Skip to main content
SpringerLink
Log in

Characterization of the human CD5 endogenous retrovirus-E in B lymphocytes

  • Full Paper
  • Published:
Genes & Immunity Submit manuscript

Abstract

All T lymphocytes and some B lymphocytes express CD5. This coreceptor is encoded by one gene that consists of 11 exons. We have previously described a B cell-specific alternative exon 1, leading to the synthesis of a protein, devoid of leader peptide, and, therefore, retained in the cytoplasm. The novel exon 1 originates from a human endogenous retrovirus (HERV) at a time interval between the divergence of New World monkeys from Old World monkeys, and prior to the divergence of humans from Old World monkeys. Based on sequence similarity to γ-retroviruses, it was categorized as class I: based on the specificity of its primer binding site, it was allotted to the subclass E, and based on its location within the cd5 gene, named HERV-E.CD5. Alternative transcripts were detected in lymphoid organs including fetal liver (not adult liver), more particularly in CD5-negative cell surface B-1b than in CD5-positive cell surface B-1a, and not at all in B-2 cells. By alignment of 5′ long terminal repeats, HERV-E.CD5 was distinguished from similar proviruses. This could be central to the regulation of membrane expression of CD5 in human B lymphocytes, and, thereby, to the strength of the B-cell antigen receptor signaling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

Accession codes

Accessions

GenBank/EMBL/DDBJ

References

  1. Padilla O, Calvo J, Vila JM et al. Genomic organization of the human CD5 gene. Immunogenetics 2000; 51: 993–1001.

    Article  CAS  PubMed  Google Scholar 

  2. Calvo J, Sole J, Simarro M, Vives J, Lozano F . Evolutionarily conserved transcription regulatory elements within the 5′-flanking region of the human CD5 gene. Tissue Antigens 1996; 47: 257–261.

    Article  CAS  PubMed  Google Scholar 

  3. Youinou P, Jamin C, Lydyard PM . CD5 expression in human B-cell populations. Immunol Today 1999; 20: 312–313.

    Article  CAS  PubMed  Google Scholar 

  4. Kasaian MT, Ikematsu H, Casali P . Identification and analysis of a novel human surface CD5-B lymphocyte subset producing natural antibodies. J Immunol 1992; 148: 2690–2702.

    CAS  PubMed  Google Scholar 

  5. Renaudineau Y, Hillion S, Saraux A, Mageed RA, Youinou P . An alternative exon 1 of the CD5 gene regulate CD5 expression in human B lymphocytes. Blood 2005, DOI 10.1182/blood-2005-02-0597.

  6. Bannert N, Kurth R . Retroelements and the human genome: new perspectives on an old relation. Proc Natl Acad Sci USA 2004; 101 (Suppl 2): 14572–14579.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Li WH, Tanimura M . The molecular clock runs more slowly in man than in apes and monkeys. Nature 1987; 326: 93–96.

    Article  CAS  PubMed  Google Scholar 

  8. Bauer VW, Squire TL, Lowe ME, Andrews MT . Expression of a chimeric retroviral-lipase mRNA confers enhanced lipolysis in hibernating mammal. Am J Physiol Integrative Comp Physiol 2001; 281: R1192–R2001.

    Article  Google Scholar 

  9. Landry JR, Rouhi A, Medstrand P, Mager DL . The Opitz syndrome gene Mid1 is transcribed from a human endogenous retroviral promoter. Mol Biol Evol 2002; 19: 1934–1942.

    Article  CAS  PubMed  Google Scholar 

  10. Schulte AM, Lai S, Kurtz A, Czubayko F, Riegel AT, Wellstein A . Human trophoblast and choriocarcinoma expression of the growth factor pleiotrophin attributable to germ-line insertion of an endogenous retrovirus. Proc Natl Acad Sci USA 1996; 93: 14759–14764.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Repaske R, Steele PE, O'Neill RR, Rabson AB, Martin MA . Nucleotide sequence of a full-length retroviral segment. J Virol 1985; 54: 764–772.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Medstrand P, Mager DL . Human specific integrations of the HERV-K. J Virol 1998; 72: 9782–9787.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Medstrand P, Landry JR, Mager DL . Long terminal repeats are used as alternative promoters for the endothelin B receptor and apolipoprotein C-I genes in humans. J Biol Chem 2001; 276: 1896–1903.

    Article  CAS  PubMed  Google Scholar 

  14. Hardy RR, Hayakawa K . CD5 B cells, a fetal B cell lineage. Adv Immunol 1994; 55: 297–339.

    Article  CAS  PubMed  Google Scholar 

  15. Page SL, Goodman M . Catarrhine phylogeny: noncoding DNA evidence for a diphyletic origin of the mangabeys and for a human-chimpanzee clade. Mol Phylogenet Evol 2001; 18: 14–25.

    Article  CAS  PubMed  Google Scholar 

  16. Bergsagel PL, Timblin CR, Eckhardt L, Laskov R, Kuehl WM . Sequence and expression of a murine cDNA encoding PC326, a novel gene expressed in plasmacytomas but not normal plasma cells. Oncogene 1992; 7: 2059–2064.

    CAS  PubMed  Google Scholar 

  17. Benoist C, Mathis D . Autoimmune diabetes. Retrovirus as trigger, precipitator or marker? Nature 1997; 338: 833–834.

    Article  Google Scholar 

  18. Perron H, Jouvin-Marche E, Michel M et al. Multiple sclerosis retrovirus particles and recombinant envelope trigger an abnormal immune response in vitro, by inducing polyclonal Vβ16 T-lymphocyte activation. Virology 2001; 287: 321–322.

    Article  CAS  PubMed  Google Scholar 

  19. Sen G, Bikah G, Venkataraman C, Bondada S . Negative regulation of antigen receptor-mediated signalling by constitutive association of CD5 with the SHP-1 protein tyrosine phosphatase in B-1 cells. Eur J Immunol 1999; 29: 3319–3328.

    Article  CAS  PubMed  Google Scholar 

  20. Lorincz MC, Schubeler D, Groudine M . Methylation-mediated proviral silencing is associated with MeCP2 recruitment and localized histone H3 deacetylation. Mol Cell Biol 2001; 21: 7313–7322.

    Article  Google Scholar 

  21. Nakao M . Epigenics: interaction of DNA methylation and chromatin. Gene 2001; 31: 25–31.

    Article  Google Scholar 

  22. Ogasawara H, Okada M, Kaneko H, Hishikawa T, Sekigawa I, Hashimoto H . Possible role of DNA hypomethylation in the induction of SLE: relationship to the transcription of human endogenous retroviruses. Clin Exp Rheumatol 2003; 21: 733–738.

    CAS  PubMed  Google Scholar 

  23. Gotzinger N, Sauter M, Roemer K, Mueller-Lantzsch N . Regulation of human endogenous retrovirus-K gag expression in teratocarcinoma cell lines and human tumours. J Gen Virol 1996; 77: 2983–2990.

    Article  PubMed  Google Scholar 

  24. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ . Basic local alignment search tool. J Mol Biol 1990; 215: 403–410.

    Article  CAS  PubMed  Google Scholar 

  25. Nicholas KB, Nicholas Jr HB, Deerfield II DW . GeneDoc: analysis and visualization of genetic variation. EMBNEW News 1997; 4: 1–4.

    Google Scholar 

  26. Saitou N, Nei M . The neighbor-joining methods: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4: 406–425.

    CAS  PubMed  Google Scholar 

  27. Felsenstein J . PHYLIP: phylogeny inference package (Version 3.2). Cladistics 1989; 5: 164–166.

    Google Scholar 

  28. Kimura M . A simple method for estimating evolutionary rates of base substitutions through imperative studies of nucleotide sequences. J Mol Evol 1980; 16: 111–120.

    Article  CAS  PubMed  Google Scholar 

  29. Schulte AM, Wellstein A . Structure and phylogenetic analysis of an endogenous retrovirus inserted into the human growth factor gene pleiotrophin. J Virol 1998; 12: 6065–6072.

    Google Scholar 

Download references

Acknowledgements

We thank S Forest and C Séné for secretarial assistance.

Author information

Authors and Affiliations

  1. Laboratory of Immunology, Brest University Medical School, Brest, France

    Y Renaudineau, C Le Dantec, S Hillion, A Saraux & P Youinou

  2. Laboratory of Virology, Brest University Medical School, Brest, France

    S Vallet

Authors
  1. Y Renaudineau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S Vallet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C Le Dantec
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S Hillion
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A Saraux
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P Youinou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P Youinou.

Additional information

Financial interests: none

Rights and permissions

Reprints and permissions

About this article

Cite this article

Renaudineau, Y., Vallet, S., Le Dantec, C. et al. Characterization of the human CD5 endogenous retrovirus-E in B lymphocytes. Genes Immun 6, 663–671 (2005). https://doi.org/10.1038/sj.gene.6364253

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.gene.6364253

  • Springer Nature Limited

Keywords

This article is cited by

Search

Navigation