Understanding the Osteosarcoma Pathobiology: A Comparative Oncology Approach
Abstract
:1. Introduction
2. Human Osteosarcoma
3. Canine Osteosarcoma
4. Mouse Models of Osteosarcoma
5. Conserved Drivers of Osteosarcoma
5.1. Genomic Alterations
5.2. Deregulation of Micrornas in Canine and Human Osteosarcoma
miRNAs Deregulated in OS | Expression Levels Compared to the Controls | Overall Function | References |
---|---|---|---|
miR-382 | Down-regulated | Poor survival outcome and metastasis marker | [70,83] |
miR-154 | Down-regulated | Poor survival outcome | [70] |
miR-33a | Up-regulated | Chemoresistance | [84] |
miR-34c | Down-regulated | Chemoresistance | [85] |
5.3. Epigenetic Changes in Osteosarcoma
6. Advantages of A Multi-Species, Comparative Osteosarcoma Study Approach
7. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Moore, D.D.; Luu, H.H. Osteosarcoma. Cancer Treat Res. 2014, 162, 65–92. [Google Scholar] [PubMed]
- Ottaviani, G.; Jaffe, N. The epidemiology of osteosarcoma. Cancer Treat Res. 2009, 152, 3–13. [Google Scholar] [PubMed]
- Letson, G.D.; Muro-Cacho, C.A. Genetic and molecular abnormalities in tumors of the bone and soft tissues. Cancer Control 2001, 8, 239–251. [Google Scholar] [PubMed]
- Karlsson, E.K.; Sigurdsson, S.; Ivansson, E.; Thomas, R.; Elvers, I.; Wright, J.; Howald, C.; Tonomura, N.; Perloski, M.; Swofford, R.; et al. Genome-wide analyses implicate 33 loci in heritable dog osteosarcoma, including regulatory variants near CDKN2A/B. Genome Biol. 2013, 14, R132. [Google Scholar] [CrossRef] [PubMed]
- Mutsaers, A.J.; Walkley, C.R. Cells of origin in osteosarcoma: Mesenchymal stem cells or osteoblast committed cells? Bone 2014, 62, 56–63. [Google Scholar] [CrossRef] [PubMed]
- Quist, T.; Jin, H.; Zhu, J.F.; Smith-Fry, K.; Capecchi, M.R.; Jones, K.B. The impact of osteoblastic differentiation on osteosarcomagenesis in the mouse. Oncogene 2015, 34, 4278–4284. [Google Scholar] [CrossRef] [PubMed]
- Yoshida, H.; Adachi, H.; Hamada, Y.; Aki, T.; Yumoto, T.; Morimoto, K.; Orido, T. Osteosarcoma. Ultrastructural and immunohistochemical studies on alkaline phosphatase-positive tumor cells constituting a variety of histologic types. Acta Pathol. Jpn. 1988, 38, 325–338. [Google Scholar] [CrossRef] [PubMed]
- Dirik, Y.; Cinar, A.; Yumrukcal, F.; Eralp, L. Popliteal lymph node metastasis of tibial osteoblastic osteosarcoma. Int. J. Surg. Case Rep. 2014, 5, 840–844. [Google Scholar] [CrossRef] [PubMed]
- Jeffree, G.M.; Price, C.H.; Sissons, H.A. The metastatic patterns of osteosarcoma. Brit. J. Cancer 1975, 32, 87–107. [Google Scholar] [CrossRef] [PubMed]
- Morello, E.; Martano, M.; Buracco, P. Biology, diagnosis and treatment of canine appendicular osteosarcoma: Similarities and differences with human osteosarcoma. Vet. J. 2011, 189, 268–277. [Google Scholar] [CrossRef] [PubMed]
- Gill, J.; Ahluwalia, M.K.; Geller, D.; Gorlick, R. New targets and approaches in osteosarcoma. Pharmacol. Ther. 2013, 137, 89–99. [Google Scholar] [CrossRef] [PubMed]
- Jaffe, N. Osteosarcoma: Review of the past, impact on the future. The American experience. Cancer Treat Res. 2009, 152, 239–262. [Google Scholar] [PubMed]
- Modiano, J.F.; Breen, M.; Lana, S.E.; Ehrhart, N.; Fosmire, S.P.; Thomas, R.; Jubala, C.M.; Lamerato-Kozicki, A.R.; Ehrhart, E.J.; Schaack, J.; et al. Naturally occurring translational models for development of cancer therapy. Gene Ther. Mol. Biol. 2006, 10, 31–40. [Google Scholar]
- Scott, M.C.; Sarver, A.L.; Gavin, K.J.; Thayanithy, V.; Getzy, D.M.; Newman, R.A.; Cutter, G.R.; Lindblad-Toh, K.; Kisseberth, W.C.; Hunter, L.E.; et al. Molecular subtypes of osteosarcoma identified by reducing tumor heterogeneity through an interspecies comparative approach. Bone 2011, 49, 356–367. [Google Scholar] [CrossRef] [PubMed]
- Paoloni, M.; Davis, S.; Lana, S.; Withrow, S.; Sangiorgi, L.; Picci, P.; Hewitt, S.; Triche, T.; Meltzer, P.; Khanna, C. Canine tumor cross-species genomics uncovers targets linked to osteosarcoma progression. BMC Genom. 2009, 10, 625. [Google Scholar] [CrossRef] [PubMed]
- Schiffman, J.D.; Breen, M. Comparative oncology: What dogs and other species can teach us about humans with cancer. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2015, 370. [Google Scholar] [CrossRef] [PubMed]
- Thomas, R.; Wang, H.J.; Tsai, P.C.; Langford, C.F.; Fosmire, S.P.; Jubala, C.M.; Getzy, D.M.; Cutter, G.R.; Modiano, J.F.; Breen, M. Influence of genetic background on tumor karyotypes: Evidence for breed-associated cytogenetic aberrations in canine appendicular osteosarcoma. Chromosome Res. 2009, 17, 365–377. [Google Scholar] [CrossRef] [PubMed]
- McNeill, C.J.; Overley, B.; Shofer, F.S.; Kent, M.S.; Clifford, C.A.; Samluk, M.; Haney, S.; van Winkle, T.J.; Sorenmo, K.U. Characterization of the biological behaviour of appendicular osteosarcoma in Rottweilers and a comparison with other breeds: A review of 258 dogs. Vet. Comp. Oncol. 2007, 5, 90–98. [Google Scholar] [CrossRef] [PubMed]
- Dobson, J.M. Breed-predispositions to cancer in pedigree dogs. ISRN Vet. Sci. 2013, 2013, 941275. [Google Scholar] [CrossRef] [PubMed]
- Paoloni, M.; Khanna, C. Translation of new cancer treatments from pet dogs to humans. Nat. Rev. Cancer 2008, 8, 147–156. [Google Scholar] [CrossRef] [PubMed]
- Isakoff, M.S.; Bielack, S.S.; Meltzer, P.; Gorlick, R. Osteosarcoma: Current treatment and a collaborative pathway to success. J. Clin. Oncol. 2015, 33, 3029–3035. [Google Scholar] [CrossRef] [PubMed]
- Ferrari, S.; Serra, M. An update on chemotherapy for osteosarcoma. Expert Opin. Pharmacother. 2015, 16, 2727–2736. [Google Scholar] [CrossRef] [PubMed]
- Perry, J.A.; Kiezun, A.; Tonzi, P.; van Allen, E.M.; Carter, S.L.; Baca, S.C.; Cowley, G.S.; Bhatt, A.S.; Rheinbay, E.; Pedamallu, C.S.; et al. Complementary genomic approaches highlight the PI3K/mTOR pathway as a common vulnerability in osteosarcoma. Proc. Natl. Acad. Sci. USA 2014, 111, 5564–5573. [Google Scholar] [CrossRef] [PubMed]
- Morrow, J.J.; Khanna, C. Osteosarcoma genetics and epigenetics: Emerging biology and candidate therapies. Crit. Rev. Oncog. 2015, 20, 173–197. [Google Scholar] [CrossRef] [PubMed]
- Li, N.; Luo, D.; Hu, X.; Luo, W.; Lei, G.; Wang, Q.; Zhu, T.; Gu, J.; Lu, Y.; Zheng, Q. RUNX2 and osteosarcoma. Anticancer Agents Med. Chem. 2015, 15, 881–887. [Google Scholar] [CrossRef] [PubMed]
- Tian, J.; He, H.; Lei, G. Wnt/beta-catenin pathway in bone cancers. Tumour Biol. 2014, 35, 9439–9445. [Google Scholar] [CrossRef] [PubMed]
- Lamora, A.; Talbot, J.; Bougras, G.; Amiaud, J.; Leduc, M.; Chesneau, J.; Taurelle, J.; Stresing, V.; Le Deley, M.C.; Heymann, M.F.; et al. Overexpression of smad7 blocks primary tumor growth and lung metastasis development in osteosarcoma. Clin. Cancer Res. 2014, 20, 5097–5112. [Google Scholar] [CrossRef] [PubMed]
- Khanna, C.; Wan, X.; Bose, S.; Cassaday, R.; Olomu, O.; Mendoza, A.; Yeung, C.; Gorlick, R.; Hewitt, S.M.; Helman, L.J. The membrane-cytoskeleton linker ezrin is necessary for osteosarcoma metastasis. Nat. Med. 2004, 10, 182–186. [Google Scholar] [CrossRef] [PubMed]
- Moriarity, B.S.; Otto, G.M.; Rahrmann, E.P.; Rathe, S.K.; Wolf, N.K.; Weg, M.T.; Manlove, L.A.; LaRue, R.S.; Temiz, N.A. A Sleeping Beauty forward genetic screen identifies new genes and pathways driving osteosarcoma development and metastasis. 2015, 47, 615–624. [Google Scholar] [CrossRef] [PubMed]
- Chang, L.; Shrestha, S.; LaChaud, G.; Scott, M.A.; James, A.W. Review of microRNA in osteosarcoma and chondrosarcoma. Med. Oncol. 2015, 32, 613. [Google Scholar] [CrossRef] [PubMed]
- Geller, D.S.; Gorlick, R. Osteosarcoma: A review of diagnosis, management, and treatment strategies. Clin. Adv. Hematol. Oncol. 2010, 8, 705–718. [Google Scholar] [PubMed]
- Mirabello, L.; Pfeiffer, R.; Murphy, G.; Daw, N.C.; Patino-Garcia, A.; Troisi, R.J.; Hoover, R.N.; Douglass, C.; Schuz, J.; Craft, A.W.; et al. Height at diagnosis and birth-weight as risk factors for osteosarcoma. Cancer Causes Control 2011, 22, 899–908. [Google Scholar] [CrossRef] [PubMed]
- Savage, S.A.; Woodson, K.; Walk, E.; Modi, W.; Liao, J.; Douglass, C.; Hoover, R.N.; Chanock, S.J. Analysis of genes critical for growth regulation identifies Insulin-like Growth Factor 2 Receptor variations with possible functional significance as risk factors for osteosarcoma. Cancer Epidemiol. Biomark. Prev. 2007, 16, 1667–1674. [Google Scholar] [CrossRef] [PubMed]
- Miller, R.W. Contrasting epidemiology of childhood osteosarcoma, Ewing's tumor, and rhabdomyosarcoma. Natl. Cancer Inst. Monogr. 1981, 56, 9–15. [Google Scholar] [PubMed]
- Jawad, M.U.; Cheung, M.C.; Min, E.S.; Schneiderbauer, M.M.; Koniaris, L.G.; Scully, S.P. Ewing sarcoma demonstrates racial disparities in incidence-related and sex-related differences in outcome: An analysis of 1631 cases from the SEER database, 1973–2005. Cancer 2009, 115, 3526–3536. [Google Scholar] [CrossRef] [PubMed]
- Savage, S.A.; Mirabello, L.; Wang, Z.; Gastier-Foster, J.M.; Gorlick, R.; Khanna, C.; Flanagan, A.M.; Tirabosco, R.; Andrulis, I.L.; Wunder, J.S.; et al. Genome-wide association study identifies two susceptibility loci for osteosarcoma. Nat. Genet. 2013, 45, 799–803. [Google Scholar] [CrossRef] [PubMed]
- Mirabello, L.; Koster, R.; Moriarity, B.S.; Spector, L.G.; Meltzer, P.S.; Gary, J.; Machiela, M.J.; Pankratz, N.; Panagiotou, O.A.; Largaespada, D.; et al. A Genome-wide scan identifies variants in NFIB associated with metastasis in patients with osteosarcoma. Cancer Discov. 2015, 5, 920–931. [Google Scholar] [CrossRef] [PubMed]
- Gorlick, R.; Khanna, C. Osteosarcoma. J. Bone Miner. Res. 2010, 25, 683–691. [Google Scholar] [CrossRef] [PubMed]
- Hameed, M.; Dorfman, H. Primary malignant bone tumors—Recent developments. Semin. Diagn. Pathol. 2011, 28, 86–101. [Google Scholar] [CrossRef] [PubMed]
- Anfinsen, K.P.; Grotmol, T.; Bruland, O.S.; Jonasdottir, T.J. Breed-specific incidence rates of canine primary bone tumors—A population based survey of dogs in Norway. Can. J. Vet. Res. 2011, 75, 209–215. [Google Scholar] [PubMed]
- Liptak, J.M.; Dernell, W.S.; Straw, R.C.; Rizzo, S.A.; Lafferty, M.H.; Withrow, S.J. Proximal radial and distal humeral osteosarcoma in 12 dogs. J. Am. Anim. Hosp. Assoc. 2004, 40, 461–467. [Google Scholar] [CrossRef] [PubMed]
- Boerman, I.; Selvarajah, G.T.; Nielen, M.; Kirpensteijn, J. Prognostic factors in canine appendicular osteosarcoma—A meta-analysis. BMC Vet. Res. 2012, 8, 56–56. [Google Scholar] [CrossRef] [PubMed]
- Fenger, J.M.; London, C.A.; Kisseberth, W.C. Canine osteosarcoma: A naturally occurring disease to inform pediatric oncology. ILAR J. 2014, 55, 69–85. [Google Scholar] [CrossRef] [PubMed]
- Szewczyk, M.; Lechowski, R.; Zabielska, K. What do we know about canine osteosarcoma treatment? Review. Vet. Res. Commun. 2015, 39, 61–67. [Google Scholar] [CrossRef] [PubMed]
- Berg, J. Canine osteosarcoma: Amputation and chemotherapy. Vet. Clin. N. Am. Small Anim. Pract. 1996, 26, 111–121. [Google Scholar] [CrossRef]
- Straw, R.C.; Withrow, S.J.; Powers, B.E. Management of canine appendicular osteosarcoma. Vet. Clin. North Am. Small Anim. Pract. 1990, 20, 1141–1161. [Google Scholar] [CrossRef]
- Gilson, S.D. Principles of surgery for cancer palliation and treatment of metastases. Clin. Tech. Small Anim. Pract. 1998, 13, 65–69. [Google Scholar] [CrossRef]
- Guijarro, M.V.; Ghivizzani, S.C.; Gibbs, C.P. Animal models in osteosarcoma. Front. Oncol. 2014, 4, 189. [Google Scholar] [PubMed]
- Ruther, U.; Komitowski, D.; Schubert, F.R.; Wagner, E.F. c-fos expression induces bone tumors in transgenic mice. Oncogene 1989, 4, 861–865. [Google Scholar] [PubMed]
- Entz-Werle, N.; Choquet, P.; Neuville, A.; Kuchler-Bopp, S.; Clauss, F.; Danse, J.M.; Simo-Noumbissie, P.; Guerin, E.; Gaub, M.P.; Freund, J.N.; et al. Targeted apc;twist double-mutant mice: A new model of spontaneous osteosarcoma that mimics the human disease. Transl. Oncol. 2010, 3, 344–353. [Google Scholar] [CrossRef] [PubMed]
- Walkley, C.R.; Qudsi, R.; Sankaran, V.G.; Perry, J.A.; Gostissa, M.; Roth, S.I.; Rodda, S.J.; Snay, E.; Dunning, P.; Fahey, F.H.; et al. Conditional mouse osteosarcoma, dependent on p53 loss and potentiated by loss of Rb, mimics the human disease. Genes Dev 2008, 22, 1662–1676. [Google Scholar] [CrossRef] [PubMed]
- Rao, P.H.; Zhao, S.; Zhao, Y.J.; Yu, A.; Rainusso, N.; Trucco, M.; Allen-Rhoades, W.; Satterfield, L.; Fuja, D.; Borra, V.J.; et al. Coamplification of Myc/Pvt1 and homozygous deletion of Nlrp1 locus are frequent genetics changes in mouse osteosarcoma. Genes Chromosomes Cancer 2015, 54, 796–808. [Google Scholar] [CrossRef] [PubMed]
- Mohseny, A.B.; Hogendoorn, P.C.; Cleton-Jansen, A.M. Osteosarcoma models: From cell lines to zebrafish. Sarcoma 2012, 2012, 417271. [Google Scholar] [CrossRef] [PubMed]
- Merchant, M.S.; Melchionda, F.; Sinha, M.; Khanna, C.; Helman, L.; Mackall, C.L. Immune reconstitution prevents metastatic recurrence of murine osteosarcoma. Cancer Immunol. Immunother. 2007, 56, 1037–1046. [Google Scholar] [CrossRef] [PubMed]
- Olive, K.P.; Tuveson, D.A.; Ruhe, Z.C.; Yin, B.; Willis, N.A.; Bronson, R.T.; Crowley, D.; Jacks, T. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004, 119, 847–860. [Google Scholar] [CrossRef] [PubMed]
- Angstadt, A.Y.; Thayanithy, V.; Subramanian, S.; Modiano, J.F.; Breen, M. A genome-wide approach to comparative oncology: High-resolution oligonucleotide aCGH of canine and human osteosarcoma pinpoints shared microaberrations. Cancer Genet. 2012, 205, 572–587. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Bahrami, A.; Pappo, A.; Easton, J.; Dalton, J.; Hedlund, E.; Ellison, D.; Shurtleff, S.; Wu, G.; Wei, L.; et al. Recurrent somatic structural variations contribute to tumorigenesis in pediatric osteosarcoma. Cell Rep. 2014, 7, 104–112. [Google Scholar] [CrossRef] [PubMed]
- Scott, M.C.; Sarver, A.L.; Tomiyasu, H.; Cornax, I.; van Etten, J.; Varshney, J.; O'Sullivan, M.G.; Subramanian, S.; Modiano, J.F. Aberrant RB-E2F transcriptional regulation defines molecular phenotypes of osteosarcoma. J. Biol. Chem. 2015. [Google Scholar] [CrossRef] [PubMed]
- Ren, W.; Gu, G. Prognostic implications of RB1 tumour suppressor gene alterations in the clinical outcome of human osteosarcoma: A meta-analysis. Eur. J. Cancer Care 2015. [Google Scholar] [CrossRef] [PubMed]
- Sampson, V.B.; Yoo, S.; Kumar, A.; Vetter, N.S.; Kolb, E.A. MicroRNAs and potential targets in osteosarcoma: Review. Front. Pediatr. 2015, 3, 69. [Google Scholar] [PubMed]
- Zhang, J.; Yan, Y.G.; Wang, C.; Zhang, S.J.; Yu, X.H.; Wang, W.J. MicroRNAs in osteosarcoma. Clin. Chim. Acta 2015, 444, 9–17. [Google Scholar] [CrossRef] [PubMed]
- Miao, J.; Wu, S.; Peng, Z.; Tania, M.; and Zhang, C. MicroRNAs in osteosarcoma: Diagnostic and therapeutic aspects. Tumour Biol. 2013, 34, 2093–2098. [Google Scholar] [CrossRef] [PubMed]
- Zhou, G.; Shi, X.; Zhang, J.; Wu, S.; Zhao, J. MicroRNAs in osteosarcoma: From biological players to clinical contributors, a review. J. Int. Med. Res. 2013, 41, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Zhang, J.; Zhang, L.; Si, M.; Yin, H.; Li, J. Diallyl trisulfide inhibits proliferation, invasion and angiogenesis of osteosarcoma cells by switching on suppressor microRNAs and inactivating of Notch-1 signaling. Carcinogenesis 2013, 34, 1601–1610. [Google Scholar] [CrossRef] [PubMed]
- Sarver, A.L.; Thayanithy, V.; Scott, M.C.; Cleton-Jansen, A.M.; Hogendoorn, P.C.; Modiano, J.F.; Subramanian, S. MicroRNAs at the human 14q32 locus have prognostic significance in osteosarcoma. Orphanet J. Rare Dis. 2013, 8, 7. [Google Scholar] [CrossRef] [PubMed]
- Namlos, H.M.; Meza-Zepeda, L.A.; Baroy, T.; Ostensen, I.H.; Kresse, S.H.; Kuijjer, M.L.; Serra, M.; Burger, H.; Cleton-Jansen, A.M.; Myklebost, O. Modulation of the osteosarcoma expression phenotype by microRNAs. PloS ONE 2012, 7, e48086. [Google Scholar] [CrossRef] [PubMed]
- Lulla, R.R.; Costa, F.F.; Bischof, J.M.; Chou, P.M.; de, F.B.M.; Vanin, E.F.; Soares, M.B. Identification of differentially expressed MicroRNAs in osteosarcoma. Sarcoma 2011, 2011, 732690. [Google Scholar] [CrossRef] [PubMed]
- Varshney, J.; Subramanian, S. MicroRNAs as potential target in human bone and soft tissue sarcoma therapeutics. Front. Mol. Biosci. 2015, 2, 31. [Google Scholar] [CrossRef] [PubMed]
- Sarver, A.L.; Phalak, R.; Thayanithy, V.; Subramanian, S. S-MED: Sarcoma microRNA expression database. Lab. Investig. J. Tech. Methods Pathol. 2010, 90, 753–761. [Google Scholar] [CrossRef] [PubMed]
- Thayanithy, V.; Sarver, A.L.; Kartha, R.V.; Li, L.; Angstadt, A.Y.; Breen, M.; Steer, C.J.; Modiano, J.F.; Subramanian, S. Perturbation of 14q32 miRNAs-cMYC gene network in osteosarcoma. Bone 2012, 50, 171–181. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Choi, P.S.; Casey, S.C.; Dill, D.L.; Felsher, D.W. MYC through miR-17–92 suppresses specific target genes to maintain survival, autonomous proliferation, and a neoplastic state. Cancer Cell 2014, 26, 262–272. [Google Scholar] [CrossRef] [PubMed]
- Schaap-Oziemlak, A.M.; Raymakers, R.A.; Bergevoet, S.M.; Gilissen, C.; Jansen, B.J.; Adema, G.J.; Kogler, G.; le Sage, C.; Agami, R.; van der Reijden, B.A.; et al. MicroRNA hsa-miR-135b regulates mineralization in osteogenic differentiation of human unrestricted somatic stem cells. Stem. Cells Dev. 2010, 19, 877–885. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wei, J.Q.; Chen, H.; Zheng, X.F.; Zhang, B.X.; Wang, Y.; Tang, P.F.; She, F.; Song, Q.; Li, T.S. Hsa-miR-654–5p regulates osteogenic differentiation of human bone marrow mesenchymal stem cells by repressing bone morphogenetic protein 2. J. Southern Med. Univ. 2012, 32, 291–295. [Google Scholar]
- Fang, S.; Deng, Y.; Gu, P.; Fan, X. MicroRNAs regulate bone development and regeneration. Int. J. Mol. Sci. 2015, 16, 8227–8253. [Google Scholar] [CrossRef] [PubMed]
- Inose, H.; Ochi, H.; Kimura, A.; Fujita, K.; Xu, R.; Sato, S.; Iwasaki, M.; Sunamura, S.; Takeuchi, Y.; Fukumoto, S.; et al. A microRNA regulatory mechanism of osteoblast differentiation. Proc. Natl. Acad. Sci. USA 2009, 106, 20794–20799. [Google Scholar] [CrossRef] [PubMed]
- Feng, Z.; Zhang, C.; Wu, R.; Hu, W. Tumor suppressor p53 meets microRNAs. J. Mol. Cell Biol. 2011, 3, 44–50. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Jia, L.S.; Yuan, W.; Wu, Z.; Wang, H.B.; Xu, T.; Sun, J.C.; Cheng, K.F.; Shi, J.G. Low miR-34a and miR-192 are associated with unfavorable prognosis in patients suffering from osteosarcoma. Am. J. Transl. Res. 2015, 7, 111–119. [Google Scholar] [PubMed]
- Zhao, H.; Ma, B.; Wang, Y.; Han, T.; Zheng, L.; Sun, C.; Liu, T.; Zhang, Y.; Qiu, X.; Fan, Q. miR-34a inhibits the metastasis of osteosarcoma cells by repressing the expression of CD44. Oncol. Rep. 2013, 29, 1027–1036. [Google Scholar] [PubMed]
- He, C.; Xiong, J.; Xu, X.; Lu, W.; Liu, L.; Xiao, D.; Wang, D. Functional elucidation of MiR-34 in osteosarcoma cells and primary tumor samples. Biochem. Biophys. Res. Commun. 2009, 388, 35–40. [Google Scholar] [CrossRef] [PubMed]
- Pazzaglia, L.; Leonardi, L.; Conti, A.; Novello, C.; Quattrini, I.; Montanini, L.; Roperto, F.; del Piero, F.; di Guardo, G.; Piro, F.; et al. miR-196a expression in human and canine osteosarcomas: A comparative study. Res. Vet. Sci. 2015, 99, 112–119. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Zhang, C.; Chen, H.; Li, L.; Tu, Y.; Liu, C.; Shi, S.; Zen, K.; Liu, Z. Evaluation of microRNAs miR-196a, miR-30a-5P, and miR-490 as biomarkers of disease activity among patients with FSGS. Clin. J. Am. Soc. Nephrol. 2014, 9, 1545–1552. [Google Scholar] [CrossRef] [PubMed]
- Gardner, H.L.; Fenger, J.M.; London, C.A. Dogs as a model for cancer. Annu. Rev. Anim. Biosci. 2015. in print. [Google Scholar] [CrossRef] [PubMed]
- Xu, M.; Jin, H.; Xu, C.X.; Sun, B.; Song, Z.G.; Bi, W.Z.; Wang, Y. miR-382 inhibits osteosarcoma metastasis and relapse by targeting Y box-binding protein 1. Mol. Ther. 2015, 23, 89–98. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.; Huang, Z.; Wu, S.; Zang, X.; Liu, M.; Shi, J. miR-33a is up-regulated in chemoresistant osteosarcoma and promotes osteosarcoma cell resistance to cisplatin by down-regulating TWIST. J. Exp. Clin. Cancer Res. 2014, 33, 12. [Google Scholar] [CrossRef] [PubMed]
- Xu, M.; Jin, H.; Xu, C.X.; Bi, W.Z.; Wang, Y. MiR-34c inhibits osteosarcoma metastasis and chemoresistance. Med. Oncol. 2014, 31, 972. [Google Scholar] [CrossRef] [PubMed]
- Rosenblum, J.M.; Wijetunga, N.A.; Fazzari, M.J.; Krailo, M.; Barkauskas, D.A.; Gorlick, R.; Greally, J.M. Predictive properties of DNA methylation patterns in primary tumor samples for osteosarcoma relapse status. Epigenetics 2015, 10, 31–39. [Google Scholar] [CrossRef] [PubMed]
- Kresse, S.H.; Rydbeck, H.; Skarn, M.; Namlos, H.M.; Barragan-Polania, A.H.; Cleton-Jansen, A.M.; Serra, M.; Liestol, K.; Hogendoorn, P.C.; Hovig, E.; et al. Integrative analysis reveals relationships of genetic and epigenetic alterations in osteosarcoma. PLoS ONE 2012, 7, e48262. [Google Scholar] [CrossRef] [PubMed]
- Oh, J.H.; Kim, H.S.; Kim, H.H.; Kim, W.H.; Lee, S.H. Aberrant methylation of p14ARF gene correlates with poor survival in osteosarcoma. Clin. Orthop. Relat. Res. 2006, 442, 216–222. [Google Scholar] [CrossRef] [PubMed]
- Park, Y.B.; Park, M.J.; Kimura, K.; Shimizu, K.; Lee, S.H.; Yokota, J. Alterations in the INK4a/ARF locus and their effects on the growth of human osteosarcoma cell lines. Cancer Genet. Cytogenet. 2002, 133, 105–111. [Google Scholar] [CrossRef]
- Al-Romaih, K.; Sadikovic, B.; Yoshimoto, M.; Wang, Y.; Zielenska, M.; Squire, J.A. Decitabine-induced demethylation of 5′ CpG island in GADD45A leads to apoptosis in osteosarcoma cells. Neoplasia 2008, 10, 471–480. [Google Scholar] [CrossRef] [PubMed]
- Badal, V.; Menendez, S.; Coomber, D.; Lane, D.P. Regulation of the p14ARF promoter by DNA methylation. Cell Cycle 2008, 7, 112–119. [Google Scholar] [CrossRef] [PubMed]
- Chen, W.; Cooper, T.K.; Zahnow, C.A.; Overholtzer, M.; Zhao, Z.; Ladanyi, M.; Karp, J.E.; Gokgoz, N.; Wunder, J.S.; Andrulis, I.L.; et al. Epigenetic and genetic loss of Hic1 function accentuates the role of p53 in tumorigenesis. Cancer Cell 2004, 6, 387–398. [Google Scholar] [CrossRef] [PubMed]
- Lu, J.; Song, G.; Tang, Q.; Zou, C.; Han, F.; Zhao, Z.; Yong, B.; Yin, J.; Xu, H.; Xie, X.; et al. IRX1 hypomethylation promotes osteosarcoma metastasis via induction of CXCL14/NF-kappaB signaling. J. Clin. Investig. 2015, 125, 1839–1856. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Meng, G.; Huang, L.; Guo, Q.N. Hypomethylation of the P3 promoter is associated with up-regulation of IGF2 expression in human osteosarcoma. Hum. Pathol. 2009, 40, 1441–1447. [Google Scholar] [CrossRef] [PubMed]
- Ulaner, G.A.; Vu, T.H.; Li, T.; Hu, J.F.; Yao, X.M.; Yang, Y.; Gorlick, R.; Meyers, P.; Healey, J.; Ladanyi, M.; et al. Loss of imprinting of IGF2 and H19 in osteosarcoma is accompanied by reciprocal methylation changes of a CTCF-binding site. Hum. Mol. Genet. 2003, 12, 535–549. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Meng, G.; Guo, Q.N. Changes in genomic imprinting and gene expression associated with transformation in a model of human osteosarcoma. Exp. Mol. Pathol. 2008, 84, 234–239. [Google Scholar] [CrossRef] [PubMed]
- Lee, D.F.; Su, J.; Kim, H.S.; Chang, B.; Papatsenko, D.; Zhao, R.; Yuan, Y.; Gingold, J.; Xia, W.; Darr, H.; et al. Modeling familial cancer with induced pluripotent stem cells. Cell 2015, 161, 240–254. [Google Scholar] [CrossRef] [PubMed]
- Thayanithy, V.; Park, C.; Sarver, A.L.; Kartha, R.V.; Korpela, D.M.; Graef, A.J.; Steer, C.J.; Modiano, J.F.; Subramanian, S. Combinatorial treatment of DNA and chromatin-modifying drugs cause cell death in human and canine osteosarcoma cell lines. PLoS ONE 2012, 7, e43720. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.; Cruz, F.D.; Terry, M.; Remotti, F.; Matushansky, I. Terminal differentiation and loss of tumorigenicity of human cancers via pluripotency-based reprogramming. Oncogene 2013, 32, 2249–2260. [Google Scholar] [CrossRef] [PubMed]
- Maniscalco, L. Canine osteosarcoma: Understanding its variability to improve treatment. Vet. J. 2015, 203, 135–136. [Google Scholar] [CrossRef] [PubMed]
- Rodriguez, C.O., Jr. Using canine osteosarcoma as a model to assess efficacy of novel therapies: Can old dogs teach us new tricks? Adv. Exp. Med. Biol. 2014, 804, 237–256. [Google Scholar] [PubMed]
- Modiano, J.F.; Bellgrau, D.; Cutter, G.R.; Lana, S.E.; Ehrhart, N.P.; Ehrhart, E.; Wilke, V.L.; Charles, J.B.; Munson, S.; Scott, M.C.; et al. Inflammation, apoptosis, and necrosis induced by neoadjuvant fas ligand gene therapy improves survival of dogs with spontaneous bone cancer. Mol. Ther. 2012, 20, 2234–2243. [Google Scholar] [CrossRef] [PubMed]
© 2016 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons by Attribution (CC-BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Varshney, J.; Scott, M.C.; Largaespada, D.A.; Subramanian, S. Understanding the Osteosarcoma Pathobiology: A Comparative Oncology Approach. Vet. Sci. 2016, 3, 3. https://doi.org/10.3390/vetsci3010003
Varshney J, Scott MC, Largaespada DA, Subramanian S. Understanding the Osteosarcoma Pathobiology: A Comparative Oncology Approach. Veterinary Sciences. 2016; 3(1):3. https://doi.org/10.3390/vetsci3010003
Chicago/Turabian StyleVarshney, Jyotika, Milcah C. Scott, David A. Largaespada, and Subbaya Subramanian. 2016. "Understanding the Osteosarcoma Pathobiology: A Comparative Oncology Approach" Veterinary Sciences 3, no. 1: 3. https://doi.org/10.3390/vetsci3010003