Canine tumor cross-species genomics uncovers targets linked to osteosarcoma progression
Open accessAbstract
BACKGROUND: Pulmonary metastasis continues to be the most common cause of death in osteosarcoma. Indeed, the 5-year survival for newly diagnosed osteosarcoma patients has not significantly changed in over 20 years. Further understanding of the mechanisms of metastasis and resistance for this aggressive pediatric cancer is necessary. Pet dogs naturally develop osteosarcoma providing a novel opportunity to model metastasis development and progression. Given the accelerated biology of canine osteosarcoma, we hypothesized that a direct comparison of canine and pediatric osteosarcoma expression profiles may help identify novel metastasis-associated tumor targets that have been missed through the study of the human cancer alone. RESULTS: Using parallel oligonucleotide array platforms, shared orthologues between species were identified and normalized. The osteosarcoma expression signatures could not distinguish the canine and human diseases by hierarchical clustering. Cross-species target mining identified two genes, interleukin-8 (IL-8) and solute carrier family 1 (glial high affinity glutamate transporter), member 3 (SLC1A3), which were uniformly expressed in dog but not in all pediatric osteosarcoma patient samples. Expression of these genes in an independent population of pediatric osteosarcoma patients was associated with poor outcome (p = 0.020 and p = 0.026, respectively). Validation of IL-8 and SLC1A3 protein expression in pediatric osteosarcoma tissues further supported the potential value of these novel targets. Ongoing evaluation will validate the biological significance of these targets and their associated pathways. CONCLUSIONS: Collectively, these data support the strong similarities between human and canine osteosarcoma and underline the opportunities provided by a comparative oncology approach as a means to improve our understanding of cancer biology and therapies.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The integrated canine approach has been particularly promising for evaluating anti-metastatic and immune-based therapeutics.
“This integrated approach has been particularly promising for the evaluation of anti-metastatic 99,234 and immune-based therapeutics 69,235 .”
From Osteosarcoma (2022) · cites this paper as [234]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Exploration, normalization, and summaries of high density oligonucleotide array probe level data
Irizarry, R. A. (2003) · Biostatistics · doi:10.1093/biostatistics/4.2.249 · Cited by 10,603 · see citing works
limma: Linear Models for Microarray Data
Smyth, G. K. (2005) · Statistics for Biology and Health · doi:10.1007/0-387-29362-0_23 · Cited by 5,796 · see citing works
A gene atlas of the mouse and human protein-encoding transcriptomes
Su, A. I., Wiltshire, T., Batalov, S., Lapp, H., Ching, K. A., Block, D., Zhang, J., Soden, R., Hayakawa, M., Kreiman, G., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400782101 · Cited by 3,475 · see citing works
Genome sequence, comparative analysis and haplotype structure of the domestic dog
members, B. S. P., Lindblad-Toh, K., Wade, C. M., Mikkelsen, T. S., Karlsson, E. K., Jaffe, D. B., Kamal, M., Clamp, M., Chang, J. L., Kulbokas, E. J., et al. (2005) · Nature · doi:10.1038/nature04338 · Cited by 2,568 · see citing works
Huang, D. W., Sherman, B. T., Tan, Q., Kir, J., Liu, D., Bryant, D., Guo, Y., Stephens, R. M., Baseler, M., Lane, H. C., et al. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm415 · Cited by 2,216 · see citing works
Rosen, G., Caparros, B., Huvos, A. G., Kosloff, C., Nirenberg, A., Cacavio, A., Marcove, R. C., Lane, J. M., Mehta, B. M., & Urban, C. (1982) · Cancer · doi:10.1002/1097-0142(19820315)49:6 · Cited by 1,088 · see citing works
Translation of new cancer treatments from pet dogs to humans
Paoloni, M., & Khanna, C. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2273 · Cited by 668 · see citing works
Self-citationBiology and Therapeutic Advances for Pediatric Osteosarcoma
Marina, N. M., Gebhardt, M. C., Teot, L. A., & Gorlick, R. G. (2004) · The Oncologist · doi:10.1634/theoncologist.9-4-422 · Cited by 663 · see citing works
Withrow & Macewen's Small Animal Clinical Oncology
Withrow, S. J., Vail, D. M., & Page, R. L. (2019) · Medical Entomology and Zoology · Cited by 637 · see citing works
Self-citationLee, J.-S., Chu, I.-S., Mikaelyan, A., Calvisi, D., Heo, J., Reddy, J., & Thorgeirsson, S. (2004) · Nature Genetics · doi:10.1038/ng1481 · Cited by 472 · see citing works
Mayer, A., Takimoto, M., Fritz, E., Schellander, G., Kofler, K., & Ludwig, H. (1993) · Cancer · doi:10.1002/1097-0142(19930415)71:8 · Cited by 413 · see citing works
Self-citationGene expression profiling of human sarcomas: insights into sarcoma biology.
Baird, K., Davis, S., Antonescu, C. R., Harper, U. L., Walker, R. L., Chen, Y., Glatfelter, A. A., Duray, P. H., & Meltzer, P. S. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-1699 · Cited by 353 · see citing works
Self-citationInterleukin-8 Is a Molecular Determinant of Androgen Independence and Progression in Prostate Cancer
Araki, S., Omori, Y., Lyn, D. A., Singh, R. K., Meinbach, D. M., Sandman, Y., Lokeshwar, V. B., & Lokeshwar, B. L. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-1162 · Cited by 275 · see citing works
Merritt, W. M., Lin, Y. G., Spannuth, W. A., Fletcher, M. S., Kamat, A. A., Han, L. Y., Landen, C. N., Jennings, N., Geest, K. D., Langley, R. R., et al. (2008) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djn024 · Cited by 257 · see citing works
Role of Interleukin-8 in Tumor Growth and Metastasis of Human Melanoma
Bar‐Eli, M. (1999) · Pathobiology · doi:10.1159/000028045 · Cited by 248 · see citing works
Comparative Aspects of Osteosarcoma
Withrow, S. J., Powers, B. E., Straw, R. C., & Wilkins, R. M. (1991) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-199109000-00023 · Cited by 239 · see citing works
Self-citationInterleukin 8 expression regulates tumorigenicity and metastasis in human bladder cancer.
Inoue, K., Slaton, J. W., Kim, S. J., Perrotte, P., Eve, B. Y., Bar‐Eli, M., Radinsky, R., & Dinney, C. P. (2000) · PubMed · Cited by 222 · see citing works
An Expression Signature Classifies Chemotherapy-Resistant Pediatric Osteosarcoma
Mintz, M., Sowers, R. S., Brown, K. M., Hilmer, S. C., Mazza, B., Huvos, A. G., Meyers, P. A., LaFleur, B., McDonough, W. S., Henry, M. M., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-2463 · Cited by 214 · see citing works
Lingaas, F. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg336 · Cited by 188 · see citing works
Parker, H. G., Kukekova, A. V., Akey, D. T., Goldstein, O., Kirkness, E. F., Baysac, K. C., Mosher, D. S., Aguirre, G. K., Acland, G. M., & Ostrander, E. A. (2007) · Genome Research · doi:10.1101/gr.6772807 · Cited by 152 · see citing works
The Multidisciplinary Management of Osteosarcoma
Federman, N. C., Bernthal, N. M., Eilber, F. C., & Tap, W. D. (2009) · Current Treatment Options in Oncology · doi:10.1007/s11864-009-0087-3 · Cited by 145 · see citing works
Expression Profiles of Osteosarcoma That Can Predict Response to Chemotherapy
Man, T., Chintagumpala, M., Visvanathan, J., Shen, J., Perlaky, L., Hicks, J. M., Johnson, M., Davino, N. A., Murray, J. C., Helman, L. J., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-0985 · Cited by 139 · see citing works
Self-citationLimb-sparing treatment for osteosarcoma in dogs
LaRue, S. Μ., Withrow, S. J., Powers, B. E., Wrigley, R. H., Gillette, E. L., Schwarz, P. D., Straw, R. C., & Richter, S. L. (1989) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.1989.195.12.1734 · Cited by 137 · see citing works
Self-citationAwano, T., Katz, M. L., O’Brien, D. P., Sohár, I., Lobel, P., Coates, J. R., Khan, S., Johnson, G. C., Giger, U., & Johnson, G. S. (2006) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2006.02.016 · Cited by 126 · see citing works
Correlation of IL-8 with induction, progression and metastatic potential of colorectal cancer
Rubie, C. (2007) · World Journal of Gastroenterology · doi:10.3748/wjg.v13.i37.4996 · Cited by 120 · see citing works
Rutkowski, P. L., Kaminska, J. A., Kowalska, M. M., Ruka, W., & Steffen, J. A. (2003) · Journal of Surgical Oncology · doi:10.1002/jso.10305 · Cited by 117 · see citing works
Comparative and integrative functional genomics of HCC
Lee, J.-S., & Thorgeirsson, S. S. (2006) · Oncogene · doi:10.1038/sj.onc.1209561 · Cited by 113 · see citing works
Tumor Suppressor PTEN is Mutated in Canine Osteosarcoma Cell Lines and Tumors
Levine, R. A., Forest, T. W., & Smith, C. (2002) · Veterinary Pathology · doi:10.1354/vp.39-3-372 · Cited by 101 · see citing works
Prediction of response to neoadjuvant chemotherapy for osteosarcoma by gene-expression profiles
Ochi, K., Daigo, Y., Katagiri, T., Nagayama, S., Tsunoda, T., Myoui, A., Naka, N., Araki, N., Kudawara, I., Ieguchi, M., et al. (2004) · International Journal of Oncology · doi:10.3892/ijo.24.3.647 · Cited by 98 · see citing works
Uehara, H., Troncoso, P., Johnston, D. A., Bucana, C. D., Dinney, C. P., Dong, Z., Fidler, I. J., & Pettaway, C. A. (2005) · The Prostate · doi:10.1002/pros.20223 · Cited by 97 · see citing works
TP53 Gene Mutations in Canine Osteosarcoma
Kirpensteijn, J., Kik, M. J. L., Teske, E., & Rutteman, G. R. (2008) · Veterinary Surgery · doi:10.1111/j.1532-950x.2008.00407.x · Cited by 96 · see citing works
Ostrander, E. A., Giger, U., & Lindblad‐Toh, K. (2006) · Medical Entomology and Zoology · Cited by 95 · see citing works
Update on the biology and management of canine osteosarcoma
Chun, R., & de Lorimier, L. (2003) · Veterinary Clinics of North America Small Animal Practice · doi:10.1016/s0195-5616(03)00021-4 · Cited by 91 · see citing works
Bioimmunotherapy for melanoma using fully human antibodies targeting MCAM/MUC18 and IL‐8
Melnikova, V. O., & Bar‐Eli, M. (2006) · Pigment Cell Research · doi:10.1111/j.1600-0749.2006.00331.x · Cited by 87 · see citing works
Regulators of G-Protein Signaling 3 and 4 (RGS3, RGS4) Are Associated with Glioma Cell Motility
Tatenhorst, L., Senner, V., Püttmann, S., & Paulus, W. (2004) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/63.3.210 · Cited by 78 · see citing works
Correlation between clinical outcome and growth factor pathway expression in osteogenic sarcoma
Abdeen, A. R., Chou, A. J., Healey, J. H., Khanna, C., Osborne, T. S., Hewitt, S. M., Kim, M., Wang, D., Moody, K. M., & Gorlick, R. G. (2009) · Cancer · doi:10.1002/cncr.24562 · Cited by 77 · see citing works
Self-citationStatus of the p53, Rb and MDM2 genes in canine osteosarcoma.
Mendoza, S., Konishi, T., Dernell, W. S., Withrow, S. J., & Cw, M. (1998) · PubMed · Cited by 75 · see citing works
Self-citationDuan, Z., Lamendola, D. E., Penson, R. T., Kronish, K., & Seiden, M. V. (2002) · Cytokine · doi:10.1006/cyto.2001.1008 · Cited by 71 · see citing works
Inactivation of p53 and Retinoblastoma Family Pathways in Canine Osteosarcoma Cell Lines
Levine, R. A., & Fleischli, M. A. (2000) · Veterinary Pathology · doi:10.1354/vp.37-1-54 · Cited by 71 · see citing works
Overexpression of the erbB-2 Proto-oncogene in Canine Osteosarcoma Cell Lines and Tumors
Flint, A. F., U’Ren, L., Legare, M. E., Withrow, S. J., Dernell, W. S., & Hanneman, W. H. (2004) · Veterinary Pathology · doi:10.1354/vp.41-3-291 · Cited by 69 · see citing works
Self-citationChase, K., Sargan, D. R., Miller, K., Ostrander, E. A., & Lark, K. G. (2006) · International Journal of Immunogenetics · doi:10.1111/j.1744-313x.2006.00593.x · Cited by 68 · see citing works
Multiple pathways are involved in drug resistance to doxorubicin in an osteosarcoma cell line
Rajkumar, T., & Yamuna, M. (2008) · Anti-Cancer Drugs · doi:10.1097/cad.0b013e3282f435b6 · Cited by 55 · see citing works
Construction of a 2-Mb resolution BAC microarray for CGH analysis of canine tumorsPreprint
Thomas, R. J., Scott, A., Langford, C. F., Fosmire, S. P., Jubala, C. M., Lorentzen, T. D., Hitte, C., Karlsson, E. K., Kirkness, E. F., Ostrander, E. A., et al. (2005) · Genome Research · doi:10.1101/gr.3825705 · Cited by 52 · see citing works
Characterization of the glutametergic system in MG-63 osteoblast-like osteosarcoma cells.
Kalariti, N., Lembessis, P., & Koutsilieris, M. (2005) · PubMed · Cited by 51 · see citing works
Met oncogene aberrant expression in canine osteosarcoma
Ferracini, R., Angelini, P., Cagliero, E. E., Linari, A., Martano, M., Wunder, J. S., & Buracco, P. (2000) · Journal of Orthopaedic Research® · doi:10.1002/jor.1100180213 · Cited by 51 · see citing works
Gene expression array profile of human osteosarcoma
Leonard, P., Sharp, T. V., Henderson, S. R., Hewitt, D., Pringle, J. A. S., Sandison, A., Goodship, A. E., Whelan, J. S., & Boshoff, C. (2003) · British Journal of Cancer · doi:10.1038/sj.bjc.6601389 · Cited by 33 · see citing works
Kalariti, N., Lembessis, P., Papageorgiou, E., Pissimissis, N., & Koutsilieris, M. (2007) · PubMed · Cited by 28 · see citing works
Follow-up study of long-term survivors of osteosarcoma in the prechemotherapy era
Gaffney, R. L., Unni, K. K., Sim, F. H., Slezák, J., Esther, R. J., & Bolander, M. E. (2006) · Human Pathology · doi:10.1016/j.humpath.2006.02.022 · Cited by 23 · see citing works
Role of interleukin-8 in the progression of estrogen receptor-negative breast cancer
Yao, C., Lin, Y., Ye, C., Bi, J., Zhu, Y., & Wang, S. (2007) · Chinese Medical Journal · doi:10.1097/00029330-200710020-00007 · Cited by 22 · see citing works
Treatment results of pediatric osteosarcoma: twenty-year experience.
Varan, A., Yazıcı, N., Aksoy, C., Gedikog̈lu, G., Yalçın, B., Akyüz, C., Kutluk, T., & Büyükpamukçu, M. (2007) · PubMed · Cited by 15 · see citing works
The role of interleukin-8 in the initiation and progression of human cutaneous melanoma.
Gutman, M., Even‐Sapir, E., Merimsky, O., Trejo, L., Klausner, J. M., & Lev‐Chelouche, D. (2002) · PubMed · Cited by 13 · see citing works
MET Oncogene Aberrant Expression in Canine Osteosarcoma
Ferracini, R., Angelini, P., Cagliero, E. E., Linari, A., Martano, M., Wunder, J., & Buracco, P. (2000) · Journal of Bone and Joint Surgery · doi:10.2106/00004623-200009000-00049 · Cited by 2 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Beird, H. C., Bielack, S. S., Flanagan, A. M., Gill, J., Heymann, D., Janeway, K. A., Livingston, J. A., Roberts, R. D., Strauss, S. J., & Gorlick, R. (2022) · Nature Reviews Disease Primers · doi:10.1038/s41572-022-00409-y · Cited by 660 · see citing works
Comparative oncology: what dogs and other species can teach us about humans with cancer
Schiffman, J. D., & Breen, M. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0231 · Cited by 420 · see citing works
Dog models of naturally occurring cancer
Rowell, J., McCarthy, D. O., & Alvarez, C. E. (2011) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2011.02.004 · Cited by 388 · see citing works
Breed-Predispositions to Cancer in Pedigree Dogs
Dobson, J. M. (2013) · ISRN Veterinary Science · doi:10.1155/2013/941275 · Cited by 340 · see citing works
Canine Osteosarcoma: A Naturally Occurring Disease to Inform Pediatric Oncology
Fenger, J. M., London, C. A., & Kisseberth, W. C. (2014) · ILAR Journal · doi:10.1093/ilar/ilu009 · Cited by 248 · see citing works
Recent advances in osteosarcoma
Botter, S. M., Neri, D., & Fuchs, B. (2014) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2014.02.002 · Cited by 249 · see citing works
Osteosarcoma: Accelerating Progress Makes for a Hopeful Future
Saraf, A. J., Fenger, J. M., & Roberts, R. D. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00004 · Cited by 237 · see citing works
Gardner, H. L., Fenger, J. M., & London, C. A. (2016) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-022114-110911 · Cited by 215 · see citing works
Improving human cancer therapy through the evaluation of pet dogs
LeBlanc, A. K., & Mazcko, C. N. (2020) · Nature reviews. Cancer · doi:10.1038/s41568-020-0297-3 · Cited by 202 · see citing works
Mason, N. J., Gnanandarajah, J. S., Engiles, J. B., Gray, F., Laughlin, D., Gaurnier-Hausser, A., Wallecha, A., Huebner, M., & Paterson, Y. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-0088 · Cited by 178 · see citing works
Toward a Drug Development Path That Targets Metastatic Progression in Osteosarcoma
Khanna, C., Fan, T. M., Gorlick, R., Helman, L. J., Kleinerman, E. S., Adamson, P. C., Houghton, P. J., Tap, W. D., Welch, D. R., Steeg, P. S., et al. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-2574 · Cited by 178 · see citing works
Self-citationKarlsson, E. K., Sigurðsson, S., Ivansson, E. L., Thomas, R. J., Elvers, I., Wright, J. B., Howald, C., Tonomura, N., Perloski, M., Swofford, R., et al. (2013) · Genome biology · doi:10.1186/gb-2013-14-12-r132 · Cited by 171 · see citing works
Perspectives from man’s best friend: National Academy of Medicine’s Workshop on Comparative Oncology
LeBlanc, A. K., Breen, M., Choyke, P., Dewhirst, M., Fan, T. M., Gustafson, D. L., Helman, L. J., Kastan, M. B., Knapp, D. W., Levin, W. J., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aaf0746 · Cited by 147 · see citing works
Self-citationBrønstad, A., Newcomer, C. E., Decelle, T., Everitt, J. I., Guillén, J., & Laber, K. (2016) · Laboratory Animals · doi:10.1177/0023677216642398 · Cited by 147 · see citing works
Koehler, J. W., Miller, A. D., Miller, C. R., Porter, B. F., Aldape, K., Beck, J. A., Brat, D. J., Cornax, I., Corps, K. N., Frank, C., et al. (2018) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nly085 · Cited by 146 · see citing works
The Promise of Combining Radiation Therapy With Immunotherapy
Jagodinsky, J. C., Harari, P. M., & Morris, Z. S. (2020) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2020.04.023 · Cited by 144 · see citing works
Çolak, D., Nofal, A., AlBakheet, A., Nirmal, M. S., Jeprel, H. A., Eldali, A., Al‐Tweigeri, T., Tulbah, A. M., Ajarim, D. S., Malik, O. A., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063204 · Cited by 144 · see citing works
Ranieri, G., Gadaleta, C. D., Patruno, R., Zizzo, N., Daidone, M. G., HANSSON, M. G., Paradiso, A., & Ribatti, D. (2013) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2013.03.005 · Cited by 137 · see citing works
Domestic Dogs and Cancer Research: A Breed-Based Genomics Approach
Davis, B. W., & Ostrander, E. A. (2014) · ILAR Journal · doi:10.1093/ilar/ilu017 · Cited by 137 · see citing works
Notch Activation as a Driver of Osteogenic Sarcoma
Tao, J., Jiang, M., Jiang, L., Salvo, J. S., Zeng, H., Dawson, B., Bertin, T., Rao, P. H., Chen, R., Donehower, L. A., et al. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.07.023 · Cited by 135 · see citing works
Gardner, H. L., Sivaprakasam, K., Briones, N., Zismann, V., Perdigones, N., Drenner, K., Facista, S., Richholt, R., Liang, W., Aldrich, J., et al. (2019) · Communications Biology · doi:10.1038/s42003-019-0487-2 · Cited by 120 · see citing works
Self-citationRoberts, R. D., Lizardo, M. M., Reed, D. R., Hingorani, P., Glover, J., Allen‐Rhoades, W., Fan, T., Khanna, C., Sweet‐Cordero, E. A., Cash, T., et al. (2019) · Cancer · doi:10.1002/cncr.32351 · Cited by 127 · see citing works
Self-citationScott, M. C., Sarver, A. L., Gavin, K., Thayanithy, V., Getzy, D. M., Newman, R. A., Cutter, G., Lindblad‐Toh, K., Kisseberth, W. C., Hunter, L., et al. (2011) · Bone · doi:10.1016/j.bone.2011.05.008 · Cited by 121 · see citing works
Canine cancer immunotherapy studies: linking mouse and human
Park, J. S., Withers, S. S., Modiano, J. F., Kent, M. S., Chen, M., Luna, J. I., Culp, W. T. N., Sparger, E. E., Rebhun, R. B., Monjazeb, A. M., et al. (2016) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-016-0200-7 · Cited by 121 · see citing works
Hernandez, B., Adissu, H. A., Wei, B., Michael, H., Merlino, G. T., & Simpson, R. M. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020394 · Cited by 121 · see citing works
Characterization of the metastatic phenotype of a panel of established osteosarcoma cells
Ren, L., Mendoza, A., Zhu, J., Briggs, J., Halsey, C., Hong, E. S., Burkett, S. S., Morrow, J. J., Lizardo, M. M., Osborne, T. S., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.5177 · Cited by 119 · see citing works
Self-citationInflammation and cancer: Till death tears them apart
Raposo, T. P., Beirão, B. C. B., Pang, L. Y., QUEIROGA, F. L., & Argyle, D. J. (2015) · The Veterinary Journal · doi:10.1016/j.tvjl.2015.04.015 · Cited by 118 · see citing works
Inflammation and Cancer: A Comparative View
Morrison, W. B. (2011) · Journal of Veterinary Internal Medicine · doi:10.1111/j.1939-1676.2011.00836.x · Cited by 118 · see citing works
Oncostatin M promotes STAT3 activation, VEGF production, and invasion in osteosarcoma cell lines
Fossey, S. L., Bear, M. D., Kisseberth, W. C., Pennell, M. L., & London, C. A. (2011) · BMC Cancer · doi:10.1186/1471-2407-11-125 · Cited by 115 · see citing works
Prkar1a is an osteosarcoma tumor suppressor that defines a molecular subclass in mice
Molyneux, S. D., Grappa, M. A. D., Beristain, A. G., McKee, T. D., Wai, D., Paderova, J., Kashyap, M., Hu, P., Maiuri, T., Narala, S., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci42391 · Cited by 98 · see citing works
Self-citationWhy is the dog an ideal model for aging research?
Gilmore, K. M., & Greer, K. A. (2015) · Experimental Gerontology · doi:10.1016/j.exger.2015.08.008 · Cited by 96 · see citing works
Companion animals in comparative oncology: One Medicine in action
Garden, O. A., Volk, S. W., Mason, N. J., & Perry, J. A. (2018) · The Veterinary Journal · doi:10.1016/j.tvjl.2018.08.008 · Cited by 93 · see citing works
Fossey, S. L., Bear, M. D., Lin, J., Li, C., Schwartz, E. B., Li, P., Fuchs, J. R., Fenger, J. M., Kisseberth, W. C., & London, C. A. (2011) · BMC Cancer · doi:10.1186/1471-2407-11-112 · Cited by 93 · see citing works
Fan, T. M., Roberts, R. D., & Lizardo, M. M. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00013 · Cited by 90 · see citing works
A tumor microenvironment-based prognostic index for osteosarcoma
Wu, C., Gong, S., Duan, Y., Deng, C., Kallendrusch, S., Berninghausen, L. K., Osterhoff, G., & Schopow, N. (2023) · Journal of Biomedical Science · doi:10.1186/s12929-023-00917-3 · Cited by 89 · see citing works
Canine sarcomas as a surrogate for the human disease
Gustafson, D. L., Duval, D. L., Regan, D. P., & Thamm, D. H. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.01.012 · Cited by 85 · see citing works
IL-6 and CXCL8 mediate osteosarcoma-lung interactions critical to metastasis
Gross, A. C., Cam, H., Phelps, D. A., Saraf, A. J., Bid, H. K., Cam, M., London, C. A., Winget, S. A., Arnold, M. A., Brandolini, L., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.99791 · Cited by 82 · see citing works
Yin, Q., Tang, L., Cai, K., Tong, R., Sternberg, R., Yang, X., Dobrucki, L. W., Borst, L. B., Kamstock, D. A., Song, Z., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1603316113 · Cited by 82 · see citing works
Angstadt, A. Y., Thayanithy, V., Subramanian, S., Modiano, J. F., & Breen, M. (2012) · Cancer Genetics · doi:10.1016/j.cancergen.2012.09.005 · Cited by 81 · see citing works
Angstadt, A. Y., Motsinger‐Reif, A. A., Thomas, R. J., Kisseberth, W. C., Couto, C. G., Duval, D. L., Nielsen, D. M., Modiano, J. F., & Breen, M. (2011) · Genes Chromosomes and Cancer · doi:10.1002/gcc.20908 · Cited by 80 · see citing works
Paoloni, M. C., Mazcko, C. N., Fox, E., Fan, T. M., Lana, S. E., Kisseberth, W. C., Vail, D. M., Nuckolls, K., Osborne, T. S., Yalkowsy, S., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011013 · Cited by 80 · see citing works
Self-citationMan's best friend: what can pet dogs teach us about non‐ H odgkin's lymphoma?
Richards, K. L., & Suter, S. E. (2014) · Immunological Reviews · doi:10.1111/imr.12238 · Cited by 80 · see citing works
Prognostic and predictive biomarkers of canine osteosarcoma
Selvarajah, G. T., & Kirpensteijn, J. (2010) · The Veterinary Journal · doi:10.1016/j.tvjl.2010.04.010 · Cited by 74 · see citing works
A Review of the Association between Osteosarcoma Metastasis and Protein Translation
Osborne, T. S., & Khanna, C. (2012) · Journal of Comparative Pathology · doi:10.1016/j.jcpa.2011.12.007 · Cited by 73 · see citing works
Self-citationGuijarro, M. V., Ghivizzani, S. C., & Gibbs, C. P. (2014) · Frontiers in Oncology · doi:10.3389/fonc.2014.00189 · Cited by 73 · see citing works
Defining the Value of a Comparative Approach to Cancer Drug Development
LeBlanc, A. K., Mazcko, C. N., & Khanna, C. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-2347 · Cited by 73 · see citing works
Self-citationPinheiro, D., Singh, Y., Grant, C. R., Appleton, R. C., Sacchini, F., Walker, K. R. L., Chadbourne, A. H., Palmer, C. A., Armitage‐Chan, E. A., Thompson, I., et al. (2010) · Immunology · doi:10.1111/j.1365-2567.2010.03346.x · Cited by 72 · see citing works
What Is New in the miRNA World Regarding Osteosarcoma and Chondrosarcoma?
Palmini, G., Marini, F., & Brandi, M. L. (2017) · Molecules · doi:10.3390/molecules22030417 · Cited by 70 · see citing works
Zhou, L., Yu, Y., Sun, S., Zhang, T., & Wang, M. (2018) · Journal of Cancer · doi:10.7150/jca.25213 · Cited by 68 · see citing works
Meta-analysis of differentially expressed genes in osteosarcoma based on gene expression data
Yang, Z., Chen, Y., Fu, Y., Yang, Y., Zhang, Y., Chen, Y., & Li, D. (2014) · BMC Medical Genetics · doi:10.1186/1471-2350-15-80 · Cited by 65 · see citing works
Searching for molecular targets in sarcoma
Teicher, B. A. (2012) · Biochemical Pharmacology · doi:10.1016/j.bcp.2012.02.009 · Cited by 65 · see citing works
Of Mice, Dogs, Pigs, and Men: Choosing the Appropriate Model for Immuno-Oncology Research
Overgaard, N. H., Fan, T. M., Schachtschneider, K. M., Principe, D. R., Schook, L. B., & Jungersen, G. (2018) · ILAR Journal · doi:10.1093/ilar/ily014 · Cited by 63 · see citing works
Rankin, K. S., Starkey, M., Lunec, J., Gerrand, C., Murphy, S., & Biswas, S. (2011) · Pediatric Blood & Cancer · doi:10.1002/pbc.23341 · Cited by 61 · see citing works
The companion dog as a unique translational model for aging
Mazzatenta, A., Carluccio, A., Robbe, D., Giulio, C. D., & Cellerino, A. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.08.024 · Cited by 56 · see citing works
Zhu, N., Hou, J., Ma, G., Guo, S., Zhao, C., & Chen, B. (2020) · Cancer Cell International · doi:10.1186/s12935-020-01352-2 · Cited by 56 · see citing works
O’Donoghue, L. E., Ptitsyn, A. A., Kamstock, D. A., Siebert, J., Thomas, R. S., & Duval, D. L. (2010) · BMC Cancer · doi:10.1186/1471-2407-10-506 · Cited by 56 · see citing works
LeBlanc, A. K., Mazcko, C. N., Cherukuri, A., Berger, E. P., Kisseberth, W. C., Brown, M. E., Lana, S. E., Weishaar, K. M., Flesner, B. K., Bryan, J. N., et al. (2021) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-21-0315 · Cited by 55 · see citing works
Self-citationPinello, K. C., Pires, I. C. R., Castro, A. F., Carvalho, P. T., Santos, A. A. F., de Matos, A., QUEIROGA, F. L., Canadas‐Sousa, A., Dias‐Pereira, P., Catarino, J., et al. (2022) · Veterinary Sciences · doi:10.3390/vetsci9040167 · Cited by 52 · see citing works
Comparative Aspects of Osteosarcoma Pathogenesis in Humans and Dogs
Fan, T. M., & Khanna, C. (2015) · Veterinary Sciences · doi:10.3390/vetsci2030210 · Cited by 52 · see citing works
Self-citationLondon, C. A., Bear, M. D., McCleese, J., Foley, K. P., Paalangara, R., Inoue, T., Ying, W., & Barsoum, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027018 · Cited by 52 · see citing works
Understanding the Osteosarcoma Pathobiology: A Comparative Oncology Approach
Varshney, J., Scott, M. C., Largaespada, D. A., & Subramanian, S. (2016) · Veterinary Sciences · doi:10.3390/vetsci3010003 · Cited by 51 · see citing works
Horise, Y., Maeda, M., Konishi, Y., Okamoto, J., Ikuta, S., Okamoto, Y., Ishii, H., Yoshizawa, S., Umemura, S., Ueyama, T., et al. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00545 · Cited by 51 · see citing works
Foltz, J. A., Somanchi, S. S., Yang, Y., Aquino‐López, A., Bishop, E. E., & Lee, D. A. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00521 · Cited by 49 · see citing works
Expression and Function of Survivin in Canine Osteosarcoma
Shoeneman, J. K., Ehrhart, E. J., Eickhoff, J. C., Charles, J. B., Powers, B. E., & Thamm, D. H. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-2315 · Cited by 46 · see citing works
Genetically engineered mouse models and human osteosarcoma
Ng, A. J., Mutsaers, A. J., Baker, E. K., & Walkley, C. R. (2012) · Clinical Sarcoma Research · doi:10.1186/2045-3329-2-19 · Cited by 45 · see citing works
Wu, C., Tan, J., Shen, H., Deng, C., Kleber, C., Osterhoff, G., & Schopow, N. (2024) · Journal of Biomedical Science · doi:10.1186/s12929-024-00999-7 · Cited by 47 · see citing works
Chen, Y., Zhao, B., & Wang, X. (2020) · BMC Cancer · doi:10.1186/s12885-020-07536-3 · Cited by 43 · see citing works
IL-17A/IL-17RA interaction promoted metastasis of osteosarcoma cells
Wang, M., Wang, L., Ren, T., Xu, L., & Wen, Z. (2013) · Cancer Biology & Therapy · doi:10.4161/cbt.22955 · Cited by 42 · see citing works
Dailey, D. D., Anfinsen, K. P., Pfaff, L. E., Ehrhart, E. J., Charles, J. B., Bønsdorff, T. B., Thamm, D. H., Powers, B. E., Jónasdóttir, T. J., & Duval, D. L. (2013) · BMC Veterinary Research · doi:10.1186/1746-6148-9-130 · Cited by 41 · see citing works
Paoloni, M. C., Webb, C. P., Mazcko, C. N., Cherba, D., Hendricks, W. P. D., Lana, S. E., Ehrhart, E. J., Charles, B., Fehling, H. L., Kumar, L., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090028 · Cited by 41 · see citing works
Self-citationTranslating Gene Expression Into Clinical Care: Sarcomas As a Paradigm
Nielsen, T. O., & West, R. B. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2009.26.1917 · Cited by 41 · see citing works
Comparative oncology: Integrating human and veterinary medicine
Sultan, F., & Ganaie, B. A. (2018) · Open Veterinary Journal · doi:10.4314/ovj.v8i1.5 · Cited by 40 · see citing works
Patient Derived Xenografts for Genome-Driven Therapy of Osteosarcoma
Landuzzi, L., Manara, M. C., Lollini, P.-L., & Scotlandi, K. (2021) · Cells · doi:10.3390/cells10020416 · Cited by 39 · see citing works
Screening of diagnostic markers for osteosarcoma
Wu, D., Chen, K., Bai, Y., Zhu, X., Chen, K., Wang, C., Zhao, Y., & Li, M. (2014) · Molecular Medicine Reports · doi:10.3892/mmr.2014.2546 · Cited by 39 · see citing works
Muff, R., Kumar, R. M. R., Botter, S. M., Born, W., & Fuchs, B. (2012) · Sarcoma · doi:10.1155/2012/937506 · Cited by 39 · see citing works
Fenger, J. M., Roberts, R. D., Iwenofu, O. H., Bear, M. D., Zhang, X., Couto, J. I., Modiano, J. F., Kisseberth, W. C., & London, C. A. (2016) · BMC Cancer · doi:10.1186/s12885-016-2837-5 · Cited by 39 · see citing works
Wu, K., Rodrigues, L., Post, G. S., Harvey, G., White, M. E., Miller, A., Lambert, L., Lewis, B., Lopes, C., & Zou, J. (2023) · npj Precision Oncology · doi:10.1038/s41698-023-00346-3 · Cited by 39 · see citing works
Bornstein, K., Gryan, G., Chang, E. S., Marchler‐Bauer, A., & Schneider, V. (2023) · BMC Genomics · doi:10.1186/s12864-023-09643-4 · Cited by 36 · see citing works
B7-H3 Specific CAR T Cells for the Naturally Occurring, Spontaneous Canine Sarcoma Model
Zhang, S., Black, R. G., Kohli, K., Hayes, B. J., Miller, C., Koehne, A. L., Schroeder, B., Abrams, K., Schulte, B. C., Alexiev, B. A., et al. (2022) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-21-0726 · Cited by 39 · see citing works
A Compendium of Canine Normal Tissue Gene Expression
Briggs, J., Paoloni, M. C., Chen, Q., Wen, X., Khan, J. I., & Khanna, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017107 · Cited by 38 · see citing works
Self-citationGatti, M., Solari, A., Pattarozzi, A., Campanella, C., Thellung, S., Maniscalco, L., Maria, R. D., Würth, R., Corsaro, A., Bajetto, A., et al. (2018) · Experimental Cell Research · doi:10.1016/j.yexcr.2018.01.002 · Cited by 38 · see citing works
Pain Management in Veterinary Patients with Cancer
Fan, T. M. (2014) · Veterinary Clinics of North America Small Animal Practice · doi:10.1016/j.cvsm.2014.05.005 · Cited by 36 · see citing works
Modeling human osteosarcoma in the mouse: From bedside to bench
Janeway, K. A., & Walkley, C. R. (2010) · Bone · doi:10.1016/j.bone.2010.07.028 · Cited by 36 · see citing works
Roy, J., Wycislo, K. L., Pondenis, H. C., Fan, T. M., & Das, A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0183930 · Cited by 36 · see citing works
Characterization and Potential Applications of Dog Natural Killer Cells in Cancer Immunotherapy
Gingrich, A. A., Modiano, J. F., & Canter, R. J. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8111802 · Cited by 36 · see citing works
A novel locus for canine osteosarcoma (OSA1) maps to CFA34, the canine orthologue of human 3q26
Phillips, J. C., Lembcke, L. M., & Chamberlin, T. (2010) · Genomics · doi:10.1016/j.ygeno.2010.07.002 · Cited by 36 · see citing works
Wang, Y., Ma, X., Xu, E., Huang, Z. Y., Chen, Y., Zhu, K., Dong, Y., & Zhang, C. (2024) · Clinical and Translational Medicine · doi:10.1002/ctm2.1586 · Cited by 36 · see citing works
Small-Molecule Procaspase-3 Activation Sensitizes Cancer to Treatment with Diverse Chemotherapeutics
Botham, R. C., Roth, H. S., Book, A. P., Roady, P. J., Fan, T. M., & Hergenrother, P. J. (2016) · ACS Central Science · doi:10.1021/acscentsci.6b00165 · Cited by 35 · see citing works
MiR-34a regulates the invasive capacity of canine osteosarcoma cell lines
López, C. M., Yu, P. Y., Zhang, X., Yilmaz, A. S., London, C. A., & Fenger, J. M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0190086 · Cited by 35 · see citing works
Identification of potential crucial genes and key pathways in osteosarcoma
Liu, J., Wu, S., Xie, X., Wang, Z., & Lei, Q. (2020) · Hereditas · doi:10.1186/s41065-020-00142-0 · Cited by 35 · see citing works
Hendricks-Wenger, A., Ruger, L. N., Gannon, J., Simon, A., Singh, N., Sheppard, H., Nagai-Singer, M. A., Imran, K. M., Lee, K., Clark‐Deener, S., et al. (2021) · IEEE Transactions on Ultrasonics Ferroelectrics and Frequency Control · doi:10.1109/tuffc.2021.3110083 · Cited by 35 · see citing works
Protein kinase C regulates ezrin–radixin–moesin phosphorylation in canine osteosarcoma cells
Hong, S. ‐., Osborne, T. S., Ren, L., Briggs, J., Mazcko, C. N., Burkett, S. S., & Khanna, C. (2010) · Veterinary and Comparative Oncology · doi:10.1111/j.1476-5829.2010.00249.x · Cited by 35 · see citing works
Self-citationRodrigues, L., Watson, J., Yuan, F., Lewis, B., Harvey, G., Post, G. S., Megquier, K., White, M. E., Lambert, L., Miller, A., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-37505-2 · Cited by 34 · see citing works
Precision medicine: an opportunity for a paradigm shift in veterinary medicine
Lloyd, K. C. K., Khanna, C., Hendricks, W. P. D., Trent, J. M., & Kotlikoff, M. I. (2015) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.248.1.45 · Cited by 34 · see citing works
Self-citationÇolak, D., Chishti, M. A., AlBakheet, A., Al-Qahtani, A. A., Shoukri, M. M., Goyns, M. H., Ozand, P. T., Quackenbush, J. F., Park, B. H., & Kaya, N. (2010) · Molecular Cancer · doi:10.1186/1476-4598-9-146 · Cited by 34 · see citing works
Canine osteosarcoma in comparative oncology: Molecular mechanisms through to treatment discovery
Simpson, S., Rizvanov, A. A., Jeyapalan, J. N., de Brot, S., & Rutland, C. S. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.965391 · Cited by 34 · see citing works
Review on Canine Oral Melanoma: An Undervalued Authentic Genetic Model of Human Oral Melanoma?
Palma, S. D., McConnell, A., Verganti, S., & Starkey, M. (2021) · Veterinary Pathology · doi:10.1177/0300985821996658 · Cited by 32 · see citing works
Shi, Y., He, R., Zhuang, Z., Ren, J., Wang, Z., Liu, Y., Wu, J., Jiang, S., & Wang, K. (2020) · Journal of Cellular Biochemistry · doi:10.1002/jcb.29622 · Cited by 31 · see citing works
Comparative oncology approach to drug repurposing in osteosarcoma
Parrales, A., McDonald, P. R., Ottomeyer, M., Roy, A., Shoenen, F. J., Broward, M. A., Bruns, T., Thamm, D. H., Weir, S. J., Neville, K. A., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0194224 · Cited by 31 · see citing works
Intra- and interspecies gene expression models for predicting drug response in canine osteosarcoma
Fowles, J. S., Brown, K. C., Hess, A. M., Duval, D. L., & Gustafson, D. L. (2016) · BMC Bioinformatics · doi:10.1186/s12859-016-0942-8 · Cited by 30 · see citing works
- Authors
- Paoloni, M., Davis, S., Lana, S., Withrow, S., Sangiorgi, L., Picci, P., Hewitt, S., Triche, T., Meltzer, P., & Khanna, C.
- Affiliations
- National Institutes of Health (US)
- Colorado State University (US)
- Istituto Ortopedico Rizzoli (IT)
- University of Southern California (US)
- Corresponding author
- Paoloni, Melissa
- Venue
- BMC Genomics
- Published
- 2009
- Volume
- 10
- Issue
- 1
- Pages
- 625
- ISSN
- 1471-2164 (ISSN-L)
- PMC
- PMC2803201
- OpenAlex
- W2116599555
- Cited by
- 291
- References
- 52
- Citations by year
- 2026: 10 · 2025: 18 · 2024: 13 · 2023: 24 · 2022: 15 · 2021: 22 · 2020: 32 · 2019: 16 · 2018: 17 · 2017: 11 · 2016: 18 · 2015: 18 · 2014: 17 · 2013: 13 · 2012: 19
- FWCI
- 13.23
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Genomics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Colorado State University
- National Human Genome Research Institute
- National Cancer Institute
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Veterinary Oncology Research
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Sarcoma Diagnosis and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
- Keywords
- canine osteosarcoma, pediatric osteosarcoma, lung metastasis, comparative oncology, cross-species gene expression, interleukin-8, GLAST, prognostic factors, orthologs
- MeSH terms
- Animals, Child, Dogs, Humans, RNA, Neoplasm, Osteosarcoma, Cluster Analysis, Interleukin-8, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Genomics, Excitatory Amino Acid Transporter 1, Cell Line, Tumor, Comparative Genomic Hybridization
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review