Cancer metastasis to the bone: Mechanisms and animal models (Review)
- This article is part of the special Issue: Bone invasion and/or metastasis by malignant tumors and its underlying mechanisms
- Authors:
- Meimei Deng
- Hao Ding
- Yuru Zhou
- Guangying Qi
- Jinfeng Gan
-
Affiliations: Guangxi Key Laboratory of Tumor Immunology and Microenvironmental Regulation, Guilin Medical University, Guilin, Guangxi 541199, P.R. China, Department of Thoracic Surgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, Sichuan 637000, P.R. China - Published online on: March 6, 2025 https://doi.org/10.3892/ol.2025.14967
- Article Number: 221
-
Copyright: © Deng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
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|
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A and Bray F: Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 71:209–249. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Coleman RE, Croucher PI, Padhani AR, Clézardin P, Chow E, Fallon M, Guise T, Colangeli S, Capanna R and Costa L: Bone metastases. Nat Rev Dis Primers. 6:832020. View Article : Google Scholar : PubMed/NCBI | |
|
Clézardin P, Coleman R, Puppo M, Ottewell P, Bonnelye E, Paycha F, Confavreux CB and Holen I: Bone metastasis: Mechanisms, therapies, and biomarkers. Physiol Rev. 101:797–855. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Papalia GF, Brigato P, Sisca L, Maltese G, Faiella E, Santucci D, Pantano F, Vincenzi B, Tonini G, Papalia R and Denaro V: Artificial intelligence in detection, management, and prognosis of bone metastasis: A systematic review. Cancers (Basel). 16:27002024. View Article : Google Scholar : PubMed/NCBI | |
|
Sousa S and Clézardin P: Bone-targeted therapies in Cancer-induced bone disease. Calcif Tissue Int. 102:227–250. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang W, Bado IL, Hu J, Wan YW, Wu L, Wang H, Gao Y, Jeong HH, Xu Z, Hao X, et al: The bone microenvironment invigorates metastatic seeds for further dissemination. Cell. 184:2471–86.e20. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Coleman R, Hadji P, Body JJ, Santini D, Chow E, Terpos E, Oudard S, Bruland Ø, Flamen P, Kurth A, et al: Bone health in cancer: ESMO Clinical Practice Guidelines. Ann Oncol. 31:1650–1663. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Trompet D, Melis S, Chagin AS and Maes C: Skeletal stem and progenitor cells in bone development and repair. J Bone Miner Res. 39:633–654. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Boyce BF: Advances in the regulation of osteoclasts and osteoclast functions. J Dent Res. 92:860–867. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Ikebuchi Y, Aoki S, Honma M, Hayashi M, Sugamori Y, Khan M, Kariya Y, Kato G, Tabata Y, Penninger JM, et al: Coupling of bone resorption and formation by RANKL reverse signalling. Nature. 561:195–200. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Yamagishi T, Kawashima H, Ogose A, Ariizumi T, Oike N, Sasaki T, Hatano H, Ohashi R, Umezu H, Ajioka Y and Endo N: Expression profiling of Receptor-activator of nuclear Factor-Kappa B ligand in soft tissue tumors. Tohoku J Exp Med. 248:87–97. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Gostage J, Kostenuik P, Goljanek-Whysall K, Bellantuono I, McCloskey E and Bonnet N: Extra-osseous roles of the RANK-RANKL-OPG axis with a focus on skeletal muscle. Curr Osteoporos Rep. 22:632–650. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Nozawa K, Fujishiro M, Kawasaki M, Kaneko H, Iwabuchi K, Yanagida M, Suzuki F, Miyazawa K, Takasaki Y, Ogawa H, et al: Connective tissue growth factor promotes articular damage by increased osteoclastogenesis in patients with rheumatoid arthritis. Arthritis Res Ther. 11:R1742009. View Article : Google Scholar : PubMed/NCBI | |
|
Aoyama E, Kubota S, Khattab HM, Nishida T and Takigawa M: CCN2 enhances RANKL-induced osteoclast differentiation via direct binding to RANK and OPG. Bone. 73:242–248. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Ren W, Sun X, Wang K, Feng H, Liu Y, Fei C, Wan S, Wang W, Luo J, Shi Q, et al: BMP9 inhibits the bone metastasis of breast cancer cells by downregulating CCN2 (connective tissue growth factor, CTGF) expression. Mol Biol Rep. 41:1373–1383. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Sims NA and Martin TJ: Coupling the activities of bone formation and resorption: A multitude of signals within the basic multicellular unit. Bonekey Rep. 3:4812014. View Article : Google Scholar : PubMed/NCBI | |
|
Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR and de Crombrugghe B: The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell. 108:17–29. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Garcia J and Delany AM: MicroRNAs regulating TGFβ and BMP signaling in the osteoblast lineage. Bone. 143:1157912021. View Article : Google Scholar : PubMed/NCBI | |
|
Caetano-Lopes J, Canhão H and Fonseca JE: Osteoblasts and bone formation. Acta Reumatol Port. 32:103–110. 2007.PubMed/NCBI | |
|
Abhishek Shah A, Chand D, Ahamad S, Porwal K, Chourasia MK, Mohanan K, Srivastava KR and Chattopadhyay N: Therapeutic targeting of Wnt antagonists by small molecules for treatment of osteoporosis. Biochem Pharmacol. 230:1165872024. View Article : Google Scholar : PubMed/NCBI | |
|
van't Hof RJ and Ralston SH: Nitric oxide and bone. Immunology. 103:255–261. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Danilchenko S, Kalinkevich A, Zhovner M, Kuznetsov V, Li H and Wang J: Anisotropic aspects of solubility behavior in the demineralization of cortical bone revealed by XRD analysis. J Biol Phys. 45:77–88. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Kitcharanant N, Chattipakorn N and Chattipakorn SC: The effect of intermittent parathyroid hormone on bone lengthening: Current evidence to inform future effective interventions. Osteoporos Int. 34:1657–1675. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Niwczyk O, Grymowicz M, Szczęsnowicz A, Hajbos M, Kostrzak A, Budzik M, Maciejewska-Jeske M, Bala G, Smolarczyk R and Męczekalski B: Bones and hormones: Interaction between hormones of the hypothalamus, pituitary, adipose tissue and bone. Int J Mol Sci. 24:68402023. View Article : Google Scholar : PubMed/NCBI | |
|
Grigoryan S and Clines GA: Hormonal control of bone architecture throughout the lifespan: Implications for fracture prediction and prevention. Endocr Pract. 30:687–694. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Nagy V and Penninger JM: The RANKL-RANK Story. Gerontology. 61:534–542. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Mastro AM, Gay CV and Welch DR: The skeleton as a unique environment for breast cancer cells. Clin Exp Metastasis. 20:275–284. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Bussard KM, Gay CV and Mastro AM: The bone microenvironment in metastasis; what is special about bone? Cancer Metastasis Rev. 27:41–55. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Sharma R, Sharma R, Khaket TP, Dutta C, Chakraborty B and Mukherjee TK: Breast cancer metastasis: Putative therapeutic role of vascular cell adhesion molecule-1. Cell Oncol (Dordr). 40:199–208. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Chen Q and Massagué J: Molecular pathways: VCAM-1 as a potential therapeutic target in metastasis. Clin Cancer Res. 18:5520–555. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Lipton A: Implications of bone metastases and the benefits of bone-targeted therapy. Semin Oncol. 37 (Suppl 2):S15–S29. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
De Leon-Oliva D, Barrena-Blázquez S, Jiménez-Álvarez L, Fraile-Martinez O, García-Montero C, López-González L, Torres-Carranza D, García-Puente LM, Carranza ST, Álvarez-Mon MÁ, et al: The RANK-RANKL-OPG System: A multifaceted regulator of homeostasis, immunity, and cancer. Medicina (Kaunas). 59:17522023. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Y, Liu Y, Huang Z, Chen X and Zhang B: The roles of osteoprotegerin in cancer, far beyond a bone player. Cell Death Discov. 8:2522022. 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 | |
|
Roodman GD: Mechanisms of bone metastasis. N Engl J Med. 350:1655–1664. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Susperregui AR, Viñals F, Ho PW, Gillespie MT, Martin TJ and Ventura F: BMP-2 regulation of PTHrP and osteoclastogenic factors during osteoblast differentiation of C2C12 cells. J Cell Physiol. 216:144–152. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Izawa T, Zou W, Chappel JC, Ashley JW, Feng X and Teitelbaum SL: c-Src links a RANK/αvβ3 integrin complex to the osteoclast cytoskeleton. Mol Cell Biol. 32:2943–2953. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou S, Li J, Ying T, Wang Y, Wang Q, Li X and Zhao F: StemRegenin 1 attenuates the RANKL-induced osteoclastogenesis via inhibiting AhR-c-src-NF-κB/p-ERK MAPK-NFATc1 signaling pathway. iScience. 27:1096822024. View Article : Google Scholar : PubMed/NCBI | |
|
Ibaragi S, Shimo T, Iwamoto M, Hassan NM, Kodama S, Isowa S and Sasaki A: Parathyroid hormone-related peptide regulates matrix metalloproteinase-13 gene expression in bone metastatic breast cancer cells. Anticancer Res. 30:5029–5036. 2010.PubMed/NCBI | |
|
Giarratana AO, Prendergast CM, Salvatore MM and Capaccione KM: TGF-β signaling: Critical nexus of fibrogenesis and cancer. J Transl Med. 22:5942024. View Article : Google Scholar : PubMed/NCBI | |
|
Juárez P and Guise TA: TGF-β in cancer and bone: Implications for treatment of bone metastases. Bone. 48:23–29. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Fan C, Wang Q, Kuipers TB, Cats D, Iyengar PV, Hagenaars SC, Mesker WE, Devilee P, Tollenaar RAEM, Mei H and Ten Dijke P: LncRNA LITATS1 suppresses TGF-β-induced EMT and cancer cell plasticity by potentiating TβRI degradation. EMBO J. 42:e1128062023. View Article : Google Scholar : PubMed/NCBI | |
|
Li Y, Drabsch Y, Pujuguet P, Ren J, van Laar T, Zhang L, van Dam H, Clément-Lacroix P and Ten Dijke P: Genetic depletion and pharmacological targeting of αv integrin in breast cancer cells impairs metastasis in zebrafish and mouse xenograft models. Breast Cancer Res. 17:282015. View Article : Google Scholar : PubMed/NCBI | |
|
Luis-Ravelo D, Antón I, Vicent S, Zandueta C, Martínez S, Valencia K, Ormazábal C and Lecanda F: Divergent effects of TGF-β inhibition in bone metastases in breast and lung cancer. Rev Osteoporos Metab Miner. 5:79–84. 2013. View Article : Google Scholar | |
|
Zhu S, Chen W, Masson A and Li YP: Cell signaling and transcriptional regulation of osteoblast lineage commitment, differentiation, bone formation, and homeostasis. Cell Discov. 10:712024. View Article : Google Scholar : PubMed/NCBI | |
|
Gkotzamanidou M, Dimopoulos MA, Kastritis E, Christoulas D, Moulopoulos LA and Terpos E: Sclerostin: A possible target for the management of cancer-induced bone disease. Expert Opin Ther Targets. 16:761–769. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Pinzone JJ, Hall BM, Thudi NK, Vonau M, Qiang YW, Rosol TJ and Shaughnessy JD: The role of Dickkopf-1 in bone development, homeostasis, and disease. Blood. 113:517–525. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Irani S, Salajegheh A, Smith RA and Lam AK: A review of the profile of endothelin axis in cancer and its management. Crit Rev Oncol Hematol. 89:314–321. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Bagnato A, Loizidou M, Pflug BR, Curwen J and Growcott J: Role of the endothelin axis and its antagonists in the treatment of cancer. Br J Pharmacol. 163:220–233. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Xin Z, Qin L, Tang Y, Guo S, Li F, Fang Y, Li G, Yao Y, Zheng B, Zhang B, et al: Immune mediated support of metastasis: Implication for bone invasion. Cancer Commun (Lond). 44:967–991. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Ma X and Yu J: Role of the bone microenvironment in bone metastasis of malignant tumors-therapeutic implications. Cell Oncol (Dordr). 43:751–761. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Baldessari C, Pipitone S, Molinaro E, Cerma K, Fanelli M, Nasso C, Oltrecolli M, Pirola M, D'Agostino E, Pugliese G, et al: Bone metastases and health in prostate cancer: From pathophysiology to clinical implications. Cancers (Basel). 15:15182023. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang X, Jiang P and Wang C: The role of prostate-specific antigen in the osteoblastic bone metastasis of prostate cancer: A literature review. Front Oncol. 13:11276372023. View Article : Google Scholar : PubMed/NCBI | |
|
Yonou H, Horiguchi Y, Ohno Y, Namiki K, Yoshioka K, Ohori M, Hatano T and Tachibana M: Prostate-specific antigen stimulates osteoprotegerin production and inhibits receptor activator of nuclear factor-kappaB ligand expression by human osteoblasts. Prostate. 67:840–848. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Christoph F, König F, Lebentrau S, Jandrig B, Krause H, Strenziok R and Schostak M: RANKL/RANK/OPG cytokine receptor system: mRNA expression pattern in BPH, primary and metastatic prostate cancer disease. World J Urol. 36:187–192. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Kuchimaru T, Hoshino T, Aikawa T, Yasuda H, Kobayashi T, Kadonosono T and Kizaka-Kondoh S: Bone resorption facilitates osteoblastic bone metastatic colonization by cooperation of insulin-like growth factor and hypoxia. Cancer Sci. 105:553–559. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Jin R, Sterling JA, Edwards JR, DeGraff DJ, Lee C, Park SI and Matusik RJ: Activation of NF-kappa B signaling promotes growth of prostate cancer cells in bone. PLoS One. 8:e609832013. View Article : Google Scholar : PubMed/NCBI | |
|
Choi SW, Sun AK, Cheung JP and Ho JC: Circulating tumour cells in the prediction of bone metastasis. Cancers (Basel). 16:2522024. View Article : Google Scholar : PubMed/NCBI | |
|
Roth ES, Fetzer DT, Barron BJ, Joseph UA, Gayed IW and Wan DQ: Does colon cancer ever metastasize to bone first? a temporal analysis of colorectal cancer progression. BMC Cancer. 9:2742009. View Article : Google Scholar : PubMed/NCBI | |
|
Uccella S, Morris JM, Bakkum-Gamez JN, Keeney GL, Podratz KC and Mariani A: Bone metastases in endometrial cancer: Report on 19 patients and review of the medical literature. Gynecol Oncol. 130:474–482. 2013. 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. 1989.PubMed/NCBI | |
|
Elkin M and Vlodavsky I: Tail vein assay of cancer metastasis. Curr Protoc Cell Biol. Chapter 19:19.2.1-19.2.7.2001.doi: 10.1002/0471143030.cb1902s12. View Article : Google Scholar : PubMed/NCBI | |
|
Kuchimaru T, Kataoka N, Nakagawa K, Isozaki T, Miyabara H, Minegishi M, Kadonosono T and Kizaka-Kondoh S: A reliable murine model of bone metastasis by injecting cancer cells through caudal arteries. Nat Commun. 9:29812018. View Article : Google Scholar : PubMed/NCBI | |
|
Neudert M, Fischer C, Krempien B, Bauss F and Seibel MJ: Site-specific human breast cancer (MDA-MB-231) metastases in nude rats: Model characterisation and in vivo effects of ibandronate on tumour growth. Int J Cancer. 107:468–477. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Hoffman RM: Patient-derived orthotopic xenografts: Better mimic of metastasis than subcutaneous xenografts. Nat Rev Cancer. 15:451–452. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Stribbling SM and Ryan AJ: The cell-line-derived subcutaneous tumor model in preclinical cancer research. Nat Protoc. 17:2108–2128. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Farhoodi HP, Segaliny AI, Wagoner ZW, Cheng JL, Liu L and Zhao W: Optimization of a syngeneic murine model of bone metastasis. J Bone Oncol. 23:1002982020. View Article : Google Scholar : PubMed/NCBI | |
|
Winnard PT Jr, Vesuna F, Bol GM, Gabrielson KL, Chenevix-Trench G, Ter Hoeve ND, van Diest PJ and Raman V: Targeting RNA helicase DDX3X with a small molecule inhibitor for breast cancer bone metastasis treatment. Cancer Lett. 604:2172602024. View Article : Google Scholar : PubMed/NCBI | |
|
Han Y, Azuma K, Watanabe S, Semba K and Nakayama J: Metastatic profiling of HER2-positive breast cancer cell lines in xenograft models. Clin Exp Metastasis. 39:467–477. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Ye X, Huang X, Fu X, Zhang X, Lin R, Zhang W, Zhang J and Lu Y: Myeloid-like tumor hybrid cells in bone marrow promote progression of prostate cancer bone metastasis. J Hematol Oncol. 16:462023. View Article : Google Scholar : PubMed/NCBI | |
|
Zhong L, Miller HD, Zhang Y, Jin B, Ge D and You Z: Intra-arterial injection to create bone metastasis of prostate cancer in mice. Am J Clin Exp Urol. 8:93–100. 2020.PubMed/NCBI | |
|
Simmons JK, Dirksen WP, Hildreth BE III, Dorr C, Williams C, Thomas R, Breen M, Toribio RE and Rosol TJ: Canine prostate cancer cell line (Probasco) produces osteoblastic metastases in vivo. Prostate. 74:1251–1265. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Abou DS, Ulmert D, Doucet M, Hobbs RF, Riddle RC and Thorek DL: Whole-Body and microenvironmental localization of Radium-223 in naïve and mouse models of prostate cancer metastasis. J Natl Cancer Inst. 108:djv3802025. View Article : Google Scholar | |
|
Pollard HB, Levine MA, Eidelman O and Pollard M: Pharmacological ascorbic acid suppresses syngeneic tumor growth and metastases in hormone-refractory prostate cancer. In Vivo. 24:249–255. 2010.PubMed/NCBI | |
|
Wang N, Reeves KJ, Brown HK, Fowles AC, Docherty FE, Ottewell PD, Croucher PI, Holen I and Eaton CL: The frequency of osteolytic bone metastasis is determined by conditions of the soil, not the number of seeds; evidence from in vivo models of breast and prostate cancer. J Exp Clin Cancer Res. 34:1242015. View Article : Google Scholar : PubMed/NCBI | |
|
Kaighn ME, Narayan KS, Ohnuki Y, Lechner JF and Jones LW: Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol. 17:16–23. 1979.PubMed/NCBI | |
|
Dai J, Hensel J, Wang N, Kruithof-de Julio M and Shiozawa Y: Mouse models for studying prostate cancer bone metastasis. Bonekey Rep. 5:7772016. View Article : Google Scholar : PubMed/NCBI | |
|
Kozlowski JM, Fidler IJ, Campbell D, Xu ZL, Kaighn ME and Hart IR: Metastatic behavior of human tumor cell lines grown in the nude mouse. Cancer Res. 44:3522–3529. 1984.PubMed/NCBI | |
|
Pettaway CA, Pathak S, Greene G, Ramirez E, Wilson MR, Killion JJ and Fidler IJ: Selection of highly metastatic variants of different human prostatic carcinomas using orthotopic implantation in nude mice. Clin Cancer Res. 2:1627–1636. 1996.PubMed/NCBI | |
|
Stone KR, Mickey DD, Wunderli H, Mickey GH and Paulson DF: Isolation of a human prostate carcinoma cell line (DU 145). Int J Cancer. 21:274–281. 1978. View Article : Google Scholar : PubMed/NCBI | |
|
Horoszewicz JS, Leong SS, Chu TM, Wajsman ZL, Friedman M, Papsidero L, Kim U, Chai LS, Kakati S, Arya SK and Sandberg AA: The LNCaP cell line-a new model for studies on human prostatic carcinoma. Prog Clin Biol Res. 37:115–132. 1980.PubMed/NCBI | |
|
Thalmann GN, Anezinis PE, Chang SM, Zhau HE, Kim EE, Hopwood VL, Pathak S, von Eschenbach AC and Chung LW: Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer. Cancer Res. 54:2577–2581. 1994.PubMed/NCBI | |
|
Sobel RE and Sadar MD: Cell lines used in prostate cancer research: A compendium of old and new lines-part 1. J Urol. 173:342–359. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Guo Q, Jin Y, Lin M, Zeng C and Zhang J: NF-κB signaling in therapy resistance of breast cancer: Mechanisms, approaches, and challenges. Life Sci. 348:1226842024. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou J and Ottewell PD: The role of IL-1B in breast cancer bone metastasis. J Bone Oncol. 46:1006082024. 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 | |
|
Shu ST, Nadella MV, Dirksen WP, Fernandez SA, Thudi NK, Werbeck JL, Lairmore MD and Rosol TJ: A novel bioluminescent mouse model and effective therapy for adult T-cell leukemia/lymphoma. Cancer Res. 67:11859–11866. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Isaacs JT, Heston WD, Weissman RM and Coffey DS: Animal models of the hormone-sensitive and -insensitive prostatic adenocarcinomas, Dunning R-3327-H, R-3327-HI, and R-3327-AT. Cancer Res. 38:4353–4359. 1978.PubMed/NCBI | |
|
Padalecki SS and Guise TA: Actions of bisphosphonates in animal models of breast cancer. Breast Cancer Res. 4:35–41. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Ooi LL, Zheng Y, Zhou H, Trivedi T, Conigrave AD, Seibel MJ and Dunstan CR: Vitamin D deficiency promotes growth of MCF-7 human breast cancer in a rodent model of osteosclerotic bone metastasis. Bone. 47:795–803. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Yin JJ, Mohammad KS, Käkönen SM, Harris S, Wu-Wong JR, Wessale JL, Padley RJ, Garrett IR, Chirgwin JM and Guise TA: A causal role for endothelin-1 in the pathogenesis of osteoblastic bone metastases. Proc Natl Acad Sci USA. 100:10954–10959. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Pulaski BA and Ostrand-Rosenberg S: Mouse 4T1 breast tumor model. Curr Protoc Immunol. Chapter 20: Unit 20.2. 2001.doi: 10.1002/0471142735.im2002s39. PubMed/NCBI | |
|
Pulaski BA and Ostrand-Rosenberg S: Reduction of established spontaneous mammary carcinoma metastases following immunotherapy with major histocompatibility complex class II and B7.1 cell-based tumor vaccines. Cancer Res. 58:1486–1493. 1998.PubMed/NCBI | |
|
Lelekakis M, Moseley JM, Martin TJ, Hards D, Williams E, Ho P, Lowen D, Javni J, Miller FR, Slavin J and Anderson RL: A novel orthotopic model of breast cancer metastasis to bone. Clin Exp Metastasis. 17:163–170. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Coleman RE: Metastatic bone disease: Clinical features, pathophysiology and treatment strategies. Cancer Treat Rev. 27:165–176. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Feeley BT, Liu NQ, Conduah AH, Krenek L, Roth K, Dougall WC, Huard J, Dubinett S and Lieberman JR: Mixed metastatic lung cancer lesions in bone are inhibited by noggin overexpression and Rank:Fc administration. Bone Miner Res. 21:1571–1580. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Miki T, Yano S, Hanibuchi M and Sone S: Bone metastasis model with multiorgan dissemination of human small-cell lung cancer (SBC-5) cells in natural killer cell-depleted SCID mice. Oncol Res. 12:209–127. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Tannehill-Gregg SH, Levine AL, Nadella MV, Iguchi H and Rosol TJ: The effect of zoledronic acid and osteoprotegerin on growth of human lung cancer in the tibias of nude mice. Clin Exp Metastasis. 23:19–31. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Taube T, Beneton MN, McCloskey EV, Rogers S, Greaves M and Kanis JA: Abnormal bone remodelling in patients with myelomatosis and normal biochemical indices of bone resorption. Eur J Haematol. 49:192–198. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Nakano T, Shimizu K, Kawashima O, Kamiyoshihara M, Kakegawa S, Sugano M, Ibe T, Nagashima T, Kaira K, Sunaga N, et al: Establishment of a human lung cancer cell line with high metastatic potential to multiple organs: Gene expression associated with metastatic potential in human lung cancer. Oncol Rep. 28:1727–1735. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Yang S, Dong Q, Yao M, Shi M, Ye J, Zhao L, Su J, Gu W, Xie W, Wang K, et al: Establishment of an experimental human lung adenocarcinoma cell line SPC-A-1BM with high bone metastases potency by (99m)Tc-MDP bone scintigraphy. Nucl Med Biol. 36:313–321. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Gravina GL, Mancini A, Muzi P, Ventura L, Biordi L, Ricevuto E, Pompili S, Mattei C, Di Cesare E, Jannini EA and Festuccia C: CXCR4 pharmacogical inhibition reduces bone and soft tissue metastatic burden by affecting tumor growth and tumorigenic potential in prostate cancer preclinical models. Prostate. 75:1227–1246. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Wu TT, Sikes RA, Cui Q, Thalmann GN, Kao C, Murphy CF, Yang H, Zhau HE, Balian G and Chung LW: Establishing human prostate cancer cell xenografts in bone: Induction of osteoblastic reaction by prostate-specific antigen-producing tumors in athymic and SCID/bg mice using LNCaP and lineage-derived metastatic sublines. Int J Cancer. 77:887–894. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Shevrin DH, Kukreja SC, Ghosh L and Lad TE: Development of skeletal metastasis by human prostate cancer in athymic nude mice. Clin Exp Metastasis. 6:401–409. 1988. View Article : Google Scholar : PubMed/NCBI | |
|
Havens AM, Pedersen EA, Shiozawa Y, Ying C, Jung Y, Sun Y, Neeley C, Wang J, Mehra R, Keller ET, et al: An in vivo mouse model for human prostate cancer metastasis. Neoplasia. 10:371–380. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Yang M, Jiang P, Sun FX, Hasegawa S, Baranov E, Chishima T, Shimada H, Moossa AR and Hoffman RM: A fluorescent orthotopic bone metastasis model of human prostate cancer. Cancer Res. 59:781–786. 1999.PubMed/NCBI | |
|
Fisher JL, Schmitt JF, Howard ML, Mackie PS, Choong PF and Risbridger GP: An in vivo model of prostate carcinoma growth and invasion in bone. Cell Tissue Res. 307:337–345. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Bonfil RD, Dong Z, Trindade Filho JC, Sabbota A, Osenkowski P, Nabha S, Yamamoto H, Chinni SR, Zhao H, Mobashery S, et al: Prostate cancer-associated membrane type 1-matrix metalloproteinase: A pivotal role in bone response and intraosseous tumor growth. Am J Pathol. 170:2100–2111. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Zou M, Jiao J, Zou Q, Xu Y, Cheng M, Xu J and Zhang Y: Multiple metastases in a novel LNCaP model of human prostate cancer. Oncol Rep. 30:615–622. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Corey E, Quinn JE, Bladou F, Brown LG, Roudier MP, Brown JM, Buhler KR and Vessella RL: Establishment and characterization of osseous prostate cancer models: Intra-tibial injection of human prostate cancer cells. Prostate. 52:20–33. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Jantscheff P, Ziroli V, Esser N, Graeser R, Kluth J, Sukolinskaya A, Taylor LA, Unger C and Massing U: Anti-metastatic effects of liposomal gemcitabine in a human orthotopic LNCaP prostate cancer xenograft model. Clin Exp Metastasis. 26:981–992. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Wetterwald A, van der Pluijm G, Que I, Sijmons B, Buijs J, Karperien M, Löwik CW, Gautschi E, Thalmann GN and Cecchini MG: Optical imaging of cancer metastasis to bone marrow: A mouse model of minimal residual disease. Am J Pathol. 160:1143–1153. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Sasaki SI, Zhang D, Iwabuchi S, Tanabe Y, Hashimoto S, Yamauchi A, Hayashi K, Tsuchiya H, Hayakawa Y, Baba T and Mukaida N: Crucial contribution of GPR56/ADGRG1, expressed by breast cancer cells, to bone metastasis formation. Cancer Sci. 112:4883–4893. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Kim B, Kim H, Jung S, Moon A, Noh DY, Lee ZH, Kim HJ and Kim HH: A CTGF-RUNX2-RANKL axis in breast and prostate cancer cells promotes tumor progression in bone. J Bone Miner Res. 35:155–166. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Yoneda T, Michigami T, Yi B, Williams PJ, Niewolna M and Hiraga T: Actions of bisphosphonate on bone metastasis in animal models of breast carcinoma. Cancer. 88:2979–2988. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Yi B, Williams PJ, Niewolna M, Wang Y and Yoneda T: Tumor-derived platelet-derived growth factor-BB plays a critical role in osteosclerotic bone metastasis in an animal model of human breast cancer. Cancer Res. 62:917–923. 2002.PubMed/NCBI | |
|
Sun J, Huang J, Lan J, Zhou K, Gao Y, Song Z, Deng Y, Liu L, Dong Y and Liu X: Overexpression of CENPF correlates with poor prognosis and tumor bone metastasis in breast cancer. Cancer Cell Int. 19:2642019. View Article : Google Scholar : PubMed/NCBI | |
|
Hung JY, Horn D, Woodruff K, Prihoda T, LeSaux C, Peters J, Tio F and Abboud-Werner SL: Colony-stimulating factor 1 potentiates lung cancer bone metastasis. Lab Invest. 94:371–381. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Liu H, Cheng Q, Xu DS, Wang W, Fang Z, Xue DD, Zheng Y, Chang AH and Lei YJ: Overexpression of CXCR7 accelerates tumor growth and metastasis of lung cancer cells. Respir Res. 21:2872020. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Q, Zhao B, Li J, Zhao J, Wang C, Li Q, Yang W, Xu L and Gong Y: Qilian formula inhibits tumor cell growth in a bone metastasis model of lung cancer. Integr Cancer Ther. 22:153473542312172742023. View Article : Google Scholar : PubMed/NCBI |
