Vascular endothelial growth factor C is increased in endometrium and promotes endothelial functions, vascular permeability and angiogenesis and growth of endometriosis

Angiogenesis

Volumn 16, Issue 3, 2013, Pages 541-551

  Xu, Hui ^a   Zhang, Tao ^a   Man, Gene Chi Wai ^a   May, Katie E ^b   Becker, Christian M ^b   Davis, Tina N ^c   Kung, Andrew L ^c   Birsner, Amy E ^c   D'Amato, Robert J ^c   Wong, Alice Wai Yee ^a   Wang, Chi Chiu ^a,d  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Angiogenesis; Endometriosis; Vascular endothelial growth factor; VEGF C

Indexed keywords

MESSENGER RNA; SMALL INTERFERING RNA; VASCULOTROPIN A; VASCULOTROPIN B; VASCULOTROPIN C; VASCULOTROPIN D;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL INVASION; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOMETRIOSIS; ENDOMETRIUM; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANALYSIS OF VARIANCE; ANIMALS; CAPILLARY PERMEABILITY; CELL MOVEMENT; ENDOMETRIOSIS; ENDOMETRIUM; ENDOTHELIAL CELLS; FEMALE; HUMANS; MICE; NEOVASCULARIZATION, PATHOLOGIC; RNA, MESSENGER; RNA, SMALL INTERFERING; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

MUS;

EID: 84879241523     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-013-9333-1     Document Type: Article

References (45)

1. Risau W (1997) Mechanisms of angiogenesis. Nature 386:671-674
2. Taylor RN, Lebovic DI, Mueller MD (2002) Angiogenic factors in endometriosis. Ann N Y Acad Sci 955:89-100
3. Nisolle M, Casanas-Roux F, Anaf V, Mine JM, Donnez J (1993) Morphometric study of the stromal vascularization in peritoneal endometriosis. Fertil Steril 59:681-684
4. Becker CM, Rohwer N, Funakoshi T, Cramer T, Bernhardt W, Birsner A, Folkman J, D'Amato RJ (2008) 2-methoxyestradiol inhibits hypoxia-inducible factor-1{alpha} and suppresses growth of lesions in a mouse model of endometriosis. Am J Pathol 172:534-544
5. Xu H, Lui WT, Chu CY, Ng PS, Wang CC, Rogers MS (2009) Anti-angiogenic effects of green tea catechin on an experimental endometriosis mouse model. Hum Reprod 24:608-618
6. Becker CM, Sampson DA, Short SM, Javaherian K, Folkman J, D'Amato RJ (2006) Short synthetic endostatin peptides inhibit endothelial migration in vitro and endometriosis in a mouse model. Fertil Steril 85:71-77
7. Groothuis PG, Nap AW, Winterhager E, Grümmer R (2005) Vascular development in endometriosis. Angiogenesis 8:147-156
8. Folkman J, Klagsbrun M (1987) Angiogenic factors. Science 235:442-447
9. Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473:298-307
10. Keck PJ, Hauser SD, Krivi G, Sanzo K, Warren T, Feder J, Connolly DT (1989) Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science 246:1309-1312
11. Ferrara N (2009) VEGF-A: a critical regulator of blood vessel growth. Eur Cytokine Netw 20:158-163
12. Nagy JA, Dvorak AM, Dvorak HF (2007) VEGF-A and the induction of pathological angiogenesis. Annu Rev Pathol 2:251-275
13. Veikkola T, Alitalo K (1999) VEGFs, receptors and angiogenesis. Sem Cancer Biol 9:211-220
14. Ferrara N (1999) Vascular endothelial growth factor: molecular and biological aspects. Curr Topics Microbiol Immunol 237:1-30
15. Donnez J, Smoes P, Gillerot S, Casanas-Roux F, Nisolle M (1998) Vascular endothelial growth factor (VEGF) in endometriosis. Hum Reprod 13:1686-1690
16. McLaren J (2000) Vascular endothelial growth factor and endometriotic angiogenesis. Hum Reprod Update 6:45-55
17. Hull ML, Charnock-Jones DS, Chan CL, Bruner-Tran KL, Osteen KG, Tom BD, Fan TP, Smith SK (2003) Antiangiogenic agents are effective inhibitors of endometriosis. J Clin Endocrinol Metab 88:2889-2899
18. Xu H, Becker CM, Lui WT, Chu CY, Davis TN, Kung AL, Birsner AE, D'Amato RJ, Wai Man GC, Wang CC (2011) Green tea epigallocatechin-3-gallate inhibits angiogenesis and suppresses vascular endothelial growth factor C/vascular endothelial growth factor receptor 2 expression and signaling in experimental endometriosis in vivo. Fertil Steril 96:1021-1028
19. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K (1996) A novel endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15:290-298
20. Lee J, Gray A, Yuan J, Luoh SM, Avraham H, Wood WI (1996) Vascular endothelial growth factor-related protein: a ligand and specific activator of the tyrosine kinase receptor Flt4. Proc Natl Acad Sci USA 93:1988-1992
21. Kukk E, Lymboussaki A, Taira S, Kaipainen A, Jeltsch M, Joukov V, Alitalo K (1996) VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development 122:3829-3837
22. American Society for Reproduction Medicine (1997) Revised American Society for Reproduction Medicine classification of endometriosis: 1996. Fertil Steril 67:817-821
23. Nap AW, Griffioen AW, Dunselman GAJ, Bouma-TerSteege JCA, Tijssen VJL, Evers JLH, Groothuis PG (2004) Antiangiogenesis therapy for endometriosis. J Clin Endocrinol Metab 89:1089-1095
24. Bruner-Tran KL, Osteen KG, Duleba AJ (2009) Simvastatin protects against the development of endometriosis in a nude mouse model. J Clin Endocrinol Metab 94:2489-2494
25. Becker CM, Sampson DA, Rupnick MA, Rohan RM, Efstathiou JA, Short SM, Taylor GA, Folkman J, D'Amato RJ (2005) Endostatin inhibits the growth of endometriotic lesions but does not affect fertility. Fertil Steril 84(Suppl 2):1144-1155
26. Ristimaki A, Narko K, Enholm B, Joukov V, Alitalo K (1998) Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C. J Biol Chem 273:8413-8418
27. Keichel S, Barcena de rellano ML, Reichelt U, Riedlinger WF, Schneider A, Köhler C, Mechsner S (2011) Lymphangiogenesis in deep infiltrating endometriosis. Hum Reprod 26:2713-2720
28. Jeltsch M, Kaipainen A, Joukov V, Meng X, Lakso M, Rauvala H, Swartz M, Fukumura D, Jain RK, Alitalo K (1997) Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science 276:1423-1425
29. Pepper MS, Mandriota SJ, Jeltsch M, Kumar V, Alitalo K (1998) Vascular endothelial growth factor (VEGF)-C synergizes with basic fibroblast growth factor and VEGF in the induction of angiogenesis in vitro and alters endothelial cell extracellular proteolytic activity. J Cell Physiol 177:439-452
30. Joukov V, Sorsa T, Kumar V, Jelisch M, Claesson-welsh L, Cao Y, Saksela O, Kalkkinen N, Alitalo K (1997) Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J 16:3898-3911
31. Adya R, Tan BK, Punn A, Chen J, Randeva HS (2008) Visfatin induces human endothelial VEGF and MMP-2/9 production via MAPK and PI3 K/Akt signalling pathways: novel insights into visfatin-induced angiogenesis. Cardiovasc Res 78:356-365
32. Li XF, Charnock-Jones DS, Zhang E, Hiby S, Malik S, Day K, Licence D, Bowen JM, Gardner L, King A, Loke YW, Smith SK (2001) Angiogenic growth factor messenger ribonucletic acids in uterine natural killer cells. J Clin Endocrinol Metab 86:1823-1834
33. Moller B, Lindblom B, Olovsson M (2002) Expression of the vascular endothelial growth factors B and C and their receptor in human endometrium during the menstrual cycle. Acta Obstet Gynecol Scand 81:817-824
34. Takehara M, Ueda M, Yamashita Y, Terai Y, Hung YC, Ueki M (2004) Vascular endothelial growth factor A and C gene expression in endometriosis. Hum Pathol 35:1369-1375
35. Reichelt U, Keichel S, Barcena de Arellano ML, Chiantera V, Schneider A, Mechsner S (2012) High lymph vessel density and expression of lymphatic growth factors in peritoneal endometriosis. Reprod Sci. doi: 10.1177/1933719112438440
36. Witzenbichler B, Asahara T, Murohara T, Silver M, Spyridopoulos I, Magner M, Principe N, Kearney M, Hu JS, Isner JM (1998) Vascular endothelial growth factor-C (VEGF-C/VEGF-2) promotes angiogenesis in the setting of tissue ischemia. Am J Pathol 153:381-394
37. Zeng Y, Opeskin K, Goad J, Williams ED (2006) Tumor-induced activation of lymphatic endothelial cells via vascular endothelial growth factor receptor-2 is critical for prostate cancer lymphatic metastasis. Cancer Res 66:9566-9575
38. Lin CI, Chen CN, Huang MT, Lee SJ, Lin CH, Chang CC, Lee H (2008) Lysophosphatidic acid up-regulates vascular endothelial growth factor-C and lymphatic marker expressions in human endothelial cells. Cell Mol Life Sci 65:2740-2751
39. Rice VM (2002) Conventional medical therapies for endometriosis. Ann N Y Acad Sci 955:343-352
40. Xu H, Wang CC (2010) Angiogenesis and Anti-angiogenesis Therapy of Endometriosis. In: Mitchell LA (ed) Endometriosis: symptoms, diagnosis and treatments. Nova Science, New York. Chapter 1, pp. 1-40
41. Dabrosin C, Gyorffy S, Margetts P, Ross C, Gauldie J (2002) Therapeutic effect of angiostatin gene transfer in a murine model of endometriosis. Am J Pathol 161:909-918
42. Yagyu T, Kobayashi H, Matsuzaki H, Wakahara K, Kondo T, Kurita N, Sekino H, Inagaki K, Suzuki M, Kanayama N, Terao T (2005) Thalidomide inhibits tumor necrosis factor-alpha-induced interleukin-8 expression in endometriotic stromal cells, possibly through suppression of nuclear factor-kappaB activation. J Clin Endocrinol Metab 90:3017-3021
43. Scarpellini F, Sbracia M, Lecchini S, Scarpellini L (2002) Anti-angiogenesis treatment with thalidomide in endometriosis: a pilot study. Fertil Steril 78:S87
44. Nyberg P, Xie L, Kalluri R (2005) Endogenous inhibitors of angiogenesis. Cancer Res 65:3967-3979
45. Klauber N, Rohan RM, Flynn E, D'Amato RJ (1997) Critical components of the female reproductive pathway are suppressed by the angiogenesis inhibitor AGM-1470. Nat Med 3:443-446