2018-2019 publications

2018-2019 Publications

Burton, Graham

Cindrova-Davies, T.C., Fogarty, N.M.E., Jones. C.J.P., Kingdom, J. and Burton, G.J. (2018) Evidence of oxidative stress-induced senescence in mature, post-mature and pathological human placentas. Placenta, 68, 15-22.

Than, N.G., Romero, R., Tarca, A.L., Kekesi, K.A., Xu, Y., Xu, Z., Juhasz, K., Bhatti, G., Leavitt, R., Gelencser, Z., Palhalmi, J., Chung, T.H., Gyorffy, B.A., Orosz, L., Demeter, A., Szecsi, A., Hunyadi-Gulyas,  E., Darula, Z., Simor, A.,  Eder, K.,   Szabo, S., Topping, V., El-Azzamy, H., LaJeunesse, C., Balogh, A., Szalai, G., Land, S., Torok, O., Dong, Z., Kovalszky, I., Falus, A., Meiri, H., Draghici, S., Hassan,  S.S., Chaiworapongsa,  T., Krispin,  M., Knöfler,  M., Erez, O., Burton, G.J., Kim, C.J., Juhasz, G. and Papp, Z. (2018) Integrated systems biology approach identifies novel maternal and placental pathways of preeclampsia. Frontiers in Immunology, 9, 1661.

Nuzzo, A-M., Camm, E.J., Sferruzzi-Perri, A.N., Ashmore, T.J., Yung, H.W., Cindrova-Davies, T., Spiroski, A-M., Sutherland, M.R., Logan, A., Austin-Williams, S., Burton,  G.J., Rolfo, A., Todros, T., Murphy, M.P. and Giussani, D.A. (2018) Placental adaptation to early-onset hypoxic pregnancy and mitochondria-targeted antioxidant therapy in the rat. American Journal of Pathology, 188, 2704-2716.

Jauniaux, E., Alfirevic, Z., Bhide, A.G., Burton, G.J., Collins, S.L., Silver, R.; Royal College of Obstetricians and Gynaecologists. (2019) Vasa Paevia: Diagnosis and management: Green-top Guideline No. 27b. British Journal of Obstetrics and Gynaecology, 126, e1-e48.

Jauniaux, E., Alfirevic, Z., Bhide, A.G., Belfort, M.A., Burton, G.J., Collins, S.L., Dornan, S., Jurkovic, D., Kayem, G., Kingdom, J., Silver, R., Sentihes, L.; Royal College of Obstetricians and Gynaecologists. (2019) Placenta Paevia and Placenta Accreta: Diagnosis and management: Green-top Guideline No. 27a. British Journal of Obstetrics and Gynaecology, 126, e49-e61.

Jauniaux, E. and Burton, G.J. (2018) Pathophysiology of Placenta Accreta Spectrum Disorders: a Review of Current Findings. Clinics in Obstetrics and Gynaecology, 61, 743-754.

Turco, M.Y., Gardner, L., Kay, R.G., Hamilton, R.S., Prater, M., Hollinshead, M., McWhinnie, A., Esposito, L., Fernando, R., Skelton, H., Reimann, F., Gribble, F., Sharkey, A., Marsh, S.G.E., O’Rahilly, S., Hemberger, M., Burton, G.J.* and Moffett, A.* (2018) Trophoblast organoids as a model for maternal-fetal interactions during human placentation. Nature, 564, 263-267.

Lee, C-L., Veerbeek, J.H.W., Rana, T.K., van Rijn, B.B., Burton, G.J. and Yung, H.W. (2018) Role of endoplasmic reticulum stress in pro-inflammatory cytokine-mediated inhibition of trophoblast invasion in placenta-related complications of pregnancy. American Journal of Pathology, 189, 467-478.

Lorenzon-Ojea, A.R., Yung, H.W., Burton, G.J. and Bevilacqua, E. (2019) The potential contribution of stromal cell-derived factor 2 (SDF2) in endoplasmic reticulum stress response in severe preeclampsia and labor-onset. Biochimica et Biophysica Acta. Molecular Basis of Disease, epub ahead of print.

Burton, Nicholas (CTR Next Generation Fellow)

Burton NO, Dwivedi VK, Burkhart KB, Kaplan REW, Baugh LR, and Horvitz HR. Neurohormonal signalling via a cytosolic sulfotransferase controls insulin sensitivity of C. elegans. Nature Communications. 2018 Dec 4;

9(1) 5152

Charnock Jones, Steve (Obstetrics Department)

Albrecht, C., Chamley, L., Charnock-Jones, D. S., Collins, S., Fujiwara, H., Golos, T., et al. (2019). IFPA meeting 2018 workshop report II: Abnormally invasive placenta; inflammation and infection; preeclampsia; gestational trophoblastic disease and drug delivery. Placenta, 1–0. http://doi.org/10.1016/j.placenta.2019.02.006

Aye, I. L. M. H., Moraitis, A. A., Stanislaus, D., Charnock-Jones, D. S., & Smith, G. C. S. (2018). Retosiban Prevents Stretch-Induced Human Myometrial Contractility and Delays Labor in Cynomolgus Monkeys. The Journal of Clinical Endocrinology and Metabolism, 103(3), 1056–1067. http://doi.org/10.1210/jc.2017-02195

Bacon, W. A., Hamilton, R. S., Yu, Z., Kieckbusch, J., Hawkes, D., Krzak, A. M., et al. (2018). Single-Cell Analysis Identifies Thymic Maturation Delay in Growth-Restricted Neonatal Mice. Frontiers in Immunology, 9, 332. http://doi.org/10.3389/fimmu.2018.02523

Cater, J. H., Kumita, J. R., Zeineddine Abdallah, R., Zhao, G., Bernardo-Gancedo, A., Henry, A., et al. (2019). Human pregnancy zone protein stabilizes misfolded proteins including preeclampsia- and Alzheimer's-associated amyloid beta peptide. Proceedings of the National Academy of Sciences of the United States of America, 116(13), 201817298–6110. http://doi.org/10.1073/pnas.1817298116

de Goffau, M. C., Lager, S., Salter, S. J., Wagner, J., Kronbichler, A., Charnock-Jones, D. S., et al. (2018). Recognizing the reagent microbiome. Nature Microbiology, 3(8), 851–853. http://doi.org/10.1038/s41564-018-0202-y

Gaccioli, F., Aye, I. L. M. H., Sovio, U., Charnock-Jones, D. S., & Smith, G. C. S. (2018a). Screening for fetal growth restriction using fetal biometry combined with maternal biomarkers. American Journal of Obstetrics and Gynecology, 218(2S), S725–S737. http://doi.org/10.1016/j.ajog.2017.12.002

Gaccioli, F., Sovio, U., Cook, E., Hund, M., Charnock-Jones, D. S., & Smith, G. C. S. (2018b). Screening for fetal growth restriction using ultrasound and the sFLT1/PlGF ratio in nulliparous women: a prospective cohort study, 2(8), 1–13. http://doi.org/10.1016/S2352-4642(18)30129-9

Gong, S., Johnson, M. D., Dopierala, J., Gaccioli, F., Sovio, U., Constância, M., et al. (2018a). Genome-wide oxidative bisulfite sequencing identifies sex-specific methylation differences in the human placenta. Epigenetics : Official Journal of the DNA Methylation Society, 13(3), 1–12. http://doi.org/10.1080/15592294.2018.1429857

Gong, S., Sovio, U., Aye, I. L., Gaccioli, F., Dopierala, J., Johnson, M. D., et al. (2018b). Placental polyamine metabolism differs by fetal sex, fetal growth restriction, and preeclampsia. JCI Insight, 3(13). http://doi.org/10.1172/jci.insight.120723

Hughes, A. E., Sovio, U., Gaccioli, F., Cook, E., Charnock-Jones, D. S., & Smith, G. C. S. (2019). The association between first trimester AFP to PAPP-A ratio and placentally-related adverse pregnancy outcome. Placenta, 81, 25–31. http://doi.org/10.1016/j.placenta.2019.04.005

Jayasuriya, N. A., Hughes, A. E., Sovio, U., Cook, E., Charnock-Jones, D. S., & Smith, G. C. S. (2019). A lower maternal cortisol to cortisone ratio precedes clinical diagnosis of preterm and term preeclampsia by many weeks. The Journal of Clinical Endocrinology and Metabolism. http://doi.org/10.1210/jc.2018-02312

Lager, S., de Goffau, M. C., Sovio, U., Peacock, S. J., Parkhill, J., Charnock-Jones, D. S., & Smith, G. C. S. (2018). Detecting eukaryotic microbiota with single-cell sensitivity in human tissue. Microbiome, 6(1), 151. http://doi.org/10.1186/s40168-018-0529-x

Page-Christiaens, L., & Klein, H.-G. (2018). Noninvasive Prenatal Testing (NIPT). Academic Press.

Pritchard, N., Kaitu'u-Lino, T. J., Gong, S., Dopierala, J., Smith, G. C. S., Charnock-Jones, D. S., & Tong, S. (2018). ELABELA/APELA Levels Are Not Decreased in the Maternal Circulation or Placenta among Women with Preeclampsia. The American Journal of Pathology, 188(8), 1749–1753. http://doi.org/10.1016/j.ajpath.2018.04.008

Sovio, U., McBride, N., Wood, A. M., Masconi, K. L., Cook, E., Gaccioli, F., et al. (2019). 4-Hydroxyglutamate is a novel predictor of pre-eclampsia. International Journal of Epidemiology, 388, 1775. http://doi.org/10.1093/ije/dyz098

Colledge, William (CTR member)

Colucci, Francesco

Spontaneous pulmonary hypertension in genetic mouse models of natural killer cell deficiency.Rätsep MT, Moore SD, Jafri S, Mitchell M, Brady HJM, Mandelboim O, Southwood M, Morrell NW, Colucci F, Ormiston ML.

Am J Physiol Lung Cell Mol Physiol. 2018 Dec 1;315(6):L977-L990. doi: 10.1152/ajplung.00477.2017. Epub 2018 Sep 20.

Report from the Killer-cell Immunoglobulin-like Receptors (KIR) component of the 17th International HLA and Immunogenetics Workshop.

Misra MK, Augusto DG, Martin GM, Nemat-Gorgani N, Sauter J, Hofmann JA, Traherne JA, González-Quezada B, Gorodezky C, Bultitude WP, Marin W, Vierra-Green C, Anderson KM, Balas A, Caro-Oleas JL, Cisneros E, Colucci F, Dandekar R, Elfishawi SM, Fernández-Viña MA, Fouda M, González-Fernández R, Große A, Herrero-Mata MJ, Hollenbach SQ, Marsh SGE, Mentzer A, Middleton D, Moffett A, Moreno-Hidalgo MA, Mossallam GI, Nakimuli A, Oksenberg JR, Oppenheimer SJ, Parham P, Petzl-Erler ML, Planelles D, Sánchez-García F, Sánchez-Gordo F, Schmidt AH, Trowsdale J, Vargas LB, Vicario JL, Vilches C, Norman PJ, Hollenbach JA.

Hum Immunol. 2018 Dec;79(12):825-833. doi: 10.1016/j.humimm.2018.10.003. Epub 2018 Oct 12.

Single-Cell Analysis Identifies Thymic Maturation Delay in Growth-Restricted Neonatal Mice. Bacon WA, Hamilton RS, Yu Z, Kieckbusch J, Hawkes D, Krzak AM, Abell C, Colucci F, Charnock-Jones DS.

Front Immunol. 2018 Nov 1;9:2523. doi: 10.3389/fimmu.2018.02523. eCollection 2018.

Molecular definition of group 1 innate lymphoid cells in the mouse uterus.Filipovic I, Chiossone L, Vacca P, Hamilton RS, Ingegnere T, Doisne JM, Hawkes DA, Mingari MC, Sharkey AM, Moretta L, Colucci F.

Nat Commun. 2018 Oct 29;9(1):4492. doi: 10.1038/s41467-018-06918-3.

High-Resolution Genetic and Phenotypic Analysis of KIR2DL1 Alleles and Their Association with Pre-Eclampsia.

Huhn O, Chazara O, Ivarsson MA, Retière C, Venkatesan TC, Norman PJ, Hilton HG, Jayaraman J, Traherne JA, Trowsdale J, Ito M, Kling C, Parham P, Ghadially H, Moffett A, Sharkey AM, Colucci F.

J Immunol. 2018 Nov 1;201(9):2593-2601. doi: 10.4049/jimmunol.1800860. Epub 2018 Sep 24. Erratum in: J Immunol. 2019 Mar 15;202(6):1904.

A comparative analysis of immune privilege in pregnancy and cancer in the context of checkpoint blockade immunotherapy.

Flint TR, Jones JO, Ferrer M, Colucci F, Janowitz T.

Semin Oncol. 2018 Jun;45(3):170-175. doi: 10.1053/j.seminoncol.2018.03.005. Epub 2018 Mar 26. Review.

Constancia, Miguel

Sex-specific regulation of stress-induced fetal glucocorticoid surge by the mouse placenta.

Wieczorek A, Perani CV, Nixon M, Constancia M, Sandovici I, Zazara DE, Leone G, Zhang MZ, Arck PC, Solano ME.

Am J Physiol Endocrinol Metab. 2019 Apr 16. doi: 10.1152/ajpendo.00551.2018. [Epub ahead of print]

Insulin-like Growth Factor II: An Essential Adult Stem Cell Niche Constituent in Brain and Intestine.

Ziegler AN, Feng Q, Chidambaram S, Testai JM, Kumari E, Rothbard DE, Constancia M, Sandovici I, Cominski T, Pang K, Gao N, Wood TL, Levison SW.

Stem Cell Reports. 2019 Apr 9;12(4):816-830. doi: 10.1016/j.stemcr.2019.02.011. Epub 2019 Mar 21.

Placental polyamine metabolism differs by fetal sex, fetal growth restriction, and preeclampsia.

Gong S, Sovio U, Aye IL, Gaccioli F, Dopierala J, Johnson MD, Wood AM, Cook E, Jenkins BJ, Koulman A, Casero RA Jr, Constância M, Charnock-Jones DS, Smith GC.

JCI Insight. 2018 Jul 12;3(13). pii: 120723. doi: 10.1172/jci.insight.120723.

Genome-wide oxidative bisulfite sequencing identifies sex-specific methylation differences in the human placenta.

Gong S, Johnson MD, Dopierala J, Gaccioli F, Sovio U, Constância M, Smith GC, Charnock-Jones DS.

Epigenetics. 2018;13(3):228-239. doi: 10.1080/15592294.2018.1429857. Epub 2018 Feb 21.

Beeson, J.H., Blackmore, H.L., Carr, S.K., Dearden, L., Duque-Guimarães, D.E., Kusinski, L.C., Pantaleão, L.C., Pinnock, A.G., Aiken, C.E., Giussani, D.A., Fernandez Twinn., D.S. & Ozanne, S.E. (2018). Maternal exercise intervention in obese pregnancy improves the cardiovascular health of the adult male offspring. Molecular Mechanisms16, 35-44.

Nuzzo, A.M., Camm, E.J., Sferruzzi-Perri, A.N., Ashmore, T.J., Yung, H.W., Cindrova-Davies, T., Spiroski, A.M., Sutherland, M.R., Logan, A., Austin-Williams, S., Burton, G.J., Rolfo, A., Todros, T., Murphy, M.P. & Giussani, D.A. (2018).  Placental adaptation to early-onset hypoxic pregnancy and mitochondria-targeted antioxidant therapy in the rat.  The American Journal of Pathology188(12), 2704-2716.

Niu, Y., Kane, A.D., Lusby, C.M., Allison, B.J., Chua, Y.Y., Kaandorp, J.J., Nevin-Dolan, R., Ashmore, T.J., Blackmore, H.L., Derks, J.B., Ozanne, S.E., & Giussani, D.A. (2018). Maternal allopurinol prevents cardiac dysfunction in adult male offspring programmed by chronic hypoxia during pregnancy. Hypertension 72, 972-978.

Tay, J., Masini,G., McEniery, C., Giussani, D.A., Shaw, C.J., Wilkinson, I.B., Bennett, P.R. & Lees, C.C. (2019).  Maternal Cardiac Output and Vascular Resistance are associated with maternal uterine and fetal umbilical artery but not cerebral Doppler changes. American Journal of Obstetrics & Gyecology220(1), 96.e1-96.e8.

Brain, K.L., Allison, B.J., Niu, Y., Cross, C.M., Itani, N., Kane, A.D., Herrera, E.A., Skeffington, K.L., Botting, K.J. & Giussani, D.A. (2019). Intervention against hypertension in the next generation programmed by developmental hypoxia PLoS Biology 17(1): e2006552. https://doi.org/10.1371/journal.pbio.2006552.

Aiken, C.E., Tarry-Adkins, J.L., Spiroski, A.M., Nuzzo, A.M., Ashmore, T.J., Rolfo, A., Sutherland, M.J., Camm, E.J., Giussani, D.A. & Ozanne, S.E. (2019).  Chronic fetal hypoxia disrupts the peri-conceptual environment in adult female rats. The Journal of Physiology597(9), 2391-2401. Manuscript chosen for an Editorial Focus by Nathanielsz, P.W.  Maternal programming by hypoxia alters the molecular composition of the oviduct of her offspring, the first pathway her grandchildren will transit: a potential novel pathway for intergenerational programming? J Physiol. 2019;597(9):2325-2326.

Aiken C.E., Tarry-Adkins, J.L., Spiroski A.M., Nuzzo A.M., Ashmore T., Giussani D.A. & Ozanne, S.E. (2019).  Chronic gestational hypoxia induces low ovarian reserve in adult female rats. FASEB J.33(6), 7758-7766.

Snelling, E.P.,  Seymour, R.S., Giussani, D.A., Fuller, A., Maloney, S.K., Farrell, A.P., Mitchell, D., George, K., Kamerman, P.R., Mitchell, G., Dzialowski, E.M., Jonker, S.S., Wube, T (2019). Scaling of heart mass is interrupted by birth in the developing sheep Ovis aries.   The Journal of Anatomy. In Press. Apr 17. doi: 10.1111/joa.12990.

Shaw C.J., Rivens, I., Civale, J., Botting, K.J., Allison, B.J., Brain, K.L., Niu, Y., Ter Haar, G., Giussani, D.A. & Lees, C.C. (2019). Maternal and fetal cardiometabolic recovery following ultrasound-guided high-intensity focused ultrasound placental vascular occlusion. J R Soc Interface16(154), 20190013.

Hamilton, Russell (CTR Bioinformatician)

Turco, M.Y., Gardner, L., Kay, R., Hamilton, R.S., Prater, M., Hollinshead, M., McWhinnie, A., Esposito, L., Fernando, R., Skelton, H., Reimann, F., Gribble, F., Sharkey, A., Marsh, S.G.E., O’Rahilly, S., Hemberger, M., Burton, G.J. and Moffett. A. (2018) Trophoblast organoids as a model for maternal-fetal interactions during human placentation. Nature, 564, 263–267 [DOI] [GitHub]

Bacon, W.A^*., Hamilton, R.S^*., Yu, Z., Kieckbusch, J., Hawkes, D., Krzak, A., Abell, C., Colucci, F. & Charnock-Jones, D.S. (2018) Single-Cell Analysis Identifies Thymic Maturation Delay in Growth-Restricted Neonatal Mice. Frontiers In Immunology, 9, 2523 [DOI] [bioRxiv] [GitHub]

Filipovic, I., Chiossone, L., Vacca, P., Hamilton, R.S., Doisne, J.M., Eberl, G., Walzer, T., Mingari, C., Sharkey, A., Moretta, L. & Colucci, F. (2018) Molecular definition of group 1 innate lymphoid cells in the mouse uterus. Nature Communications, 9:1, 4492 [DOI][bioRxiv] [GitHub]

Ong, C-K & Hamilton, R.S.^± (2018) Constructing Computational Pipelines. Encyclopedia of Bioinformatics and Computational Biology. In Reference Module in Life Sciences, Elsevier, 2018, ISBN 9780128096338 [DOI] [GitHub] [Book]

Prater, M. & Hamilton, R.S.^± (2018) Epigenetics: Analysis of cytosine modifications at single base resolution. Encyclopedia of Bioinformatics and Computational Biology. In Reference Module in Life Sciences, Elsevier, 2018, ISBN 9780128096338 [DOI][Book]

Taylor, W.R., and Hamilton, R.S. (2017) Exploring RNA conformational space under sparse distance constraints. Scientific Reports, 7, 44074 [DOI] [GitHub]

Single-cell reconstruction of the early maternal-fetal interface in humans.

Vento-Tormo R, Efremova M, Botting RA, Turco MY, Vento-Tormo M, Meyer KB, Park JE, Stephenson E, Polański K, Goncalves A, Gardner L, Holmqvist S, Henriksson J, Zou A, Sharkey AM, Millar B, Innes B, Wood L, Wilbrey-Clark A, Payne RP, Ivarsson MA, Lisgo S, Filby A, Rowitch DH, Bulmer JN, Wright GJ, Stubbington MJT, Haniffa M, Moffett A, Teichmann SA.

Nature. 2018 Nov;563(7731):347-353. doi: 10.1038/s41586-018-0698-6. Epub 2018 Nov 14.

PMID: 30429548

High-Resolution Genetic and Phenotypic Analysis of KIR2DL1 Alleles and Their Association with Pre-Eclampsia.

Huhn O, Chazara O, Ivarsson MA, Retière C, Venkatesan TC, Norman PJ, Hilton HG, Jayaraman J, Traherne JA, Trowsdale J, Ito M, Kling C, Parham P, Ghadially H, Moffett A, Sharkey AM, Colucci F.

J Immunol. 2018 Nov 1;201(9):2593-2601. doi: 10.4049/jimmunol.1800860. Epub 2018 Sep 24. Erratum in: J Immunol. 2019 Mar 15;202(6):1904. 

PMID: 30249807

Integrin α2 marks a niche of trophoblast progenitor cells in first trimester human placenta.

Lee CQE, Turco MY, Gardner L, Simons BD, Hemberger M, Moffett A.

Development. 2018 Apr 16;145(16). pii: dev162305. doi: 10.1242/dev.162305.

PMID: 29540503

Perez Garcia, Vicente (new CTR Next Generation Fellow started June 2018)

Lopez-Tello J, Perez-Garcia V,  Khaira J, Kusinski LC, Cooper W, Andreani A, Grant I,  Fernandez de Liger E, Lam B, Hemberger M, Sandovici I, Constancia M, N. Sferruzzi-Perri A. Fetal and trophoblast PI3K p110α have distinct roles in regulating resource supply to the growing fetus. Elife, under review.

Woods L, Perez-Garcia V*, Hemberger M*. Regulation of Placental Development and Its Impact on Fetal Growth-New Insights From Mouse Models. Front Endocrinol. 27;9:570 (2018). * Equal contribution.

Chrysanthou S, Senner CE, Woods L, Fineberg E, Burge S, Perez-Garcia V and Hemberger M. A novel role of Tet1/2 proteins in cell cycle progression in trophoblast stem cells. Stem Cell Reports, 10(4): 1355– 1368 (2018).

Perez-Garcia V*, Fineberg E*, Wilson R, Murray A, Icoresi C, Tudor C, Sienerth A, White JK, E Tuck E, Ryder E, Gleeson D, Siragher E, Wardle-Jones H, Collins J, Geyer S, Busch E, Galli A, Smith JC, Robertson E, Adams DJ, Weninger WJ, Mohun T, Hemberger M. Placental malformations are highly prevalent in embryonic lethal mouse mutants. Nature, 555(7697):463-468 (2018). * Equal contribution.

Rugg-Gunn, Peter (CTR Associate Babraham Institute)

Reik, Wolf

Montalbán-Loro R, Lozano-Ureña A, Ito M, Krueger C, Reik W, Ferguson-Smith AC,

Ferrón SR. TET3 prevents terminal differentiation of adult NSCs by a

non-catalytic action at Snrpn. Nat Commun. 2019 Apr 12;10(1):1726. doi:

10.1038/s41467-019-09665-1. PubMed PMID: 30979904; PubMed Central PMCID:

PMC6461695.

Pijuan-Sala B, Griffiths JA, Guibentif C, Hiscock TW, Jawaid W, Calero-Nieto

FJ, Mulas C, Ibarra-Soria X, Tyser RCV, Ho DLL, Reik W, Srinivas S, Simons BD,

Nichols J, Marioni JC, Göttgens B. A single-cell molecular map of mouse

gastrulation and early organogenesis. Nature. 2019 Feb;566(7745):490-495. doi:

10.1038/s41586-019-0933-9. Epub 2019 Feb 20. PubMed PMID: 30787436; PubMed

Central PMCID: PMC6522369.

Linker SM, Urban L, Clark SJ, Chhatriwala M, Amatya S, McCarthy DJ,

Ebersberger I, Vallier L, Reik W, Stegle O, Bonder MJ. Combined single-cell

profiling of expression and DNA methylation reveals splicing regulation and

heterogeneity. Genome Biol. 2019 Feb 11;20(1):30. doi: 10.1186/s13059-019-1644-0.

PubMed PMID: 30744673; PubMed Central PMCID: PMC6371455.

Eckersley-Maslin M, Alda-Catalinas C, Blotenburg M, Kreibich E, Krueger C,

Reik W. Dppa2 and Dppa4 directly regulate the Dux-driven zygotic transcriptional

program. Genes Dev. 2019 Feb 1;33(3-4):194-208. doi: 10.1101/gad.321174.118. Epub

2019 Jan 28. PubMed PMID: 30692203; PubMed Central PMCID: PMC6362816.

Messmer T, von Meyenn F, Savino A, Santos F, Mohammed H, Lun ATL, Marioni JC,

Reik W. Transcriptional Heterogeneity in Naive and Primed Human Pluripotent Stem

Cells at Single-Cell Resolution. Cell Rep. 2019 Jan 22;26(4):815-824.e4. doi:

10.1016/j.celrep.2018.12.099. PubMed PMID: 30673604; PubMed Central PMCID:

PMC6344340.

Gdula MR, Nesterova TB, Pintacuda G, Godwin J, Zhan Y, Ozadam H, McClellan M,

Moralli D, Krueger F, Green CM, Reik W, Kriaucionis S, Heard E, Dekker J,

Brockdorff N. The non-canonical SMC protein SmcHD1 antagonises TAD formation and

compartmentalisation on the inactive X chromosome. Nat Commun. 2019 Jan

3;10(1):30. doi: 10.1038/s41467-018-07907-2. PubMed PMID: 30604745; PubMed

Central PMCID: PMC6318279.

Hahn O, Stubbs TM, Reik W, Grönke S, Beyer A, Partridge L. Hepatic gene body

hypermethylation is a shared epigenetic signature of murine longevity. PLoS

Genet. 2018 Nov 21;14(11):e1007766. doi: 10.1371/journal.pgen.1007766.

eCollection 2018 Nov. PubMed PMID: 30462643; PubMed Central PMCID: PMC6281273.

Boroviak T, Stirparo GG, Dietmann S, Hernando-Herraez I, Mohammed H, Reik W,

Smith A, Sasaki E, Nichols J, Bertone P. Single cell transcriptome analysis of

human, marmoset and mouse embryos reveals common and divergent features of

preimplantation development. Development. 2018 Nov 9;145(21). pii: dev167833.

doi: 10.1242/dev.167833. PubMed PMID: 30413530; PubMed Central PMCID: PMC6240320.

Raiber EA, Portella G, Martínez Cuesta S, Hardisty R, Murat P, Li Z, Iurlaro

M, Dean W, Spindel J, Beraldi D, Liu Z, Dawson MA, Reik W, Balasubramanian S.

5-Formylcytosine organizes nucleosomes and forms Schiff base interactions with

histones in mouse embryonic stem cells. Nat Chem. 2018 Dec;10(12):1258-1266. doi:

10.1038/s41557-018-0149-x. Epub 2018 Oct 22. PubMed PMID: 30349137.

Sarker G, Berrens R, von Arx J, Pelczar P, Reik W, Wolfrum C, Peleg-Raibstein

D. Transgenerational transmission of hedonic behaviors and metabolic phenotypes

induced by maternal overnutrition. Transl Psychiatry. 2018 Oct 12;8(1):195. doi:

10.1038/s41398-018-0243-2. PubMed PMID: 30315171; PubMed Central PMCID:

PMC6185972.

Rulands S, Lee HJ, Clark SJ, Angermueller C, Smallwood SA, Krueger F,

Mohammed H, Dean W, Nichols J, Rugg-Gunn P, Kelsey G, Stegle O, Simons BD, Reik

W. Genome-Scale Oscillations in DNA Methylation during Exit from Pluripotency.

Cell Syst. 2018 Jul 25;7(1):63-76.e12. doi: 10.1016/j.cels.2018.06.012. PubMed

PMID: 30031774; PubMed Central PMCID: PMC6066359.

Sun W, Dong H, Becker AS, Dapito DH, Modica S, Grandl G, Opitz L, Efthymiou

V, Straub LG, Sarker G, Balaz M, Balazova L, Perdikari A, Kiehlmann E, Bacanovic

S, Zellweger C, Peleg-Raibstein D, Pelczar P, Reik W, Burger IA, von Meyenn F,

Wolfrum C. Cold-induced epigenetic programming of the sperm enhances brown

adipose tissue activity in the offspring. Nat Med. 2018 Sep;24(9):1372-1383. doi:

10.1038/s41591-018-0102-y. Epub 2018 Jul 9. Erratum in: Nat Med. 2018 Aug 7;:.

Nat Med. 2018 Aug 7. PubMed PMID: 29988127.

Eckersley-Maslin MA, Alda-Catalinas C, Reik W. Dynamics of the epigenetic

landscape during the maternal-to-zygotic transition. Nat Rev Mol Cell Biol. 2018

Jul;19(7):436-450. doi: 10.1038/s41580-018-0008-z. Review. PubMed PMID: 29686419.

Santos, Fatima (CTR member, Babraham Institute)

Sferruzi-Perri, Amanda (CTR member)

Smith, Gordon (CTR Manager)

De Goffau MC, Lager SM, Sovio U, Gaccioli F, Cook E, Peacock SJ, Parkhill J, Charnock-Jones DS, Smith GCS. Article: Human placenta has no microbiome but can harbor potential pathogens. Nature 2019, in press.

Wastlund D, Moraitis AA, Dacey A, Wilson ECF, Sovio U, Smith GCS. Screening for breech presentation using universal late pregnancy ultrasonography: A prospective cohort study and cost-effectiveness analysis. PLoS Medicine 2019 6(4):e1002778.

de Goffau MC, Lager SM, Salter SJ, Wagner J, Charnock-Jones DS, Peacock SJ, Smith GCS, Parkhill J. Recognizing the reagent microbiome. Nature Microbiology 2018;3:851-853.

Gaccioli F, Sovio U, Cook E, Hund M, Charnock-Jones DS, Smith GCS. Screening for fetal growth restriction using ultrasound and the sFLT1:PlGF ratio in a prospective cohort study of nulliparous women The Lancet Child and Adolescent Health 2018;2:569-581

Sovio, Ulla (Dept of Obstetrics and Gynaecology, CTR member)

Lager S, de Goffau MC, Sovio U, Peacock SJ, Parkhill J, Charnock-Jones DS, Smith GCS. Detecting eukaryotic microbiota with single-cell sensitivity in human tissue. Microbiome 2018;6(1):151.

Gaccioli F*, Sovio U*, Cook E, Hund M, Charnock-Jones DS, Smith GCS. Screening for fetal growth restriction using ultrasound and the sFLT1/PlGF ratio in nulliparous women: a prospective cohort study. Lancet Child Adolesc Health 2018;2(8):569-581.

Gong S*, Sovio U*, Aye ILMH*, Gaccioli F*, Dopierala J, Johnson MD, Wood AM, Cook E, Jenkings BJ, Koulman A, Casero RA Jr, ConstânciaM, Charnock-Jones DS, Smith GCS. Placental polyamine metabolism differs by fetal sex, fetal growth restriction, and preeclampsia. JCI Insight 2018;3(13):e120723.

Sovio U, Smith GCS. Blinded ultrasonic fetal biometry at 36 weeks and the risk of emergency Cesarean delivery in a prospective cohort study of low-risk nulliparous women. Ultrasound Obstet Gynecol. 2018;52(1):78-86.

Hughes AE*, Sovio U*, Gaccioli F*, Cook E, Charnock-Jones DS, Smith GCS. The association between first trimester AFP to PAPP-A ratio and placentally-related adverse pregnancy outcome. Placenta 2019;81:25-31.

Sovio U, McBride N, Wood AM, Masconi KL, Cook E, Gaccioli F, Charnock-Jones DS, Lawlor DA, Smith GCS. 4-Hydroxyglutamate is a novel predictor of pre-eclampsia. Int J Epidemiol 2019, published online https://academic.oup.com/ije/article-lookup/doi/10.1093/ije/dyz098.

Wastlund D, Moraitis AA, Dacey A, Sovio U, Wilson ECF, Smith GCS. Screening for breech presentation using universal late pregnancy ultrasonography: A prospective cohort study and cost-effectiveness analysis. PLOS Med 2019;16(4):e1002778.

Sovio U, Smith GCS. Evaluation of a simple risk score to predict preterm preeclampsia using maternal characteristics: a prospective cohort study. BJOG 2019, published online https://doi.org/10.1093/ije/dyz098. 

Jayasuriya NA*, Hughes AE*, Sovio U, Cook E, Charnock-Jones DS, Smith GCS. A lower maternal cortisol-to-cortisone ratio precedes clinical diagnosis of preterm and term preeclampsia by many weeks. J Clin Endocrinol Metab 2019;104(6):2355-2366.

Surani, Azim

Ramos-Ibeas, P., Sang, F., Zhu, Q., Tang, W. W. C., Withey, S., Klisch, D., . . . Alberio, R. (2019). Pluripotency and X chromosome dynamics revealed in pig pre-gastrulating embryos by single cell analysis.. Nat Commun, 10(1), 500. doi:10.1038/s41467-019-08387-8

Sybirna, A., Tang, W., Dietmann, S., Gruhn, W., & Surani, A. (2019). A critical but divergent role of PRDM14 in human primordial germ cell fate revealed by inducible degrons. doi:10.1101/563072

Adashi, E. Y., Cohen, I. G., Hanna, J. H., Surani, A. M., & Hayashi, K. (2019). Stem Cell-Derived Human Gametes: The Public Engagement Imperative.. Trends Mol Med, 25(3), 165-167. doi:10.1016/j.molmed.2019.01.005

Hackett, J. A., Huang, Y., Günesdogan, U., Gretarsson, K. A., Kobayashi, T., & Surani, M. A. (2018). Publisher Correction: Tracing the transitions from pluripotency to germ cell fate with CRISPR screening.. Nat Commun, 9(1), 5328. doi:10.1038/s41467-018-07765-y

Do, D. V., Strauss, B., Cukuroglu, E., Macaulay, I., Wee, K. B., Hu, T. X., . . . Surani, M. A. (2018). SRSF3 maintains transcriptome integrity in oocytes by regulation of alternative splicing and transposable elements.. Cell Discov, 4, 33. doi:10.1038/s41421-018-0032-3

Cheetham, S. W., Gruhn, W. H., van den Ameele, J., Krautz, R., Southall, T. D., Kobayashi, T., . . . Brand, A. H. (2018). Targeted DamID reveals differential binding of mammalian pluripotency factors.. Development, 145(20). doi:10.1242/dev.170209

Hackett, J. A., Huang, Y., Günesdogan, U., Gretarsson, K. A., Kobayashi, T., & Surani, M. A. (2018). Tracing the transitions from pluripotency to germ cell fate with CRISPR screening.. Nat Commun, 9(1), 4292. doi:10.1038/s41467-018-06230-0

Tischler, J., Gruhn, W. H., Reid, J., Allgeyer, E., Buettner, F., Marr, C., . . . Surani, M. A. (2019). Metabolic regulation of pluripotency and germ cell fate through α-ketoglutarate.. EMBO J, 38(1). doi:10.15252/embj.201899518

Ramakrishna, N. B., & Surani, M. A. (2018). Staged profiling of sperm development in sync.. Cell Res, 28(10), 965-966. doi:10.1038/s41422-018-0088-5

Penfold, C. A., Sybirna, A., Reid, J. E., Huang, Y., Wernisch, L., Ghahramani, Z., . . . Surani, M. A. (2018). Branch-recombinant Gaussian processes for analysis of perturbations in biological time series.. Bioinformatics, 34(17), i1005-i1013. doi:10.1093/bioinformatics/bty603

Kobayashi, T., & Surani, M. A. (2018). On the origin of the human germline.. Development, 145(16). doi:10.1242/dev.150433

Tong Wen (CTR funded PhD student)

Preeclampsia link to gestational hypoxia.

Tong W, Giussani DA.

J Dev Orig Health Dis. 2019 Apr 10:1-12. doi: 10.1017/S204017441900014X

Trowsdale, John

Sci Immunol. 2018 Nov 9;3(29). pii: eaao2892. doi:

10.1126/sciimmunol.aao2892. Inhibitory killer cell immunoglobulin-like receptors strengthen CD8+ T cell-mediated control of HIV-1, HCV, and HTLV-1.

Boelen L, Debebe B1, Silveira M, Salam A, Makinde J, Roberts CH, Wang ECY, Frater J, Gilmour J, Twigger K, Ladell K, Miners KL, Jayaraman J, Traherne JA, Price DA, Qi Y, Martin MP, Macallan DC, Thio CL, Astemborski J, Kirk G, Donfield SM, Buchbinder S, Khakoo SI, Goedert JJ, Trowsdale J, Carrington M, Kollnberger S, Asquith B.

Report from the Killer-cell Immunoglobulin-like Receptors (KIR) component of the 17th International HLA and Immunogenetics Workshop. Misra MK, Augusto DG, Martin GM, Nemat-Gorgani N, Sauter J, Hofmann JA, Traherne JA, González-Quezada B, Gorodezky C, Bultitude WP, Marin W, Vierra-Green C, Anderson KM, Balas A, Caro-Oleas JL, Cisneros E, Colucci F, Dandekar R, Elfishawi SM, Fernández-Viña MA, Fouda M, González-Fernández R, Große A, Herrero-Mata MJ, Hollenbach SQ, Marsh SGE, Mentzer A, Middleton D, Moffett A, Moreno-Hidalgo MA, Mossallam GI, Nakimuli A, Oksenberg JR, Oppenheimer SJ, Parham P, Petzl-Erler ML, Planelles D, Sánchez-García F, Sánchez-Gordo F, Schmidt AH, Trowsdale J, Vargas LB, Vicario JL, Vilches C, Norman PJ, Hollenbach JA. Hum Immunol. 2018 Dec;79(12):825-833. doi:

10.1016/j.humimm.2018.10.003. Epub 2018 Oct 12

High-Resolution Genetic and Phenotypic Analysis of KIR2DL1 Alleles and Their Association with Pre-Eclampsia. Huhn O, Chazara O, Ivarsson MA, Retière C, Venkatesan TC, Norman PJ, Hilton HG, Jayaraman J, Traherne JA, Trowsdale J, Ito M, Kling C, Parham P, Ghadially H, Moffett A, Sharkey AM, Colucci F. J Immunol. 2018 Nov 1;201(9):2593-2601. doi:

10.4049/jimmunol.1800860.

Genetics of antigen processing and presentation.

Kelly A, Trowsdale J.

Immunogenetics. 2019 Mar;71(3):161-170.

Tunster, Simon (CTR New Generation Research Fellow)

 S.J. Millership, S.J. Tunster, M. Van de Pette, A.I. Choudhury, E.E. Irvine, M. Christian, A.G. Fisher, R.M. John, J. Scott, D.J. Withers, Neuronatin deletion causes postnatal growth restriction and adult obesity in 129S2/Sv mice, Mol Metab 18 (2018) 97-106.

S.J. Tunster, R. Boque-Sastre, G.I. McNamara, S.M. Hunter, H.D.J. Creeth, R.M. John, Peg3 Deficiency Results in Sexually Dimorphic Losses and Gains in the Normal Repertoire of Placental Hormones, Front Cell Dev Biol 6 (2018) 123.

M. Van de Pette, S.J. Tunster, R.M. John, Loss of Imprinting of Cdkn1c Protects against Age and Diet-Induced Obesity, Int J Mol Sci 19(9) (2018).

S.J. Tunster, M. Van de Pette, H.D.J. Creeth, L. Lefebvre, R.M. John, Fetal growth restriction in a genetic model of sporadic Beckwith-Wiedemann Syndrome. Dis Model Mech (2018)

 H.D.J. Creeth, G.I. McNamara, S.J. Tunster, R. Boque-Sastre, B. Allen, L. Sumption, J.B. Eddy, A.R. Isles, R.M. John. Maternal care boosted by paternal imprinting in mammals. PLoS Biol 16(7) (2018) e2006599.

Watson, Erica (CTR manager)

Padmanabhan N, Menelaou K, Gao J, Anderson A, Blake GET, Li T, Daw BN, & Watson ED. (2018) Abnormal folate metabolism causes age-, sex-, and parent-of-origin specific haematological defects in mice. The Journal of Physiology 596(18): 4341-4360. [Editor’s Choice]

Zernicka-Goetz, Magdalena (CTR member)

Concerted cell divisions in embryonic visceral endoderm guide anterior visceral endoderm migration.

Antonica F, Orietti LC, Mort RL, Zernicka-Goetz M.

Dev Biol. 2019 Jun 15;450(2):132-140. doi: 10.1016/j.ydbio.2019.03.016. Epub 2019 Mar 30.

CARM1 and Paraspeckles Regulate Pre-implantation Mouse Embryo Development.

Hupalowska A, Jedrusik A, Zhu M, Bedford MT, Glover DM, Zernicka-Goetz M.

Cell. 2018 Dec 13;175(7):1902-1916.e13. doi: 10.1016/j.cell.2018.11.027.

Debate ethics of embryo models from stem cells.

Rivron N, Pera M, Rossant J, Martinez Arias A, Zernicka-Goetz M, Fu J, van den Brink S, Bredenoord A, Dondorp W, de Wert G, Hyun I, Munsie M, Isasi R.

Nature. 2018 Dec;564(7735):183-185. doi: 10.1038/d41586-018-07663-9.

Sequential formation and resolution of multiple rosettes drive embryo remodelling after implantation.

Christodoulou N, Kyprianou C, Weberling A, Wang R, Cui G, Peng G, Jing N, Zernicka-Goetz M.

Nat Cell Biol. 2018 Nov;20(11):1278-1289. doi: 10.1038/s41556-018-0211-3. Epub 2018 Oct 15. Erratum in: Nat Cell Biol. 2018 Dec;20(12):1434. 

Self-assembly of embryonic and two extra-embryonic stem cell types into gastrulating embryo-like structures.

Sozen B, Amadei G, Cox A, Wang R, Na E, Czukiewska S, Chappell L, Voet T, Michel G, Jing N, Glover DM, Zernicka-Goetz M.

Nat Cell Biol. 2018 Aug;20(8):979-989. doi: 10.1038/s41556-018-0147-7. Epub 2018 Jul 23. Erratum in: Nat Cell Biol. 2018 Oct;20(10):1229. 

Deconstructing and reconstructing the mouse and human early embryo.

Shahbazi MN, Zernicka-Goetz M.

Nat Cell Biol. 2018 Aug;20(8):878-887. doi: 10.1038/s41556-018-0144-x. Epub 2018 Jul 23.

In vitro generation of mouse polarized embryo-like structures from embryonic and trophoblast stem cells.

Harrison SE, Sozen B, Zernicka-Goetz M.

Nature Protoc. 2018 Jul;13(7):1586-1602. doi: 10.1038/s41596-018-0005-x.

Tracing the origin of heterogeneity and symmetry breaking in the early mammalian embryo.

Chen Q, Shi J, Tao Y, Zernicka-Goetz M.

Nature Commun. 2018 May 8;9(1):1819. doi: 10.1038/s41467-018-04155-2.