Molecular Oncology
Volume 1, Issue 3 , Pages 288-302 , December 2007

Vascular endothelial growth factor restores delayed tumor progression in tumors depleted of macrophages

  • Elaine Y. Lin

      Affiliations

    • Department of Medicine, Oncology Division, Albert Einstein College of Medicine, Bronx, NY, USA
  • ,
  • Jiu-feng Li

      Affiliations

    • Department of Developmental and Molecular Biology, Center of Reproductive Biology and Women's Health, Albert Einstein Cancer Center, Albert Einstein College of Medicine, 607 Chanin Bldg., 1300 Morris Park Avenue, Bronx, NY 10461, USA
  • ,
  • Gabriel Bricard

      Affiliations

    • Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, NY, USA
  • ,
  • Weigang Wang

      Affiliations

    • Department of Anatomy and Structural Biology, Albert Einstein College of Medicine, Bronx, NY, USA
  • ,
  • Yan Deng

      Affiliations

    • Analytical and Imaging Facility, Albert Einstein Cancer Center, Albert Einstein College of Medicine, Bronx, NY, USA
  • ,
  • Rani Sellers

      Affiliations

    • Department of Pathology, Albert Einstein College of Medicine, Bronx, NY, USA
  • ,
  • Steven A. Porcelli

      Affiliations

    • Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, NY, USA
  • ,
  • Jeffrey W. Pollard

      Affiliations

    • Department of Developmental and Molecular Biology, Center of Reproductive Biology and Women's Health, Albert Einstein Cancer Center, Albert Einstein College of Medicine, 607 Chanin Bldg., 1300 Morris Park Avenue, Bronx, NY 10461, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 718 430 2090.

Received 16 August 2007 ,Revised 10 October 2007 ,Accepted 12 October 2007.

References 

  1. Barleon B, Sozzani S, Zhou D, Weich HA, Mantovani A, Marme D. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood. 1996;87:3336–3343
  2. Cho CH, Koh YJ, Han J, Sung HK, Jong Lee H, Morisada T, et al. Angiogenic role of LYVE-1-positive macrophages in adipose tissue. Circ. Res. 2007;100:e47–e57
  3. Dong J, Grunstein J, Tejada M, Peale F, Frantz G, Liang WC, et al. VEGF-null cells require PDGFR alpha signaling-mediated stromal fibroblast recruitment for tumorigenesis. EMBO J. 2004;23:2800–2810
  4. Donnelly ML, Hughes LE, Luke G, Mendoza H, ten Dam E, Gani D, et al. The ‘cleavage’ activities of foot-and-mouth disease virus 2A site-directed mutants and naturally occurring ‘2A-like’ sequences. J. Gen. Virol. 2001;82:1027–1041
  5. Dvorak HF. Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J. Clin. Oncol. 2002;20:4368–4380
  6. Eubank TD, Galloway M, Montague CM, Waldman WJ, Marsh CB. M-CSF induces vascular endothelial growth factor production and angiogenic activity from human monocytes. J. Immunol. 2003;171:2637–2643
  7. de Felipe P. Skipping the co-expression problem: the new 2A “CHYSEL” technology. Genet. Vaccines Ther. 2004;2:13
  8. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 2004;25:581–611
  9. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat. Med. 2003;9:669–676
  10. Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin. Oncol. 2002;29:15–18
  11. Giraudo E, Inoue M, Hanahan D. An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J. Clin. Invest. 2004;114:623–633
  12. Gouon-Evans V, Rothenberg ME, Pollard JW. Postnatal mammary gland development requires macrophages and eosinophils. Development. 2000;127:2269–2282
  13. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Jung S, et al. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell. 2006;124:175–189
  14. Gunther EJ, Belka GK, Wertheim GBW, Wang J, Hartman JL, Boxer RB, et al. A novel doxycycline-inducible system for the transgenic analysis of mammary gland biology. FASEB J. 2002;16:283–292
  15. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomovirus middle T oncogenes: a transgenic mouse mode of a metastatic disease. Mol. Cell. Biol. 1992;12:954–961
  16. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 1996;86:353–364
  17. Jain RK, Duda DG, Clark JW, Loeffler JS. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nat. Clin. Pract. Oncol. 2006;3:24–40
  18. Keyt BA, Berleau LT, Nguyen HV, Chen H, Heinsohn H, Vandlen R, et al. The carboxyl-terminal domain (111–165) of vascular endothelial growth factor is critical for its mitogenic potency. J. Biol. Chem. 1996;271:7788–7795
  19. Kumaraswamy E, Carlson BA, Morgan F, Miyoshi K, Robinson GW, Su D, et al. Selective removal of the selenocysteine tRNA[Ser}Sec gene (Trsp) in mouse mammary epithelium. Mol. Cell. Biol. 2003;23:1477–1488
  20. Leek RD, Harris AL. Tumor-associated macrophages in breast cancer. J. Mamm. Gland Biol. Neoplasia. 2002;7:177–189
  21. Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res. 1996;56:4625–4629
  22. Leek RD, Hunt NC, Landers RJ, Lewis CE, Royds JA, Harris AL. Macrophage infiltration is associated with VEGF and EGFR expression in breast cancer. J. Pathol. 2000;190:430–436
  23. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246:1306–1309
  24. Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006;66:605–612
  25. Lin EY, Pollard JW. Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Res. 2007;67:5064–5066
  26. Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J. Exp. Med. 2001;193:727–740
  27. Lin EY, Gouon-Evans V, Nguyen AV, Pollard JW. The macrophage growth factor, CSF-1, in mammary gland development and tumor progression. J. Mamm. Gland Biol. Neoplasia. 2002;7:147–162
  28. Lin EY, Li JF, Gnatovskiy L, Deng Y, Zhu L, Grzesik DA, et al. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 2006;66:11238–11246
  29. Lobov IB, Rao S, Carroll TJ, Vallance JE, Ito M, Ondr JK, et al. WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature. 2005;437:417–421
  30. Mok E, Golovkina TV, Ross SR. A mouse mammary tumor virus mammary gland enhancer confers tissue-specific but not lactation-dependent expression in transgenic mice. J. Virol. 1992;66:7529–7532
  31. Naumov GN, Akslen LA, Folkman J. Role of angiogenesis in human tumor dormancy: animal models of the angiogenic switch. Cell Cycle. 2006;5:1779–1787
  32. Pollard JW, Stanley ER. Pleiotropic roles for CSF-1 in development defined by the mouse mutation osteopetrotic (op). Adv. Dev. Biochem. 1996;4:153–193
  33. Ross SR, Hsu C-LL, Choi Y, Mok E, Dudley JP. Negative regulation in correct tissue-specific expression of mouse mammary tumor virus in transgenic mice. Mol. Cell. Biol. 1990;10:5822–5829
  34. Sasmono RT, Oceandy D, Pollard JW, Tong W, Pavli P, Wainwright BJ, et al. A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood. 2003;101:1155–1163
  35. Schoeffner DJ, Matheny SL, Akahane T, Factor V, Berry A, Merlino G, et al. VEGF contributes to mammary tumor growth in transgenic mice through paracrine and autocrine mechanisms. Lab. Invest. 2005;85:608–623
  36. Scholl SM, Pallud C, Beuvon F, Hacene K, Stanley ER, Rohrschneider LR, et al. Anti-colony-stimulating factor-1 antibody staining in primary breast adenocarcinomas correlates with marked inflammatory cell infiltrates and prognosis. J. Natl. Cancer Inst. 1994;86:120–126
  37. Shima DT, Kuroki M, Deutsch U, Ng YS, Adamis AP, D'Amore PA. The mouse gene for vascular endothelial growth factor. Genomic structure, definition of the transcriptional unit, and characterization of transcriptional and post-transcriptional regulatory sequences. J. Biol. Chem. 1996;271:3877–3883
  38. Sunderkotter C, Steinbrink K, GoebelerBhardwaj R, Sorg C. Macrophages and angiogenesis. J. Leukocyte Biol. 1994;55:410–422
  39. Varney ML, Olsen KJ, Mosley RL, Singh RK. Paracrine regulation of vascular endothelial growth factor–a expression during macrophage-melanoma cell interaction: role of monocyte chemotactic protein-1 and macrophage colony-stimulating factor. J. Interferon Cytokine Res. 2005;25:674–683
  40. Yoshida A, Anand-Apte B, Zetter BR. Differential endothelial migration and proliferation to basic fibroblast growth factor and vascular endothelial growth factor. Growth Factors. 1996;13:57–64

PII: S1574-7891(07)00076-2

doi: 10.1016/j.molonc.2007.10.003

Molecular Oncology
Volume 1, Issue 3 , Pages 288-302 , December 2007