoblasts through soluble factors. Ultrasonics. 2014;54:1358–65.CrossRefPubMed Fung C-H, Cheung W-H, Pounder NM, Harrison A, Leung K-S. Osteocytes exposed to far field of therapeutic ultrasound promotes osteogenic cellular activities in pre-osteoblasts through soluble factors. Ultrasonics. 2014;54:1358–65.CrossRefPubMed
36.
go back to reference Li X, Li J, Cheng K, Lin Q, Wang D, Zhang H, et al. Effect of low-intensity pulsed ultrasound on MMP-13 and MAPKs signaling pathway in rabbit knee osteoarthritis. Cell Biochem Biophys. 2011;61:427–34.CrossRefPubMed Li X, Li J, Cheng K, Lin Q, Wang D, Zhang H, et al. Effect of low-intensity pulsed ultrasound on MMP-13 and MAPKs signaling pathway in rabbit knee osteoarthritis. Cell Biochem Biophys. 2011;61:427–34.CrossRefPubMed
37.
go back to reference Sawai Y, Murata H, Koto K, Matsui T, Horie N, Ashihara E, et al. Effects of low-intensity pulsed ultrasound on osteosarcoma and cancer cells. Oncol Rep. 2012;28:481–6.CrossRefPubMed Sawai Y, Murata H, Koto K, Matsui T, Horie N, Ashihara E, et al. Effects of low-intensity pulsed ultrasound on osteosarcoma and cancer cells. Oncol Rep. 2012;28:481–6.CrossRefPubMed
38.
go back to reference Guo Y, Tiedemann K, Khalil JA, Russo C, Siegel PM, Komarova SV. Osteoclast precursors acquire sensitivity to breast cancer derived factors early in differentiation. Bone. 2008;43:386–93.CrossRefPubMed Guo Y, Tiedemann K, Khalil JA, Russo C, Siegel PM, Komarova SV. Osteoclast precursors acquire sensitivity to breast cancer derived factors early in differentiation. Bone. 2008;43:386–93.CrossRefPubMed
39.
go back to reference Raimondi L, De Luca A, Amodio N, Manno M, Raccosta S, Taverna S, et al. Involvement of multiple myeloma cell-derived exosomes in osteoclast differentiation. Oncotarget. 2015;6:13772–89.CrossRefPubMedPubMedCentral Raimondi L, De Luca A, Amodio N, Manno M, Raccosta S, Taverna S, et al. Involvement of multiple myeloma cell-derived exosomes in osteoclast differentiation. Oncotarget. 2015;6:13772–89.CrossRefPubMedPubMedCentral
40.
go back to reference Lin C-W, Shen S-C, Ko C-H, Lin H-Y, Chen Y-C. Reciprocal activation of macrophages and breast carcinoma cells by nitric oxide and colony-stimulating factor-1. Carcinogenesis. 2010;31:2039–48.CrossRefPubMed Lin C-W, Shen S-C, Ko C-H, Lin H-Y, Chen Y-C. Reciprocal activation of macrophages and breast carcinoma cells by nitric oxide and colony-stimulating factor-1. Carcinogenesis. 2010;31:2039–48.CrossRefPubMed
41.
go back to reference Carina V, Costa V, Raimondi L, Pagani S, Sartori M, Figallo E, et al. Effect of low-intensity pulsed ultrasound on osteogenic human mesenchymal stem cells commitment in a new bone scaffold. J Appl Biomater Funct Mater. 2017;15:e215–22.PubMed Carina V, Costa V, Raimondi L, Pagani S, Sartori M, Figallo E, et al. Effect of low-intensity pulsed ultrasound on osteogenic human mesenchymal stem cells commitment in a new bone scaffold. J Appl Biomater Funct Mater. 2017;15:e215–22.PubMed
42.
go back to reference Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C (T)) method. Methods San Diego Calif. 2001;25:402–8.CrossRef Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C (T)) method. Methods San Diego Calif. 2001;25:402–8.CrossRef
45.
go back to reference Zhang N, Chow SK-H, Leung K-S, Cheung W-H. Ultrasound as a stimulus for musculoskeletal disorders. J Orthop Transl. 2017;9:52–9. Zhang N, Chow SK-H, Leung K-S, Cheung W-H. Ultrasound as a stimulus for musculoskeletal disorders. J Orthop Transl. 2017;9:52–9.
46.
48.
go back to reference El-Mowafi H, Mohsen M. The effect of low-intensity pulsed ultrasound on callus maturation in tibial distraction osteogenesis. Int Orthop. 2005;29:121–4.CrossRefPubMedPubMedCentral El-Mowafi H, Mohsen M. The effect of low-intensity pulsed ultrasound on callus maturation in tibial distraction osteogenesis. Int Orthop. 2005;29:121–4.CrossRefPubMedPubMedCentral
49.
go back to reference Akiyama H, Hachiya Y, Otsuka H, Kurisuno M, Kawanabe K, Katayama N, et al. Low-intensity pulsed ultrasound therapy stimulates callus formation between host femur and cortical onlay strut allograft. Ultrasound Med Biol. 2014;40:1197–203.CrossRefPubMed Akiyama H, Hachiya Y, Otsuka H, Kurisuno M, Kawanabe K, Katayama N, et al. Low-intensity pulsed ultrasound therapy stimulates callus formation between host femur and cortical onlay strut allograft. Ultrasound Med Biol. 2014;40:1197–203.CrossRefPubMed
50.
go back to reference Bashardoust Tajali S, Houghton P, MacDermid JC, Grewal R. Effects of low-intensity pulsed ultrasound therapy on fracture healing: a systematic review and meta-analysis. Am J Phys Med Rehabil. 2012;91:349–67.CrossRefPubMed Bashardoust Tajali S, Houghton P, MacDermid JC, Grewal R. Effects of low-intensity pulsed ultrasound therapy on fracture healing: a systematic review and meta-analysis. Am J Phys Med Rehabil. 2012;91:349–67.CrossRefPubMed
51.
go back to reference Unsworth J, Kaneez S, Harris S, Ridgway J, Fenwick S, Chenery D, et al. Pulsed low intensity ultrasound enhances mineralisation in preosteoblast cells. Ultrasound Med Biol. 2007;33:1468–74.CrossRefPubMed Unsworth J, Kaneez S, Harris S, Ridgway J, Fenwick S, Chenery D, et al. Pulsed low intensity ultrasound enhances mineralisation in preosteoblast cells. Ultrasound Med Biol. 2007;33:1468–74.CrossRefPubMed
52.
go back to reference Busse JW, Bhandari M, Einhorn TA, Heckman JD, Leung K-S, Schemitsch E, et al. Trial to re-evaluate ultrasound in the treatment of tibial fractures (TRUST): a multicenter randomized pilot study. Trials. 2014;15:206.CrossRefPubMedPubMedCentral Busse JW, Bhandari M, Einhorn TA, Heckman JD, Leung K-S, Schemitsch E, et al. Trial to re-evaluate ultrasound in the treatment of tibial fractures (TRUST): a multicenter randomized pilot study. Trials. 2014;15:206.CrossRefPubMedPubMedCentral
53.
54.
go back to reference Napoli A, Anzidei M, Ciolina F, Marotta E, Cavallo Marincola B, Brachetti G, et al. MR-guided high-intensity focused ultrasound: current status of an emerging technology. Cardiovasc Intervent Radiol. 2013;36:1190–203.CrossRefPubMed Napoli A, Anzidei M, Ciolina F, Marotta E, Cavallo Marincola B, Brachetti G, et al. MR-guided high-intensity focused ultrasound: current status of an emerging technology. Cardiovasc Intervent Radiol. 2013;36:1190–203.CrossRefPubMed
55.
go back to reference Hurwitz MD, Ghanouni P, Kanaev SV, Iozeffi D, Gianfelice D, Fennessy FM, et al. Magnetic resonance-guided focused ultrasound for patients with painful bone metastases: phase III trial results. J Natl Cancer Inst. 2014;106(5). Hurwitz MD, Ghanouni P, Kanaev SV, Iozeffi D, Gianfelice D, Fennessy FM, et al. Magnetic resonance-guided focused ultrasound for patients with painful bone metastases: phase III trial results. J Natl Cancer Inst. 2014;106(5).
56.
go back to reference Malietzis G, Monzon L, Hand J, Wasan H, Leen E, Abel M, et al. High-intensity focused ultrasound: advances in technology and experimental trials support enhanced utility of focused ultrasound surgery in oncology. Br J Radiol. 2013;86:20130044.CrossRefPubMedPubMedCentral Malietzis G, Monzon L, Hand J, Wasan H, Leen E, Abel M, et al. High-intensity focused ultrasound: advances in technology and experimental trials support enhanced utility of focused ultrasound surgery in oncology. Br J Radiol. 2013;86:20130044.CrossRefPubMedPubMedCentral
57.
go back to reference Wu J, Nyborg WL. Ultrasound, cavitation bubbles and their interaction with cells. Adv Drug Deliv Rev. 2008;60:1103–16.CrossRefPubMed Wu J, Nyborg WL. Ultrasound, cavitation bubbles and their interaction with cells. Adv Drug Deliv Rev. 2008;60:1103–16.CrossRefPubMed
58.
go back to reference Yudina A, Moonen C. Ultrasound-induced cell permeabilisation and hyperthermia: strategies for local delivery of compounds with intracellular mode of action. Int J Hyperth Off J Eur Soc Hyperthermic Oncol North Am Hyperth Group. 2012;28:311–9.CrossRef Yudina A, Moonen C. Ultrasound-induced cell permeabilisation and hyperthermia: strategies for local delivery of compounds with intracellular mode of action. Int J Hyperth Off J Eur Soc Hyperthermic Oncol North Am Hyperth Group. 2012;28:311–9.CrossRef
59.
go back to reference Evjen TJ, Hagtvet E, Moussatov A, Røgnvaldsson S, Mestas J-L, Fowler RA, et al. In vivo monitoring of liposomal release in tumours following ultrasound stimulation. Eur J Pharm Biopharm Off J Arbeitsgemeinschaft Pharm Verfahrenstechnik EV. 2013;84:526–31.CrossRef Evjen TJ, Hagtvet E, Moussatov A, Røgnvaldsson S, Mestas J-L, Fowler RA, et al. In vivo monitoring of liposomal release in tumours following ultrasound stimulation. Eur J Pharm Biopharm Off J Arbeitsgemeinschaft Pharm Verfahrenstechnik EV. 2013;84:526–31.CrossRef
60.
go back to reference Raimondi L, Amodio N, Di Martino MT, Altomare E, Leotta M, Caracciolo D, et al. Targeting of multiple myeloma-related angiogenesis by miR-199a-5p mimics: in vitro and in vivo anti-tumor activity. Oncotarget. 2014;5:3039–54.CrossRefPubMedPubMedCentral Raimondi L, Amodio N, Di Martino MT, Altomare E, Leotta M, Caracciolo D, et al. Targeting of multiple myeloma-related angiogenesis by miR-199a-5p mimics: in vitro and in vivo anti-tumor activity. Oncotarget. 2014;5:3039–54.CrossRefPubMedPubMedCentral
61.
go back to reference Costa AG, Cusano NE, Silva BC, Cremers S, Bilezikian JP. Cathepsin K: its skeletal actions and role as a therapeutic target in osteoporosis. Nat Rev Rheumatol. 2011;7:447–56.CrossRefPubMed Costa AG, Cusano NE, Silva BC, Cremers S, Bilezikian JP. Cathepsin K: its skeletal actions and role as a therapeutic target in osteoporosis. Nat Rev Rheumatol. 2011;7:447–56.CrossRefPubMed
62.
go back to reference Aimes RT, Quigley JP. Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4- and 1/4-length fragments. J Biol Chem. 1995;270:5872–6.CrossRefPubMed Aimes RT, Quigley JP. Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4- and 1/4-length fragments. J Biol Chem. 1995;270:5872–6.CrossRefPubMed
63.
go back to reference Kusano K, Miyaura C, Inada M, Tamura T, Ito A, Nagase H, et al. Regulation of matrix metalloproteinases (MMP-2, −3, −9, and −13) by interleukin-1 and interleukin-6 in mouse calvaria: association of MMP induction with bone resorption. Endocrinology. 1998;139:1338–45.CrossRefPubMed Kusano K, Miyaura C, Inada M, Tamura T, Ito A, Nagase H, et al. Regulation of matrix metalloproteinases (MMP-2, −3, −9, and −13) by interleukin-1 and interleukin-6 in mouse calvaria: association of MMP induction with bone resorption. Endocrinology. 1998;139:1338–45.CrossRefPubMed
64.
go back to reference Feres MFN, Kucharski C, Diar-Bakirly S, El-Bialy T. Effect of low-intensity pulsed ultrasound on the activity of osteoclasts: an in vitro study. Arch Oral Biol. 2016;70:73–8.CrossRefPubMed Feres MFN, Kucharski C, Diar-Bakirly S, El-Bialy T. Effect of low-intensity pulsed ultrasound on the activity of osteoclasts: an in vitro study. Arch Oral Biol. 2016;70:73–8.CrossRefPubMed
65.
go back to reference Miyazaki T, Miyauchi S, Anada T, Imaizumi H, Suzuki O. Evaluation of osteoclastic resorption activity using calcium phosphate coating combined with labeled polyanion. Anal Biochem. 2011;410:7–12.CrossRefPubMed Miyazaki T, Miyauchi S, Anada T, Imaizumi H, Suzuki O. Evaluation of osteoclastic resorption activity using calcium phosphate coating combined with labeled polyanion. Anal Biochem. 2011;410:7–12.CrossRefPubMed
66.
go back to reference Monici M, Bernabei PA, Basile V, Romano G, Conti A, Breschi L, et al. Can ultrasound counteract bone loss? Effect of low-intensity ultrasound stimulation on a model of osteoclastic precursor. Acta Astronaut. 2007;60:383–90.CrossRef Monici M, Bernabei PA, Basile V, Romano G, Conti A, Breschi L, et al. Can ultrasound counteract bone loss? Effect of low-intensity ultrasound stimulation on a model of osteoclastic precursor. Acta Astronaut. 2007;60:383–90.CrossRef
68.
go back to reference De Luca A, Raimondi L, Salamanna F, Carina V, Costa V, Bellavia D, et al. Relevance of 3d culture systems to study osteosarcoma environment. J Exp Clin Cancer Res CR. 2018;37:2. De Luca A, Raimondi L, Salamanna F, Carina V, Costa V, Bellavia D, et al. Relevance of 3d culture systems to study osteosarcoma environment. J Exp Clin Cancer Res CR. 2018;37:2.
69.
go back to reference Fini M, Salamanna F, Parrilli A, Martini L, Cadossi M, Maglio M, et al. Electrochemotherapy is effective in the treatment of rat bone metastases. Clin Exp Metastasis. 2013;30:1033–45.CrossRefPubMed Fini M, Salamanna F, Parrilli A, Martini L, Cadossi M, Maglio M, et al. Electrochemotherapy is effective in the treatment of rat bone metastases. Clin Exp Metastasis. 2013;30:1033–45.CrossRefPubMed
Metadata
Title
Inhibitory effects of low intensity pulsed ultrasound on osteoclastogenesis induced in vitro by breast cancer cells
Authors
Valeria Carina
Viviana Costa
Stefania Pagani
Angela De Luca
Lavinia Raimondi
Daniele Bellavia
Stefania Setti
Milena Fini
Gianluca Giavaresi
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Experimental & Clinical Cancer Research / Issue 1/2018
Electronic ISSN: 1756-9966
DOI
https://doi.org/10.1186/s13046-018-0868-2

Other articles of this Issue 1/2018

Journal of Experimental & Clinical Cancer Research 1/2018 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine