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Extracellular Vesicle-Mediated Bone Remodeling and Bone Metastasis: Implications in Prostate Cancer

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New Frontiers: Extracellular Vesicles

Part of the book series: Subcellular Biochemistry ((SCBI,volume 97))

Abstract

Bone metastasis is the tendency of certain primary tumors to spawn and dictate secondary neoplasia in the bone. The process of bone metastasis is regulated by the dynamic crosstalk between metastatic cancer cells, cellular components of the bone marrow microenvironment (osteoblasts, osteoclasts, and osteocytes), and the bone matrix. The feed-forward loop mechanisms governs the co-option of homeostatic bone remodeling by cancer cells in bone. Recent developments have highlighted the discovery of extracellular vesicles (EVs) and their diverse roles in distant outgrowths. Several studies have implicated EV-mediated interactions between cancer cells and the bone microenvironment in synergistically promoting pathological skeletal metabolism in the metastatic site. Nevertheless, the potential role that EVs serve in arbitrating intricate sequences of coordinated events within the bone microenvironment remains an emerging field. In this chapter, we review the role of cellular participants and molecular mechanisms in regulating normal bone physiology and explore the progress of current research into bone-derived EVs in directly triggering and coordinating the processes of physiological bone remodeling. In view of the emerging role of EVs in interorgan crosstalk, this review also highlights the multiple systemic pathophysiological processes orchestrated by the EVs to direct organotropism in bone in prostate cancer. Given the deleterious consequences of bone metastasis and its clinical importance, in-depth knowledge of the multifarious role of EVs in distant organ metastasis is expected to open new possibilities for prognostic evaluation and therapeutic intervention for advanced bone metastatic prostate cancer.

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References

  • Adrianzen Herrera DA, Goldberg-Stein S, Sankin A, Sarungbam J, Sharma J, Gartrell BA (2018) Synchronous bone metastasis from multiple myeloma and prostate adenocarcinoma as initial presentation of coexistent malignancies. Front Oncol 8:137

    Article  PubMed  PubMed Central  Google Scholar 

  • Agheli A, Patsiornik Y, Chen Y, Chaudhry MR, Gerber H, Wang JC (2009) Prostate carcinoma, presenting with a solitary osteolytic bone lesion to the right hip. Radiol Case Rep 4(4):288

    Article  PubMed  Google Scholar 

  • Allen BR, Burr DB (2014) Bone Modeling and Remodeling. In: Allen BR, Burr DB (eds) Basic and applied bone biology. Academic, USA, pp 75–90

    Chapter  Google Scholar 

  • Alsulaiman M, Bais MV, Trackman PC (2016) Lysyl oxidase propeptide stimulates osteoblast and osteoclast differentiation and enhances PC3 and DU145 prostate cancer cell effects on bone in vivo. J Cell Commun Signal 10(1):17–31

    Article  PubMed  Google Scholar 

  • Ammann P, Rizzoli R, Bonjour JP, Bourrin S, Meyer JM, Vassalli P et al (1997) Transgenic mice expressing soluble tumor necrosis factor-receptor are protected against bone loss caused by estrogen deficiency. J Clin Invest 99(7):1699–1703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen TL, Abdelgawad ME, Kristensen HB, Hauge EM, Rolighed L, Bollerslev J et al (2013) Understanding coupling between bone Resorption and formation: are reversal cells the missing link? Am J Pathol 183(1):235–246

    Article  CAS  PubMed  Google Scholar 

  • Andersen TL, del Carmen Ovejero M, Kirkegaard T, Lenhard T, Foged NT, Delaisse JM (2004) A scrutiny of matrix metalloproteinases in osteoclasts: evidence for heterogeneity and for the presence of MMPs synthesized by other cells. Bone 35(5):1107–1119

    Article  CAS  PubMed  Google Scholar 

  • Ang J, Lijovic M, Ashman LK, Kan K, Frauman AG (2004) CD151 protein expression predicts the clinical outcome of low-grade primary prostate cancer better than histologic grading: a new prognostic indicator? Cancer epidemiology biomarkers. Prevention 13(11):1717

    CAS  Google Scholar 

  • Angelucci A, D'Ascenzo S, Festuccia C, Gravina GL, Bologna M, Dolo V et al (2000) Vesicle-associated urokinase plasminogen activator promotes invasion in prostate cancer cell lines. Clin Exp Metastasis 18(2):163–170

    Article  CAS  PubMed  Google Scholar 

  • Ansari MS, Nabi G, Aron M (2003) Solitary radial head metastasis with wrist drop: a rare presentation of metastatic prostate carcinoma. Urol Int 70(1):77–79

    Article  CAS  PubMed  Google Scholar 

  • Antonyak MA, Li B, Boroughs LK, Johnson JL, Druso JE, Bryant KL et al (2011) Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc Natl Acad Sci U S A 108(12):4852–4857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arai F, Miyamoto T, Ohneda O, Inada T, Sudo T, Brasel K et al (1999) Commitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor kappaB (RANK) receptors. J Exp Med 190(12):1741–1754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Araya HF, Sepulveda H, Lizama CO, Vega OA, Jerez S, Briceño PF et al (2018) Expression of the ectodomain-releasing protease ADAM17 is directly regulated by the osteosarcoma and bone-related transcription factor RUNX2. J Cell Biochem 119(10):8204–8219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azmi AS, Bao B, Sarkar FH (2013) Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev 32(3-4):623–642

    Article  CAS  PubMed  Google Scholar 

  • Balani DH, Ono N, Kronenberg HM (2017) Parathyroid hormone regulates fates of murine osteoblast precursors in vivo. J Clin Invest 127:3327–3338

    Article  PubMed  PubMed Central  Google Scholar 

  • Baniwal SK, Khalid O, Gabet Y, Shah RR, Purcell DJ, Mav D et al (2010) Runx2 transcriptome of prostate cancer cells: insights into invasiveness and bone metastasis. Mol Cancer 9:258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baron R, Kneissel M (2013) WNT signaling in bone homeostasis and disease: from human mutations to treatments. Nat Med 19(2):179–192

    Article  CAS  PubMed  Google Scholar 

  • Beach A, Zhang HG, Ratajczak MZ, Kakar SS (2014) Exosomes: an overview of biogenesis, composition and role in ovarian cancer. J Ovarian Res 7:14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H, Lyden D (2016) Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell 30(6):836–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bellido T, Ali AA, Gubrij I, Plotkin LI, Fu Q, O'Brien CA et al (2005) Chronic elevation of parathyroid hormone in mice reduces expression of sclerostin by osteocytes: a novel mechanism for hormonal control of osteoblastogenesis. Endocrinology 146(11):4577–4583

    Article  CAS  PubMed  Google Scholar 

  • Bellido T, Saini V, Pajevic PD (2013) Effects of PTH on osteocyte function. Bone 54(2):250–257

    Article  CAS  PubMed  Google Scholar 

  • Ben-awadh AN, Delgado-Calle J, Tu X, Kuhlenschmidt K, Allen MR, Plotkin LI et al (2014) Parathyroid hormone receptor signaling induces bone resorption in the adult skeleton by directly regulating the RANKL gene in osteocytes. Endocrinology 155(8):2797–2809

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bhattacharyya RS, Husbeck B, Feldman D, Knox SJ (2008) Selenite treatment inhibits LAPC-4 tumor growth and prostate-specific antigen secretion in a xenograft model of human prostate cancer. Int J Radiat Oncol Biol Phys 72(3):935–940

    Article  CAS  PubMed  Google Scholar 

  • Bhushan R, Grünhagen J, Becker J, Robinson PN, Ott CE, Knaus P (2013) miR-181a promotes osteoblastic differentiation through repression of TGF-β signaling molecules. Int J Biochem Cell Biol 45(3):696–705

    Article  CAS  PubMed  Google Scholar 

  • Bidwell JP, Yang J, Robling AG (2008) Is HMGB1 an osteocyte alarmin? J Cell Biochem 103(6):1671–1680

    Article  CAS  PubMed  Google Scholar 

  • Bonci D, De Maria R (2015) miR-15/miR-16 loss, miR-21 upregulation, or deregulation of their target genes predicts poor prognosis in prostate cancer patients. Mol Cell Oncol 3(4):e1109744

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bonewald LF (2011) The amazing osteocyte. J Bone Miner Res 26(2):229–238

    Article  CAS  PubMed  Google Scholar 

  • Boyce BF, Xing L (2008) Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch Biochem Biophys 473(2):139–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brubaker KD, Vessella RL, Brown LG, Corey E (2003) Prostate cancer expression of runt-domain transcription factor Runx2, a key regulator of osteoblast differentiation and function. Prostate 56(1):13–22

    Article  CAS  PubMed  Google Scholar 

  • Brzozowski JS, Bond DR, Jankowski H, Goldie BJ, Burchell R, Naudin C et al (2018) Extracellular vesicles with altered tetraspanin CD9 and CD151 levels confer increased prostate cell motility and invasion. Sci Rep 8(1):8822

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bussard KM, Gay CV, Mastro AM (2008) The bone microenvironment in metastasis; what is special about bone? Cancer Metastasis Rev 27(1):41–55

    Article  PubMed  Google Scholar 

  • Camussi G, Deregibus MC, Bruno S, Grange C, Fonsato V, Tetta C (2011) Exosome/microvesicle-mediated epigenetic reprogramming of cells. Am J Cancer Res 1(1):98–110

    PubMed  Google Scholar 

  • Canalis E (2013) Skeletal growth factors. In: Marcus R, Feldman D, Dempster DW, Luckey M, Cauley JA (eds) Osteoporosis, 4th edn. Academic, San Diego, USA, pp 391–410

    Chapter  Google Scholar 

  • Cappariello A, Loftus A, Muraca M, Maurizi A, Rucci N, Teti A (2018) Osteoblast-derived extracellular vesicles are biological tools for the delivery of active molecules to bone. J Bone Miner Res 33(3):517–533

    Article  CAS  PubMed  Google Scholar 

  • Cashman KD, Ginty F (2003) Bone. In: Caballero B, Finglas P, Toldra F (eds) Encyclopedia of food sciences and nutrition, 2nd edn. Academic, USA, pp 557–565

    Chapter  Google Scholar 

  • Cenci S, Weitzmann MN, Roggia C, Namba N, Novack D, Woodring J et al (2000) Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest 106(10):1229–1237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chambers TJ, Chambers JC, Symonds J, Darby JA (1986) The effect of human calcitonin on the cytoplasmic spreading of rat osteoclasts*. J Clin Endocrinol Metabol 63(5):1080–1085

    Article  CAS  Google Scholar 

  • Chambers TJ, Magnus CJ (1982) Calcitonin alters behaviour of isolated osteoclasts. J Pathol 136(1):27–39

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Cheng P, Xie H, Zhou HD, Wu XP, Liao EY et al (2014) MiR-503 regulates osteoclastogenesis via targeting RANK. J Bone Miner Res 29(2):338–347

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Hoffmann AD, Liu H, Liu X (2018) Organotropism: new insights into molecular mechanisms of breast cancer metastasis. npj Precision Oncology 2(1):4

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Jacamo R, Shi YX, Wang RY, Battula VL, Konoplev S et al (2012) Human extramedullary bone marrow in mice: a novel in vivo model of genetically controlled hematopoietic microenvironment. Blood 119(21):4971–4980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng P, Chen C, He HB, Hu R, Zhou HD, Xie H et al (2013) miR-148a regulates osteoclastogenesis by targeting V-maf musculoaponeurotic fibrosarcoma oncogene homolog B. J Bone Miner Res 28(5):1180–1190

    Article  CAS  PubMed  Google Scholar 

  • Cheng X, Kinosaki M, Murali R, Greene MI (2003) The TNF receptor superfamily. Immunol Res 27(2):287–294

    Article  CAS  PubMed  Google Scholar 

  • Chu K, Cheng CJ, Ye X, Lee YC, Zurita AJ, Chen DT et al (2008) Cadherin-11 promotes the metastasis of prostate cancer cells to bone. Mol Cancer Res 6(8):1259–1267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke NW, McClure J, George NJ (1991) Morphometric evidence for bone resorption and replacement in prostate cancer. Br J Urol 68(1):74–80

    Article  CAS  PubMed  Google Scholar 

  • Clevers H, Nusse R (2012) Wnt/β-catenin signaling and disease. Cell 149(6):1192–1205

    Article  CAS  PubMed  Google Scholar 

  • Clines GA, Mohammad KS, Bao Y, Stephens OW, Suva LJ, Shaughnessy JD Jr et al (2007) Dickkopf homolog 1 mediates endothelin-1-stimulated new bone formation. Mol Endocrinol 21(2):486–498

    Article  CAS  PubMed  Google Scholar 

  • Cook LM, Shay G, Araujo A, Lynch CC (2014) Integrating new discoveries into the "vicious cycle" paradigm of prostate to bone metastases. Cancer Metastasis Rev 33(2-3):511–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cox TR, Rumney RMH, Schoof EM, Perryman L, Høye AM, Agrawal A et al (2015) The hypoxic cancer secretome induces pre-metastatic bone lesions through lysyl oxidase. Nature 522(7554):106–110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croucher PI, Parker BS, Corcoran N, Rogers MJ (2015) Bone turnover markers and prostate cancer: not just a measure of bone disease? Eur Urol 68(1):51–52

    Article  PubMed  Google Scholar 

  • Cui Y, Luan J, Li H, Zhou X, Han J (2016) Exosomes derived from mineralizing osteoblasts promote ST2 cell osteogenic differentiation by alteration of microRNA expression. FEBS Lett 590(1):185–192

    Article  CAS  PubMed  Google Scholar 

  • Dailey L, Ambrosetti D, Mansukhani A, Basilico C (2005) Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev 16(2):233–247

    Article  CAS  PubMed  Google Scholar 

  • Dallas SL, Prideaux M, Bonewald LF (2013) The osteocyte: an endocrine cell ... And more. Endocr Rev 34(5):658–690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies OG, Cox SC, Williams RL, Tsaroucha D, Dorrepaal RM, Lewis MP et al (2017) Annexin-enriched osteoblast-derived vesicles act as an extracellular site of mineral nucleation within developing stem cell cultures. Sci Rep 7(1):12639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deftos LJ (2000) Prostate carcinoma: production of bioactive factors. Cancer 88:3002–3008

    Article  CAS  PubMed  Google Scholar 

  • Delaisse J-M (2014) The reversal phase of the bone-remodeling cycle: cellular prerequisites for coupling resorption and formation. Bonekey Rep 3:561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng L, Wang Y, Peng Y, Wu Y, Ding Y, Jiang Y et al (2015) Osteoblast-derived microvesicles: a novel mechanism for communication between osteoblasts and osteoclasts. Bone 79:37–42

    Article  CAS  PubMed  Google Scholar 

  • Detchokul S, Williams ED, Parker MW, Frauman AG (2014) Tetraspanins as regulators of the tumour microenvironment: implications for metastasis and therapeutic strategies. Br J Pharmacol 171(24):5462–5490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egea V, Zahler S, Rieth N et al (2012) Tissue inhibitor of metalloproteinase-1 (TIMP-1) regulates mesenchymal stem cells through let-7f microRNA and Wnt/β-catenin signaling. Proc Natl Acad Sci U S A 109(6):E309–E316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2(3):161–174

    Article  CAS  PubMed  Google Scholar 

  • Eriksen EF (2010) Cellular mechanisms of bone remodeling. Rev Endocr Metab Disord 11(4):219–227

    Article  PubMed  PubMed Central  Google Scholar 

  • Esposito M, Guise T, Kang Y (2018) The biology of bone metastasis. Cold Spring Harb Perspect Med 8(6)

    Google Scholar 

  • Festuccia C, Giunciuglio D, Guerra F, Villanova I, Angelucci A, Manduca P et al (1999) Osteoblasts modulate secretion of urokinase-type plasminogen activator (uPA) and matrix metalloproteinase-9 (MMP-9) in human prostate cancer cells promoting migration and matrigel invasion. Oncol Res 11(1):17–31

    CAS  PubMed  Google Scholar 

  • Festuccia C, Angelucci A, Gravina GL, Villanova I, Teti A, Albini A et al (2000) Osteoblast-derived TGF-beta1 modulates matrix degrading protease expression and activity in prostate cancer cells. Int J Cancer 85(3):407–415

    Article  CAS  PubMed  Google Scholar 

  • Fizazi K, Massard C, Smith M, Rader M, Brown J, Milecki P et al (2015) Bone-related parameters are the Main prognostic factors for Overall survival in men with bone metastases from castration-resistant prostate cancer. Eur Urol 68(1):42–50

    Article  PubMed  Google Scholar 

  • Fretz JA, Zella LA, Kim S, Shevde NK, Pike JW (2007) 1,25-Dihydroxyvitamin D3 induces expression of the Wnt signaling co-regulator LRP5 via regulatory elements located significantly downstream of the gene's transcriptional start site. J Steroid Biochem Mol Biol 103(3-5):440–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frost HM (2001) From Wolff's law to the Utah paradigm: insights about bone physiology and its clinical applications. Anat Rec 262(4):398–419

    Article  CAS  PubMed  Google Scholar 

  • Fuller K, Wong B, Fox S, Choi Y, Chambers TJ (1998) TRANCE is necessary and sufficient for osteoblast-mediated activation of bone resorption in osteoclasts. J Exp Med 188(5):997–1001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gandaglia G, Karakiewicz PI, Briganti A, Passoni NM, Schiffmann J, Trudeau V et al (2015) Impact of the site of metastases on survival in patients with metastatic prostate cancer. Eur Urol 68(2):325–334

    Article  PubMed  Google Scholar 

  • Ge M, Ke R, Cai T, Yang J, Mu X (2015) Identification and proteomic analysis of osteoblast-derived exosomes. Biochem Biophys Res Commun 467(1):27–32

    Google Scholar 

  • Ghajar CM, Peinado H, Mori H, Matei IR, Evason KJ, Brazier H et al (2013) The perivascular niche regulates breast tumour dormancy. Nat Cell Biol 15(7):807–817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glass DA, Bialek P, Ahn JD, Starbuck M, Patel MS, Clevers H et al (2005) Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell 8(5):751–764

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Begne M, Lu B, Han X, Hagen FK, Hand AR, Melvin JE et al (2009) Proteomic analysis of human parotid gland exosomes by multidimensional protein identification technology (MudPIT). J Proteome Res 8(3):1304–1314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grau-Bove X, Ruiz-Trillo I, Rodriguez-Pascual F (2015) Origin and evolution of lysyl oxidases. Sci Rep 5:10568

    Article  PubMed  PubMed Central  Google Scholar 

  • Guise TA, Yin JJ, Taylor SD, Kumagai Y, Dallas M, Boyce BF et al (1996) Evidence for a causal role of parathyroid hormone-related protein in the pathogenesis of human breast cancer-mediated osteolysis. J Clin Invest 98(7):1544–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gururajan M, Josson S, Chu GC, Lu CL, Lu YT, Haga CL et al (2014) miR-154* and miR-379 in the DLK1-DIO3 microRNA mega-cluster regulate epithelial to mesenchymal transition and bone metastasis of prostate cancer. Clin Cancer Res 20(24):6559–6569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harmey D, Hessle L, Narisawa S, Johnson KA, Terkeltaub R, Millan JL (2004) Concerted regulation of inorganic pyrophosphate and osteopontin by akp2, enpp1, and ank: an integrated model of the pathogenesis of mineralization disorders. Am J Pathol 164(4):1199–1209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hashimoto K, Ochi H, Sunamura S, Kosaka N, Mabuchi Y, Fukuda T et al (2018) Cancer-secreted hsa-miR-940 induces an osteoblastic phenotype in the bone metastatic microenvironment via targeting ARHGAP1 and FAM134A. Proc Natl Acad Sci U S A 115(9):2204–2209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hassan MQ, Maeda Y, Taipaleenmaki H, Zhang W, Jafferji M, Gordon JA et al (2012) miR-218 directs a Wnt signaling circuit to promote differentiation of osteoblasts and osteomimicry of metastatic cancer cells. J Biol Chem 287(50):42084–42092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hauge EM, Qvesel D, Eriksen EF, Mosekilde L, Melsen F (2001) Cancellous bone remodeling occurs in specialized compartments lined by cells expressing osteoblastic markers. J Bone Miner Res 16(9):1575–1582

    Article  CAS  PubMed  Google Scholar 

  • Haussler MR, Whitfield GK, Kaneko I, Haussler CA, Hsieh D, Hsieh J-C et al (2013) Molecular mechanisms of vitamin D action. Calcif Tissue Int 92(2):77–98

    Article  CAS  PubMed  Google Scholar 

  • Henriksen K, Bollerslev J, Everts V, Karsdal MA (2011) Osteoclast activity and subtypes as a function of physiology and pathology—implications for future treatments of osteoporosis. Endocr Rev 32(1):31–63

    Article  CAS  PubMed  Google Scholar 

  • Hirvonen MJ, Mulari MTK, Büki KG, Vihko P, Härkönen PL, Väänänen HK (2012) Rab13 is upregulated during osteoclast differentiation and associates with small vesicles revealing polarized distribution in resorbing cells. J Histochem Cytochem 60(7):537–549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hofbauer LC, Khosla S, Dunstan CR (1999) Estrogen stimulates gene expression and protein production of osteoprotegerin in human osteoblastic cells. Endocrinology 140(9):4367–4370

    Article  CAS  PubMed  Google Scholar 

  • Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Boyle WJ, Riggs BL (2000) The roles of osteoprotegerin and osteoprotegerin ligand in the paracrine regulation of bone resorption. J Bone Miner Res 15(1):2–12

    Article  CAS  PubMed  Google Scholar 

  • Horwood NJ, Elliott J, Martin TJ, Gillespie MT (1998) Osteotropic agents regulate the expression of osteoclast differentiation factor and osteoprotegerin in osteoblastic stromal cells. Endocrinology 139:4743–4746

    Article  CAS  PubMed  Google Scholar 

  • Hsiao CY, Chen TH, Chu TH, Ting YN, Tsai PJ, Shyu JF (2020) Calcitonin induces bone formation by increasing expression of Wnt10b in osteoclasts in ovariectomy-induced osteoporotic rats. Front Endocrinol (Lausanne) 11:613

    Article  Google Scholar 

  • Huynh N, VonMoss L, Smith D, Rahman I, Felemban MF, Zuo J et al (2016) Characterization of regulatory extracellular vesicles from osteoclasts. J Dent Res 95(6):673–679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ibrahim T, Flamini E, Mercatali L, Sacanna E, Serra P, Amadori D (2010) Pathogenesis of osteoblastic bone metastases from prostate cancer. Cancer 116(6):1406–1418

    Article  CAS  PubMed  Google Scholar 

  • Ikeda I, Miura T, Kondo I (1996) Pyridinium cross-links as urinary markers of bone metastasis in patients with prostate cancer. Br J Urol 77(1):102–106

    Article  CAS  PubMed  Google Scholar 

  • Inder KL, Ruelcke JE, Petelin L, Moon H, Choi E, Rae J et al (2014) Cavin-1/PTRF alters prostate cancer cell-derived extracellular vesicle content and internalization to attenuate extracellular vesicle-mediated osteoclastogenesis and osteoblast proliferation. Journal of extracellular vesicles 3

    Google Scholar 

  • Irie N, Takada Y, Watanabe Y, Matsuzaki Y, Naruse C, Asano M et al (2009) Bidirectional signaling through ephrinA2-EphA2 enhances osteoclastogenesis and suppresses osteoblastogenesis. J Biol Chem 284(21):14637–14644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itoh T, Ito Y, Ohtsuki Y, Ando M, Tsukamasa Y, Yamada N et al (2012) Microvesicles released from hormone-refractory prostate cancer cells facilitate mouse pre-osteoblast differentiation. J Mol Histol 43(5):509–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jadaan DY, Jadaan MM, McCabe JP (2015) Cellular plasticity in prostate cancer bone metastasis. Prostate Cancer 2015:651580

    Article  PubMed  PubMed Central  Google Scholar 

  • Jee WS, Mori S, Li XJ, Chan S (1990) Prostaglandin E2 enhances cortical bone mass and activates intracortical bone remodeling in intact and ovariectomized female rats. Bone 11(4):253–266

    Article  CAS  PubMed  Google Scholar 

  • Jing D, Baik AD, Lu XL, Zhou B, Lai X, Wang L et al (2014) In situ intracellular calcium oscillations in osteocytes in intact mouse long bones under dynamic mechanical loading. FASEB J 28(4):1582–1592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Josson S, Gururajan M, Hu P, Shao C, Chu GY, Zhau HE et al (2014) miR-409-3p/−5p promotes tumorigenesis, epithelial-to-mesenchymal transition, and bone metastasis of human prostate cancer. Clin Cancer Res 20(17):4636–4646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung Y, Shiozawa Y, Wang J, McGregor N, Dai J, Park SI et al (2012) Prevalence of prostate cancer metastases after intravenous inoculation provides clues into the molecular basis of dormancy in the bone marrow microenvironment. Neoplasia 14(5):429–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang Y, Pantel K (2013) Tumor cell dissemination: emerging biological insights from animal models and cancer patients. Cancer Cell 23(5):573–581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karlsson T, Lundholm M, Widmark A, Persson E (2016) Tumor cell-derived Exosomes from the prostate cancer cell line TRAMP-C1 impair osteoclast formation and differentiation. PLoS One 11(11):e0166284

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Karsenty G, Kronenberg HM, Settembre C (2009) Genetic control of bone formation. Annu Rev Cell Dev Biol 25:629–648

    Article  CAS  PubMed  Google Scholar 

  • Karsenty G, Oury F (2014) Regulation of male fertility by the bone-derived hormone osteocalcin. Mol Cell Endocrinol 382(1):521–526

    Article  CAS  PubMed  Google Scholar 

  • Kato H, Ochiai-Shino H, Onodera S, Saito A, Shibahara T, Azuma T (2015) Promoting effect of 1,25(OH)2 vitamin D3 in osteogenic differentiation from induced pluripotent stem cells to osteocyte-like cells. Open Biol 5(2):140201

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kawaguchi J, Kii I, Sugiyama Y, Takeshita S, Kudo A (2001) The transition of cadherin expression in osteoblast differentiation from mesenchymal cells: consistent expression of cadherin-11 in osteoblast lineage. J Bone Miner Res 16(2):260–269

    Article  CAS  PubMed  Google Scholar 

  • Ke K, Sul OJ, Rajasekaran M, Choi HS (2015) MicroRNA-183 increases osteoclastogenesis by repressing heme oxygenase-1. Bone 81:237–246

    Article  CAS  PubMed  Google Scholar 

  • Keller H, Kneissel M (2005) SOST is a target gene for PTH in bone. Bone 37(2):148–158

    Article  CAS  PubMed  Google Scholar 

  • Kenkre JS, Bassett JHD (2018) The bone remodelling cycle. Ann Clin Biochem 55(3):308–327

    Article  CAS  PubMed  Google Scholar 

  • Khosla S, Oursler MJ, Monroe DG (2012) Estrogen and the skeleton. Trends Endocrinol Metab 23(11):576–581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimble RB, Srivastava S, Ross FP, Matayoshi A, Pacifici R (1996) Estrogen deficiency increases the ability of stromal cells to support murine Osteoclastogenesis via an interleukin-1and tumor necrosis factor-mediated stimulation of macrophage Colony-stimulating factor production. J Biol Chem 271(46):28890–28897

    Article  CAS  PubMed  Google Scholar 

  • Kingsley LA, Fournier PG, Chirgwin JM, Guise TA (2007) Molecular biology of bone metastasis. Mol Cancer Ther 6(10):2609–2617

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi A, Okuda H, Xing F, Pandey PR, Watabe M, Hirota S et al (2011) Bone morphogenetic protein 7 in dormancy and metastasis of prostate cancer stem-like cells in bone. J Exp Med 208(13):2641–2655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kokabu S, Rosen V (2017) BMP3 expression by osteoblast lineage cells is regulated by canonical Wnt signaling. FEBS Open Bio 8(2):168–176

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Komori T (2010) Regulation of bone development and extracellular matrix protein genes by RUNX2. Cell Tissue Res 339(1):189–195

    Article  CAS  PubMed  Google Scholar 

  • Kopp HG, Avecilla ST, Hooper AT, Rafii S (2005) The bone marrow vascular niche: home of HSC differentiation and mobilization. Physiology (Bethesda) 20:349–356

    CAS  Google Scholar 

  • Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S et al (1999) IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103(9):1345–1352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kousteni S, Bellido T, Plotkin LI et al (2001) Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104(5):719–730

    CAS  PubMed  Google Scholar 

  • Kousteni S, Han L, Chen J-R, Almeida M, Plotkin LI, Bellido T et al (2003) Kinase-mediated regulation of common transcription factors accounts for the bone-protective effects of sex steroids. J Clin Invest 111(11):1651–1664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kristensen HB, Andersen TL, Marcussen N, Rolighed L, Delaisse JM (2014) Osteoblast recruitment routes in human cancellous bone remodeling. Am J Pathol 184(3):778–789

    Article  CAS  PubMed  Google Scholar 

  • Kurata K, Heino TJ, Higaki H, Vaananen HK (2006) Bone marrow cell differentiation induced by mechanically damaged osteocytes in 3D gel-embedded culture. J Bone Miner Res 21(4):616–625

    Article  PubMed  Google Scholar 

  • Lacey DL, Timms E, Tan HL et al (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93(2):165–176

    Article  CAS  PubMed  Google Scholar 

  • Lane NE, Yao W, Balooch M, Nalla RK, Balooch G, Habelitz S et al (2006) Glucocorticoid-treated mice have localized changes in trabecular bone material properties and osteocyte lacunar size that are not observed in placebo-treated or estrogen-deficient mice. J Bone Miner Res Off J Am Soc Bone Miner Res 21(3):466–476

    Article  CAS  Google Scholar 

  • Langdahl B, Ferrari S, Dempster DW (2016) Bone modeling and remodeling: potential as therapeutic targets for the treatment of osteoporosis. Ther Adv Musculoskelet Dis 8(6):225–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanske B, Densmore MJ, Erben RG (2014) Vitamin D endocrine system and osteocytes. Bonekey Rep 3:494

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lara-Castillo N, Kim-Weroha NA, Kamel MA, Javaheri B, Ellies DL, Krumlauf RE et al (2015) In vivo mechanical loading rapidly activates β-catenin signaling in osteocytes through a prostaglandin mediated mechanism. Bone 76:58–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lazaro-Ibanez E, Neuvonen M, Takatalo M, Thanigai Arasu U, Capasso C, Cerullo V et al (2017) Metastatic state of parent cells influences the uptake and functionality of prostate cancer cell-derived extracellular vesicles. J Extracell Vesicles 6(1):1354645

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee C, Whang YM, Campbell P, Mulcrone PL, Elefteriou F, Cho SW et al (2018) Dual targeting c-met and VEGFR2 in osteoblasts suppresses growth and osteolysis of prostate cancer bone metastasis. Cancer Lett 414:205–213

    Article  CAS  PubMed  Google Scholar 

  • Lerner UH, Ohlsson C (2015) The WNT system: background and its role in bone. J Intern Med 277(6):630–649

    Article  CAS  PubMed  Google Scholar 

  • Levanon D, Negreanu V, Bernstein Y, Bar-Am I, Avivi L, Groner Y (1994) AML1, AML2, and AML3, the human members of the runt domain gene-family: cDNA structure, expression, and chromosomal localization. Genomics 23(2):425–432

    Article  CAS  PubMed  Google Scholar 

  • Li SL, An N, Liu B et al (2019) Exosomes from LNCaP cells promote osteoblast activity through miR-375 transfer. Oncol Lett 17:4463–4473

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li D, Liu J, Guo B, Liang C, Dang L, Lu C et al (2016) Osteoclast-derived exosomal miR-214-3p inhibits osteoblastic bone formation. Nat Commun 7:10872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Qin L, Bergenstock M, Bevelock LM, Novack DV, Partridge NC (2007) Parathyroid hormone stimulates osteoblastic expression of MCP-1 to recruit and increase the fusion of pre/osteoclasts. J Biol Chem 282:33098–33106

    Article  CAS  PubMed  Google Scholar 

  • Li X, Loberg R, Liao J, Ying C, Snyder LA, Pienta KJ et al (2009) A destructive cascade mediated by CCL2 facilitates prostate cancer growth in bone. Cancer Res 69(4):1685–1692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Toraldo G, Li A, Yang X, Zhang H, Qian WP et al (2007) B cells and T cells are critical for the preservation of bone homeostasis and attainment of peak bone mass in vivo. Blood 109(9):3839–3848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Zhang Y, Kang H, Liu W, Liu P, Zhang J et al (2005) Sclerostin binds to LRP5/6 and antagonizes canonical Wnt signaling. J Biol Chem 280(20):19883–19887

    Article  CAS  PubMed  Google Scholar 

  • Li J, Zhang H, Yang C, Li Y, Dai Z (2016) An overview of osteocalcin progress. J Bone Miner Metab 34(4):367–379

    Article  CAS  PubMed  Google Scholar 

  • Liao J, Li X, Koh AJ, Berry JE, Thudi N, Rosol TJ et al (2008) Tumor expressed PTHrP facilitates prostate cancer-induced osteoblastic lesions. Int J Cancer 123(10):2267–2278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin C, Jiang X, Dai Z, Guo X, Weng T, Wang J et al (2009) Sclerostin mediates bone response to mechanical unloading through antagonizing Wnt/β-catenin signaling. J Bone Miner Res 24(10):1651–1661

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Li D, Wu X, Dang L, Lu A, Zhang G (2017) Bone-derived exosomes. Curr Opin Pharmacol 34:64–69

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Walter TS, Huang P, Zhang S, Zhu X, Wu Y et al (2010) Structural and functional insights of RANKL-RANK interaction and signaling. J Immunol 184(12):6910–6919

    Article  CAS  PubMed  Google Scholar 

  • Lu XL, Huo B, Chiang V, Guo XE (2012) Osteocytic network is more responsive in calcium signaling than osteoblastic network under fluid flow. J Bone Miner Res Off J Am Soc Bone Miner Res 27(3):563–574

    Article  CAS  Google Scholar 

  • Lu X, Mu E, Wei Y, Riethdorf S, Yang Q, Yuan M et al (2011) VCAM-1 promotes osteolytic expansion of indolent bone micrometastasis of breast cancer by engaging alpha4beta1-positive osteoclast progenitors. Cancer Cell 20(6):701–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu X, Wang Q, Hu G, Van Poznak C, Fleisher M, Reiss M et al (2009) ADAMTS1 and MMP1 proteolytically engage EGF-like ligands in an osteolytic signaling cascade for bone metastasis. Genes Dev 23(16):1882–1894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luther G, Wagner ER, Zhu G, Kang Q, Luo Q, Lamplot J et al (2011) BMP-9 induced osteogenic differentiation of mesenchymal stem cells: molecular mechanism and therapeutic potential. Curr Gene Ther 11(3):229–240

    Article  CAS  PubMed  Google Scholar 

  • Lyu H, Xiao Y, Guo Q, Huang Y, Luo X (2020) The role of bone-derived Exosomes in regulating skeletal metabolism and Extraosseous diseases. Frontiers in cell and developmental biology 8:89

    Article  PubMed  PubMed Central  Google Scholar 

  • MacDonald BT, Tamai K, He X (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17(1):9–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malladi S, Macalinao DG, Jin X, He L, Basnet H, Zou Y et al (2016) Metastatic latency and immune evasion through Autocrine inhibition of WNT. Cell 165(1):45–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manolagas SC (2016) Normal skeletal development and regulation of bone formation and resorption. UpToDate

    Google Scholar 

  • Manolagas SC, Jilka RL (1995) Bone marrow, cytokines, and bone remodeling—emerging insights into the pathophysiology of osteoporosis. N Engl J Med 332(5):305–311

    Article  CAS  PubMed  Google Scholar 

  • Marie PJ, Coffin JD, Hurley MM (2005) FGF and FGFR signaling in chondrodysplasias and craniosynostosis. J Cell Biochem 96(5):888–896

    Article  CAS  PubMed  Google Scholar 

  • Matsuo K, Otaki N (2012) Bone cell interactions through Eph/ephrin: bone modeling, remodeling and associated diseases. Cell Adhes Migr 6(2):148–156

    Article  Google Scholar 

  • McGarry JG, Klein-Nulend J, Prendergast PJ (2005) The effect of cytoskeletal disruption on pulsatile fluid flow-induced nitric oxide and prostaglandin E2 release in osteocytes and osteoblasts. Biochem Biophys Res Commun 330(1):341–348

    Article  CAS  PubMed  Google Scholar 

  • Medhora MM, Teitelbaum S, Chappel J, Alvarez J, Mimura H, Ross FP, Hruska K (1993) 1 alpha,25-dihydroxyvitamin D3 up-regulates expression of the osteoclast integrin alpha v beta 3. J Biol Chem 268(2):1456–1461

    Article  CAS  PubMed  Google Scholar 

  • Mera P, Laue K, Ferron M, Confavreux C, Wei J, Galán-Díez M et al (2016) Osteocalcin signaling in Myofibers is necessary and sufficient for optimum adaptation to exercise. Cell Metab 23(6):1078–1092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mercer RR, Miyasaka C, Mastro AM (2004) Metastatic breast cancer cells suppress osteoblast adhesion and differentiation. Clin Exp Metastasis 21(5):427–435

    Article  CAS  PubMed  Google Scholar 

  • Millimaggi D, Festuccia C, Angelucci A, D'Ascenzo S, Rucci N, Flati S et al (2006) Osteoblast-conditioned media stimulate membrane vesicle shedding in prostate cancer cells. Int J Oncol 28(4):909–914

    CAS  PubMed  Google Scholar 

  • Montero A, Okada Y, Tomita M, Ito M, Tsurukami H, Nakamura T et al (2000) Disruption of the fibroblast growth factor-2 gene results in decreased bone mass and bone formation. J Clin Invest 105:1085–1093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morhayim J, van de Peppel J, Demmers JA, Kocer G, Nigg AL, van Driel M et al (2015) Proteomic signatures of extracellular vesicles secreted by nonmineralizing and mineralizing human osteoblasts and stimulation of tumor cell growth. FASEB J 29(1):274–285

    Article  CAS  PubMed  Google Scholar 

  • Morhayim J, van de Peppel J, Dudakovic A, Chiba H, van Wijnen AJ, van Leeuwen JP (2017) Molecular characterization of human osteoblast-derived extracellular vesicle mRNA using next-generation sequencing. Biochim Biophys Acta, Mol Cell Res 1864(7):1133–1141

    Article  CAS  Google Scholar 

  • Morrell AE, Brown GN, Robinson ST, Sattler RL, Baik AD, Zhen G et al (2018) Mechanically induced Ca(2+) oscillations in osteocytes release extracellular vesicles and enhance bone formation. Bone Res 6:6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME et al (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410(6824):50–56

    Article  CAS  PubMed  Google Scholar 

  • Mundy GR (1997) Mechanisms of bone metastasis. Cancer 80(8 Suppl):1546–1556

    Article  CAS  PubMed  Google Scholar 

  • Mundy GR (2002) Metastasis to bone: causes, consequences and therapeutic opportunities. Nat Rev Cancer 2(8):584–593

    Article  CAS  PubMed  Google Scholar 

  • Nagata T, Kaho K, Nishikawa S, Shinohara H, Wakano Y, Ishida H (1994) Effect of prostaglandin E2 on mineralization of bone nodules formed by fetal rat calvarial cells. Calcif Tissue Int 55(6):451–457

    Article  CAS  PubMed  Google Scholar 

  • Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-hora M, Feng JQ et al (2011) Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med 17(10):1231–1234

    Article  CAS  PubMed  Google Scholar 

  • Narayanan R, Huang CC, Ravindran S (2016) Hijacking the cellular mail: exosome mediated differentiation of mesenchymal stem cells. Stem Cells Int 2016:3808674. https://doi.org/10.1155/2016/3808674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen DX, Bos PD, Massague J (2009) Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 9(4):274–284

    Article  CAS  PubMed  Google Scholar 

  • Nguyen HCN, Xie W, Yang M, Hsieh C-L, Drouin S, Lee G-SM et al (2013) Expression differences of circulating microRNAs in metastatic castration resistant prostate cancer and low-risk, localized prostate cancer. Prostate 73(4):346–354

    Article  CAS  PubMed  Google Scholar 

  • O’Brien CA, Plotkin LI, Galli C, Goellner JJ, Gortazar AR, Allen MR et al (2008) Control of bone mass and remodeling by PTH receptor signaling in osteocytes. PLoS One 3(8):e2942

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oades GM, Coxon J, Colston KW (2002) The potential role of bisphosphonates in prostate cancer. Prostate Cancer Prostatic Dis 5(4):264–272

    Article  CAS  PubMed  Google Scholar 

  • Okada Y, Morimoto I, Ura K, Watanabe K, Eto S, Kumegawa M, Raisz L, Pilbeam C, Tanaka Y (2002) Cell-to-cell adhesion via intercellular adhesion molecule-1 and leukocyte functionassociated antigen-1 pathway is involved in 1α,25(OH)2D3, PTH and IL-1α-induced osteoclast differentiation and bone resorption. Endocr J 49:483–495

    Article  CAS  PubMed  Google Scholar 

  • Okazaki M, Takeshita S, Kawai S, Kikuno R, Tsujimura A, Kudo A et al (1994) Molecular cloning and characterization of OB-cadherin, a new member of cadherin family expressed in osteoblasts. J Biol Chem 269(16):12092–12098

    Article  CAS  PubMed  Google Scholar 

  • Ornitz DM, Itoh N (2015) The fibroblast growth factor signaling pathway. Wiley Interdiscip Rev Dev Biol 4(3):215–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ottewell PD (2016) The role of osteoblasts in bone metastasis. J Bone Oncol 5(3):124–127

    Article  PubMed  PubMed Central  Google Scholar 

  • Ottewell PD, Wang N, Meek J, Fowles CA, Croucher PI, Eaton CL et al (2014) Castration-induced bone loss triggers growth of disseminated prostate cancer cells in bone. Endocr Relat Cancer 21(5):769–781

    Article  CAS  PubMed  Google Scholar 

  • Overall CM, Lopez-Otin C (2002) Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer 2(9):657–672

    Article  CAS  PubMed  Google Scholar 

  • Pacifici R, Brown C, Puscheck E, Friedrich E, Slatopolsky E, Maggio D et al (1991) Effect of surgical menopause and estrogen replacement on cytokine release from human blood mononuclear cells. Proc Natl Acad Sci U S A 88(12):5134–5138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Page JM, Merkel AR, Ruppender NS, Guo R, Dadwal UC, Cannonier S et al (2015) Matrix rigidity regulates the transition of tumor cells to a bone-destructive phenotype through integrin β3 and TGF-β receptor type II. Biomaterials 64:33–44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8(3):221–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paget S (1989) The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev 8(2):98–101

    CAS  PubMed  Google Scholar 

  • Park JH, Lee NK, Lee SY (2017) Current understanding of RANK signaling in osteoclast differentiation and maturation. Mol Cells 40(10):706–713

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pedersen EA, Shiozawa Y, Pienta KJ, Taichman RS (2012) The prostate cancer bone marrow niche: more than just 'fertile soil'. Asian J Androl 14(3):423–427

    Article  PubMed  PubMed Central  Google Scholar 

  • Pethő A, Chen Y, George A (2018) Exosomes in extracellular matrix bone biology. Curr Osteoporos Rep 16(1):58–64

    Article  PubMed  PubMed Central  Google Scholar 

  • Pezaro C, Omlin A, Lorente D, Rodrigues DN, Ferraldeschi R, Bianchini D et al (2014) Visceral disease in castration-resistant prostate cancer. Eur Urol 65(2):270–273

    Article  CAS  PubMed  Google Scholar 

  • Pols MS, Klumperman J (2009) Trafficking and function of the tetraspanin CD63. Exp Cell Res 315(9):1584–1592

    Article  CAS  PubMed  Google Scholar 

  • Prince M, Banerjee C, Javed A, Green J, Lian JB, Stein GS et al (2001) Expression and regulation of Runx2/Cbfa1 and osteoblast phenotypic markers during the growth and differentiation of human osteoblasts. J Cell Biochem 80:424–440

    Article  CAS  PubMed  Google Scholar 

  • Probert C, Dottorini T, Speakman A, Hunt S, Nafee T, Fazeli A et al (2019) Communication of prostate cancer cells with bone cells via extracellular vesicle RNA; a potential mechanism of metastasis. Oncogene 38(10):1751–1763

    Article  CAS  PubMed  Google Scholar 

  • Provot S, Schipani E, Wu JY et al (2013) Development of the skeleton. In: Marcus R, Dempster D (eds) Osteoporosis, 4th edn. Academic, USA, pp 97–126

    Chapter  Google Scholar 

  • Qin Y, Wang L, Gao Z, Chen G, Zhang C (2016) Bone marrow stromal/stem cell-derived extracellular vesicles regulate osteoblast activity and differentiation in vitro and promote bone regeneration in vivo. Sci Rep 6:21961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qing H, Ardeshirpour L, Pajevic PD, Dusevich V, Jahn K, Kato S et al (2012) Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation. J Bone Miner Res 27(5):1018–1029

    Article  CAS  PubMed  Google Scholar 

  • Quax PHA, de Bart ACW, Schalken JA, Verheijen JH (1997) Plasminogen activator and matrix metalloproteinase production and extracellular matrix degradation by rat prostate cancer cells in vitro: correlation with metastatic behavior in vivo. Prostate 32(3):196–204

    Article  CAS  PubMed  Google Scholar 

  • Quiroz-Munoz M, Izadmehr S, Arumugam D, Wong B, Kirschenbaum A, Levine AC (2019) Mechanisms of osteoblastic bone metastasis in prostate cancer: role of prostatic acid phosphatase. J Endocr Soc 3(3):655–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raggatt LJ, Partridge NC (2010) Cellular and molecular mechanisms of bone remodeling. J Biol Chem 285(33):25103–25108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raisz LG, Fall PM, Gabbitas BY, McCarthy TL, Kream BE, Canalis E (1993) Effects of prostaglandin E2 on bone formation in cultured fetal rat calvariae: role of insulin-like growth factor-I. Endocrinology 133(4):1504–1510

    Article  CAS  PubMed  Google Scholar 

  • Rajendiran G, Green L, Chhabra G (2011) A rare presentation of prostate cancer with diffuse osteolytic metastasis and PSA of 7242 ng/ml. International Journal of Case Reports and Images 2(9):16–20

    Article  Google Scholar 

  • Rani S, Ryan AE, Griffin MD, Ritter T (2015) Mesenchymal stem cell-derived extracellular vesicles: toward cell-free therapeutic applications. Mol Ther 23(5):812–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raouf A, Seth A (2000) Ets transcription factors and targets in osteogenesis. Oncogene 19(55):6455–6463

    Article  CAS  PubMed  Google Scholar 

  • Rhee Y, Lee EY, Lezcano V, Ronda AC, Condon KW, Allen MR et al (2013) Resorption controls bone anabolism driven by parathyroid hormone (PTH) receptor signaling in osteocytes. J Biol Chem 288(41):29809–29820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rochefort GY, Pallu S, Benhamou CL (2010) Osteocyte: the unrecognized side of bone tissue. Osteoporos Int 21(9):1457–1469

    Article  CAS  PubMed  Google Scholar 

  • Roodman GD (2004) Mechanisms of bone metastasis. N Engl J Med 350(16):1655–1664

    Article  CAS  PubMed  Google Scholar 

  • Roodman G (2018) Mechanisms of bone metastasis. UpToDate.

    Google Scholar 

  • Rucci N (2008) Molecular biology of bone remodelling. Clin Cases Miner Bone Metab 5(1):49–56

    PubMed  PubMed Central  Google Scholar 

  • Runz S, Keller S, Rupp C, Stoeck A, Issa Y, Koensgen D et al (2007) Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol Oncol 107(3):563–571

    Article  CAS  PubMed  Google Scholar 

  • Sánchez CA, Andahur EI, Valenzuela R, Castellón EA, Fullá JA, Ramos CG et al (2016) Exosomes from bulk and stem cells from human prostate cancer have a differential microRNA content that contributes cooperatively over local and pre-metastatic niche. Oncotarget 7(4):3993–4008

    Article  PubMed  Google Scholar 

  • Saraswati S, Block AS, Davidson MK, Rank RG, Mahadevan M, Diekman AB (2011) Galectin-3 is a substrate for prostate specific antigen (PSA) in human seminal plasma. Prostate 71(2):197–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato M, Morii E, Komori T, Kawahata H, Sugimoto M, Terai K et al (1998) Transcriptional regulation of osteopontin gene in vivo by PEBP2αA/CBFA1 and ETS1 in the skeletal tissues. Oncogene 17(12):1517–1525

    Article  CAS  PubMed  Google Scholar 

  • Schaffler MB, Cheung W-Y, Majeska R, Kennedy O (2014) Osteocytes: master orchestrators of bone. Calcif Tissue Int 94(1):5–24

    Article  CAS  PubMed  Google Scholar 

  • Scimeca M, Urbano N, Bonfiglio R et al (2018) Prostate osteoblast-like cells: a reliable prognostic marker of bone metastasis in prostate cancer patients. Contrast Media Mol Imaging 2018:9840962

    Google Scholar 

  • Se Kyoung P, In Sook L, Kil Ho C, Jae Hyuck Y, Sung Moon L, Sun Joo L et al (2014) Systematic approach of sclerotic bone lesions basis on imaging findings. J Korean Soc Radiol 71(1):39–48

    Article  Google Scholar 

  • Segamwenge IL, Mgori NK, Abdallahyussuf S, Mukulu CN, Nakangombe P, Ngalyuka PK et al (2012) Cancer of the prostate presenting with diffuse osteolytic metastatic bone lesions: a case report. J Med Case Rep 6:425

    Article  PubMed  PubMed Central  Google Scholar 

  • Sementchenko VI, Watson DK (2000) Ets target genes: past, present and future. Oncogene 19(55):6533–6548

    Article  CAS  PubMed  Google Scholar 

  • Sethi N, Dai X, Winter CG, Kang Y (2011) Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells. Cancer Cell 19(2):192–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shevde NK, Bendixen AC, Dienger KM, Pike JW (2000) Estrogens suppress RANK ligand-induced osteoclast differentiation via a stromal cell independent mechanism involving c-Jun repression. Proc Natl Acad Sci U S A 97(14):7829–7834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi K, Lu J, Zhao Y, Wang L, Li J, Qi B et al (2013) MicroRNA-214 suppresses osteogenic differentiation of C2C12 myoblast cells by targeting Osterix. Bone 55(2):487–494

    Article  CAS  PubMed  Google Scholar 

  • Shiozawa Y, Pedersen EA, Havens AM, Jung Y, Mishra A, Joseph J et al (2011) Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest 121(4):1298–1312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shiozawa Y, Pedersen EA, Patel LR, Ziegler AM, Havens AM, Jung Y et al (2010) GAS6/AXL axis regulates prostate cancer invasion, proliferation, and survival in the bone marrow niche. Neoplasia 12(2):116–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shiozawa Y, Pienta KJ, Taichman RS (2011) Hematopoietic stem cell niche is a potential therapeutic target for bone metastatic tumors. Clin Cancer Res 17(17):5553–5558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shupp AB, Kolb AD, Mukhopadhyay D, Bussard KM (2018) Cancer metastases to bone: concepts, mechanisms, and interactions with bone osteoblasts. Cancers (Basel) 10(6):182

    Article  CAS  Google Scholar 

  • Siddiqui JA, Partridge NC (2016) Physiological bone remodeling: systemic regulation and growth factor involvement. Physiology 31(3):233–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinha KM, Zhou X (2013) Genetic and molecular control of osterix in skeletal formation. J Cell Biochem 114(5):975–984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith MR, Brown GA, Saad F (2009) New opportunities in the management of prostate cancer–related bone complications. Urologic Oncology: Seminars and Original Investigations 27(6, Supplement):S1–S20

    Article  Google Scholar 

  • Soekmadji C, Corcoran NM, Oleinikova I, Jovanovic L, Australian Prostate Cancer Collaboration B, Ramm GA et al (2017) Extracellular vesicles for personalized therapy decision support in advanced metastatic cancers and its potential impact for prostate cancer. Prostate 77(14):1416–1423

    Article  CAS  PubMed  Google Scholar 

  • Soekmadji C, Riches JD, Russell PJ, Ruelcke JE, McPherson S, Wang C et al (2016) Modulation of paracrine signaling by CD9 positive small extracellular vesicles mediates cellular growth of androgen deprived prostate cancer. Oncotarget 8(32):52237–52255

    Article  PubMed  PubMed Central  Google Scholar 

  • Solberg LB, Stang E, Brorson SH, Andersson G, Reinholt FP (2015) Tartrate-resistant acid phosphatase (TRAP) co-localizes with receptor activator of NF-KB ligand (RANKL) and osteoprotegerin (OPG) in lysosomal-associated membrane protein 1 (LAMP1)-positive vesicles in rat osteoblasts and osteocytes. Histochem Cell Biol 143(2):195–207

    Article  CAS  PubMed  Google Scholar 

  • Sosnoski DM, Norgard RJ, Grove CD, Foster SJ, Mastro AM (2015) Dormancy and growth of metastatic breast cancer cells in a bone-like microenvironment. Clin Exp Metastasis 32(4):335–344

    Article  CAS  PubMed  Google Scholar 

  • Sugatani T, Vacher J, Hruska KA (2011) A microRNA expression signature of osteoclastogenesis. Blood 117(13):3648–3657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun H, Kim JK, Mortensen R, Mutyaba LP, Hankenson KD, Krebsbach PH (2013) Osteoblast-targeted suppression of PPARγ increases osteogenesis through activation of mTOR signaling. Stem cells (Dayton Ohio) 31(10):2183–2192

    Article  CAS  Google Scholar 

  • Sun Y-X, Schneider A, Jung Y, Wang J, Dai J, Wang J et al (2005) Skeletal localization and neutralization of the SDF-1(CXCL12)/CXCR4 Axis blocks prostate cancer metastasis and growth in osseous sites in vivo. J Bone Miner Res 20(2):318–329

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Zhao C, Li Y, Wang L, Nie G, Peng J et al (2016) Osteoclast-derived microRNA-containing exosomes selectively inhibit osteoblast activity. Cell Discov 2:16015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Syn N, Wang L, Sethi G, Thiery JP, Goh BC (2016) Exosome-mediated metastasis: from epithelial-Mesenchymal transition to escape from Immunosurveillance. Trends Pharmacol Sci 37(7):606–617

    Article  CAS  PubMed  Google Scholar 

  • Taichman RS (2005) Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 105(7):2631–2639

    Article  CAS  PubMed  Google Scholar 

  • Taichman RS, Cooper C, Keller ET, Pienta KJ, Taichman NS, McCauley LK (2002) Use of the stromal cell-derived Factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res 62(6):1832

    CAS  PubMed  Google Scholar 

  • Taichman RS, Patel LR, Bedenis R, Wang J, Weidner S, Schumann T et al (2013) GAS6 receptor status is associated with dormancy and bone metastatic tumor formation. PLoS One 8(4):e61873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi N, Akatsu T, Udagawa N, Sasaki T, Yamaguchi A, Moseley JM et al (1988) Osteoblastic cells are involved in osteoclast formation. Endocrinology 123(5):2600–2602

    Article  CAS  PubMed  Google Scholar 

  • Tamasi JA, Vasilov A, Shimizu E, Benton N, Johnson J, Bitel CL et al (2013) Monocyte chemoattractant protein-1 is a mediator of the anabolic action of parathyroid hormone on bone. J Bone Miner Res 28(9):1975–1986

    Article  CAS  PubMed  Google Scholar 

  • Tamma R, Ribatti D (2017) Bone niches, hematopoietic stem cells, and vessel formation. Int J Mol Sci 18(1)

    Google Scholar 

  • Tamma R, Zallone A (2012) Osteoblast and osteoclast crosstalks: from OAF to Ephrin. Inflamm Allergy Drug Targets 11(3):196–200

    Article  CAS  PubMed  Google Scholar 

  • Tan SD, de Vries TJ, Kuijpers-Jagtman AM, Semeins CM, Everts V, Klein-Nulend J (2007) Osteocytes subjected to fluid flow inhibit osteoclast formation and bone resorption. Bone 41(5):745–751

    Article  CAS  PubMed  Google Scholar 

  • Tao S-C, Guo S-C (2019) Extracellular vesicles in bone: “dogrobbers” in the “eternal battle field”. Cell Communication and Signaling 17(1):6

    Article  PubMed  PubMed Central  Google Scholar 

  • Tat SK, Padrines M, Theoleyre S, Couillaud-Battaglia S, Heymann D, Redini F et al (2006) OPG/membranous–RANKL complex is internalized via the clathrin pathway before a lysosomal and a proteasomal degradation. Bone 39(4):706–715

    Article  CAS  PubMed  Google Scholar 

  • Thompson WR, Rubin CT, Rubin J (2012) Mechanical regulation of signaling pathways in bone. Gene 503(2):179–193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian Y, Xu Y, Fu Q, He M (2011) Parathyroid hormone regulates osteoblast differentiation in a Wnt/β-catenin-dependent manner. Mol Cell Biochem 355(1–2):211–216

    Article  CAS  PubMed  Google Scholar 

  • Tu X, Rhee Y, Condon KW, Bivi N, Allen MR, Dwyer D et al (2012) Sost downregulation and local Wnt signaling are required for the osteogenic response to mechanical loading. Bone 50(1):209–217

    Article  CAS  PubMed  Google Scholar 

  • Udagawa N, Takahashi N, Akatsu T, Sasaki T, Yamaguchi A, Kodama H et al (1989) The bone marrow-derived stromal cell lines MC3T3-G2/PA6 and ST2 support osteoclast-like cell differentiation in cocultures with mouse spleen cells. Endocrinology 125(4):1805–1813

    Article  CAS  PubMed  Google Scholar 

  • Urwin GH, Percival RC, Harris S, Beneton MN, Williams JL, Kanis JA (1985) Generalised increase in bone resorption in carcinoma of the prostate. Br J Urol 57(6):721–723

    Article  CAS  PubMed  Google Scholar 

  • van Driel M, van Leeuwen JPTM (2014) Vitamin D endocrine system and osteoblasts. Bonekey Rep 3:493

    PubMed  PubMed Central  Google Scholar 

  • Vezeridis PS, Semeins CM, Chen Q, Klein-Nulend J (2006) Osteocytes subjected to pulsating fluid flow regulate osteoblast proliferation and differentiation. Biochem Biophys Res Commun 348(3):1082–1088

    Article  CAS  PubMed  Google Scholar 

  • Wang J-C, Bégin LR, Bérubé NG, Chevalier S, Aprikian AG, Gourdeau H et al (2007) Down-regulation of CD9 expression during prostate carcinoma progression is associated with CD9 mRNA modifications. Clin Cancer Res 13(8):2354

    Article  CAS  PubMed  Google Scholar 

  • Wang N, Docherty FE, Brown HK, Reeves KJ, Fowles AC, Ottewell PD et al (2014) Prostate cancer cells preferentially home to osteoblast-rich areas in the early stages of bone metastasis: evidence from in vivo models. J Bone Miner Res Off J Am Soc Bone Miner Res 29(12):2688–2696

    Article  CAS  Google Scholar 

  • Wang X, Guo B, Li Q, Peng J, Yang Z, Wang A et al (2013) miR-214 targets ATF4 to inhibit bone formation. Nat Med 19(1):93–100

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Hendrix A, Hernot S, Lemaire M, De Bruyne E, Van Valckenborgh E et al (2014) Bone marrow stromal cell–derived exosomes as communicators in drug resistance in multiple myeloma cells. Blood 124(4):555–566

    Article  CAS  PubMed  Google Scholar 

  • Watanuki M, Sakai A, Sakata T, Tsurukami H, Miwa M, Uchida Y et al (2002) Role of inducible nitric oxide synthase in skeletal adaptation to acute increases in mechanical loading. J Bone Miner Res 17(6):1015–1025

    Article  CAS  PubMed  Google Scholar 

  • Wei J, Li H, Wang S, Li T, Fan J, Liang X et al (2014) Let-7 enhances osteogenesis and bone formation while repressing adipogenesis of human stromal/mesenchymal stem cells by regulating HMGA2. Stem Cells Dev 23(13):1452–1463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wein MN, Kronenberg HM (2018) Regulation of bone remodeling by parathyroid hormone. Cold Spring Harb Perspect Med 8(8)

    Google Scholar 

  • Weitzmann M (2013) The role of inflammatory cytokines, the RANKL/OPG Axis, and the Immunoskeletal Interface in physiological bone turnover and osteoporosis. Scientifica 2013:125705

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wilson A, Trumpp A (2006) Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 6(2):93–106

    Article  CAS  PubMed  Google Scholar 

  • Wu M, Chen G, Li Y-P (2016) TGF-β and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease. Bone Research 4(1):16009

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie Y, Chen Y, Zhang L, Ge W, Tang P (2017) The roles of bone-derived exosomes and exosomal microRNAs in regulating bone remodelling. J Cell Mol Med 21(5):1033–1041

    Article  PubMed  Google Scholar 

  • Xiong J, Onal M, Jilka RL, Weinstein RS, Manolagas SC, O'Brien CA (2011) Matrix-embedded cells control osteoclast formation. Nat Med 17(10):1235–1241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu S, Santini GC, De Veirman K, Broek IV, Leleu X, De Becker A et al (2013) Upregulation of miR-135b is involved in the impaired osteogenic differentiation of mesenchymal stem cells derived from multiple myeloma patients. PLoS One 8(11):e79752

    Google Scholar 

  • Xu J-F, Yang G-H, Pan X-H, Zhang S-J, Zhao C, Qiu B-S et al (2014) Altered microRNA expression profile in exosomes during osteogenic differentiation of human bone marrow-derived mesenchymal stem cells. PLoS One 9(12):e114627

    Google Scholar 

  • Yang M, Arai A, Udagawa N, Hiraga T, Lijuan Z, Ito S et al (2017) Osteogenic factor Runx2 Marks a subset of Leptin receptor-positive cells that sit atop the bone marrow stromal cell hierarchy. Sci Rep 7(1):4928

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yao GQ, Sun BH, Weir EC, Insogna KL (2002) A role for cell surface CSF-1 in osteoblast-mediated osteoclastogenesis. Calcif Tissue Int 70:339–346

    Article  CAS  PubMed  Google Scholar 

  • Ye Y, Li SL, Ma YY, Diao YJ, Yang L, Su MQ et al (2017) Exosomal miR-141-3p regulates osteoblast activity to promote the osteoblastic metastasis of prostate cancer. Oncotarget 8(55):94834–94849

    Article  PubMed  PubMed Central  Google Scholar 

  • Yin T, Li L (2006) The stem cell niches in bone. J Clin Invest 116(5):1195–1201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • You L, Gu W, Chen L, Pan L, Chen J, Peng Y (2014) MiR-378 overexpression attenuates high glucose-suppressed osteogenic differentiation through targeting CASP3 and activating PI3K/Akt signaling pathway. Int J Clin Exp Pathol 7(10):7249–7261

    PubMed  PubMed Central  Google Scholar 

  • Yuan FL, Wu QY, Miao ZN, Xu MH, Xu RS, Jiang DL et al (2018) Osteoclast-derived extracellular vesicles: novel regulators of Osteoclastogenesis and osteoclast-osteoblasts communication in bone remodeling. Front Physiol 9:628

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu-Lee LY, Yu G, Lee YC, Lin SC, Pan J, Pan T et al (2018) Osteoblast-secreted factors mediate dormancy of metastatic prostate cancer in the bone via activation of the TGFbetaRIII-p38MAPK-pS249/T252RB pathway. Cancer Res 78(11):2911–2924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yumoto K, Eber MR, Wang J, Cackowski FC, Decker AM, Lee E et al (2016) Axl is required for TGF-β2-induced dormancy of prostate cancer cells in the bone marrow. Sci Rep 6:36520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zayzafoon M, Abdulkadir SA, McDonald JM (2004) Notch signaling and ERK activation are important for the osteomimetic properties of prostate cancer bone metastatic cell lines. J Biol Chem 279(5):3662–3670

    Article  CAS  PubMed  Google Scholar 

  • Zhang YH, Heulsmann A, Tondravi MM, Mukherjee A, Abu-Amer Y (2001) Tumor necrosis factor-alpha (TNF) stimulates RANKL-induced osteoclastogenesis via coupling of TNF type 1 receptor and RANK signaling pathways. J Biol Chem 276(1):563–568

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Tu Q, Bonewald LF, He X, Stein G, Lian J et al (2011) Effects of miR-335-5p in modulating osteogenic differentiation by specifically downregulating Wnt antagonist DKK1. J Bone Miner Res 26(8):1953–1963

    Article  CAS  PubMed  Google Scholar 

  • Zhang W-B, Zhong W-J, Wang L (2014) A signal-amplification circuit between miR-218 and Wnt/β-catenin signal promotes human adipose tissue-derived stem cells osteogenic differentiation. Bone 58:59–66

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Jiang S, Hantash BM (2010) Transforming growth factor beta1 induces osteogenic differentiation of murine bone marrow stromal cells. Tissue Eng Part A 16(2):725–733

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Sun W, Zhang P, Ling S, Li Y, Zhao D et al (2015) miR-214 promotes osteoclastogenesis by targeting Pten/PI3k/Akt pathway. RNA Biol 12(3):343–353

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao S, Zhang YK, Harris S, Ahuja SS, Bonewald LF (2002) MLO-Y4 osteocyte-like cells support osteoclast formation and activation. J Bone Miner Res 17(11):2068–2079

    Article  CAS  PubMed  Google Scholar 

  • Zhou H, Lu S (2010) Dempster, D bone remodeling: cellular activities in bone. In: Orwoll E, Bilezikian J, Vanderschueren D (eds) Osteoporosis in men the effects of gender on skeletal health. Academic, USA, pp 15–24

    Google Scholar 

  • Zhu S, Yao F, Qiu H, Zhang G, Xu H, Xu J (2018) Coupling factors and exosomal packaging microRNAs involved in the regulation of bone remodelling. Biol Rev 93(1):469–480

    Article  PubMed  Google Scholar 

  • Zomer A, Vendrig T, Hopmans ES, van Eijndhoven M, Middeldorp JM, Pegtel DM (2010) Exosomes: fit to deliver small RNA. Commun Integr Biol 3(5):447–450

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zvereff V, Wang JC, Shun K, Lacoste J, Chevrette M (2007) Colocalisation of CD9 and mortalin in CD9-induced mitotic catastrophe in human prostate cancer cells. Br J Cancer 97(7):941–948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Patil, K.C., Soekmadji, C. (2021). Extracellular Vesicle-Mediated Bone Remodeling and Bone Metastasis: Implications in Prostate Cancer. In: Mathivanan, S., Fonseka, P., Nedeva, C., Atukorala, I. (eds) New Frontiers: Extracellular Vesicles. Subcellular Biochemistry, vol 97. Springer, Cham. https://doi.org/10.1007/978-3-030-67171-6_12

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