Role of tumor‑derived exosomes in bone metastasis (Review)
- Authors:
- Fu‑Xing‑Zi Li
- Jun‑Jie Liu
- Feng Xu
- Xiao Lin
- Jia‑Yu Zhong
- Feng Wu
- Ling‑Qing Yuan
-
Affiliations: Department of Endocrinology and Metabolism, Hunan Provincial Key Laboratory of Metabolic Bone Diseases, National Clinical Research Center for Metabolic Disease, The Second Xiang‑Ya Hospital, Central South University, Changsha, Hunan 410011, P.R. China, Department of Pathology, The Xiangya Stomatological Hospital, Central South University, Changsha, Hunan 410011, P.R. China, Department of Geriatrics, The Second Xiang‑Ya Hospital, Central South University, Changsha, Hunan 410011, P.R. China, Department of Pathology, The Second Xiang‑Ya Hospital, Central South University, Changsha, Hunan 410011, P.R. China - Published online on: August 22, 2019 https://doi.org/10.3892/ol.2019.10776
- Pages: 3935-3945
-
Copyright: © Li et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Bray F, Jemal A, Grey N, Ferlay J and Forman D: Global cancer transitions according to the Human Development Index (2008–2030): A population-based study. Lancet Oncol. 13:790–801. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gupta GP and Massagué J: Cancer metastasis: Building a framework. Cell. 127:679–695. 2006. View Article : Google Scholar : PubMed/NCBI | |
Mundy GR: Metastasis to bone: Causes, consequences and therapeutic opportunities. Nat Rev Cancer. 2:584–593. 2002. View Article : Google Scholar : PubMed/NCBI | |
Weilbaecher KN, Guise TA and McCauley LK: Cancer to bone: A fatal attraction. Nat Rev Cancer. 11:411–425. 2011. View Article : Google Scholar : PubMed/NCBI | |
Lalle M, De Rosa L, Marzetti L and Montuoro A: Detection of breast cancer cells in the bone marrow or peripheral blood: Methods and prognostic significance. Tumori. 86:183–190. 2000. View Article : Google Scholar : PubMed/NCBI | |
Van Der Pluijm G, Sijmons B, Vloedgraven H, Deckers M, Papapoulos S and Löwik C: Monitoring metastatic behavior of human tumor cells in mice with species-specific polymerase chain reaction: Elevated expression of angiogenesis and bone resorption stimulators by breast cancer in bone metastases. J Bone Miner Res. 16:1077–1091. 2001. View Article : Google Scholar : PubMed/NCBI | |
Jemal A, Siegel R, Xu J and Ward E: Cancer statistics, 2010. CA Cancer J Clin. 60:277–300. 2010. View Article : Google Scholar : PubMed/NCBI | |
Van Driel M and Van Leeuwen JP: Cancer and bone: A complex complex. Arch Biochem Biophys. 561:159–166. 2014. View Article : Google Scholar : PubMed/NCBI | |
Lynch ME and Fischbach C: Biomechanical forces in the skeleton and their relevance to bone metastasis: Biology and engineering considerations. Adv Drug Deliv Rev. 79-80:119–134. 2014. View Article : Google Scholar : PubMed/NCBI | |
Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, Becker A, Hoshino A, Mark MT, Molina H, et al: Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 17:816–826. 2015. View Article : Google Scholar : PubMed/NCBI | |
Sceneay J, Parker BS, Smyth MJ and Möller A: Hypoxia-driven immunosuppression contributes to the pre-metastatic niche. Oncoimmunology. 2:e223552013. View Article : Google Scholar : PubMed/NCBI | |
Sceneay J, Smyth MJ and Möller A: The pre-metastatic niche: Finding common ground. Cancer Metastasis Rev. 32:449–464. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hu Y, Rao SS, Wang ZX, Cao J, Tan YJ, Luo J, Li HM, Zhang WS, Chen CY and Xie H: Exosomes from human umbilical cord blood accelerate cutaneous wound healing through miR-21-3p-mediated promotion of angiogenesis and fibroblast function. Theranostics. 8:169–184. 2018. View Article : Google Scholar : PubMed/NCBI | |
Chen CY, Rao SS, Ren L, Hu XK, Tan YJ, Hu Y, Luo J, Liu YW, Yin H, Huang J, et al: Exosomal DMBT1 from human urine-derived stem cells facilitates diabetic wound repair by promoting angiogenesis. Theranostics. 8:1607–1623. 2018. View Article : Google Scholar : PubMed/NCBI | |
Record M, Silvente-Poirot S, Poirot M and Wakelam MJO: Extracellular vesicles: Lipids as key components of their biogenesis and functions. J Lipid Res. 59:1316–1324. 2018. View Article : Google Scholar : PubMed/NCBI | |
Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM and Breakefield XO: Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 10:1470–1476. 2008. View Article : Google Scholar : PubMed/NCBI | |
Sun Y and Liu J: Potential of cancer cell derived exosomes in clinical application: A review of recent research advances. Clin Ther. 36:863–872. 2014. View Article : Google Scholar : PubMed/NCBI | |
Yáñezmó M, Siljander PR, Andreu Z, Zavec AB, Borràs FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, et al: Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 4:270662015. View Article : Google Scholar : PubMed/NCBI | |
Zeelenberg IS, Ostrowski M, Krumeich S, Bobrie A, Jancic C, Boissonnas A, Delcayre A, Le Pecq JB, Combadière B, Amigorena S and Théry C: Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res. 68:1228–1235. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kumar S and Reddy PH: Are circulating microRNAs peripheral biomarkers for Alzheimer's disease? Biochim Biophys Acta. 1862:1617–1627. 2016. View Article : Google Scholar : PubMed/NCBI | |
Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ and Lötvall JO: Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 9:654–659. 2007. View Article : Google Scholar : PubMed/NCBI | |
Li JJ, Wang B, Kodali MC, Chao C, Kim E, Patters BJ, Lan L, Kumar S, Wang X, Yue J and Liao FF: In vivo evidence for the contribution of peripheral circulating inflammatory exosomes to neuroinflammation. J Neuroinflammation. 15:82018. View Article : Google Scholar : PubMed/NCBI | |
Lässer C, Alikhani VS, Ekström K, Eldh M, Paredes PT, Bossios A, Sjöstrand M, Gabrielsson S, Lötvall J and Valadi H: Human saliva, plasma and breast milk exosomes contain RNA: Uptake by macrophages. J Transl Med. 9:92011. View Article : Google Scholar : PubMed/NCBI | |
Admyre C, Johansson SM, Qazi KR, Filén JJ, Lahesmaa R, Norman M, Neve EP, Scheynius A and Gabrielsson S: Exosomes with immune modulatory features are present in human breast milk. J Immunol. 179:1969–1978. 2007. View Article : Google Scholar : PubMed/NCBI | |
Street JM, Barran PE, Mackay CL, Weidt S, Balmforth C, Walsh TS, Chalmers RT, Webb DJ and Dear JW: Identification and proteomic profiling of exosomes in human cerebrospinal fluid. J Transl Med. 10:52012. View Article : Google Scholar : PubMed/NCBI | |
Vojtech L, Woo S, Hughes S, Levy C, Ballweber L, Sauteraud RP, Strobl J, Westerberg K, Gottardo R, Tewari M and Hladik F: Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res. 42:7290–7304. 2014. View Article : Google Scholar : PubMed/NCBI | |
Hong BS, Cho JH, Kim H, Choi EJ, Rho S, Kim J, Kim JH, Choi DS, Kim YK, Hwang D and Gho YS: Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells. BMC Genomics. 10:5562009. View Article : Google Scholar : PubMed/NCBI | |
Kumar B, Garcia M, Murakami JL and Chen CC: Exosome-mediated microenvironment dysregulation in leukemia. Biochim Biophys Acta. 1863:464–470. 2016. View Article : Google Scholar : PubMed/NCBI | |
Suetsugu A, Honma K, Saji S, Moriwaki H, Ochiya T and Hoffman RM: Imaging exosome transfer from breast cancer cells to stroma at metastatic sites in orthotopic nude-mouse models. Adv Drug Deliv Rev. 65:383–390. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kogure T, Lin WL, Yan IK, Braconi C and Patel T: Intercellular nanovesicle-mediated microRNA transfer: A mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology. 54:1237–1248. 2011. View Article : Google Scholar : PubMed/NCBI | |
Yu S, Cao H, Shen B and Feng J: Tumor-derived exosomes in cancer progression and treatment failure. Oncotarget. 6:37151–37168. 2015. View Article : Google Scholar : PubMed/NCBI | |
Luga V and Wrana JL: Tumor-stroma interaction: Revealing fibroblast-secreted exosomes as potent regulators of Wnt-planar cell polarity signaling in cancer metastasis. Cancer Res. 73:6843–6847. 2013. View Article : Google Scholar : PubMed/NCBI | |
Shao Y, Shen Y, Chen T, Xu F, Chen X and Zheng S: The functions and clinical applications of tumor-derived exosomes. Oncotarget. 7:60736–60751. 2016. View Article : Google Scholar : PubMed/NCBI | |
Corrado C, Raimondo S, Chiesi A, Ciccia F, De Leo G and Alessandro R: Exosomes as intercellular signaling organelles involved in health and disease: Basic science and clinical applications. Int J Mol Sci. 14:5338–5366. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kowal J, Tkach M and Théry C: Biogenesis and secretion of exosomes. Curr Opin Cell Biol. 29:116–125. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ekström EJ, Bergenfelz C, von Bülow V, Serifler F, Carlemalm E, Jönsson G, Andersson T and Leandersson K: WNT5A induces release of exosomes containing pro-angiogenic and immunosuppressive factors from malignant melanoma cells. Mol Cancer. 13:882014. View Article : Google Scholar : PubMed/NCBI | |
Man YG, Stojadinovic A, Mason J, Avital I, Bilchik A, Bruecher B, Protic M, Nissan A, Izadjoo M, Zhang X and Jewett A: Tumor-infiltrating immune cells promoting tumor invasion and metastasis: Existing theories. J Cancer. 4:84–95. 2013. View Article : Google Scholar : PubMed/NCBI | |
Xue M, Zhuo Y and Shan B: MicroRNAs, long noncoding RNAs, and their functions in human disease. Methods Mol Biol. 1617:1–25. 2017. View Article : Google Scholar : PubMed/NCBI | |
Thomou T, Mori MA, Dreyfuss JM, Konishi M, Sakaguchi M, Wolfrum C, Rao TN, Winnay JN, Garcia-Martin R, Grinspoon SK, et al: Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature. 542:450–455. 2017. View Article : Google Scholar : PubMed/NCBI | |
Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, Chiu E, Buchanan M, Hosein AN, Basik M and Wrana JL: Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell. 151:1542–1556. 2012. View Article : Google Scholar : PubMed/NCBI | |
van Balkom BW, de Jong OG, Smits M, Brummelman J, den Ouden K, de Bree PM, van Eijndhoven MA, Pegtel DM, Stoorvogel W, Würdinger T and Verhaar MC: Endothelial cellsrequire miR-214 to secrete exosomes that suppress senescence and induce angiogenesis in human and mouse endothelial cells. Blood. 121:3997–4006. 2013. View Article : Google Scholar : PubMed/NCBI | |
Cui Y, Luan J, Li H, Zhou X and Han J: Exosomes derived from mineralizing osteoblasts promote ST2 cell osteogenic differentiation by alteration of microRNA expression. FEBS Lett. 590:185–192. 2016. View Article : Google Scholar : PubMed/NCBI | |
Henderson MC and Azorsa DO: The genomic and proteomic content of cancer cellderived exosomes. Front Oncol. 2:382012. View Article : Google Scholar : PubMed/NCBI | |
Nolte-'t Hoen EN, Buermans HP, Waasdorp M, Stoorvogel W, Wauben MH and 't Hoen PA: Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res. 40:9272–9285. 2012. View Article : Google Scholar : PubMed/NCBI | |
Cazzoli R, Buttitta F, Di Nicola M, Malatesta S, Marchetti A, Rom WN and Pass HI: microRNAs derived from circulating exosomes as noninvasive biomarkers for screening and diagnosing lung cancer. J Thorac Oncol. 8:1156–1162. 2013. View Article : Google Scholar : PubMed/NCBI | |
Corcoran C, Friel AM, Duffy MJ, Crown J and O'Driscoll L: Intracellular and extracellular microRNAs in breast cancer. Clin Chem. 57:18–32. 2011. View Article : Google Scholar : PubMed/NCBI | |
Paget S: The distribution of secondary growths in cancer of the breast. 1889 Cancer Metastasis Rev. 8:98–101. 1889. | |
Brennan MF and Ekman L: Metabolic consequences of nutritional support of the cancer patient. Cancer. 54 (11 Suppl):S2627–S2634. 1984. View Article : Google Scholar | |
Guise TA, Mohammad KS, Clines G, Stebbins EG, Wong DH, Higgins LS, Vessella R, Corey E, Padalecki S, Suva L and Chirgwin JM: Basic mechanisms responsible for osteolytic and osteoblastic bone metastases. Clin Cancer Res. 12:6213s–6216s. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kingsley LA, Fournier PG, Chirgwin JM and Guise TA: Molecular biology of bone metastasis. Mol Cancer Ther. 6:2609–2617. 2007. View Article : Google Scholar : PubMed/NCBI | |
Pantel K, Müller V, Auer M, Nusser N, Harbeck N and Braun S: Detection and clinical implications of early systemic tumor cell dissemination in breast cancer. Clin Cancer Res. 9:6326–6334. 2003.PubMed/NCBI | |
Aft R, Naughton M, Trinkaus K, Watson M, Ylagan L, Chavez-Macgregor M, Zhai J, Kuo S, Shannon W, Diemer K, et al: Effect of zoledronic acid on disseminated tumour cells in women with locally advanced breast cancer: An open label, randomised, phase 2 trial. Lancet Oncol. 11:421–428. 2010. View Article : Google Scholar : PubMed/NCBI | |
Chen H, Senda T and Kubo KY: The osteocyte plays multiple roles in bone remodeling and mineral homeostasis. Med Mol Morphol. 48:61–68. 2015. View Article : Google Scholar : PubMed/NCBI | |
Nguyen DX, Bos PD and Massagué J: Metastasis: From dissemination to organ-specific colonization. Nat Rev Cancer. 9:274–284. 2009. View Article : Google Scholar : PubMed/NCBI | |
Saleem SN and Abdel-Mageed AB: Tumor-derived exosomes in oncogenic reprogramming and cancer progression. Cell Mol Life Sci. 72:1–10. 2015. View Article : Google Scholar : PubMed/NCBI | |
Clézardin P: The role of RANK/RANKL/osteoprotegerin (OPG) triad in cancer-induced bone diseases: Physiopathology and clinical implications. Bull Cancer. 98:837–846. 2011.(In French). View Article : Google Scholar : PubMed/NCBI | |
Sanders JL, Chattopadhyay N, Kifor O, Yamaguchi T, Butters RR and Brown EM: Extracellular calcium-sensing receptor expression and its potential role in regulating parathyroid hormone-related peptide secretion in human breast cancer cell lines. Endocrinology. 141:4357–4364. 2000. View Article : Google Scholar : PubMed/NCBI | |
Siveen KS, Prabhu K, Krishnankutty R, Kuttikrishnan S, Tsakou M, Alali FQ, Dermime S, Mohammad RM and Uddin S: Vascular endothelial growth factor (VEGF) signaling in tumour vascularization: Potential and challenges. Curr Vasc Pharmacol. 15:339–351. 2017. View Article : Google Scholar : PubMed/NCBI | |
Heldin CH, Lennartsson J and Westermark B: Involvement of platelet-derived growth factor ligands and receptors in tumorigenesis. J Intern Med. 283:16–44. 2018. View Article : Google Scholar : PubMed/NCBI | |
Chirgwin JM, Mohammad KS and Guise TA: Tumor-bone cellular interactions in skeletal metastases. J Musculoskeletal Neuronal Interact. 4:308–318. 2004. | |
Chang AC, Chen PC, Lin YF, Su CM, Liu JF, Lin TH, Chuang SM and Tang CH: Osteoblast-secreted WISP-1 promotes adherence of prostate cancer cells to bone via the VCAM-1/integrin α4β1 system. Cancer Lett. 426:47–56. 2018. View Article : Google Scholar : PubMed/NCBI | |
D'Oronzo S, Brown J and Coleman R: The role of biomarkers in the management of bone-homing malignancies. J Bone Oncol. 9:1–9. 2017. View Article : Google Scholar : PubMed/NCBI | |
Berruti A, Libè R, Laganà M, Ettaieb H, Sukkari MA, Bertherat J, Feelders RA, Grisanti S, Cartry J, Mazziotti G, et al: Morbidity and mortality of bone metastases in advanced adrenocortical carcinoma: A multicenter retrospective study. Eur J Endocrinol. 180:311–320. 2019. View Article : Google Scholar : PubMed/NCBI | |
Liao EY, Zhang ZL, Xia WB, Lin H, Cheng Q, Wang L, Hao YQ, Chen DC, Tang H, Peng YD, et al: Clinical characteristics associated with bone mineral density improvement after 1-year alendronate/vitamin d3 or calcitriol treatment: Exploratory results from a phase 3, randomized, controlled trial on postmenopausal osteoporotic women in China. Medicine (Baltimore). 97:e116942018. View Article : Google Scholar : PubMed/NCBI | |
Stopeck AT, Lipton A, Body JJ, Steger GG, Tonkin K, de Boer RH, Lichinitser M, Fujiwara Y, Yardley DA, Viniegra M, et al: Denosumab compared with zoledronic acid for the treatment of bone metastases in patients with advanced breast cancer: A randomized, double-blind study. J Clin Oncol. 28:5132–5139. 2010. View Article : Google Scholar : PubMed/NCBI | |
Body JJ, Lipton A, Gralow J, Steger GG, Gao G, Yeh H and Fizazi K: Effects of denosumab in patients with bone metastases with and without previous bisphosphonate exposure. J Bone Miner Res. 25:440–446. 2010. View Article : Google Scholar : PubMed/NCBI | |
Fizazi K, Lipton A, Mariette X, Body JJ, Rahim Y, Gralow JR, Gao G, Wu L, Sohn W and Jun S: Randomized phase II trial of denosumab in patients with bone metastases from prostate cancer, breast cancer, or other neoplasms after intravenous bisphosphonates. J Clin Oncol. 27:1564–1571. 2009. View Article : Google Scholar : PubMed/NCBI | |
Hirbe A, Morgan EA, Uluçkan O and Weilbaecher K: Skeletal complications of breast cancer therapies. Clin Cancer Res. 12:6309s–6314s. 2006. View Article : Google Scholar : PubMed/NCBI | |
Fizazi K, Carducci M, Smith M, Damião R, Brown J, Karsh L, Milecki P, Shore N, Rader M, Wang H, et al: Denosumab versus zoledronic acid for treatment of bone metastases in men with castration-resistant prostate cancer: A randomised, double-blind study. Lancet. 377:813–822. 2011. View Article : Google Scholar : PubMed/NCBI | |
Zeng Z, Li Y, Pan Y, Lan X, Song F, Sun J, Zhou K, Liu X, Ren X, Wang F, et al: Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis. Nat Commun. 9:53952018. View Article : Google Scholar : PubMed/NCBI | |
Sethi N and Kang Y: Unravelling the complexity of metastasis-molecular understanding and targeted therapies. Nat Rev Cancer. 11:735–748. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, et al: VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 438:820–827. 2005. View Article : Google Scholar : PubMed/NCBI | |
Psaila B and Lyden D: The metastatic niche: Adapting the foreign soil. Nat Rev Cancer. 9:285–293. 2009. View Article : Google Scholar : PubMed/NCBI | |
O'Brien K, Rani S, Corcoran C, Wallace R, Hughes L, Friel AM, McDonnell S, Crown J, Radomski MW and O'Driscoll L: Exosomes from triple-negative breast cancer cells can transfer phenotypic traits representing their cells of origin to secondary cells. Eur J Cancer. 49:1845–1859. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kahlert C and Kalluri R: Exosomes in tumor microenvironment influence cancer progression and metastasis. J Mol Med (Berl). 91:431–437. 2013. View Article : Google Scholar : PubMed/NCBI | |
Logozzi M, De Milito A, Lugini L, Borghi M, Calabrò L, Spada M, Perdicchio M, Marino ML, Federici C, Iessi E, et al: High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One. 4:e52192009. View Article : Google Scholar : PubMed/NCBI | |
Tavoosidana G, Ronquist G, Darmanis S, Yan J, Carlsson L, Wu D, Conze T, Ek P, Semjonow A, Eltze E, et al: Multiple recognition assay reveals prostasomes as promising plasma biomarkers for prostate cancer. Proc Natl Acad Sci USA. 108:8809–8814. 2011. View Article : Google Scholar : PubMed/NCBI | |
Steinbichler TB, Dudás J, Riechelmann H and Skvortsovab II: The role of exosomes in cancer metastasis. Semin Cancer Biol. 44:170–181. 2017. View Article : Google Scholar : PubMed/NCBI | |
Gao D, Nolan D, McDonnell K, Vahdat L, Benezra R, Altorki N and Mittal V: Bone marrow-derived endothelial progenitor cells contribute to the angiogenic switch in tumor growth and metastatic progression. Biochim Biophys Acta. 1796:33–40. 2009.PubMed/NCBI | |
Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A, Le QT and Giaccia AJ: Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell. 15:35–44. 2009. View Article : Google Scholar : PubMed/NCBI | |
Hiratsuka S, Watanabe A, Aburatani H and Maru Y: Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol. 8:1369–1375. 2006. View Article : Google Scholar : PubMed/NCBI | |
Han C, Zhou J, Liu B, Liang C, Pan X, Zhang Y, Zhang Y, Wang Y, Shao L, Zhu B, et al: Delivery of miR-675 by stem cell-derived exosomes encapsulated in silk fibroin hydrogel prevents aging-induced vascular dysfunction in mouse hindlimb. Mater Sci Eng C Mater Biol Appl. 99:322–332. 2019. View Article : Google Scholar : PubMed/NCBI | |
Wiklander OP, Nordin JZ, O'Loughlin A, Gustafsson Y, Corso G, Mäger I, Vader P, Lee Y, Sork H, Seow Y, et al: Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. J Extracell Vesicles. 4:263162015. View Article : Google Scholar : PubMed/NCBI | |
Peinado H, Alečković M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, García-Santos G, Ghajar C, et al: Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 18:883–891. 2012. View Article : Google Scholar : PubMed/NCBI | |
Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, Molina H, Kohsaka S, Di Giannatale A, Ceder S, et al: Tumour exosome integrins determine organotropic metastasis. Nature. 527:329–335. 2015. View Article : Google Scholar : PubMed/NCBI | |
Peinado H, Lavotshkin S and Lyden D: The secreted factors responsible for pre-metastatic niche formation: Old sayings and new thoughts. Semin Cancer Biol. 21:139–146. 2011. View Article : Google Scholar : PubMed/NCBI | |
Hameed A, Brady JJ, Dowling P, Clynes M and O'Gorman P: Bone disease in multiple myeloma: Pathophysiology and management. Cancer Growth Metastasis. 7:33–42. 2014. View Article : Google Scholar : PubMed/NCBI | |
Abdi J, Chen G and Chang H: Drug resistance in multiple myeloma: Latest findings and new concepts on molecular mechanisms. Oncotarget. 4:2186–2207. 2013. View Article : Google Scholar : PubMed/NCBI | |
Rossi M, Pitari MR, Amodio N, Di Martino MT, Conforti F, Leone E, Botta C, Paolino FM, Del Giudice T, Iuliano E, et al: miR-29b negatively regulates human osteoclastic cell differentiation and function: Implications for the treatment of multiple myeloma-related bone disease. J Cell Physiol. 228:1506–1515. 2013. View Article : Google Scholar : PubMed/NCBI | |
Heider U, Fleissner C, Zavrski I, Kaiser M, Hecht M, Jakob C and Sezer O: Bone markers in multiple myeloma. Eur J Cancer. 42:1544–1553. 2006. View Article : Google Scholar : PubMed/NCBI | |
Raimondi L, De Luca A, Amodio N, Manno M, Raccosta S, Taverna S, Bellavia D, Naselli F, Fontana S, Schillaci O, et al: Involvement of multiple myeloma cell-derived exosomes in osteoclast differentiation. Oncotarget. 6:13772–13789. 2015. View Article : Google Scholar : PubMed/NCBI | |
Garimella R, Washington L, Isaacson J, Vallejo J, Spence M, Tawfik O, Rowe P, Brotto M and Perez R: Extracellular membrane vesicles derived from 143B osteosarcoma cells contain pro-osteoclastogenic cargo: A novel communication mechanism in osteosarcoma bone microenvironment. Transl Oncol. 7:331–340. 2014. View Article : Google Scholar : PubMed/NCBI | |
Raimondo S, Saieva L, Vicario E, Pucci M, Toscani D, Manno M, Raccosta S, Giuliani N and Alessandro R: Multiple myeloma-derived exosomes are enriched of amphiregulin (AREG) and activate the epidermal growth factor pathway in the bone microenvironment leading to osteoclastogenesis. J Hematol Oncol. 12:22019. View Article : Google Scholar : PubMed/NCBI | |
Deng X, He G, Liu J, Luo F, Peng X, Tang S, Gao Z, Lin Q, Keller JM, Yang T and Keller ET: Recent advances in bone-targeted therapies of metastatic prostate cancer. Cancer Treat Rev. 40:730–738. 2014. View Article : Google Scholar : PubMed/NCBI | |
Karlsson T, Lundholm M, Widmark A and Persson E: Tumor cell-derived exosomes from the prostate cancer cell line TRAMP-C1 impair osteoclast formation and differentiation. PLoS One. 11:e01662842016. View Article : Google Scholar : PubMed/NCBI | |
Inder KL, Ruelcke JE, Petelin L, Moon H, Choi E, Rae J, Blumenthal A, Hutmacher D, Saunders NA, Stow JL, et al: Cavin-1/PTRF alters prostate cancer cell-derived extracellular vesicle content and internalization to attenuate extracellular vesicle-mediated osteoclastogenesis and osteoblast proliferation. J Extracell Vesicles. 3:2014. View Article : Google Scholar : PubMed/NCBI | |
Shiozawa Y, Pedersen EA, Havens AM, Jung Y, Mishra A, Joseph J, Kim JK, Patel LR, Ying C, Ziegler AM, et al: Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest. 121:1298–1312. 2011. View Article : Google Scholar : PubMed/NCBI | |
Morrissey C, Lai JS, Brown LG, Wang YC, Roudier MP, Coleman IM, Gulati R, Vakar-Lopez F, True LD, Corey E, et al: The expression of osteoclastogenesis-associated factors and osteoblast response to osteolytic prostate cancer cells. Prostate. 70:412–424. 2010.PubMed/NCBI | |
Itoh T, Ito Y, Ohtsuki Y, Ando M, Tsukamasa Y, Yamada N, Naoe T and Akao Y: Microvesicles released from hormone-refractory prostate cancer cells facilitate mouse pre-osteoblast differentiation. J Mol Histol. 43:509–515. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ye Y, Li SL, Ma YY, Diao YJ, Yang L, Su MQ, Li Z, Ji Y, Wang J, Lei L, et al: Exosomal miR-141-3p regulates osteoblast activity to promote the osteoblastic metastasis of prostate cancer. Oncotarget. 8:94834–94849. 2017. View Article : Google Scholar : PubMed/NCBI | |
Hashimoto K, Ochi H, Sunamura S, Kosaka N, Mabuchi Y, Fukuda T, Yao K, Kanda H, Ae K, Okawa A, et al: Cancer-secreted hsa-miR-940 induces an osteoblastic phenotype in the bone metastatic microenvironment via targeting ARHGAP1 and FAM134A. Proc Natl Acad Sci USA. 115:2204–2209. 2018. View Article : Google Scholar : PubMed/NCBI | |
Morhayim J, van de Peppel J, Demmers JA, Kocer G, Nigg AL, van Driel M, Chiba H and van Leeuwen JP: Proteomic signatures of extracellular vesicles secreted by nonmineralizing and mineralizing human osteoblasts and stimulation of tumor cell growth. FASEB J. 29:274–285. 2015. View Article : Google Scholar : PubMed/NCBI | |
Peng X, Guo W, Ren T, Lou Z, Lu X, Zhang S, Lu Q and Sun Y: Differential expression of the RANKL/RANK/OPG system is associated with bone metastasis in human non-small cell lung cancer. PLoS One. 8:e583612013. View Article : Google Scholar : PubMed/NCBI | |
Taverna S, Pucci M, Giallombardo M, Di Bella MA, Santarpia M, Reclusa P, Gil-Bazo I, Rolfo C and Alessandro R: Amphiregulin contained in NSCLC-exosomes induces osteoclast differentiation through the activation of EGFR pathway. Sci Rep. 7:31702017. View Article : Google Scholar : PubMed/NCBI | |
Valencia K, Luis-Ravelo D, Bovy N, Antón I, Martínez-Canarias S, Zandueta C, Ormazábal C, Struman I, Tabruyn S, Rebmann V, et al: miRNA cargo within exosome like vesicle transfer influences metastatic bone colonization. Mol Oncol. 8:689–703. 2014. View Article : Google Scholar : PubMed/NCBI | |
Kumar B, Garcia M, Weng L, Jung X, Murakami JL, Hu X, McDonald T, Lin A, Kumar AR, DiGiusto DL, et al: Acute myeloid leukemia transforms the bone marrow niche into a leukemia-permissive microenvironment through exosome secretion. Leukemia. 32:575–587. 2018. View Article : Google Scholar : PubMed/NCBI | |
Guise TA: Breast cancer bone metastases: It's all about the neighborhood. Cell. 154:957–959. 2013. View Article : Google Scholar : PubMed/NCBI |