Regulation of soluble vascular endothelial growth factor receptor 1 secretion from human endothelial cells by tissue inhibitor of metalloproteinase 1

Molecular Human Reproduction

Volumn 15, Issue 11, 2009, Pages 749-756

  Bruegmann, E ^a   Gruemmer, R ^b   Neulen, J ^a   Motejlek, K ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

Endothelial cells; Granulosa cells; Ovarian angiogenesis; sVEGFR 1; TIMP 1

Indexed keywords

RECOMBINANT PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; VASCULOTROPIN RECEPTOR 1;

ADULT; ANGIOGENESIS; ARTICLE; BLOOD SAMPLING; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; FEMALE; GRANULOSA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; OVARY; OVARY FOLLICLE FLUID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; REGULATORY MECHANISM; RNA INTERFERENCE; SUPERNATANT; UMBILICAL VEIN; BLOOD; CELL CULTURE; DRUG EFFECT; METABOLISM; SECRETION;

ADULT; CELL PROLIFERATION; CELLS, CULTURED; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOTHELIAL CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; RNA INTERFERENCE; TISSUE INHIBITOR OF METALLOPROTEINASE-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 74049158663     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gap053     Document Type: Article

References (59)

1. Akahane T, Akahane M, Shah A, Connor CM, Thorgeirsson UP. TIMP-1 inhibits microvascular endothelial cell migration by MMP-dependent and MMP-independent mechanisms. Exp Cell Res 2004;301:158-167.
2. Baker AH, Zaltsman AB, George SJ, Newby AC. Divergent effects of tissue inhibitor of metalloproteinase-1, -2, or -3 overexpression on rat vascular smooth muscle cell invasion, proliferation, and death in vitro. J Clin Invest 1998;101:1478-1487.
3. Barleon B, Reusch P, Totzke F, Herzog C, Keck C, Martiny-Baron G, Marmé D. Soluble VEGFR-1 secreted by endothelial cells and monocytes is present in human serum and plasma from healthy donors. Angiogenesis 2001;4:143-154.
4. Bartoli M, Platt D, Lemtalsi T, Gu X, Brooks SE, Marrero MB, Caldwell RB. VEGF differentially activates STAT3 in microvascular endothelial cells. FASEB J 2003;17:1562-1564.
5. Cébe-Suarez S, Zehnder-Fjällman A, Ballmer-Hofer K. The role of VEGF receptors in angiogenesis; complex partnerships. Cell Mol Life Sci 2006;63:601-615.
6. Charnock-Jones DS. Soluble flt-1 and the angiopoietins in the development and regulation of placental vasculature. J Anat 2002;200:607-615.
7. Chirco R, Liu X-W, Jung K-K, Kim H-R. Novel functions of TIMPs in cell signaling. Cancer Metastasis Rev 2006;25:99-113.
8. Dickson SE, Bicknell R, Fraser HM. Mid-luteal angiogenesis and function in the primate is dependent on vascular endothelial growth factor. J Endocrinol 2001;168:409-416.
9. Douglas NC, Nakhuda GS, Sauer MV, Zimmermann RC. Angiogenesis and ovarian function. J Fertil Reprod 2005;13:7-15.
10. Duncan WC. The human corpus luteum: remodelling during luteolysis and maternal recognition of pregnancy. Rev Reprod 2000;5:12-17.
11. Eubank TD, Roberts R, Galloway M, Wang Y, Cohn DE, Marsh CB. GM-CSF induces expression of soluble VEGF receptor-1 from human monocytes and inhibits angiogenesis in mice. Immunity 2004;21:831-842.
12. Ferrara N, Chen H, Davis-Smyth T, Gerber HP, Nguyen TN, Peers D, Chisholm V, Hillan KJ, Schwall RH. Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nat Med 1998;4:336-340.
13. Fraser HM. Regulation of the ovarian follicular vasculature. Reprod Biol Endocrinol 2006;4:18-26.
14. Fraser HM, Lunn SF. Angiogenesis and its control in the female reproductive system. Br Med Bull 2000;56:787-797.
15. Fraser HM, Lunn SF. Regulation and manipulation of angiogenesis in the primate corpus luteum. Reproduction 2001;121:355-362.
16. Geva E, Jaffe RB. Role of vascular endothelial growth factor in ovarian physiology and pathology. Fertil Steril 2000;74:429-438.
17. Gruemmer R, Motejlek K, Berghaus D, Weich HA, Neulen J. Regulation of soluble vascular endothelial growth factor receptor (sFlt-1/sVEGFR-1) expression and release in endothelial cells by human follicular fluid and granulosa cells. Reprod Biol Endocrinol 2005a;3:57-63.
18. Gruemmer R, Klein-Hitpass L, Neulen J. Regulation of gene expression in endothelial cells: the role of human follicular fluid. J Mol Endocrinol 2005b;34:37-46.
19. Harslund J, Nielsen OL, Brünner N, Offenberg H. Gender-dependent physiological implications of combined PAI-1 and TIMP-1 gene deficiency characterized in a mouse model. Am J Physiol Regul Integr Comp Physiol 2007;293:1630-1639.
20. Hazzard TM, Xu F, Stouffer RL. Injection of soluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal function in rhesus monkeys. Biol Reprod 2002;67:1305-1312.
21. Hornig C, Barleon B, Ahmad S, Vuorela P, Ahmed A, Weich HA. Release and complex formation of soluble VEGFR-1 from endothelial cells and biological fluids. Lab Invest 2000;80:443-454.
22. Huo N, Ichikawa Y, Kamiyama M, Ishikawa T, Hamaguchi Y, Hasegawa S, Nagashima Y, Miyazaki K, Shimada H. MMp-7 (matrilysin) accelerated growth of human umbilical vein endothelial cells. Cancer Lett 2002; 177:95-100.
23. Ito T-K, Ishii G, Saito S, Yano K, Hoshino A, Suzuki T, Ochiai A. Degradation of soluble VEGF receptor-1 by MMP-7 allows VEGF access to endothelial cells. Blood 2009;113:2363-2369.
24. Jackson CJ, Nguyen M. Human microvascular endothelial cells differ from macrovascular endothelial cells in their expression of matrix metalloproteinases. Int J Biochem Cell Biol 1997;29:1167-1177.
25. Kaczmarek MM, Schams D, Ziecik AJ. Role of vascular endothelial growth factor in ovarian physiology-an overview. Reprod Biol 2005;5:111-136.
26. Koga K, Osuga Y, Yoshino O, Hirota Y, Ruimeng X, Hirata T, Takeda S, Yano T, Tsutsumi O, Taketani Y. Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 2003;88:2348-2351.
27. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-685.
28. Lahav-Baratz S, Kraiem Z, Shiloh H, Koifman M, Ishai D, Dirnfeld M. Decreased expression of tissue inhibitor of matrix metalloproteinases in follicular fluid from women with polycystic ovaries compared with normally ovulating patients undergoing in vitro fertilization. Fertil Steril 2003;79:567-571.
29. Lamszus K, Ulbricht U, Matschke J, Brockmann MA, Fillbrandt R, Westphal M. Levels of soluble vascular endothelial growth factor (VEGF) receptor 1 in astrocytic tumors and its relation to malignancy, vascularity, and VEGF-A. Clin Cancer Res 2003;9:1399-1405.
30. 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 2005a;169:681-691.
31. Lee MM, Yoon BJ, Osiewicz K, Preston M, Bundy B, van Heeckeren AM, Werb Z, Soloway PD. Tissue inhibitor of metalloproteinase 1 regulates resistance to infection. Infect Immun 2005b;73:661-665.
32. Lockwood CJ, Toti P, Arcuri F, Norwitz E, Funai EF, Huang S-T, Buchwalder LF, Krikun G, Schatz F. Thrombin regulates soluble fms-like tyrosine kinase-1 (sFlt-1) expression in first trimester decidua. Am J Pathol 2007;170:1398-1405.
33. Mannello F, Gazzanelli G. Tissue inhibitors of metalloproteinases and programmed cell death: Conundrums, controversies and potential implications. Apoptosis 2001;6:479-482.
34. Matsumoto H, Fukui E, Yoshizawa M. Uterine angiogenesis during implantation in mice. J Mamm Ova Res 2007;24:45-49.
35. Motejlek K, Palluch F, Neulen J, Gruemmer R. Smoking impairs angiogenesis during maturation of human oocytes. Fertil Steril 2006;86:186-191.
36. Moussiopoulos N, Sahm P, Kunz R, Vogele T, Schneider C, Kessler C, Jackson CJ, Minh N. Human microvascular endothelial cells differ from macrovascular endothelial cells in their expression of matrix metalloproteinases. Int J Biochem Cell Biol 1997;29:1167-1177.
37. Munaut C, Lorquet S, Pequeux C, Blacher S, Berndt S, Frankenne F, Foidart J-M. Hypoxia is responsible for soluble vascular endothelial growth factor receptor-1 (VEGFR-1) but not for soluble endoglin induction in villous trophoblast. Hum Reprod 2008;23:1407-1415.
38. Murphy AN, Unsworth EJ, Stetler-Stevenson WG. Tissue inhibitor of metalloproteinases-2 inhibits bFGF-induced human microvascular endothelial cell proliferation. J Cell Physiol 1993;157:351-358.
39. Nagamatsu T, Fujii T, Kusumi M, Zou L, Yamashita T, Osuga Y, Momoeda M, Kozuma S, Taketani Y. Cytotrophoblasts up-regulate soluble fms-like tyrosine kinase-1 expression under reduced oxygen: An implication for the placental vascular development and the pathophysiology of preeclampsia. Endocrinology 2004;145:4838-4845.
40. Neulen J, Wenzel D, Hornig C, Wünsch E, Weissenborn U, Grunwald K, Büttner R, Weich H. Poor responder-high responder: the importance of soluble vascular endothelial growth factor receptor 1 in ovarian stimulation protocols. Hum Reprod 2001;16:621-626.
41. Nevo O, Soleymanlou N, Wu Y, Xu J, Kingdom J, Many A, Zamudio S, Caniggia I. Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am J Physiol Regul Integr Comp Physiol 2006;291:1085-1093.
42. Nothnick WB. Tissue inhibitor of metalloproteinase-1 (TIMP-1) deficient mice display reduced serum progesterone levels during corpus luteum development. Endocrinology 2003;144:5-8.
43. Pau E, Alonso-Muriel I, Gómez R, Novella E, Ruiz A, García-Velasco JA, Simón C, Pellicer A. Plasma levels of soluble vascular endothelial growth factor receptor-1 may determine the onset of early and late ovarian hyperstimulation syndrome. Hum Reprod 2006;21:1453-1460.
44. Phan B, Rakenius A, Pietrowski D, Bettendorf H, Keck C, Herr D. hCG-dependent regulation of angiogenic factors in human granulosa lutein cells. Mol Reprod Dev 2006;73:878-884.
45. Plendl J. Angiogenesis and vascular regression in the ovary. Anat Histol Embryol 2000;29:257-266.
46. Rahimi N, Golde TE, Meyer RD. Identification of ligand-induced proteolytic cleavage and ectodomain shedding of VEGFR-1/FLT1 in leukemic cancer cells. Cancer Res 2009;69:2607-2614.
47. Reduta T, Laudańska H, Laudanski P. Tissue inhibitors of matrix metalloproteinase-1 levels are increased in serum of patients with allergic contact dermatitis. Contact Dermatitis 2007;57:100-104.
48. Reed MJ, Koike T, Sadoun E, Sage EH, Puolakkainen P. Inhibition of TIMP1 enhances angiogenesis in vivo and cell migration in vitro. Microvasc Res 2003;65:9-17.
49. Reynolds LP, Redmer DA. Angiogenesis in the placenta. Biol Reprod 2001; 64:1033-1040.
50. Robak E, Sysa-Jedrzejewska A, Robak T. Vascular endothelial growth factor and its soluble receptors VEGFR-1 and VEGFR-2 in the serum of patients with systemic lupus erythematosus. Mediators Inflamm 2003;12:293-298.
51. Rundhaug JE. Matrix metalloproteinases, angiogenesis, and cancer. Clin Cancer Res 2003;9:551-554.
52. Sherer DM, Abulafia O. Angiogenesis during implantation, and placental and early embryonic development. Placenta 2001;22:1-13.
53. Shores EM, Hunter MG. Production of tissue inhibitors of metalloproteinases (TIMPs) by pig ovarian cells in vivo and the effect of TIMP-1 on steroidogenesis in vitro. J Reprod Fertil 2000;120:73-81.
54. Stetler-Stevenson WG. The tumor microenvironment: regulation by MMP-independent effects of tissue inhibitor of metalloproteinases-2. Cancer Metastasis Rev 2008;27:57-66.
55. Stetler-Stevenson WG, Seo DW. TIMP-2: an endogenous inhibitor of angiogenesis. Trends Mol Med 2005;11:97-103.
56. Viemann D, Goebeler M, Schmid S, Nordhues U, Klimmek K, Sorg C, Roth J. TNF induces distinct gene expression programs in microvascular and macrovascular human endothelial cells. J Leukoc Biol 2006;80:174-185.
57. Wulff C, Fraser HM, Kreienberg R. Angiogenesis in the human corpus luteum of the normal menstrual cycle and during early pregnancy. Geburtsh Frauenheilk 2004;64:690-699.
58. Yamada E, Tobe T, Yamada H, Okamoto N, Zack DJ, Werb Z, Soloway PD, Campochiaro PA. TIMP-1 promotes VEGF-induced neovascularization in the retina. Histol Histopathol 2001;16:87-97.
59. Ylä-Herttuala S, Rissanen TT, Vajanto I, Hartikainen J. Vascular endothelial growth factors. J Am Coll Cardiol 2007;49:1015-1026.