Microenvironment alters epigenetic and gene expression profiles in Swarm rat chondrosarcoma tumors

BMC Cancer

Volumn 10, Issue , 2010, Pages

  Hamm, Christopher A ^a   Stevens, Jeff W ^b   Xie, Hehuang ^a,c   Vanin, Elio F ^a   Morcuende, Jose A ^b   Abdulkawy, Hakeem ^a   Seftor, Elisabeth A ^a   Sredni, Simone T ^a   Bischof, Jared M ^a   Wang, Deli ^c   Malchenko, Sergey ^a,c   de Fatima Bonaldo, Maria ^a,c   Casavant, Thomas L ^a   Hendrix, Mary J C ^a,c   Soares, Marcelo B ^a,c  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; PROTEIN C FOS; THYMOSIN BETA4; CTGF PROTEIN, RAT; THYMOSIN; THYMOSIN BETA(4); TUMOR MARKER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER GRADING; CANCER INVASION; CANCER TRANSPLANTATION; CARCINOGENESIS; CHONDROSARCOMA; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LIBRARY; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENOME ANALYSIS; MALE; NONHUMAN; PHENOTYPE; PYROSEQUENCING; RAT; SERIAL ANALYSIS OF GENE EXPRESSION; SPRAGUE DAWLEY RAT; SURVIVAL RATE; TUMOR GROWTH; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; CARTILAGE; COMPARATIVE STUDY; DNA MICROARRAY; GENETIC EPIGENESIS; GENETICS; HUMAN; LUNG TUMOR; METABOLISM; METASTASIS; MOUSE; NUDE MOUSE; ONCOGENE; PATHOLOGY; PHYSIOLOGY; SUBCUTANEOUS DRUG ADMINISTRATION; TIBIA; TRANSPLANTATION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CARTILAGE; CHONDROSARCOMA; CONNECTIVE TISSUE GROWTH FACTOR; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENES, FOS; HUMANS; INJECTIONS, SUBCUTANEOUS; LUNG NEOPLASMS; MALE; MICE; MICE, NUDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; RATS; RATS, SPRAGUE-DAWLEY; THYMOSIN; TIBIA; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL;

EID: 77956491337     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-10-471     Document Type: Article

References (65)

1. Ozaki T, Lindner N, Hillmann A, Rodl R, Blasius S, Winkelmann W. Influence of intralesional surgery on treatment outcome of chondrosarcoma. Cancer 1996, 77(7):1292-1297. 10.1002/(SICI)1097-0142(19960401)77:7<1292::AID-CNCR10>3.0.CO;2-X, 8608505.
2. Sandberg AA, Bridge JA. Updates on the cytogenetics and molecular genetics of bone and soft tissue tumors: osteosarcoma and related tumors. Cancer Genet Cytogenet 2003, 145(1):1-30. 10.1016/S0165-4608(03)00105-5, 12885459.
3. Gitelis S, Bertoni F, Picci P, Campanacci M. Chondrosarcoma of bone. The experience at the Istituto Ortopedico Rizzoli. J Bone Joint Surg Am 1981, 63(8):1248-1257.
4. Mitchell AD, Ayoub K, Mangham DC, Grimer RJ, Carter SR, Tillman RM. Experience in the treatment of dedifferentiated chondrosarcoma. J Bone Joint Surg Br 2000, 82(1):55-61. 10.1302/0301-620X.82B1.9020, 10697315.
5. Aigner T. Towards a new understanding and classification of chondrogenic neoplasias of the skeleton--biochemistry and cell biology of chondrosarcoma and its variants. Virchows Arch 2002, 441(3):219-230. 10.1007/s00428-002-0641-x, 12242518.
6. Breitkreutz D, Diaz de Leon L, Paglia L, Gay S, Swarm RL, Stern R. Histological and biochemical studies of a transplantable rat chondrosarcoma. Cancer Res 1979, 39(12):5093-5100.
7. Kenan S, Steiner GC. Experimental transplantation of the Swarm rat chondrosarcoma into bone: radiological and pathological studies. J Orthop Res 1991, 9(3):445-451. 10.1002/jor.1100090317, 2010849.
8. Grimaud E, Damiens C, Rousselle AV, Passuti N, Heymann D, Gouin F. Bone remodelling and tumour grade modifications induced by interactions between bone and swarm rat chondrosarcoma. Histol Histopathol 2002, 17(4):1103-1111.
9. Hamm CA, Xie H, Costa FF, Vanin EF, Seftor EA, Sredni ST, Bischof J, Wang D, Bonaldo MF, Hendrix MJ, et al. Global demethylation of rat chondrosarcoma cells after treatment with 5-aza-2'-deoxycytidine results in increased tumorigenicity. PLoS One 2009, 4(12):e8340. 10.1371/journal.pone.0008340, 2790612, 20019818.
10. Velculescu VE, Zhang L, Vogelstein B, Kinzler KW. Serial analysis of gene expression. Science 1995, 270(5235):484-487. 10.1126/science.270.5235.484, 7570003.
11. Stevens JW, Patil SR, Jordan DK, Kimura JH, Morcuende JA. Cytogenetics of swarm rat chondrosarcoma. Iowa Orthop J 2005, 25:135-140. 1888785, 16089086.
12. Morcuende JA, Huang XD, Stevens J, Kucaba TA, Brown B, Abdulkawy H, Scheetz TE, Malchenko S, Bonaldo F, Casavant TL, et al. Identification and initial characterization of 6,000 expressed sequenced tags (ESTs) from rat normal-growing cartilage and swarm rat chondrosarcoma cDNA libraries. Iowa Orthop J 2002, 22:28-34. 1888380, 12180607.
13. Rosenthal DI, Schiller AL, Mankin HJ. Chondrosarcoma: correlation of radiological and histological grade. Radiology 1984, 150(1):21-26.
14. O'Neal LW, Ackerman LV. Chondrosarcoma of bone. Cancer 1952, 5(3):551-577. 10.1002/1097-0142(195205)5:3<551::AID-CNCR2820050317>3.0.CO;2-Z, 14925925.
15. Adams MD, Soares MB, Kerlavage AR, Fields C, Venter JC. Rapid cDNA sequencing (expressed sequence tags) from a directionally cloned human infant brain cDNA library. Nat Genet 1993, 4(4):373-380. 10.1038/ng0893-373, 8401585.
16. Anisimov SV. A large-scale screening of the normalized mammalian mitochondrial gene expression profiles. Genet Res 2005, 86(2):127-138. 10.1017/S0016672305007718, 16356286.
17. Zhu LJ, Altmann SW. mRNA and 18S-RNA coapplication-reverse transcription for quantitative gene expression analysis. Anal Biochem 2005, 345(1):102-109. 10.1016/j.ab.2005.07.028, 16139233.
18. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45. 10.1093/nar/29.9.e45, 55695, 11328886.
19. Rose JK, Gallione CJ. Nucleotide sequences of the mRNA's encoding the vesicular stomatitis virus G and M proteins determined from cDNA clones containing the complete coding regions. J Virol 1981, 39(2):519-528. 171362, 6268840.
20. King KB, Kimura JH. The establishment and characterization of an immortal cell line with a stable chondrocytic phenotype. J Cell Biochem 2003, 89(5):992-1004. 10.1002/jcb.10571, 12874833.
21. Hendrix MJ, Seftor EA, Seftor RE, Fidler IJ. A simple quantitative assay for studying the invasive potential of high and low human metastatic variants. Cancer Lett 1987, 38(1-2):137-147. 10.1016/0304-3835(87)90209-6, 3690504.
22. Sood AK, Coffin JE, Schneider GB, Fletcher MS, DeYoung BR, Gruman LM, Gershenson DM, Schaller MD, Hendrix MJ. Biological significance of focal adhesion kinase in ovarian cancer: role in migration and invasion. Am J Pathol 2004, 165(4):1087-1095. 1618649, 15466376.
23. Ruijter JM, Van Kampen AH, Baas F. Statistical evaluation of SAGE libraries: consequences for experimental design. Physiol Genomics 2002, 11(2):37-44.
24. Yang AS, Estecio MR, Doshi K, Kondo Y, Tajara EH, Issa JP. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res 2004, 32(3):e38. 10.1093/nar/gnh032, 373427, 14973332.
25. Aigner T, Muller S, Neureiter D, Illstrup DM, Kirchner T, Bjornsson J. Prognostic relevance of cell biologic and biochemical features in conventional chondrosarcomas. Cancer 2002, 94(8):2273-2281. 10.1002/cncr.10461, 12001127.
26. Soderstrom M, Ekfors T, Bohling T, Aho A, Aro HT, Vuorio E. Cysteine proteinases in chondrosarcomas. Matrix Biol 2001, 19(8):717-725. 10.1016/S0945-053X(00)00124-4, 11223331.
27. Soderstrom M, Aro HT, Ahonen M, Johansson N, Aho A, Ekfors T, Bohling T, Kahari VM, Vuorio E. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human chondrosarcomas. Apmis 2001, 109(4):305-315. 10.1034/j.1600-0463.2001.d01-125.x, 11469503.
28. Blain EJ, Mason DJ, Duance VC. The effect of thymosin beta4 on articular cartilage chondrocyte matrix metalloproteinase expression. Biochem Soc Trans 2002, 30(Pt 6):879-882.
29. Kobayashi T, Okada F, Fujii N, Tomita N, Ito S, Tazawa H, Aoyama T, Choi SK, Shibata T, Fujita H, et al. Thymosin-beta4 regulates motility and metastasis of malignant mouse fibrosarcoma cells. Am J Pathol 2002, 160(3):869-882. 1867176, 11891186.
30. Eferl R, Wagner EF. AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 2003, 3(11):859-868. 10.1038/nrc1209, 14668816.
31. Weisstein JS, Majeska RJ, Klein MJ, Einhorn TA. Detection of c-fos expression in benign and malignant musculoskeletal lesions. J Orthop Res 2001, 19(3):339-345. 10.1016/S0736-0266(00)90020-2, 11398843.
32. Wang ZQ, Grigoriadis AE, Mohle-Steinlein U, Wagner EF. A novel target cell for c-fos-induced oncogenesis: development of chondrogenic tumours in embryonic stem cell chimeras. EMBO J 1991, 10(9):2437-2450. 452939, 1714376.
33. Tuckermann JP, Vallon R, Gack S, Grigoriadis AE, Porte D, Lutz A, Wagner EF, Schmidt J, Angel P. Expression of collagenase-3 (MMP-13) in c-fos-induced osteosarcomas and chondrosarcomas is restricted to a subset of cells of the osteo-/chondrogenic lineage. Differentiation 2001, 69(1):49-57. 10.1046/j.1432-0436.2001.690105.x, 11776394.
34. Shakunaga T, Ozaki T, Ohara N, Asaumi K, Doi T, Nishida K, Kawai A, Nakanishi T, Takigawa M, Inoue H. Expression of connective tissue growth factor in cartilaginous tumors. Cancer 2000, 89(7):1466-1473. 10.1002/1097-0142(20001001)89:7<1466::AID-CNCR8>3.0.CO;2-G, 11013359.
35. Kondo S, Kubota S, Mukudai Y, Moritani N, Nishida T, Matsushita H, Matsumoto S, Sugahara T, Takigawa M. Hypoxic regulation of stability of connective tissue growth factor/CCN2 mRNA by 3'-untranslated region interacting with a cellular protein in human chondrosarcoma cells. Oncogene 2006, 25(7):1099-1110. 10.1038/sj.onc.1209129, 16247469.
36. Chang CC, Shih JY, Jeng YM, Su JL, Lin BZ, Chen ST, Chau YP, Yang PC, Kuo ML. Connective tissue growth factor and its role in lung adenocarcinoma invasion and metastasis. J Natl Cancer Inst 2004, 96(5):364-375. 10.1093/jnci/djh059, 14996858.
37. Pan LH, Beppu T, Kurose A, Yamauchi K, Sugawara A, Suzuki M, Ogawa A, Sawai T. Neoplastic cells and proliferating endothelial cells express connective tissue growth factor (CTGF) in glioblastoma. Neurol Res 2002, 24(7):677-683. 10.1179/016164102101200573, 12392205.
38. Lee FY, Mankin HJ, Fondren G, Gebhardt MC, Springfield DS, Rosenberg AE, Jennings LC. Chondrosarcoma of bone: an assessment of outcome. J Bone Joint Surg Am 1999, 81(3):326-338.
39. Shahrzad S, Bertrand K, Minhas K, Coomber BL. Induction of DNA hypomethylation by tumor hypoxia. Epigenetics 2007, 2(2):119-125. 10.4161/epi.2.2.4613, 17965619.
40. Hoffmann MJ, Schulz WA. Causes and consequences of DNA hypomethylation in human cancer. Biochem Cell Biol 2005, 83(3):296-321. 10.1139/o05-036, 15959557.
41. Eden A, Gaudet F, Waghmare A, Jaenisch R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science 2003, 300(5618):455. 10.1126/science.1083557, 12702868.
42. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, Leonhardt H, Jaenisch R. Induction of tumors in mice by genomic hypomethylation. Science 2003, 300(5618):489-492. 10.1126/science.1083558, 12702876.
43. Bromme D, Okamoto K, Wang BB, Biroc S. Human cathepsin O2, a matrix protein-degrading cysteine protease expressed in osteoclasts. Functional expression of human cathepsin O2 in Spodoptera frugiperda and characterization of the enzyme. J Biol Chem 1996, 271(4):2126-2132. 10.1074/jbc.271.4.2126, 8567669.
44. Cha HJ, Jeong MJ, Kleinman HK. Role of thymosin beta4 in tumor metastasis and angiogenesis. J Natl Cancer Inst 2003, 95(22):1674-1680.
45. Ridley A. Molecular switches in metastasis. Nature 2000, 406(6795):466-467. 10.1038/35020170, 10952292.
46. Huang WQ, Wang QR. Bone marrow endothelial cells secrete thymosin beta4 and AcSDKP. Exp Hematol 2001, 29(1):12-18. 10.1016/S0301-472X(00)00634-2, 11164101.
47. Papachristou DJ, Papachristou GI, Papaefthimiou OA, Agnantis NJ, Basdra EK, Papavassiliou AG. The MAPK-AP-1/-Runx2 signalling axes are implicated in chondrosarcoma pathobiology either independently or via up-regulation of VEGF. Histopathology 2005, 47(6):565-574.
48. Tan TW, Yang WH, Lin YT, Hsu SF, Li TM, Kao ST, Chen WC, Fong YC, Tang CH. Cyr61 increases migration and MMP-13 expression via alphavbeta3 integrin, FAK, ERK and AP-1-dependent pathway in human chondrosarcoma cells. Carcinogenesis 2009, 30(2):258-268. 10.1093/carcin/bgn284, 19126648.
49. Hou CH, Hsiao YC, Fong YC, Tang CH. Bone morphogenetic protein-2 enhances the motility of chondrosarcoma cells via activation of matrix metalloproteinase-13. Bone 2009, 44(2):233-242. 10.1016/j.bone.2008.09.021, 19038372.
50. Yosimichi G, Nakanishi T, Nishida T, Hattori T, Takano-Yamamoto T, Takigawa M. CTGF/Hcs24 induces chondrocyte differentiation through a p38 mitogen-activated protein kinase (p38MAPK), and proliferation through a p44/42 MAPK/extracellular-signal regulated kinase (ERK). Eur J Biochem 2001, 268(23):6058-6065. 10.1046/j.0014-2956.2001.02553.x, 11732999.
51. Masi L, Malentacchi C, Campanacci D, Franchi A. Transforming growth factor-beta isoform and receptor expression in chondrosarcoma of bone. Virchows Arch 2002, 440(5):491-497. 10.1007/s00428-001-0544-2, 12021923.
52. Furumatsu T, Nishida K, Kawai A, Namba M, Inoue H, Ninomiya Y. Human chondrosarcoma secretes vascular endothelial growth factor to induce tumor angiogenesis and stores basic fibroblast growth factor for regulation of its own growth. Int J Cancer 2002, 97(3):313-322. 10.1002/ijc.1607, 11774282.
53. Hoshijima M, Hattori T, Inoue M, Araki D, Hanagata H, Miyauchi A, Takigawa M. CT domain of CCN2/CTGF directly interacts with fibronectin and enhances cell adhesion of chondrocytes through integrin alpha5beta1. FEBS Lett 2006, 580(5):1376-1382. 10.1016/j.febslet.2006.01.061, 16457822.
54. Wu S, Platteau A, Chen S, McNamara G, Whitsett J, Bancalari E. Conditional Over-expression of Connective Tissue Growth Factor Disrupts Postnatal Lung Development. Am J Respir Cell Mol Biol 2009, 42(5):552-63. 10.1165/rcmb.2009-0068OC, 19541844.
55. Rishikof DC, Ricupero DA, Kuang PP, Liu H, Goldstein RH. Interleukin-4 regulates connective tissue growth factor expression in human lung fibroblasts. J Cell Biochem 2002, 85(3):496-504. 10.1002/jcb.10144, 11967989.
56. Shimo T, Nakanishi T, Nishida T, Asano M, Kanyama M, Kuboki T, Tamatani T, Tezuka K, Takemura M, Matsumura T, et al. Connective tissue growth factor induces the proliferation, migration, and tube formation of vascular endothelial cells in vitro, and angiogenesis in vivo. J Biochem 1999, 126(1):137-145.
57. Brigstock DR. Regulation of angiogenesis and endothelial cell function by connective tissue growth factor (CTGF) and cysteine-rich 61 (CYR61). Angiogenesis 2002, 5(3):153-165. 10.1023/A:1023823803510, 12831056.
58. Xia W, Kong W, Wang Z, Phan TT, Lim IJ, Longaker MT, Yang GP. Increased CCN2 transcription in keloid fibroblasts requires cooperativity between AP-1 and SMAD binding sites. Ann Surg 2007, 246(5):886-895. 10.1097/SLA.0b013e318070d54f, 17968183.
59. Noma T, Glick AB, Geiser AG, O'Reilly MA, Miller J, Roberts AB, Sporn MB. Molecular cloning and structure of the human transforming growth factor-beta 2 gene promoter. Growth Factors 1991, 4(4):247-255. 10.3109/08977199109043910, 1764261.
60. Caricasole A, Ward A. Transactivation of mouse insulin-like growth factor II (IGF-II) gene promoters by the AP-1 complex. Nucleic Acids Res 1993, 21(8):1873-1879. 10.1093/nar/21.8.1873, 309427, 8493103.
61. Cho ML, Jung YO, Moon YM, Min SY, Yoon CH, Lee SH, Park SH, Cho CS, Jue DM, Kim HY. Interleukin-18 induces the production of vascular endothelial growth factor (VEGF) in rheumatoid arthritis synovial fibroblasts via AP-1-dependent pathways. Immunol Lett 2006, 103(2):159-166. 10.1016/j.imlet.2005.10.020, 16368150.
62. Piechaczyk M, Blanchard JM. c-fos proto-oncogene regulation and function. Crit Rev Oncol Hematol 1994, 17(2):93-131. 10.1016/1040-8428(94)90021-3, 7818789.
63. Karin M, Liu Z, Zandi E. AP-1 function and regulation. Curr Opin Cell Biol 1997, 9(2):240-246. 10.1016/S0955-0674(97)80068-3, 9069263.
64. Lo YY, Cruz TF. Involvement of reactive oxygen species in cytokine and growth factor induction of c-fos expression in chondrocytes. J Biol Chem 1995, 270(20):11727-11730. 10.1074/jbc.270.20.11727, 7744816.
65. Yang SP, Lee HJ, Su Y. Molecular cloning and structural characterization of the functional human thymosin beta4 gene. Mol Cell Biochem 2005, 272(1-2):97-105. 10.1007/s11010-005-7642-4, 16010977.