Expression and regulation of the endogenous retrovirus 3 in Hodgkin's lymphoma cells

Frontiers in Oncology

Volumn 3 JUL, Issue , 2013, Pages

  Kewitz, Stefanie ^a   Staege, Martin Sebastian ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Endogenous retrovirus ERV3; Gene expression; Histone deacetylase inhibitor; Hodgkin's lymphoma; Hypoxia mimetic cobalt(II) chloride

Indexed keywords

COBALT CHLORIDE; COMPLEMENTARY DNA; VORINOSTAT;

ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; ENDOGENOUS RETROVIRUS; GENE EXPRESSION; HUMAN; HUMAN CELL; INCUBATION TIME; LARGE CELL LYMPHOMA; MOLECULARLY TARGETED THERAPY; NONHUMAN; NUCLEOTIDE SEQUENCE; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; TUMOR SUPPRESSOR GENE; VALIDATION STUDY; VIRUS EXPRESSION;

EID: 84891077034     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00179     Document Type: Article

References (76)

1. Tzankov A, and Dirnhofer S. Pathobiology of classical Hodgkin lymphoma. Pathobiology (2006) 73:107-25. doi:10.1159/000095558
2. Drexler HG, and Minowada J. Hodgkin's disease derived cell lines: a review. Hum Cell (2009) 5:42-53.
3. Schwering I, Bräuninger A, Klein U, Jungnickel B, Tinguely M, Diehl V, et al. Loss of the B-lineage-specific gene expression program in Hodgkin and Reed-Sternberg cells of Hodgkin lymphoma. Blood (2003) 101:1505-12. doi:10.1182/blood-2002-03-0839
4. Staege MS, Banning-Eichenseer U, Weissflog G, Volkmer I, Burdach S, Richter G, et al. Gene expression profiles of Hodgkin's lymphoma cell lines with different sensitivity to cytotoxic drugs. Exp Hematol (2008) 36:886-96. doi:10.1016/j.exphem.2008.02.014
5. Körholz D, Claviez A, Hasenclever D, Kluge R, Hirsch W, Kamprad F, et al. The concept of the GPOH-HD 2003 therapy study for pediatric Hodgkin's disease: evolution in the tradition of the DAL/GPOH studies. Klin Padiatr (2004) 216:150-6. doi:10.1055/s-2004-822627
6. Mauz-Körholz C, Hasenclever D, Dörffel W, Ruschke K, Pelz T, Voigt A, et al. Procarbazine-free OEPA-COPDAC chemotherapy in boys and standard OPPA-COPP in girls have comparable effectiveness in pediatric Hodgkin's lymphoma: the GPOH-HD-2002 study. J Clin Oncol (2010) 28:3680-6. doi:10.1200/JCO.2009.26.9381
7. Lamprecht B, Walter K, Kreher S, Kumar R, Hummel M, Lenze D, et al. Derepression of an endogenous long terminal repeat activates the CSF1R proto-oncogene in human lymphoma. Nat Med (2010) 16:571-9. doi:10.1038/nm.2129
8. Weiss RA. The discovery of endogenous retroviruses. Retrovirology (2006) 3:67. doi:10.1186/1742-4690-3-S1-S67
9. Buzdin A. Human-specific endogenous retroviruses. ScientificWorldJournal (2007) 7:1848-68. doi:10.1100/tsw.2007.270
10. Basta HA, Cleveland SB, Clinton RA, Dimitrov AG, and McClure MA. Evolution of teleost fish retroviruses: characterization of new retroviruses with cellular genes. J Virol (2009) 83:10152-62. doi:10.1128/JVI.02546-08
11. Du J, Tian Z, Hans CS, Laten HM, Cannon SB, Jackson SA, et al. Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. Plant J (2010) 63:584-98. doi:10.1111/j.1365-313X.2010.04263.x
12. Cui J, and Holmes EC. Endogenous RNA viruses of plants in insect genomes. Virology (2012) 427:77-9. doi:10.1016/j.virol.2012.02.014
13. Harzmann R, Löwer J, Löwer R, Bichler KH, and Kurth R. Synthesis of retrovirus-like particles in testicular teratocarcinomas. J Urol (1982) 128:1055-9.
14. Stefanov Y, Salenko V, and Glukhov I. Drosophila errantiviruses. Mob Genet Elements (2012) 2:36-45. doi:10.4161/mge.19234
15. Bieda K, Hoffmann A, and Boller K. Phenotypic heterogeneity of human endogenous retrovirus particles produced by teratocarcinoma cell lines. J Gen Virol (2001) 82:591-6.
16. Dupressoir A, Lavialle C, and Heidmann T. From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta (2012) 33:663-71. doi:10.1016/j.placenta.2012.05.005
17. Beyer U, Moll-Rocek J, Moll UM, and Dobbelstein M. Endogenous retrovirus drives hitherto unknown proapoptotic p63 isoforms in the male germ line of humans and great apes. Proc Natl Acad Sci U S A (2011) 108:3624-9. doi:10.1073/pnas.1016201108
18. Meylan F, De Smedt M, Leclercq G, Plum J, Leupin O, Marguerat S, et al. Negative thymocyte selection to HERV-K18 superantigens in humans. Blood (2005) 105:4377-82. doi:10.1182/blood-2004-07-2596
19. Sutkowski N, Conrad B, Thorley-Lawson DA, and Huber BT. Epstein-Barr virus transactivates the human endogenous retrovirus HERV-K18 that encodes a superantigen. Immunity (2001) 15:579-89. doi:10.1016/S1074-7613(01)00210-2
20. Wang-Johanning F, Radvanyi L, Rycaj K, Plummer JB, Yan P, Sastry KJ, et al. Human endogenous retrovirus K triggers an antigen-specific immune response in breast cancer patients. Cancer Res (2008) 68:5869-77. doi:10.1158/0008-5472.CAN-07-6838
21. Hahn S, Ugurel S, Hanschmann KM, Strobel H, Tondera C, Schadendorf D, et al. Serological response to human endogenous retrovirus K in melanoma patients correlates with survival probability. AIDS Res Hum Retroviruses (2008) 4:717-23. doi:10.1089/aid.2007.0286
22. Schiavetti F, Thonnard J, Colau D, Boon T, and Coulie PG. A human endogenous retroviral sequence encoding an antigen recognized on melanoma by cytolytic T lymphocytes. Cancer Res (2002) 62:5510-6.
23. Mullins CS, and Linnebacher M. Endogenous retrovirus sequences as a novel class of tumor-specific antigens: an example of HERV-H env encoding strong CTL epitopes. Cancer Immunol Immunother (2012) 61:1093-100. doi:10.1007/s00262-011-1183-3
24. Takahashi Y, Harashima N, Kajigaya S, Yokoyama H, Cherkasova E, McCoy JP, et al. Regression of human kidney cancer following allogeneic stem cell transplantation is associated with recognition of an HERV-E antigen by T cells. J Clin Invest (2008) 118:1099-109. doi:10.1172/JCI34409
25. Wang-Johanning F, Rycaj K, Plummer JB, Li M, Yin B, Frerich K, et al. Immunotherapeutic potential of anti-human endogenous retrovirus-K envelope protein antibodies in targeting breast tumors. J Natl Cancer Inst (2012) 104:189-210. doi:10.1093/jnci/djr540
26. Sacha JB, Kim IJ, Chen L, Ullah JH, Goodwin DA, Simmons HA, et al. Vaccination with cancer-and HIV infection-associated endogenous retrotransposable elements is safe and immunogenic. J Immunol (2012) 189:1467-79. doi:10.4049/jimmunol.1200079
27. Peggs KS, Hunter A, Chopra R, Parker A, Mahendra P, Milligan D, et al. Clinical evidence of a graft-versus-Hodgkin's-lymphoma effect after reduced-intensity allogeneic transplantation. Lancet (2005) 365:1934-41. doi:10.1016/S0140-6736(05)66659-7
28. Staege MS, Hattenhorst UE, Neumann UE, Hutter C, Foja S, and Burdach S. DNA-microarrays as tools for the identification of tumor specific gene expression profiles: applications in tumor biology, diagnosis and therapy. Klin Padiatr (2003) 215:135-9. doi:10.1055/s-2003-39371
29. Drexler HG, Gaedicke G, Lok MS, Diehl V, and Minowada J. Hodgkin's disease derived cell lines HDLM-2 and L-428: comparison of morphology, immunological and isoenzyme profiles. Leuk Res (1986) 10:487-500. doi:10.1016/0145-2126(86)90084-6
30. Kamesaki H, Fukuhara S, Tatsumi E, Uchino H, Yamabe H, Miwa H, et al. Cytochemical, immunologic, chromosomal, and molecular genetic analysis of a novel cell line derived from Hodgkin's disease. Blood (1986) 68:285-92.
31. Wolf J, Kapp U, Bohlen H, Kornacker M, Schoch C, Stahl B, et al. Peripheral blood mononuclear cells of a patient with advanced Hodgkin's lymphoma give rise to permanently growing Hodgkin-Reed Sternberg cells. Blood (1996) 87:3418-28.
32. Schaadt M, Fonatsch C, Kirchner H, and Diehl V. Establishment of a malignant, Epstein-Barr-virus (EBV)-negative cell-line from the pleura effusion of a patient with Hodgkin's disease. Blut (1979) 38:185-90. doi:10.1007/BF01007965
33. Diehl V, Kirchner HH, Burrichter H, Stein H, Fonatsch C, Gerdes J, et al. Characteristics of Hodgkin's disease-derived cell lines. Cancer Treat Rep (1982) 66:615-32.
34. Schuhmacher M, Staege MS, Pajic A, Polack A, Weidle UH, Bornkamm GW, et al. Control of cell growth by c-Myc in the absence of cell division. Curr Biol (1999) 9:1255-8. doi:10.1016/S0960-9822(99)80507-7
35. Pajic A, Spitkovsky D, Christoph B, Kempkes B, Schuhmacher M, Staege MS, et al. Cell cycle activation by c-myc in a Burkitt lymphoma model cell line. Int J Cancer (2000) 87:787-93. doi:10.1002/1097-0215(20000915)87:6<787::AID-IJC4>3.0.CO;2-6
36. Pajic A, Staege MS, Dudziak D, Schuhmacher M, Spitkovsky D, Eissner G, et al. Antagonistic effects of c-myc and Epstein-Barr virus latent genes on the phenotype of human B cells. Int J Cancer (2001) 93:810-6. doi:10.1002/ijc.1404
37. Kewitz S, Bernig T, and Staege MS. Histone deacetylase inhibition restores cisplatin sensitivity of Hodgkin's lymphoma cells. Leuk Res (2012) 36:773-8. doi:10.1016/j.leukres.2012.02.021
38. Livak KJ, and Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) method. Methods (2001) 25:402-8. doi:10.1006/meth.2001.1262
39. Kewitz S, Müller J, Winkler C, and Staege MS. Retinoic acid signaling and immunotherapy of cancer. In: LH Cheng and Y Ito editors. Retinoic Acid: Structure, Metabolism and Roles in Disease. Hauppauge: Nova Science Publishers (2012). p. 87-104.
40. Shehadeh LA, Yu K, Wang L, Guevara A, Singer C, Vance J, et al. SRRM2, a potential blood biomarker revealing high alternative splicing in Parkinson's disease. PLoS ONE (2010) 5:e9104. doi:10.1371/journal.pone.0009104
41. Ji H, Wu G, Zhan X, Nolan A, Koh C, De Marzo A, et al. Cell-type independent MYC target genes reveal a primordial signature involved in biomass accumulation. PLoS ONE (2011) 6:e26057. doi:10.1371/journal.pone.0026057
42. Grigoryev YA, Kurian SM, Nakorchevskiy AA, Burke JP, Campbell D, Head SR, et al. Genome-wide analysis of immune activation in human T and B cells reveals distinct classes of alternatively spliced genes. PLoS ONE (2009) 4:e7906. doi:10.1371/journal.pone.0007906
43. Price AM, Tourigny JP, Forte E, Salinas RE, Dave SS, and Luftig MA. Analysis of Epstein-Barr virus-regulated host gene expression changes through primary B-cell outgrowth reveals delayed kinetics of latent membrane protein 1-mediated NF-κB activation. J Virol (2012) 86:11096-106. doi:10.1128/JVI.01069-12
44. Sturn A, Quackenbush J, and Trajanoski Z. Genesis: cluster analysis of microarray data. Bioinformatics (2002) 18:207-8. doi:10.1093/bioinformatics/18.1.207
45. Abrink M, Larsson E, and Hellman L. Demethylation of ERV3, an endogenous retrovirus regulating the Krüppel-related zinc finger gene H-plk, in several human cell lines arrested during early monocyte development. DNA Cell Biol (1998) 7:27-37. doi:10.1089/dna.1998.17.27
46. Kempkes B, Spitkovsky D, Jansen-Dürr P, Ellwart JW, Kremmer E, Delecluse HJ, et al. B-cell proliferation and induction of early G1-regulating proteins by Epstein-Barr virus mutants conditional for EBNA2. EMBO J (1995) 14:88-96.
47. McClain K, and Wilkowski C. Activation of endogenous retroviral sequences in human leukemia. Biochem Biophys Res Commun (1985) 133:945-50. doi:10.1016/0006-291X(85)91227-6
48. Tomita N, Horii A, Doi S, Yokouchi H, Ogawa M, Mori T, et al. Transcription of human endogenous retroviral long terminal repeat (LTR) sequence in a lung cancer cell line. Biochem Biophys Res Commun (1990) 166:1-10. doi:10.1016/0006-291X(90)91904-7
49. Löwer R, Boller K, Hasenmaier B, Korbmacher C, Müller-Lantzsch N, Löwer J, et al. Identification of human endogenous retroviruses with complex mRNA expression and particle formation. Proc Natl Acad Sci U S A (1993) 90:4480-4. doi:10.1073/pnas.90.10.4480
50. Patience C, Simpson GR, Colletta AA, Welch HM, Weiss RA, and Boyd MT. Human endogenous retrovirus expression and reverse transcriptase activity in the T47D mammary carcinoma cell line. J Virol (1996) 70:2654-7.
51. Wang-Johanning F, Frost AR, Johanning GL, Khazaeli MB, LoBuglio AF, Shaw DR, et al. Expression of human endogenous retrovirus k envelope transcripts in human breast cancer. Clin Cancer Res (2001) 7:1553-60.
52. Balada E, Vilardell-Tarrés M, and Ordi-Ros J. Implication of human endogenous retroviruses in the development of autoimmune diseases. Int Rev Immunol (2010) 29:351-70. doi:10.3109/08830185.2010.485333
53. Antony JM, Deslauriers AM, Bhat RK, Ellestad KK, and Power C. Human endogenous retroviruses and multiple sclerosis: innocent bystanders or disease determinants? Biochim Biophys Acta (2011) 812:162-76. doi:10.1016/j.bbadis.2010.07.016
54. Douville R, Liu J, Rothstein J, and Nath A. Identification of active loci of a human endogenous retrovirus in neurons of patients with amyotrophic lateral sclerosis. Ann Neurol (2011) 69:141-51. doi:10.1002/ana.22149
55. Liu AY, and Abraham BA. Subtractive cloning of a hybrid human endogenous retrovirus and calbindin gene in the prostate cell line PC3. Cancer Res (1991) 51:4107-10.
56. Feuchter-Murthy AE, Freeman JD, and Mager DL. Splicing of a human endogenous retrovirus to a novel phospholipase A2 related gene. Nucleic Acids Res (1993) 21:135-43. doi:10.1093/nar/21.1.135
57. Landry JR, Rouhi A, Medstrand P, and Mager DL. The Opitz syndrome gene Mid1 is transcribed from a human endogenous retroviral promoter. Mol Biol Evol (2002) 19:1934-42. doi:10.1093/oxfordjournals.molbev.a004017
58. Kowalski PE, and Mager DL. A human endogenous retrovirus suppresses translation of an associated fusion transcript, PLA2L. J Virol (1998) 72:6164-8.
59. Gosenca D, Gabriel U, Steidler A, Mayer J, Diem O, Erben P, et al. HERV-E-mediated modulation of PLA2G4A transcription in urothelial carcinoma. PLoS ONE (2012) 7:e49341. doi:10.1371/journal.pone.0049341
60. Denne M, Sauter M, Armbruester V, Licht JD, Roemer K, and Mueller-Lantzsch N. Physical and functional interactions of human endogenous retrovirus proteins Np9 and rec with the promyelocytic leukemia zinc finger protein. J Virol (2007) 81:5607-16. doi:10.1128/JVI.02771-06
61. Matsuda T, Sasaki M, Kato H, Yamada H, Cohen M, Barrett JC, et al. Human chromosome 7 carries a putative tumor suppressor gene(s) involved in choriocarcinoma. Oncogene (1997) 15:2773-81. doi:10.1038/sj.onc.1201461
62. Cohen M, Kato N, and Larsson E. ERV3 human endogenous provirus mRNAs are expressed in normal and malignant tissues and cells, but not in choriocarcinoma tumor cells. J Cell Biochem (1988) 36:121-8. doi:10.1002/jcb.240360203
63. Lin L, Xu B, and Rote NS. The cellular mechanism by which the human endogenous retrovirus ERV-3 env gene affects proliferation and differentiation in a human placental trophoblast model, BeWo. Placenta (2000) 21:73-8. doi:10.1053/plac.1999.0443
64. Larsson E, Venables P, Andersson AC, Fan W, Rigby S, Botling J, et al. Tissue and differentiation specific expression on the endogenous retrovirus ERV3 (HERV-R) in normal human tissues and during induced monocytic differentiation in the U-937 cell line. Leukemia (1997) 11(Suppl 3):142-4.
65. Andersson AC, Yun Z, Sperber GO, Larsson E, and Blomberg J. ERV3 and related sequences in humans: structure and RNA expression. J Virol (2005) 79:9270-84. doi:10.1128/JVI.79.14.9270-9284.2005
66. Hervé CA, Forrest G, Löwer R, Griffiths DJ, and Venables PJ. Conservation and loss of the ERV3 open reading frame in primates. Genomics (2004) 83:940-3. doi:10.1016/j.ygeno.2003.10.003
67. de Parseval N, and Heidmann T. Physiological knockout of the envelope gene of the single-copy ERV-3 human endogenous retrovirus in a fraction of the Caucasian population. J Virol (1998) 72:3442-5.
68. Kato N, Shimotohno K, VanLeeuwen D, and Cohen M. Human proviral mRNAs down regulated in choriocarcinoma encode a zinc finger protein related to Krüppel. Mol Cell Biol (1990) 10:4401-5.
69. Rasmussen HB, Geny C, Deforges L, Perron H, Tourtelotte W, Heltberg A, et al. Expression of endogenous retroviruses in blood mononuclear cells and brain tissue from multiple sclerosis patients. Mult Scler (1995) 1:82-7.
70. Bae S, Jeong HJ, Cha HJ, Kim K, Choi YM, An IS, et al. The hypoxia-mimetic agent cobalt chloride induces cell cycle arrest and alters gene expression in U266 multiple myeloma cells. Int J Mol Med (2012) 30:1180-6. doi:10.3892/ijmm.2012.1115
71. Guo M, Song LP, Jiang Y, Liu W, Yu Y, and Chen GQ. Hypoxia-mimetic agents desferrioxamine and cobalt chloride induce leukemic cell apoptosis through different hypoxia-inducible factor-1alpha independent mechanisms. Apoptosis (2006) 11:67-77. doi:10.1007/s10495-005-3085-3
72. Zeno S, Zaaroor M, Leschiner S, Veenman L, and Gavish M. CoCl(2) induces apoptosis via the 18 kDa translocator protein in U118MG human glioblastoma cells. Biochemistry (2009) 48:4652-61. doi:10.1021/bi900064t
73. Kim HJ, Yang SJ, Kim YS, and Kim TU. Cobalt chloride-induced apoptosis and extracellular signal-regulated protein kinase activation in human cervical cancer HeLa cells. J Biochem Mol Biol (2003) 36:468-74. doi:10.5483/BMBRep.2003.36.5.468
74. Buglio D, Georgakis GV, Hanabuchi S, Arima K, Khaskhely NM, Liu YJ, et al. Vorinostat inhibits STAT6-mediated TH2 cytokine and TARC production and induces cell death in Hodgkin lymphoma cell lines. Blood (2008) 112:1424-33. doi:10.1182/blood-2008-01-133769
75. Hartlapp I, Pallasch C, Weibert G, Kemkers A, Hummel M, and Re D. Depsipeptide induces cell death in Hodgkin lymphoma-derived cell lines. Leuk Res (2009) 33:929-36. doi:10.1016/j.leukres.2008.12.013
76. Lemoine M, Derenzini E, Buglio D, Medeiros LJ, Davis RE, Zhang J, et al. The pan-deacetylase inhibitor panobinostat induces cell death and synergizes with everolimus in Hodgkin lymphoma cell lines. Blood (2012) 119:4017-25. doi:10.1182/blood-2011-01-331421