Hypermethylation of the DLC1 CpG island does not alter gene expression in canine lymphoma

BMC Genetics

Volumn 10, Issue , 2009, Pages

  Bryan, Jeffrey N ^a,b   Jabbes, Mohamed ^b   Berent, Linda M ^c   Arthur, Gerald L ^d   Taylor, Kristen H ^d   Rissetto, Kerry C ^a   Henry, Carolyn J ^a,d   Rahmatpanah, Farah ^d   Rankin, Wendi V ^a   Villamil, Jose A ^a   Lewis, Michael R ^a,e   Caldwell, Charles W ^a,d  

^a UNIVERSITY OF MISSOURI   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

^d University of Missouri   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN DLCI; TRANSCRIPTION FACTOR SP1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B CELL LYMPHOMA; CANCER SURVIVAL; CONTROLLED STUDY; CPG ISLAND; DNA FLANKING REGION; DNA METHYLATION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE SILENCING; GENETIC DIFFERENCE; GENETIC SIMILARITY; MALE; NONHODGKIN LYMPHOMA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYMERASE CHAIN REACTION; PROMOTER REGION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RESTRICTION MAPPING; RNA SEQUENCE; T CELL LYMPHOMA; AMINO ACID SEQUENCE; ANIMAL; ANIMAL DISEASE; CHEMISTRY; DOG; DOG DISEASE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MOLECULAR GENETICS; SEQUENCE ALIGNMENT;

CANIS FAMILIARIS;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; CPG ISLANDS; DNA METHYLATION; DOG DISEASES; DOGS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPHOMA, NON-HODGKIN; MALE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; SEQUENCE ALIGNMENT; TUMOR SUPPRESSOR PROTEINS;

EID: 71049183611     PISSN: None     EISSN: 14712156     Source Type: Journal    
DOI: 10.1186/1471-2156-10-73     Document Type: Article

References (52)

1. Hayes HM, Tarone RE, Cantor KP, Jessen CR, McCurnin DM, Richardson RC. Case-control study of canine malignant lymphoma: positive association with dog owner's use of 2,4-dichlorophenoxyacetic acid herbicides. J Natl Cancer Inst 1991, 83:1226-1231. 10.1093/jnci/83.17.1226, 1870148.
2. Fournel-Fleury C, Magnol JP, Bricaire P, Marchal T, Chabanne L, Delverdier A, Bryon PA, Felman P. Cytohistological and immunological classification of canine malignant lymphomas: comparison with human non-Hodgkin's lymphomas. J Comp Pathol 1997, 117:35-59. 10.1016/S0021-9975(97)80065-5, 9263843.
3. Hansen K, Khanna C. Spontaneous and genetically engineered animal models; use in preclinical cancer drug development. Eur J Cancer 2004, 40:858-880. 10.1016/j.ejca.2003.11.031, 15120042.
4. Greenlee PG, Filippa DA, Quimby FW, Patnaik AK, Calvano SE, Matus RE, Kimmel M, Hurvitz AI, Lieberman PH. Lymphomas in dogs. A morphologic, immunologic, and clinical study. Cancer 1990, 66:480-490. 10.1002/1097-0142(19900801)66:3<480::AID-CNCR2820660314>3.0.CO;2-X, 2364361.
5. Burnett RC, Vernau W, Modiano JF, Olver CS, Moore PF, Avery AC. Diagnosis of canine lymphoid neoplasia using clonal rearrangements of antigen receptor genes. Vet Pathol 2003, 40:32-41. 10.1354/vp.40-1-32, 12627711.
6. Hahn KA, Richardson RC, Hahn EA, Chrisman CL. Diagnostic and prognostic importance of chromosomal aberrations identified in 61 dogs with lymphosarcoma. Vet Pathol 1994, 31:528-540.
7. Lana SE, Ogilvie GK, Hansen RA, Powers BE, Dernell WS, Withrow SJ. Identification of matrix metalloproteinases in canine neoplastic tissue. Am J Vet Res 2000, 61:111-114. 10.2460/ajvr.2000.61.111, 10685678.
8. Valli VE, Vernau W, de Lorimier LP, Graham PS, Moore PF. Canine indolent nodular lymphoma. Vet Pathol 2006, 43:241-256. 10.1354/vp.43-3-241, 16672571.
9. Johnston PB, Bondly C, Micallef IN. Ibritumomab tiuxetan for non-Hodgkin's lymphoma. Expert Rev Anticancer Ther 2006, 6:861-869. 10.1586/14737140.6.6.861, 16761929.
10. Fosmire SP, Thomas R, Jubala CM, Wojcieszyn JW, Valli VE, Getzy DM, Smith TL, Gardner LA, Ritt MG, Bell JS, Freeman KP, Greenfield BE, Lana SE, Kisseberth WC, Helfand SC, Cutter GR, Breen M, Modiano JF. Inactivation of the p16 cyclin-dependent kinase inhibitor in high-grade canine non-Hodgkin's T-cell lymphoma. Vet Pathol 2007, 44:467-478. 10.1354/vp.44-4-467, 17606508.
11. Modiano JF, Breen M, Valli VE, Wojcieszyn JW, Cutter GR. Predictive value of p16 or Rb inactivation in a model of naturally occurring canine non-Hodgkin's lymphoma. Leukemia 2007, 21:184-187. 10.1038/sj.leu.2404392, 16990767.
12. Sokolowska J, Cywinska A, Malicka E. p53 expression in canine lymphoma. J Vet Med A Physiol Pathol Clin Med 2005, 52:172-175.
13. Yuan BZ, Miller MJ, Keck CL, Zimonjic DB, Thorgeirsson SS, Popescu NC. Cloning, characterization, and chromosomal localization of a gene frequently deleted in human liver cancer (DLC-1) homologous to rat RhoGAP. Cancer Res 1998, 58:2196-2199.
14. Xue W, Krasnitz A, Lucito R, Sordella R, Vanaelst L, Cordon-Cardo C, Singer S, Kuehnel F, Wigler M, Powers S, Zender L, Lowe SW. DLC1 is a chromosome 8p tumor suppressor whose loss promotes hepatocellular carcinoma. Genes Dev 2008, 22:1439-1444. 2418580, 18519636, 10.1101/gad.1672608.
15. Wong CM, Lee JM, Ching YP, Jin DY, Ng IO. Genetic and epigenetic alterations of DLC-1 gene in hepatocellular carcinoma. Cancer Res 2003, 63:7646-7651.
16. Sahai E, Marshall CJ. RHO-GTPases and cancer. Nat Rev Cancer 2002, 2:133-142. 10.1038/nrc725, 12635176.
17. Ullmannova-Benson V, Guan M, Zhou X, Tripathi V, Yang XY, Zimonjic DB, Popescu NC. DLC1 tumor suppressor gene inhibits migration and invasion of multiple myeloma cells through RhoA GTPase pathway. Leukemia 2009, 23:383-390. 10.1038/leu.2008.285, 18923442.
18. Yuan BZ, Jefferson AM, Baldwin KT, Thorgeirsson SS, Popescu NC, Reynolds SH. DLC-1 operates as a tumor suppressor gene in human non-small cell lung carcinomas. Oncogene 2004, 23:1405-1411. 10.1038/sj.onc.1207291, 14661059.
19. Goodison S, Yuan J, Sloan D, Kim R, Li C, Popescu NC, Urquidi V. The RhoGAP protein DLC-1 functions as a metastasis suppressor in breast cancer cells. Cancer Res 2005, 65:6042-6053. 1360170, 16024604, 10.1158/0008-5472.CAN-04-3043.
20. Wu PP, Jin YL, Shang YF, Jin Z, Wu P, Huang PL. Restoration of DLC1 gene inhibits proliferation and migration of human colon cancer HT29 cells. Ann Clin Lab Sci 2009, 39:263-269.
21. Liao YC, Si L, Vere White RW, Lo SH. The phosphotyrosine-independent interaction of DLC-1 and the SH2 domain of cten regulates focal adhesion localization and growth suppression activity of DLC-1. J Cell Biol 2007, 176:43-49. 2063623, 17190795, 10.1083/jcb.200608015.
22. Wong CM, Yam JW, Ching YP, Yau TO, Leung TH, Jin DY, Ng IO. Rho GTPase-activating protein deleted in liver cancer suppresses cell proliferation and invasion in hepatocellular carcinoma. Cancer Res 2005, 65:8861-8868. 10.1158/0008-5472.CAN-05-1318, 16204057.
23. Scholz RP, Regner J, Theil A, Erlmann P, Holeiter G, Jahne R, Schmid S, Hausser A, Olayioye MA. DLC1 interacts with 14-3-3 proteins to inhibit RhoGAP activity and block nucleocytoplasmic shuttling. J Cell Sci 2009, 122:92-102. 10.1242/jcs.036251, 19066281.
24. Chan LK, Ko FC, Ng IO, Yam JW. Deleted in liver cancer 1 (DLC1) utilizes a novel binding site for Tensin2 PTB domain interaction and is required for tumor-suppressive function. PLoS ONE 2009, 4:e5572. 2680019, 19440389, 10.1371/journal.pone.0005572.
25. Yam JW, Ko FC, Chan CY, Jin DY, Ng IO. Interaction of deleted in liver cancer 1 with tensin2 in caveolae and implications in tumor suppression. Cancer Res 2006, 66:8367-8372. 10.1158/0008-5472.CAN-05-2850, 16951145.
26. Yang XY, Guan M, Vigil D, Der CJ, Lowy DR, Popescu NC. p120Ras-GAP binds the DLC1 Rho-GAP tumor suppressor protein and inhibits its RhoA GTPase and growth-suppressing activities. Oncogene 2009, 28:1401-1409. 2715999, 19151751, 10.1038/onc.2008.498.
27. Shi H, Guo J, Duff DJ, Rahmatpanah F, Chitima-Matsiga R, Al-Kuhlani M, Taylor KH, Sjahputera O, Andreski M, Wooldridge JE, Caldwell CW. Discovery of novel epigenetic markers in non-Hodgkin's lymphoma. Carcinogenesis 2006, 28:60-70. 10.1093/carcin/bgl092, 16774933.
28. Pelham JT, Irwin PJ, Kay PH. Genomic hypomethylation in neoplastic cells from dogs with malignant lymphoproliferative disorders. Res Vet Sci 2003, 74:101-104. 10.1016/S0034-5288(02)00179-0, 12507572.
29. Bryan JN, Taylor KH, Henry CJ, Selting KA, Rahmatpanah F, Lewis MR, Caldwell CW. DNA methylation in cancer: techniques and preliminary evidence of hypermethylation in canine lymphoma. Cancer Therapy 2008, 6:137-148.
30. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003, 349:2042-2054. 10.1056/NEJMra023075, 14627790.
31. Pang JC, Chang Q, Chung YF, Teo JG, Poon WS, Zhou LF, Kong X, Ng HK. Epigenetic inactivation of DLC-1 in supratentorial primitive neuroectodermal tumor. Hum Pathol 2005, 36:36-43. 10.1016/j.humpath.2004.09.021, 15712180.
32. Kim TY, Jong HS, Song SH, Dimtchev A, Jeong SJ, Lee JW, Kim TY, Kim NK, Jung M, Bang YJ. Transcriptional silencing of the DLC-1 tumor suppressor gene by epigenetic mechanism in gastric cancer cells. Oncogene 2003, 22:3943-3951. 10.1038/sj.onc.1206573, 12813468.
33. Yuan BZ, Durkin ME, Popescu NC. Promoter hypermethylation of DLC-1, a candidate tumor suppressor gene, in several common human cancers. Cancer Genet Cytogenet 2003, 140:113-117. 10.1016/S0165-4608(02)00674-X, 12645648.
34. Ullmannova V, Popescu NC. Expression profile of the tumor suppressor genes DLC-1 and DLC-2 in solid tumors. Int J Oncol 2006, 29:1127-1132.
35. Seng TJ, Low JS, Li H, Cui Y, Goh HK, Wong ML, Srivastava G, Sidransky D, Califano J, Steenbergen RD, Rha SY, Tan J, Hsieh WS, Ambinder RF, Lin X, Chan AT, Tao Q. The major 8p22 tumor suppressor DLC1 is frequently silenced by methylation in both endemic and sporadic nasopharyngeal, esophageal, and cervical carcinomas, and inhibits tumor cell colony formation. Oncogene 2007, 26:934-944. 10.1038/sj.onc.1209839, 16862168.
36. Siegfried Z, Eden S, Mendelsohn M, Feng X, Tsuberi BZ, Cedar H. DNA methylation represses transcription in vivo. Nat Genet 1999, 22:203-206. 10.1038/9727, 10369268.
37. Guan M, Zhou X, Soulitzis N, Spandidos DA, Popescu NC. Aberrant methylation and deacetylation of deleted in liver cancer-1 gene in prostate cancer: potential clinical applications. Clin Cancer Res 2006, 12:1412-1419. 10.1158/1078-0432.CCR-05-1906, 16533763.
38. Butcher DT, Mancini-DiNardo DN, Archer TK, Rodenhiser DI. DNA binding sites for putative methylation boundaries in the unmethylated region of the BRCA1 promoter. Int J Cancer 2004, 111:669-678. 10.1002/ijc.20324, 15252835.
39. Devereux TR, Horikawa I, Anna CH, Annab LA, Afshari CA, Barrett JC. DNA methylation analysis of the promoter region of the human telomerase reverse transcriptase (hTERT) gene. Cancer Res 1999, 59:6087-6090.
40. Dessain SK, Yu H, Reddel RR, Beijersbergen RL, Weinberg RA. Methylation of the human telomerase gene CpG island. Cancer Res 2000, 60:537-541.
41. Nomoto K, Maekawa M, Sugano K, Ushiama M, Fukayama N, Fujita S, Kakizoe T. Methylation status and expression of human telomerase reverse transcriptase mRNA in relation to hypermethylation of the p16 gene in colorectal cancers as analyzed by bisulfite PCR-SSCP. Jpn J Clin Oncol 2002, 32:3-8. 10.1093/jjco/hyf001, 11932355.
42. Zinn RL, Pruitt K, Eguchi S, Baylin SB, Herman JG. hTERT is expressed in cancer cell lines despite promoter DNA methylation by preservation of unmethylated DNA and active chromatin around the transcription start site. Cancer Res 2007, 67:194-201. 10.1158/0008-5472.CAN-06-3396, 17210699.
43. Taylor KH, Pena-Hernandez KE, Davis JW, Arthur GL, Duff DJ, Shi H, Rahmatpanah FB, Sjahputera O, Caldwell CW. Large-scale CpG methylation analysis identifies novel candidate genes and reveals methylation hotspots in acute lymphoblastic leukemia. Cancer Res 2007, 67:2617-2625. 10.1158/0008-5472.CAN-06-3993, 17363581.
44. Fraga MF, Agrelo R, Esteller M. Cross-talk between aging and cancer: the epigenetic language. Ann N Y Acad Sci 2007, 1100:60-74. 10.1196/annals.1395.005, 17460165.
45. Guo J, Burger M, Nimmrich I, Maier S, Becker E, Genc B, Duff D, Rahmatpanah F, Chitma-Matsiga R, Shi H, Berlin K, Huang TH, Caldwell CW. Differential DNA methylation of gene promoters in small B-cell lymphomas. Am J Clin Pathol 2005, 124:430-439. 10.1309/LCGNV77J464LNFD6, 16191512.
46. Rahmatpanah FB, Carstens S, Guo J, Sjahputera O, Taylor KH, Duff D, Shi H, Davis JW, Hooshmand SI, Chitma-Matsiga R, Caldwell CW. Differential DNA methylation patterns of small B-cell lymphoma subclasses with different clinical behavior. Leukemia 2006, 20:1855-1862. 10.1038/sj.leu.2404345, 16900213.
47. Taylor KH, Kramer RS, Davis JW, Guo J, Duff DJ, Xu D, Caldwell CW, Shi H. Ultradeep bisulfite sequencing analysis of DNA methylation patterns in multiple gene promoters by 454 sequencing. Cancer Res 2007, 67:8511-8518. 10.1158/0008-5472.CAN-07-1016, 17875690.
48. Culmsee K, Simon D, Mischke R, Nolte I. Possibilities of flow cytometric analysis for immunophenotypic characterization of canine lymphoma. J Vet Med A Physiol Pathol Clin Med 2001, 48:199-206.
49. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948. 10.1093/bioinformatics/btm404, 17846036.
50. Zdobnov EM, Apweiler R. InterProScan--an integration platform for the signature-recognition methods in InterPro. Bioinformatics 2001, 17:847-848. 10.1093/bioinformatics/17.9.847, 11590104.
51. McCaw DL, Chan AS, Stegner AL, Mooney B, Bryan JN, Turnquist SE, Henry CJ, Alexander H, Alexander S. Proteomics of canine lymphoma identifies potential cancer-specific protein markers. Clin Cancer Res 2007, 13:2496-2503. 10.1158/1078-0432.CCR-06-2699, 17438110.
52. Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 2002, 18:1427-1431. 10.1093/bioinformatics/18.11.1427, 12424112.