Cancer Letters
Volume 298, Issue 2 , Pages 264-272 , 8 December 2010

Tumor microenvironment modifications induced by soluble VEGF receptor expression in a rat liver metastasis model

  • Samuel Bertin

      Affiliations

    • INSERM Unité 638, Université de Nice-Sophia Antipolis, Faculté de Médecine, Avenue de Valombrose, 06107 Nice cédex 2, France
    • These authors are participated equally to this work.
  • ,
  • Tala Mohsen-Kanson

      Affiliations

    • INSERM Unité 638, Université de Nice-Sophia Antipolis, Faculté de Médecine, Avenue de Valombrose, 06107 Nice cédex 2, France
    • These authors are participated equally to this work.
  • ,
  • Patrick Baqué

      Affiliations

    • INSERM Unité 638, Université de Nice-Sophia Antipolis, Faculté de Médecine, Avenue de Valombrose, 06107 Nice cédex 2, France
    • Service de Chirurgie d’Urgence, Hôpital St Roch, Rue Pierre Devoluy, Nice F-06107, France
  • ,
  • Adolfo Gavelli

      Affiliations

    • INSERM Unité 638, Université de Nice-Sophia Antipolis, Faculté de Médecine, Avenue de Valombrose, 06107 Nice cédex 2, France
    • Service de Chirurgie Générale et Digestive, Centre Hospitalier Princesse Grace, Monaco
  • ,
  • David Momier

      Affiliations

    • GéPITOs, Université de Nice-Sophia Antipolis, CNRS, UMR 6235, Faculté de Médecine, Avenue de Valombrose, 06107 Nice cédex 2, France
  • ,
  • Fabienne Anjuere

      Affiliations

    • INSERM Unité 634, Université de Nice-Sophia Antipolis, Faculté de Médecine, Avenue de Valombrose, 06107 Nice cédex 2, France
  • ,
  • Georges F. Carle

      Affiliations

    • GéPITOs, Université de Nice-Sophia Antipolis, CNRS, UMR 6235, Faculté de Médecine, Avenue de Valombrose, 06107 Nice cédex 2, France
  • ,
  • Valérie Pierrefite-Carle

      Affiliations

    • INSERM Unité 638, Université de Nice-Sophia Antipolis, Faculté de Médecine, Avenue de Valombrose, 06107 Nice cédex 2, France
    • GéPITOs, Université de Nice-Sophia Antipolis, CNRS, UMR 6235, Faculté de Médecine, Avenue de Valombrose, 06107 Nice cédex 2, France
    • Corresponding Author InformationCorresponding author at: GéPITOS, UMR 6235, CNRS, UNSA, Faculté de Médecine, Avenue de Valombrose, 06107 Nice cédex 2, France. Tel.: +33 4 93 37 77 06; fax: +33 4 93 53 30 71.

Received 12 January 2010 ,Revised 13 July 2010 ,Accepted 19 July 2010.

References 

  1. Ferrara N, Hillan KJ, Gerber HP, Novotny W. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat. Rev. Drug Discov. 2004;3:391–400
  2. de Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science. 1992;255:989–991
  3. Terman BI, Dougher-Vermazen M, Carrion ME, Dimitrov D, Armellino DC, Gospodarowicz D, et al. Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor. Biochem. Biophys. Res. Commun. 1992;187:1579–1586
  4. Gabrilovich DI, Chen HL, Girgis KR, Cunningham HT, Meny GM, Nadaf S, et al. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nature Med. 1996;2:1096–1103
  5. Gabrilovich D, Ishida T, Oyama T, Ran S, Kravtsov V, Nadaf S, et al. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood. 1998;92:4150–4166
  6. Kusmartsev S, Gabrilovich DI. STAT1 signaling regulates tumor-associated macrophage-mediated T cell deletion. J. Immunol. 2005;174:4880–4891
  7. Melani C, Chiodoni C, Forni G, Colombo MP. Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity. Blood. 2003;102:2138–2145
  8. Kusmartsev S, Nefedova Y, Yoder D, Gabrilovich DI. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J. Immunol. 2004;172:989–999
  9. Sinha P, Clements VK, Ostrand-Rosenberg S. Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J. Immunol. 2005;174:636–645
  10. Ochoa AC, Zea AH, Hernandez C, Rodriguez PC. Arginase, prostaglandins, and myeloid-derived suppressor cells in renal cell carcinoma. Clin. Cancer Res. 2007;13:721s–726s
  11. Almand B, Clark JI, Nikitina E, van Beynen J, English NR, Knight SC, et al. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J. Immunol. 2001;166:678–689
  12. Ohm JE, Carbone DP. VEGF as a mediator of tumor associated immunodeficiency. Immunol. Res. 2001;23:263–272
  13. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nature Rev. Cancer. 2008;8:592–603
  14. Fischer C, Jonckx B, Mazzone M, Zacchigna S, Loges S, Pattarini L, et al. Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell. 2007;131:463–475
  15. Shojaei F, Wu X, Malik AK, Zhong C, Baldwin ME, Schanz S, et al. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nature Biotech. 2007;25:911–920
  16. Fischer C, Mazzone M, Jonckx B, Carmeliet P. FLT1 and its ligands VEGFB and PlGF: drug targets for anti-angiogenic therapy?. Nat. Rev. Cancer. 2008;8:942–956
  17. Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc. Natl. Acad. Sci. USA. 1993;90:10705–10709
  18. Kendall RL, Wang G, Thomas KA. Identification of a natural soluble form of the vascular endothelial growth factor receptor FLT-1, and its heterodimerization with KDR. Biochem. Biophys. Res. Commun. 1996;226:324–328
  19. Park JE, Chen HH, Winer J, Houck KA, Ferrara N. Placenta growth factor. J. Biol. Chem. 1994;269:25646–25654
  20. Yamaguchi T, Bando H, Mori T, Takahashi K, Matsumoto H, Yasutome M, et al. Overexpression of soluble vascular endothelial growth factor receptor 1 in colorectal cancer: association with progression and prognosis. Cancer Sci. 2007;98:405–410
  21. Martin F, Caignard A, Jeannin JF, Leclerc A, Martin M. Selection by trypsin of two sublines of rat colon cancer cells forming progressive or regressive tumors. Int. J. Cancer. 1983;32:623–627
  22. Auerbach R, Morissey LW, Sidky YA. Regional differences in the incidence and growth of mouse tumors following intradermal or subcutaneous inoculation. Cancer Res. 1978;38:1739–1744
  23. Bertin S, Neves S, Gavelli A, Baqué P, Brossette N, Simões S, et al. Cellular and molecular events associated with the antitumor response induced by the cytosine deaminase/5-fluorocytosine suicide gene therapy system in a rat liver metastasis model. Cancer Gene Ther. 2007;14:858–866
  24. Yoshimura I, Mizuguchi Y, Miyajima A, Asano T, Tadakuma T, Hayakawa M. Suppression of lung metastasis of renal cell carcinoma by the intramuscular gene transfer of a soluble form of vascular endothelial growth factor receptor I. J. Urol. 2004;171:2467–2470
  25. Schmidt K, Hoffend J, Altmann A, Strauss LG, Dimitrakopoulou-Strauss A, Engelhardt B, et al. Transfer of the sFLT-1 gene in Morris hepatoma results in decreased growth and perfusion and induction of genes associated with stress response. Clin. Cancer Res. 2005;11:2132–2140
  26. Kommareddy S, Amiji M. Antiangiogenic gene therapy with systemically administered sFlt-1 plasmid DNA in engineered gelatin-based nanovectors. Cancer Gene Ther. 2007;14:488–498
  27. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell. 2009;15:232–239
  28. Pàez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Viñals F, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009;15:220–231
  29. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438:820–827
  30. Li B, Vincent A, Cates J, Brantley-Sieders DM, Polk DB, Young PP. Low levels of tumor necrosis factor alpha increase tumor growth by inducing an endothelial phenotype of monocytes recruited to the tumor site. Cancer Res. 2009;69:338–348
  31. Sanchez-Elsner T, Botella LM, Velasco B, Corbi A, Attisano L, Bernabeu C. Synergistic cooperation between hypoxia and transforming growth factor-beta pathways on human vascular endothelial growth factor gene expression. J. Biol. Chem. 2001;276:38527–38535
  32. Bar D, Apte RN, Voronov E, Dinarello CA, Cohen S. A continuous delivery system of IL-1 receptor antagonist reduces angiogenesis and inhibits tumor development. FASEB J. 2004;18:161–163
  33. Hedrick JA, Zlotnik A. Lymphotactin. Clin. Immunol. Immunopathol. 1998;87:218–222
  34. Yoshida T, Imai T, Takagi S, Nishimura M, Ishikawa I, Yaoi T, et al. Structure and expression of two highly related genes encoding SCM-1/human lymphotactin. FEBS Lett. 1996;395:82–88
  35. Broxmeyer HE, Kim CH, Cooper SH, Hangoc G, Hromas R, Pelus LM. Effects of CC, CXC, C, and CX3C chemokines on proliferation of myeloid progenitor cells, and insights into SDF-1-induced chemotaxis of progenitors. Ann. NY Acad. Sci. 1999;872:142–162
  36. Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006;66:605–612
  37. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer. 2004;4:71–78
  38. Makarenkova VP, Bansal V, Matta BM, Perez LA, Ochoa JB. CD11b+/Gr-1+ myeloid suppressor cells cause T cell dysfunction after traumatic stress. J. Immunol. 2006;176:2085–2094

PII: S0304-3835(10)00365-4

doi: 10.1016/j.canlet.2010.07.017

Cancer Letters
Volume 298, Issue 2 , Pages 264-272 , 8 December 2010