Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Paper
  • Published:

Global transcription analysis of immature avian erythrocytic progenitors: from self-renewal to differentiation

Abstract

The molecular mechanisms regulating the cell fate decision between self-renewal and differentiation/apoptosis in stem and progenitor cells are poorly understood. Here, we report the first comprehensive identification of genes potentially involved in the switch from self-renewal toward differentiation of primary, non-immortalized erythroid avian progenitor cells (T2EC cells). We used the Serial Analysis of Gene Expression (SAGE) technique in order to identify and quantify the genome fraction functionally active in a self-renewing versus a differentiating cell population. We generated two SAGE libraries and sequenced a total of 37 589 tags, thereby obtaining the first transcriptional profile characterization of a chicken cell. Tag identification was performed using a new relational database (Identitag) developed in the laboratory, which allowed a highly satisfactory level of identification. Among 123 differentially expressed genes, 11 were investigated further and for nine of them the differential expression was subsequently confirmed by real-time PCR. The comparison of tag abundance between the two libraries revealed that only a small fraction of transcripts was differentially expressed. The analysis of their functions argue against a prominent role for a master switch in T2EC cells decision-making, but are in favor of a critical role for coordinated small variations in a relatively small number of genes that can lead to essential cellular identity changes.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

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

Similar content being viewed by others

References

  • Abe I and Prestwich GD . (1995). Proc. Natl. Acad. Sci. USA, 92, 9274–9278.

  • Al-Hajj M, Becker MW, Wicha M, Weissman I and Clarke MF . (2004). Curr. Opin. Genet. Dev., 14, 43–47.

  • Antica M, Wu L and Scollay R . (1997). Immunol. Lett., 55, 47–51.

  • Bauer A, Gandrillon O, Samarut J and Beug H . (2001) In Zon, L. (ed.), Hematopoiesis: a developmental approach. Oxford University Press, New York, pp. 368–390.

    Google Scholar 

  • Bauer A, Tronche F, Wessely O, Kellendonk C, Reichardt HM, Steinlein P, Schutz G and Beug H . (1999). Genes Dev., 13, 2996–3002.

  • Becquet C, Blachon S, Jeudy B, Boulicaut JF and Gandrillon O . (2002). Genome Biol., 3, RESEARCH0067.

  • Boheler KR and Stern MD . (2003). Trends Biotechnol., 21, 55–57.

  • Cao A and Moi P . (2002). Pediatr. Res, 51, 415–421.

  • Chen J, Sun M, Lee S, Zhou G, Rowley JD and Wang SM . (2002). Proc. Natl. Acad. Sci. U S A, 99, 12257–12262.

  • Dazy S, Damiola F, Parisey N, Beug H and Gandrillon O . (2003). Oncogene, 22 (58), 9205–9216.

  • Detmer K, Walker AN, Jenkins TM, Steele TA and Dannawi H . (2000). Blood Cells Mol. Dis., 26, 360–372.

  • Dolznig H, Boulme F, Stangl K, Deiner EM, Mikulits W, Beug H and Mullner EW . (2001). Faseb J., 15, 1442–1444.

  • Fortunel NO, Otu HH, Ng HH, Chen J, Mu X, Chevassut T, Li X, Joseph M, Bailey C, Hatzfeld JA, Hatzfeld A, Usta F, Vega VB, Long PM, Libermann TA and Lim B . (2003). Science, 302, 393 author reply 393.

  • Freed E, Symons M, Macdonald SG, McCormick F and Ruggieri R . (1994). Science, 265, 1713–1716.

  • Gandrillon O and Samarut J . (1998). Interference with the v-erbA and p135gap-myb-ets nuclear oncogenes. Oncogene, 16, 563–574.

    Article  CAS  Google Scholar 

  • Gandrillon O, Schmidt U, Beug H and Samarut J . (1999). EMBO J., 18, 2764–2781.

  • Heller S, Sheane CA, Javed Z and Hudspeth AJ . (1998). Proc. Natl. Acad. Sci. USA, 95, 11400–11405.

  • Hinssen H, Vandekerckhove J and Lazarides E . (1987). J. Cell Biol., 105, 1425–1433.

  • Ito CY, Li CY, Bernstein A, Dick JE and Stanford WL . (2003). Blood, 101, 517–523.

  • Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA and Lemischka IR . (2002). Science, 298, 601–604.

  • Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA and Lemischka IR . (2003). Science, 302, 393.

  • Kal AJ, van Zonneveld AJ, Benes V, van den Berg M, Koerkamp MG, Albermann K, Strack N, Ruijter JM, Richter A, Dujon B, Ansorge W and Tabak HF . (1999). Mol. Biol. Cell, 10, 1859–1872.

  • Keime C, Damiola F, Mouchiroud D, Duret L and Gandrillon O . (2004). submitted.

  • Keith WN . (2004). Oncogene, 23, 5092–5094.

  • Kolbus A, Blazques-Domingo M, Carotta S, Bakker W, Luedemann S, Von Lindern M, Steinlein P and Beug H . (2003). Blood, 102 (9), 3136–3146.

  • Man MZ, Wang X and Wang Y . (2000). Bioinformatics, 16, 953–959.

  • Margulies EH and Innis JW . (2000). Bioinformatics, 16, 650–651.

  • Marone M, Scambia G, Bonanno G, Rutella S, de Ritis D, Guidi F, Leone G and Pierelli L . (2002). Leukemia, 16, 94–105.

  • Matsumura F, Totsukawa G, Yamakita Y and Yamashiro S . (2001). Cell Struct. Funct., 26, 639–644.

  • Muller J, Ory S, Copeland T, Piwnica-Worms H and Morrison DK . (2001). Mol. Cell, 8, 983–993.

  • Pfaffl MW . (2001). Nucleic Acids Res., 29, e45.

  • Piquemal D, Commes T, Manchon L, Lejeune M, Ferraz C, Pugnere D, Demaille J, Elalouf J and Marti J . (2002). Genomics, 80, 361–371.

  • Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC and Melton DA . (2002). Science, 298, 597–600.

  • Reya T, Morrison SJ, Clarke MF and Weissman IL . (2001). Nature, 414, 105–111.

  • Roessler E, Mittaz L, Du Y, Scott HS, Chang J, Rossier C, Guipponi M, Matsuda SP, Muenke M and Antonarakis SE . (1999). Hum. Genet., 105, 489–495.

  • Terskikh AV, Miyamoto T, Chang C, Diatchenko L and Weissman IL . (2003). Blood, 102, 94–101.

  • Velculescu VE, Madden SL, Zhang L, Lash AE, Yu J, Rago C, Lal A, Wang CJ, Beaudry GA, Ciriello KM, Cook BP, Dufault MR, Ferguson AT, Gao Y, He TC, Hermeking H, Hiraldo SK, Hwang PM, Lopez MA, Luderer HF, Mathews B, Petroziello JM, Polyak K, Zawel L and Kinzler KW . (1999). Nat. Genet., 23, 378–387.

  • Velculescu VE, Zhang L, Vogelstein B and Kinzler KW . (1995). Science, 270, 484–487.

  • Vinogradov AE . (1998). Cytometry, 31, 100–109.

  • Watt FM and Hogan BL . (2000). Science, 287, 1427–1430.

  • Weissman IL . (2000). Cell, 100, 157–168.

  • Wessely O, Bauer A, Quang CT, Deiner EM, von Lindern M, Mellitzer G, Steinlein P, Ghysdael J and Beug H . (1999). Biol. Chem., 380, 187–202.

  • Yaffe MB . (2002). FEBS. Lett., 513, 53–57.

  • Zhou G, Chen J, Lee S, Clark T, Rowley JD and Wang SM . (2001). Proc. Natl. Acad. Sci. USA, 98, 13966–13971.

Download references

Acknowledgements

We thank the SIGENAE group (especially Patrice Deshais, Christophe Klopp and Madeleine Douaire) for sharing chicken EST clusters sequences. This work was supported by the CNRS, UCBL, INRA (‘AGENA’ Program), Région Rhône-Alpes (‘Génomique fonctionnelle des récepteurs d’hormone’ Program), Fondation de France, Association pour la Recherche contre le Cancer and a joint INSERM/AFM program (‘Cellules souches’ Program). Sequencing was partially funded through an InterEPST program (‘Séquençage à grande échelle’, call 2002). FD is a fellow of the EU RTN ‘Hematopoiesis’ program (contract HPRN-CT-2000-00083). SGG is a fellow of the Région Rhône-Alpes. SD is a fellow of the Ligue contre le Cancer and the Association pour la Recherche contre le Cancer.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francesca Damiola.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Damiola, F., Keime, C., Gonin-Giraud, S. et al. Global transcription analysis of immature avian erythrocytic progenitors: from self-renewal to differentiation. Oncogene 23, 7628–7643 (2004). https://doi.org/10.1038/sj.onc.1208061

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1208061

Keywords

This article is cited by

Search

Quick links