Fertility and Sterility
Volume 91, Issue 2 , Pages 535-541 , February 2009

The production of vascular endothelial growth factor and metalloproteinase via protease-activated receptor in human endometrial stromal cells

Received 1 June 2007 ,Revised 26 November 2007 ,Accepted 26 November 2007.

References 

  1. Torry DS, Torry RJ. Angiogenesis and the expression of vascular endothelial growth factor in endometrium and placenta. Am J Reprod Immunol. 1997;37:21–29
  2. Leung DW, Cachianes G, Kuang WJ, Goeddle DV, Ferrara N. Vascular endothelial growth factor is secreted angiogenic mitogen. Science. 1989;246:1306–1309
  3. Anthony FW, Wheeler T, Elcock CL, Pickett M, Thomas EJ. Short report: identification of a specific pattern of vascular endothelial growth factor mRNA expression in human placenta and cultured placental fibroblasts. Placenta. 1994;15:557–561
  4. De Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science. 1992;255:989–991
  5. Terman BI, Dougher-Vermazen M, Carrion ME, Dimitrov D, Armellino DC, Gospodarowicz D, et al. Identification of the KDR tyrosine kinase as a receptor for vascular endothelial growth factor. Biochem Biophys Res Commun. 1992;187:1579–1586
  6. Kaipainen A, Korhonen J, Pajusola K, Aprelikova O, Persico MG, Terman BI, et al. The related FLT4, FLT1, and KDR receptor tyrosine kinase show distinct expression pattern in human fetal endothelial cells. J Exp Med. 1993;178:2077–2088
  7. Charnock-Jones DS, Sharkey AM, Boocock CA, Ahmed A, Plevin R, Ferrara N, et al. Vascular endothelial growth factor receptor localization and activation in human trophoblast and choriocarcinoma cells. Biol Reprod. 1994;51:524–530
  8. Moses M, Langer R. Inhibitors of angiogenesis. Biotechnology. 1991;9:630–634
  9. Matrisian LM. The matrix-degrading metalloproteinases. Bioassays. 1992;14:455–463
  10. Woessner JF. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 1991;5:2145–2154
  11. Brass LF, Manning DR, Williams AG, Woolkalis MJ, Poncz M. Receptor and G protein-mediated responses to thrombin in HEL cells. J Biol Chem. 1991;266:958–965
  12. Mitchell CA, Jefferson AB, Bejeck BE, Brugge JS, Deuel TF, Majeus PW. Thrombin-stimulated immunoprecipitation of phosphatidylinositol 3-kinase from human platelets. Proc Natl Acad Sci USA. 1990;87:9396–9400
  13. Gutkind JS, Lacal PM, Robbins KC. Thrombin-dependent association of phosphatidylinositol 3-kinase with p60c-src and p59fyn in human platelets. Mol Cell Biol. 1990;10:3806–3809
  14. Babich M, King KL, Nissenson RA. Thrombin stimulates inositol phosphate production and intracellular free calcium by a pertussis toxin-insensitive mechanism of osteosarcoma cells. Endocrinology. 1990;126:948–954
  15. Gospodarowicz D, Brown KD, Birdwell CR, Zetter BR. Control of proliferation of human vascular endothelial cells. Characterization of the response of human umbilical vein endothelial cells to fibroblast growth factor, epidermal growth factor, and thrombin. J Cell Biol. 1978;77:774–788
  16. Chen LB, Buchanan JM. Mitogenic activity of blood components. I. Thrombin and prothrombin. Proc Natl Acad Sci USA. 1975;72:131–135
  17. Vu TK, Hung DT, Wheaton VI, Coughlin SR. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell. 1991;64:1057–1068
  18. Rasmussen UB, Vouret-Craviari V, Jallat S, Schlesinger Y, Pages G, Pavirani A, et al. cDNA cloning and expression of a hamster α-thrombin receptor coupled to Ca2+ mobilization. FEBS Lett. 1991;288:123–128
  19. Vu TK, Wheaton VI, Hung DT, Charo I, Coughlin SR. Domains specifying thrombin-receptor interaction. Nature. 1991;353:674–677
  20. Chen J, Ishii M, Wang L, Ishii K, Coughlin SR. Thrombin receptor activation. Confirmation of the intramolecular tethered liganding hypothesis and discovery of an alternative intermolecular liganding mode. J Biol Chem. 1994;269:16041–16045
  21. Vassallo RJ, Kieber ET, Cichowski K, Brass LF. Structure-function relationships in the activation of platelet thrombin receptors by receptor-derived peptides. J Biol Chem. 1992;267:6081–6085
  22. Scarborough RM, Naughton MA, Teng W, Hung DT, Rose J, Vu TK, et al. Tethered ligand agonist peptide. J Biol Chem. 1992;267:13146–13149
  23. Naor Z, Benard O, Seger R. Activation of MAPK cascades by G-protein–coupled receptors: the case of gonadotropin-releasing hormone receptor. Trends Endocrinol Metab. 2000;11:91–99
  24. Della Rocca GJ, Maudsley S, Daaka Y, Lefkowitz RJ, Luttrell LM. Pleiotropic coupling of G protein–coupled receptors to the mitogen-activated protein kinase cascade. Role of focal adhesions and receptor tyrosine kinases. J Biol Chem. 1999;274:13978–13984
  25. Marinissen MJ, Servitja JM, Offermanns S, Simon MI, Gutkind JS. Thrombin protease-activated receptor-1 signals through Gq- and G13-initiated MAPK cascades regulating c-Jun expression to induce cell transformation. J Biol Chem. 2003;278:46814–46825
  26. Wang H, Ubl JJ, Stricker R, Reiser G. Thrombin (PAR-1)-induced proliferation in astrocytes via MAPK involves multiple signaling pathways. Am J Physiol Cell Physiol. 2002;283:C1351–C1364
  27. Li XF, Gregory J, Ahmed A. Immunolocalization of vascular endothelial growth factor in human endometrium. Growth Factors. 1994;11:277–282
  28. Kawano Y, Matsui N, Kamihigashi S, Narahara H, Miyakawa I. Effects of interferon-γ on secretion of vascular endothelial growth factor by endometrial stromal cells. Am J Reprod Immunol. 2000;43:47–52
  29. Lee A, Christenson LK, Patton PE, Burry KA, Touffer RL. Vascular endothelial growth factor production by human luteinized granulosa cells in vitro. Hum Reprod. 1997;12:2756–2761
  30. Shifren JL, Tseng JF, Zaloudek CJ, Ryan IP, Meng YG, Ferrara N, et al. Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis. J Clin Endocrinol Metab. 1996;81:3112–3118
  31. Kawano Y, Nakamura S, Nasu K, Narahara H, Miyakawa I. The effect of epidermal growth factor on vascular endothelial growth factor secretion by endometrial stromal cells. Clin Exp Med. 2002;2:69–75
  32. Sharkey AM, Charnock-Jones DS, Boocock CA, Brown KD, Smith SK. Expression of mRNA for vascular endothelial growth factor in human placenta. J Reprod Fertil. 1993;99:609–615
  33. Kawano Y, Nakamura S, Fukuda J, Miyakawa I. The effect of insulin-like growth factor-I on production of vascular endothelial growth factor by amnion-derived (WISH) cells. Growth Horm IGF Res. 2004;14:376–381
  34. Charnock-Jones DS, Sharkey AM, Rajput-Williams J, Burch D, Schofield JP, Fountain SA, et al. Identification and localization of alternately spliced mRNAs for vascular endothelial growth factor in human uterus and estrogen regulation in endometrial carcinoma cell lines. Biol Reprod. 1993;48:1120–1128
  35. Meduri G, Bausero P, Perrot-Applanat M. Expression of vascular endothelial growth factor receptor in the human endometrium: modulation during the menstrual cycle. Biol Reprod. 2000;62:439–447
  36. Gargett CE, Lederman F, Heryanto B, Gambino LS, Rogers PAW. Focal vascular endothelial growth factor correlates with angiogenesis in human endometrium. Role of intravascular neurophil. Hum Reprod. 2001;16:1065–1075
  37. Lockwood CJ, Krikun G, Koo AB, Kadner S, Schatz F. Differential effects of thrombin and hypoxia on endometrial stromal and glandular epithelial cell vascular endothelial growth factor expression. J Clin Endocrinol Metab. 2002;87:4280–4286
  38. Smith SK. Growth factors in human endometrium. Human Reprod. 1994;9:936–946
  39. Goodger AM. Rogers PA Blood vessels growth in the endometrium. Microcirculation. 1995;2:329–343
  40. Tazuke SI, Giudice LC. Growth factors and cytokines in endometrium, embryonic development, and maternal:embryonic interactions. Semin Reprod Endocrinol. 1996;14:231–245
  41. Tsopanoglou NE, Maragoudakis ME. On the mechanism of thrombin-induced angiogenesis: potentiation of vascular endothelial growth factor activity on endothelial cells by up-regulation of its receptors. J Biol Chem. 1999;274:23969–23976
  42. Johnson K, Choi Y, DeGroot E, Samuels I, Creasey A, Aarden L. Potential mechanisms for a proinflammatory vascular cytokine response to coagulation activation. J Immunol. 1998;160:5130–5135
  43. Hou L, Ravenall S, Macey MG, Harriott P, Kapas S, Howells GL. Protease-activated receptors and their role in IL-6 and NF-IL-6 expression in human gingival fibroblasts. J Periodontal Res. 1998;33:205–211
  44. Hoffman M, Cooper ST. Thrombin enhances monocyte secretion of tumor necrosis factor and interleukin-1β by two distinct mechanisms. Blood Cells Mol Dis. 1995;21:156–167
  45. Lockwood CJ, Krikun G, Aigner S, Schatz F. Effects of thrombin on steroid-modulated cultured endometrial stromal cell fibrinolytic potential. J Clin Endocrinol Metab. 1996;81:107–112
  46. Minden A, Lin A, McMahon M, Lange-Carter C, Derijard B, Davis RJ, et al. Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science. 1994;266:1719–1723
  47. Dent P, Haser W, Haystead TAJ, Vincent LA, Roberts TM, Sturgill TW. Activation of mitogen-activated protein kinase kinase by v-Raf in NIH 3T3 cells and in vitro. Science. 1992;257:1404–1407
  48. Kyriakis JM, Zhang XF, Banerjee P, Brautigan DL, Rapp UR, Avruch J. Raf-1activates MAP kinase-kinase. Nature. 1992;358:417–421
  49. Howe LR, Leevers SJ, Gomez N, Nakielny S, Cohen P, Marshall CJ. Activation of the MAP kinase pathway by the protein kinase raf. Cell. 1992;71:335–342
  50. Sanchez I, Hughes RT, Mayer BJ, Yee K, Woodgett JR, Avruch J, et al. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature. 1994;372:794–798
  51. Yan M, Dai T, Deak JC, Kyriakis JM, Zon LI, Woodgett JR, et al. Activation of stress-activated protein kinase by MEKK1 phosphorylation of its activator SEK1. Nature. 1994;372:798–800
  52. Pelech SL. Networking with protein kinase. Current Biol. 1993;3:513–515
  53. Crews CM, Erikson RL. Extracellular signals and reversible protein phosphorylation: what to Mek of it all. Cell. 1993;74:215–217
  54. Egan SE, Weinberg RA. The pathway to signal achievement. Nature. 1993;365:781–783
  55. Dikic I, Blaukat A. Protein tyrosine kinase-mediated pathways in G protein–coupled receptor signaling. Cell Biochem Biophys. 1999;30:369–387

 Y.F. has nothing to disclose. Y.K. has nothing to disclose. J.F. has nothing to disclose. H.M. has nothing to disclose. H.N. has nothing to disclose.

 Supported in part by a Grant-in-Aid (No. 15591766) for Specific Research from the Ministry of Education, Sports, Science, and Culture of Japan.

PII: S0015-0282(07)04145-3

doi: 10.1016/j.fertnstert.2007.11.080

Fertility and Sterility
Volume 91, Issue 2 , Pages 535-541 , February 2009