Placenta-derived extracellular vesicles: their cargo and possible functions
Mary Familari A C , Tina Cronqvist B , Zahra Masoumi B and Stefan R. Hansson BA School of Biosciences, University of Melbourne, Parkville, Vic. 3010, Australia.
B Lund University, Department of Clinical Sciences, Lund, Obstetrics and Gynecology, Klinikgatan 28, 221 85 Lund, Sweden.
C Corresponding author. Email: m.familari@unimelb.edu.au
Reproduction, Fertility and Development 29(3) 433-447 https://doi.org/10.1071/RD15143
Submitted: 11 April 2015 Accepted: 29 August 2015 Published: 28 September 2015
Abstract
The literature on extracellular vesicles consists of rapidly expanding and often contradictory information. In this paper we attempt to review what is currently known regarding extracellular vesicles released specifically from human placental syncytiotrophoblast cells with a focus on the common but complex pregnancy-associated syndrome pre-eclampsia, where the level of syncytiotrophoblast extracellular vesicle release is significantly increased. We review common methods for syncytiotrophoblast extracellular vesicle derivation and isolation and we discuss the cargo of syncytiotrophoblast extracellular vesicles including proteins, RNA and lipids and their possible functions. A meta-analysis of available trophoblast-derived extracellular vesicle proteomic datasets revealed only three proteins in common: albumin, fibronectin-1 and plasminogen activator inhibitor-1, suggesting some variability in vesicle cargo, most likely reflecting stage and cell type of origin. We discuss the possible sources of variability that may have led to the low number of common markers, which has led us to speculate that markers and density in common use may not be strict criteria for identifying and isolating placenta-derived exosomes.
Additional keywords: endothelial cells, exosomes, lipidomics, meta-analysis, proteomics, syncytiotrophoblast cells, transcriptome, trophoblast cells.
References
Andreu, Z., and Yanez-Mo, M. (2014). Tetraspanins in extracellular vesicle formation and function. Front. Immunol. 5, 442.| Tetraspanins in extracellular vesicle formation and function.Crossref | GoogleScholarGoogle Scholar |
Askelund, K. J., and Chamley, L. W. (2011). Trophoblast deportation part I: review of the evidence demonstrating trophoblast shedding and deportation during human pregnancy. Placenta 32, 716–723.
| Trophoblast deportation part I: review of the evidence demonstrating trophoblast shedding and deportation during human pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MfktlWrug%3D%3D&md5=890e75bf8fdbdd8e2b721b59581c347dCAS |
Atay, S., Gercel-Taylor, C., Kesimer, M., and Taylor, D. D. (2011). Morphologic and proteomic characterisation of exosomes released by cultured extravillous trophoblast cells. Exp. Cell Res. 317, 1192–1202.
| Morphologic and proteomic characterisation of exosomes released by cultured extravillous trophoblast cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkt12ntrY%3D&md5=704bd9535925038c36ad2d9bf07c693eCAS |
Baig, S., Lim, J. Y., Fernandis, A. Z., Wenk, M. R., Kale, A., Su, L. L., Biswas, A., Vasoo, S., Shui, G., and Choolani, M. (2013). Lipidomic analysis of human placental syncytiotrophoblast microvesicles in adverse pregnancy outcomes. Placenta 34, 436–442.
| Lipidomic analysis of human placental syncytiotrophoblast microvesicles in adverse pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsFyhur8%3D&md5=33fef1b55a0bc11e4cf44120bca74636CAS |
Baig, S., Kothandaraman, N., Manikandan, J., Rong, L., Ee, K. H., Hill, J., Lai, C. W., Tan, W. Y., Yeoh, F., Kale, A., Su, L. L., Biswas, A., Vasoo, S., and Choolani, M. (2014). Proteomic analysis of human placental syncytiotrophoblast microvesicles in pre-eclampsia. Clin. Proteomics 11, 40.
| Proteomic analysis of human placental syncytiotrophoblast microvesicles in pre-eclampsia.Crossref | GoogleScholarGoogle Scholar |
Bellingham, S. A., Coleman, B. M., and Hill, A. F. (2012). Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res. 40, 10 937–10 949.
| Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhslalu7fM&md5=68680cacf39a28b33909b20220412de7CAS |
Booth, A. M., Fang, Y., Fallon, J. K., Yang, J. M., Hildreth, J. E., and Gould, S. J. (2006). Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J. Cell Biol. 172, 923–935.
| Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKisLs%3D&md5=4c188996e715b2a6d6e31b1e90bc7729CAS |
Buchan, J. R. (2014). mRNP granules. Assembly, function and connections with disease. RNA Biol. 11, 1019–1030.
| mRNP granules. Assembly, function and connections with disease.Crossref | GoogleScholarGoogle Scholar |
Bustelo, X. R., Sauzeau, V., and Berenjeno, I. M. (2007). GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo. BioEssays 29, 356–370.
| GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkslSls7c%3D&md5=3ce5155ee4bfc8f574d9099325d3fd14CAS |
Camerini, S., and Mauri, P. (2015). The role of protein and peptide separation before mass spectrometry analysis in clinical proteomics. J. Chromatogr. A 1381, 1–12.
| The role of protein and peptide separation before mass spectrometry analysis in clinical proteomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFygsbzF&md5=cdc169c57d25667bbb2e3e9349e8f6c7CAS |
Centlow, M., Carninci, P., Nemeth, K., Mezey, E., Brownstein, M., and Hansson, S. R. (2008). Placental expression profiling in pre-eclampsia: local overproduction of haemoglobin may drive pathological changes. Fertil. Steril. 90, 1834–1843.
| Placental expression profiling in pre-eclampsia: local overproduction of haemoglobin may drive pathological changes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOhurrL&md5=ba4140424cf3c6ee365f09081aa0b97cCAS |
Centlow, M., Junus, K., Nystrom, H., May, K., Larsson, I., Olsson, M. G., Akerstrom, B., Sager, R., Schneider, H., and Hansson, S. R. (2009). Perfusion of the human placenta with red blood cells and xanthine oxidase mimics pre-eclampsia in vitro. Z. Geburtshilfe Neonatol. 213, 89–95.
| Perfusion of the human placenta with red blood cells and xanthine oxidase mimics pre-eclampsia in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MvivVSqtw%3D%3D&md5=c5a1cae91503461726ec31151de8f758CAS |
Chaiworapongsa, T., Chaemsaithong, P., Yeo, L., and Romero, R. (2014). Pre-eclampsia part 1: current understanding of its pathophysiology. Nat. Rev. Nephrol. 10, 466–480.
| Pre-eclampsia part 1: current understanding of its pathophysiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFCkt7%2FI&md5=d4778e0106b2f3f9392be6a7d6d6674bCAS |
Chen, D. B., and Wang, W. (2013). Human placental microRNAs and pre-eclampsia. Biol. Reprod. 88, 130.
| Human placental microRNAs and pre-eclampsia.Crossref | GoogleScholarGoogle Scholar |
Chen, L. M., Liu, B., Zhao, H. B., Stone, P., Chen, Q., and Chamley, L. (2010). IL-6, TNF alpha and TGF beta promote nonapoptotic trophoblast deportation and subsequently cause endothelial cell activation. Placenta 31, 75–80.
| IL-6, TNF alpha and TGF beta promote nonapoptotic trophoblast deportation and subsequently cause endothelial cell activation.Crossref | GoogleScholarGoogle Scholar |
Choi, D. S., Kim, D. K., Kim, Y. K., and Gho, Y. S. (2013). Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics 13, 1554–1571.
| Proteomics, transcriptomics and lipidomics of exosomes and ectosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjslajt7Y%3D&md5=4daa1dbe17613cb3261bb475077937e1CAS |
Cirelli, N., Lebrun, P., Gueuning, C., Delogne-Desnoeck, J., Vanbellinghen, A. M., Graff, G., and Meuris, S. (2001). Physiological concentrations of albumin stimulate chorionic gonadotrophin and placental lactogen release from human term placental explants. Hum. Reprod. 16, 441–448.
| Physiological concentrations of albumin stimulate chorionic gonadotrophin and placental lactogen release from human term placental explants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXislCgtL4%3D&md5=9d629a8be80a78afd5fcbab94c39566aCAS |
Collart, M. A., and Panasenko, O. O. (2012). The Ccr4–NOT complex. Gene 492, 42–53.
| The Ccr4–NOT complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1KrurrK&md5=d1e62645e4ae2e219943b9e3dafce709CAS |
Colombo, M., Moita, C., van Niel, G., Kowal, J., Vigneron, J., Benaroch, P., Manel, N., Moita, L. F., Thery, C., and Raposo, G. (2013). Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J. Cell Sci. 126, 5553–5565.
| Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFyksLY%3D&md5=372317fd651ddc94ef9efe635f46107dCAS |
Cronqvist, T., Salje, K., Familari, M., Guller, S., Schneider, H., Gardiner, C., Sargent, I. L., Redman, C. W., Morgelin, M., Akerstrom, B., Gram, M., and Hansson, S. R. (2014). Syncytiotrophoblast vesicles show altered microRNA and haemoglobin content after ex vivo perfusion of placentas with haemoglobin to mimic pre-eclampsia. PLoS One 9, e90020.
| Syncytiotrophoblast vesicles show altered microRNA and haemoglobin content after ex vivo perfusion of placentas with haemoglobin to mimic pre-eclampsia.Crossref | GoogleScholarGoogle Scholar |
Cronqvist, T., Tannetta, D., Hansson, S. R., and Familari, M. (2015). Primary endothelial cell uptake of syncytiotrophoblast vesicles from normal and pre-eclamptic placentas. J. Extracellular Vesicles 4, P-XVI-7.
Delorme-Axford, E., Donker, R. B., Mouillet, J. F., Chu, T., Bayer, A., Ouyang, Y., Wang, T., Stolz, D. B., Sarkar, S. N., Morelli, A. E., Sadovsky, Y., and Coyne, C. B. (2013). Human placental trophoblasts confer viral resistance to recipient cells. Proc. Natl. Acad. Sci. USA 110, 12 048–12 053.
| Human placental trophoblasts confer viral resistance to recipient cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1emurfJ&md5=2e19272f83a565800e030d0720978214CAS |
Donker, R. B., Mouillet, J. F., Chu, T., Hubel, C. A., Stolz, D. B., Morelli, A. E., and Sadovsky, Y. (2012). The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes. Mol. Hum. Reprod. 18, 417–424.
| The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVeisr3K&md5=2804c49e54f500b2f5ac2d741f3fdf5fCAS |
Douglas, G. C., Moreira-Cali, P., King, B. F., and Lonnerdal, B. (1998). Uptake of 125I-labelled alpha2-macroglobulin and albumin by human placental syncytiotrophoblast in vitro. J. Cell. Biochem. 68, 427–435.
| Uptake of 125I-labelled alpha2-macroglobulin and albumin by human placental syncytiotrophoblast in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXpsFGgtA%3D%3D&md5=0fa38ce857266817b59d786bf8dd4a7dCAS |
Dragovic, R. A., Gardiner, G., Brooks, A. S., Tannetta, D. S., Ferguson, D. J. P., Hole, P., Carr, B., Redman, C. W. G., Harris, A. L., Dobson, P. J., Harrison, P., and Sargent, I. L. (2011). Sizing and phenotyping of cellular vesicles using nanoparticle tracking analysis. Nanomedicine 7, 780–788.
| 1:CAS:528:DC%2BC38XhtFWmurw%3D&md5=5ca84891de35fad8d856ae7a1ccc1600CAS |
Dragovic, R. A., Southcombe, J. H., Tannetta, D. S., Redman, C. W., and Sargent, I. L. (2013). Multicolour flow cytometry and nanoparticle tracking analysis of extracellular vesicles in the plasma of normal pregnant and pre-eclamptic women. Biol. Reprod. 89, 151.
| Multicolour flow cytometry and nanoparticle tracking analysis of extracellular vesicles in the plasma of normal pregnant and pre-eclamptic women.Crossref | GoogleScholarGoogle Scholar |
Dragovic, R. A., Collett, G. P., Hole, P., Ferguson, D. J. P., Redman, C. W., Sargent, I. L., and Tannetta, D. S (2015). Isolation of syncytiotrophoblast microvesicles and exosomes and their characterisation by multicolour flow cytometry and fluorescence nanoparticle tracking analysis. Methods. , .
| Isolation of syncytiotrophoblast microvesicles and exosomes and their characterisation by multicolour flow cytometry and fluorescence nanoparticle tracking analysis.Crossref | GoogleScholarGoogle Scholar |
Epiney, M., Ribaux, P., Arboit, P., Irion, O., and Cohen, M. (2012). Comparative analysis of secreted proteins from normal and preeclamptic trophoblastic cells using proteomic approaches. J. Proteomics 75, 1771–1777.
| Comparative analysis of secreted proteins from normal and preeclamptic trophoblastic cells using proteomic approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt1yiu74%3D&md5=448e2ffe2f3c03ababf72ba44c3f4257CAS |
Erickson, H. P. (2009). Size and shape of protein molecules at the nanometre level determined by sedimentation, gel filtration and electron microscopy. Biol. Proced. Online 11, 32–51.
| Size and shape of protein molecules at the nanometre level determined by sedimentation, gel filtration and electron microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXislOqt7s%3D&md5=2374f604090704a6231a3f52e0695c10CAS |
Fackler, O. T., and Grosse, R. (2008). Cell motility through plasma membrane blebbing. J. Cell Biol. 181, 879–884.
| Cell motility through plasma membrane blebbing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXns1yms7o%3D&md5=6aab01b4717560af1ead8db7834baa5fCAS |
Germain, S. J., Sacks, G. P., Sooranna, S. R., Sargent, I. L., and Redman, C. W. (2007). Systemic inflammatory priming in normal pregnancy and pre-eclampsia: the role of circulating syncytiotrophoblast microparticles. J. Immunol. 178, 5949–5956.
| Systemic inflammatory priming in normal pregnancy and pre-eclampsia: the role of circulating syncytiotrophoblast microparticles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktlWhsbk%3D&md5=0eb6f8a4ae7fdf27e07801c268e86a53CAS |
Goulopoulou, S., and Davidge, S. T. (2015). Molecular mechanisms of maternal vascular dysfunction in pre-eclampsia. Trends Mol. Med. 21, 88–97.
| Molecular mechanisms of maternal vascular dysfunction in pre-eclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitF2jsrk%3D&md5=e806930c8687a38ea75a9b690f8c08a9CAS |
Graham, C. H., Hawley, T. S., Hawley, R. G., MacDougall, J. R., Kerbel, R. S., Khoo, N., and Lala, P. K. (1993). Establishment and characterisation of first-trimester human trophoblast cells with extended lifespan. Exp. Cell Res. 206, 204–211.
| Establishment and characterisation of first-trimester human trophoblast cells with extended lifespan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1OisL0%3D&md5=3f875f981d94bbcf9d51c92d8df13433CAS |
Guller, S., Ma, Y., Malek, A., Di Santo, S., and Schneider, H. (2007). Differential release of plasminogen activator inhibitors (PAIs) during dual perfusion of human placenta: implications in pre-eclampsia. Placenta 28, 278–285.
| Differential release of plasminogen activator inhibitors (PAIs) during dual perfusion of human placenta: implications in pre-eclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFGmsb0%3D&md5=1fd6e51c67b4264e31c5755218efd78fCAS |
Guller, S., Buhimschi, C. S., Ma, Y. Y., Huang, S. T., Yang, L., Kuczynski, E., Zambrano, E., Lockwood, C. J., and Buhimschi, I. A. (2008). Placental expression of ceruloplasmin in pregnancies complicated by severe pre-eclampsia. Lab. Invest. 88, 1057–1067.
| Placental expression of ceruloplasmin in pregnancies complicated by severe pre-eclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFGhs7jI&md5=257b481c5ff59675a109c0462e5cb224CAS |
Guller, S., Tang, Z., Ma, Y. Y., Di Santo, S., Sager, R., and Schneider, H. (2011). Protein composition of microparticles shed from human placenta during placental perfusion: potential role in angiogenesis and fibrinolysis in pre-eclampsia. Placenta 32, 63–69.
| Protein composition of microparticles shed from human placenta during placental perfusion: potential role in angiogenesis and fibrinolysis in pre-eclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2isr%2FP&md5=5253633410c955ecf714d3bab8ebda34CAS |
Gupta, A. K., Holzgreve, W., Huppertz, B., Malek, A., Schneider, H., and Hahn, S. (2004). Detection of fetal DNA and RNA in placenta-derived syncytiotrophoblast microparticles generated in vitro. Clin. Chem. 50, 2187–2190.
| Detection of fetal DNA and RNA in placenta-derived syncytiotrophoblast microparticles generated in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsVWms7w%3D&md5=e677e52958757de996f12cac3407ba62CAS |
György, B., Hung, M. E., Breakefield, X. O., and Leonard, J. N. (2015). Therapeutic applications of extracellular vesicles: clinical promise and open questions. Annu. Rev. Pharmacol. Toxicol. 55, 439–464.
| Therapeutic applications of extracellular vesicles: clinical promise and open questions.Crossref | GoogleScholarGoogle Scholar |
Hannan, N. J., Paiva, P., Dimitriadis, E., and Salamonsen, L. A. (2010). Models for study of human embryo implantation: choice of cell lines? Biol. Reprod. 82, 235–245.
| Models for study of human embryo implantation: choice of cell lines?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVSns7k%3D&md5=8e65308e439cb9b6950cf40b05cf6b62CAS |
Hansson, S. R., Nääv, A., and Erlandsson, L. (2014). Oxidative stress in pre-eclampsia and the role of free fetal haemoglobin. Front. Physiol. 5, 516.
Hayashi, M., Sakata, M., Takeda, T., Tahara, M., Yamamoto, T., Minekawa, R., Isobe, A., Tasaka, K., and Murata, Y. (2005). Hypoxia upregulates hypoxia-inducible factor-1alpha expression through RhoA activation in trophoblast cells. J. Clin. Endocrinol. Metab. 90, 1712–1719.
| Hypoxia upregulates hypoxia-inducible factor-1alpha expression through RhoA activation in trophoblast cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisVOhtb4%3D&md5=0c2d64c87b3f8fe0a1eb0849cbc9eee3CAS |
Huppertz, B., Weiss, G., and Moser, G. (2014). Trophoblast invasion and oxygenation of the placenta: measurements versus presumptions. J. Reprod. Immunol. 101–102, 74–79.
| Trophoblast invasion and oxygenation of the placenta: measurements versus presumptions.Crossref | GoogleScholarGoogle Scholar |
Johnstone, R. M., Adam, M., Hammond, J. R., Orr, L., and Turbide, C. (1987). Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem. 262, 9412–9420.
| 1:CAS:528:DyaL2sXksFKmsbo%3D&md5=4c642a18aa9326dbc3fd31c3dfc4f2caCAS |
Kaitu’u-Lino, T. J., Tong, S., Beard, S., Hastie, R., Tuohey, L., Brownfoot, F., Onda, K., and Hannan, N. J. (2014). Characterisation of protocols for primary trophoblast purification, optimised for functional investigation of sFlt-1 and soluble endoglin. Pregnancy Hypertens. 4, 287–295.
| Characterisation of protocols for primary trophoblast purification, optimised for functional investigation of sFlt-1 and soluble endoglin.Crossref | GoogleScholarGoogle Scholar |
Kalra, H., Simpson, R. J., Ji, H., Aikawa, E., Altevogt, P., Askenase, P., Bond, V. C., Borras, F. E., Breakefield, X., Budnik, V., Buzas, E., Camussi, G., Clayton, A., Cocucci, E., Falcon-Perez, J. M., Gabrielsson, S., Gho, Y. S., Gupta, D., Harsha, H. C., Hendrix, A., Hill, A. F., Inal, J. M., Jenster, G., Kramer-Albers, E. M., Lim, S. K., Llorente, A., Lotvall, J., Marcilla, A., Mincheva-Nilsson, L., Nazarenko, I., Nieuwland, R., Nolte-’t Hoen, E. N., Pandey, A., Patel, T., Piper, M. G., Pluchino, S., Prasad, T. S., Rajendran, L., Raposo, G., Record, M., Reid, G. E., Sanchez-Madrid, F., Schiffelers, R. M., Siljander, P., Stensballe, A., Stoorvogel, W., Taylor, D., Thery, C., Valadi, H., van Balkom, B. W., Vazquez, J., Vidal, M., Wauben, M. H., Yanez-Mo, M., Zoeller, M., and Mathivanan, S. (2012). Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 10, e1001450.
| Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsFSrtw%3D%3D&md5=04800c77cc9532150d480bed63a91cacCAS |
Kertesz, Z., Hurst, G., Ward, M., Willis, A. C., Caro, H., Linton, E. A., Sargent, I. L., and Redman, C. W. (1999). Purification and characterisation of a complex from placental syncytiotrophoblast microvillous membranes which inhibits the proliferation of human umbilical vein endothelial cells. Placenta 20, 71–79.
| Purification and characterisation of a complex from placental syncytiotrophoblast microvillous membranes which inhibits the proliferation of human umbilical vein endothelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXht1Glurk%3D&md5=0f1ed201e7d50b8ab7bf6d5cca1c8eebCAS |
Kleinrouweler, C. E., van Uitert, M., Moerland, P. D., Ris-Stalpers, C., van der Post, J. A., and Afink, G. B. (2013). Differentially expressed genes in the pre-eclamptic placenta: a systematic review and meta-analysis. PLoS One 8, e68991.
| Differentially expressed genes in the pre-eclamptic placenta: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFymt7zL&md5=fc0fa4785e9a69012ca90de9ca734f4fCAS |
Knight, M., Redman, C. W., Linton, E. A., and Sargent, I. L. (1998). Shedding of syncytiotrophoblast microvilli into the maternal circulation in pre-eclamptic pregnancies. Br. J. Obstet. Gynaecol. 105, 632–640.
| Shedding of syncytiotrophoblast microvilli into the maternal circulation in pre-eclamptic pregnancies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czgvFeluw%3D%3D&md5=f6a87c7f16cc5dd79d3ea9b6ab6e7ec2CAS |
Korkes, H. A., Sass, N., Moron, A. F., Camara, N. O., Bonetti, T., Cerdeira, A. S., Da Silva, I. D., and De Oliveira, L. (2014). Lipidomic assessment of plasma and placenta of women with early-onset pre-eclampsia. PLoS One 9, e110747.
| Lipidomic assessment of plasma and placenta of women with early-onset pre-eclampsia.Crossref | GoogleScholarGoogle Scholar |
Kumpel, B., King, M. J., Sooranna, S., Jackson, D., Eastlake, J., Cheng, R., and Johnson, M. (2008). Phenotype and mRNA expression of syncytiotrophoblast microparticles isolated from human placenta. Ann. N. Y. Acad. Sci. 1137, 144–147.
| Phenotype and mRNA expression of syncytiotrophoblast microparticles isolated from human placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtF2qurrO&md5=5b8af2b810d9e38db7934590013acf0eCAS |
Lai, C. P., Mardini, O., Ericsson, M., Prabhakar, S., Maguire, C. A., Chen, J. W., Tannous, B. A., and Breakefield, X. O. (2014). Dynamic biodistribution of extracellular vesicles in vivo using a multimodal imaging reporter. ACS Nano 8, 483–494.
| Dynamic biodistribution of extracellular vesicles in vivo using a multimodal imaging reporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsl2qtA%3D%3D&md5=2759c283acb31747689720d77ba554a5CAS |
Lambot, N., Lybaert, P., Boom, A., Delogne-Desnoeck, J., Vanbellinghen, A. M., Graff, G., Lebrun, P., and Meuris, S. (2006). Evidence for a clathrin-mediated recycling of albumin in human term placenta. Biol. Reprod. 75, 90–97.
| Evidence for a clathrin-mediated recycling of albumin in human term placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmtlyisb8%3D&md5=133cf5d08085ea0bb43abb31ef59322cCAS |
Larance, M., and Lamond, A. I. (2015). Multidimensional proteomics for cell biology. Nat. Rev. Mol. Cell Biol. 16, 269–280.
| Multidimensional proteomics for cell biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmtlKlsLc%3D&md5=0023d0f91afc0cf2ceb45b58d49cee18CAS |
Leventis, P. A., and Grinstein, S. (2010). The distribution and function of phosphatidylserine in cellular membranes. Annu. Rev. Biophys. 39, 407–427.
| The distribution and function of phosphatidylserine in cellular membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotFKjsb8%3D&md5=92d95aca7560c9e6fde1c7d7e544b0e8CAS |
Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15–20.
| Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXot1ChsA%3D%3D&md5=44a3d5c90dc15489f5799fb0dc07f423CAS |
Li, M., Zeringer, E., Barta, T., Schageman, J., Cheng, A., and Vlassov, A. V. (2014). Analysis of the RNA content of the exosomes derived from blood serum and urine and its potential as biomarkers. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130502.
| Analysis of the RNA content of the exosomes derived from blood serum and urine and its potential as biomarkers.Crossref | GoogleScholarGoogle Scholar |
Liu, S., Cui, H., Li, Q., Zhang, L., Na, Q., and Liu, C. (2014). RhoGDI2 is expressed in human trophoblasts and involved in their migration by inhibiting the activation of RAC1. Biol. Reprod. 90, 88.
| RhoGDI2 is expressed in human trophoblasts and involved in their migration by inhibiting the activation of RAC1.Crossref | GoogleScholarGoogle Scholar |
Longtine, M. S., and Nelson, D. M. (2011). Placental dysfunction and fetal programming: the importance of placental size, shape, histopathology and molecular composition. Semin. Reprod. Med. 29, 187–196.
| Placental dysfunction and fetal programming: the importance of placental size, shape, histopathology and molecular composition.Crossref | GoogleScholarGoogle Scholar |
Lumbreras, B., Porta, M., Marquez, S., Pollán, M., Parker, L. A., and Hernández-Aguado, I. (2009). Sources of error and its control in studies on the diagnostic accuracy of ‘-omics’ technologies. Proteomics Clin. Appl. 3, 173–184.
| Sources of error and its control in studies on the diagnostic accuracy of ‘-omics’ technologies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXislWiu7w%3D&md5=bd4d6216ef097ef28da2b67220add8ffCAS |
Luo, S. S., Ishibashi, O., Ishikawa, G., Ishikawa, T., Katayama, A., Mishima, T., Takizawa, T., Shigihara, T., Goto, T., Izumi, A., Ohkuchi, A., Matsubara, S., Takeshita, T., and Takizawa, T. (2009). Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol. Reprod. 81, 717–729.
| Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFyhsLnP&md5=f0d01e4eb62706fda1773cf01fefb512CAS |
Mathivanan, S., Fahner, C. J., Reid, G. E., and Simpson, R. J. (2012). ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res. 40, D1241–D1244.
| ExoCarta 2012: database of exosomal proteins, RNA and lipids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs12htbzJ&md5=04ce4123b81ad9c712caac3ef49d1146CAS |
May, K., Rosenlof, L., Olsson, M. G., Centlow, M., Morgelin, M., Larsson, I., Cederlund, M., Rutardottir, S., Siegmund, W., Schneider, H., Akerstrom, B., and Hansson, S. R. (2011). Perfusion of human placenta with haemoglobin introduces pre-eclampsia-like injuries that are prevented by alpha1-microglobulin. Placenta 32, 323–332.
| Perfusion of human placenta with haemoglobin introduces pre-eclampsia-like injuries that are prevented by alpha1-microglobulin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs12ju7g%3D&md5=2f65ec67396e5826f0f4ac7e5627b815CAS |
Melo, S. A., Luecke, L. B., Kahlert, C., Fernandez, A. F., Gammo, S. T., Kaye, J., LeBle, V. S., Mittendorf, E. A., Weitz, J., Rahbari, N., Reissfelder, C., Pilarsky, C., Fraga, M. F., Piwnica-Worms, D., and Kalluri, R. (2015). Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature 523, 177–182.
| Glypican-1 identifies cancer exosomes and detects early pancreatic cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1entr7E&md5=ee585f3a3ab6fc75a48734b6544ab840CAS |
Messerli, M., May, K., Hansson, S. R., Schneider, H., Holzgreve, W., Hahn, S., and Rusterholz, C. (2010). Feto–maternal interactions in pregnancies: placental microparticles activate peripheral blood monocytes. Placenta 31, 106–112.
| Feto–maternal interactions in pregnancies: placental microparticles activate peripheral blood monocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlGjs7c%3D&md5=d133bb834da11e7c437a8db3027c9bd0CAS |
Mincheva-Nilsson, L., and Baranov, V. (2014). Placenta-derived exosomes and syncytiotrophoblast microparticles and their role in human reproduction: immune modulation for pregnancy success. Am. J. Reprod. Immunol. 72, 440–457.
| Placenta-derived exosomes and syncytiotrophoblast microparticles and their role in human reproduction: immune modulation for pregnancy success.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslSrs73N&md5=e1c10b2854042369ca886e7594665827CAS |
Mitchell, S. F., and Parker, R. (2014). Principles and properties of eukaryotic mRNPs. Mol. Cell 54, 547–558.
| Principles and properties of eukaryotic mRNPs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXoslyls7o%3D&md5=8ad3dfbc5021b33fe1e7d15aaa5221aeCAS |
Moisan, E., and Girard, D. (2006). Cell surface expression of intermediate filament proteins vimentin and lamin B1 in human neutrophil spontaneous apoptosis. J. Leukoc. Biol. 79, 489–498.
| Cell surface expression of intermediate filament proteins vimentin and lamin B1 in human neutrophil spontaneous apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKnu74%3D&md5=ea960e56605603de723ba2bf976cba9eCAS |
Morales-Prieto, D. M., Chaiwangyen, W., Ospina-Prieto, S., Schneider, U., Herrmann, J., Gruhn, B., and Markert, U. R. (2012). MicroRNA expression profiles of trophoblastic cells. Placenta 33, 725–734.
| MicroRNA expression profiles of trophoblastic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1egt7nM&md5=bfdfea87eaba661fc49ae75c9833edbdCAS |
Morales-Prieto, D. M., Ospina-Prieto, S., Schmidt, A., Chaiwangyen, W., and Markert, U. R. (2014). Elsevier Trophoblast Research Award Lecture: origin, evolution and future of placenta miRNAs. Placenta 35, S39–S45.
| Elsevier Trophoblast Research Award Lecture: origin, evolution and future of placenta miRNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtlartQ%3D%3D&md5=077bd6526aa81941a20e39ee960b4269CAS |
Myatt, L., Muralimanoharan, S., and Maloyan, A. (2014). Effect of pre-eclampsia on placental function: influence of sexual dimorphism, microRNAs and mitochondria. Adv. Exp. Med. Biol. 814, 133–146.
| Effect of pre-eclampsia on placental function: influence of sexual dimorphism, microRNAs and mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmvVWjtbY%3D&md5=c7b1ff7992d4c9f2bbabe2337ae35c72CAS |
Nelson, D. M., Johnson, R. D., Smith, S. D., Anteby, E. Y., and Sadovsky, Y. (1999). Hypoxia limits differentiation and upregulates expression and activity of prostaglandin H synthase 2 in cultured trophoblast from term human placenta. Am. J. Obstet. Gynecol. 180, 896–902.
| Hypoxia limits differentiation and upregulates expression and activity of prostaglandin H synthase 2 in cultured trophoblast from term human placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivFeksLY%3D&md5=b06f7f42b8af441742210ce4e4c7e418CAS |
Nolte-’t Hoen, E. N., Buermans, H. P., Waasdorp, M., Stoorvogel, W., Wauben, M. H., and ‘t Hoen, P. A. (2012). Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res. 40, 9272–9285.
| Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFWktbjL&md5=4bf6fa43a6b451e961694c871829bc37CAS |
Quesenberry, P. J., and Aliotta, J. M. (2010). Cellular phenotype switching and microvesicles. Adv. Drug Deliv. Rev. 62, 1141–1148.
| Cellular phenotype switching and microvesicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVGitb%2FO&md5=9f5465de101ac1125dbb99ecb64ca674CAS |
Raimondo, F., Morosi, L., Chinello, C., Magni, F., and Pitto, M. (2011). Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery. Proteomics 11, 709–720.
| Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVSnurk%3D&md5=9ca95fe1b43b7c63c919d963efcda43aCAS |
Raposo, G., and Stoorvogel, W. (2013). Extracellular vesicles: exosomes, microvesicles and friends. J. Cell Biol. 200, 373–383.
| Extracellular vesicles: exosomes, microvesicles and friends.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtFCnsbk%3D&md5=256ffbaa78563000c8f93850112d94e0CAS |
Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A., and Ratajczak, M. Z. (2006). Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20, 1487–1495.
| Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVSjsrk%3D&md5=12f9e51a89da6b9991a511e1279364f7CAS |
Record, M. (2014). Intercellular communication by exosomes in placenta: a possible role in cell fusion? Placenta 35, 297–302.
| Intercellular communication by exosomes in placenta: a possible role in cell fusion?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXksleksbg%3D&md5=db45cc4f67bec6259846d5a94a4002bdCAS |
Redman, C. W., and Sargent, I. L. (2007). Microparticles and immunomodulation in pregnancy and pre-eclampsia. J. Reprod. Immunol. 76, 61–67.
| Microparticles and immunomodulation in pregnancy and pre-eclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlals7zI&md5=ec14ffb9e89ba92406705d00bc068554CAS |
Redman, C. W., and Sargent, I. L. (2009). Placental stress and pre-eclampsia: a revised view. Placenta 30, S38–S42.
| Placental stress and pre-eclampsia: a revised view.Crossref | GoogleScholarGoogle Scholar |
Redman, C. W., Tannetta, D. S., Dragovic, R. A., Gardiner, C., Southcombe, J. H., Collett, G. P., and Sargent, I. L. (2012). Review: does size matter? Placental debris and the pathophysiology of pre-eclampsia. Placenta 33, S48–S54.
| Review: does size matter? Placental debris and the pathophysiology of pre-eclampsia.Crossref | GoogleScholarGoogle Scholar |
Roberts, J. M., and Escudero, C. (2012). The placenta in pre-eclampsia. Pregnancy Hypertens. 2, 72–83.
| The placenta in pre-eclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmslOrtbY%3D&md5=01d5128266374cc0ac911f3aa2cc444cCAS |
Roberts, J. M., Taylor, R. N., Musci, T. J., Rodgers, G. M., Hubel, C. A., and McLaughlin, M. K. (1989). Pre-eclampsia: an endothelial cell disorder. Am. J. Obstet. Gynecol. 161, 1200–1204.
| Pre-eclampsia: an endothelial cell disorder.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c%2Fnt1artQ%3D%3D&md5=ec18f8f0f5af5ee3faee504f4ccae64dCAS |
Rodgers, G. M., Taylor, R. N., and Roberts, J. M. (1988). Pre-eclampsia is associated with a serum factor cytotoxic to human endothelial cells. Am. J. Obstet. Gynecol. 159, 908–914.
| Pre-eclampsia is associated with a serum factor cytotoxic to human endothelial cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M%2Fitlekuw%3D%3D&md5=de02f7e1d4ea6fb4e84f8ba4fd4536a1CAS |
Salomon, C., Kobayashi, M., Ashman, K., Sobrevia, L., Mitchell, M. D., and Rice, G. E. (2013a). Hypoxia-induced changes in the bioactivity of cytotrophoblast-derived exosomes. PLoS One 8, e79636.
| Hypoxia-induced changes in the bioactivity of cytotrophoblast-derived exosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslyls7vE&md5=a104cebbd42d7368bdaebcf396df59deCAS |
Salomon, C., Ryan, J., Sobrevia, L., Kobayashi, M., Ashman, K., Mitchell, M., and Rice, G. E. (2013b). Exosomal signalling during hypoxia mediates microvascular endothelial cell migration and vasculogenesis. PLoS One 8, e68451.
| Exosomal signalling during hypoxia mediates microvascular endothelial cell migration and vasculogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFOmt7rP&md5=74e3d29f63f0a94afd37bccba3a080d0CAS |
Salomon, C., Torres, M. J., Kobayashi, M., Scholz-Romero, K., Sobrevia, L., Dobierzewska, A., Illanes, S. E., Mitchell, M. D., and Rice, G. E. (2014a). A gestational profile of placental exosomes in maternal plasma and their effects on endothelial cell migration. PLoS One 9, e98667.
| A gestational profile of placental exosomes in maternal plasma and their effects on endothelial cell migration.Crossref | GoogleScholarGoogle Scholar |
Salomon, C., Yee, S., Scholz-Romero, K., Kobayashi, M., Vaswani, K., Kvaskoff, D., Illanes, S. E., Mitchell, M. D., and Rice, G. E. (2014b). Extravillous trophoblast cell-derived exosomes promote vascular smooth muscle cell migration. Front. Pharmacol. 5, 175.
| Extravillous trophoblast cell-derived exosomes promote vascular smooth muscle cell migration.Crossref | GoogleScholarGoogle Scholar |
Sarker, S., Scholz-Romero, K., Perez, A., Illanes, S. E., Mitchell, M. D., Rice, G. E., and Salomon, C. (2014). Placental-derived exosomes continuously increase in maternal circulation over the first trimester of pregnancy. J. Translational Medicine 12, 204.
| Placental-derived exosomes continuously increase in maternal circulation over the first trimester of pregnancy.Crossref | GoogleScholarGoogle Scholar |
Schageman, J., Zeringer, E., Li, M., Barta, T., Lea, K., Gu, J., Magdaleno, S., Setterquist, R., and Vlassov, A. V. (2013). The complete exosome workflow solution: from isolation to characterisation of RNA cargo. BioMed Res. Int. 2013, 253957.
| The complete exosome workflow solution: from isolation to characterisation of RNA cargo.Crossref | GoogleScholarGoogle Scholar |
Schey, K. L., Luther, J. M., and Rose, K. L. (2015). Proteomics characterisation of exosome cargo. Methods. , .
| Proteomics characterisation of exosome cargo.Crossref | GoogleScholarGoogle Scholar |
Schneider, H., and Huch, A. (1985). Dual in vitro perfusion of an isolated lobe of human placenta: method and instrumentation. Contrib. Gynecol. Obstet. 13, 40–47.
| 1:STN:280:DyaL2M3gt1ygtw%3D%3D&md5=940a8aec74b6f4a9a2ac1d7929dbd5c3CAS |
Shiokawa, S., Iwashita, M., Akimoto, Y., Nagamatsu, S., Sakai, K., Hanashi, H., Kabir-Salmani, M., Nakamura, Y., Uehata, M., and Yoshimura, Y. (2002). Small guanosine triphospatase RhoA and Rho-associated kinase as regulators of trophoblast migration. J. Clin. Endocrinol. Metab. 87, 5808–5816.
| Small guanosine triphospatase RhoA and Rho-associated kinase as regulators of trophoblast migration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpslWmsrY%3D&md5=fbce62cdbd432b8cc935ffa71876e483CAS |
Shomer, E., Katzenell, S., Zipori, Y., Sammour, R. N., Isermann, B., Brenner, B., and Aharon, A. (2013). Microvesicles of women with gestational hypertension and pre-eclampsia affect human trophoblast fate and endothelial function. Hypertension 62, 893–898.
| Microvesicles of women with gestational hypertension and pre-eclampsia affect human trophoblast fate and endothelial function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1amt7bO&md5=3b92a76a16eaa1b9dc930b324a5aca05CAS |
Smárason, A. K., Sargent, I. L., Starkey, P. M., and Redman, C. W. (1993). The effect of placental syncytiotrophoblast microvillous membranes from normal and pre-eclamptic women on the growth of endothelial cells in vitro. Br. J. Obstet. Gynaecol. 100, 943–949.
| The effect of placental syncytiotrophoblast microvillous membranes from normal and pre-eclamptic women on the growth of endothelial cells in vitro.Crossref | GoogleScholarGoogle Scholar |
Smith, N. C., Brush, M. G., and Luckett, S. (1974). Preparation of human placental villous surface membrane. Nature 252, 302–303.
| Preparation of human placental villous surface membrane.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2M%2FksFeltw%3D%3D&md5=15f0e9c5ebde6886b2a6b191dd56eb5dCAS |
Soo, C. Y., Song, Y., Zheng, Y., Campbell, E. C., Riches, A. C., Gunn-Moore, F., and Powis, S. J. (2012). Nanoparticle tracking analysis monitors microvesicle and exosome secretion from immune cells. Immunology 136, 192–197.
| Nanoparticle tracking analysis monitors microvesicle and exosome secretion from immune cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntV2nsbc%3D&md5=9ad0e4bbe0efe43d71ace8221bc7ff3cCAS |
Southcombe, J., Tannetta, D., Redman, C., and Sargent, I. (2011). The immunomodulatory role of syncytiotrophoblast microvesicles. PLoS One 6, e20245.
| The immunomodulatory role of syncytiotrophoblast microvesicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFCrtr4%3D&md5=827776cd3fd8819743b344b7c04176abCAS |
Straszewski-Chavez, S. L., Abrahams, V. M., Alvero, A. B., Aldo, P. B., Ma, Y., Guller, S., Romero, R., and Mor, G. (2009). The isolation and characterisation of a novel telomerase-immortalised first-trimester trophoblast cell line, Swan 71. Placenta 30, 939–948.
| The isolation and characterisation of a novel telomerase-immortalised first-trimester trophoblast cell line, Swan 71.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlCms73I&md5=076aeff7926af2e1ad3f3f785c4fb8aaCAS |
Taglauer, E. S., Wilkins-Haug, L., and Bianchi, D. W. (2014). Review: cell-free fetal DNA in the maternal circulation as an indication of placental health and disease. Placenta 35, S64–S68.
| Review: cell-free fetal DNA in the maternal circulation as an indication of placental health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjt1GktQ%3D%3D&md5=05ee5d6eb1bed0f0d046dd041da69149CAS |
Tannetta, D. S., Dragovic, R. A., Gardiner, C., Redman, C. W., and Sargent, I. L. (2013). Characterisation of syncytiotrophoblast vesicles in normal pregnancy and pre-eclampsia: expression of Flt-1 and endoglin. PLoS One 8, e56754.
| Characterisation of syncytiotrophoblast vesicles in normal pregnancy and pre-eclampsia: expression of Flt-1 and endoglin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsF2isbc%3D&md5=58f554e9ee4305b721363578b7c7bccdCAS |
Teng, Y. C., Lin, Q. D., Lin, J. H., Ding, C. W., and Zuo, Y. (2009). Coagulation and fibrinolysis related cytokine imbalance in pre-eclampsia: the role of placental trophoblasts. J. Perinat. Med. 37, 343–348.
| Coagulation and fibrinolysis related cytokine imbalance in pre-eclampsia: the role of placental trophoblasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFehsLs%3D&md5=5273655b89611eb79912353ac6167c35CAS |
Théry, C., Zitvogel, L., and Amigorena, S. (2002). Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2, 569–579.
Thomsen, L. C. (2015). Pre-eclampsia: specific genetic risk factors and shared predisposition with cardiovascular disease. Ph.D. Thesis. University of Bergen, Norway.
Tong, M., and Chamley, L. W. (2015). Placental extracellular vesicles and feto–maternal communication. Cold Spring Harb. Perspect. Med. 5, a023028.
| Placental extracellular vesicles and feto–maternal communication.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MrgvFKgtg%3D%3D&md5=00918b96828ff8f0b96594a4074b42d5CAS |
Tranquilli, A. L., Dekker, G., Magee, L., Roberts, J., Sibai, B. M., Steyn, W., Zeeman, G. G., and Brown, M. A. (2014). The classification, diagnosis and management of the hypertensive disorders of pregnancy: a revised statement from the ISSHP. Pregnancy Hypertens. 4, 97–104.
| 1:STN:280:DC%2BC2Mbms1WhsQ%3D%3D&md5=f4f6084abf9e615d812424f41d03b148CAS |
Tsochandaridis, M., Nasca, L., Toga, C., and Levy-Mozziconacci, A. (2015). Circulating microRNAs as clinical biomarkers in the predictions of pregnancy complications. BioMed Res. Int. 2015, 294954.
| Circulating microRNAs as clinical biomarkers in the predictions of pregnancy complications.Crossref | GoogleScholarGoogle Scholar |
van Meeteren, L. A., and ten Dijke, P. (2012). Regulation of endothelial cell plasticity by TGF-beta. Cell Tissue Res. 347, 177–186.
| Regulation of endothelial cell plasticity by TGF-beta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xkslequw%3D%3D&md5=c89db840981464e7cd3116d5e742794bCAS |
Vlassov, A. V., Magdaleno, S., Setterquist, R., and Conrad, R. (2012). Exosomes: current knowledge of their composition, biological functions and diagnostic and therapeutic potentials. Biochim. Biophys. Acta 1820, 940–948.
| Exosomes: current knowledge of their composition, biological functions and diagnostic and therapeutic potentials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnslSjt7c%3D&md5=457f18c796b7594d1fe8861b1a1a44c4CAS |
Zhang, J., Li, S., Li, L., Li, M., Guo, C., Yao, J., and Mi, S. (2015). Exosome and exosomal microRNA: trafficking, sorting and function. Genomics Proteomics Bioinformatics 13, 17–24.
| Exosome and exosomal microRNA: trafficking, sorting and function.Crossref | GoogleScholarGoogle Scholar |