Dual Inhibition of Plasminogen Kringle 5 on Angiogenesis and Chemotaxis Suppresses Tumor Metastasis by Targeting HIF-1α Pathway

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Cai, Wei Bin ^a   Zhang, Yang ^a   Cheng, Rui ^a   Wang, Zheng ^a   Fang, Shu Huan ^a,b   Xu, Zu Min ^a   Yang, Xia ^a,c   Yang, Zhong Han ^a   Ma, Jian Xing ^d   Shao, Chun Kui ^c   Gao, Guo Quan ^a,c  

^a SUN YAT SEN UNIVERSITY   (China)

^b GUANGZHOU UNIVERSITY OF CHINESE MEDICINE   (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; CHEMOKINE RECEPTOR CXCR4; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PLASMINOGEN KRINGLE 5; SMALL INTERFERING RNA; STROMAL CELL DERIVED FACTOR 1ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL MOTILITY; CELL NUCLEUS; CELL PROLIFERATION; CHEMOTAXIS; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; IN VIVO STUDY; LEWIS CARCINOMA; LUNG METASTASIS; METASTASIS INHIBITION; MICROMETASTASIS; MIGRATION INHIBITION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; TRANSACTIVATION; TUMOR GROWTH; TUMOR VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; APOPTOSIS; CARCINOMA, LEWIS LUNG; CELL LINE, TUMOR; CELL PROLIFERATION; CHEMOKINE CXCL12; CHEMOTAXIS; DOWN-REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LUNG NEOPLASMS; MICE; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PEPTIDE FRAGMENTS; PLASMINOGEN; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MUS;

EID: 84871774384     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053152     Document Type: Article

References (47)

1. Folkman J, (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1: 27-31.
2. Lee SL, Rouhi P, Dahl Jensen L, Zhang D, Ji H, et al. (2009) Hypoxia-induced pathological angiogenesis mediates tumor cell dissemination, invasion, and metastasis in a zebrafish tumor model. Proc Natl Acad Sci U S A 106: 19485-19490.
3. Dachs GU, Tozer GM, (2000) Hypoxia modulated gene expression: Angiogenesis, metastasis and therapeutic exploitation. Eur J Cancer 36: 1649-1660.
4. Maxwell PH, Dachs GU, Gleadle JM, Nicholls LG, Harris AL, et al. (1997) Hypoxia-inducible factor-1 modulates gene expression in solid tumors and influences both angiogenesis and tumor growth. Proc Natl Acad Sci U S A 94: 8104-8109.
5. Pugh CW, Ratcliffe PJ, (2003) The von hippel-lindau tumor suppressor, hypoxia-inducible factor-1 (hif-1) degradation, and cancer pathogenesis. Semin Cancer Biol 13: 83-89.
6. Cao Y, Chen A, An SS, Ji RW, Davidson D, et al. (1997) Kringle 5 of plasminogen is a novel inhibitor of endothelial cell growth. J Biol Chem 272: 22924-22928.
7. Cai W, Ma J, Li C, Yang Z, Yang X, Liu W, et al. (2005) Enhanced anti-angiogenic effect of a deletion mutant of plasminogen kringle 5 on neovascularization. J Cell Biochem 96: 1254-1261.
8. Yang X, Cheng R, Li C, Cai W, Ma JX, et al. (2006) Kringle 5 of human plasminogen suppresses hepatocellular carcinoma growth both in grafted and xenografted mice by anti-angiogenic activity. Cancer Biol Ther 5: 399-405.
9. Zhang Z, Ma JX, Gao G, Li C, Luo L, et al. (2005) Plasminogen kringle 5 inhibits alkali-burn-induced corneal neovascularization. Invest Ophthalmol Vis Sci 46: 4062-4071.
10. Zhang SX, Sima J, Shao C, Fant J, Chen Y, et al. (2004) Plasminogen kringle 5 reduces vascular leakage in the retina in rat models of oxygen-induced retinopathy and diabetes. Diabetologia 47: 124-131.
11. Zhang D, Kaufman PL, Gao G, Saunders RA, Ma JX, (2001) Intravitreal injection of plasminogen kringle 5, an endogenous angiogenic inhibitor, arrests retinal neovascularization in rats. Diabetologia 44: 757-765.
12. Yang X, Cai W, Xu Z, Chen J, Li C, et al. (2010) High efficacy and minimal peptide required for the anti-angiogenic and anti-hepatocarcinoma activities of plasminogen k5. J Cell Mol Med 14: 2519-2530.
13. Jiang W, Jin G, Ma D, Wang F, Fu T, et al. (2012) Modification of cyclic ngr tumor neovasculature-homing motif sequence to human plasminogen kringle 5 improves inhibition of tumor growth. PLoS One 7: e37132.
14. Perri SR, Nalbantoglu J, Annabi B, Koty Z, Lejeune L, et al. (2005) Plasminogen kringle 5-engineered glioma cells block migration of tumor-associated macrophages and suppress tumor vascularization and progression. Cancer Res 65: 8359-8365.
15. Ji WR, Barrientos LG, Llinas M, Gray H, Villarreal X, et al. (1998) Selective inhibition by kringle 5 of human plasminogen on endothelial cell migration, an important process in angiogenesis. Biochem Biophys Res Commun 247: 414-419.
16. Perri SR, Martineau D, Francois M, Lejeune L, Bisson L, et al. (2007) Plasminogen kringle 5 blocks tumor progression by antiangiogenic and proinflammatory pathways. Mol Cancer Ther 6: 441-449.
17. Chang Q, Qin R, Huang T, Gao J, Feng Y, (2006) Effect of antisense hypoxia-inducible factor 1alpha on progression, metastasis, and chemosensitivity of pancreatic cancer. Pancreas 32: 297-305.
18. de Nigris F, Crudele V, Giovane A, Casamassimi A, Giordano A, et al. (2010) Cxcr4/yy1 inhibition impairs vegf network and angiogenesis during malignancy. Proc Natl Acad Sci U S A 107: 14484-14489.
19. Ottaiano A, Franco R, Aiello Talamanca A, Liguori G, Tatangelo F, et al. (2006) Overexpression of both cxc chemokine receptor 4 and vascular endothelial growth factor proteins predicts early distant relapse in stage ii-iii colorectal cancer patients. Clin Cancer Res 12: 2795-2803.
20. Phillips RJ, Mestas J, Gharaee-Kermani M, Burdick MD, Sica A, et al. (2005) Epidermal growth factor and hypoxia-induced expression of cxc chemokine receptor 4 on non-small cell lung cancer cells is regulated by the phosphatidylinositol 3-kinase/pten/akt/mammalian target of rapamycin signaling pathway and activation of hypoxia inducible factor-1alpha. J Biol Chem 280: 22473-22481.
21. Ziel KA, Campbell CC, Wilson GL, Gillespie MN, (2004) Ref-1/ape is critical for formation of the hypoxia-inducible transcriptional complex on the hypoxic response element of the rat pulmonary artery endothelial cell vegf gene. FASEB J 18: 986-988.
22. Gao G, Li Y, Gee S, Dudley A, Fant J, et al. (2002) Down-regulation of vascular endothelial growth factor and up-regulation of pigment epithelium-derived factor: A possible mechanism for the anti-angiogenic activity of plasminogen kringle 5. J Biol Chem 277: 9492-9497.
23. O'Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, et al. (1994) Angiostatin: A novel angiogenesis inhibitor that mediates the suppression of metastases by a lewis lung carcinoma. Cell 79: 315-328.
24. Weidner N, Semple JP, Welch WR, Folkman J, (1991) Tumor angiogenesis and metastasis-correlation in invasive breast carcinoma. N Engl J Med 324: 1-8.
25. Gao G, Li Y, Fant J, Crosson CE, Becerra SP, et al. (2002) Difference in ischemic regulation of vascular endothelial growth factor and pigment epithelium-derived factor in brown norway and sprague dawley rats contributing to different susceptibilities to retinal neovascularization. Diabetes 51: 1218-1225.
26. Zhu B, Lu L, Cai W, Yang X, Li C, et al. (2007) Kallikrein-binding protein inhibits growth of gastric carcinoma by reducing vascular endothelial growth factor production and angiogenesis. Mol Cancer Ther 6: 3297-3306.
27. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, et al. (2005) Vegfr1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438: 820-827.
28. Muller A, Homey B, Soto H, Ge N, Catron D, et al. (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410: 50-56.
29. Jin GH, Ma DY, Wu N, Marikar FM, Jin SZ, et al. (2007) Combination of human plasminogen kringle 5 with ionizing radiation significantly enhances the efficacy of antitumor effect. Int J Cancer 121: 2539-2546.
30. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, et al. (1989) Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246: 1306-1309.
31. Gonzalez-Gronow M, Kalfa T, Johnson CE, Gawdi G, Pizzo SV, (2003) The voltage-dependent anion channel is a receptor for plasminogen kringle 5 on human endothelial cells. J Biol Chem 278: 27312-27318.
32. Davidson DJ, Haskell C, Majest S, Kherzai A, Egan DA, et al. (2005) Kringle 5 of human plasminogen induces apoptosis of endothelial and tumor cells through surface-expressed glucose-regulated protein 78. Cancer Res 65: 4663-4672.
33. McFarland BC, Stewart J Jr, Hamza A, Nordal R, et al. (2009) Plasminogen kringle 5 induces apoptosis of brain microvessel endothelial cells: Sensitization by radiation and requirement for grp78 and lrp1. Cancer Res 69: 5537-5545.
34. Burns JM, Summers BC, Wang Y, Melikian A, Berahovich R, et al. (2006) A novel chemokine receptor for sdf-1 and i-tac involved in cell survival, cell adhesion, and tumor development. J Exp Med 203: 2201-2213.
35. Reddy K, Zhou Z, Jia SF, Lee TH, Morales-Arias J, et al. (2008) Stromal cell-derived factor-1 stimulates vasculogenesis and enhances ewing's sarcoma tumor growth in the absence of vascular endothelial growth factor. Int J Cancer 123: 831-837.
36. Guleng B, Tateishi K, Ohta M, Kanai F, Jazag A, et al. (2005) Blockade of the stromal cell-derived factor-1/cxcr4 axis attenuates in vivo tumor growth by inhibiting angiogenesis in a vascular endothelial growth factor-independent manner. Cancer Res 65: 5864-5871.
37. Liang Z, Brooks J, Willard M, Liang K, Yoon Y, et al. (2007) Cxcr4/cxcl12 axis promotes vegf-mediated tumor angiogenesis through akt signaling pathway. Biochem Biophys Res Commun 359: 716-722.
38. Wang J, Loberg R, Taichman RS, (2006) The pivotal role of cxcl12 (sdf-1)/cxcr4 axis in bone metastasis. Cancer Metastasis Rev 25: 573-587.
39. Hockel M, Vaupel P, (2001) Tumor hypoxia: Definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst 93: 266-276.
40. Staller P, Sulitkova J, Lisztwan J, Moch H, Oakeley EJ, et al. (2003) Chemokine receptor cxcr4 downregulated by von hippel-lindau tumour suppressor pvhl. Nature 425: 307-311.
41. Melillo G, (2006) Inhibiting hypoxia-inducible factor 1 for cancer therapy. Mol Cancer Res 4: 601-605.
42. Nordgren IK, Tavassoli A, (2011) Targeting tumour angiogenesis with small molecule inhibitors of hypoxia inducible factor. Chem Soc Rev 40: 4307-4317.
43. Shin J, Lee HJ, Jung DB, Jung JH, Lee EO, et al. (2011) Suppression of stat3 and hif-1 alpha mediates anti-angiogenic activity of betulinic acid in hypoxic pc-3 prostate cancer cells. PLoS One (6):: e21492.
44. Salceda S, Caro J, (1997) Hypoxia-inducible factor 1alpha (hif-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J Biol Chem 272: 22642-22647.
45. Chilov D, Camenisch G, Kvietikova I, Ziegler U, Gassmann M, et al. (1999) Induction and nuclear translocation of hypoxia-inducible factor-1 (hif-1): Heterodimerization with arnt is not necessary for nuclear accumulation of hif-1alpha. J Cell Sci 112 (Pt 8): 1203-1212.
46. Rohwer N, Lobitz S, Daskalow K, Jons T, Vieth M, et al. (2009) Hif-1alpha determines the metastatic potential of gastric cancer cells. Br J Cancer 100: 772-781.
47. Cheng ZX, Sun B, Wang SJ, Gao Y, Zhang YM, et al. (2011) Nuclear factor-kappab-dependent epithelial to mesenchymal transition induced by hif-1alpha activation in pancreatic cancer cells under hypoxic conditions. PLoS One 6: e23752.