NKD2, a negative regulator of Wnt signaling, suppresses tumor growth and metastasis in osteosarcoma

Oncogene

Volumn 34, Issue 39, 2015, Pages 5069-5079

  Zhao, S ^a   Kurenbekova, L ^a   Gao, Y ^a   Roos, A ^a   Creighton, C J ^a   Rao, P ^a   Hicks, J ^a   Man, T K ^a   Lau, C ^a   Brown, A M C ^b   Jones, S N ^c   Lazar, A J ^d   Ingram, D ^d   Lev, D ^e   Donehower, L A ^a   Yustein, J T ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d UNIVERSITY OF TEXAS   (United States)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CRE RECOMBINASE; DICKKOPF 3 PROTEIN; NAKED CUTICLE HOMOLOG 2 PROTEIN; PROTEIN P53; REGULATOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; NKD2 PROTEIN, MOUSE;

ALLELE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; GENETICALLY ENGINEERED MOUSE STRAIN; GENOMIC INSTABILITY; GENOTYPE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; METASTASIS INHIBITION; METASTASIS POTENTIAL; MICROARRAY ANALYSIS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; OSTEOSARCOMA; OSTEOSARCOMA CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR GROWTH; TUMOR LOCALIZATION; TUMOR VOLUME; UPREGULATION; WNT SIGNALING PATHWAY; ANIMAL; BONE TUMOR; METABOLISM; METASTASIS; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; BONE NEOPLASMS; CARRIER PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; MICE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; OSTEOSARCOMA; WNT SIGNALING PATHWAY;

EID: 84942550511     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.429     Document Type: Article

References (46)

1. Ottaviani G, Jaffe N. The epidemiology of osteosarcoma. Cancer Treat Res 2009; 152: 3-13.
2. Wang LL. Biology of osteogenic sarcoma. Cancer J 2005; 11: 294-305.
3. Bacci G, Briccoli A, Rocca M, Ferrari S, Donati D, Longhi A et al. Neoadjuvant chemotherapy for osteosarcoma of the extremities with metastases at presentation: recent experience at the Rizzoli Institute in 57 patients treated with cisplatin, doxorubicin, and a high dose of methotrexate and ifosfamide. Ann Oncol 2003; 14: 1126-1134.
4. Kager L, Zoubek A, Potschger U, Kastner U, Flege S, Kempf-Bielack B et al. Primary metastatic osteosarcoma: presentation and outcome of patients treated on neoadjuvant Cooperative Osteosarcoma Study Group protocols. J Clin Oncol 2003; 21: 2011-2018.
5. Meyers PA, Heller G, Healey JH, Huvos A, Applewhite A, Sun M et al. Osteogenic sarcoma with clinically detectable metastasis at initial presentation. J Clin Oncol 1993; 11: 449-453.
6. Chen X, Bahrami A, Pappo A, Easton J, Dalton J, Hedlund E et al. Recurrent somatic structural variations contribute to tumorigenesis in pediatric osteosarcoma. Cell Rep 2014; 7: 104-112.
7. Kansara M, Thomas DM. Molecular pathogenesis of osteosarcoma. DNA Cell Biol 2007; 26: 1-18.
8. Petitjean A, Mathe E, Kato S, Ishioka C, Tavtigian SV, Hainaut P et al. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum Mutat 2007; 28: 622-629.
9. Brosh R, Rotter V. When mutants gain new powers: news from the mutant p53 field. Nat Rev Cancer 2009; 9: 701-713.
10. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA Jr., Butel JS et al. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992; 356: 215-221.
11. Donehower LA, Lozano G. 20 years studying p53 functions in genetically engineered mice. Nat Rev Cancer 2009; 9: 831-841.
12. Liu G, McDonnell TJ, Montes de Oca Luna R, Kapoor M, Mims B, El-Naggar AK et al. High metastatic potential in mice inheriting a targeted p53 missense mutation. Proc Natl Acad Sci USA 2000; 97: 4174-4179.
13. Olive KP, Tuveson DA, Ruhe ZC, Yin B, Willis NA, Bronson RT et al. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004; 119: 847-860.
14. Feng W, Shen L, Wen S, Rosen DG, Jelinek J, Hu X et al. Correlation between CpG methylation profiles and hormone receptor status in breast cancers. Breast Cancer Res 2007; 9: R57.
15. Lauvrak SU, Munthe E, Kresse SH, Stratford EW, Namlos HM, Meza-Zepeda LA et al. Functional characterisation of osteosarcoma cell lines and identification of mRNAs and miRNAs associated with aggressive cancer phenotypes. Br J Cancer 2013; 109: 2228-2236.
16. Baranwal S, Alahari SK. miRNA control of tumor cell invasion and metastasis. Int J Cancer 2009; 126: 1283-1290.
17. Luu HH, Kang Q, Park JK, Si W, Luo Q, Jiang W et al. An orthotopic model of human osteosarcoma growth and spontaneous pulmonary metastasis. Clin Exp Metastasis 2005; 22: 319-329.
18. Edamura K, Nasu Y, Takaishi M, Kobayashi T, Abarzua F, Sakaguchi M et al. Adenovirus-mediated REIC/Dkk-3 gene transfer inhibits tumor growth and metastasis in an orthotopic prostate cancer model. Cancer Gene Ther 2007; 14: 765-772.
19. Hsieh SY, Hsieh PS, Chiu CT, Chen WY. Dickkopf-3/REIC functions as a suppressor gene of tumor growth. Oncogene 2004; 23: 9183-9189.
20. Mizobuchi Y, Matsuzaki K, Kuwayama K, Kitazato K, Mure H, Kageji T et al. REIC/Dkk-3 induces cell death in human malignant glioma. Neuro-oncol 2008; 10: 244-253.
21. Veeck J, Bektas N, Hartmann A, Kristiansen G, Heindrichs U, Knuchel R et al. Wnt signalling in human breast cancer: expression of the putative Wnt inhibitor Dickkopf-3 (DKK3) is frequently suppressed by promoter hypermethylation in mammary tumours. Breast Cancer Res 2008; 10: R82.
22. Hoang BH, Kubo T, Healey JH, Yang R, Nathan SS, Kolb EA et al. Dickkopf 3 inhibits invasion and motility of Saos-2 osteosarcoma cells by modulating the Wnt-betacatenin pathway. Cancer Res 2004; 64: 2734-2739.
23. Miretti S, Roato I, Taulli R, Ponzetto C, Cilli M, Olivero M et al. A mouse model of pulmonary metastasis from spontaneous osteosarcoma monitored in vivo by Luciferase imaging. PLoS ONE 2008; 3: e1828.
24. Hong SH, Briggs J, Newman R, Hoffman K, Mendoza A, LeRoith D et al. Murine osteosarcoma primary tumour growth and metastatic progression is maintained after marked suppression of serum insulin-like growth factor I. Int J Cancer 2009; 124: 2042-2049.
25. Hu T, Li C, Cao Z, Van Raay TJ, Smith JG, Willert K et al. Myristoylated Naked2 antagonizes Wnt-beta-catenin activity by degrading Dishevelled-1 at the plasma membrane. J Biol Chem 2010; 285: 13561-13568.
26. Rousset R, Mack JA, Wharton KA Jr., Axelrod JD, Cadigan KM, Fish MP et al. Naked cuticle targets dishevelled to antagonize Wnt signal transduction. Genes Dev 2001; 15: 658-671.
27. Yan D, Wallingford JB, Sun TQ, Nelson AM, Sakanaka C, Reinhard C et al. Cell autonomous regulation of multiple Dishevelled-dependent pathways by mammalian Nkd. Proc Natl Acad Sci USA 2001; 98: 3802-3807.
28. Guo Y, Zi X, Koontz Z, Kim A, Xie J, Gorlick R et al. Blocking Wnt/LRP5 signaling by a soluble receptor modulates the epithelial to mesenchymal transition and suppresses met and metalloproteinases in osteosarcoma Saos-2 cells. J Orthop Res 2007; 25: 964-971.
29. Gotze S, Wolter M, Reifenberger G, Muller O, Sievers S. Frequent promoter hypermethylation of Wnt pathway inhibitor genes in malignant astrocytic gliomas. Int J Cancer 2010; 126: 2584-2593.
30. Nguyen DX, Massague J. Genetic determinants of cancer metastasis. Nat Rev 2007; 8: 341-352.
31. Baron R, Rawadi G. Wnt signaling and the regulation of bone mass. Curr Osteoporos Rep 2007; 5: 73-80.
32. Johnson AS, Couto CG, Weghorst CM. Mutation of the p53 tumor suppressor gene in spontaneously occurring osteosarcomas of the dog. Carcinogenesis 1998; 19: 213-217.
33. Flores RJ, Li Y, Yu A, Shen J, Rao PH, Lau SS et al. A systems biology approach reveals common metastatic pathways in osteosarcoma. BMC Syst Biol 2012; 6: 50.
34. Brennecke P, Arlt MJ, Campanile C, Husmann K, Gvozdenovic A, Apuzzo T et al. CXCR4 antibody treatment suppresses metastatic spread to the lung of intratibial human osteosarcoma xenografts in mice. Clin Exp Metastasis 2014; 31: 339-349.
35. Husmann K, Arlt MJ, Muff R, Langsam B, Bertz J, Born W et al. Matrix Metalloproteinase 1 promotes tumor formation and lung metastasis in an intratibial injection osteosarcoma mouse model. Biochim Biophys Acta 2013; 1832: 347-354.
36. Kimura R, Ishikawa C, Rokkaku T, Janknecht R, Mori N. Phosphorylated c-Jun and Fra-1 induce matrix metalloproteinase-1 and thereby regulate invasion activity of 143B osteosarcoma cells. Biochim Biophys Acta 2011; 1813: 1543-1553.
37. Muff R, Ram Kumar RM, Botter SM, Born W, Fuchs B. Genes regulated in metastatic osteosarcoma: evaluation by microarray analysis in four human and two mouse cell line systems. Sarcoma 2012; 2012: 937506.
38. Cheng JH, She H, Han YP, Wang J, Xiong S, Asahina K et al. Wnt antagonism inhibits hepatic stellate cell activation and liver fibrosis. Am J Physiol 2008; 294: G39-G49.
39. Kanda M, Nomoto S, Okamura Y, Hayashi M, Hishida M, Fujii T et al. Promoter hypermethylation of fibulin 1 gene is associated with tumor progression in hepatocellular carcinoma. Mol Carcinog 2011; 50: 571-579.
40. Wlazlinski A, Engers R, Hoffmann MJ, Hader C, Jung V, Muller M et al. Downregulation of several fibulin genes in prostate cancer. Prostate 2007; 67: 1770-1780.
41. Li C, Franklin JL, Graves-Deal R, Jerome WG, Cao Z, Coffey RJ. Myristoylated Naked2 escorts transforming growth factor alpha to the basolateral plasma membrane of polarized epithelial cells. Proc Natl Acad Sci USA 2004; 101: 5571-5576.
42. Li C, Hao M, Cao Z, Ding W, Graves-Deal R, Hu J et al. Naked2 acts as a cargo recognition and targeting protein to ensure proper delivery and fusion of TGFalpha containing exocytic vesicles at the lower lateral membrane of polarized MDCK cells. Mol Biol Cell 2007; 18: 3081-3093.
43. Liu F, Woitge HW, Braut A, Kronenberg MS, Lichtler AC, Mina M et al. Expression and activity of osteoblast-targeted Cre recombinase transgenes in murine skeletal tissues. Int J Dev Biol 2004; 48: 645-653.
44. Dumble ML, Donehower LA, Lu X. Generation and characterization of p53 mutant mice. Methods Mol Biol 2003; 234: 29-49.
45. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012; 9: 671-675.
46. Molenaar JJ, Koster J, Zwijnenburg DA, van Sluis P, Valentijn LJ, van der Ploeg I et al. Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes. Nature 2012; 483: 589-593.