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.

  • Short Report
  • Published:

Angiogenesis is an early event in the generation of myc-induced lymphomas

Oncogene volume 19, pages 2780–2785 (2000)Cite this article

Abstract

Angiogenesis was identified as an early consequence of myc gene overexpression in two models of retroviral lymphomagenesis. Avian leukosis virus (ALV) induces bursal lymphoma in chickens after proviral c-myc gene integration, while the HB-1 retrovirus carries a v-myc oncogene and also induces metastatic lymphoma. Immunohistochemical studies of the effects of increased c-myc or v-myc overexpression revealed early angiogenesis within myc-transformed bursal follicles, which persisted in lymphomas and metastases. Abnormal vessel growth was consistently detected within 13 days after transplantation of a few myc-overexpressing progenitors into ablated bursal follicles, suggesting that these angiogenic changes may support the initial expansion of tumor precursors, as well as later stage lymphomagenesis. Conditioned media from myc-overexpressing B cell lines promoted proliferation of vascular endothelium in vitro, while media from B cells expressing low myc levels showed little effect. Moreover, ectopic myc overexpression in the low myc B cell lines increased production of the endothelial growth activity, indicating that myc induces secretion of angiogenic factors from B cells. These findings demonstrate that myc overexpression in lymphocytes generates an angiogenic phenotype in vitro as well as in vivo.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • Bister K, Jansen HW, Graf T, Enrietto P and Hayman MJ . 1983 J Virol 46: 337–346

  • Bouck N, Stellmach V and Hsu SC . 1996 Adv Cancer Res 69: 135–174

  • Bowers WJ, Baglia LA and Ruddell A . 1996 J Virol 70: 3051–3059

  • Cooper MD, Payne LN, Dent PB, Burmester BR and Good RA . 1968 J Natl Cancer Inst 41: 373–378

  • Ewert DL, Avdalovic N and Goldstein C . 1989 Virology 170: 433–441

  • Ewert DL and deBoer GF . 1988 Adv Vet Sci Comp Med 32: 37–55

  • Gong M, Semus HL, Bird KJ, Stramer BJ and Ruddell A . 1998 J Virol 72: 5517–5525

  • Grandori C and Eisenman RN . 1997 Trends Biochem Sci 22: 177–181

  • Hanahan D and Folkman J . 1996 Cell 86: 353–364

  • Hann SR, Abrams HD, Rohrschneider LR and Eisenman RN . 1983 Cell 34: 789–798

  • Henriksson M and Luscher B . 1996 Adv Cancer Res 68: 110–182

  • Holash J, Wiegand SJ and Yancopoulos GD . 1999 Oncogene 18: 5736–5762

  • Iritani BM and Eisenman RN . 1999 Proc Natl Acad Sci USA 96: 13180–13185

  • Kerbel RS, Viloria-Petit A, Okada F and Rak J . 1998 Mol Med 4: 286–295

  • Kraemer M, Tournaire R, Dejong V, Montreau N, Briane D, Derbin C and Binetruy B . 1999 Cell Growth Differ 10: 193–200

  • Lewis RB, McClure J, Rup B, Niesel DW, Garry RF, Hoelzer JD, Nazerian K and Bose HR . 1981 Cell 25: 421–431

  • Neiman P, Wolf C, Enrietto PJ and Cooper GM . 1985 Proc Natl Acad Sci USA 82: 222–225

  • Neiman PE . 1994 Adv Immun 56: 467–484

  • Neiman PE, Thomas SJ and Loring G . 1991 Proc Natl Acad Sci USA 88: 5857–5861

  • Nesbit CE, Tersak JM and Prochownik EV . 1999 Oncogene 18: 3004–3016

  • Pelengaris S, Littlewood T, Khan M, Elia G and Evan G . 1999 Molec Cell 3: 565–577

  • Perez-Atayde AR, Sallan SE, Tedrow U, Connors S, Allred E and Folkman J . 1997 Am J Pathol 150: 815–821

  • Ribatti D, Nico B, Vacca A, Marzullo A, Calvi N, Roncali L and Dammacco F . 1998 Br J Cancer 77: 1900–1906

  • Tikhonenko AT, Black DJ and Linial ML . 1996 J Biol Chem 271: 30741–30747

  • Vacca A, Ribatti D, Iurlaro M, Albini A, Minischetti M, Bussolino F, Pellegrino A, Ria R, Rusnati M, Presta M, Vincenti V, Persico MG and Dammacco F . 1998 Inter J Clin Lab Res 28: 55–68

  • Vacca A, Ribatti D, Ruco L, Giacchetta F, Nico B, Quondamatteo F, Ria R, Iurlaro M and Dammacco F . 1999 Br J Cancer 79: 965–970

Download references

Acknowledgements

We thank Drs Helene Sage, Patricia Parsons-Wingerter and Mark Groudine for their helpful suggestions, Andrei Tikhonenko for generously providing advice and tsp-1 analysis, and Kelly Bird, Sandra Jo Thomas and Gilbert Loring for technical assistance. This work was supported by NCI RO1 grant CA68328 to A Ruddell and NCI R01 grant CA20068 to P Neiman.

Author information

Authors and Affiliations

  1. Fred Hutchinson Cancer Research Center, Seattle, 98109-1024, Washington, WA, USA

    Kimberly A Brandvold, Paul Neiman & Alanna Ruddell

  2. Departments of Medicine and Pathology, University of Washington, Seattle, 98109-1024, Washington, USA

    Paul Neiman

Authors
  1. Kimberly A Brandvold
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul Neiman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alanna Ruddell
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brandvold, K., Neiman, P. & Ruddell, A. Angiogenesis is an early event in the generation of myc-induced lymphomas. Oncogene 19, 2780–2785 (2000). https://doi.org/10.1038/sj.onc.1203589

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1203589

Keywords

This article is cited by

Search

Advanced search

Quick links