Role of extracellular signal-regulated kinase and AKT cascades in regulating hypoxia-induced angiogenic factors produced by a trophoblast-derived cell line

Journal of Endocrinology

Volumn 206, Issue 1, 2010, Pages 131-140

  Fujita, Daisuke ^a   Tanabe, Akiko ^a   Sekijima, Tatsuharu ^a   Soen, Hekiko ^a   Narahara, Keijirou ^a   Yamashita, Yoshiki ^a   Terai, Yoshito ^a   Kamegai, Hideki ^a   Ohmichi, Masahide ^a  

^a OSAKA MEDICAL COLLEGE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOGLIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA; VASCULOTROPIN;

ARTICLE; CELL HYPOXIA; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TROPHOBLAST;

ANGIOGENESIS INDUCING AGENTS; ANTIGENS, CD; CELL HYPOXIA; CELL LINE; CELL LINE, TUMOR; CHORIOCARCINOMA; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; OXYGEN; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, CELL SURFACE; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION; TROPHOBLASTS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77953854774     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1677/JOE-10-0027     Document Type: Article

References (57)

1. Bernabeu C, Conley BA & Vary CP 2007 Novel biochemical pathways of endoglin in vascular cell physiology. Journal of Cellular Biochemistry 102 1375-1388.
2. Berra E, Pages G & Pouyssegur J 2000 MAP kinases and hypoxia in the control of VEGF expression. Cancer Metastasis Reviews 19 139-145.
3. Brekken RA, Li C & Kumar S 2002 Strategies for vascular targeting in tumors. International Journal of Cancer 100 123-130.
4. Burton GJ, Jauniaux E & Watson AL 1999 Maternal arterial connections to the placental intervillous space during the first trimester of human pregnancy: the Boyd collection revisited. American Journal of Obstetrics and Gynecology 181 718-724.
5. Cheifetz S, Bellon T, Cales C, Vera S, Bernabeu C, Massague J & Letarte M 1992 Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. Journal of Biological Chemistry 267 19027-19030.
6. Chen JX & Meyrick B 2004 Hypoxia increases Hsp90 binding to eNOS via PI3K-Akt in porcine coronary artery endothelium. Laboratory Investigation 84 182-190.
7. Cooper JC, Sharkey AM, McLaren J, Charnock-Jones DS & Smith SK 1995 Localization of vascular endothelial growth factor and its receptor, flt, in human placenta and decidua by immunohistochemistry. Journal of Reproduction and Fertility 105 205-213. (Pubitemid 26008010)
8. Crocker IP, Strachan BK, Lash GE, Cooper S, Warren AY & Baker PN 2001 Vascular endothelial growth factor but not placental growth factor promotes trophoblast syncytialization in vitro. Journal of the Society for Gynecologic Investigation 8 341-346.
9. Damsky CH & Fisher SJ 1998 Trophoblast pseudo-vasculogenesis: faking it with endothelial adhesion receptors. Current Opinion in Cell Biology 10 660-666.
10. Demir R, Kayisli UA, Seval Y, Celik-Ozenci C, Korgun ET, Demir-Weusten AY & 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.
11. Diaz-Gonzalez JA, Russell J, Rouzaut A, Gil-Bazo I & Montuenga L 2005 Targeting hypoxia and angiogenesis through HIF-1alpha inhibition. Cancer Biology and Therapy 4 1055-1062.
12. Duff SE, Li C, Garland JM & Kumar S 2003 CD105 is important for angiogenesis: evidence and potential applications. FASEB Journal 17 984-992.
13. Ellinger I, Schwab M, Stefanescu A, Hunziker W & Fuchs R 1999 IgG transport across trophoblast-derived BeWo cells: a model system to study IgG transport in the placenta. European Journal of Immunology 29 733-744. (Pubitemid 29119052)
14. Ferrara N, Gerber HP & LeCouter J 2003 The biology of VEGF and its receptors. Nature Medicine 9 669-676.
15. Gangloff YG, Mueller M, Dann SG, Svoboda P, Sticker M, Spetz JF, Um SH, Brown EJ, Cereghini S, Thomas G et al. 2004 Disruption of the mouse mTOR gene leads to early postimplantation lethality and prohibits embryonic stem cell development. Molecular and Cellular Biology 24 9508-9516.
16. Garcia-Lloret MI, Morrish DW, Wegmann TG, Honore L, Turner AR & Guilbert LJ 1994 Demonstration of functional cytokine-placental interactions: CSF-1 and GM-CSF stimulate human cytotrophoblast differentiation and peptide hormone secretion. Experimental Cell Research 214 46-54.
17. Gougos A, St Jacques S, Greaves A, O'Connell PJ, d'Apice AJ, Buhring HJ, Bernabeu C, van Mourik JA & Letarte M 1992 Identification of distinct epitopes of endoglin, an RGD-containing glycoprotein of endothelial cells, leukemic cells, and syncytiotrophoblasts. International Immunology 4 83-92.
18. Heaton SJ, Eady JJ, Parker ML, Gotts KL, Dainty JR, Fairweather-Tait SJ, McArdle HJ, Srai KS & Elliott RM2008 The use of BeWo cells as an in vitro model for placental iron transport. American Journal of Physiology. Cell Physiology 295 C1445-C1453.
19. Hisamoto K, Ohmichi M, Kanda Y, Adachi K, Nishio Y, Hayakawa J, Mabuchi S, Takahashi K, Tasaka K, Miyamoto Y et al. 2001a Induction of endothelial nitric-oxide synthase phosphorylation by the raloxifene analog LY117018 is differentially mediated by Akt and extracellular signalregulated protein kinase in vascular endothelial cells. Journal of Biological Chemistry 276 47642-47649.
20. Hisamoto K, Ohmichi M, Kurachi H, Hayakawa J, Kanda Y, Nishio Y, Adachi K, Tasaka K, Miyoshi E, Fujiwara N et al. 2001b Estrogen induces the Akt-dependent activation of endothelial nitric-oxide synthase in vascular endothelial cells. Journal of Biological Chemistry 276 3459-3467.
21. Jaffe R &Woods JR Jr 1993 Color Doppler imaging and in vivo assessment of the anatomy and physiology of the early uteroplacental circulation. Fertility and Sterility 60 293-297. (Pubitemid 23228161)
22. Jaffe R, Jauniaux E & Hustin J 1997 Maternal circulation in the first-trimester human placenta - myth or reality? American Journal of Obstetrics and Gynecology 176 695-705.
23. James JL, Stone PR & Chamley LW 2006 The regulation of trophoblast differentiation by oxygen in the first trimester of pregnancy. Human Reproduction Update 12 137-144.
24. Jauniaux E, Watson A & Burton G 2001 Evaluation of respiratory gases and acid-base gradients in human fetal fluids and uteroplacental tissue between 7 and 16 weeks' gestation. American Journal of Obstetrics and Gynecology 184 998-1003.
25. Jauniaux E, Hempstock J, Greenwold N & Burton GJ 2003 Trophoblastic oxidative stress in relation to temporal and regional differences in maternal placental blood flow in normal and abnormal early pregnancies. American Journal of Pathology 162 115-125. (Pubitemid 36041994)
26. Jauniaux E, Poston L & Burton GJ 2006 Placental-related diseases of pregnancy: involvement of oxidative stress and implications in human evolution. Human Reproduction Update 12 747-755.
27. Kendall RL, Wang G & Thomas KA 1996 Identification of a natural soluble form of the vascular endothelial growth factor receptor, FLT-1, and its heterodimerization with KDR. Biochemical and Biophysical Research Communications 226 324-328.
28. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH et al. 2004 Circulating angiogenic factors and the risk of preeclampsia. New England Journal of Medicine 350 672-683.
29. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R et al. 2006 Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. New England Journal of Medicine 355 992-1005.
30. Li H, Dakour J, Guilbert LJ, Winkler-Lowen B, Lyall F & Morrish DW 2005 PL74 a novel member of the transforming growth factor-beta superfamily, is overexpressed in preeclampsia and causes apoptosis in trophoblast cells. Journal of Clinical Endocrinology and Metabolism 90 3045-3053.
31. Luo Z, Fujio Y, Kureishi Y, Rudic RD, Daumerie G, Fulton D, Sessa WC & Walsh K 2000 Acute modulation of endothelial Akt/PKB activity alters nitric oxide-dependent vasomotor activity in vivo. Journal of Clinical Investigation 106 493-499.
32. Lyall F 2005 Priming and remodelling of human placental bed spiral arteries during pregnancy - a review. Placenta 26 S31-S36.
33. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE et al. 2003 Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. Journal of Clinical Investigation 111 649-658.
34. McAllister KA, Grogg KM, Johnson DW, Gallione CJ, Baldwin MA, Jackson CE, Helmbold EA, Markel DS, McKinnon WC, Murrell J et al. 1994 Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nature Genetics 8 345-351.
35. Meekins JW, Pijnenborg R, Hanssens M, McFadyen IR & van Asshe A 1994 A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. British Journal of Obstetrics and Gynaecology 101 669-674. (Pubitemid 24251519) (Pubitemid 24251519)
36. Minet E, Michel G, Mottet D, Raes M & Michiels C 2001 Transduction pathways involved in hypoxia-inducible factor-1 phosphorylation and activation. Free Radical Biology and Medicine 31 847-855.
37. Morrish DW, Bhardwaj D, Dabbagh LK, Marusyk H & Siy O 1987 Epidermal growth factor induces differentiation and secretion of human chorionic gonadotropin and placental lactogen in normal human placenta. Journal of Clinical Endocrinology and Metabolism 65 1282-1290. (Pubitemid 18026872)
38. Murakami M, Ichisaka T, Maeda M, Oshiro N, Hara K, Edenhofer F, Kiyama H, Yonezawa K & Yamanaka S 2004 mTOR is essential for growth and proliferation in early mouse embryos and embryonic stem cells. Molecular and Cellular Biology 24 6710-6718.
39. Neelima PS & Rao AJ 2008 Gene expression profiling during Forskolin induced differentiation of BeWo cells by differential display RT-PCR. Molecular and Cellular Endocrinology 281 37-46.
40. Northcott CA, Poy MN, Najjar SM & Watts SW 2002 Phosphoinositide 3-kinase mediates enhanced spontaneous and agonist-induced contraction in aorta of deoxycorticosterone acetate-salt hypertensive rats. Circulation Research 91 360-369.
41. Park JE, Chen HH, Winer J, Houck KA & Ferrara N 1994 Placenta growth factor. Potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR. Journal of Biological Chemistry 269 25646-25654.
42. Phung TL, Ziv K, Dabydeen D, Eyiah-Mensah G, Riveros M, Perruzzi C, Sun J, Monahan-Earley RA, Shiojima I, Nagy JA et al. 2006 Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10 159-170.
43. Pijnenborg R, Anthony J, Davey DA, Rees A, Tiltman A, Vercruysse L & van Assche A 1991 Placental bed spiral arteries in the hypertensive disorders of pregnancy. British Journal of Obstetrics and Gynaecology 98 648-655.
44. Rodesch F, Simon P, Donner C & Jauniaux E 1992 Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstetrics and Gynecology 80 283-285.
45. Sanchez-Elsner T, Botella LM, Velasco B, Langa C & Bernabeu C 2002 Endoglin expression is regulated by transcriptional cooperation between the hypoxia and transforming growth factor-beta pathways. Journal of Biological Chemistry 277 43799-43808.
46. Starzyk KA, Salafia CM, Pezzullo JC, Lage JM, Parkash V, Vercruysse L, Hanssens M & Pijnenborg R 1997 Quantitative differences in arterial morphometry define the placental bed in preeclampsia. Human Pathology 28 353-358.
47. St-Jacques S, Forte M, Lye SJ & Letarte M 1994 Localization of endoglin, a transforming growth factor-beta binding protein, and of CD44 and integrins in placenta during the first trimester of pregnancy. Biology of Reproduction 51 405-413. (Pubitemid 24297612)
48. Toporsian M, Gros R, Kabir MG, Vera S, Govindaraju K, Eidelman DH, Husain M& LetarteM2005 A role for endoglin in coupling eNOS activity and regulating vascular tone revealed in hereditary hemorrhagic telangiectasia. Circulation Research 96 684-692.
49. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA et al. 2006 Soluble endoglin contributes to the pathogenesis of preeclampsia. Nature Medicine 12 642-649. (Pubitemid 43865232) (Pubitemid 43865232)
50. Wen HY, Abbasi S, Kellems RE & Xia Y 2005 mTOR: a placental growth signaling sensor. Placenta 26 S63-S69.
51. Yamakawa M, Liu LX, Date T, Belanger AJ, Vincent KA, Akita GY, Kuriyama T, Cheng SH, Gregory RJ & Jiang C 2003 Hypoxia-inducible factor-1 mediates activation of cultured vascular endothelial cells by inducing multiple angiogenic factors. Circulation Research 93 664-673.
52. Yang M, Lei ZM & Rao Ch V 2003a The central role of human chorionic gonadotropin in the formation of human placental syncytium. Endocrinology 144 1108-1120.
53. Yang ZZ, Tschopp O, Hemmings-Mieszczak M, Feng J, Brodbeck D, Perentes E & Hemmings BA 2003b Protein kinase B alpha/Akt1 regulates placental development and fetal growth. Journal of Biological Chemistry 278 32124-32131.
54. YungHW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS & Burton GJ 2008 Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. American Journal of Pathology 173 451-462.
55. Zhou Y, Damsky CH & Fisher SJ 1997 Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome? Journal of Clinical Investigation 99 2152-2164.
56. Zhou Y, Bellingard V, Feng KT, McMaster M & Fisher SJ 2003 Human cytotrophoblasts promote endothelial survival and vascular remodeling through secretion of Ang2, PlGF, and VEGF-C. Developmental Biology 263 114-125.
57. Zygmunt M, Herr F, Munstedt K, Lang U & Liang OD 2003 Angiogenesis and vasculogenesis in pregnancy. European Journal of Obstetrics, Gynecology, and Reproductive Biology 110 S10-S18.