Vascular endothelial growth factor-dependent spatiotemporal dual roles of placental growth factor in modulation of angiogenesis and tumor growth

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 34, 2013, Pages 13932-13937

  Yang, Xiaojuan ^a   Zhang, Yin ^a   Yang, Yunlong ^a   Lim, Sharon ^a   Cao, Ziquan ^b   Rak, Janusz ^c   Cao, Yihai ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b LINKÖPING UNIVERSITY   (Sweden)

^c MONTREAL CHILDREN S HOSPITAL   (Canada)

Author keywords

Antiangiogenic therapy; Neovascularization; VEGF receptor signaling

Indexed keywords

PLACENTAL GROWTH FACTOR; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL; CANCER GROWTH; CANCER INHIBITION; CONTROLLED STUDY; FIBROSARCOMA; GROWTH RATE; LEWIS CARCINOMA; LUNG CARCINOMA; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION;

ANTIANGIOGENIC THERAPY; NEOVASCULARIZATION; VEGF RECEPTOR SIGNALING;

ANIMALS; CELL LINE, TUMOR; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; MALE; MICE; MICE, INBRED C57BL; MICE, SCID; MICROSCOPY, CONFOCAL; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PREGNANCY PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84882805811     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1309629110     Document Type: Article

References (39)

1. Jain RK (2005) Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science 307(5706):58-62.
2. Cao Y (2009) Tumor angiogenesis and molecular targets for therapy. Front Biosci 14:3962-3973.
3. Ferrara N, Kerbel RS (2005) Angiogenesis as a therapeutic target. Nature 438(7070): 967-974.
4. Nagy JA, Chang SH, Dvorak AM, Dvorak HF (2009) Why are tumour blood vessels abnormal and why is it important to know? Br J Cancer 100(6):865-869.
5. Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1(1):27-31.
6. Cao Y, et al. (2011) Forty-year journey of angiogenesis translational research. Sci Transl Med 3(114):114rv113.
7. Kerbel RS (2008) Tumor angiogenesis. N Engl J Med 358(19):2039-2049.
8. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9(6):669-676.
9. Senger DR, et al. (1993) Vascular permeability factor (VPF, VEGF) in tumor biology. Cancer Metastasis Rev 12(3-4):303-324.
10. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M (1998) Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92(6):735-745.
11. Shalaby F, et al. (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376(6535):62-66.
12. Cao Y (2009) Positive and negative modulation of angiogenesis by VEGFR1 ligands. Sci Signal 2(59):re1.
13. Fong GH, Rossant J, Gertsenstein M, Breitman ML (1995) Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376(6535): 66-70.
14. Lee J, et al. (1996) Vascular endothelial growth factor-related protein: A ligand and specific activator of the tyrosine kinase receptor Flt4. Proc Natl Acad Sci USA 93(5): 1988-1992.
15. Mancuso MR, et al. (2006) Rapid vascular regrowth in tumors after reversal of VEGF inhibition. J Clin Invest 116(10):2610-2621.
16. Olofsson B, et al. (1998) Vascular endothelial growth factor B (VEGF-B) binds to VEGF receptor-1 and regulates plasminogen activator activity in endothelial cells. Proc Natl Acad Sci USA 95(20):11709-11714.
17. Hedlund EM, Hosaka K, Zhong Z, Cao R, Cao Y (2009) Malignant cell-derived PlGF promotes normalization and remodeling of the tumor vasculature. Proc Natl Acad Sci USA 106(41):17505-17510.
18. Hedlund EM, et al. (2013) Tumor cell-derived placental growth factor sensitizes antiangiogenic and antitumor effects of anti-VEGF drugs. Proc Natl Acad Sci USA 110(2): 654-659.
19. Eriksson A, et al. (2002) Placenta growth factor-1 antagonizes VEGF-induced angiogenesis and tumor growth by the formation of functionally inactive PlGF-1/VEGF heterodimers. Cancer Cell 1(1):99-108.
20. Viloria-Petit A, et al. (2003) Contrasting effects of VEGF gene disruption in embryonic stem cell-derived versus oncogene-induced tumors. EMBO J 22(16):4091-4102.
21. Hormigo A, Gutin PH, Rafii S (2007) Tracking normalization of brain tumor vasculature by magnetic imaging and proangiogenic biomarkers. Cancer Cell 11(1):6-8.
22. Winkler F, et al. (2004) Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 6(6):553-563.
23. Cao Y, et al. (1996) Heterodimers of placenta growth factor/vascular endothelial growth factor. Endothelial activity, tumor cell expression, and high affinity binding to Flk-1/KDR. J Biol Chem 271(6):3154-3162.
24. Rolny C, et al. (2011) HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 19(1):31-44.
25. Cao R, et al. (2010) VEGFR1-mediated pericyte ablation links VEGF and PlGF to cancerassociated retinopathy. Proc Natl Acad Sci USA 107(2):856-861.
26. Xue Y, et al. (2009) Hypoxia-independent angiogenesis in adipose tissues during cold acclimation. Cell Metab 9(1):99-109.
27. Cao Y, Zhong W, Sun Y (2009) Improvement of antiangiogenic cancer therapy by understanding the mechanisms of angiogenic factor interplay and drug resistance. Semin Cancer Biol 19(5):338-343.
28. Cao Y, Linden P, Shima D, Browne F, Folkman J (1996) In vivo angiogenic activity and hypoxia induction of heterodimers of placenta growth factor/vascular endothelial growth factor. J Clin Invest 98(11):2507-2511.
29. Luttun A, et al. (2002) Loss of placental growth factor protects mice against vascular permeability in pathological conditions. Biochem Biophys Res Commun 295(2): 428-434.
30. Carmeliet P, et al. (2001) Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 7(5):575-583.
31. Fischer C, et al. (2007) Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 131(3):463-475.
32. Bais C, et al. (2010) PlGF blockade does not inhibit angiogenesis during primary tumor growth. Cell 141(1):166-177.
33. Xu L, et al. (2006) Placenta growth factor overexpression inhibits tumor growth, angiogenesis, and metastasis by depleting vascular endothelial growth factor homodimers in orthotopic mouse models. Cancer Res 66(8):3971-3977.
34. Schomber T, et al. (2007) Placental growth factor-1 attenuates vascular endothelial growth factor-A-dependent tumor angiogenesis during beta cell carcinogenesis. Cancer Res 67(22):10840-10848.
35. Björndahl M, Cao R, Eriksson A, Cao Y (2004) Blockage of VEGF-induced angiogenesis by preventing VEGF secretion. Circ Res 94(11):1443-1450.
36. Fischer C, Mazzone M, Jonckx B, Carmeliet P (2008) FLT1 and its ligands VEGFB and PlGF: Drug targets for anti-angiogenic therapy? Nat Rev Cancer 8(12):942-956.
37. Dong J, et al. (2004) VEGF-null cells require PDGFR alpha signaling-mediated stromal fibroblast recruitment for tumorigenesis. EMBO J 23(14):2800-2810.
38. Bhandarkar SS, et al. (2009) Fulvene-5 potently inhibits NADPH oxidase 4 and blocks the growth of endothelial tumors in mice. J Clin Invest 119(8):2359-2365.
39. Munson JM, et al. (2012) Anti-invasive adjuvant therapy with imipramine blue enhances chemotherapeutic efficacy against glioma. Sci Transl Med 4(127):127ra136.