Reduced tumor growth and angiogenesis in endoglin-haploinsufficient mice

Tumor Biology

Volumn 28, Issue 1, 2007, Pages 1-8

  Düwel, Annette ^a   Eleno, Nélida ^a   Jerkic, Mirjana ^a   Arevalo, Miguel ^a   Bolaños, Juan P ^a   Bernabeu, Carmelo ^b   López Novoa, Jose M ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Angiogenesis; Endoglin; Endothelial nitric oxide synthase; Hypoxia inducible factor; Mice; Tumorigenesis; Vascular endothelial growth factor

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CD31 ANTIGEN; ENDOGLIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEMOGLOBIN; HYPOXIA INDUCIBLE FACTOR 1; OXYGEN; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY DENSITY; CARCINOGENESIS; CARCINOMA CELL; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HAPLOTYPE; HETEROZYGOTE; IMMUNOHISTOCHEMISTRY; LASER DOPPLER FLOWMETRY; LEWIS CARCINOMA; MALE; MOUSE; NONHUMAN; PERFUSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR GROWTH; TUMOR VASCULARIZATION; TUMOR VOLUME; VASCULAR TUMOR; WESTERN BLOTTING;

EID: 33845752037     PISSN: 10104283     EISSN: None     Source Type: Journal    
DOI: 10.1159/000097040     Document Type: Article

References (41)

1. Carmeliet P, Collen D: Transgenic mouse models in angiogenesis and cardiovascular disease. J Pathol 2000;190:387-405.
2. Gougos A, Letarte M: Identification of human endothelial cell antigen with monoclonal antibody 44G4 produced against a pre-B leukemic cell line. J Immunol 1988;141:1925-1933.
3. Lastres P, Letamendia A, Zhang H, Rius C, Almendro N, Raab U, López LA, Langa C, Fabra A, Letarte M, Bernabéu C: Endoglin modulates cellular responses to TGF-beta 1. J Cell Biol 1996;133:1109-1121.
4. Pece-Barbara N, Wrana JL, Letarte M: Endoglin is an accessory protein that interacts with the signalling receptor complex of multiple members of the transforming growth factor-beta superfamily. J Biol Chem 1999;274:584-594.
5. Diez-Marques L, Ortega-Velazquez R, Langa C, Rodriguez-Barbero A, Lopez-Novoa JM, Lamas S, Bernabeu C: Expression of endoglin in human mesangial cells: modulation of extracellular matrix synthesis. Biochim Biophys Acta 2002;1587:36-44.
6. McAllister KA, Grogg KM, Johnson DW, Gallione CJ, Baldwin MA, Jackson CE, Helmbold EA, Markel DS, McKinnon WC, Murrell J, McCormick MK, Pericak-Vance MA, et al: Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet 1994;8:345-351.
7. Fonsatti E, Altomonte M, Nicotra MR, Natali PG, Maio M: Endoglin (CD105): a powerful therapeutic target on tumor-associated angiogenetic blood vessels. Oncogene 2003;22:6557-6563.
8. Burrows FJ, Derbyshire EJ, Tazzari PL, Amlot P, Gazdar AF, King SW, Letarte M, Vitetta ES, Thorpe PE: Up-regulation of endoglin on vascular endothelial cells in human solid tumors: implications for diagnosis and therapy. Clin Cancer Res 1995;1:1623-1634.
9. Wang JM, Kumar S, Pye D, van Agthoven AJ, Krupinski J, Hunter RD: A monoclonal antibody detects heterogeneity in vascular endothelium of tumors and normal tissues. Int J Cancer 1993;54:363-370.
10. Duff SE, Li C, Garland JM, Kumar S: CD105 is important for angiogenesis: evidence and potential applications. FASEB J 2003;17:984-992.
11. Quintanilla M, Ramirez JR, Perez-Gomez E, Romero D, Velasco B, Letarte M, Lopez-Novoa JM, Bernabeu C: Expression of the TGF-beta coreceptor endoglin in epidermal keratinocytes and its dual role in multistage mouse skin carcinogenesis. Oncogene 2003;22:5976-5985.
12. Jerkic M, Rodríguez-Barbero A, Prieto M, Toporsian M, Pericacho M, Rivas-Elena JV, Obreo J, Chan A, Pérez-Barriocanal F, Arévalo M, Bernabéu C, Letarte M, López-Novoa JM: Reduced angiogenic responses in adult endoglin heterozygous mice. Cardiovasc Res 2006;69:845-854.
13. Bourdeau A, Dumont DJ, Letarte M: A murine model of hereditary hemorrhagic telangiectasia. J Clin Invest 1999;104:1343-1351.
14. Rodriguez-Peña A, Eleno N, Duwell A, Arevalo M, Perez-Barriocanal F, Flores O, Docherty N, Bernabeu C, Letarte M, Lopez-Novoa JM: Endoglin upregulation during experimental renal interstitial fibrosis in mice. Hypertension 2002;40:713-720.
15. Ge AZ, Butcher EC: Cloning and expression of a cDNA encoding mouse endoglin, an endothelial cell TGF-beta ligand. Gene 1994;138:201-206.
16. Jerkic M, Rivas-Elena JV, Prieto M, Carrón R, Sanz- Rodríguez F, Pérez-Barriocanal F, Rodriguez-Barbero A, Bernabeu C, Lopez-Novoa JM: Endoglin regulates nitric oxide-dependent vasodilatation. FASEB J 2004;18:609-611.
17. Toporsian M, Gros R, Kabir MG, Vera S, Govindaraju K, Eidelman DH, Husain M, Letarte M: Role for endoglin in coupling eNOS activity and regulating vascular tone revealed in hereditary hemorrhagic telangiectasia. Circ Res 2005;96:684-692.
18. Griffioen AW, Molema G: Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation. Pharmacol Rev 2000;52:237-268.
19. Carmeliet P, Jain RK: Angiogenesis in cancer and other diseases. Nature 2000;407:249-257.
20. Torsney E, Charlton R, Diamond AG, Burn J, Soames JV, Arthur HM: Mouse model for hereditary hemorrhagic telangiectasia has a generalized vascular abnormality. Circulation 2003;107:1653-1657.
21. Arthur HM, Ure J, Smith AJ, Renforth G, Wilson DI, Torsney E, Charlton R, Parums DV, Jowett T, Marchuk DA, Burn J, Diamond AG: Endoglin, an ancillary TGF-beta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev Biol 2000;217:42-53.
22. Li DY, Sorensen LK, Brooke BS, Urness LD, Davis EC, Taylor DG, Boak BB, Wendel DP: Defective angiogenesis in mice lacking endoglin. Science 1999;284:1534-1537.
23. Miller DW, Graulich W, Karges B, Stahl S, Ernst M, Ramaswamy A, Sedlacek HH, Müller R, Adamkiewicz J: Elevated expression of endoglin, a component of the TGF-β-receptor complex, correlates with proliferation of tumor endothelial cells. Int J Cancer 1999;81:568-572.
24. Wang JM, Kumar S, Pye D, Haboubi N, Al-Nakib L: Breast carcinoma: comparative study of tumor vasculature using two endothelial cell markers. J Natl Cancer Inst 1994;86:386-388.
25. Bodey B, Bodey B Jr, Siegel SE, Kaiser HE: Over-expression of endoglin (CD105): a marker of breast carcinoma-induced neovascularization. Anticancer Res 1998;18:3621-3628.
26. 2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 1999;15:551-578.
27. Shweiki D, Itin A, Soffer D, Keshet E: Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992;359:843-845.
28. Sanchez-Elsner T, Botella LM, Velasco B, Langa C, Bernabeu C: Endoglin expression is regulated by transcriptional cooperation between the hypoxia and transforming growth factor-beta pathways. J Biol Chem 2002;277:43799-43808.
29. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, Kearney M, Chen D, Symes JF, Fishman MC, Huang PL, Isner JM: Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 1998;101:2567-2578.
30. Lee PC, Salyapongse AN, Bragdon GA, Shears LL 2nd, Watkins SC, Edington HD, Billiar TR: Impaired wound healing and angiogenesis in eNOS-deficient mice. Am J Physiol 1999;277:H1600-H1608.
31. Amano K, Matsubara H, Iba O, Okigaki M, Fujiyama S, Imada T, Kojima H, Nozawa Y, Kawashima S, Yokoyama M, Iwasaka T: Enhancement of ischemia-induced angiogenesis by eNOS overexpression. Hypertension 2003;41:156-162.
32. Jadeski LC, Hum KO, Chakraborty C, Lala PK: Nitric oxide promotes murine mammary tumour growth and metastasis by stimulating tumour cell migration, invasiveness and angiogenesis. Int J Cancer 2000;86:30-39.
33. Letamendía A, Lastres P, Botella LM, Raab U, Langa C, Velasco B, Attisano L, Bernabeu C: Role of endoglin in cellular responses to transforming growth factor-R. J Biol Chem 1998;273:33011-33019.
34. Li C, Hampson IN, Hampson L, Kumar P, Bernabeu C, Kumar S: CD105 antagonizes the inhibitory signaling of transforming growth factor β1 on human vascular endothelial cells. FASEB J 2000;14:55-64.
35. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, ten Dijke P: Balancing the activation state of the endothelium via two distinct TGF-β type I receptors. EMBO J 2002;21:1743-1753.
36. Sun L, Vitolo MI, Qiao M, Anglin IE, Passaniti A: Regulation of TGFβ1-mediated growth inhibition and apoptosis by RUNX2 isoforms in endothelial cells. Oncogene 2004;23:4722-4734.
37. Li C, Issa R, Guo B, Kumar P, Lopez-Novoa JM, Bernabeu C, Kumar S: CD105 prevents apoptosis in hypoxic endothelial cells. J Cell Sci 2003;116:2677-2685.
38. She X, Matsuno F, Harada N, Tsai H, Seon BK: Synergy between anti-endoglin (CD105) monoclonal antibodies and TGF-beta in suppression of growth of human endothelial cells. Int J Cancer 2004;108:251-257.
39. Lebrin F, Goumans MJ, Jonker L, Carvalho RL, Valdimarsdottir G, Thorikay M, et al: Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J 2004;23:4018-4028.
40. Warrington K, Hillarby MC, Li C, Letarte M, Kumar S: Functional role of CD105 in TGF-β1 signalling in murine and human endothelial cells. Anticancer Res 2005;25:1851-1864.
41. Fonsatti E, Maio M: Highlights on endoglin (CD105): from basic findings towards clinical applications in human cancer. J Transl Med 2004;2:18.