Effect of matrigel on human extravillous trophoblasts differentiation: Modulation of protease pattern gene expression

[en] The human placenta is characterized by extensive trophoblast invasion of the uterus. Indeed, extravillous cytotrophoblast cells invade the. decidua and the upper third of uterine spiral arteries in the myometrium. This invasion is reflected in situ by the expression of specific markers. In order to study this invasion process, we have established an in vitro culture model of human extravillous trophoblast isolated from first trimester chorionic villi. The aim of this study was to investigate the effect of a composite matrix, the Matrigel required for the culture of this homogenous population of extravillous trophoblasts (EVCT), on their in vitro differentiation. The effect of Matrigel was studied on different markers characterized by immunocytochemistry and by real-time polymerase chain reaction assay of transcripts. In addition, the expression of 12 different matrix metalloproteases and their inhibitors were investigated. We show that human extravillous cytotrophoblasts acquire an invasive phenotype on Matrigel associated with a specific pattern of protease gene expression. This in vitro model will be of interest to study the cellular mechanisms involved in abnormal trophoblast invasion observed in poor placentation and preeclampsia.

Disciplines :

Anatomy (cytology, histology, embryology...) & physiology

Author, co-author :

Tarrade, A.

Goffin, Frédéric ; Centre Hospitalier Universitaire de Liège - CHU > Gynécologie-Obstétrique CHR

Munaut, Carine ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement

Lai-Kuen, R.

Tricottet, V.

Foidart, Jean-Michel ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique - Labo de biologie des tumeurs et du développement

Vidaud, M.

Frankenne, F.

Evain-Brion, D.

Language :

English

Title :

Effect of matrigel on human extravillous trophoblasts differentiation: Modulation of protease pattern gene expression

Publication date :

November 2002

Journal title :

Biology of Reproduction

ISSN :

0006-3363

eISSN :

1529-7268

Publisher :

Society for the Study of Reproduction, Madison, United States - Wisconsin

Volume :

Issue :

Pages :

1628-1637

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 21 January 2010

Statistics

Number of views

51 (0 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Aplin JD. Implantation, trophoblast differentiation, and haemochorial placentation: Mechanistic evidence in vivo and in vitro. J Cell Sci 1991; 99:681-692.
Redman C, Sargent I, Starkey P. The Human Placenta. Oxford: Blackwell Scientific Publications; 1993.
Kaufmann P, Scheffen I. Placental Development. Orlando, FL: Saunders; 1990.
Loke YW, King A. Human Implantation: Cell Biology and Immunology. Cambridge: Cambridge University Press; 1995.
Albrecht ED, Pepe GJ. Placental steroid hormone biosynthesis in primate pregnancy. Endocr Rev 1990; 11:124-150.
Jameson J, Hollenberg A. Regulation of chorionic gonadotropin gene expression. Endocr Rev 1993; 14:203-221.
Handwerger S. Clinical counterpoint: The physiology of placental lactogen in human pregnancy. Endocr Rev 1991; 12:329-336.
Alsat E, Guibourdenche J, Luton D, Frankenne F, Evain-Brion D. Human placental growth hormone. Am J Obstet Gynecol 1997; 177:1526-1534.
Kaufmann P, Castellucci M. Extravillous trophoblast in the human placenta. Trophoblast Res 1997; 10:21-65.
Damsky C, Fitzgerald M, Fisher S. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester CT differentiation along the invasive pathway, in vivo. J Clin Invest 1992; 89:210-222.
Aplin J. Expression of integrin alpha6-beta4 in human trophoblast and its loss from extravillous cells. Placenta 1993; 14:203-215.
Damsky C, Librach C, Lim K, Fitzgerald M, McMaster M, Janatpour M, Zhou Y, Logan S, Fisher S. Integrin switching regulates normal trophoblast invasion. Development 1994; 120:3657-3666.
Genbacev O, McMaster M, Fisher S. A repertoire of cell cycle regulators whose expression is coordinated with human cytotrophoblast differentiation. Am J Pathol 2000; 157:1337-1351.
Jokhi P, King A, Loke YW. Reciprocal expression of epidermal growth factor receptor and c-erbB2 by non-invasive and invasive human trophoblast populations. Cytokine 1994; 6:433-442.
Mühlhauser J, Crescimanno C, Kaufmann P, Höfler H, Zaccheo D, Castellucci M. Differentiation and proliferation patterns in human trophoblast revealed by c-erbB2 oncogene product and EGF-R. J Histochem Cytochem 1993; 41:165-173.
Cronier L, Bastide B, Hervé J, Deleze J, Malassiné A. Gap junctional communication during human trophoblast differentiation: Influence of human chronic gonadotropin. Endocrinology 1994; 135:402-408.
MacCalman C, Furth E, Omigbodun A, Bronner M, Coutifaris C, Strauss III JE Regulated expression of cadherin-11 in human epithelial cells: A role for cadherin-11 in trophoblast-endometrium interactions? Dev Dyn 1996; 206:201-211.
Loke YW, King A. Immunological aspects of human implantation. J Reprod Fertil Suppl 2000; 55:83-90.
Nagase H, Woessner JJ. Matrix metalloproteinases. J Biol Chem 1999; 274:21491-21494.
Fassina G, Ferrari N, Brigati C, Benelli R, Santi L, Noonan D, Albini A. Tissue inhibitors of metalloproteases: Regulation and biological activities. Clin Exp Metastasis 2000; 18:111-120.
Andreasen P, Kjoller L, Christensen L, Duffy M. The urokinase-type plasminogen activator system in cancer metastasis: A review. Int J Cancer 1997; 72:1-22.
Queenan JJ, Kao L, Arboleda C, Ulloa-Aguirre A, Golos T, Cines D, Strauss Jr. Regulation of urokinase-type plasminogen activator production by cultured human cytotrophoblasts. J Biol Chem 1987; 262:10903-10906.
Zini J, Murray S, Graham C, Lala P, Kariko K, Barnathan E, Mazar A, Henkin J, Cines D, McCrae K. Characterization of urokinase receptor expression by human placental trophoblasts. Blood 1992; 79: 2917-2929.
Bischof P, Haenggeli L, Campana A. Gelatinase and oncofetal fibronectin secretion is dependent on integrin expression on human cytotrophoblasts. Mol Hum Reprod 1995; 10:734-742.
Fisher S, Cui T, Zhang L, Hartman L, Grahl K, Zhang G, Tarpey J, Damsky C. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol 1989; 109:891-902.
Librach CL, Werb Z, Fitzgerald ML, Chiu K, Corwin NM, Esteves RA, Grobelny D, Galardy R, Damsky CH, Fisher SJ. 92 kd type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol 1991; 113:437-449.
Emonard H, Christiane Y, Smet M, Grimaud J, Foidart J. Type IV and interstitial collagenolytic activities in normal and malignant trophoblast cells are specifically regulated by the extracellular matrix. Invasion Metastasis 1990; 10:170-177.
Moll UM, Lane BL. Proteolytic activity of first trimester human placenta: Localization of interstitial collagenase in villous and extravillous trophoblast. Histochemistry 1990; 94:555-560.
Maquoi E, Polette M, Nawrocki B, Bischof P, Noël A, Pintiaux A, Santavicca M, Schaaps J, Pijnenborg R, Birembaut P, Foidard J. Expression of stromelysin-3 in the human placenta and placental bed. Placenta 1997; 18:277-285.
Bjorn S, Hastrup N, Lund L, Dano K, Larsen J, Pyke C. Co-ordinated expression of MMP-2 and its putative activator, MT1-MMP, in human placentation. Mol Hum Reprod 1997; 3:713-723.
Nawrocki B, Polette M, Marchand V, Maquoi E, Beorchia A, Tournier J, Foidart J, Birembaut P. Membrane-type matrix metalloproteinase-1 expression at the site of human placentation. Placenta 1996; 17:565-572.
Huppertz B, Kertschanska S, demir AY, Frank HG, Kaufman P. Immunohistochemistry of MMP, their substrates, and their inhibitors (TIMP) during trophoblast invasion in the human placenta. Cell Tissue Res 1998; 291:133-148.
Feinberg RF, Kao LC, Haimowitz JE, Queenan JT Jr, Wun TC, Strauss JFD, Kliman HJ. Plasminogen activator inhibitor types 1 and 2 in human trophoblasts. PAI-1 is an immunocytochemical marker of invading trophoblasts. Lab Invest 1989; 61:20-26.
Bass K, Li H, Hawkes S, Howard E, Bullen E, Vu T, McMaster M, Janatpour M, Fisher S. Tissue inhibitor of metalloproteinase-3 expression is upregulated during human cytotrophoblast invasion in vitro. Dev Genet 1997; 21:61-67.
Bergers G, Coussens L. Extrinsic regulators of epithelial tumor progression: Metalloproteinases. Curr Opin Genet Dev 2000; 10:120-127.
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 1998; 13:893-906.
Rifkin D, Mazzieri R, Munger J, Noguera I, Sung J. Proteolytic control of growth factor availability. APMIS 1999; 107:80-85.
Loke Y, Burland K. Human trophoblast cells cultured in modified medium and supported by extracellular matrix. Placenta 1988; 9:173-182.
Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest 1996; 97:540-550.
Tarrade A, Lai Kuen R, Malassiné A, Tricottet V, Blain P, Vidaud M, Evain-Brion D. Characterization of human villous and extravillous trophoblasts isolated from first trimester placenta. Lab Invest 2001; 81:1199-1211.
Frendo J, Vidaud M, Guibourdenche J, Luton D, Muller F, Bellet D, Giovagrandi Y, Tarrade A, Porquet D, Blot P, Evain-Brion D. Defect of villous cytotrophoblast differentiation into syncytiotrophoblast in Down's syndrome. J Clin Endocrinol Metab 2000; 85:3700-3707.
Lambert C, Colige A, Munaut C, Lapiere C, Nusgens B. Distinct pathways in the over-expression of matrix metalloproteinases in human fibroblasts by relaxation of mechanical tension. Matrix Biol 2001; 20:397-408.
Lambert C, Colige A, Lapiere C, Nusgens B. Coordinated regulation of procollagens I and III and their post-translational enzymes by dissipation of mechanical tension in human dermal fibroblasts. Eur J Cell Biol 2001; 80:479-485.
Cronier L, Hervé J, Malassiné A. Regulation of gap junctional communication during human trophoblast differentiation. Microsc Res Tech 1997; 38:21-28.
Maquoi E, Van den Brûle FA, Castrononvo V, Foidart JM. Changes in the distribution pattern of galectin-1 and galectin-3 in human placenta correlates with the differentiation pathways of trophoblasts. Placenta 1997; 18:433-439.
Winterhager E, Von Ostau C, Gerke M, Gruemmer R, Traub O, Kaufmann P. Connexin expression patterns in human trophoblast cells during placental development. Placenta 1999; 20:627-638.
Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. Regulation of human placental development by oxygen tension. Science 1997; 277:1669-1672.
Schwarting R. Little missed markers and Ki-67. Lab Invest 1993; 68: 597-599.
Huppertz B, Frank H, Reister F, Kingdom J, Korr H, Kaufmann P. Apoptosis cascade progresses during turnover of human trophoblast: Analysis of villous cytotrophoblast and syncytial fragments in vitro. Lab Invest 1999; 79:1687-1702.
Aplin JD, Haigh T, Lacey H, Chen CP, Jones CJ. Tissue interactions in the control of trophoblast invasion. J Reprod Fertil Suppl 2000; 55:57-64.
Blaschitz A, Lenfant F, Mallet V, Hartmann M, Bensussan A, Geraghty D, Le Bouteiller P, Dohr G. Endothelial cells in chorionic fetal vessels of first trimester placenta express HLA-G. Eur J Immunol 1997; 27:3380-3388.
Chumbley G, King A, Holmes N, Loke Y. In situ hybridization and Northern blot demonstration of HLA-G mRNA in human trophoblast populations by locus-specific oligonucleotide. Hum Immunol 1993; 37:17-22.
Hurskainen T, Hoyhtya M, Tuuttila A, Oikarinen A, Autio-Harmainen H. mRNA expressions of TIMP-1, -2, and -3 and 92-KD type IV collagenase in early human placenta and decidual membrane as studied by in situ hybridization. J Histochem Cytochem 1996; 44:1379-1388.
Polette M, Nawrocki B, Pintiaux A, Massenat C, Maquoi E, Volders L, Schaaps J, Birembaut P, Foidart J. Expression of gelatinases A and B and their tissue inhibitors by cells of early and term human placenta and gestational endometrium. Lab Invest 1994; 71:838-846.
Floridon C, Nielsen O, Holund B, Sunde L, Westergaard J, Thomsen S, Teisner B. Localization and significance of urokinase plasminogen activator and its receptor in placental tissue from intrauterine, ectopic and molar pregnancies. Placenta 1999; 20:711-721.
Hu Z, Liu Y, Liu K, Byrne S, Ny T, Feng Q, Ockleford C. Expression of tissue type and urokinase type plasminogen activators as well as plasminogen activator inhibitor type-1 and type-2 in human and rhesus monkey placenta. J Anat 1999; 194:183-195.
Bischof P, Martelli M, Campana A, Itoh Y, Ogata Y, Nagase H. Importance of matrix metalloproteinases in human trophoblast invasion. Early Pregnancy 1995; 1:263-269.
Vegh G, Selcuk TZ, Fulop V, Genest D, Mok S, Berkowitz R. Matrix metalloproteinases and their inhibitors in gestational trophoblastic diseases and normal placenta. Gynecol Oncol 1999; 75:248-253.
Noël A, Hajitou A, L'Hoir C, Maquoi E, Baramova E, Lewalle J, Remacle A, Kebers F, Brown P, Calberg-Bacq C, Foidart J. Inhibition of stromal matrix metalloproteases: Effects on breast-tumor promotion by fibroblasts. Int J Cancer 1998; 76:267-273.