1887

Journal of General Virology header logo

Volume 92, Issue 10

Human endogenous retrovirus transcription profiles of the kidney and kidney-derived cell lines Free

Abstract

The human genome comprises approximately 8–9 % of human endogenous retroviruses (HERVs) that are transcribed with tissue specificity. However, relatively few organs have been examined in detail for individual differences in HERV transcription pattern, nor have tissue-to-cell culture comparisons been frequently performed. Using an HERV-specific DNA microarray, a core HERV transcription profile was established for the human kidney comparing 10 tissue samples. This core represents HERV groups expressed uniformly or nearly so in non-tumour kidney tissue. The profiles obtained from non-tumour tissues were compared to 10 renal tumour tissues (renal cell carcinoma, RCC) derived from the same individuals and additionally, to 22 RCC cell lines. No RCC cell line or tumour-specific differences were observed, suggesting that HERV transcription is not altered in RCC. However, when comparing tissue transcription to cell line transcription, there were consistent differences. The differences were irrespective of cancer state and included cell lines derived from non-tumour kidney tissue, suggesting that a specific alteration of HERV transcription occurs when establishing cell lines. In contrast to previous publications, all known HERV-derived tumour antigens, including those identified in RCC, were expressed both in multiple RCC cell lines and several non-tumour tissue-derived cell lines, a result that contrasts with findings from patient samples. The results establish the core kidney transcription pattern of HERVs and reveal differences between cell culture lines and tissue samples.

  • Received:
  • Accepted:
  • Published Online:
© 2011 SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.031518-0
2011-10-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/10/2356.html?itemId=/content/journal/jgv/10.1099/vir.0.031518-0&mimeType=html&fmt=ahah

References

  1. Alves P. M. S., Lévy N., Stevenson B. J., Bouzourene H., Theiler G., Bricard G., Viatte S., Ayyoub M., Vuilleumier H. et al.& other authors ( 2008; Identification of tumor-associated antigens by large-scale analysis of genes expressed in human colorectal cancer. Cancer Immun 8:11[PubMed]
     [Google Scholar]
  2. Balada E., Ordi-Ros J., Vilardell-Tarrés M. 2009; Molecular mechanisms mediated by human endogenous retroviruses (HERVs) in autoimmunity. Rev Med Virol 19:273–286 [View Article][PubMed]
     [Google Scholar]
  3. Chen Y., Demir Y., Valujskikh A., Heeger P. S. 2004; Antigen location contributes to the pathological features of a transplanted heart graft. Am J Pathol 164:1407–1415 [View Article][PubMed]
     [Google Scholar]
  4. Flockerzi A., Ruggieri A., Frank O., Santer M., Maldener E., Kopper B., Wullich B., Seifarth W., Müller-Lantzsch N.& other authors ( 2008; Expression patterns of transcribed human endogenous retrovirus HERV-K (HML-2) loci in human tissues and the need for a HERV transcriptome project. BMC Genomics 9:354 [View Article][PubMed]
     [Google Scholar]
  5. Frank O., Giehl M., Zheng C., Hehlmann R., Leib-Mösch C., Seifarth W. 2005; Human endogenous retrovirus expression profiles in samples from brains of patients with schizophrenia and bipolar disorders. J Virol 79:10890–10901 [View Article][PubMed]
     [Google Scholar]
  6. Frank O., Verbeke C., Schwarz N., Mayer J., Fabarius A., Hehlmann R., Leib-Mösch C., Seifarth W. 2008; Variable transcriptional activity of endogenous retroviruses in human breast cancer. J Virol 82:1808–1818 [View Article][PubMed]
     [Google Scholar]
  7. Fuhrman S. A., Lasky L. C., Limas C. 1982; Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol 6:655–663 [View Article][PubMed]
     [Google Scholar]
  8. Greenwood A. D., Stengel A., Erfle V., Seifarth W., Leib-Mösch C. 2005; The distribution of pol containing human endogenous retroviruses in non-human primates. Virology 334:203–213 [View Article][PubMed]
     [Google Scholar]
  9. Griffiths D. J. 2001; Endogenous retroviruses in the human genome sequence. Genome Biol 2:REVIEWS1017 [View Article][PubMed]
     [Google Scholar]
  10. Herbst H., Sauter M., Kühler-Obbarius C., Löning T., Mueller-Lantzsch N. 1998; Human endogenous retrovirus (HERV)-K transcripts in germ cell and trophoblastic tumours. APMIS 106:216–220 [View Article][PubMed]
     [Google Scholar]
  11. Iliopoulos O., Kibel A., Gray S., Kaelin W. G. Jr 1995; Tumour suppression by the human von Hippel-Lindau gene product. Nat Med 1:822–826 [View Article][PubMed]
     [Google Scholar]
  12. Ishida T., Obata Y., Ohara N., Matsushita H., Sato S., Uenaka A., Saika T., Miyamura T., Chayama K. et al.& other authors ( 2008; Identification of the HERV-K gag antigen in prostate cancer by SEREX using autologous patient serum and its immunogenicity. Cancer Immun 8:15[PubMed]
     [Google Scholar]
  13. Jern P., Sperber G. O., Blomberg J. 2005; Use of endogenous retroviral sequences (ERVs) and structural markers for retroviral phylogenetic inference and taxonomy. Retrovirology 2:50 [View Article][PubMed]
     [Google Scholar]
  14. Kawakami T., Chano T., Minami K., Okabe H., Okada Y., Okamoto K. 2006; Imprinted DLK1 is a putative tumor suppressor gene and inactivated by epimutation at the region upstream of GTL2 in human renal cell carcinoma. Hum Mol Genet 15:821–830 [View Article][PubMed]
     [Google Scholar]
  15. Komohara Y., Suekane S., Noguchi M., Matsuoka K., Yamada A., Itoh K. 2007; Expression of APOBEC3G in kidney cells. Tissue Antigens 69:95–98 [View Article][PubMed]
     [Google Scholar]
  16. Leisegang M., Turqueti-Neves A., Engels B., Blankenstein T., Schendel D. J., Uckert W., Noessner E. 2010; T-cell receptor gene-modified T cells with shared renal cell carcinoma specificity for adoptive T-cell therapy. Clin Cancer Res 16:2333–2343 [View Article][PubMed]
     [Google Scholar]
  17. Löwer R., Boller K., Hasenmaier B., Korbmacher C., Müller-Lantzsch N., Löwer J., Kurth R. 1993; Identification of human endogenous retroviruses with complex mRNA expression and particle formation. Proc Natl Acad Sci U S A 90:4480–4484 [View Article][PubMed]
     [Google Scholar]
  18. Medstrand P., van de Lagemaat L. N., Mager D. L. 2002; Retroelement distributions in the human genome: variations associated with age and proximity to genes. Genome Res 12:1483–1495 [View Article][PubMed]
     [Google Scholar]
  19. Nakano O., Sato M, Naito Y., Suzuki K., Orikasa S., Aizawa M., Suzuki Y., Shintaku I., Nagura H., Ohtani H. 2001; Proliferative activity of intratumoral CD8+ T-lymphocytes as a prognostic factor in human renal cell carcinoma: clinicopathologic demonstration of antitumor immunity. Cancer Res 61:5132–5136 [View Article][PubMed]
     [Google Scholar]
  20. Nelson P. N., Carnegie P. R., Martin J., Davari Ejtehadi H., Hooley P., Roden D., Rowland-Jones S., Warren P., Astley J., Murray P. G. 2003; Demystified. Human endogenous retroviruses. Mol Pathol 56:11–18 [View Article][PubMed]
     [Google Scholar]
  21. Rakoff-Nahoum S., Kuebler P. J., Heymann J. J., Sheehy M. E., Ortiz G. M., Ogg G. S., Barbour J. D., Lenz J., Steinfeld A. D., Nixon D. F. 2006; Detection of T lymphocytes specific for human endogenous retrovirus K (HERV-K) in patients with seminoma. AIDS Res Hum Retroviruses 22:52–56 [View Article][PubMed]
     [Google Scholar]
  22. Romanish M. T., Cohen C. J., Mager D. L. 2010; Potential mechanisms of endogenous retroviral-mediated genomic instability in human cancer. Semin Cancer Biol 20:246–253 [View Article][PubMed]
     [Google Scholar]
  23. Ruprecht K., Ferreira H., Flockerzi A., Wahl S., Sauter M., Mayer J., Mueller-Lantzsch N. 2008a; Human endogenous retrovirus family HERV-K(HML-2) RNA transcripts are selectively packaged into retroviral particles produced by the human germ cell tumor line Tera-1 and originate mainly from a provirus on chromosome 22q11.21. J Virol 82:10008–10016 [View Article][PubMed]
     [Google Scholar]
  24. Ruprecht K., Mayer J., Sauter M., Roemer K., Mueller-Lantzsch N. 2008b; Endogenous retroviruses and cancer. Cell Mol Life Sci 65:3366–3382 [View Article][PubMed]
     [Google Scholar]
  25. Sauter M., Schommer S., Kremmer E., Remberger K., Dölken G., Lemm I., Buck M., Best B., Neumann-Haefelin D., Mueller-Lantzsch N. 1995; Human endogenous retrovirus K10: expression of Gag protein and detection of antibodies in patients with seminomas. J Virol 69:414–421[PubMed]
     [Google Scholar]
  26. Schiavetti F., Thonnard J., Colau D., Boon T., Coulie P. G. 2002; A human endogenous retroviral sequence encoding an antigen recognized on melanoma by cytolytic T lymphocytes. Cancer Res 62:5510–5516[PubMed]
     [Google Scholar]
  27. Seifarth W., Spiess B., Zeilfelder U., Speth C., Hehlmann R., Leib-Mösch C. 2003; Assessment of retroviral activity using a universal retrovirus chip. J Virol Methods 112:79–91 [View Article][PubMed]
     [Google Scholar]
  28. Seifarth W., Frank O., Zeilfelder U., Spiess B., Greenwood A. D., Hehlmann R., Leib-Mösch C. 2005; Comprehensive analysis of human endogenous retrovirus transcriptional activity in human tissues with a retrovirus-specific microarray. J Virol 79:341–352 [View Article][PubMed]
     [Google Scholar]
  29. Shastri N. 1996; Needles in haystacks: identifying specific peptide antigens for T cells. Curr Opin Immunol 8:271–277 [View Article][PubMed]
     [Google Scholar]
  30. Shih A., Misra R., Rush M. G. 1989; Detection of multiple, novel reverse transcriptase coding sequences in human nucleic acids: relation to primate retroviruses. J Virol 63:64–75[PubMed]
     [Google Scholar]
  31. Takahashi Y., Harashima N., Kajigaya S., Yokoyama H., Cherkasova E., McCoy J. P., Hanada K., Mena O., Kurlander R. et al.& other authors ( 2008; 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 118:1099–1109 [View Article][PubMed]
     [Google Scholar]
  32. Villesen P., Aagaard L., Wiuf C., Pedersen F. S. 2004; Identification of endogenous retroviral reading frames in the human genome. Retrovirology 1:32 [View Article][PubMed]
     [Google Scholar]
  33. Wang-Johanning F., Frost A. R., Jian B., Epp L., Lu D. W., Johanning G. L. 2003; Quantitation of HERV-K env gene expression and splicing in human breast cancer. Oncogene 22:1528–1535 [View Article][PubMed]
     [Google Scholar]
  34. Wang-Johanning F., Radvanyi L., Rycaj K., Plummer J. B., Yan P., Sastry K. J., Piyathilake C. J., Hunt K. K., Johanning G. L. 2008; Human endogenous retrovirus K triggers an antigen-specific immune response in breast cancer patients. Cancer Res 68:5869–5877 [View Article][PubMed]
     [Google Scholar]
  35. Weiss R. A. 2006; The discovery of endogenous retroviruses. Retrovirology 3:67 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.031518-0
Loading
Human endogenous retrovirus transcription profiles of the kidney and kidney-derived cell lines
J. Gen. Virol. 92, 2356 (2011); https://doi.org/10.1099/vir.0.031518-0
/content/journal/jgv/10.1099/vir.0.031518-0
/content/journal/jgv/10.1099/vir.0.031518-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error