Noncatalytic domain of uPA stimulates human extravillous trophoblast migration by using phospholipase C, phosphatidylinositol 3-kinase and mitogen-activated protein kinase

Experimental Cell Research

Volumn 286, Issue 1, 2003, Pages 138-151

  Liu, Jessica ^a   Chakraborty, Chandan ^a   Graham, Charles H ^b   Barbin, Youssef P ^a   Dixon, S Jeffrey ^a   Lala, Peeyush K ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

Extravillous trophoblast; Intracellular calcium; Migration; Mitogen activated protein kinase; Phosphatidylinositol 3 kinase; Phospholipase C; Urokinase type plasminogen activator; Urokinase type plasminogen activator receptors

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 2,5 PYRROLIDINEDIONE; 1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 MORPHOLINO 8 PHENYLCHROMONE; ANTIBODY; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; POLYCARBONATE; THAPSIGARGIN; UROKINASE; UROKINASE RECEPTOR;

AMINO TERMINAL SEQUENCE; ARTICLE; ASSAY; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL MIGRATION; CELL STIMULATION; CHORIOCARCINOMA; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; POROSITY; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; SPECTROFLUOROMETRY; SPONTANEOUS ABORTION; TROPHOBLAST;

EID: 0242418203     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4827(03)00089-2     Document Type: Article

References (65)

1. Kurman R.J. The morphology, biology, and pathology of intermediate trophoblast a look back to the present . Hum. Pathol. 22:1991;847-855.
2. Graham C.H., Lala P.K. Mechanisms of placental invasion of the uterus and their control. Biochem. Cell Biol. 70:1992;867-874.
3. Kaufmann P., Castellucci M. Extravillous trophoblasts in the human placenta. Trophoblast Res. 10:1997;21-65.
4. Lala P.K., Graham C.H. Mechanisms of trophoblast invasiveness and their control the role of proteases and protease inhibitors . Cancer Metast. Rev. 9:1990;369-379.
5. Graham C.H. Effect of transforming growth factor-beta on the plasminogen activator system in cultured first trimester human cytotrophoblasts. Placenta. 18:1997;137-143.
6. Andreasen P.A., Egelund R., Peterson H.H. The plasminogen activation system in tumor growth, invasion, and metastasis. Cell Mol. Life Sci. 57:2000;25-40.
7. Reuning U., Magdolen V., Wilhelm O., Fischer K., Lutz V., Graeff H., Schmitt M. Multifunctional potential of the plasminogen activation system in tumor invasion and metastasis. Int. J. Oncol. 13:1998;893-906.
8. Vassalli J.D., Sappino A.P., Belin D. The plasminogen activator/plasmin system. J. Clin. Invest. 88:1991;1067-1072.
9. Andreasen P.A., Kjoller L., Christensen L., Duffy M.J. The urokinase-type plasminogen activator system in cancer metastasis a review . Int. J. Cancer. 72:1997;1-22.
10. Yagel S., Parhar R.S., Jeffrey J.J., Lala P.K. Normal nonmetastatic human trophoblast cells share in vitro invasive properties of malignant cells. J. Cell Physiol. 136:1988;455-462.
11. Odekon L.E., Sato Y., Rifkin D.B. Urokinase-type plasminogen activator mediates basic fibroblast growth factor-induced bovine endothelial cell migration independent of its proteolytic activity. J. Cell Physiol. 150:1992;258-263.
12. Busso N., Masur S.K., Lazega D., Waxman S., Ossowski L. Induction of cell migration by pro-urokinase binding to its receptor possible mechanism for signal transduction in human epithelial cells . J. Cell Biol. 126:1994;259-270.
13. Resnati M., Guttinger M., Valcamonica S., Sidenius N., Blasi F., Fazioli F. Proteolytic cleavage of the urokinase receptor substitutes for the agonist-induced chemotactic effect. EMBO J. 15:1996;1572-1582.
14. Nguyen D.H., Hussaini I.M., Gonias S.L. Binding of urokinase-type plasminogen activator to its receptor in MCF-7 cells activates extracellular signal-regulated kinase 1 and 2 which is required for increased cellular motility. J. Biol. Chem. 273:1998;8502-8507.
15. Nguyen D.H., Catling A.D., Webb D.J., Sankovic M., Walker L.A., Somlyo A.V., Weber M.J., Gonias S.L. Myosin light chain kinase functions downstream of Ras/ERK to promote migration of urokinase-type plasminogen activator-stimulated cells in an integrin-selective manner. J. Cell Biol. 146:1999;149-164.
16. Yebra M., Goretzki L., Pfeifer M., Mueller B.M. Urokinase-type plasminogen activator binding to its receptor stimulates tumor cell migration by enhancing integrin-mediated signal transduction. Exp. Cell Res. 250:1999;231-240.
17. Fazioli F., Resnati M., Sidenius N., Higashimoto Y., Appella E., Blasi F. A urokinase sensitive region of the human urokinase receptor is responsible for its chemotactic ability. EMBO J. 16:1997;7279-7286.
18. Zini J.M., Murray S.C., Graham C.H., Lala P.K., Kariko K., Barnathan E.S., Mazar A., Henkin J., Cines D.B., McCrae K.R. Characterization of urokinase receptor expression by human placental trophoblasts. Blood. 79:1992;2917-2929.
19. Blasi F. The urokinase receptor a cell surface, regulated chemokine . APMIS. 107:1999;96-101.
20. Tecimer C., Doering D.L., Goldsmith L.J., Meyer J.S., Abdulhay G., Wittliff J.L. Clinical relevance of urokinase-type plasminogen activator, its receptor, and its inhibitor type 1 in endometrial cancer. Gynecol. Oncol. 80:2001;48-55.
21. Vassalli J.D., Baccino D., Belin D. A cellular binding site for the Mr 55,000 form of the human plasminogen activator, urokinase. J. Cell Biol. 100:1985;86-92.
22. Behrendt N., Ploug M., Pathy L., Houren G., Blasi F., Dano K. The ligand-binding domain of the cell surface receptor for urokinase-type plasminogen activator. J. Biol. Chem. 266:1991;7842-7847.
23. Multhaupt H.A., Mazar A., Cines D.B., Warhol M.J., McCrae K.R. Expression of urokinase receptors by human trophoblast a histochemical and ultrastructural analysis . Lab. Invest. 71:1994;392-400.
24. Estreicher A., Muhlhauser J., Carpentier J.L., Orci L., Vassalli J.D. The receptor for urokinase type plasminogen activator polarizes expression of the protease to the leading edge of migrating monocytes and promotes degradation of enzyme inhibitor complexes. J. Cell Biol. 111:1990;783-792.
25. McCrae K.R., DeMichele A.M., Pandhi P., Balsai M.J., Samuels P., Graham C., Lala P.K., Cines D.B. Detection of antitrophoblast antibodies in the sera of patients with anticardiolipin antibodies and fetal loss. Blood. 82:1993;2730-2741.
26. 2(+)-ATPase. Proc. Natl. Acad. Sci. USA. 87:1990;2466-2470.
27. Graham C.H., Hawley T.S., Hawley R.G., MacDougall J.R., Kerbel R.S., Khoo N., Lala P.K. Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp. Cell Res. 206:1993;204-211.
28. Graham C.H., Lysiak J.J., McCrae K.R., Lala P.K. Localization of transforming growth factor-beta at the human fetal-maternal interface role in trophoblast growth and differentiation . Biol. Reprod. 46:1992;561-572.
29. Irving J.A., Lala P.K. Functional role of cell surface integrins on human trophoblast cell migration regulation by TGF-beta, IGF-II, and IGFBP-1 . Exp. Cell Res. 217:1995;419-427.
30. Zdravkovic M., Aboagye-Mathiesen G., Guimond M.J., Hager H., Ebbesen P., Lala P.K. Susceptibility of MHC class 1 expressing extravillous trophoblast cell lines to killing by natural killer cells. Placenta. 20:1999;431-440.
31. Gleeson L.M., Chakraborty C., McKinnon T., Lala P.K. Insulin-like growth factor-binding protein 1 stimulates human trophoblast migration by signaling through alpha 5 beta 1 integrin via mitogen-activated protein kinase pathway. J. Clin. Endocrinol. Metab. 86:2001;2484-2493.
32. McKinnon T., Chakraborty C., Gleeson L.M., Chidiac P., Lala P.K. Stimulation of human extravillous trophoblast migration by IGF-II is mediated by IGF type 2 receptor involving inhibitory G protein(s) and phosphorylation of MAPK. J. Clin. Endocrinol. Metab. 86:2001;3665-3674.
33. Lala P.K., Graham C.H. TGFB-responsive human trophoblast-derived cell lines. Placenta. 22:2001;889-890.
34. Kilburn B.A., Wang J., Duniec-Dmuchkowski Z., Leach R.E., Ramero R., Armant D.R. ECM and hypoxia regulate the expression of HLA-G and integrins in a human trophoblast cell line. Biol. Reprod. 62:2000;739-747.
35. Graham C.H., Fitzpatrick T.E., McCrae K.R. Hypoxia stimulates urokinase receptor expression through a heme protein-dependent pathway. Blood. 91:1998;3300-3307.
36. Chen Y., Shyu J.F., Snathanagopal A., Inoue D., David J.P., Dixon S.J., Horne W.C., Baron R. The calcitonin receptor stimulates She tyrosine phosphorylation and Erk1/2 activation involvement of Gi, protein kinase C, and calcium . J. Biol. Chem. 273:1998;19809-19816.
37. Calabrese E.J. Cell migration/chemotaxis biphasic dose responses . Crit. Rev. Toxicol. 31:2001;615-624.
38. Conese M., Blasi F. Urokinase/urokinase receptor system mechanism and regulation . Biol. Chem. Hoppe-Seyler. 376:1995;143-155.
39. Ploug M., Behrendt N., Lober D., Dano K. Protein structure and membrane anchorage of the cellular receptor for urokinase-type plasminogen activator. Semin. Thromb. Hemo. 17:1991;183-193.
40. Chapman H.A. Plasminogen activators, integrins, and the coordinated regulation of cell adhesion and migration. Curr. Opin. Cell. Biol. 9:1997;714-724.
41. Kusch A., Tkachuk S., Haller H., Dietz R., Gulba D.C., Lipp M., Dumler I. Urokinase stimulates human vascular smooth muscle cell migration via a phosphatidylinositol 3-kinase-Tyk2 interaction. J. Biol. Chem. 275:2000;39466-39473.
42. Aguirre-Ghiso J.A., Kovalsi K., Ossowski L. Tumor dormancy induced by downregulation of urokinase type plasminogen receptor in human carcinoma involves integrins and MAPK signalling. J. Cell Biol. 147:1999;89-104.
43. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1:2000;11-21.
44. 2+ (CRAC) channels in human T cells. J. Cell Biol. 150:2000;1435-1444.
45. Christow S.P., Bychkov R., Schroeder C., Dietz R., Haller H., Dumler I., Gulba D.C. Urokinase activates calcium-dependent potassium channels in U937 cells via calcium release from intracellular stores. Eur. J. Biochem. 265:1999;264-272.
46. Stein R.C. Prospects for phosphoinositide 3-kinase inhibition as a cancer treatment. Endocr. Relat. Cancer. 8:2001;237-248.
47. Khwaja A., Rodriguez-Viciana P., Wennstrom S., Warne P.H., Downward J. Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/Akt cellular survival pathway. EMBO J. 16:1997;2783-2793.
48. Kauffmann-Zeh A., Rodriguez-Viciana P., Ulrich E., Gilbert C., Coffer P., Downward J., Evan G. Suppression of c-Myc-induced apoptosis by Ras signalling through PI(3)K and PKB. Nature. 385:1997;544-548.
49. Lin J., Adam R.M., Santiestevan E., Freeman M.R. The phosphatidylinositol 3′-kinase pathway is a dominant growth factor-activated cell survival pathway in LNCaP human prostate carcinoma cells. Cancer Res. 59:1999;2891-2897.
50. Sawyer S.T., Jacobs-Helber S.M. Unraveling distinct intracellular signals that promote survival and proliferation study of erythropoietin, stem cell factor, and constitutive signaling in leukemic cells . J. Hemo. Stem Cell Res. 9:2000;21-29.
51. Barker S.A., Lujan D., Wilson B.S. Multiple roles for PI3-kinase in the regulation of PLCgamma activity and Ca2+ mobilization in antigen-stimulated mast cells. J. Leukoc. Biol. 65:1999;321-329.
52. Broad L.M., Braun F.J., Lievremont J.P., Bird G.S., Kurosaki T., Putney J.W. Jr. Role of the phospholipase C-inositol 1,4,5-trisphosphate pathway in calcium release-activated calcium current and capacitative calcium entry. J. Biol. Chem. 276:2001;15945-15952.
53. Rebecchi M.J., Pentyala S.N. Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol. Rev. 80:2000;1291-1335.
54. Klemke R.L., Cai S., Giannini A.L., Gallagher P.J., de Lanerolle P., Cheresh D.A. Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137:1997;481-492.
55. Ma Z., Webb D.J., Jo M., Gonias S.L. Endogenously produced urokinase-type plasminogen activator is a major determinant of the basal level of activated ERK/MAP kinase and prevents apoptosis in MDA-MB-231 breast cancer cells. J. Cell Sci. 114:2000;3387-3396.
56. Shliom O., Huang M., Sachais B., Kuo A., Weisel J.W., Nagaswami C., Nassar T., Bdeir K., Hiss E., Gawlak S., Harris S., Mazar A., Higazi A.A. Novel interactions between urokinase and its receptor. J. Biol. Chem. 275:2000;24304-24312.
57. Koopman J.L., Slomp J., de Bart A.C., Quax P.H., Verheijen J.H. Mitogenic effects of urokinase on melanoma cells are independent of high affinity binding to the urokinase receptor. J. Biol. Chem. 273:1998;33267-33272.
58. 2+ store depletion in rat liver epithelial cells. Am. J. Physiol. 276:1999;C221-C230.
59. Choudhury G.G., Karamitsos C., Hernandez J., Gentilini A., Bardgette J., Abboud H.E. PI-3-kinase and MAPK regulate mesangial cell proliferation and migration in response to PDGF. Am. J. Physiol. 273:1997;F931-F938.
60. Imai Y., Clemmons D.R. Roles of phosphatidylinositol 3-kinase and mitogen-activated protein kinase pathways in stimulation of vascular smooth muscle cell migration and deoxyriboncleic acid synthesis by insulin-like growth factor-I. Endocrinology. 140:1999;4228-4235.
61. Irving J.A., Lala P.K. Functional role of cell surface integrins on human trophoblast cell migration regulation by TGF-beta, IGF-II, and IGFBP-1 . Exp. Cell Res. 217:1995;419-427.
62. Xu G., Guimond M.J., Chakraborty C., Lala P.K. Control of proliferation, migration and invasiveness of the human trophoblast by decorin, a decidual product. Biol. Reprod. 67:2002;681-689.
63. Graham C.H., Lala P.K. Mechanisms of control of trophoblast invasion in situ. J. Physiol. 148:1991;228-234.
64. Lala P.K., Hamilton G.S. Growth factors, proteases and protease inhibitors in the maternal-fetal dialogue. Placenta. 17:1996;545-555.
65. Lindoff C., Astedt B. Plasminogen activator of urokinase type and its inhibitor of placental type in hypertensive pregnancies and in intrauterine growth retardation possible markers of placental function . Am. J. Obstet Gynecol. 178:1994;1067-1071.