EMMPRIN promotes angiogenesis through hypoxia-inducible factor-2α-mediated regulation of soluble VEGF isoforms and their receptor VEGFR-2

Blood

Volumn 114, Issue 27, 2009, Pages 5547-5556

  Bougatef, Faten ^a,b,c   Quemener, Cathy ^a,b,c   Kellouche, Sabrina ^a,b   Naïmi, Benyoussef ^a,d   Podgorniak, Marie Pierre ^a,b,c   Millot, Guy ^a,b   Gabison, Eric E ^d,e   Calvo, Fabien ^a,b,c   Dosquet, Christine ^a,b   Lebbé, Céleste ^a,b,c   Menashi, Suzanne ^d,e   Mourah, Samia ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DIDEROT   (France)

^c SAINT LOUIS HOSPITAL   (France)

^d UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^e CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD147 ANTIGEN; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MATRIX METALLOPROTEINASE; PROTEINASE; UNCLASSIFIED DRUG; UROKINASE RECEPTOR; VASCULOTROPIN; VASCULOTROPIN 121; VASCULOTROPIN 165; VASCULOTROPIN 189; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN CONTAINING PROTEIN 1; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; ISOPROTEIN; VASCULOTROPIN A;

ANGIOGENESIS; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; STROMA; XERORADIOGRAPHY; ANIMAL; CELL CULTURE; CELL LINE; CELL MOTION; CHO CELL; CRICETULUS; CYTOLOGY; DRUG EFFECT; EXPERIMENTAL NEOPLASM; GENETICS; HAMSTER; IMMUNOBLOTTING; METABOLISM; MOUSE; NUDE MOUSE; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SOLUBILITY; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD147; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; ENDOTHELIAL CELLS; HUMANS; IMMUNOBLOTTING; MICE; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN ISOFORMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SOLUBILITY; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 76249112702     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-04-217380     Document Type: Article

References (50)

1. Folkman J, Shing Y. Angiogenesis. J Biol Chem. 1992;267:10931-10934.
2. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 2000; 407:242-248.
3. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. 2004;25:581-611.
4. Takahashi Y, Kitadai Y, Bucana CD, Cleary KR, Ellis LM. Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res. 1995;55:3964-3968.
5. Inoue K, Ozeki Y, Suganuma T, Sugiura Y, Tanaka S. Vascular endothelial growth factor expression in primary esophageal squamous cell carcinoma: association with angiogenesis and tumor progression. Cancer. 1997;79:206-213.
6. Maeda K, Chung YS, Ogawa Y, et al. Prognostic value of vascular endothelial growth factor expression in gastric carcinoma. Cancer. 1996;77: 858-863.
7. Kim KJ, Li B, Winer J, et al. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumor growth in vivo. Nature. 1993; 362:841-844.
8. Oku T, Tjuvajev JG, Miyagawa T, et al. Tumor growth modulation by sense and antisense vascular endothelial growth factor gene expression: effects on angiogenesis, vascular permeability, blood volume, blood flow, fluorodeoxyglucose uptake, and proliferation of human melanoma intracerebral xenografts. Cancer Res. 1998;58: 4185-4192.
9. Robinson CJ, Stringer SE. The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J Cell Sci. 2001;114:853-865.
10. Wellmann S, Taube T, Paal K, et al. Specific reverse transcription-PCR quantification of vascular endothelial growth factor (VEGF) splice variants by LightCycler technology. Clin Chem. 2001;47: 654-660.
11. Park JE, Keller GA, Ferrara N. The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol Biol Cell. 1993;4:1317-1326.
12. Mustonen T, Alitalo K. Endothelial receptor tyrosine kinases involved in angiogenesis. J Cell Biol. 1995;129:895-898.
13. Millauer B, Wizigmann-Voos S, Schnurch H, et al. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell. 1993;72: 835-846.
14. Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol. 2005;23:1011-1027.
15. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9:669-676.
16. Shibuya M. Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J Biochem Mol Biol. 2006;39:469-478.
17. Shibuya M, Claesson-Welsh L. Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp Cell Res. 2006; 312:549-560.
18. Shibuya M. Vascular endothelial growth factor receptor-1 (VEGFR-1/Flt-1): a dual regulator for angiogenesis. Angiogenesis. 2006;9:225-230, discussion 231.
19. Maharaj AS, Saint-Geniez M, Maldonado AE, D'Amore PA. Vascular endothelial growth factor localization in the adult. Am J Pathol. 2006;168: 639-648.
20. Lee S, Chen TT, Barber CL, et al. Autocrine VEGF signaling is required for vascular homeostasis. Cell. 2007;130:691-703.
21. Biswas C, Zhang Y, DeCastro R, et al. The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res. 1995; 55:434-439.
22. Toole BP. Emmprin (CD147), a cell surface regulator of matrix metalloproteinase production and function. Curr Top Dev Biol. 2003;54:371-389.
23. Polette M, Gilles C, Marchand V, et al. Tumor collagenase stimulatory factor (TCSF) expression and localization in human lung and breast cancers. J Histochem Cytochem. 1997;45:703-709.
24. Quemener C, Gabison EE, Naimi B, et al. Extracellular matrix metalloproteinase inducer up-regulates the urokinase-type plasminogen activator system promoting tumor cell invasion. Cancer Res. 2007;67:9-15.
25. Kanekura T, Chen X, Kanzaki T. Basigin (CD147) is expressed on melanoma cells and induces tumor cell invasion by stimulating production of matrix metalloproteinases by fibroblasts. Int J Cancer. 2002;99:520-528.
26. Reimers N, Zafrakas K, Assmann V, et al. Expression of extracellular matrix metalloproteases inducer on micrometastatic and primary mammary carcinoma cells. Clin Cancer Res. 2004;10:3422-3428.
27. Rosenthal EL, Shreenivas S, Peters GE, Grizzle WE, Desmond R, Gladson CL. Expression of extracellular matrix metalloprotease inducer in laryngeal squamous cell carcinoma. Laryngoscope. 2003;113:1406-1410.
28. Davidson B, Goldberg I, Berner A, Kristensen GB, Reich R. EMMPRIN (extracellular matrix metalloproteinase inducer) is a novel marker of poor outcome in serous ovarian carcinoma. Clin Exp Metastasis. 2003;20:161-169.
29. Ishibashi Y, Matsumoto T, Niwa M, et al. CD147 and matrix metalloproteinase-2 protein expression as significant prognostic factors in esophageal squamous cell carcinoma. Cancer. 2004; 101:1994-2000.
30. Zucker S, Hymowitz M, Rollo EE, et al. Tumorigenic potential of extracellular matrix metalloproteinase inducer. Am J Pathol. 2001;158:1921-1928.
31. Tang Y, Nakada MT, Kesavan P, et al. Extracellular matrix metalloproteinase inducer stimulates tumor angiogenesis by elevating vascular endothelial cell growth factor and matrix metalloproteinases. Cancer Res. 2005;65:3193-3199.
32. Gabison EE, Mourah S, Steinfels E, et al. Differential expression of extracellular matrix metalloproteinase inducer (CD147) in normal and ulcerated corneas: role in epithelio-stromal interactions and matrix metalloproteinase induction. Am J Pathol. 2005;166:209-219.
33. Dardik R, Solomon A, Loscalzo J, et al. Novel proangiogenic effect of factor XIII associated with suppression of thrombospondin 1 expression. Arterioscler Thromb Vasc Biol. 2003;23:1472-1477.
34. Sounni NE, Roghi C, Chabottaux V, et al. Up-regulation of vascular endothelial growth factor-A by active membrane-type 1 matrix metalloproteinase through activation of Src-tyrosine kinases. J Biol Chem. 2004;279:13564-13574.
35. Caudroy S, Polette M, Nawrocki-Raby B, et al. EMMPRIN-mediated MMP regulation in tumor and endothelial cells. Clin Exp Metastasis. 2002; 19:697-702.
36. Lee S, Jilani SM, Nikolova GV, Carpizo D, Iruela-Arispe ML. Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J Cell Biol. 2005;169: 681-691.
37. Plouet J, Moro F, Bertagnolli S, et al. Extracellular cleavage of the vascular endothelial growth factor 189-amino acid form by urokinase is required for its mitogenic effect. J Biol Chem. 1997;272: 13390-13396.
38. Tang Y, Nakada MT, Rafferty P, et al. Regulation of vascular endothelial growth factor expression by EMMPRIN via the PI3K-Akt signaling pathway. Mol Cancer Res. 2006;4:371-377.
39. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling: in control of vascular function. Nat Rev Mol Cell Biol. 2006;7:359-371.
40. Sounni NE, Devy L, Hajitou A, et al. MT1-MMP expression promotes tumor growth and angiogenesis through an up-regulation of vascular endothelial growth factor expression. FASEB J. 2002;16:555-564.
41. Sameshima T, Nabeshima K, Toole BP, et al. Glioma cell extracellular matrix metalloproteinase inducer (EMMPRIN) (CD147) stimulates production of membrane-type matrix metalloproteinases and activated gelatinase A in co-cultures with brain-derived fibroblasts. Cancer Lett. 2000;157: 177-184.
42. Sun J, Hemler ME. Regulation of MMP-1 and MMP-2 production through CD147/extracellular matrix metalloproteinase inducer interactions. Cancer Res. 2001;61:2276-2281.
43. Bates DO, Cui TG, Doughty JM, et al. VEGF165b, an inhibitory splice variant of vascular endothelial growth factor, is down-regulated in renal cell carcinoma. Cancer Res. 2002;62:4123-4131.
44. Cohen CD, Doran PP, Blattner SM, et al. Sam68-like mammalian protein 2, identified by digital differential display as expressed by podocytes, is induced in proteinuria and involved in splice site selection of vascular endothelial growth factor. J Am Soc Nephrol. 2005;16:1958-1965.
45. Dowhan DH, Hong EP, Auboeuf D, et al. Steroid hormone receptor coactivation and alternative RNA splicing by U2AF65-related proteins CAPERalpha and CAPERbeta. Mol Cell. 2005; 17:429-439.
46. Gordan JD, Simon MC. Hypoxia-inducible factors: central regulators of the tumor phenotype. Curr Opin Genet Dev. 2007;17:71-77.
47. Elvert G, Kappel A, Heidenreich R, et al. Cooperative interaction of hypoxia-inducible factor-2alpha (HIF-2alpha) and Ets-1 in the transcriptional activation of vascular endothelial growth factor receptor-2 (Flk-1). J Biol Chem. 2003;278: 7520-7530.
48. Lofstedt T, Fredlund E, Holmquist-Mengelbier L, et al. Hypoxia inducible factor-2alpha in cancer. Cell Cycle. 2007;6:919-926.
49. Carroll VA, Ashcroft M. Role of hypoxia-inducible factor (HIF)-1alpha versus HIF-2alpha in the regulation of HIF target genes in response to hypoxia, insulin-like growth factor-I, or loss of von Hippel-Lindau function: implications for targeting the HIF pathway. Cancer Res. 2006;66:6264-6270.
50. Petrella BL, Lohi J, Brinckerhoff CE. Identification of membrane type-1 matrix metalloproteinase as a target of hypoxia-inducible factor-2alpha in von Hippel-Lindau renal cell carcinoma. Oncogene. 2005;24:1043-1052.