Syncytial Knots (Tenney-Parker Changes) in the Human Placenta
Open accessAbstract
Syncytiotrophoblast is the multinucleated epithelium of the placenta. Although many nuclei are dispersed within the syncytioplasm, others are aggregated into specializations referred to as true and false syncytial knots, and syncytial sprouts. Nuclei within true knots display highly condensed chromatin and are thought to be aged and effete. True knots increase in frequency with gestational age. Excessive formation (Tenney-Parker change) is associated with placental pathology, and a knotting index is used to assess severity. However, this index is potentially confounded by the creation of artifactual appearances (false knots) through tangential sectioning. In addition, knots must be distinguished from syncytial sprouts, which are markers of trophoblast proliferation. Here, we distinguish between sprouts, true knots, and false knots using serial sections and perform IHC for proliferating cell nuclear antigen, upstream binding factor, RNA polymerase II, and 8-oxo-deoxyguanosine as markers of recent incorporation, transcriptional activity, and oxidative damage. Villous explants were exposed to hydrogen peroxide to test the relationship between transcriptional activity and oxidative damage. Sprouts and false knots were found to contain recently incorporated and transcriptionally active nuclei. By contrast, most nuclei within true knots are negative for transcriptional markers but positive for 8-oxo-deoxyguanosine. In vitro, we observed a negative correlation between transcriptional activity and oxidative damage. These findings demonstrate that true knots contain effete damaged nuclei and provide IHC markers for their identification.
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Nuclei that display particularly condensed chromatin aggregate in syncytial knots and are transcriptionally inactive.
“Nuclei that display particularly condensed chromatin aggregate in syncytial knots and are transcriptionally inactive (188).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [188]
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Cites
The Pathology of the Human Placenta
Benirschke, K., & Driscoll, S. G. (1967) · Springer eBooks · doi:10.1007/978-1-4612-9809-0 · Cited by 2,123 · see citing works
Oxidative stress in the placenta
Myatt, L., & Cui, X.-L. (2004) · Histochemistry and Cell Biology · doi:10.1007/s00418-004-0677-x · Cited by 803 · see citing works
Mayer, C., & Grummt, I. (2006) · Oncogene · doi:10.1038/sj.onc.1209883 · Cited by 568 · see citing works
Pathology of the Human Placenta
Benirschke, K., Burton, G. J., & Baergen, R. N. (2012) · doi:10.1007/978-3-642-23941-0 · Cited by 502 · see citing works
Self-citationAssays for 8-hydroxy-2′-deoxyguanosine: A biomarker of in vivo oxidative DNA damage
Shigenaga, M. K., & Ames, B. N. (1991) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(91)90078-h · Cited by 365 · see citing works
Huppertz, B., Kingdom, J. C., Caniggia, I., Desoyé, G., Black, S., Korr, H., & Kaufmann, P. (2003) · Placenta · doi:10.1053/plac.2002.0903 · Cited by 288 · see citing works
Human placental explants in culture: Approaches and assessments
Miller, R. K., Genbačev, O., Turner, M. A., Aplin, J., Caniggia, I., & Huppertz, B. (2004) · Placenta · doi:10.1016/j.placenta.2004.10.002 · Cited by 257 · see citing works
Investigating RNA polymerase II carboxyl‐terminal domain (CTD) phosphorylation
Palancade, B., & Bensaude, O. (2003) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2003.03794.x · Cited by 250 · see citing works
Formation of Syncytial Knots is Increased by Hyperoxia, Hypoxia and Reactive Oxygen Species
Heazell, A. E. P., Moll, S. J., Jones, C. J. P., Baker, P. N., & Crocker, I. P. (2007) · Placenta · doi:10.1016/j.placenta.2006.10.007 · Cited by 204 · see citing works
Mayhew, T. M., Leach, L., McGee, R., Ismail, W. W., Myklebust, R., & Lammiman, M. (1999) · Placenta · doi:10.1053/plac.1999.0399 · Cited by 167 · see citing works
Syncytial Knots, Sprouts, Apoptosis, and Trophoblast Deportation from the Human Placenta
Burton, G. J., & Jones, C. (2009) · Taiwanese Journal of Obstetrics and Gynecology · doi:10.1016/s1028-4559(09)60032-2 · Cited by 167 · see citing works
Self-citationVillous sprouting: fundamental mechanisms of human placental development
Castellucci, M. (2000) · Human Reproduction Update · doi:10.1093/humupd/6.5.485 · Cited by 166 · see citing works
Loukeris, K., Sela, R., & Baergen, R. N. (2009) · Pediatric and Developmental Pathology · doi:10.2350/09-08-0692-oa.1 · Cited by 166 · see citing works
The placenta in toxemia of pregnancy
Tenney, B., & Parker, F. (1940) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(40)90458-6 · Cited by 150 · see citing works
Watson, A. L., Skepper, J. N., Jauniaux, E. R. M., & Burton, G. J. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.5.4830 · Cited by 149 · see citing works
Self-citationSimpson, R. A., Mayhew, T. M., & Barnes, P. (1992) · Placenta · doi:10.1016/0143-4004(92)90055-x · Cited by 141 · see citing works
Interpretation of syncytial sprouts and bridges in the human placenta
Cantle, S. J., Kaufmann, P., Luckhardt, M., & Schweikhart, G. (1987) · Placenta · doi:10.1016/0143-4004(87)90046-4 · Cited by 111 · see citing works
Syncytial knots and intervillous bridges in the human placenta: an ultrastructural study.
Jones, C., & Fox, H. (1977) · PubMed · Cited by 98 · see citing works
THE SIGNIFICANCE OF VILLOUS SYNCYTIAL KNOTS IN THE HUMAN PLACENTA
Fox, H. (1965) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1965.tb01469.x · Cited by 94 · see citing works
Evidence for Transcriptional Activity in the Syncytiotrophoblast of the Human Placenta
Ellery, P., Cindrová‐Davies, T., Jauniaux, E. R. M., Ferguson‐Smith, A. C., & Burton, G. J. (2009) · Placenta · doi:10.1016/j.placenta.2009.01.002 · Cited by 82 · see citing works
Self-citationCross-sectional features and three-dimensional structure of human placental Villi
Kaufmann, P., Luckhardt, M., Schweikhart, G., & Cantle, S. J. (1987) · Placenta · doi:10.1016/0143-4004(87)90047-6 · Cited by 80 · see citing works
Watson, A. L. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.5.1697 · Cited by 80 · see citing works
Trophoblast Apoptosis in Placentas from Pregnancies Complicated by Preeclampsia
Tomaš, S. Z., Prusac, I. K., Roje, D., & Tadin, I. (2011) · Gynecologic and Obstetric Investigation · doi:10.1159/000320289 · Cited by 75 · see citing works
Palmer, M. E., Watson, A. L., & Burton, G. J. (1997) · Human Reproduction · doi:10.1093/humrep/12.2.379 · Cited by 69 · see citing works
Self-citationAlia, K. Z. M., Burton, G. J., Morad, N., & Ali, M. E. (1996) · Placenta · doi:10.1016/s0143-4004(96)80018-x · Cited by 64 · see citing works
Self-citationThe fine structure of the human placental villus as revealed by scanning electron microscopy.
Burton, G. J. (1987) · PubMed · Cited by 59 · see citing works
Self-citationPre-eclampsia: Etiology and Clinical Practice
Lyall, F., & Belfort, M. A. (2007) · Medical Entomology and Zoology · Cited by 57 · see citing works
DNA CONTENT OF PLACENTAL NUCLEI
Galton, M. (1962) · The Journal of Cell Biology · doi:10.1083/jcb.13.2.183 · Cited by 57 · see citing works
Mayhew, T. M., & Simpson, R. A. (1994) · Placenta · doi:10.1016/s0143-4004(05)80185-7 · Cited by 51 · see citing works
Full-term birth weight and placental morphology at high and low altitude
Khalid, M. E. M., Ali, M. E., & Ali, K. Z. M. (1997) · International Journal of Gynecology & Obstetrics · doi:10.1016/s0020-7292(97)00067-2 · Cited by 51 · see citing works
Spectrum of changes in placenta in toxemia of pregnancy
Narasimha, A., & Vasudeva, D. (2011) · Indian Journal of Pathology and Microbiology · doi:10.4103/0377-4929.77317 · Cited by 50 · see citing works
Fogarty, N. M. E., Mayhew, T. M., Ferguson‐Smith, A. C., & Burton, G. J. (2011) · Journal of Anatomy · doi:10.1111/j.1469-7580.2011.01417.x · Cited by 49 · see citing works
Self-citationKar, M., Ghosh, D., & Sengupta, J. (2007) · Human Reproduction · doi:10.1093/humrep/dem284 · Cited by 43 · see citing works
Burton, G. J. (1986) · PubMed · Cited by 33 · see citing works
Self-citationThe RNA Polymerase I Transcription Factor UBF Is the Product of a Primary Response Gene
Glibetić, M., Taylor, L. J., Larson, D. E., Hannan, R. D., Sells, B. H., & Rothblum, L. I. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.9.4209 · Cited by 31 · see citing works
Expression of proliferationg cell nuclear antigen during the cell cycle of human diploid fibroblasts
Stewart, C., & Dell’Orco, R. T. (1992) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/bf02631094 · Cited by 14 · see citing works
[Molecular structures in DNA replication].
Tsurimoto, T. (1999) · PubMed · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
Self-citationIFPA Senior Award Lecture: Making sense of pre-eclampsia – Two placental causes of preeclampsia?
Redman, C. W. G., Sargent, I. L., & Staff, A. C. (2014) · Placenta · doi:10.1016/j.placenta.2013.12.008 · Cited by 437 · see citing works
Syncytiotrophoblast stress in preeclampsia: the convergence point for multiple pathways
Redman, C. W. G., Staff, A. C., & Roberts, J. M. (2021) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2020.09.047 · Cited by 411 · see citing works
Type I interferons instigate fetal demise after Zika virus infection
Yockey, L. J., Jurado, K. A., Arora, N., Millet, A., Rakib, T., Milano, K. M., Hastings, A. K., Fikrig, E., Kong, Y., Horváth, T. L., et al. (2018) · Science Immunology · doi:10.1126/sciimmunol.aao1680 · Cited by 253 · see citing works
McElwain, C. J., Tuboly, E., McCarthy, F. P., & McCarthy, C. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00655 · Cited by 224 · see citing works
The Placental Basis of Fetal Growth Restriction
Zur, R. L., Kingdom, J. C., Parks, W. T., & Hobson, S. R. (2019) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/j.ogc.2019.10.008 · Cited by 214 · see citing works
HYPOXIA AND REPRODUCTIVE HEALTH: Oxygen and development of the human placenta
Burton, G. J., Cindrová‐Davies, T., Yung, H. W., & Jauniaux, E. R. M. (2020) · Reproduction · doi:10.1530/rep-20-0153 · Cited by 188 · see citing works
Self-citationEarly human trophoblast development: from morphology to function
Gauster, M., Moser, G., Wernitznig, S., Kupper, N., & Huppertz, B. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04377-0 · Cited by 159 · see citing works
Roland, C., Hu, J. J., Ren, C., Chen, H., Li, J., Varvoutis, M. S., Leaphart, L. W., Byck, D. B., Zhu, X., & Jiang, S. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2069-x · Cited by 156 · see citing works
Mitochondrial – Endoplasmic reticulum interactions in the trophoblast: Stress and senescence
Burton, G. J., Yung, H. W., & Murray, A. J. (2016) · Placenta · doi:10.1016/j.placenta.2016.04.001 · Cited by 155 · see citing works
Self-citationJones, H. N., Olbrych, S. K., Smith, K. L., Cnota, J. F., Habli, M. A., Ramos-Gonzales, O., Owens, K. J., Hinton, A. C., POLZIN, W. J., Muglia, L. J., et al. (2015) · Placenta · doi:10.1016/j.placenta.2015.08.003 · Cited by 121 · see citing works
Mayhew, T. M. (2014) · Placenta · doi:10.1016/j.placenta.2014.01.011 · Cited by 113 · see citing works
Placenta-Derived Exosomes as a Modulator in Maternal Immune Tolerance During Pregnancy
Bai, K., Li, X., Zhong, J., Ng, E. H. Y., Yeung, W. S. B., Lee, C., & Chiu, P. C. N. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.671093 · Cited by 106 · see citing works
Immune and Apoptosis Mechanisms Regulating Placental Development and Vascularization in Preeclampsia
Raguema, N., Moustadraf, S., & Bertagnolli, M. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00098 · Cited by 103 · see citing works
Wang, M., Liu, Y., Sun, R., Liu, F.-T., Li, J., Long, Y., Zhang, J., Xie, X., Li, D., Wang, Y., et al. (2024) · Nature Genetics · doi:10.1038/s41588-023-01647-w · Cited by 98 · see citing works
Foetoplacental communication via extracellular vesicles in normal pregnancy and preeclampsia
Chiarello, D. I., Salsoso, R., Toledo, F., Mate, A., Vázquez, C. M., & Sobrevía, L. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.12.002 · Cited by 86 · see citing works
Farah, O., Nguyen, C., Tekkatte, C., & Parast, M. M. (2020) · Placenta · doi:10.1016/j.placenta.2020.02.007 · Cited by 81 · see citing works
Placental Mitochondrial Function and Dysfunction in Preeclampsia
Jahan, F., Vasam, G., Green, A. E., Bainbridge, S. A., & Menzies, K. J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24044177 · Cited by 81 · see citing works
Placental hypoxia: The lesions of maternal malperfusion
Parks, W. T. (2014) · Seminars in Perinatology · doi:10.1053/j.semperi.2014.10.003 · Cited by 75 · see citing works
Cell dynamics in human villous trophoblast
Aplin, J., & Jones, C. J. P. (2021) · Human Reproduction Update · doi:10.1093/humupd/dmab015 · Cited by 68 · see citing works
Placental pathology of the third trimester pregnant women from COVID-19
Gao, L., Ren, J., Xu, L., Ke, X., Xiong, L., Tian, X., Fan, C., Yan, H., & Yuan, J. (2021) · Diagnostic Pathology · doi:10.1186/s13000-021-01067-6 · Cited by 65 · see citing works
Gibbs, I., Leavey, K., Benton, S. J., Grynspan, D., Bainbridge, S. A., & Cox, B. (2018) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2018.10.003 · Cited by 65 · see citing works
Omics Approaches to Study Formation and Function of Human Placental Syncytiotrophoblast
Jaremek, A., Jeyarajah, M. J., Bhattad, G. J., & Renaud, S. J. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.674162 · Cited by 59 · see citing works
Broady, A. J., Loichinger, M. H., Ahn, H. J., Davy, P. M. C., Allsopp, R., & Bryant‐Greenwood, G. D. (2016) · Placenta · doi:10.1016/j.placenta.2016.12.018 · Cited by 58 · see citing works
Fogarty, N. M. E., Burton, G. J., & Ferguson-Smith, A. C. (2015) · Placenta · doi:10.1016/j.placenta.2015.05.006 · Cited by 57 · see citing works
Self-citationSIRT1 regulates trophoblast senescence in premature placental aging in preeclampsia
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Syncytiotrophoblast stress in early onset preeclampsia: The issues perpetuating the syndrome
Carrasco‐Wong, I., Aguilera-Olguín, M., Escalona‐Rivano, R., Chiarello, D. I., Barragán‐Zuñiga, L. J., Sosa‐Macías, M., Galavíz-Hernández, C., Martín, S. S., & Gutiérrez, J. (2021) · Placenta · doi:10.1016/j.placenta.2021.05.002 · Cited by 48 · see citing works
Alqudah, A. M., Eastwood, K., Jerotić, D., Todd, N., Hoch, D., McNally, R. P., Obradović, D. D., Dugalić, S., Hunter, A. J., Holmes, V. A., et al. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.650328 · Cited by 46 · see citing works
United we stand not dividing: The syncytiotrophoblast and cell senescence
Goldman-Wohl, D., & Yagel, S. (2014) · Placenta · doi:10.1016/j.placenta.2014.03.012 · Cited by 44 · see citing works
Gusella, A., Martignoni, G., & Giacometti, C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25147886 · Cited by 41 · see citing works
Obiri, D., Erskine, I. J., Oduro, D., Kusi, K. A., Amponsah, J. A., Gyan, B. A., Adu‐Bonsaffoh, K., & Ofori, M. F. (2020) · Scientific Reports · doi:10.1038/s41598-020-64736-4 · Cited by 39 · see citing works
Placental Senescence and the Two‐Stage Model of Preeclampsia
Sugulle, M., Fiskå, B. S., Jacobsen, D. P., Fjeldstad, H. E., & Staff, A. C. (2024) · American Journal of Reproductive Immunology · doi:10.1111/aji.13904 · Cited by 38 · see citing works
Dutta, A., Khramtsova, G. F., Brito, K., Alexander, D., Mueller, A., Chinthala, S., Adu, D., Ibigbami, T., Olamijulo, J., Odetunde, A., et al. (2017) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2017.11.091 · Cited by 38 · see citing works
García‐Honduvilla, N., Ortega, M. A., Asúnsolo, Á., Álvarez-Rocha, M. J., Romero, B., León-Luis, J. A. D., Álvarez‐Mon, M., & Buján, J. (2018) · Human Pathology · doi:10.1016/j.humpath.2018.03.022 · Cited by 37 · see citing works
Zur, R. L., McLaughlin, K., Aalto, L., Jiang, Y., Huszti, E., Parks, W. T., & Kingdom, J. C. (2024) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.17837 · Cited by 35 · see citing works
Manifestations of Hypoxia in the Second and Third Trimester Placenta
Parks, W. T. (2017) · Birth Defects Research · doi:10.1002/bdr2.1143 · Cited by 31 · see citing works
Systemic and placental α-klotho: Effects of preeclampsia in the last trimester of gestation
Loichinger, M. H., Towner, D., Thompson, K. S., Ahn, H. J., & Bryant‐Greenwood, G. D. (2016) · Placenta · doi:10.1016/j.placenta.2016.03.004 · Cited by 30 · see citing works
Placentation in the Human and Higher Primates
Burton, G. J., & Jauniaux, E. R. M. (2021) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-030-77360-1_11 · Cited by 28 · see citing works
Self-citationÖlmez, F., Oğlak, S. C., & Özköse, Z. G. (2021) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.15129 · Cited by 28 · see citing works
Eerdekens, A., Verhaeghe, J., Darras, V., Naulaers, G., den Berghe, G. V., Langouche, L., & Vanhole, C. (2019) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2019.1586875 · Cited by 27 · see citing works
Barnea, E. R., Vialard, F., Moindjie, H., Ornaghi, S., Dieudonné, M., & Paidas, M. J. (2015) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2015.06.002 · Cited by 26 · see citing works
Placental pathology predicts infantile neurodevelopment
Ueda, M., Tsuchiya, K. J., Yaguchi, C., Furuta‐Isomura, N., Horikoshi, Y., Matsumoto, M., Suzuki, M., Oda, T., Kawai, K., Itoh, T., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-06300-w · Cited by 25 · see citing works
Calvert, S., Jones, C. J. P., Sibley, C. P., Aplin, J. D., & Heazell, A. E. P. (2013) · Placenta · doi:10.1016/j.placenta.2013.10.001 · Cited by 23 · see citing works
Studies of the dynamics of nuclear clustering in human syncytiotrophoblast
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Castro, K. R., do Prado, K. M., Lorenzon, A. R., Hoshida, M. S., Alves, E. A., Francisco, R. P. V., Zugaib, M., Marques, A. L. X., da Silva, E. C. O., Fonseca, E. J. S., et al. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2021.799653 · Cited by 22 · see citing works
Gardnerella vaginalis infection in pregnancy: Effects on placental development and neonatal outcomes
Wong, Y. P., Cheah, F., Wong, K. K., Shah, S. A., Phon, S. E., Ng, B. K., Lim, P. S., Khong, T. Y., & Tan, G. C. (2022) · Placenta · doi:10.1016/j.placenta.2022.02.018 · Cited by 21 · see citing works
Placental histology in clinically unexpected severe fetal acidemia at term
Avagliano, L., Locatelli, A., Danti, L., Felis, S., Mecacci, F., & Bulfamante, G. (2015) · Early Human Development · doi:10.1016/j.earlhumdev.2015.03.004 · Cited by 21 · see citing works
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Morphomics: An integral part of systems biology of the human placenta
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He, B., Li, Q. Y., Wu, Y., Ruan, J. L., Teng, X., Li, D. J., & Tang, C. L. (2020) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-020-00658-0 · Cited by 19 · see citing works
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Brink, L. T., Roberts, D. J., Wright, C. A., Nel, D. G., Schubert, P. T., Boyd, T. K., Hall, D. R., & Odendaal, H. J. (2022) · Placenta · doi:10.1016/j.placenta.2022.06.004 · Cited by 18 · see citing works
Moodley, M., Moodley, J., & Naicker, T. (2020) · Current Hypertension Reports · doi:10.1007/s11906-020-01047-z · Cited by 18 · see citing works
Cruz-Holguín, V. J., González-García, L. D., Velázquez-Cervantes, M. A., Arévalo-Romero, H., Jesús‐González, L. A. D., Helguera‐Repetto, A. C., León‐Reyes, G., Salazar, M. I., Cedillo‐Barrón, L., & León‐Juárez, M. (2024) · Diseases · doi:10.3390/diseases12030059 · Cited by 17 · see citing works
Apicella, C., Ruano, C. S. M., Jacques, S., Gascoin-Lachambre, G., Méhats, C., Vaiman, D., & Miralles, F. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.633937 · Cited by 17 · see citing works
Yamazaki, K., Masaki, N., Kohmura‐Kobayashi, Y., Yaguchi, C., Hayasaka, T., Itoh, H., Setou, M., & Kanayama, N. (2015) · PLoS ONE · doi:10.1371/journal.pone.0142609 · Cited by 17 · see citing works
Singh, R., Shah, B. L., Allred, E. N., Grzybowski, M., Martin, C. R., Leviton, A., & for the ELGAN Study co-investigators (2016) · Journal of Neonatal-Perinatal Medicine · doi:10.3233/npm-16915100 · Cited by 17 · see citing works
Fjeldstad, H. E., Jacobsen, D. P., Johnsen, G. M., Sugulle, M., Chae, A., Kanaan, S. B., Gammill, H. S., & Staff, A. C. (2023) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.14547 · Cited by 16 · see citing works
Chagas disease affects the human placental barrier’s turnover dynamics during pregnancy
Mezzano, L., Morán, J. P., Moreira‐Espinoza, M. J., Triquell, M. F., Mezzano, J., Díaz-Luján, C. M., & Fretes, R. (2022) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/0074-02760210304 · Cited by 14 · see citing works
Yue, T., Guo, Y., Qi, X., Zheng, W., Zhang, H., Wang, B., Liu, K., Zhou, B., Zeng, X., Ouzhuluobu, et al. (2023) · eLife · doi:10.7554/elife.89004 · Cited by 13 · see citing works
Yaguchi, C., Itoh, H., Tsuchiya, K. J., Furuta‐Isomura, N., Horikoshi, Y., Matsumoto, M., Ferdous, U. J., Muramatsu‐Kato, K., Kohmura‐Kobayashi, Y., Tamura, N., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0194988 · Cited by 13 · see citing works
Microchimerism and pregnancy complications with placental dysfunction
Jacobsen, D. P., Fjeldstad, H. E., Olsen, M. B., Sugulle, M., & Staff, A. C. (2025) · Seminars in Immunopathology · doi:10.1007/s00281-025-01045-w · Cited by 12 · see citing works
Increased Syncytial Knot Formation
Parks, W. T. (2018) · Springer eBooks · doi:10.1007/978-3-319-97214-5_17 · Cited by 12 · see citing works
New Insights Into the Role of Placental Aquaporins and the Pathogenesis of Preeclampsia
Szpilbarg, N., Martínez, N., Paola, M. D., Reppetti, J., Medina, Y., Seyahian, A., Castro-Parodi, M., & Damiano, A. E. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01507 · Cited by 12 · see citing works
Yaguchi, C., Ueda, M., Mizuno, Y., Fukuchi, C., Matsumoto, M., Furuta‐Isomura, N., & Itoh, H. (2024) · Nutrients · doi:10.3390/nu16111786 · Cited by 11 · see citing works
Oğlak, S. C., Aşir, F., Yılmaz, E. Z., Bolluk, G., Korak, T., & Ağaçayak, E. (2024) · Zeitschrift für Geburtshilfe und Neonatologie · doi:10.1055/a-2451-2223 · Cited by 11 · see citing works
Cheah, F., Lai, C., Tan, G. C., Swaminathan, A., Wong, K. K., Wong, Y. P., & Tan, T.-L. (2021) · Frontiers in Pediatrics · doi:10.3389/fped.2020.593802 · Cited by 10 · see citing works
Syncytial nuclei accumulate at the villous surface in IUGR while proliferation is unchanged
Haeussner, E., Schmitz, C., Grynspan, D., von Koch, F. E., & Frank, H. (2017) · Placenta · doi:10.1016/j.placenta.2017.10.004 · Cited by 9 · see citing works
Hermans, S., Pilon, J., Eschweiler, D., Stegmaier, J., Severens‐Rijvers, C., Al‐Nasiry, S., van Zandvoort, M. A. M. J., & Kapsokalyvas, D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043240 · Cited by 9 · see citing works
Working towards a Reproducible Method for Quantifying Placental Syncytial Knots
Senagore, P. K., Holzman, C., Parks, W. T., & Catov, J. M. (2015) · Pediatric and Developmental Pathology · doi:10.2350/15-08-1701-oa.1 · Cited by 9 · see citing works
Jírsová, D., Füssy, Z., Richtová, J., Gruber, A., & Obornı́k, M. (2019) · Microorganisms · doi:10.3390/microorganisms7080240 · Cited by 9 · see citing works
Syncytiotrophoblast Markers Are Downregulated in Placentas from Idiopathic Stillbirths
Vasconcelos, S., Moustakas, I., Branco, M. R., Guimarães, S., Caniçais, C., van der Helm, T., Ramalho, C. M. A., Marques, C. J., Lopes, S. M. C. D. S., & Dória, S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25105180 · Cited by 7 · see citing works
Trophoblast Side-Population Markers are Dysregulated in Preeclampsia and Fetal Growth Restriction
Wong, G. P., Hartmann, S., Simmons, D. G., Ellis, S. L., Nonn, O., Cannon, P., Nguyen, T. V., Nguyen, A., Bartho, L. A., Tong, S. Y. C., et al. (2024) · Stem Cell Reviews and Reports · doi:10.1007/s12015-024-10764-w · Cited by 7 · see citing works
Preeclampsia as a Study Model for Aging: The Klotho Gene Paradigm
Cecati, M., Fumarola, S., Vaiasicca, S., Cianfruglia, L., Vignini, A., Giannubilo, S. R., Emanuelli, M., & Ciavattini, A. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26030902 · Cited by 6 · see citing works
Association of placental pathology and gross morphology with autism spectrum disorders
Soullane, S., Spence, A. R., & Abenhaim, H. A. (2021) · Autism Research · doi:10.1002/aur.2658 · Cited by 6 · see citing works
Falkner, F., Mayer, S. A., Thomas, B., Zimmermann, S. O., Walter, S., Heimel, P., Thiele, W., Sleeman, J. P., Bigdeli, A. K., Kiss, H., et al. (2023) · Bioengineering · doi:10.3390/bioengineering10030337 · Cited by 6 · see citing works
Achieving multifunctionality in a single, tissue-sized syncytiotrophoblast cell in humans
Keenen, M. M., Jalihal, A. P., & Gladfelter, A. S. (2025) · Placenta · doi:10.1016/j.placenta.2025.06.004 · Cited by 5 · see citing works
Feenstra, M. E., Bourgonje, M. F., Bourgonje, A. R., Schoots, M. H., Hillebrands, J., Kobold, A. C. M., Prins, J. R., van Goor, H., Ganzevoort, W., & Gordijn, S. J. (2023) · Antioxidants · doi:10.3390/antiox13010046 · Cited by 5 · see citing works
Moodley, M., Moodley, J., & Naicker, T. (2019) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2019.12.025 · Cited by 5 · see citing works
Yue, T., Guo, Y., Qi, X., Zheng, W., Zhang, H., Wang, B., Liu, K., Zhou, B., Zeng, X., Ouzhuluobu, et al. (2023) · eLife · doi:10.7554/elife.89004.2 · Cited by 5 · see citing works
Three-dimensional microarchitecture of the human placental villous tree in health and disease
Barapatre, N., & Frank, H. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1639740 · Cited by 4 · see citing works
Basic Structure of a Placental Villus
Burton, G. J. (2021) · Springer eBooks · doi:10.1007/978-3-030-84725-8_6 · Cited by 4 · see citing works
Self-citationThe Placenta and Umbilical Cord
Khong, T. Y. (2015) · Springer eBooks · doi:10.1007/978-3-319-19207-9_4 · Cited by 4 · see citing works
Liu, Y., Zhang, L., Gu, M., Xiao, Y., Yu, T., Tao, X., Zhang, Q., Wang, Y., Shen, D. G., & Li, Q. (2024) · Computerized Medical Imaging and Graphics · doi:10.1016/j.compmedimag.2024.102482 · Cited by 3 · see citing works
Cadmium exposure causes trophoblast abnormal syncytization and endocrine dysfunction in preeclampsia
Lin, W., Li, X., An, X., Yin, J., Zhao, Z., Yan, X., Xu, R. H., Zhao, B., Du, X., Cheng, H., et al. (2025) · Reproductive Toxicology · doi:10.1016/j.reprotox.2025.108934 · Cited by 3 · see citing works
Sharma, M., Bhatia, J. K., & Malik, A. (2021) · Medical Journal of Dr D Y Patil Vidyapeeth · doi:10.4103/mjdrdypu.mjdrdypu_179_20 · Cited by 3 · see citing works
Abnormal Microscopic Findings in the Placenta Correlate With the Severity of Fetal Heart Failure
Miyoshi, T., Matsuyama, T., Nakai, M., Miyazato, M., Yoshimatsu, J., Hatakeyama, K., & Hosoda, H. (2022) · Circulation Journal · doi:10.1253/circj.cj-22-0568 · Cited by 3 · see citing works
Xodo, S., Celante, L., Liviero, S., Orsaria, M., Mariuzzi, L., Luca, M. D., Damante, G., Driul, L., Cagnacci, A., Ferino, A., et al. (2023) · Histochemistry and Cell Biology · doi:10.1007/s00418-023-02212-6 · Cited by 3 · see citing works
Ortega, M. A., Fraile‐Μartinez, O., Montero, C. G., Rodriguez-Martín, S., Moñux, R. M. F., Pekarek, L., Bravo, C., León-Luis, J. A. D., Sáez, M. A., Guijarro, L. G., et al. (2023) · PubMed · doi:10.14670/hh-18-605 · Cited by 3 · see citing works
Yue, T., Guo, Y., Qi, X., Zheng, W., Zhang, H., Wang, B., Liu, K., Zhou, B., Zeng, X., Ouzhuluobu, et al. (2024) · eLife · doi:10.7554/elife.89004.3 · Cited by 3 · see citing works
An epigenetic blueprint for placental syncytiotrophoblast development
Renaud, S. J. (2026) · Placenta · doi:10.1016/j.placenta.2026.02.003 · Cited by 2 · see citing works
Placental Anatomy and Physiology
Burton, G. J., Sibley, C. P., & Jauniaux, E. R. M. (2017) · Elsevier eBooks · doi:10.1016/b978-0-323-32108-2.00001-9 · Cited by 2 · see citing works
Self-citationHISTOLOGICAL CHANGES OF PLACENTA IN WOMEN WITH COVID-19
Al-Allaf, L. I. K., & Al-Nauimi, H. A. H. (2023) · Military Medical Science Letters · doi:10.31482/mmsl.2023.005 · Cited by 2 · see citing works
ATIGAN, A., Kılıç, D., Güler, T., & Karakaya, Y. A. (2022) · Journal of Istanbul Faculty of Medicine / İstanbul Tıp Fakültesi Dergisi · doi:10.26650/iuitfd.982918 · Cited by 2 · see citing works
A review of the Evidence for Placental Ageing in Prolonged Pregnancy.
Carroll, A., Lee, S., Desforges, M., & Heazell, A. E. P. (2020) · Medical Research Archives · doi:10.18103/mra.v8i8.2188 · Cited by 2 · see citing works
Quadruplet pregnancy with widespread Tenney-Parker changes: A case report
Thomas, S., Enakpene, C. A., Sanchez, A., & Ventolini, G. (2022) · Journal of Case Reports and Images in Obstetrics and Gynecology · doi:10.5348/100120z08st2022cr · Cited by 1 · see citing works
Transcription Factor EB (TFEB) Expression and Localization in the Third-Trimester Placenta
Giacometti, C., Ambrosi, A., Cavaliere, S., Caliò, A., Mautone, D., & Martignoni, G. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262110294 · Cited by 1 · see citing works
Barapatre, N., & Frank, H. (2026) · Placenta · doi:10.1016/j.placenta.2026.04.011 · Cited by 1 · see citing works
Exposure to Treponema pallidum Alters Villous Histomorphology of Human Placentae
Tetteh‐Quarcoo, P. B., Twasam, J., Ahenkorah, J., Hottor, B. A., Dayie, N. T. K. D., Nyarko, S., Appiah, P. O., Afutu, E., Kotey, F. C. N., Donkor, E. S., et al. (2025) · Acta Microbiologica Hellenica · doi:10.3390/amh70030031 · Cited by 1 · see citing works
- Authors
- Fogarty, N. M. E., Ferguson-Smith, A. C., & Burton, G. J.
- Affiliations
- University of Cambridge (GB)
- Corresponding author
- Burton, Graham J.
- Venue
- The American Journal of Pathology
- Publisher
- Elsevier BV
- Published
- 2013-07
- Volume
- 183
- Issue
- 1
- Pages
- 144-152
- ISSN
- 0002-9440 (ISSN-L)
- OpenAlex
- W1994022598
- Cited by
- 116
- References
- 37
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 13 · 2023: 13 · 2022: 11 · 2021: 16 · 2020: 9 · 2019: 5 · 2018: 7 · 2017: 5 · 2016: 6 · 2015: 12 · 2014: 4 · 2013: 1
- FWCI
- 8.52
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- American Journal Of Pathology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust (095606, 095606/Z/11/Z)
- Medical Research Council (MR/J001597/1)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Gestational Trophoblastic Disease Studies
- Keywords
- syncytial knots, syncytiotrophoblast, placental pathology, proliferating cell nuclear antigen, UBF, RNA polymerase II, oxidative DNA damage, transcriptional activity, hydrogen peroxide, gestational age
- MeSH terms
- 8-Hydroxy-2'-Deoxyguanosine, Cell Nucleus, Deoxyguanosine, Female, Humans, Immunohistochemistry, Placenta, Pregnancy, RNA Polymerase II, Trophoblasts, Biomarkers, Transcriptional Activation, Oxidative Stress, Proliferating Cell Nuclear Antigen, Pol1 Transcription Initiation Complex Proteins
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