Molecular characterization of EG-VEGF-mediated angiogenesis: Differential effects on microvascular and macrovascular endothelial cells

Molecular Biology of the Cell

Volumn 21, Issue 16, 2010, Pages 2832-2843

  Brouillet, Sophie ^a,b,c   Hoffmann, Pascale ^a,b,c,d   Benharouga, Mohamed ^b,c,e   Salomon, Aude ^a,b,c   Schaal, Jean Patrick ^d   Feige, Jean Jacques ^a,b,c   Alfaidy, Nadia ^a,b,c  

^a INSERM   (France)

^b CEA GRENOBLE   (France)

^c UNIV GRENOBLE ALPES   (France)

^d GRENOBLE UNIVERSITY HOSPITAL   (France)

^e CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOCRINE GLAND DERIVED VASCULAR ENDOTHELIAL GROWTH FACTOR; NEUTRALIZING ANTIBODY; PROKINETICIN RECEPTOR 1; PROKINETICIN RECEPTOR 2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANGIOGENESIS; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PERMEABILIZATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSPORT; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN PLACENTAL MICROVASCULAR ENDOTHELIAL CELL; HUMAN TISSUE; HUMAN UMBILICAL VEIN MACROVASCULAR ENDOTHELIAL CELL; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

EID: 77955631554     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-01-0059     Document Type: Article

References (42)

1. Burton, G. J., and Jauniaux, E. (1995). Sonographic, stereological and Doppler flow velocimetric assessments of placental maturity. Br. J. Obstet. Gynaecol. 102, 818-825.
2. Charnock-Jones, D. S., and Burton, G. J. (2000). Placental vascular morphogenesis. Baillieres Best Pract. Res. Clin. Obstet. Gynaecol. 14, 953-968.
3. Charnock-Jones, D. S., Kaufmann, P., and Mayhew, T. M. (2004). Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular regulation. Placenta 25, 103-113.
4. Chen, J., Kuei, C., Sutton, S., Wilson, S., Yu, J., Kamme, F., Mazur, C., Lovenberg, T., and Liu, C. (2005). Identification and pharmacological characterization of prokineticin 2 beta as a selective ligand for prokineticin receptor 1. Mol. Pharmacol. 67, 2070-2076.
5. Dellian, M., Witwer, B. P., Salehi, H. A., Yuan, F., and Jain, R. K. (1996). Quantitation and physiological characterization of angiogenic vessels in mice: effect of basic fibroblast growth factor, vascular endothelial growth factor/vascular permeability factor, and host microenvironment. Am. J. Pathol. 149, 59-71.
6. Demir, R., Kayisli, U. A., Seval, Y., Celik-Ozenci, C., Korgun, E. T., Demir-Weusten, A. Y., and Huppertz, B. (2004). Sequential expression of VEGF and its receptors in human placental villi during very early pregnancy: differences between placental vasculogenesis and angiogenesis. Placenta 25, 560-572. (Pubitemid 38701900)
7. Demir, R., Seval, Y., and Huppertz, B. (2007). Vasculogenesis and angiogenesis in the early human placenta. Acta Histochem. 109, 257-265. (Pubitemid 46962081)
8. Denison, F. C., Battersby, S., King, A. E., Szuber, M., and Jabbour, H. N. (2008). Prokineticin-1, a novel mediator of the inflammatory response in third-trimester human placenta. Endocrinology 149, 3470-3477. (Pubitemid 351919616)
9. Gallery, E. D., Rowe, J., Schrieber, L., and Jackson, C. J. (1991). Isolation and purification of microvascular endothelium from human decidual tissue in the late phase of pregnancy. Am. J. Obstet. Gynecol. 165, 191-196.
10. Guilini, C., Urayama, K., Turkeri, G., Dedeoglu, D. B., Kurose, H., Messaddeq, N., and Nebigil, C. G. (2010). Divergent roles of prokineticin receptors in the endothelial cells: angiogenesis and fenestration. Am. J. Physiol. Heart Circ. Physiol. 298, H844-H852.
11. Hebert, C. A., Luscinskas, F. W., Kiely, J. M., Luis, E. A., Darbonne, W. C., Bennett, G. L., Liu, C. C., Obin, M. S., Gimbrone, M. A., Jr., and Baker, J. B. (1990). Endothelial and leukocyte forms of IL-8. Conversion by thrombin and interactions with neutrophils. J. Immunol. 145, 3033-3040.
12. Hoffmann, P., Feige, J. J., and Alfaidy, N. (2006). Expression and oxygen regulation of endocrine gland-derived vascular endothelial growth factor/prokineticin-1 and its receptors in human placenta during early pregnancy. Endocrinology 147, 1675-1684.
13. Hoffmann, P., Feige, J. J., and Alfaidy, N. (2007). Placental expression of EG-VEGF and its receptors PKR1 (prokineticin receptor-1) and PKR2 throughout mouse gestation. Placenta 28, 1049-1058. (Pubitemid 47370899)
14. Hoffmann, P., Saoudi, Y., Benharouga, M., Graham, C. H., Schaal, J. P., Mazouni, C., Feige, J. J., and Alfaidy, N. (2009). Role of EG-VEGF in human placentation: physiological and pathological implications. J. Cell Mol. Med. 13, 2224-2235.
15. Jinga, V. V., Gafencu, A., Antohe, F., Constantinescu, E., Heltianu, C., Raicu, M., Manolescu, I., Hunziker, W., and Simionescu, M. (2000). Establishment of a pure vascular endothelial cell line from human placenta. Placenta 21, 325-336.
16. Kisliouk, T., Levy, N., Hurwitz, A., and Meidan, R. (2003). Presence and regulation of endocrine gland vascular endothelial growth factor/prokineticin-1 and its receptors in ovarian cells. J. Clin. Endocrinol. Metab. 88, 3700-3707.
17. Lang, I., Hoffmann, C., Olip, H., Pabst, M. A., Hahn, T., Dohr, G., and Desoye, G. (2001). Differential mitogenic responses of human macrovascular and microvascular endothelial cells to cytokines underline their phenotypic heterogeneity. Cell Prolif. 34, 143-155. (Pubitemid 32523216)
18. Lang, I., Pabst, M. A., Hiden, U., Blaschitz, A., Dohr, G., Hahn, T., and Desoye, G. (2003). Heterogeneity of microvascular endothelial cells isolated from human term placenta and macrovascular umbilical vein endothelial cells. Eur. J. Cell Biol. 82, 163-173.
19. Leach, L., Babawale, M. O., Anderson, M., and Lammiman, M. (2002). Vasculogenesis, angiogenesis and the molecular organisation of endothelial junctions in the early human placenta. J. Vasc. Res. 39, 246-259.
20. LeCouter, J., et al. (2001). Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 412, 877-884.
21. Lin, D. C., Bullock, C. M., Ehlert, F. J., Chen, J. L., Tian, H., and Zhou, Q. Y. (2002a). Identification and molecular characterization of two closely related G protein-coupled receptors activated by prokineticins/endocrine gland vascular endothelial growth factor. J. Biol. Chem. 277, 19276-19280.
22. Lin, R., LeCouter, J., Kowalski, J., and Ferrara, N. (2002b). Characterization of endocrine gland-derived vascular endothelial growth factor signaling in adrenal cortex capillary endothelial cells. J. Biol. Chem. 277, 8724-8729.
23. Maldonado-Perez, D., Evans, J., Denison, F., Millar, R. P., and Jabbour, H. N. (2007). Potential roles of the prokineticins in reproduction. Trends Endocrinol. Metab. 18, 66-72.
24. Masri, B., Morin, N., Pedebernade, L., Knibiehler, B., and Audigier, Y. (2006). The apelin receptor is coupled to Gi1 or Gi2 protein and is differentially desensitized by apelin fragments. J. Biol. Chem. 281, 18317-18326.
25. Massotte, D., Brillet, K., Kieffer, B., and Milligan, G. (2002). Agonists activate Gi1 alpha or Gi2 alpha fused to the human mu opioid receptor differently. J. Neurochem. 81, 1372-1382.
26. Metz, J., Heinrich, D., and Forssmann, W. G. (1976). Gap junctions in hemodichorial and hemotrichorial placentae. Cell Tissue Res. 171, 305-315.
27. Murray, J. D. (2003). On the mechanochemical theory of biological pattern formation with application to vasculogenesis. CR Biol. 326, 239-252.
28. Murthi, P., So, M., Gude, N. M., Doherty, V. L., Brennecke, S. P., and Kalionis, B. (2007). Homeobox genes are differentially expressed in macrovascular human umbilical vein endothelial cells and microvascular placental endothelial cells. Placenta 28, 219-223.
29. Neufeld, G., Cohen, T., Gengrinovitch, S., and Poltorak, Z. (1999). Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13, 9-22. (Pubitemid 29038270)
30. Ngan, E. S., Shum, C. K., Poon, H. C., Sham, M. H., Garcia-Barcelo, M. M., Lui, V. C., and Tam, P. K. (2008). Prokineticin-1 (Prok-1) works coordinately with glial cell line-derived neurotrophic factor (GDNF) to mediate proliferation and differentiation of enteric neural crest cells. Biochim. Biophys. Acta 1783, 467-478.
31. Palade, G. E., Simionescu, M., and Simionescu, N. (1979). Structural aspects of the permeability of the microvascular endothelium. Acta Physiol. Scand. Suppl. 463, 11-32.
32. Rabiet, M. J., Plantier, J. L., Rival, Y., Genoux, Y., Lampugnani, M. G., and Dejana, E. (1996). Thrombin-induced increase in endothelial permeability is associated with changes in cell-to-cell junction organization. Arterioscler. Thromb. Vasc. Biol. 16, 488-496.
33. Risau, W. (1997). Mechanisms of angiogenesis. Nature 386, 671-674.
34. Roberts, W. G., Delaat, J., Nagane, M., Huang, S., Cavenee, W. K., and Palade, G. E. (1998). Host microvasculature influence on tumor vascular morphology and endothelial gene expression. Am. J. Pathol. 153, 1239-1248.
35. Rodgers, G. M. (1988). Hemostatic properties of normal and perturbed vascular cells. FASEB J. 2, 116-123.
36. Sibai, B., Dekker, G., and Kupferminc, M. (2005). Pre-eclampsia. Lancet 365, 785-799.
37. Slessareva, J. E., Ma, H., Depree, K. M., Flood, L. A., Bae, H., Cabrera-Vera, T. M., Hamm, H. E., and Graber, S. G. (2003). Closely related G-protein-coupled receptors use multiple and distinct domains on G-protein alpha-subunits for selective coupling. J. Biol. Chem. 278, 50530-50536.
38. Stewart, P. A., and Wiley, M. J. (1981). Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras. Dev. Biol. 84, 183-192.
39. te Velde, E. A., Exalto, N., Hesseling, P., and van der Linden, H. C. (1997). First trimester development of human chorionic villous vascularization studied with CD34 immunohistochemistry. Hum. Reprod. 12, 1577-1581.
40. Urayama, K., Dedeoglu, D. B., Guilini, C., Frantz, S., Ertl, G., Messaddeq, N., and Nebigil, C. G. (2009). Transgenic myocardial overexpression of prokineticin receptor-2 (GPR73b) induces hypertrophy and capillary vessel leakage. Cardiovasc. Res. 81, 28-37.
41. Urayama, K., Guilini, C., Turkeri, G., Takir, S., Kurose, H., Messaddeq, N., Dierich, A., and Nebigil, C. G. (2008). Prokineticin receptor-1 induces neovascularization and epicardial-derived progenitor cell differentiation. Arterioscler. Thromb. Vasc. Biol. 28, 841-849.
42. Voyta, J. C., Via, D. P., Butterfield, C. E., and Zetter, B. R. (1984). Identification and isolation of endothelial cells based on their increased uptake of acetylated-low density lipoprotein. J. Cell Biol. 99, 2034-2040.