Review ArticleReview

Relationship of VEGF/VEGFR with immune and cancer cells: staggering or forward?

Yu-Ling Li, Hua Zhao and Xiu-Bao Ren
Cancer Biology & Medicine June 2016, 13 (2) 206-214; DOI: https://doi.org/10.20892/j.issn.2095-3941.2015.0070

References

  1. 1.↵
    2. Leung DW,
    3. Cachianes G,
    4. Kuang WJ,
    5. Goeddel DV,
    6. Ferrara N.
    Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989; 246: 1306–9.
    OpenUrlAbstract/FREE Full Text
  2. 2.↵
    2. Senger DR.
    Vascular endothelial growth factor: much more than an angiogenesis factor. Mol Biol Cell. 2010; 21: 377–9.
    OpenUrlAbstract/FREE Full Text
  3. 3.↵
    2. Ferrara N,
    3. Carver-Moore K,
    4. Chen H,
    5. Dowd M,
    6. Lu L,
    7. O'Shea KS, et al.
    Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 1996; 380: 439–42.
    OpenUrlCrossRefPubMedWeb of Science
  4. 4.↵
    2. Ziegler BL,
    3. Valtieri M,
    4. Porada GA,
    5. De Maria R,
    6. Muller R,
    7. Masella B, et al.
    KDR receptor: a key marker defining hematopoietic stem cells. Science. 1999; 285: 1553–8.
    OpenUrlAbstract/FREE Full Text
  5. 5.↵
    2. Yaqoob U,
    3. Cao S,
    4. Shergill U,
    5. Jagavelu K,
    6. Geng Z,
    7. Yin M, et al.
    Neuropilin-1 stimulates tumor growth by increasing fibronectin fibril assembly in the tumor microenvironment. Cancer Res. 2012; 72: 4047–59.
    OpenUrlAbstract/FREE Full Text
  6. 6.↵
    2. Hansen W,
    3. Hutzler M,
    4. Abel S,
    5. Alter C,
    6. Stockmann C,
    7. Kliche S, et al.
    Neuropilin 1 deficiency on CD4+Foxp3+ regulatory T cells impairs mouse melanoma growth. J Exp Med. 2012; 209: 2001–16.
    OpenUrlAbstract/FREE Full Text
  7. 7.↵
    2. Beck B,
    3. Driessens G,
    4. Goossens S,
    5. Youssef KK,
    6. Kuchnio A,
    7. Caauwe A, et al.
    A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours. Nature. 2011; 478: 399-403.
    OpenUrlCrossRefPubMedWeb of Science
  8. 8.↵
    2. Philip B,
    3. Ito K,
    4. Moreno-Sanchez R,
    5. Ralph SJ.
    HIF expression and the role of hypoxic microenvironments within primary tumours as protective sites driving cancer stem cell renewal and metastatic progression. Carcinogenesis. 2013; 34: 1699–707.
    OpenUrlCrossRefPubMedWeb of Science
  9. 9.↵
    2. Koch S,
    3. Claesson-Welsh L.
    Signal transduction by vascular endothelial growth factor receptors. Cold Spring Harb Perspect Med. 2012; 2: a006502.
    OpenUrlAbstract/FREE Full Text
  10. 10.↵
    2. Roberts WG,
    3. Palade GE.
    Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci. 1995; 108 (Pt 6): 2369–79.
    OpenUrlAbstract/FREE Full Text
  11. 11.↵
    2. Brogi E,
    3. Wu T,
    4. Namiki A,
    5. Isner JM.
    Indirect angiogenic cytokines upregulate VEGF and bFGF gene expression in vascular smooth muscle cells, whereas hypoxia upregulates VEGF expression only. Circulation. 1994; 90: 649–52.
    OpenUrlAbstract/FREE Full Text
  12. 12.↵
    2. Kikuchi K,
    3. Kusama K,
    4. Sano M,
    5. Nakanishi Y,
    6. Ishige T,
    7. Ohni S, et al.
    Vascular endothelial growth factor and dendritic cells in human squamous cell carcinoma of the oral cavity. Anticancer Res. 2006; 26: 1833–48.
    OpenUrlAbstract/FREE Full Text
  13. 13.↵
    2. Kowanetz M,
    3. Ferrara N.
    Vascular endothelial growth factor signaling pathways: therapeutic perspective. Clin Cancer Res. 2006;12:5018–22.
    OpenUrlAbstract/FREE Full Text
  14. 14.↵
    2. Shibuya M,
    3. Yamaguchi S,
    4. Yamane A,
    5. Ikeda T,
    6. Tojo A,
    7. Matsushime H, et al.
    Nucleotide sequence and expression of a novel human receptor-type tyrosine kinase gene (flt) closely related to the fms family. Oncogene. 1990; 5: 519–24.
    OpenUrlPubMedWeb of Science
  15. 15.↵
    2. Neufeld G,
    3. Kessler O,
    4. Herzog Y.
    The interaction of Neuropilin-1 and Neuropilin-2 with tyrosine-kinase receptors for VEGF. Adv Exp Med Biol. 2002;515:81–90.
    OpenUrlCrossRefPubMedWeb of Science
  16. 16.↵
    2. Jiang T,
    3. Zhuang J,
    4. Duan H,
    5. Luo Y,
    6. Zeng Q,
    7. Fan K, et al.
    CD146 is a coreceptor for VEGFR-2 in tumor angiogenesis. Blood. 2012; 120: 2330–9.
    OpenUrlAbstract/FREE Full Text
  17. 17.↵
    2. Kendall RL,
    3. Thomas KA.
    Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci U S A. 1993; 90: 10705–9.
    OpenUrlAbstract/FREE Full Text
  18. 18.↵
    2. Singh N,
    3. Tiem M,
    4. Watkins R,
    5. Cho YK,
    6. Wang Y, et al.
    Soluble vascular endothelial growth factor receptor 3 is essential for corneal alymphaticity. Blood. 2013; 121: 4242–9.
    OpenUrlAbstract/FREE Full Text
  19. 19.↵
    2. Dikov MM,
    3. Ohm JE,
    4. Ray N,
    5. Tchekneva EE,
    6. Burlison J,
    7. Moghanaki D, et al.
    Differential roles of vascular endothelial growth factor receptors 1 and 2 in dendritic cell differentiation. J Immunol. 2005; 174: 215–22.
    OpenUrlAbstract/FREE Full Text
  20. 20.↵
    2. Ginhoux F,
    3. Tacke F,
    4. Angeli V,
    5. Bogunovic M,
    6. Loubeau M,
    7. Dai XM, et al.
    Langerhans cells arise from monocytes in vivo. Nat Immunol. 2006; 7: 265–73.
    OpenUrlCrossRefPubMedWeb of Science
  21. 21.↵
    2. Hoehn GT,
    3. Stokland T,
    4. Amin S,
    5. Ramirez M,
    6. Hawkins AL,
    7. Griffin CA, et al.
    Tnk1: a novel intracellular tyrosine kinase gene isolated from human umbilical cord blood CD34+/Lin-/CD38-stem/progenitor cells. Oncogene. 1996; 12: 903–13.
    OpenUrlPubMedWeb of Science
  22. 22.↵
    2. Katoh O,
    3. Tauchi H,
    4. Kawaishi K,
    5. Kimura A,
    6. Satow Y.
    Expression of the vascular endothelial growth factor (VEGF) receptor gene, KDR, in hematopoietic cells and inhibitory effect of VEGF on apoptotic cell death caused by ionizing radiation. Cancer Res. 1995; 55: 5687-92.
    OpenUrlAbstract/FREE Full Text
  23. 23.↵
    2. Kaipainen A,
    3. Korhonen J,
    4. Mustonen T,
    5. van Hinsbergh VW,
    6. Fang GH,
    7. Dumont D, et al.
    Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc Natl Acad Sci U S A. 1995; 92: 3566–70.
    OpenUrlAbstract/FREE Full Text
  24. 24.↵
    2. Partanen TA,
    3. Arola J,
    4. Saaristo A,
    5. Jussila L,
    6. Ora A,
    7. Miettinen M, et al.
    VEGF-C and VEGF-D expression in neuroendocrine cells and their receptor, VEGFR-3, in fenestrated blood vessels in human tissues. FASEB J. 2000; 14: 2087–96.
    OpenUrlCrossRefPubMedWeb of Science
  25. 25.↵
    2. Wilting J,
    3. Eichmann A,
    4. Christ B.
    Expression of the avian VEGF receptor homologues Quek1 and Quek2 in blood-vascular and lymphatic endothelial and non-endothelial cells during quail embryonic development. Cell Tissue Res. 1997; 288: 207–23.
    OpenUrlCrossRefPubMedWeb of Science
  26. 26.↵
    2. Mimura T,
    3. Amano S,
    4. Usui T,
    5. Kaji Y,
    6. Oshika T,
    7. Ishii Y.
    Expression of vascular endothelial growth factor C and vascular endothelial growth factor receptor 3 in corneal lymphangiogenesis. Exp Eye Res. 2001; 72: 71–8.
    OpenUrlCrossRefPubMedWeb of Science
  27. 27.↵
    2. Cursiefen C,
    3. Schlotzer-Schrehardt U,
    4. Kuchle M,
    5. Sorokin L,
    6. Breiteneder-Geleff S,
    7. Alitalo K, et al.
    Lymphatic vessels in vascularized human corneas: immunohistochemical investigation using LYVE-1 and podoplanin. Invest Ophthalmol Vis Sci. 2002; 43: 2127–35.
    OpenUrlAbstract/FREE Full Text
  28. 28.↵
    2. Hamrah P,
    3. Zhang Q,
    4. Dana MR.
    Expression of vascular endothelial growth factor receptor-3 (VEGFR-3) in the conjunctiva--a potential link between lymphangiogenesis and leukocyte trafficking on the ocular surface. Adv Exp Med Biol. 2002; 506: 851–60.
    OpenUrlPubMedWeb of Science
  29. 29.↵
    2. Gabrilovich DI,
    3. Chen HL,
    4. Girgis KR,
    5. Cunningham HT,
    6. Meny GM,
    7. Nadaf S, et al.
    Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat Med. 1996; 2: 1096–103.
    OpenUrlCrossRefPubMedWeb of Science
  30. 30.↵
    2. Oyama T,
    3. Ran S,
    4. Ishida T,
    5. Nadaf S,
    6. Kerr L,
    7. Carbone DP, et al.
    Vascular endothelial growth factor affects dendritic cell maturation through the inhibition of nuclear factor-kappa B activation in hemopoietic progenitor cells. J Immunol. 1998; 160: 1224–32.
    OpenUrlAbstract/FREE Full Text
  31. 31.↵
    2. Ohm JE,
    3. Carbone DP.
    VEGF as a mediator of tumor-associated immunodeficiency. Immunol Res. 2001; 23: 263–72.
    OpenUrlCrossRefPubMedWeb of Science
  32. 32.↵
    2. Chapoval SP,
    3. Lee CG,
    4. Tang C,
    5. Keegan AD,
    6. Cohn L,
    7. Bottomly K, et al.
    Lung vascular endothelial growth factor expression induces local myeloid dendritic cell activation. Clin Immunol. 2009; 132: 371–84.
    OpenUrlCrossRefPubMed
  33. 33.↵
    2. Riboldi E,
    3. Musso T,
    4. Moroni E,
    5. Urbinati C,
    6. Bernasconi S,
    7. Rusnati M, et al.
    Cutting edge: proangiogenic properties of alternatively activated dendritic cells. J Immunol. 2005; 175: 2788–92.
    OpenUrlAbstract/FREE Full Text
  34. 34.↵
    2. Fernandez Pujol B,
    3. Lucibello FC,
    4. Gehling UM,
    5. Lindemann K,
    6. Weidner N,
    7. Zuzarte ML, et al.
    Endothelial-like cells derived from human CD14 positive monocytes. Differentiation. 2000; 65: 287-300.
    OpenUrlCrossRefPubMedWeb of Science
  35. 35.↵
    2. Peichev M,
    3. Naiyer AJ,
    4. Pereira D,
    5. Zhu Z,
    6. Lane WJ,
    7. Williams M, et al.
    Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood. 2000; 95: 952–8.
    OpenUrlAbstract/FREE Full Text
  36. 36.↵
    2. Su JL,
    3. Yen CJ,
    4. Chen PS,
    5. Chuang SE,
    6. Hong CC,
    7. Kuo IH, et al.
    The role of the VEGF-C/VEGFR-3 axis in cancer progression. Br J Cancer. 2007; 96: 541–5.
    OpenUrlCrossRefPubMedWeb of Science
  37. 37.↵
    2. Ohm JE,
    3. Gabrilovich DI,
    4. Sempowski GD,
    5. Kisseleva E,
    6. Parman KS,
    7. Nadaf S, et al.
    VEGF inhibits T-cell development and may contribute to tumor-induced immune suppression. Blood. 2003; 101: 4878–86.
    OpenUrlAbstract/FREE Full Text
  38. 38.↵
    2. Basu A,
    3. Hoerning A,
    4. Datta D,
    5. Edelbauer M,
    6. Stack MP,
    7. Calzadilla K, et al.
    Cutting edge: Vascular endothelial growth factor-mediated signaling in human CD45RO+ CD4+ T cells promotes Akt and ERK activation and costimulates IFN-gamma production. J Immunol. 2010; 184: 545–9.
    OpenUrlAbstract/FREE Full Text
  39. 39.↵
    2. Krebs R,
    3. Tikkanen JM,
    4. Ropponen JO,
    5. Jeltsch M,
    6. Jokinen JJ,
    7. Yla-Herttuala S, et al.
    Critical role of VEGF-C/VEGFR-3 signaling in innate and adaptive immune responses in experimental obliterative bronchiolitis. Am J Pathol. 2012; 181: 1607–20.
    OpenUrlCrossRefPubMed
  40. 40.↵
    2. Wada J,
    3. Suzuki H,
    4. Fuchino R,
    5. Yamasaki A,
    6. Nagai S,
    7. Yanai K, et al.
    The contribution of vascular endothelial growth factor to the induction of regulatory T-cells in malignant effusions. Anticancer Res. 2009; 29: 881–8.
    OpenUrlAbstract/FREE Full Text
  41. 41.↵
    2. Wang FQ,
    3. Barfield E,
    4. Dutta S,
    5. Pua T,
    6. Fishman DA.
    VEGFR-2 silencing by small interference RNA (siRNA) suppresses LPA-induced epithelial ovarian cancer (EOC) invasion. Gynecol Oncol. 2009; 115: 414–23.
    OpenUrlPubMed
  42. 42.↵
    2. Wang FQ,
    3. So J,
    4. Reierstad S,
    5. Fishman DA.
    Vascular endothelial growth factor-regulated ovarian cancer invasion and migration involves expression and activation of matrix metalloproteinases. Int J Cancer. 2006; 118: 879–88.
    OpenUrlCrossRefPubMedWeb of Science
  43. 43.↵
    2. Dias S,
    3. Choy M,
    4. Alitalo K,
    5. Rafii S.
    Vascular endothelial growth factor (VEGF)-C signaling through FLT-4 (VEGFR-3) mediates leukemic cell proliferation, survival, and resistance to chemotherapy. Blood. 2002; 99: 2179–84.
    OpenUrlAbstract/FREE Full Text
  44. 44.↵
    2. Hamerlik P,
    3. Lathia JD,
    4. Rasmussen R,
    5. Wu Q,
    6. Bartkova J,
    7. Lee M, et al.
    Autocrine VEGF-VEGFR2-Neuropilin-1 signaling promotes glioma stem-like cell viability and tumor growth. J Exp Med. 2012; 209: 507–20.
    OpenUrlAbstract/FREE Full Text
  45. 45.↵
    2. Penna G,
    3. Adorini L.
    1 Alpha, 25-dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J Immunol. 2000; 164: 2405–11.
    OpenUrlAbstract/FREE Full Text
  46. 46.↵
    2. Goerdt S,
    3. Orfanos CE.
    Other functions, other genes: alternative activation of antigen-presenting cells. Immunity. 1999; 10: 137–42.
    OpenUrlCrossRefPubMedWeb of Science
  47. 47.↵
    2. Ferrara N,
    3. Gerber HP,
    4. LeCouter J.
    The biology of VEGF and its receptors. Nat Med. 2003; 9: 669–76.
    OpenUrlCrossRefPubMedWeb of Science
  48. 48.↵
    2. Fernandez Pujol B,
    3. Lucibello FC,
    4. Zuzarte M,
    5. Lutjens P,
    6. Muller R,
    7. Havemann K.
    Dendritic cells derived from peripheral monocytes express endothelial markers and in the presence of angiogenic growth factors differentiate into endothelial-like cells. Eur J Cell Biol. 2001; 80: 99–110.
    OpenUrlCrossRefPubMedWeb of Science
  49. 49.↵
    2. Fantin A,
    3. Vieira JM,
    4. Gestri G,
    5. Denti L,
    6. Schwarz Q,
    7. Prykhozhij S, et al.
    Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood. 2010; 116: 829–40.
    OpenUrlAbstract/FREE Full Text
  50. 50.↵
    2. Takeda Y,
    3. Costa S,
    4. Delamarre E,
    5. Roncal C,
    6. Leite de Oliveira R,
    7. Squadrito ML, et al.
    Macrophage skewing by Phd2 haplodeficiency prevents ischaemia by inducing arteriogenesis. Nature. 2011; 479: 122–6.
    OpenUrlCrossRefPubMedWeb of Science
  51. 51.↵
    2. Wynn TA,
    3. Chawla A,
    4. Pollard JW.
    Macrophage biology in development, homeostasis and disease. Nature. 2013; 496: 445–55.
    OpenUrlCrossRefPubMedWeb of Science
  52. 52.↵
    2. Barleon B,
    3. Sozzani S,
    4. Zhou D,
    5. Weich HA,
    6. Mantovani A,
    7. 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: 3336–43.
    OpenUrlAbstract/FREE Full Text
  53. 53.↵
    2. Sawano A,
    3. Iwai S,
    4. Sakurai Y,
    5. Ito M,
    6. Shitara K,
    7. Nakahata T, et al.
    Flt-1, vascular endothelial growth factor receptor 1, is a novel cell surface marker for the lineage of monocyte-macrophages in humans. Blood. 2001; 97: 785–91.
    OpenUrlAbstract/FREE Full Text
  54. 54.↵
    2. Schoppmann SF,
    3. Birner P,
    4. Stockl J,
    5. Kalt R,
    6. Ullrich R,
    7. Caucig C, et al.
    Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol. 2002; 161: 947–56.
    OpenUrlCrossRefPubMedWeb of Science
  55. 55.↵
    2. Zhang Y,
    3. Lu Y,
    4. Ma L,
    5. Cao X,
    6. Xiao J,
    7. Chen J, et al.
    Activation of vascular endothelial growth factor receptor-3 in macrophages restrains TLR4-NF-kappaB signaling and protects against endotoxin shock. Immunity. 2014; 40: 501–14.
    OpenUrlCrossRefPubMed
  56. 56.↵
    2. Gavalas NG,
    3. Tsiatas M,
    4. Tsitsilonis O,
    5. Politi E,
    6. Ioannou K,
    7. Ziogas AC, et al.
    VEGF directly suppresses activation of T cells from ascites secondary to ovarian cancer via VEGF receptor type 2. Br J Cancer. 2012; 107: 1869–75.
    OpenUrlCrossRefPubMed
  57. 57.↵
    2. Chung GG,
    3. Yoon HH,
    4. Zerkowski MP,
    5. Ghosh S,
    6. Thomas L,
    7. Harigopal M, et al.
    Vascular endothelial growth factor, FLT-1, and FLK-1 analysis in a pancreatic cancer tissue microarray. Cancer. 2006; 106: 1677–84.
    OpenUrlCrossRefPubMed
  58. 58.↵
    2. Lichtenberger BM,
    3. Tan PK,
    4. Niederleithner H,
    5. Ferrara N,
    6. Petzelbauer P,
    7. Sibilia M.
    Autocrine VEGF signaling synergizes with EGFR in tumor cells to promote epithelial cancer development. Cell. 2010; 140: 268–79.
    OpenUrlCrossRefPubMedWeb of Science
  59. 59.↵
    2. Ogawa E,
    3. Takenaka K,
    4. Yanagihara K,
    5. Kurozumi M,
    6. Manabe T,
    7. Wada H, et al.
    Clinical significance of VEGF-C status in tumour cells and stromal macrophages in non-small cell lung cancer patients. Br J Cancer. 2004; 91: 498–503.
    OpenUrlCrossRefPubMedWeb of Science
  60. 60.↵
    2. Schoppmann SF,
    3. Fenzl A,
    4. Nagy K,
    5. Unger S,
    6. Bayer G,
    7. Geleff S, et al.
    VEGF-C expressing tumor-associated macrophages in lymph node positive breast cancer: impact on lymphangiogenesis and survival. Surgery. 2006; 139: 839–46.
    OpenUrlCrossRefPubMedWeb of Science
  61. 61.↵
    2. Kerjaschki D.
    The crucial role of macrophages in lymphangiogenesis. J Clin Invest. 2005; 115: 2316–9.
    OpenUrlCrossRefPubMedWeb of Science
  62. 62.↵
    2. Maruyama K,
    3. Ii M,
    4. Cursiefen C,
    5. Jackson DG,
    6. Keino H,
    7. Tomita M, et al.
    Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest. 2005; 115: 2363-72.
    OpenUrlCrossRefPubMedWeb of Science
  63. 63.↵
    2. Li C,
    3. Liu B,
    4. Dai Z,
    5. Tao Y.
    Knockdown of VEGF receptor-1 (VEGFR-1) impairs macrophage infiltration, angiogenesis and growth of clear cell renal cell carcinoma (CRCC). Cancer Biol Ther. 2011; 12: 872–80.
    OpenUrlCrossRefPubMed
  64. 64.↵
    2. Lo HW,
    3. Hung MC.
    Nuclear EGFR signalling network in cancers: linking EGFR pathway to cell cycle progression, nitric oxide pathway and patient survival. Br J Cancer. 2006; 94: 184–8.
    OpenUrlCrossRefPubMedWeb of Science
  65. 65.↵
    2. Lee S,
    3. Chen TT,
    4. Barber CL,
    5. Jordan MC,
    6. Murdock J,
    7. Desai S, et al.
    Autocrine VEGF signaling is required for vascular homeostasis. Cell. 2007; 130: 691–703.
    OpenUrlCrossRefPubMedWeb of Science
  66. 66.↵
    2. Zindl CL,
    3. Chaplin DD.
    Immunology. Tumor immune evasion. Science. 2010; 328: 697–8.
    OpenUrlAbstract/FREE Full Text
  67. 67.↵
    2. Bergers G,
    3. Benjamin LE.
    Tumorigenesis and the angiogenic switch. Nat Rev Cancer. 2003; 3: 401–10.
    OpenUrlCrossRefPubMedWeb of Science
  68. 68.↵
    2. Toi M,
    3. Taniguchi T,
    4. Yamamoto Y,
    5. Kurisaki T,
    6. Suzuki H,
    7. Tominaga T.
    Clinical significance of the determination of angiogenic factors. Eur J Cancer. 1996; 32A: 2513-9.
    OpenUrlCrossRef
  69. 69.↵
    2. Jüttner S,
    3. Wissmann C,
    4. Jöns T,
    5. Vieth M,
    6. Hertel J,
    7. Gretschel S, et al.
    Vascular endothelial growth factor-D and its receptor VEGFR-3: two novel independent prognostic markers in gastric adenocarcinoma. J Clin Oncol. 2006; 24: 228–40.
    OpenUrlAbstract/FREE Full Text
  70. 70.↵
    2. Su JL,
    3. Yang PC,
    4. Shih JY,
    5. Yang CY,
    6. Wei LH,
    7. Hsieh CY, et al.
    The VEGF-C/Flt-4 axis promotes invasion and metastasis of cancer cells. Cancer Cell. 2006; 9: 209–23.
    OpenUrlCrossRefPubMedWeb of Science
  71. 71.↵
    2. Pizon M,
    3. Zimon DS,
    4. Pachmann U,
    5. Pachmann K.
    Insulin-like growth factor receptor I (IGF-IR) and vascular endothelial growth factor receptor 2 (VEGFR-2) are expressed on the circulating epithelial tumor cells of breast cancer patients. PLoS One. 2013; 8: e56836.
  72. 72.↵
    2. Meng Y,
    3. Kang S,
    4. So J,
    5. Reierstad S,
    6. Fishman DA.
    Translocation of Fas by LPA prevents ovarian cancer cells from anti-Fas-induced apoptosis. Gynecol Oncol. 2005; 96: 462–9.
    OpenUrlCrossRefPubMedWeb of Science
  73. 73.↵
    2. Hu YL,
    3. Tee MK,
    4. Goetzl EJ,
    5. Auersperg N,
    6. Mills GB,
    7. Ferrara N, et al.
    Lysophosphatidic acid induction of vascular endothelial growth factor expression in human ovarian cancer cells. J Natl Cancer Inst. 2001; 93: 762–8.
    OpenUrlCrossRefPubMedWeb of Science
  74. 74.↵
    2. Dutta S,
    3. Wang FQ,
    4. Wu HS,
    5. Mukherjee TJ,
    6. Fishman DA.
    The NF-kappaB pathway mediates lysophosphatidic acid (LPA)-induced VEGF signaling and cell invasion in epithelial ovarian cancer (EOC). Gynecol Oncol. 2011; 123: 129–37.
    OpenUrlCrossRefPubMed
  75. 75.↵
    2. Waldner MJ,
    3. Wirtz S,
    4. Jefremow A,
    5. Warntjen M,
    6. Neufert C,
    7. Atreya R, et al.
    VEGF receptor signaling links inflammation and tumorigenesis in colitis-associated cancer. J Exp Med. 2010; 207: 2855–68.
    OpenUrlAbstract/FREE Full Text
Back to top

In this issue

Print
Download PDF
Email Article
Citation Tools

Jump to section

Keywords